Mast Cells and Natural Killer Cells—A Potentially Critical Interaction
Abstract
1. Mast Cells
2. NK Cell–Mast Cell Interactions
2.1. Viral Infection
2.2. Cancer
2.3. Allergic Asthma
3. Conclusions
Funding
Acknowledgments
Conflicts of Interest
References
- Rivera, J.; Fierro, N.A.; Olivera, A.; Suzuki, R. New insights on mast cell activation via the high affinity receptor for ige. Adv. Immunol. 2008, 98, 85–120. [Google Scholar] [PubMed]
- Lorentz, A.; Wilke, M.; Sellge, G.; Worthmann, H.; Klempnauer, J.; Manns, M.P.; Bischoff, S.C. IL-4-induced priming of human intestinal mast cells for enhanced survival and th2 cytokine generation is reversible and associated with increased activity of erk1/2 and c-fos. J. Immunol. 2005, 174, 6751–6756. [Google Scholar] [CrossRef] [PubMed]
- Shelburne, C.P.; Ryan, J.J. The role of th2 cytokines in mast cell homeostasis. Immunol. Rev. 2001, 179, 82–93. [Google Scholar] [CrossRef] [PubMed]
- Oldford, S.A.; Salsman, S.P.; Portales-Cervantes, L.; Alyazidi, R.; Anderson, R.; Haidl, I.D.; Marshall, J.S. Interferon alpha2 and interferon gamma induce the degranulation independent production of vegf-a and il-1 receptor antagonist and other mediators from human mast cells. Immun. Inflamm. Dis. 2018, 6, 176–189. [Google Scholar] [CrossRef] [PubMed]
- Tore, F.; Tuncel, N. Mast cells: Target and source of neuropeptides. Curr. Pharm. Des. 2009, 15, 3433–3445. [Google Scholar] [CrossRef] [PubMed]
- Enoksson, M.; Lyberg, K.; Moller-Westerberg, C.; Fallon, P.G.; Nilsson, G.; Lunderius-Andersson, C. Mast cells as sensors of cell injury through il-33 recognition. J. Immunol. 2011, 186, 2523–2528. [Google Scholar] [CrossRef]
- Gulliksson, M.; Carvalho, R.F.; Ulleras, E.; Nilsson, G. Mast cell survival and mediator secretion in response to hypoxia. PLoS ONE 2010, 5, e12360. [Google Scholar] [CrossRef] [PubMed]
- Galli, S.J.; Tsai, M. Ige and mast cells in allergic disease. Nat. Med. 2012, 18, 693–704. [Google Scholar] [CrossRef] [PubMed]
- Amin, K. The role of mast cells in allergic inflammation. Respir. Med. 2012, 106, 9–14. [Google Scholar] [CrossRef]
- Akahoshi, M.; Song, C.H.; Piliponsky, A.M.; Metz, M.; Guzzetta, A.; Abrink, M.; Schlenner, S.M.; Feyerabend, T.B.; Rodewald, H.R.; Pejler, G.; et al. Mast cell chymase reduces the toxicity of gila monster venom, scorpion venom, and vasoactive intestinal polypeptide in mice. J. Clin. Invest. 2011, 121, 4180–4191. [Google Scholar] [CrossRef]
- Grujic, M.; Paivandy, A.; Gustafson, A.M.; Thomsen, A.R.; Ohrvik, H.; Pejler, G. The combined action of mast cell chymase, tryptase and carboxypeptidase a3 protects against melanoma colonization of the lung. Oncotarget 2017, 8, 25066–25079. [Google Scholar] [CrossRef] [PubMed]
- Marichal, T.; Starkl, P.; Reber, L.L.; Kalesnikoff, J.; Oettgen, H.C.; Tsai, M.; Metz, M.; Galli, S.J. A beneficial role for immunoglobulin e in host defense against honeybee venom. Immunity 2013, 39, 963–975. [Google Scholar] [CrossRef]
- Roy, A.; Ganesh, G.; Sippola, H.; Bolin, S.; Sawesi, O.; Dagalv, A.; Schlenner, S.M.; Feyerabend, T.; Rodewald, H.R.; Kjellen, L.; et al. Mast cell chymase degrades the alarmins heat shock protein 70, biglycan, hmgb1, and interleukin-33 (IL-33) and limits danger-induced inflammation. J. Biol. Chem. 2014, 289, 237–250. [Google Scholar] [CrossRef] [PubMed]
- Ha, T.Y.; Reed, N.D.; Crowle, P.K. Delayed expulsion of adult trichinella spiralis by mast cell-deficient w/wv mice. Infect. Immun. 1983, 41, 445–447. [Google Scholar] [PubMed]
- Hepworth, M.R.; Danilowicz-Luebert, E.; Rausch, S.; Metz, M.; Klotz, C.; Maurer, M.; Hartmann, S. Mast cells orchestrate type 2 immunity to helminths through regulation of tissue-derived cytokines. Proc. Natl. Acad. Sci. USA 2012, 109, 6644–6649. [Google Scholar] [CrossRef] [PubMed]
