Aging of the Immune System: Focus on Natural Killer Cells Phenotype and Functions
Abstract
:1. Introduction
2. NK Cells in Immunity: An Overview
3. Changes in NK Cell Numbers and Subpopulations with Age
4. Effect of Age on NK Cell Cytokine Production and Secretion
5. Changes in NK Cell Cytotoxic Activity with Age
6. Effect of Age on NK Cell Signal Transduction
7. NK Cell Exhaustion
8. Impact of the Aging Systemic Milieu on NK Cells
9. Neuroendocrine Signaling and NK Cell Aging
10. Reducing the Impacts of Secondary Aging on NK Cell Function
10.1. Micronutrient Deficiency
10.2. Stress Reduction
10.3. Sleep Health and Circadian Alignment
11. Harnessing NK Cells as Immunosenolytics
12. Perspective and Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sierra, F. Geroscience and the challenges of aging societies. Aging Med. 2019, 2, 132–134. [Google Scholar] [CrossRef] [PubMed]
- Rae, M.J.; Butler, R.N.; Campisi, J.; de Grey, A.D.; Finch, C.E.; Gough, M.; Martin, G.M.; Vijg, J.; Perrott, K.M.; Logan, B.J. The demographic and biomedical case for late-life interventions in aging. Sci. Transl. Med. 2010, 2, 40cm21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Austad, S.N. The Geroscience Hypothesis: Is It Possible to Change the Rate of Aging? In Advances in Geroscience; Sierra, F., Kohanski, R., Eds.; Springer International Publishing: Cham, Switzerland, 2016; pp. 1–36. [Google Scholar]
- Akbar, A.N.; Gilroy, D.W. Aging immunity may exacerbate COVID-19. Science 2020, 369, 256–257. [Google Scholar] [CrossRef] [PubMed]
- O’Driscoll, M.; Ribeiro Dos Santos, G.; Wang, L.; Cummings, D.A.T.; Azman, A.S.; Paireau, J.; Fontanet, A.; Cauchemez, S.; Salje, H. Age-specific mortality and immunity patterns of SARS-CoV-2. Nature 2021, 590, 140–145. [Google Scholar] [CrossRef] [PubMed]
- Fülöp, T.; Dupuis, G.; Witkowski, J.M.; Larbi, A. The Role of Immunosenescence in the Development of Age-Related Diseases. Rev. Investig. Clin. 2016, 68, 84–91. [Google Scholar]
- Barbé-Tuana, F.; Funchal, G.; Schmitz, C.R.R.; Maurmann, R.M.; Bauer, M.E. The interplay between immunosenescence and age-related diseases. Semin. Immunopathol. 2020, 42, 545–557. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Huang, B. The Development and Diversity of ILCs, NK Cells and Their Relevance in Health and Diseases. Adv. Exp. Med. Biol. 2017, 1024, 225–244. [Google Scholar] [CrossRef] [PubMed]
- Vivier, E.; Tomasello, E.; Baratin, M.; Walzer, T.; Ugolini, S. Functions of natural killer cells. Nat. Immunol. 2008, 9, 503–510. [Google Scholar] [CrossRef] [PubMed]
- Song, P.; An, J.; Zou, M.H. Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases. Cells 2020, 9, 671. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Antonangeli, F.; Zingoni, A.; Soriani, A.; Santoni, A. Senescent cells: Living or dying is a matter of NK cells. J. Leukoc. Biol. 2019, 105, 1275–1283. [Google Scholar] [CrossRef] [PubMed]
- Kale, A.; Sharma, A.; Stolzing, A.; Desprez, P.Y.; Campisi, J. Role of immune cells in the removal of deleterious senescent cells. Immun. Ageing 2020, 17, 16. [Google Scholar] [CrossRef] [PubMed]
- Van Deursen, J.M. The role of senescent cells in ageing. Nature 2014, 509, 439–446. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pignolo, R.J.; Passos, J.F.; Khosla, S.; Tchkonia, T.; Kirkland, J.L. Reducing Senescent Cell Burden in Aging and Disease. Trends Mol. Med. 2020, 26, 630–638. [Google Scholar] [CrossRef] [PubMed]
- Nikolich-Žugich, J. The twilight of immunity: Emerging concepts in aging of the immune system. Nat. Immunol. 2018, 19, 10–19. [Google Scholar] [CrossRef] [PubMed]
- Paul, S.; Lal, G. The Molecular Mechanism of Natural Killer Cells Function and Its Importance in Cancer Immunotherapy. Front. Immunol. 2017, 8, 1124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin-Fontecha, A.; Thomsen, L.L.; Brett, S.; Gerard, C.; Lipp, M.; Lanzavecchia, A.; Sallusto, F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 2004, 5, 1260–1265. [Google Scholar] [CrossRef] [PubMed]
- Blum, K.S.; Pabst, R. Lymphocyte numbers and subsets in the human blood. Do they mirror the situation in all organs? Immunol. Lett. 2007, 108, 45–51. [Google Scholar] [CrossRef] [PubMed]
- Carrega, P.; Ferlazzo, G. Natural killer cell distribution and trafficking in human tissues. Front. Immunol. 2012, 3, 347. [Google Scholar] [CrossRef] [Green Version]
- Michel, T.; Poli, A.; Cuapio, A.; Briquemont, B.; Iserentant, G.; Ollert, M.; Zimmer, J. Human CD56bright NK Cells: An Update. J. Immunol. 2016, 196, 2923–2931. [Google Scholar] [CrossRef] [Green Version]
- Penack, O.; Gentilini, C.; Fischer, L.; Asemissen, A.M.; Scheibenbogen, C.; Thiel, E.; Uharek, L. CD56dimCD16neg cells are responsible for natural cytotoxicity against tumor targets. Leukemia 2005, 19, 835840. [Google Scholar] [CrossRef] [Green Version]
- Carrega, P.; Bonaccorsi, I.; Di Carlo, E.; Morandi, B.; Paul, P.; Rizzello, V.; Cipollone, G.; Navarra, G.; Mingari, M.C.; Moretta, L.; et al. CD56(bright)perforin(low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J. Immunol. 2014, 192, 3805–3815. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lugthart, G.; Melsen, J.E.; Vervat, C.; van Ostaijen-Ten Dam, M.M.; Corver, W.E.; Roelen, D.L.; van Bergen, J.; van Tol, M.J.; Lankester, A.C.; Schilham, M.W. Human Lymphoid Tissues Harbor a Distinct CD69+CXCR6+ NK Cell Population. J. Immunol. 2016, 197, 78–84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caligiuri, M.A. Human natural killer cells. Blood 2008, 112, 461–469. [Google Scholar] [CrossRef] [PubMed]
- Yu, J.; Freud, A.G.; Caligiuri, M.A. Location and cellular stages of natural killer cell development. Trends Immunol. 2013, 34, 573–582. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Klein Wolterink, R.G.; Garcia-Ojeda, M.E.; Vosshenrich, C.A.; Hendriks, R.W.; Di Santo, J.P. The intrathymic crossroads of T and NK cell differentiation. Immunol. Rev. 2010, 238, 126137. [Google Scholar] [CrossRef] [PubMed]
- Cichocki, F.; Grzywacz, B.; Miller, J.S. Human NK Cell Development: One Road or Many? Front. Immunol. 2019, 10, 2078. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luetke-Eversloh, M.; Killig, M.; Romagnani, C. Signatures of human NK cell development and terminal differentiation. Front. Immunol. 2013, 4, 499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rabinowich, H.; Pricop, L.; Herberman, R.B.; Whiteside, T.L. Expression and function of CD7 molecule on human natural killer cells. J. Immunol. 1994, 152, 517–526. [Google Scholar] [PubMed]
- Higuchi, Y.; Zeng, H.; Ogawa, M. CD38 expression by hematopoietic stem cells of newborn and juvenile mice. Leukemia 2003, 17, 171–174. [Google Scholar] [CrossRef] [Green Version]
- Zingoni, A.; Sornasse, T.; Cocks, B.G.; Tanaka, Y.; Santoni, A.; Lanier, L.L. Cross-talk between activated human NK cells and CD4+ T cells via OX40-OX40 ligand interactions. J. Immunol. 2004, 173, 3716–3724. [Google Scholar] [CrossRef] [Green Version]
- Blanca, I.R.; Bere, E.W.; Young, H.A.; Ortaldo, J.R. Human B cell activation by autologous NK cells is regulated by CD40-CD40 ligand interaction: Role of memory B cells and CD5+ B cells. J. Immunol. 2001, 167, 6132–6139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moretta, L.; Montaldo, E.; Vacca, P.; Del Zotto, G.; Moretta, F.; Merli, P.; Locatelli, F.; Mingari, M.C. Human natural killer cells: Origin, receptors, function, and clinical applications. Int. Arch. Allergy Immunol. 2014, 164, 253–264. [Google Scholar] [CrossRef] [PubMed]
- Bryceson, Y.T.; March, M.E.; Ljunggren, H.G.; Long, E.O. Activation, coactivation, and costimulation of resting human natural killer cells. Immunol. Rev. 2006, 214, 73–91. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, K.M.; Wu, J.; Bakker, A.B.; Phillips, J.H.; Lanier, L.L. Ly-49D and Ly-49H associate with mouse DAP12 and form activating receptors. J. Immunol. 1998, 161, 7–10. [Google Scholar] [PubMed]
- Cosman, D.; Mullberg, J.; Sutherland, C.L.; Chin, W.; Armitage, R.; Fanslow, W.; Kubin, M.; Chalupny, N.J. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001, 14, 123–133. [Google Scholar] [CrossRef]
- Jamieson, A.M.; Diefenbach, A.; McMahon, C.W.; Xiong, N.; Carlyle, J.R.; Raulet, D.H. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 2002, 17, 19–29. [Google Scholar] [CrossRef] [Green Version]
- Martinez-Lostao, L.; Anel, A.; Pardo, J. How Do Cytotoxic Lymphocytes Kill Cancer Cells? Clin. Cancer Res. 2015, 21, 5047–5056. [Google Scholar] [CrossRef] [Green Version]