- Ronnberg, E.; Guss, B.; Pejler, G. Infection of mast cells with live streptococci causes a toll-like receptor 2- and cell-cell contact-dependent cytokine and chemokine response. Infect. Immun. 2010, 78, 854–864. [Google Scholar] [CrossRef] [PubMed]
- Supajatura, V.; Ushio, H.; Nakao, A.; Okumura, K.; Ra, C.; Ogawa, H. Protective roles of mast cells against enterobacterial infection are mediated by toll-like receptor 4. J. Immunol. 2001, 167, 2250–2256. [Google Scholar] [CrossRef] [PubMed]
- Malaviya, R.; Ikeda, T.; Ross, E.; Abraham, S.N. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through tnf-alpha. Nature 1996, 381, 77–80. [Google Scholar] [CrossRef] [PubMed]
- Dawicki, W.; Jawdat, D.W.; Xu, N.; Marshall, J.S. Mast cells, histamine, and il-6 regulate the selective influx of dendritic cell subsets into an inflamed lymph node. J. Immunol. 2010, 184, 2116–2123. [Google Scholar] [CrossRef]
- Merluzzi, S.; Frossi, B.; Gri, G.; Parusso, S.; Tripodo, C.; Pucillo, C. Mast cells enhance proliferation of b lymphocytes and drive their differentiation toward iga-secreting plasma cells. Blood 2010, 115, 2810–2817. [Google Scholar] [CrossRef]
- Shelburne, C.P.; Nakano, H.; St John, A.L.; Chan, C.; McLachlan, J.B.; Gunn, M.D.; Staats, H.F.; Abraham, S.N. Mast cells augment adaptive immunity by orchestrating dendritic cell trafficking through infected tissues. Cell Host Microbe 2009, 6, 331–342. [Google Scholar] [CrossRef] [PubMed]
- Nakae, S.; Suto, H.; Kakurai, M.; Sedgwick, J.D.; Tsai, M.; Galli, S.J. Mast cells enhance t cell activation: Importance of mast cell-derived tnf. Proc. Natl. Acad. Sci. USA 2005, 102, 6467–6472. [Google Scholar] [CrossRef] [PubMed]
- Zarnegar, B.; Westin, A.; Evangelidou, S.; Hallgren, J. Innate immunity induces the accumulation of lung mast cells during influenza infection. Front. Immunol. 2018, 9, 2288. [Google Scholar] [CrossRef]
- St John, A.L.; Rathore, A.P.; Raghavan, B.; Ng, M.L.; Abraham, S.N. Contributions of mast cells and vasoactive products, leukotrienes and chymase, to dengue virus-induced vascular leakage. Elife 2013, 2, e00481. [Google Scholar] [CrossRef] [PubMed]
- Sun, Q.; Li, W.; She, R.; Wang, D.; Han, D.; Li, R.; Ding, Y.; Yue, Z. Evidence for a role of mast cells in the mucosal injury induced by newcastle disease virus. Poult. Sci. 2009, 88, 554–561. [Google Scholar] [CrossRef] [PubMed]
- Brown, M.G.; Hermann, L.L.; Issekutz, A.C.; Marshall, J.S.; Rowter, D.; Al-Afif, A.; Anderson, R. Dengue virus infection of mast cells triggers endothelial cell activation. J. Virol. 2011, 85, 1145–1150. [Google Scholar] [CrossRef] [PubMed]
- St John, A.L.; Rathore, A.P.; Yap, H.; Ng, M.L.; Metcalfe, D.D.; Vasudevan, S.G.; Abraham, S.N. Immune surveillance by mast cells during dengue infection promotes natural killer (nk) and nkt-cell recruitment and viral clearance. Proc. Natl. Acad. Sci. USA 2011, 108, 9190–9195. [Google Scholar] [CrossRef] [PubMed]
- Burke, S.M.; Issekutz, T.B.; Mohan, K.; Lee, P.W.; Shmulevitz, M.; Marshall, J.S. Human mast cell activation with virus-associated stimuli leads to the selective chemotaxis of natural killer cells by a cxcl8-dependent mechanism. Blood 2008, 111, 5467–5476. [Google Scholar] [CrossRef] [PubMed]
- Henney, C.S.; Kuribayashi, K.; Kern, D.E.; Gillis, S. Interleukin-2 augments natural killer cell activity. Nature 1981, 291, 335–338. [Google Scholar] [CrossRef]
- Boieri, M.; Ulvmoen, A.; Sudworth, A.; Lendrem, C.; Collin, M.; Dickinson, A.M.; Kveberg, L.; Inngjerdingen, M. Il-12, il-15, and il-18 pre-activated nk cells target resistant t cell acute lymphoblastic leukemia and delay leukemia development in vivo. Oncoimmunology 2017, 6, e1274478. [Google Scholar] [CrossRef]
- Borg, C.; Jalil, A.; Laderach, D.; Maruyama, K.; Wakasugi, H.; Charrier, S.; Ryffel, B.; Cambi, A.; Figdor, C.; Vainchenker, W.; et al. Nk cell activation by dendritic cells (dcs) requires the formation of a synapse leading to il-12 polarization in dcs. Blood 2004, 104, 3267–3275. [Google Scholar] [CrossRef] [PubMed]
- Ferlazzo, G.; Tsang, M.L.; Moretta, L.; Melioli, G.; Steinman, R.M.; Munz, C. Human dendritic cells activate resting natural killer (nk) cells and are recognized via the nkp30 receptor by activated nk cells. J. Exp. Med. 2002, 195, 343–351. [Google Scholar] [CrossRef] [PubMed]
- Portales-Cervantes, L.; Haidl, I.D.; Lee, P.W.; Marshall, J.S. Virus-infected human mast cells enhance natural killer cell functions. J. Innate. Immun. 2017, 9, 94–108. [Google Scholar] [CrossRef] [PubMed]
- Zwirner, N.W.; Domaica, C.I. Cytokine regulation of natural killer cell effector functions. Biofactors 2010, 36, 274–288. [Google Scholar] [CrossRef] [PubMed]
- Chun, Y.H.; Park, J.Y.; Lee, H.; Kim, H.S.; Won, S.; Joe, H.J.; Chung, W.J.; Yoon, J.S.; Kim, H.H.; Kim, J.T.; et al. Rhinovirus-infected epithelial cells produce more IL-8 and rantes compared with other respiratory viruses. Allergy Asthma Immunol. Res. 2013, 5, 216–223. [Google Scholar] [CrossRef] [PubMed]
- Matsukura, S.; Kokubu, F.; Noda, H.; Tokunaga, H.; Adachi, M. Expression of IL-6, IL-8, and rantes on human bronchial epithelial cells, nci-h292, induced by influenza virus a. J. Allergy Clin. Immunol. 1996, 98, 1080–1087. [Google Scholar] [CrossRef]
- Vosskuhl, K.; Greten, T.F.; Manns, M.P.; Korangy, F.; Wedemeyer, J. Lipopolysaccharide-mediated mast cell activation induces ifn-gamma secretion by nk cells. J. Immunol. 2010, 185, 119–125. [Google Scholar] [CrossRef]
- Erick, T.K.; Brossay, L. Phenotype and functions of conventional and non-conventional nk cells. Curr. Opin. Immunol. 2016, 38, 67–74. [Google Scholar] [CrossRef]
- Ivanova, D.; Krempels, R.; Ryfe, J.; Weitzman, K.; Stephenson, D.; Gigley, J.P. Nk cells in mucosal defense against infection. Biomed. Res. Int. 2014, 2014, 413982. [Google Scholar] [CrossRef]
- Sojka, D.K.; Plougastel-Douglas, B.; Yang, L.; Pak-Wittel, M.A.; Artyomov, M.N.; Ivanova, Y.; Zhong, C.; Chase, J.M.; Rothman, P.B.; Yu, J.; et al. Tissue-resident natural killer (nk) cells are cell lineages distinct from thymic and conventional splenic nk cells. Elife 2014, 3, e01659. [Google Scholar] [CrossRef]
- Esposito, I.; Menicagli, M.; Funel, N.; Bergmann, F.; Boggi, U.; Mosca, F.; Bevilacqua, G.; Campani, D. Inflammatory cells contribute to the generation of an angiogenic phenotype in pancreatic ductal adenocarcinoma. J. Clin. Pathol. 2004, 57, 630–636. [Google Scholar] [CrossRef] [PubMed]
- Xu, W.; Qian, J.; Zeng, F.; Li, S.; Guo, W.; Chen, L.; Li, G.; Zhang, Z.; Wang, Q.J.; Deng, F. Protein kinase ds promote tumor angiogenesis through mast cell recruitment and expression of angiogenic factors in prostate cancer microenvironment. J. Exp. Clin. Cancer Res 2019, 38, 114. [Google Scholar] [CrossRef] [PubMed]
- Gulubova, M.; Manolova, I.; Kyurkchiev, D.; Julianov, A.; Altunkova, I. Decrease in intrahepatic cd56+ lymphocytes in gastric and colorectal cancer patients with liver metastases. APMIS 2009, 117, 870–879. [Google Scholar] [CrossRef] [PubMed]
- Takanami, I.; Takeuchi, K.; Naruke, M. Mast cell density is associated with angiogenesis and poor prognosis in pulmonary adenocarcinoma. Cancer 2000, 88, 2686–2692. [Google Scholar] [CrossRef]
- Ribatti, D.; Ennas, M.G.; Vacca, A.; Ferreli, F.; Nico, B.; Orru, S.; Sirigu, P. Tumor vascularity and tryptase-positive mast cells correlate with a poor prognosis in melanoma. Eur. J. Clin. Invest. 2003, 33, 420–425. [Google Scholar] [CrossRef] [PubMed]