- Gayoso, I.; Sanchez-Correa, B.; Campos, C.; Alonso, C.; Pera, A.; Casado, J.G.; Morgado, S.; Tarazona, R.; Solana, R. Immunosenescence of human natural killer cells. J. Innate Immun. 2011, 3, 337–343. [Google Scholar] [CrossRef]
- Narni-Mancinelli, E.; Ugolini, S.; Vivier, E. Tuning the threshold of natural killer cell responses. Curr. Opin. Immunol. 2013, 25, 53–58. [Google Scholar] [CrossRef]
- Canossi, A.; Aureli, A.; Del Beato, T.; Rossi, P.; Franceschilli, L.; De Sanctis, F.; Sileri, P.; di Lorenzo, N.; Buonomo, O.; Lauro, D.; et al. Role of KIR and CD16A genotypes in colorectal carcinoma genetic risk and clinical stage. J. Transl. Med. 2016, 14, 239. [Google Scholar] [CrossRef]
- Lee, N.; Llano, M.; Carretero, M.; Ishitani, A.; Navarro, F.; Lopez-Botet, M.; Geraghty, D.E. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 1998, 95, 5199–5204. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Braud, V.M.; Allan, D.S.; O’Callaghan, C.A.; Soderstrom, K.; D’Andrea, A.; Ogg, G.S.; Lazetic, S.; Young, N.T.; Bell, J.I.; Phillips, J.H.; et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 1998, 391, 795–799. [Google Scholar] [CrossRef] [PubMed]
- Veillette, A.; Latour, S.; Davidson, D. Negative regulation of immunoreceptor signaling. Annu. Rev. Immunol. 2002, 20, 669–707. [Google Scholar] [CrossRef] [PubMed]
- Yokoyama, W.M.; Kim, S. Licensing of natural killer cells by self-major histocompatibility complex class I. Immunol. Rev. 2006, 214, 143–154. [Google Scholar] [CrossRef] [PubMed]
- Kadri, N.; Thanh, T.L.; Höglund, P. Selection, tuning, and adaptation in mouse NK cell education. Immunol. Rev. 2015, 267, 167–177. [Google Scholar] [CrossRef]
- Pahl, J.; Cerwenka, A. Tricking the balance: NK cells in anti-cancer immunity. Immunobiology 2017, 222, 11–20. [Google Scholar] [CrossRef]
- Moesta, A.K.; Parham, P. Diverse functionality among human NK cell receptors for the C1 epitope of HLA-C: KIR2DS2, KIR2DL2, and KIR2DL3. Front. Immunol. 2012, 3, 336. [Google Scholar] [CrossRef] [Green Version]
- Makrigiannis, A.P.; Anderson, S.K. Ly49 gene expression in different inbred mouse strains. Immunol. Res. 2000, 21, 39–47. [Google Scholar] [CrossRef]
- Sternberg-Simon, M.; Brodin, P.; Pickman, Y.; Onfelt, B.; Karre, K.; Malmberg, K.J.; Hoglund, P.; Mehr, R. Natural killer cell inhibitory receptor expression in humans and mice: A closer look. Front. Immunol. 2013, 4, 65. [Google Scholar] [CrossRef] [Green Version]
- Muzzioli, M.; Stecconi, R.; Moresi, R.; Provinciali, M. Zinc improves the development of human CD34+ cell progenitors towards NK cells and increases the expression of GATA-3 transcription factor in young and old ages. Biogerontology 2009, 10, 593–604. [Google Scholar] [CrossRef]
- Ligthart, G.J.; van Vlokhoven, P.C.; Schuit, H.R.; Hijmans, W. The expanded null cell compartment in ageing: Increase in the number of natural killer cells and changes in T-cell and NK-cell subsets in human blood. Immunology 1986, 59, 353–357. [Google Scholar] [PubMed]
- Facchini, A.; Mariani, E.; Mariani, A.R.; Papa, S.; Vitale, M.; Manzoli, F.A. Increased number of circulating Leu 11+ (CD 16) large granular lymphocytes and decreased NK activity during human ageing. Clin. Exp. Immunol. 1987, 68, 340–347. [Google Scholar] [PubMed]
- Krishnaraj, R.; Svanborg, A. Preferential accumulation of mature NK cells during human immunosenescence. J. Cell. Biochem. 1992, 50, 386–391. [Google Scholar] [CrossRef] [PubMed]
- Vitale, M.; Zamai, L.; Neri, L.M.; Galanzi, A.; Facchini, A.; Rana, R.; Cataldi, A.; Papa, S. The impairment of natural killer function in the healthy aged is due to a postbinding deficient mechanism. Cell. Immunol. 1992, 145, 1–10. [Google Scholar] [CrossRef]
- Sansoni, P.; Cossarizza, A.; Brianti, V.; Fagnoni, F.; Snelli, G.; Monti, D.; Marcato, A.; Passeri, G.; Ortolani, C.; Forti, E.; et al. Lymphocyte subsets and natural killer cell activity in healthy old people and centenarians. Blood 1993, 82, 2767–2773. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mariani, E.; Monaco, M.C.; Cattini, L.; Sinoppi, M.; Facchini, A. Distribution and lytic activity of NK cell subsets in the elderly. Mech. Ageing Dev. 1994, 76, 177–187. [Google Scholar] [CrossRef]
- Kutza, J.; Murasko, D.M. Effects of aging on natural killer cell activity and activation by interleukin-2 and IFN-α. Cell. Immunol. 1994, 155, 195–204. [Google Scholar] [CrossRef] [PubMed]
- Kutza, J.; Murasko, D.M. Age-associated decline in IL-2 and IL-12 induction of LAK cell activity of human PBMC samples. Mech. Ageing Dev. 1996, 90, 209–222. [Google Scholar] [CrossRef]
- Mariani, E.; Sgobbi, S.; Meneghetti, A.; Tadolini, M.; Tarozzi, A.; Sinoppi, M.; Cattini, L.; Facchini, A. Perforins in human cytolytic cells: The effect of age. Mech. Ageing Dev. 1996, 92, 195–209. [Google Scholar] [CrossRef]
- Mariani, E.; Mariani, A.R.; Meneghetti, A.; Tarozzi, A.; Cocco, L.; Facchini, A. Age-dependent decreases of NK cell phosphoinositide turnover during spontaneous but not Fc-mediated cytolytic activity. Int. Immunol. 1998, 10, 981–989. [Google Scholar] [CrossRef] [Green Version]
- Borrego, F.; Alonso, M.C.; Galiani, M.D.; Carracedo, J.; Ramirez, R.; Ostos, B.; Pena, J.; Solana, R. NK phenotypic markers and IL2 response in NK cells from elderly people. Exp. Gerontol. 1999, 34, 253–265. [Google Scholar] [CrossRef]
- Lutz, C.T.; Moore, M.B.; Bradley, S.; Shelton, B.J.; Lutgendorf, S.K. Reciprocal age related change in natural killer cell receptors for MHC class I. Mech. Ageing Dev. 2005, 126, 722–731. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Le Garff-Tavernier, M.; Beziat, V.; Decocq, J.; Siguret, V.; Gandjbakhch, F.; Pautas, E.; Debre, P.; Merle-Beral, H.; Vieillard, V. Human NK cells display major phenotypic and functional changes over the life span. Aging Cell 2010, 9, 527–535. [Google Scholar] [CrossRef] [PubMed]
- Hayhoe, R.P.; Henson, S.M.; Akbar, A.N.; Palmer, D.B. Variation of human natural killer cell phenotypes with age: Identification of a unique KLRG1-negative subset. Hum. Immunol. 2010, 71, 676–681. [Google Scholar] [CrossRef] [PubMed]
- Almeida-Oliveira, A.; Smith-Carvalho, M.; Porto, L.C.; Cardoso-Oliveira, J.; Ribeiro Ados, S.; Falcao, R.R.; Abdelhay, E.; Bouzas, L.F.; Thuler, L.C.; Ornellas, M.H.; et al. Age-related changes in natural killer cell receptors from childhood through old age. Hum. Immunol. 2011, 72, 319–329. [Google Scholar] [CrossRef] [PubMed]
- Muller-Durovic, B.; Lanna, A.; Covre, L.P.; Mills, R.S.; Henson, S.M.; Akbar, A.N. Killer Cell Lectin-like Receptor G1 Inhibits NK Cell Function through Activation of Adenosine 5’-Monophosphate-Activated Protein Kinase. J. Immunol. 2016, 197, 2891–2899. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gounder, S.S.; Abdullah, B.J.J.; Radzuanb, N.; Zain, F.; Sait, N.B.M.; Chua, C.; Subramani, B. Effect of Aging on NK Cell Population and Their Proliferation at Ex Vivo Culture Condition. Anal. Cell. Pathol. 2018, 2018, 7871814. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Y.; Wallace, D.L.; de Lara, C.M.; Ghattas, H.; Asquith, B.; Worth, A.; Griffin, G.E.; Taylor, G.P.; Tough, D.F.; Beverley, P.C.; et al. In vivo kinetics of human natural killer cells: The effects of ageing and acute and chronic viral infection. Immunology 2007, 121, 258–265. [Google Scholar] [CrossRef] [PubMed]
- Crinier, A.; Milpied, P.; Escaliere, B.; Piperoglou, C.; Galluso, J.; Balsamo, A.; Spinelli, L.; Cervera-Marzal, I.; Ebbo, M.; Girard-Madoux, M.; et al. High-Dimensional Single-Cell Analysis Identifies Organ-Specific Signatures and Conserved NK Cell Subsets in Humans and Mice. Immunity 2018, 49, 971–986.e5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, C.; Siebert, J.R.; Burns, R.; Gerbec, Z.J.; Bonacci, B.; Rymaszewski, A.; Rau, M.; Riese, M.J.; Rao, S.; Carlson, K.S.; et al. Heterogeneity of human bone marrow and blood natural killer cells defined by single-cell transcriptome. Nat. Commun. 2019, 10, 3931. [Google Scholar] [CrossRef] [Green Version]
- Smith, S.L.; Kennedy, P.R.; Stacey, K.B.; Worboys, J.D.; Yarwood, A.; Seo, S.; Solloa, E.H.; Mistretta, B.; Chatterjee, S.S.; Gunaratne, P.; et al. Diversity of peripheral blood human NK cells identified by single-cell RNA sequencing. Blood Adv. 2020, 4, 1388–1406. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Liu, X.; Le, W.; Xie, L.; Li, H.; Wen, W.; Wang, S.; Ma, S.; Huang, Z.; Ye, J.; et al. A human circulating immune cell landscape in aging and COVID-19. Protein Cell 2020, 11, 740–770. [Google Scholar] [CrossRef] [PubMed]