- Sammarco, G.; Gadaleta, C.D.; Zuccala, V.; Albayrak, E.; Patruno, R.; Milella, P.; Sacco, R.; Ammendola, M.; Ranieri, G. Tumor-associated macrophages and mast cells positive to tryptase are correlated with angiogenesis in surgically-treated gastric cancer patients. Int. J. Mol. Sci. 2018, 19, 1176. [Google Scholar] [CrossRef]
- Xiong, Y.; Liu, L.; Xia, Y.; Qi, Y.; Chen, Y.; Chen, L.; Zhang, P.; Kong, Y.; Qu, Y.; Wang, Z.; et al. Tumor infiltrating mast cells determine oncogenic hif-2alpha-conferred immune evasion in clear cell renal cell carcinoma. Cancer Immunol. Immunother. 2019, 68, 731–741. [Google Scholar] [CrossRef]
- Liu, Z.; Zhu, Y.; Xu, L.; Zhang, J.; Xie, H.; Fu, H.; Zhou, Q.; Chang, Y.; Dai, B.; Xu, J. Tumor stroma-infiltrating mast cells predict prognosis and adjuvant chemotherapeutic benefits in patients with muscle invasive bladder cancer. Oncoimmunology 2018, 7, e1474317. [Google Scholar] [CrossRef]
- Tu, J.F.; Pan, H.Y.; Ying, X.H.; Lou, J.; Ji, J.S.; Zou, H. Mast cells comprise the major of interleukin 17-producing cells and predict a poor prognosis in hepatocellular carcinoma. Medicine (Baltimore) 2016, 95, e3220. [Google Scholar] [CrossRef]
- Lv, Y.P.; Peng, L.S.; Wang, Q.H.; Chen, N.; Teng, Y.S.; Wang, T.T.; Mao, F.Y.; Zhang, J.Y.; Cheng, P.; Liu, Y.G.; et al. Degranulation of mast cells induced by gastric cancer-derived adrenomedullin prompts gastric cancer progression. Cell Death Dis. 2018, 9, 1034. [Google Scholar] [CrossRef]
- Yang, Z.; Zhang, B.; Li, D.; Lv, M.; Huang, C.; Shen, G.X.; Huang, B. Mast cells mobilize myeloid-derived suppressor cells and treg cells in tumor microenvironment via il-17 pathway in murine hepatocarcinoma model. PLoS ONE 2010, 5, e8922. [Google Scholar] [CrossRef] [PubMed]
- Danelli, L.; Frossi, B.; Gri, G.; Mion, F.; Guarnotta, C.; Bongiovanni, L.; Tripodo, C.; Mariuzzi, L.; Marzinotto, S.; Rigoni, A.; et al. Mast cells boost myeloid-derived suppressor cell activity and contribute to the development of tumor-favoring microenvironment. Cancer Immunol. Res. 2015, 3, 85–95. [Google Scholar] [CrossRef] [PubMed]
- Siebenhaar, F.; Metz, M.; Maurer, M. Mast cells protect from skin tumor development and limit tumor growth during cutaneous de novo carcinogenesis in a kit-dependent mouse model. Exp. Dermatol. 2014, 23, 159–164. [Google Scholar] [CrossRef] [PubMed]
- Rajput, A.B.; Turbin, D.A.; Cheang, M.C.; Voduc, D.K.; Leung, S.; Gelmon, K.A.; Gilks, C.B.; Huntsman, D.G. Stromal mast cells in invasive breast cancer are a marker of favourable prognosis: A study of 4,444 cases. Breast Cancer Res. Treat. 2008, 107, 249–257. [Google Scholar] [CrossRef] [PubMed]
- Fu, H.; Zhu, Y.; Wang, Y.; Liu, Z.; Zhang, J.; Wang, Z.; Xie, H.; Dai, B.; Xu, J.; Ye, D. Tumor infiltrating mast cells (tims) confers a marked survival advantage in nonmetastatic clear-cell renal cell carcinoma. Ann. Surg. Oncol. 2017, 24, 1435–1442. [Google Scholar] [CrossRef]
- Wang, B.; Li, L.; Liao, Y.; Li, J.; Yu, X.; Zhang, Y.; Xu, J.; Rao, H.; Chen, S.; Zhang, L.; et al. Mast cells expressing interleukin 17 in the muscularis propria predict a favorable prognosis in esophageal squamous cell carcinoma. Cancer Immunol. Immunother. 2013, 62, 1575–1585. [Google Scholar] [CrossRef]
- Chan, J.K.; Magistris, A.; Loizzi, V.; Lin, F.; Rutgers, J.; Osann, K.; DiSaia, P.J.; Samoszuk, M. Mast cell density, angiogenesis, blood clotting, and prognosis in women with advanced ovarian cancer. Gynecol. Oncol. 2005, 99, 20–25. [Google Scholar] [CrossRef] [PubMed]
- Hedstrom, G.; Berglund, M.; Molin, D.; Fischer, M.; Nilsson, G.; Thunberg, U.; Book, M.; Sundstrom, C.; Rosenquist, R.; Roos, G.; et al. Mast cell infiltration is a favourable prognostic factor in diffuse large b-cell lymphoma. Br. J. Haematol. 2007, 138, 68–71. [Google Scholar] [CrossRef]