- Dogra, P.; Rancan, C.; Ma, W.; Toth, M.; Senda, T.; Carpenter, D.J.; Kubota, M.; Matsumoto, R.; Thapa, P.; Szabo, P.A.; et al. Tissue Determinants of Human NK Cell Development, Function, and Residence. Cell 2020, 180, 749–763.e13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ogata, K.; An, E.; Shioi, Y.; Nakamura, K.; Luo, S.; Yokose, N.; Minami, S.; Dan, K. Association between natural killer cell activity and infection in immunologically normal elderly people. Clin. Exp. Immunol. 2001, 124, 392–397. [Google Scholar] [CrossRef] [PubMed]
- Ogata, K.; Yokose, N.; Tamura, H.; An, E.; Nakamura, K.; Dan, K.; Nomura, T. Natural killer cells in the late decades of human life. Clin. Immunol. Immunopathol. 1997, 84, 269–275. [Google Scholar] [CrossRef]
- Pierson, B.; Miller, J. CD56+bright and CD56+dim natural killer cells in patients with chronic myelogenous leukemia progressively decrease in number, respond less to stimuli that recruit clonogenic natural killer cells, and exhibit decreased proliferation on a per cell basis. Blood 1996, 88, 2279–2287. [Google Scholar] [CrossRef] [Green Version]
- Judge, S.J.; Murphy, W.J.; Canter, R.J. Characterizing the Dysfunctional NK Cell: Assessing the Clinical Relevance of Exhaustion, Anergy, and Senescence. Front. Cell. Infect. Microbiol. 2020, 10, 49. [Google Scholar] [CrossRef] [Green Version]
- Parameswaran, N.; Patial, S. Tumor necrosis factor-α signaling in macrophages. Crit. Rev. Eukaryot. Gene Expr. 2010, 20, 87–103. [Google Scholar] [CrossRef]
- Vieira, S.M.; Lemos, H.P.; Grespan, R.; Napimoga, M.H.; Dal-Secco, D.; Freitas, A.; Cunha, T.M.; Verri, W.A., Jr.; Souza-Junior, D.A.; Jamur, M.C.; et al. A crucial role for TNF-alpha in mediating neutrophil influx induced by endogenously generated or exogenous chemokines, KC/CXCL1 and LIX/CXCL5. Br. J. Pharm. 2009, 158, 779–789. [Google Scholar] [CrossRef] [Green Version]
- Billiau, A. Interferon-gamma: Biology and role in pathogenesis. Adv. Immunol. 1996, 62, 61–130. [Google Scholar] [CrossRef]
- Boehm, U.; Klamp, T.; Groot, M.; Howard, J.C. Cellular responses to interferon-γ. Annu. Rev. Immunol. 1997, 15, 749–795. [Google Scholar] [CrossRef] [PubMed]
- Soto-Gamez, A.; Quax, W.J.; Demaria, M. Regulation of Survival Networks in Senescent Cells: From Mechanisms to Interventions. J. Mol. Biol. 2019, 431, 2629–2643. [Google Scholar] [CrossRef] [PubMed]
- Carson, W.E.; Fehniger, T.A.; Haldar, S.; Eckhert, K.; Lindemann, M.J.; Lai, C.F.; Croce, C.M.; Baumann, H.; Caligiuri, M.A. A potential role for interleukin-15 in the regulation of human natural killer cell survival. J. Clin. Investig. 1997, 99, 937–943. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cooper, M.A.; Fehniger, T.A.; Caligiuri, M.A. The biology of human natural killer-cell subsets. Trends Immunol. 2001, 22, 633–640. [Google Scholar] [CrossRef]
- Pahlavani, M.A.; Richardson, A. The effect of age on the expression of interleukin-2. Mech. Ageing Dev. 1996, 89, 125–154. [Google Scholar] [CrossRef]
- Wu, Y.; Tian, Z.; Wei, H. Developmental and Functional Control of Natural Killer Cells by Cytokines. Front. Immunol. 2017, 8, 930. [Google Scholar] [CrossRef] [PubMed]
- Kaszubowska, L.; Foerster, J.; Schetz, D.; Kmiec, Z. CD56bright cells respond to stimulation until very advanced age revealing increased expression of cellular protective proteins SIRT1, HSP70 and SOD2. Immun. Ageing 2018, 15, 31. [Google Scholar] [CrossRef] [PubMed]
- Kaszubowska, L.; Foerster, J.; Kaczor, J.J.; Schetz, D.; Slebioda, T.J.; Kmiec, Z. NK cells of the oldest seniors represent constant and resistant to stimulation high expression of cellular protective proteins SIRT1 and HSP70. Immun. Ageing 2018, 15, 12. [Google Scholar] [CrossRef]
- Zhang, C.; Zhang, J.; Niu, J.; Zhou, Z.; Zhang, J.; Tian, Z. Interleukin-12 improves cytotoxicity of natural killer cells via upregulated expression of NKG2D. Hum. Immunol. 2008, 69, 490–500. [Google Scholar] [CrossRef]
- Gately, M.K.; Renzetti, L.M.; Magram, J.; Stern, A.S.; Adorini, L.; Gubler, U.; Presky, D.H. The interleukin-12/interleukin-12-receptor system: Role in normal and pathologic immune responses. Annu. Rev. Immunol. 1998, 16, 495–521. [Google Scholar] [CrossRef]
- Krishnaraj, R.; Bhooma, T. Cytokine sensitivity of human NK cells during immunosenescence. 2. IL2-induced interferon gamma secretion. Immunol. Lett. 1996, 50, 59–63. [Google Scholar] [CrossRef]
- Krishnaraj, R. Senescence and cytokines modulate the NK cell expression. Mech. Ageing Dev. 1997, 96, 89–101. [Google Scholar] [CrossRef]
- Mariani, E.; Pulsatelli, L.; Neri, S.; Dolzani, P.; Meneghetti, A.; Silvestri, T.; Ravaglia, G.; Forti, P.; Cattini, L.; Facchini, A. RANTES and MIP-1alpha production by T lymphocytes, monocytes and NK cells from nonagenarian subjects. Exp. Gerontol. 2002, 37, 219–226. [Google Scholar] [CrossRef]
- Mariani, E.; Meneghetti, A.; Neri, S.; Ravaglia, G.; Forti, P.; Cattini, L.; Facchini, A. Chemokine production by natural killer cells from nonagenarians. Eur. J. Immunol. 2002, 32, 1524–1529. [Google Scholar] [CrossRef]
- Mariani, E.; Pulsatelli, L.; Meneghetti, A.; Dolzani, P.; Mazzetti, I.; Neri, S.; Ravaglia, G.; Forti, P.; Facchini, A. Different IL-8 production by T and NK lymphocytes in elderly subjects. Mech. Ageing Dev. 2001, 122, 1383–1395. [Google Scholar] [CrossRef]
- Orange, J.S.; Ballas, Z.K. Natural killer cells in human health and disease. Clin. Immunol. 2006, 118, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Jost, S.; Altfeld, M. Control of human viral infections by natural killer cells. Annu. Rev. Immunol. 2013, 31, 163–194. [Google Scholar] [CrossRef] [PubMed]
- Hazeldine, J.; Lord, J.M. The impact of ageing on natural killer cell function and potential consequences for health in older adults. Ageing Res. Rev. 2013, 12, 1069–1078. [Google Scholar] [CrossRef] [PubMed]
- Henley, S.J.; Singh, S.D.; King, J.; Wilson, R.J.; O’Neil, M.E.; Ryerson, A.B. Invasive Cancer Incidence and Survival-United States, 2013. MMWR Morb. Mortal. Wkly. Rep. 2017, 66, 69–75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Balducci, L.; Ershler, W.B. Cancer and ageing: A nexus at several levels. Nat. Rev. Cancer 2005, 5, 655–662. [Google Scholar] [CrossRef] [PubMed]
- Moon, W.Y.; Powis, S.J. Does Natural Killer Cell Deficiency (NKD) Increase the Risk of Cancer? NKD May Increase the Risk of Some Virus Induced Cancer. Front. Immunol. 2019, 10, 1703. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kang, T.W.; Yevsa, T.; Woller, N.; Hoenicke, L.; Wuestefeld, T.; Dauch, D.; Hohmeyer, A.; Gereke, M.; Rudalska, R.; Potapova, A.; et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 2011, 479, 547–551. [Google Scholar] [CrossRef] [PubMed]
- Waldhauer, I.; Steinle, A. NK cells and cancer immunosurveillance. Oncogene 2008, 27, 5932–5943. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gross, E.; Sunwoo, J.B.; Bui, J.D. Cancer Immunosurveillance and Immunoediting by Natural Killer Cells. Cancer J. 2013, 19, 483–489. [Google Scholar] [CrossRef] [PubMed]
- López-Soto, A.; Gonzalez, S.; Smyth, M.J.; Galluzzi, L. Control of Metastasis by NK Cells. Cancer Cell 2017, 32, 135–154. [Google Scholar] [CrossRef] [PubMed]
- Talmadge, J.E.; Meyers, K.M.; Prieur, D.J.; Starkey, J.R. Role of NK cells in tumour growth and metastasis in beige mice. Nature 1980, 284, 622–624. [Google Scholar] [CrossRef] [PubMed]
- Hersey, P.; Edwards, A.; Honeyman, M.; McCarthy, W.H. Low natural-killer-cell activity in familial melanoma patients and their relatives. Br. J. Cancer 1979, 40, 113–122. [Google Scholar] [CrossRef] [Green Version]
- Strayer, D.R.; Carter, W.A.; Mayberry, S.D.; Pequignot, E.; Brodsky, I. Low natural cytotoxicity of peripheral blood mononuclear cells in individuals with high familial incidences of cancer. Cancer Res. 1984, 44, 370–374. [Google Scholar]
- Nakajima, T.; Mizushima, N.; Kanai, K. Relationship between natural killer activity and development of hepatocellular carcinoma in patients with cirrhosis of the liver. Jpn. J. Clin. Oncol. 1987, 17, 327–332. [Google Scholar]
- Imai, K.; Matsuyama, S.; Miyake, S.; Suga, K.; Nakachi, K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: An 11-year follow-up study of a general population. Lancet 2000, 356, 1795–1799. [Google Scholar] [CrossRef]
- Tarazona, R.; DelaRosa, O.; Alonso, C.; Ostos, B.; Espejo, J.; Pena, J.; Solana, R. Increased expression of NK cell markers on T lymphocytes in aging and chronic activation of the immune system reflects the accumulation of effector/senescent T cells. Mech. Ageing Dev. 2000, 121, 77–88. [Google Scholar] [CrossRef]
- Hazeldine, J.; Hampson, P.; Lord, J.M. Reduced release and binding of perforin at the immunological synapse underlies the age-related decline in natural killer cell cytotoxicity. Aging Cell 2012, 11, 751–759. [Google Scholar] [CrossRef] [PubMed]
- Maxwell, L.D.; Ross, O.A.; Curran, M.D.; Rea, I.M.; Middleton, D. Investigation of KIR diversity in immunosenescence and longevity within the Irish population. Exp. Gerontol. 2004, 39, 1223–1232. [Google Scholar] [CrossRef] [PubMed]
- Listi, F.; Caruso, C.; Colonna-Romano, G.; Lio, D.; Nuzzo, D.; Candore, G. HLA and KIR frequencies in Sicilian Centenarians. Rejuvenation Res. 2010, 13, 314–318. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rukavina, D.; Laskarin, G.; Rubesa, G.; Strbo, N.; Bedenicki, I.; Manestar, D.; Glavas, M.; Christmas, S.E.; Podack, E.R. Age-related decline of perforin expression in human cytotoxic T lymphocytes and natural killer cells. Blood 1998, 92, 2410–2420. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dustin, M.L.; Long, E.O. Cytotoxic immunological synapses. Immunol. Rev. 2010, 235, 24–34. [Google Scholar] [CrossRef] [PubMed]
- Maul-Pavicic, A.; Chiang, S.C.; Rensing-Ehl, A.; Jessen, B.; Fauriat, C.; Wood, S.M.; Sjoqvist, S.; Hufnagel, M.; Schulze, I.; Bass, T.; et al. ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc. Natl. Acad. Sci. USA 2011, 108, 3324–3329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McCarl, C.A.; Khalil, S.; Ma, J.; Oh-hora, M.; Yamashita, M.; Roether, J.; Kawasaki, T.; Jairaman, A.; Sasaki, Y.; Prakriya, M.; et al. Store-operated Ca2+ entry through ORAI1 is critical for T cell-mediated autoimmunity and allograft rejection. J. Immunol. 2010, 185, 5845–5858. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zweifach, A. Target-cell contact activates a highly selective capacitative calcium entry pathway in cytotoxic T lymphocytes. J. Cell Biol. 2000, 148, 603–614. [Google Scholar] [CrossRef] [Green Version]
- Schwindling, C.; Quintana, A.; Krause, E.; Hoth, M. Mitochondria positioning controls local calcium influx in T cells. J. Immunol. 2010, 184, 184–190. [Google Scholar] [CrossRef] [Green Version]
- Pores-Fernando, A.T.; Zweifach, A. Calcium influx and signaling in cytotoxic T-lymphocyte lytic granule exocytosis. Immunol. Rev. 2009, 231, 160–173. [Google Scholar] [CrossRef] [PubMed]
- Segal, M.; Korkotian, E. Endoplasmic reticulum calcium stores in dendritic spines. Front. Neuroanat. 2014, 8, 64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kopf, A.; Kiermaier, E. Dynamic Microtubule Arrays in Leukocytes and Their Role in Cell Migration and Immune Synapse Formation. Front. Cell Dev. Biol. 2021, 9, 635511. [Google Scholar] [CrossRef] [PubMed]
- Banerjee, P.P.; Pandey, R.; Zheng, R.; Suhoski, M.M.; Monaco-Shawver, L.; Orange, J.S. Cdc42-interacting protein-4 functionally links actin and microtubule networks at the cytolytic NK cell immunological synapse. J. Exp. Med. 2007, 204, 2305–2320. [Google Scholar] [CrossRef] [PubMed]
- Krzewski, K.; Coligan, J.E. Human NK cell lytic granules and regulation of their exocytosis. Front. Immunol. 2012, 3, 335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rabinowich, H.; Goses, Y.; Reshef, T.; Klajman, A. Interleukin-2 production and activity in aged humans. Mech. Ageing Dev. 1985, 32, 213–226. [Google Scholar] [CrossRef]
- Blank, C.U.; Haining, W.N.; Held, W.; Hogan, P.G.; Kallies, A.; Lugli, E.; Lynn, R.C.; Philip, M.; Rao, A.; Restifo, N.P.; et al. Defining ‘T cell exhaustion’. Nat. Rev. Immunol. 2019, 19, 665–674. [Google Scholar] [CrossRef] [PubMed]
- Wherry, E.J.; Kurachi, M. Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol. 2015, 15, 486–499. [Google Scholar] [CrossRef]
- Peng, Y.P.; Zhu, Y.; Zhang, J.J.; Xu, Z.K.; Qian, Z.Y.; Dai, C.C.; Jiang, K.R.; Wu, J.L.; Gao, W.T.; Li, Q.; et al. Comprehensive analysis of the percentage of surface receptors and cytotoxic granules positive natural killer cells in patients with pancreatic cancer, gastric cancer, and colorectal cancer. J. Transl. Med. 2013, 11, 262. [Google Scholar] [CrossRef] [Green Version]
- Sun, C.; Sun, H.Y.; Xiao, W.H.; Zhang, C.; Tian, Z.G. Natural killer cell dysfunction in hepatocellular carcinoma and NK cell-based immunotherapy. Acta Pharm. Sin. 2015, 36, 1191–1199. [Google Scholar] [CrossRef] [Green Version]
- Fali, T.; Papagno, L.; Bayard, C.; Mouloud, Y.; Boddaert, J.; Sauce, D.; Appay, V. New Insights into Lymphocyte Differentiation and Aging from Telomere Length and Telomerase Activity Measurements. J. Immunol. 2019, 202, 1962–1969. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mariani, E.; Meneghetti, A.; Formentini, I.; Neri, S.; Cattini, L.; Ravaglia, G.; Forti, P.; Facchini, A. Telomere length and telomerase activity: Effect of ageing on human NK cells. Mech. Ageing Dev. 2003, 124, 403–408. [Google Scholar] [CrossRef]
- Ouyang, Q.; Baerlocher, G.; Vulto, I.; Lansdorp, P.M. Telomere length in human natural killer cell subsets. Ann. N. Y. Acad. Sci. 2007, 1106, 240–252. [Google Scholar] [CrossRef] [PubMed]
- Rea, I.M.; Gibson, D.S.; McGilligan, V.; McNerlan, S.E.; Alexander, H.D.; Ross, O.A. Age and Age-Related Diseases: Role of Inflammation Triggers and Cytokines. Front. Immunol. 2018, 9, 586. [Google Scholar] [CrossRef] [PubMed]
- Alemán, H.; Esparza, J.; Ramirez, F.A.; Astiazaran, H.; Payette, H. Longitudinal evidence on the association between interleukin-6 and C-reactive protein with the loss of total appendicular skeletal muscle in free-living older men and women. Age Aging 2011, 40, 469–475. [Google Scholar] [CrossRef] [Green Version]
- Wang, T.; He, C. Pro-inflammatory cytokines: The link between obesity and osteoarthritis. Cytokine Growth Factor Rev. 2018, 44, 38–50. [Google Scholar] [CrossRef]
- Swardfager, W.; Lanctôt, K.; Rothenburg, L.; Wong, A.; Cappell, J.; Herrmann, N. A Meta-Analysis of Cytokines in Alzheimer’s Disease. Biol. Psychiatry 2010, 68, 930–941. [Google Scholar] [CrossRef]
- Shehata, H.M.; Hoebe, K.; Chougnet, C.A. The aged nonhematopoietic environment impairs natural killer cell maturation and function. Aging Cell 2015, 14, 191–199. [Google Scholar] [CrossRef]
- Sungur, C.M.; Murphy, W.J. Utilization of mouse models to decipher natural killer cell biology and potential clinical applications. Hematology 2013, 2013, 227–233. [Google Scholar] [CrossRef]
- Quinn, L.S.; Anderson, B.G.; Strait-Bodey, L.; Wolden-Hanson, T. Serum and muscle interleukin-15 levels decrease in aging mice: Correlation with declines in soluble interleukin-15 receptor alpha expression. Exp. Gerontol. 2010, 45, 106–112. [Google Scholar] [CrossRef] [Green Version]
- Jergovic, M.; Thompson-Ryder, H.L.; Asghar, A.; Nikolich-Zugich, J. The role of Interleukin-6 in age-related frailty syndrome. J. Immunol. 2020, 204, 59.17. [Google Scholar]
- Liu, H.; Huang, Y.; Lyu, Y.; Dai, W.; Tong, Y.; Li, Y. GDF15 as a biomarker of ageing. Exp. Gerontol. 2021, 146, 111228. [Google Scholar] [CrossRef] [PubMed]
- Tavenier, J.; Rasmussen, L.J.H.; Andersen, A.L.; Houlind, M.B.; Langkilde, A.; Andersen, O.; Petersen, J.; Nehlin, J.O. Association of GDF15 with Inflammation and Physical Function during Aging and Recovery after Acute Hospitalization: A Longitudinal Study of Older Patients and Age-Matched Controls. J. Gerontol. Ser. A 2021, 76, 964–974. [Google Scholar] [CrossRef]
- Tomescu, C.; Chehimi, J.; Maino, V.C.; Montaner, L.J. Retention of viability, cytotoxicity, and response to IL-2, IL-15, or IFN-alpha by human NK cells after CD107a degranulation. J. Leukoc. Biol. 2009, 85, 871–876. [Google Scholar] [CrossRef] [PubMed]
- Widowati, W.; Jasaputra, D.K.; Sumitro, S.B.; Widodo, M.A.; Mozef, T.; Rizal, R.; Kusuma, H.S.; Laksmitawati, D.R.; Murti, H.; Bachtiar, I.; et al. Effect of interleukins (IL-2, IL-15, IL-18) on receptors activation and cytotoxic activity of natural killer cells in breast cancer cell. Afr. Health Sci. 2020, 20, 822–832. [Google Scholar] [CrossRef] [PubMed]
- Hammarsten, J.; Holm, J.; Schersten, T. Incidence of bacteria after skin wash of surgical patients in hospitals. Lakartidningen 1979, 76, 969–970. [Google Scholar]
- Ligthart, G.J.; Corberand, J.X.; Fournier, C.; Galanaud, P.; Hijmans, W.; Kennes, B.; Müller-Hermelink, H.K.; Steinmann, G.G. Admission criteria for immunogerontological studies in man: The SENIEUR protocol. Mech. Ageing Dev. 1984, 28, 47–55. [Google Scholar] [CrossRef]