- Ali, G.; Boldrini, L.; Lucchi, M.; Mussi, A.; Corsi, V.; Fontanini, G. Tryptase mast cells in malignant pleural mesothelioma as an independent favorable prognostic factor. J. Thorac. Oncol. 2009, 4, 348–354. [Google Scholar] [CrossRef]
- Glajcar, A.; Szpor, J.; Pacek, A.; Tyrak, K.E.; Chan, F.; Streb, J.; Hodorowicz-Zaniewska, D.; Okon, K. The relationship between breast cancer molecular subtypes and mast cell populations in tumor microenvironment. Virchows Arch. 2017, 470, 505–515. [Google Scholar] [CrossRef]
- Rojas, I.G.; Spencer, M.L.; Martinez, A.; Maurelia, M.A.; Rudolph, M.I. Characterization of mast cell subpopulations in lip cancer. J. Oral. Pathol. Med. 2005, 34, 268–273. [Google Scholar] [CrossRef] [PubMed]
- Ribatti, D.; Belloni, A.S.; Nico, B.; Sala, G.; Longo, V.; Mangieri, D.; Crivellato, E.; Nussdorfer, G.G. Tryptase- and leptin-positive mast cells correlate with vascular density in uterine leiomyomas. Am. J. Obstet. Gynecol. 2007, 196, 470.e1–470.e7. [Google Scholar] [CrossRef] [PubMed]
- Rao, Q.; Chen, Y.; Yeh, C.R.; Ding, J.; Li, L.; Chang, C.; Yeh, S. Recruited mast cells in the tumor microenvironment enhance bladder cancer metastasis via modulation of erbeta/ccl2/ccr2 emt/mmp9 signals. Oncotarget 2016, 7, 7842–7855. [Google Scholar] [CrossRef] [PubMed]
- Soucek, L.; Lawlor, E.R.; Soto, D.; Shchors, K.; Swigart, L.B.; Evan, G.I. Mast cells are required for angiogenesis and macroscopic expansion of myc-induced pancreatic islet tumors. Nat. Med. 2007, 13, 1211–1218. [Google Scholar] [CrossRef] [PubMed]
- Soucek, L.; Buggy, J.J.; Kortlever, R.; Adimoolam, S.; Monclus, H.A.; Allende, M.T.; Swigart, L.B.; Evan, G.I. Modeling pharmacological inhibition of mast cell degranulation as a therapy for insulinoma. Neoplasia 2011, 13, 1093–1100. [Google Scholar] [CrossRef] [PubMed]
- Oldford, S.A.; Haidl, I.D.; Howatt, M.A.; Leiva, C.A.; Johnston, B.; Marshall, J.S. A critical role for mast cells and mast cell-derived il-6 in tlr2-mediated inhibition of tumor growth. J. Immunol. 2010, 185, 7067–7076. [Google Scholar] [CrossRef] [PubMed]
- Bodduluri, S.R.; Mathis, S.; Maturu, P.; Krishnan, E.; Satpathy, S.R.; Chilton, P.M.; Mitchell, T.C.; Lira, S.; Locati, M.; Mantovani, A.; et al. Mast cell-dependent cd8(+) t-cell recruitment mediates immune surveillance of intestinal tumors in apc(min/+) mice. Cancer Immunol. Res. 2018. [Google Scholar] [CrossRef] [PubMed]
- Forward, N.A.; Furlong, S.J.; Yang, Y.; Lin, T.J.; Hoskin, D.W. Mast cells down-regulate cd4+cd25+ t regulatory cell suppressor function via histamine h1 receptor interaction. J. Immunol. 2009, 183, 3014–3022. [Google Scholar] [CrossRef]
- Roder, J.C.; Haliotis, T.; Klein, M.; Korec, S.; Jett, J.R.; Ortaldo, J.; Heberman, R.B.; Katz, P.; Fauci, A.S. A new immunodeficiency disorder in humans involving nk cells. Nature 1980, 284, 553–555. [Google Scholar] [CrossRef]
- Sullivan, J.L.; Byron, K.S.; Brewster, F.E.; Purtilo, D.T. Deficient natural killer cell activity in x-linked lymphoproliferative syndrome. Science 1980, 210, 543–545. [Google Scholar] [CrossRef]
- 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]
- Strayer, D.R.; Carter, W.A.; Brodsky, I. Familial occurrence of breast cancer is associated with reduced natural killer cytotoxicity. Breast Cancer Res. Treat. 1986, 7, 187–192. [Google Scholar] [CrossRef]
- 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] [PubMed]
- Schroder, K.; Hertzog, P.J.; Ravasi, T.; Hume, D.A. Interferon-gamma: An overview of signals, mechanisms and functions. J. Leukoc. Biol. 2004, 75, 163–189. [Google Scholar] [CrossRef]
- Caretto, D.; Katzman, S.D.; Villarino, A.V.; Gallo, E.; Abbas, A.K. Cutting edge: The th1 response inhibits the generation of peripheral regulatory t cells. J. Immunol. 2010, 184, 30–34. [Google Scholar] [CrossRef]