- Wiencke, J.K.; Butler, R.; Hsuang, G.; Eliot, M.; Kim, S.; Sepulveda, M.A.; Siegel, D.; Houseman, E.A.; Kelsey, K.T. The DNA methylation profile of activated human natural killer cells. Epigenetics 2016, 11, 363–380. [Google Scholar] [CrossRef] [Green Version]
- Schenk, A.; Bloch, W.; Zimmer, P. Natural Killer Cells—An Epigenetic Perspective of Development and Regulation. Int. J. Mol. Sci. 2016, 17, 326. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cichocki, F.; Miller, J.; Anderson, S.; Bryceson, Y. Epigenetic regulation of NK cell differentiation and effector functions. Front. Immunol. 2013, 4, 55. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merino, A.; Zhang, B.; Dougherty, P.; Luo, X.; Wang, J.; Blazar, B.R.; Miller, J.S.; Cichocki, F. Chronic stimulation drives human NK cell dysfunction and epigenetic reprograming. J. Clin. Investig. 2019, 129, 3770–3785. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zimmer, P.; Bloch, W.; Schenk, A.; Zopf, E.M.; Hildebrandt, U.; Streckmann, F.; Beulertz, J.; Koliamitra, C.; Schollmayer, F.; Baumann, F. Exercise-induced Natural Killer Cell Activation is Driven by Epigenetic Modifications. Int. J. Sports Med. 2015, 36, 510–515. [Google Scholar] [CrossRef] [PubMed]
- Misale, M.S.; Witek Janusek, L.; Tell, D.; Mathews, H.L. Chromatin organization as an indicator of glucocorticoid induced natural killer cell dysfunction. Brain Behav. Immun. 2018, 67, 279–289. [Google Scholar] [CrossRef] [PubMed]
- Jonkman, T.H.; Dekkers, K.F.; Slieker, R.C.; Grant, C.D.; Ikram, M.A.; van Greevenbroek, M.M.J.; Franke, L.; Veldink, J.H.; Boomsma, D.I.; Slagboom, P.E.; et al. Functional genomics analysis identifies T and NK cell activation as a driver of epigenetic clock progression. Genome Biol. 2022, 23, 24. [Google Scholar] [CrossRef]
- Wyman, P.A.; Moynihan, J.; Eberly, S.; Cox, C.; Cross, W.; Jin, X.; Caserta, M.T. Association of Family Stress with Natural Killer Cell Activity and the Frequency of Illnesses in Children. Arch. Pediatrics Adolesc. Med. 2007, 161, 228–234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Holbrook, N.J.; Cox, W.I.; Horner, H.C. Direct suppression of natural killer activity in human peripheral blood leukocyte cultures by glucocorticoids and its modulation by interferon. Cancer Res. 1983, 43, 4019–4025. [Google Scholar] [PubMed]
- Nair, M.P.; Schwartz, S.A. Immunomodulatory effects of corticosteroids on natural killer and antibody-dependent cellular cytotoxic activities of human lymphocytes. J. Immunol. 1984, 132, 2876–2882. [Google Scholar]
- Parrillo, J.E.; Fauci, A.S. Comparison of the Effector Cells in Human Spontaneous Cellular Cytotoxicity and Antibody-Dependent Cellular Cytotoxicity: Differential Sensitivity of Effector Cells to In Vivo and In Vitro Corticosteroids. Scand. J. Immunol. 1978, 8, 99–107. [Google Scholar] [CrossRef]
- Yiallouris, A.; Tsioutis, C.; Agapidaki, E.; Zafeiri, M.; Agouridis, A.P.; Ntourakis, D.; Johnson, E.O. Adrenal Aging and Its Implications on Stress Responsiveness in Humans. Front. Endocrinol. 2019, 10, 54. [Google Scholar] [CrossRef]
- Luz, C.; Dornelles, F.; Preissler, T.; Collaziol, D.; da Cruz, I.M.; Bauer, M.E. Impact of psychological and endocrine factors on cytokine production of healthy elderly people. Mech. Ageing Dev. 2003, 124, 887–895. [Google Scholar] [CrossRef]
- Gatti, G.; Cavallo, R.; Sartori, M.L.; del Ponte, D.; Masera, R.; Salvadori, A.; Carignola, R.; Angeli, A. Inhibition by cortisol of human natural killer (NK) cell activity. J. Steroid Biochem. 1987, 26, 49–58. [Google Scholar] [CrossRef]
- Eddy, J.L.; Krukowski, K.; Janusek, L.; Mathews, H.L. Glucocorticoids regulate natural killer cell function epigenetically. Cell. Immunol. 2014, 290, 120–130. [Google Scholar] [CrossRef] [Green Version]
- Duan, X.; Lu, J.; Wang, H.; Liu, X.; Wang, J.; Zhou, K.; Jiang, W.; Wang, Y.; Fang, M. Bidirectional factors impact the migration of NK cells to draining lymph node in aged mice during influenza virus infection. Exp. Gerontol. 2017, 96, 127–137. [Google Scholar] [CrossRef] [PubMed]
- Hellstrand, K.; Hermodsson, S.; Strannegård, O. Evidence for a beta-adrenoceptor-mediated regulation of human natural killer cells. J. Immunol. 1985, 134, 4095–4099. [Google Scholar] [PubMed]
- Sun, Z.; Hou, D.; Liu, S.; Fu, W.; Wang, J.; Liang, Z. Norepinephrine inhibits the cytotoxicity of NK92-MI cells via the β2-adrenoceptor/cAMP/PKA/p-CREB signaling pathway. Mol. Med. Rep. 2018, 17, 8530–8535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stepien, H.; Zelazowski, P.; Döhler, K.D.; Pawlikowski, M. Neuropeptides and Natural Killer Cell Activity. In Progress in Neuropeptide Research; Birkhäuser: Basel, Switzerland, 1988; pp. 25–31. [Google Scholar] [CrossRef]
- Koller, A.; Bianchini, R.; Schlager, S.; Münz, C.; Kofler, B.; Wiesmayr, S. The neuropeptide galanin modulates natural killer cell function. Neuropeptides 2017, 64, 109–115. [Google Scholar] [CrossRef] [PubMed]
- Feistritzer, C.; Clausen, J.; Sturn, D.H.; Djanani, A.; Gunsilius, E.; Wiedermann, C.J.; Kähler, C.M. Natural killer cell functions mediated by the neuropeptide substance P. Regul. Pept. 2003, 116, 119–126. [Google Scholar] [CrossRef]
- Mazzatenta, A.; Marconi, G.D.; Zara, S.; Cataldi, A.; Porzionato, A.; Di Giulio, C. In the carotid body, galanin is a signal for neurogenesis in young, and for neurodegeneration in the old and in drug-addicted subjects. Front. Physiol. 2014, 5, 427. [Google Scholar] [CrossRef] [Green Version]
- Barbariga, M.; Rabiolo, A.; Fonteyne, P.; Bignami, F.; Rama, P.; Ferrari, G. The Effect of Aging on Nerve Morphology and Substance P Expression in Mouse and Human Corneas. Investig. Ophthalmol. Vis. Sci. 2018, 59, 5329–5335. [Google Scholar] [CrossRef] [Green Version]
- Ni, F.; Sun, R.; Fu, B.; Wang, F.; Guo, C.; Tian, Z.; Wei, H. IGF-1 promotes the development and cytotoxic activity of human NK cells. Nat. Commun. 2013, 4, 1479. [Google Scholar] [CrossRef]
- Bidlingmaier, M.; Friedrich, N.; Emeny, R.T.; Spranger, J.; Wolthers, O.D.; Roswall, J.; Körner, A.; Obermayer-Pietsch, B.; Hübener, C.; Dahlgren, J.; et al. Reference intervals for insulin-like growth factor-1 (igf-i) from birth to senescence: Results from a multicenter study using a new automated chemiluminescence IGF-I immunoassay conforming to recent international recommendations. J. Clin. Endocrinol. Metab. 2014, 99, 1712–1721. [Google Scholar] [CrossRef] [PubMed]
- Sonntag, W.E.; Ramsey, M.; Carter, C.S. Growth hormone and insulin-like growth factor-1 (IGF-1) and their influence on cognitive aging. Ageing Res. Rev. 2005, 4, 195–212. [Google Scholar] [CrossRef]
- Salminen, A. Feed-forward regulation between cellular senescence and immunosuppression promotes the aging process and age-related diseases. Ageing Res. Rev. 2021, 67, 101280. [Google Scholar] [CrossRef]
- O’Connor, J.C.; McCusker, R.H.; Strle, K.; Johnson, R.W.; Dantzer, R.; Kelley, K.W. Regulation of IGF-I function by proinflammatory cytokines: At the interface of immunology and endocrinology. Cell. Immunol. 2008, 252, 91–110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, S.; Tang, T.; Wu, X.; Mansour, A.G.; Lu, T.; Zhang, J.; Wang, L.S.; Caligiuri, M.A.; Yu, J. PDGF-D-PDGFRβ signaling enhances IL-15-mediated human natural killer cell survival. Proc. Natl. Acad. Sci. USA 2022, 119, e2114134119. [Google Scholar] [CrossRef] [PubMed]
- Barrow, A.D.; Edeling, M.A.; Trifonov, V.; Luo, J.; Goyal, P.; Bohl, B.; Bando, J.K.; Kim, A.H.; Walker, J.; Andahazy, M.; et al. Natural Killer Cells Control Tumor Growth by Sensing a Growth Factor. Cell 2018, 172, 534–548.e19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Drubaix, I.; Giakoumakis, A.; Robert, L.; Robert, A.M. Preliminary data on the age-dependent decrease in basic fibroblast growth factor and platelet-derived growth factor in the human vein wall and in their influence on cell proliferation. Gerontology 1998, 44, 9–14. [Google Scholar] [CrossRef] [PubMed]
- Benatti, B.B.; Silvério, K.G.; Casati, M.Z.; Sallum, E.A.; Nociti, F.H., Jr. Influence of aging on biological properties of periodontal ligament cells. Connect. Tissue Res. 2008, 49, 401–408. [Google Scholar] [CrossRef]
- Zhou, L.; Dong, J.; Yu, M.; Yin, H.; She, M. Age-dependent increase of NF-κB translocation and PDGF-B expression in aortic endothelial cells of hypercholesterolemic rats. Exp. Gerontol. 2003, 38, 1161–1168. [Google Scholar] [CrossRef]
- Slattery, K.; Gardiner, C.M. NK Cell Metabolism and TGF–Implications for Immunotherapy. Front. Immunol. 2019, 10, 2915. [Google Scholar] [CrossRef] [Green Version]
- Wilson, E.B.; El-Jawhari, J.J.; Neilson, A.L.; Hall, G.D.; Melcher, A.A.; Meade, J.L.; Cook, G.P. Human tumour immune evasion via TGF-β blocks NK cell activation but not survival allowing therapeutic restoration of anti-tumour activity. PLoS ONE 2011, 6, e22842. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Viel, S.; Marçais, A.; Guimaraes, F.S.-F.; Loftus, R.; Rabilloud, J.; Grau, M.; Degouve, S.; Djebali, S.; Sanlaville, A.; Charrier, E. TGF-β inhibits the activation and functions of NK cells by repressing the mTOR pathway. Sci. Signal. 2016, 9, ra19. [Google Scholar] [CrossRef] [PubMed]
- Castriconi, R.; Cantoni, C.; Della Chiesa, M.; Vitale, M.; Marcenaro, E.; Conte, R.; Biassoni, R.; Bottino, C.; Moretta, L.; Moretta, A. Transforming growth factor β1 inhibits expression of NKp30 and NKG2D receptors: Consequences for the NK-mediated killing of dendritic cells. Proc. Natl. Acad. Sci. USA 2003, 100, 4120–4125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lazarova, M.; Steinle, A. Impairment of NKG2D-Mediated Tumor Immunity by TGF-β. Front. Immunol. 2019, 10, 2689. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Frippiat, C.; Chen, Q.M.; Zdanov, S.; Magalhaes, J.P.; Remacle, J.; Toussaint, O. Subcytotoxic H2O2 stress triggers a release of transforming growth factor-beta 1, which induces biomarkers of cellular senescence of human diploid fibroblasts. J. Biol. Chem. 2001, 276, 2531–2537. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Forsey, R.J.; Thompson, J.M.; Ernerudh, J.; Hurst, T.L.; Strindhall, J.; Johansson, B.; Nilsson, B.O.; Wikby, A. Plasma cytokine profiles in elderly humans. Mech. Ageing Dev. 2003, 124, 487–493. [Google Scholar] [CrossRef]
- Anstey, K.; Stankov, L.; Lord, S. Primary aging, secondary aging, and intelligence. Psychol. Aging 1993, 8, 562–570. [Google Scholar] [CrossRef] [PubMed]
- Busse, E.W.; Pfeiffer, E. Behavior and Adaptation in Late Life; Little, Brown: Boston, MA, USA, 1977. [Google Scholar]
- Zhimulev, I.F.; Belyaeva, E.S.; Bgatov, A.V.; Baricheva, E.M.; Vlassova, I.E. Cytogenetic and molecular aspects of position effect variegation in Drosophila melanogaster. II. Peculiarities of morphology and genetic activity of the 2B region in the T(1;2)dorvar7 chromosome in males. Chromosoma 1988, 96, 255–261. [Google Scholar] [CrossRef] [PubMed]
- Zealley, B.; de Grey, A.D. Strategies for engineered negligible senescence. Gerontology 2013, 59, 183–189. [Google Scholar] [CrossRef] [PubMed]
- Cabrera, Á.J.R. Zinc, aging, and immunosenescence: An overview. Pathobiol. Aging Age-Relat. Dis. 2015, 5, 25592. [Google Scholar] [CrossRef]
- Prasad, A.S.; Fitzgerald, J.T.; Hess, J.W.; Kaplan, J.; Pelen, F.; Dardenne, M. Zinc deficiency in elderly patients. Nutrition 1993, 9, 218–224. [Google Scholar] [PubMed]
- Stover, P.J. Vitamin B12 and older adults. Curr. Opin. Clin. Nutr. Metab. Care 2010, 13, 24–27. [Google Scholar] [CrossRef] [PubMed]
- Wolters, M.; Ströhle, A.; Hahn, A. Age-associated changes in the metabolism of vitamin B(12) and folic acid: Prevalence, aetiopathogenesis and pathophysiological consequences. Z. Gerontol. Geriatr. 2004, 37, 109–135. [Google Scholar] [CrossRef] [PubMed]
- Wintergerst, E.S.; Maggini, S.; Hornig, D.H. Contribution of selected vitamins and trace elements to immune function. Ann. Nutr. Metab. 2007, 51, 301–323. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haase, H.; Mocchegiani, E.; Rink, L. Correlation between zinc status and immune function in the elderly. Biogerontology 2006, 7, 421–428. [Google Scholar] [CrossRef] [PubMed]
- Elmadfa, I.; Meyer, A.L. The Role of the Status of Selected Micronutrients in Shaping the Immune Function. Endocr. Metab. Immune Disord. Drug Targets 2019, 19, 1100–1115. [Google Scholar] [CrossRef] [PubMed]
- Mikkelsen, K.; Apostolopoulos, V. Vitamin B12, Folic Acid, and the Immune System. In Nutrition and Immunity; Springer: Cham, Switzerland, 2019; pp. 103–114. [Google Scholar] [CrossRef]
- Nour Zahi Gammoh, L.R. Zinc in Infection and Inflammation. Nutrients 2017, 9, 624. [Google Scholar] [CrossRef] [Green Version]
- Mertens, K.; Lowes, D.A.; Webster, N.R.; Talib, J.; Hall, L.; Davies, M.J.; Beattie, J.H.; Galley, H.F. Low zinc and selenium concentrations in sepsis are associated with oxidative damage and inflammation. Br. J. Anasthesia 2015, 114, 990–999. [Google Scholar] [CrossRef] [Green Version]
- Busse, B.; Bale, H.A.; Zimmermann, E.A.; Panganiban, B.; Barth, H.D.; Carriero, A.; Vettorazzi, E.; Zustin, J.; Hahn, M.; Ager, J.W., 3rd; et al. Vitamin D deficiency induces early signs of aging in human bone, increasing the risk of fracture. Sci. Transl. Med. 2013, 5, 193ra188. [Google Scholar] [CrossRef] [PubMed]
- Chung, M.; Lee, J.; Terasawa, T.; Lau, J.; Trikalinos, T.A. Vitamin D with or without calcium supplementation for prevention of cancer and fractures: An updated meta-analysis for the U.S. Preventive Services Task Force. Ann. Intern. Med. 2011, 155, 827–838. [Google Scholar] [CrossRef] [Green Version]
- Kruman, I.I.; Kumaravel, T.S.; Lohani, A.; Pedersen, W.A.; Cutler, R.G.; Kruman, Y.; Haughey, N.; Lee, J.; Evans, M.; Mattson, M.P. Folic Acid Deficiency and Homocysteine Impair DNA Repair in Hippocampal Neurons and Sensitize Them to Amyloid Toxicity in Experimental Models of Alzheimer’s Disease. J. Neurosci. 2002, 22, 1752–1762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clarke, R.; Smith, A.D.; Jobst, K.A.; Refsum, H.; Sutton, L.; Ueland, P.M. Folate, vitamin B12, and serum total homocysteine levels in confirmed Alzheimer disease. Arch. Neurol. 1998, 55, 1449–1455. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Partearroyo, T.; Úbeda, N.; Montero, A.; Achón, M.; Varela-Moreiras, G. Vitamin B12 and Folic Acid Imbalance Modifies NK Cytotoxicity, Lymphocytes B and Lymphoprolipheration in Aged Rats. Nutrients 2013, 5, 4836–4848. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vassiliou, A.G.; Jahaj, E.; Pratikaki, M.; Keskinidou, C.; Detsika, M.; Grigoriou, E.; Psarra, K.; Orfanos, S.E.; Tsirogianni, A.; Dimopoulou, I.; et al. Vitamin D deficiency correlates with a reduced number of natural killer cells in intensive care unit (ICU) and non-ICU patients with COVID-19 pneumonia. Hell. J. Cardiol. 2021, 62, 381. [Google Scholar] [CrossRef] [PubMed]
- Tamura, J.; Kubota, K.; Murakami, H.; Sawamura, M.; Matsushima, T.; Tamura, T.; Saitoh, T.; Kurabayshi, H.; Naruse, T. Immunomodulation by vitamin B12: Augmentation of CD8+ T lymphocytes and natural killer (NK) cell activity in vitamin B12-deficient patients by methyl-B12 treatment. Clin. Exp. Immunol. 2001, 116, 28–32. [Google Scholar] [CrossRef] [PubMed]
- Mariani, E.; Neri, S.; Cattini, L.; Mocchegiani, E.; Malavolta, M.; Dedoussis, G.V.; Kanoni, S.; Rink, L.; Jajte, J.; Facchini, A. Effect of zinc supplementation on plasma IL-6 and MCP-1 production and NK cell function in healthy elderly: Interactive influence of +647 MT1a and −174 IL-6 polymorphic alleles. Exp. Gerontol. 2008, 43, 462–471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gill, H.S.; Rutherfurd, K.J.; Cross, M.L. Dietary probiotic supplementation enhances natural killer cell activity in the elderly: An investigation of age-related immunological changes. J. Clin. Immunol. 2001, 21, 264–271. [Google Scholar] [CrossRef] [PubMed]
- Bunout, D.; Barrera, G.; Hirsch, S.; Gattas, V.; de la Maza, M.P.; Haschke, F.; Steenhout, P.; Klassen, P.; Hager, C.; Avendaño, M.; et al. Effects of a nutritional supplement on the immune response and cytokine production in free-living Chilean elderly. JPEN J. Parenter. Enter. Nutr. 2004, 28, 348–354. [Google Scholar] [CrossRef]
- Martineau, A.R.; Jolliffe, D.A.; Hooper, R.L.; Greenberg, L.; Aloia, J.F.; Bergman, P.; Dubnov-Raz, G.; Esposito, S.; Ganmaa, D.; Ginde, A.A.; et al. Vitamin D supplementation to prevent acute respiratory tract infections: Systematic review and meta-analysis of individual participant data. BMJ 2017, 356, i6583. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, J.; Mei, K.; Xie, L.; Yuan, P.; Ma, J.; Yu, P.; Zhu, W.; Zheng, C.; Liu, X. Low vitamin D levels do not aggravate COVID-19 risk or death, and vitamin D supplementation does not improve outcomes in hospitalized patients with COVID-19: A meta-analysis and GRADE assessment of cohort studies and RCTs. Nutr. J. 2021, 20, 89. [Google Scholar] [CrossRef]