- Olalekan, S.A.; Cao, Y.; Hamel, K.M.; Finnegan, A. B cells expressing ifn-gamma suppress treg-cell differentiation and promote autoimmune experimental arthritis. Eur. J. Immunol. 2015, 45, 988–998. [Google Scholar] [CrossRef] [PubMed]
- Hu, X.; Paik, P.K.; Chen, J.; Yarilina, A.; Kockeritz, L.; Lu, T.T.; Woodgett, J.R.; Ivashkiv, L.B. IFN-gamma suppresses il-10 production and synergizes with tlr2 by regulating gsk3 and creb/ap-1 proteins. Immunity 2006, 24, 563–574. [Google Scholar] [CrossRef]
- Wen, F.Q.; Liu, X.; Kobayashi, T.; Abe, S.; Fang, Q.; Kohyama, T.; Ertl, R.; Terasaki, Y.; Manouilova, L.; Rennard, S.I. Interferon-gamma inhibits transforming growth factor-beta production in human airway epithelial cells by targeting smads. Am. J. Respir. Cell Mol. Biol. 2004, 30, 816–822. [Google Scholar] [CrossRef]
- Kochupurakkal, B.S.; Wang, Z.C.; Hua, T.; Culhane, A.C.; Rodig, S.J.; Rajkovic-Molek, K.; Lazaro, J.B.; Richardson, A.L.; Biswas, D.K.; Iglehart, J.D. Rela-induced interferon response negatively regulates proliferation. PLoS ONE 2015, 10, e0140243. [Google Scholar] [CrossRef]
- Wang, L.; Wang, Y.; Song, Z.; Chu, J.; Qu, X. Deficiency of interferon-gamma or its receptor promotes colorectal cancer development. J. Interferon Cytokine Res. 2015, 35, 273–280. [Google Scholar] [CrossRef]
- Zaidi, M.R. The interferon-gamma paradox in cancer. J. Interferon Cytokine Res. 2019, 39, 30–38. [Google Scholar] [CrossRef] [PubMed]
- Salih, H.R.; Antropius, H.; Gieseke, F.; Lutz, S.Z.; Kanz, L.; Rammensee, H.G.; Steinle, A. Functional expression and release of ligands for the activating immunoreceptor nkg2d in leukemia. Blood 2003, 102, 1389–1396. [Google Scholar] [CrossRef] [PubMed]
- Doubrovina, E.S.; Doubrovin, M.M.; Vider, E.; Sisson, R.B.; O’Reilly, R.J.; Dupont, B.; Vyas, Y.M. Evasion from nk cell immunity by mhc class i chain-related molecules expressing colon adenocarcinoma. J. Immunol. 2003, 171, 6891–6899. [Google Scholar] [CrossRef] [PubMed]
- Vasievich, E.A.; Huang, L. The suppressive tumor microenvironment: A challenge in cancer immunotherapy. Mol. Pharm. 2011, 8, 635–641. [Google Scholar] [CrossRef] [PubMed]
- Halama, N.; Braun, M.; Kahlert, C.; Spille, A.; Quack, C.; Rahbari, N.; Koch, M.; Weitz, J.; Kloor, M.; Zoernig, I.; et al. Natural killer cells are scarce in colorectal carcinoma tissue despite high levels of chemokines and cytokines. Clin. Cancer Res. 2011, 17, 678–689. [Google Scholar] [CrossRef]
- Takanami, I.; Takeuchi, K.; Giga, M. The prognostic value of natural killer cell infiltration in resected pulmonary adenocarcinoma. J. Thorac. Cardiovasc. Surg. 2001, 121, 1058–1063. [Google Scholar] [CrossRef]
- Ishigami, S.; Natsugoe, S.; Tokuda, K.; Nakajo, A.; Che, X.; Iwashige, H.; Aridome, K.; Hokita, S.; Aikou, T. Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 2000, 88, 577–583. [Google Scholar] [CrossRef]
- Sznurkowski, J.J.; Zawrocki, A.; Biernat, W. Subtypes of cytotoxic lymphocytes and natural killer cells infiltrating cancer nests correlate with prognosis in patients with vulvar squamous cell carcinoma. Cancer Immunol. Immunother. 2014, 63, 297–303. [Google Scholar] [CrossRef][Green Version]
- Prestwich, R.J.; Errington, F.; Steele, L.P.; Ilett, E.J.; Morgan, R.S.; Harrington, K.J.; Pandha, H.S.; Selby, P.J.; Vile, R.G.; Melcher, A.A. Reciprocal human dendritic cell-natural killer cell interactions induce antitumor activity following tumor cell infection by oncolytic reovirus. J. Immunol. 2009, 183, 4312–4321. [Google Scholar] [CrossRef]
- Bhat, R.; Dempe, S.; Dinsart, C.; Rommelaere, J. Enhancement of nk cell antitumor responses using an oncolytic parvovirus. Int. J. Cancer 2011, 128, 908–919. [Google Scholar] [CrossRef]