- Dancer, R.C.; Parekh, D.; Lax, S.; D’Souza, V.; Zheng, S.; Bassford, C.R.; Park, D.; Bartis, D.G.; Mahida, R.; Turner, A.M.; et al. Vitamin D deficiency contributes directly to the acute respiratory distress syndrome (ARDS). Thorax 2015, 70, 617–624. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Al-Beltagi, M.; Rowiesha, M.; Elmashad, A.; Elrifaey, S.M.; Elhorany, H.; Koura, H.G. Vitamin D status in preterm neonates and the effects of its supplementation on respirat.tory distress syndrome. Pediatr. Pulmonol. 2020, 55, 108–115. [Google Scholar] [CrossRef] [PubMed]
- Mariani, E.; Ravaglia, G.; Forti, P.; Meneghetti, A.; Tarozzi, A.; Maioli, F.; Boschi, F.; Pratelli, L.; Pizzoferrato, A.; Piras, F.; et al. Vitamin D, thyroid hormones and muscle mass influence natural killer (NK) innate immunity in healthy nonagenarians and centenarians. Clin. Exp. Immunol. 1999, 116, 19–27. [Google Scholar] [CrossRef] [PubMed]
- Lewis, E.D.; Meydani, S.N.; Wu, D. Regulatory role of vitamin E in the immune system and inflammation. IUBMB Life 2019, 71, 487–494. [Google Scholar] [CrossRef] [PubMed]
- Wu, D.; Meydani, S.N. Age-associated changes in immune function: Impact of vitamin E intervention and the underlying mechanisms. Endocr. Metab. Immune Disord. Drug Targets 2014, 14, 283–289. [Google Scholar] [CrossRef]
- Madison, A.A.; Shrout, M.R.; Renna, M.E.; Kiecolt-Glaser, J.K. Psychological and Behavioral Predictors of Vaccine Efficacy: Considerations for COVID-19. Perspect. Psychol. Sci. 2021, 16, 191–203. [Google Scholar] [CrossRef] [PubMed]
- Cohen, S.; Tyrrell, D.A.; Smith, A.P. Psychological stress and susceptibility to the common cold. N. Engl. J. Med. 1991, 325, 606–612. [Google Scholar] [CrossRef]
- Glaser, R.; Sheridan, J.; Malarkey, W.B.; MacCallum, R.C.; Kiecolt-Glaser, J.K. Chronic stress modulates the immune response to a pneumococcal pneumonia vaccine. Psychosom. Med. 2000, 62, 804–807. [Google Scholar] [CrossRef]
- Kohut, M.L.; Lee, W.; Martin, A.; Arnston, B.; Russell, D.W.; Ekkekakis, P.; Yoon, K.J.; Bishop, A.; Cunnick, J.E. The exercise-induced enhancement of influenza immunity is mediated in part by improvements in psychosocial factors in older adults. Brain Behav. Immun. 2005, 19, 357–366. [Google Scholar] [CrossRef]
- De Lorenzo, B.H.; de Oliveira Marchioro, L.; Greco, C.R.; Suchecki, D. Sleep-deprivation reduces NK cell number and function mediated by β-adrenergic signalling. Psychoneuroendocrinology 2015, 57, 134–143. [Google Scholar] [CrossRef]
- Vedhara, K.; Ayling, K.; Sunger, K.; Caldwell, D.M.; Halliday, V.; Fairclough, L.; Avery, A.; Robles, L.; Garibaldi, J.; Welton, N.J.; et al. Psychological interventions as vaccine adjuvants: A systematic review. Vaccine 2019, 37, 3255–3266. [Google Scholar] [CrossRef] [PubMed]
- Held, K.; Antonijevic, I.A.; Künzel, H.; Uhr, M.; Wetter, T.C.; Golly, I.C.; Steiger, A.; Murck, H. Oral Mg2+ supplementation reverses age-related neuroendocrine and sleep EEG changes in humans. Pharmacopsychiatry 2002, 35, 135–143. [Google Scholar] [CrossRef] [PubMed]
- Abbasi, B.; Kimiagar, M.; Sadeghniiat, K.; Shirazi, M.M.; Hedayati, M.; Rashidkhani, B. The effect of magnesium supplementation on primary insomnia in elderly: A double-blind placebo-controlled clinical trial. J. Res. Med. Sci. 2012, 17, 1161–1169. [Google Scholar] [PubMed]
- Mander, B.A.; Winer, J.R.; Walker, M.P. Sleep and Human Aging. Neuron 2017, 94, 19–36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abbott, S.M.; Videnovic, A. Chronic sleep disturbance and neural injury: Links to neurodegenerative disease. Nat. Sci. Sleep 2016, 8, 55–61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, T.; Mariani, S.; Redline, S. Sleep Irregularity and Risk of Cardiovascular Events: The Multi-Ethnic Study of Atherosclerosis. J. Am. Coll. Cardiol. 2020, 75, 991–999. [Google Scholar] [CrossRef]
- Garbarino, S.; Lanteri, P.; Bragazzi, N.L.; Magnavita, N.; Scoditti, E. Role of sleep deprivation in immune-related disease risk and outcomes. Commun. Biol. 2021, 4, 1304. [Google Scholar] [CrossRef] [PubMed]
- Guida, J.L.; Alfini, A.J.; Gallicchio, L.; Spira, A.P.; Caporaso, N.E.; Green, P.A. Association of objectively measured sleep with frailty and 5-year mortality in community-dwelling older adults. Sleep 2021, 44, zsab003. [Google Scholar] [CrossRef]
- Cappuccio, F.P.; D’Elia, L.; Strazzullo, P.; Miller, M.A. Sleep duration and all-cause mortality: A systematic review and meta-analysis of prospective studies. Sleep 2010, 33, 585–592. [Google Scholar] [CrossRef]
- Kripke, D.F.; Langer, R.D.; Elliott, J.A.; Klauber, M.R.; Rex, K.M. Mortality related to actigraphic long and short sleep. Sleep Med. 2011, 12, 28–33. [Google Scholar] [CrossRef] [Green Version]
- Besedovsky, L.; Lange, T.; Haack, M. The Sleep-Immune Crosstalk in Health and Disease. Physiol. Rev. 2019, 99, 1325–1380. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Besedovsky, L.; Lange, T.; Born, J. Sleep and immune function. Pflug. Arch. 2012, 463, 121–137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matsumoto, Y.; Mishima, K.; Satoh, K.; Tozawa, T.; Mishima, Y.; Shimizu, T.; Hishikawa, Y. Total sleep deprivation induces an acute and transient increase in NK cell activity in healthy young volunteers. Sleep 2001, 24, 804–809. [Google Scholar] [PubMed] [Green Version]
- Irwin, M.; McClintick, J.; Costlow, C.; Fortner, M.; White, J.; Gillin, J.C. Partial night sleep deprivation reduces natural killer and cellular immune responses in humans. FASEB J. 1996, 10, 643–653. [Google Scholar] [CrossRef] [PubMed]
- Irwin, M.; Mascovich, A.; Gillin, J.C.; Willoughby, R.; Pike, J.; Smith, T.L. Partial sleep deprivation reduces natural killer cell activity in humans. Psychosom. Med. 1994, 56, 493–498. [Google Scholar] [CrossRef] [PubMed]
- Fondell, E.; Axelsson, J.; Franck, K.; Ploner, A.; Lekander, M.; Bälter, K.; Gaines, H. Short natural sleep is associated with higher T cell and lower NK cell activities. Brain Behav. Immun. 2011, 25, 1367–1375. [Google Scholar] [CrossRef] [PubMed]
- Shakhar, K.; Valdimarsdottir, H.B.; Guevarra, J.S.; Bovbjerg, D.H. Sleep, fatigue, and NK cell activity in healthy volunteers: Significant relationships revealed by within subject analyses. Brain Behav. Immun. 2007, 21, 180–184. [Google Scholar] [CrossRef]
- De Lorenzo, B.H.P.; Novaes, E.B.R.R.; Paslar Leal, T.; Piqueira Garcia, N.; Martins Dos Santos, R.M.; Alvares-Saraiva, A.M.; Perez Hurtado, E.C.; Braga Dos Reis, T.C.; Duarte Palma, B. Chronic Sleep Restriction Impairs the Antitumor Immune Response in Mice. Neuroimmunomodulation 2018, 25, 59–67. [Google Scholar] [CrossRef] [PubMed]
- Huang, J.; Song, P.; Hang, K.; Chen, Z.; Zhu, Z.; Zhang, Y.; Xu, J.; Qin, J.; Wang, B.; Qu, W.; et al. Sleep Deprivation Disturbs Immune Surveillance and Promotes the Progression of Hepatocellular Carcinoma. Front. Immunol. 2021, 12, 727959. [Google Scholar] [CrossRef] [PubMed]
- Collins, K.P.; Geller, D.A.; Antoni, M.; Donnell, D.M.; Tsung, A.; Marsh, J.W.; Burke, L.; Penedo, F.; Terhorst, L.; Kamarck, T.W.; et al. Sleep duration is associated with survival in advanced cancer patients. Sleep Med. 2017, 32, 208–212. [Google Scholar] [CrossRef] [Green Version]
- Palesh, O.; Aldridge-Gerry, A.; Zeitzer, J.M.; Koopman, C.; Neri, E.; Giese-Davis, J.; Jo, B.; Kraemer, H.; Nouriani, B.; Spiegel, D. Actigraphy-measured sleep disruption as a predictor of survival among women with advanced breast cancer. Sleep 2014, 37, 837–842. [Google Scholar] [CrossRef] [PubMed]
- Edinger, J.D.; Arnedt, J.T.; Bertisch, S.M.; Carney, C.E.; Harrington, J.J.; Lichstein, K.L.; Sateia, M.J.; Troxel, W.M.; Zhou, E.S.; Kazmi, U.; et al. Behavioral and psychological treatments for chronic insomnia disorder in adults: An American Academy of Sleep Medicine clinical practice guideline. J. Clin. Sleep Med. 2021, 17, 255–262. [Google Scholar] [CrossRef] [PubMed]
- Raymann, R.J.; Swaab, D.F.; Van Someren, E.J. Skin temperature and sleep-onset latency: Changes with age and insomnia. Physiol. Behav. 2007, 90, 257–266. [Google Scholar] [CrossRef] [PubMed]
- Ko, Y.; Lee, J.Y. Effects of feet warming using bed socks on sleep quality and thermoregulatory responses in a cool environment. J. Physiol. Anthr. 2018, 37, 13. [Google Scholar] [CrossRef] [PubMed]
- Haghayegh, S.; Khoshnevis, S.; Smolensky, M.H.; Diller, K.R.; Castriotta, R.J. Before-bedtime passive body heating by warm shower or bath to improve sleep: A systematic review and meta-analysis. Sleep Med. Rev. 2019, 46, 124–135. [Google Scholar] [CrossRef] [PubMed]
- Deng, X.; Terunuma, H.; Nieda, M. Immunosurveillance of Cancer and Viral Infections with Regard to Alterations of Human NK Cells Originating from Lifestyle and Aging. Biomedicines 2021, 9, 557. [Google Scholar] [CrossRef]
- d’Adda di Fagagna, F. Living on a break: Cellular senescence as a DNA-damage response. Nat. Rev. Cancer 2008, 8, 512–522. [Google Scholar] [CrossRef] [PubMed]
- Kirkland, J.L.; Tchkonia, T. Clinical strategies and animal models for developing senolytic agents. Exp. Gerontol. 2015, 68, 19–25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kirkland, J.L.; Tchkonia, T. Senolytic drugs: From discovery to translation. J. Intern. Med. 2020, 288, 518–536. [Google Scholar] [CrossRef] [PubMed]
- Johmura, Y.; Yamanaka, T.; Omori, S.; Wang, T.W.; Sugiura, Y.; Matsumoto, M.; Suzuki, N.; Kumamoto, S.; Yamaguchi, K.; Hatakeyama, S.; et al. Senolysis by glutaminolysis inhibition ameliorates various age-associated disorders. Science 2021, 371, 265–270. [Google Scholar] [CrossRef]
- Muñoz, D.P.; Yannone, S.M.; Daemen, A.; Sun, Y.; Vakar-Lopez, F.; Kawahara, M.; Freund, A.M.; Rodier, F.; Wu, J.D.; Desprez, P.Y.; et al. Targetable mechanisms driving immunoevasion of persistent senescent cells link chemotherapy-resistant cancer to aging. JCI Insight 2019, 5, e124716. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zingoni, A.; Cecere, F.; Vulpis, E.; Fionda, C.; Molfetta, R.; Soriani, A.; Petrucci, M.T.; Ricciardi, M.R.; Fuerst, D.; Amendola, M.G.; et al. Genotoxic Stress Induces Senescence-Associated ADAM10-Dependent Release of NKG2D MIC Ligands in Multiple Myeloma Cells. J. Immunol. 2015, 195, 736–748. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pereira, B.I.; Devine, O.P.; Vukmanovic-Stejic, M.; Chambers, E.S.; Subramanian, P.; Patel, N.; Virasami, A.; Sebire, N.J.; Kinsler, V.; Valdovinos, A.; et al. Senescent cells evade immune clearance via HLA-E-mediated NK and CD8+ T cell inhibition. Nat. Commun. 2019, 10, 2387. [Google Scholar] [CrossRef] [PubMed]
- Valipour, B.; Velaei, K.; Abedelahi, A.; Karimipour, M.; Darabi, M.; Charoudeh, H.N. NK cells: An attractive candidate for cancer therapy. J. Cell. Physiol. 2019, 234, 19352–19365. [Google Scholar] [CrossRef] [PubMed]
- Barrow, A.D.; Colonna, M. Tailoring Natural Killer cell immunotherapy to the tumour microenvironment. Semin. Immunol. 2017, 31, 30–36. [Google Scholar] [CrossRef] [PubMed]
- Bachanova, V.; Miller, J.S. NK cells in therapy of cancer. Crit. Rev. Oncog. 2014, 19, 133–141. [Google Scholar] [CrossRef] [PubMed]
- Amor, C.; Feucht, J.; Leibold, J.; Ho, Y.J.; Zhu, C.; Alonso-Curbelo, D.; Mansilla-Soto, J.; Boyer, J.A.; Li, X.; Giavridis, T.; et al. Senolytic CAR T cells reverse senescence-associated pathologies. Nature 2020, 583, 127–132. [Google Scholar] [CrossRef] [PubMed]
- Islam, R.; Pupovac, A.; Evtimov, V.; Boyd, N.; Shu, R.; Boyd, R.; Trounson, A. Enhancing a Natural Killer: Modification of NK Cells for Cancer Immunotherapy. Cells 2021, 10, 1058. [Google Scholar] [CrossRef]
- Wang, L.; Dou, M.; Ma, Q.; Yao, R.; Liu, J. Chimeric antigen receptor (CAR)-modified NK cells against cancer: Opportunities and challenges. Int. Immunopharmacol. 2019, 74, 105695. [Google Scholar] [CrossRef] [PubMed]
- Lang, P.O.; Mitchell, W.A.; Lapenna, A.; Pitts, D.; Aspinall, R. Immunological pathogenesis of main age-related diseases and frailty: Role of immunosenescence. Eur. Geriatr. Med. 2010, 1, 112–121. [Google Scholar] [CrossRef]
- Horowitz, A.; Strauss-Albee, D.M.; Leipold, M.; Kubo, J.; Nemat-Gorgani, N.; Dogan, O.C.; Dekker, C.L.; Mackey, S.; Maecker, H.; Swan, G.E.; et al. Genetic and Environmental Determinants of Human NK Cell Diversity Revealed by Mass Cytometry. Sci. Transl. Med. 2013, 5, 208ra145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benjamin, J.E.; Gill, S.; Negrin, R.S. Biology and clinical effects of natural killer cells in allogeneic transplantation. Curr. Opin. Oncol. 2010, 22, 130–137. [Google Scholar] [CrossRef] [PubMed]
- Lupo, K.B.; Matosevic, S. Natural Killer Cells as Allogeneic Effectors in Adoptive Cancer Immunotherapy. Cancers 2019, 11, 769. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rezvani, K.; Rouce, R.; Liu, E.; Shpall, E. Engineering Natural Killer Cells for Cancer Immunotherapy. Mol. Ther. 2017, 25, 1769–1781. [Google Scholar] [CrossRef] [PubMed]
- Labanieh, L.; Majzner, R.G.; Mackall, C.L. Programming CAR-T cells to kill cancer. Nat. Biomed. Eng. 2018, 2, 377–391. [Google Scholar] [CrossRef]
- Pfefferle, A.; Huntington, N.D. You Have Got a Fast CAR: Chimeric Antigen Receptor NK Cells in Cancer Therapy. Cancers 2020, 12, 706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, G.; Dong, H.; Liang, Y.; Ham, J.D.; Rizwan, R.; Chen, J. CAR-NK cells: A promising cellular immunotherapy for cancer. EBioMedicine 2020, 59, 102975. [Google Scholar] [CrossRef] [PubMed]
Young Donor Age Range | Old Donor Age Range | NK Cell Definition | NK Numbers | Aged Phenotype | Target Cell | Cytotoxic Potential | Assay | IL-2 Activation | Ref |
---|---|---|---|---|---|---|---|---|---|
25–34 | 75–84 | *CD16+/Leu7± | Increased with age | CD16+ and Leu7+ increased | - | - | - | - | [52] |
21–38 | 71–97 | *Leu7+/Leu11a± | Increased with age | - | K562 | Decreased cytotoxic potential with age in both subsets of NK cells | Cr Release Assay | - | [53] |
20–60 | 80+ | CD16+ CD56+ CD5± | - | CD16+ CD57+ increased; CD56+/CD57− decreased | K562 | Increase in cytotoxic potential with age | Cr Release Assay | - | [54] |
27 ± 6 | 81 ± 7 | CD16+ | Increased with age | - | K562 | Similar binding capacity, Decreased cytotoxicity with age | Flow Cytometry | - | [55] |
19–36; 50–68 | 100–106 | CD16+ CD57± | Increased with age | CD16+ CD57− increased; no change in CD16+ CD57+ | K562 | No significant difference between age groups | Cr Release Assay | - | [56] |
25–35 | 75–94 | CD16+ CD56+ KIRDL+ or CD16+ CD56+ KIR2DL3− | Increased with age | CD16+, CD56+ and GL138+ increased | K562 | Decrease in lytic activity of CD16+ cells | Cr Release Assay | Yes | [57] |
23–35 | 65–100 | CD3− CD56+ | No change | - | K562 | No significant difference between age groups | Cr Release Assay | Yes | [58] |
23–35 | 67–95 | CD3− CD56+ | No change | - | K562 | Decrease in cytotoxic with age | Cr Release Assay | Yes | [59] |
30 ± 2 | 85 ± 2 | CD16+ | Increased with age | - | K562 | Decrease in cytotoxic potential with age | Cr Release Assay | - | [60] |
30 ± 2 | 85 ± 2 | CD3− CD16+ CD56+ | Increased with age | - | K562 | Decrease in cytotoxic potential with age | Cr Release Assay | - | [61] |
19–39 | 77–89 | CD3− CD56dim or CD3− CD56bright | Increased with age | CD56dim Increased; CD56bright decreased | - | - | - | - | [62] |
21–30 | 65+ | CD3− CD56+ | - | CD94 and NKG2A decreased; KIR increased | P815 | CD16 mediated cytotoxicity did not vary with age | Cr Release Assay | Yes | [63] |
Cord blood; Young <60 | 60–75; 75–80 | CD3− CD56dim or CD3− CD56bright | Increased in very old | CD56bright decreased; NKp30 decreased; NKp46 decreased; KIRs increased | K562 | No significant difference between age groups | Cr Release Assay | Yes | [64] |
<60 | 60+ | CD3− CD56dim or CD3− CD56bright | - | CD56dim increased; CD56bright decreased; NKG2A decreased; KLRG1 increased | - | - | - | - | [65] |
Children <18; adults 19–59 | 60+ | CD3− CD56dim or CD3− CD56bright | Increased in elderly, no difference between children and adults | CD56dim increased, CD56bright decreased, NKp30 and NKp46 decreased with age | K562 | No significant difference between age groups | Flow Cytometry | Yes | [66] |
20–34 | 70–86 | CD16+ CD56dim or CD16+ CD56bright | - | CD56dim increased, CD56bright decreased, KLRG1 increased with age | MCF-10A | - | - | Yes | [67] |
41–50, 51–60 | 61–70, 71–80 | CD3− CD56dim or CD3− CD56bright | Increased with age | CD56dim increased, CD56bright decreased | - | - | - | Yes | [68] |
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Brauning, A.; Rae, M.; Zhu, G.; Fulton, E.; Admasu, T.D.; Stolzing, A.; Sharma, A. Aging of the Immune System: Focus on Natural Killer Cells Phenotype and Functions. Cells 2022, 11, 1017. https://doi.org/10.3390/cells11061017
Brauning A, Rae M, Zhu G, Fulton E, Admasu TD, Stolzing A, Sharma A. Aging of the Immune System: Focus on Natural Killer Cells Phenotype and Functions. Cells. 2022; 11(6):1017. https://doi.org/10.3390/cells11061017
Chicago/Turabian StyleBrauning, Ashley, Michael Rae, Gina Zhu, Elena Fulton, Tesfahun Dessale Admasu, Alexandra Stolzing, and Amit Sharma. 2022. "Aging of the Immune System: Focus on Natural Killer Cells Phenotype and Functions" Cells 11, no. 6: 1017. https://doi.org/10.3390/cells11061017