- Chen, X.; Han, J.; Chu, J.; Zhang, L.; Zhang, J.; Chen, C.; Chen, L.; Wang, Y.; Wang, H.; Yi, L.; et al. A combinational therapy of egfr-car nk cells and oncolytic herpes simplex virus 1 for breast cancer brain metastases. Oncotarget 2016, 7, 27764–27777. [Google Scholar] [CrossRef] [PubMed]
- Bhat, R.; Rommelaere, J. Nk-cell-dependent killing of colon carcinoma cells is mediated by natural cytotoxicity receptors (ncrs) and stimulated by parvovirus infection of target cells. BMC Cancer 2013, 13, 367. [Google Scholar] [CrossRef] [PubMed]
- Bachanova, V.; Cooley, S.; Defor, T.E.; Verneris, M.R.; Zhang, B.; McKenna, D.H.; Curtsinger, J.; Panoskaltsis-Mortari, A.; Lewis, D.; Hippen, K.; et al. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using il-2 diphtheria toxin fusion protein. Blood 2014, 123, 3855–3863. [Google Scholar] [CrossRef] [PubMed]
- Curti, A.; Ruggeri, L.; D’Addio, A.; Bontadini, A.; Dan, E.; Motta, M.R.; Trabanelli, S.; Giudice, V.; Urbani, E.; Martinelli, G.; et al. Successful transfer of alloreactive haploidentical kir ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood 2011, 118, 3273–3279. [Google Scholar] [CrossRef] [PubMed]
- Miller, J.S.; Soignier, Y.; Panoskaltsis-Mortari, A.; McNearney, S.A.; Yun, G.H.; Fautsch, S.K.; McKenna, D.; Le, C.; Defor, T.E.; Burns, L.J.; et al. Successful adoptive transfer and in vivo expansion of human haploidentical nk cells in patients with cancer. Blood 2005, 105, 3051–3057. [Google Scholar] [CrossRef]
- Rubnitz, J.E.; Inaba, H.; Ribeiro, R.C.; Pounds, S.; Rooney, B.; Bell, T.; Pui, C.H.; Leung, W. Nkaml: A pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J. Clin. Oncol. 2010, 28, 955–959. [Google Scholar] [CrossRef]
- Brentjens, R.J.; Davila, M.L.; Riviere, I.; Park, J.; Wang, X.; Cowell, L.G.; Bartido, S.; Stefanski, J.; Taylor, C.; Olszewska, M.; et al. Cd19-targeted t cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 2013, 5, 177ra138. [Google Scholar] [CrossRef]
- Maude, S.L.; Frey, N.; Shaw, P.A.; Aplenc, R.; Barrett, D.M.; Bunin, N.J.; Chew, A.; Gonzalez, V.E.; Zheng, Z.; Lacey, S.F.; et al. Chimeric antigen receptor t cells for sustained remissions in leukemia. N. Engl. J. Med. 2014, 371, 1507–1517. [Google Scholar] [CrossRef]
- Yu, Z.; Chan, M.K.; O-charoenrat, P.; Eisenberg, D.P.; Shah, J.P.; Singh, B.; Fong, Y.; Wong, R.J. Enhanced nectin-1 expression and herpes oncolytic sensitivity in highly migratory and invasive carcinoma. Clin. Cancer Res. 2005, 11, 4889–4897. [Google Scholar] [CrossRef]
- Anderson, B.D.; Nakamura, T.; Russell, S.J.; Peng, K.W. High cd46 receptor density determines preferential killing of tumor cells by oncolytic measles virus. Cancer Res. 2004, 64, 4919–4926. [Google Scholar] [CrossRef]
- Mansour, M.; Palese, P.; Zamarin, D. Oncolytic specificity of newcastle disease virus is mediated by selectivity for apoptosis-resistant cells. J. Virol. 2011, 85, 6015–6023. [Google Scholar] [CrossRef] [PubMed]
- Sborov, D.W.; Nuovo, G.J.; Stiff, A.; Mace, T.; Lesinski, G.B.; Benson, D.M., Jr.; Efebera, Y.A.; Rosko, A.E.; Pichiorri, F.; Grever, M.R.; et al. A phase i trial of single-agent reolysin in patients with relapsed multiple myeloma. Clin. Cancer Res. 2014, 20, 5946–5955. [Google Scholar] [CrossRef] [PubMed]
- Forsyth, P.; Roldan, G.; George, D.; Wallace, C.; Palmer, C.A.; Morris, D.; Cairncross, G.; Matthews, M.V.; Markert, J.; Gillespie, Y.; et al. A phase i trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol. Ther. 2008, 16, 627–632. [Google Scholar] [CrossRef] [PubMed]
- Galanis, E.; Markovic, S.N.; Suman, V.J.; Nuovo, G.J.; Vile, R.G.; Kottke, T.J.; Nevala, W.K.; Thompson, M.A.; Lewis, J.E.; Rumilla, K.M.; et al. Phase ii trial of intravenous administration of reolysin((r)) (reovirus serotype-3-dearing strain) in patients with metastatic melanoma. Mol. Ther. 2012, 20, 1998–2003. [Google Scholar] [CrossRef] [PubMed]
- White, C.L.; Twigger, K.R.; Vidal, L.; De Bono, J.S.; Coffey, M.; Heinemann, L.; Morgan, R.; Merrick, A.; Errington, F.; Vile, R.G.; et al. Characterization of the adaptive and innate immune response to intravenous oncolytic reovirus (dearing type 3) during a phase i clinical trial. Gene Ther. 2008, 15, 911–920. [Google Scholar] [CrossRef] [PubMed]
- Errington, F.; Steele, L.; Prestwich, R.; Harrington, K.J.; Pandha, H.S.; Vidal, L.; de Bono, J.; Selby, P.; Coffey, M.; Vile, R.; et al. Reovirus activates human dendritic cells to promote innate antitumor immunity. J. Immunol. 2008, 180, 6018–6026. [Google Scholar] [CrossRef] [PubMed]
- Prestwich, R.J.; Errington, F.; Ilett, E.J.; Morgan, R.S.; Scott, K.J.; Kottke, T.; Thompson, J.; Morrison, E.E.; Harrington, K.J.; Pandha, H.S.; et al. Tumor infection by oncolytic reovirus primes adaptive antitumor immunity. Clin. Cancer Res. 2008, 14, 7358–7366. [Google Scholar] [CrossRef] [PubMed]
- Gujar, S.A.; Pan, D.A.; Marcato, P.; Garant, K.A.; Lee, P.W. Oncolytic virus-initiated protective immunity against prostate cancer. Mol. Ther. 2011, 19, 797–804. [Google Scholar] [CrossRef] [PubMed]
- Gomez, G.; Ramirez, C.D.; Rivera, J.; Patel, M.; Norozian, F.; Wright, H.V.; Kashyap, M.V.; Barnstein, B.O.; Fischer-Stenger, K.; Schwartz, L.B.; et al. Tgf-beta 1 inhibits mast cell fc epsilon ri expression. J. Immunol. 2005, 174, 5987–5993. [Google Scholar] [CrossRef] [PubMed]
- Ndaw, V.S.; Abebayehu, D.; Spence, A.J.; Paez, P.A.; Kolawole, E.M.; Taruselli, M.T.; Caslin, H.L.; Chumanevich, A.P.; Paranjape, A.; Baker, B.; et al. Tgf-beta1 suppresses il-33-induced mast cell function. J. Immunol. 2017, 199, 866–873. [Google Scholar] [CrossRef] [PubMed]
- Zaiatz-Bittencourt, V.; Finlay, D.K.; Gardiner, C.M. Canonical tgf-beta signaling pathway represses human nk cell metabolism. J. Immunol. 2018, 200, 3934–3941. [Google Scholar] [CrossRef] [PubMed]
- Taipale, J.; Lohi, J.; Saarinen, J.; Kovanen, P.T.; Keski-Oja, J. Human mast cell chymase and leukocyte elastase release latent transforming growth factor-beta 1 from the extracellular matrix of cultured human epithelial and endothelial cells. J. Biol. Chem. 1995, 270, 4689–4696. [Google Scholar] [CrossRef] [PubMed]
- Lindstedt, K.A.; Wang, Y.; Shiota, N.; Saarinen, J.; Hyytiainen, M.; Kokkonen, J.O.; Keski-Oja, J.; Kovanen, P.T. Activation of paracrine tgf-beta1 signaling upon stimulation and degranulation of rat serosal mast cells: A novel function for chymase. FASEB J. 2001, 15, 1377–1388. [Google Scholar] [CrossRef] [PubMed]
- Hutzen, B.; Chen, C.Y.; Wang, P.Y.; Sprague, L.; Swain, H.M.; Love, J.; Conner, J.; Boon, L.; Cripe, T.P. Tgf-beta inhibition improves oncolytic herpes viroimmunotherapy in murine models of rhabdomyosarcoma. Mol. Ther. Oncolytics 2017, 7, 17–26. [Google Scholar] [CrossRef] [PubMed]
- Esaki, S.; Nigim, F.; Moon, E.; Luk, S.; Kiyokawa, J.; Curry, W., Jr.; Cahill, D.P.; Chi, A.S.; Iafrate, A.J.; Martuza, R.L.; et al. Blockade of transforming growth factor-beta signaling enhances oncolytic herpes simplex virus efficacy in patient-derived recurrent glioblastoma models. Int. J. Cancer 2017, 141, 2348–2358. [Google Scholar] [CrossRef] [PubMed]
- Geevarghese, S.K.; Geller, D.A.; de Haan, H.A.; Horer, M.; Knoll, A.E.; Mescheder, A.; Nemunaitis, J.; Reid, T.R.; Sze, D.Y.; Tanabe, K.K.; et al. Phase i/ii study of oncolytic herpes simplex virus nv1020 in patients with extensively pretreated refractory colorectal cancer metastatic to the liver. Hum. Gene. Ther. 2010, 21, 1119–1128. [Google Scholar] [CrossRef] [PubMed]
- Cary, Z.D.; Willingham, M.C.; Lyles, D.S. Oncolytic vesicular stomatitis virus induces apoptosis in u87 glioblastoma cells by a type ii death receptor mechanism and induces cell death and tumor clearance in vivo. J. Virol. 2011, 85, 5708–5717. [Google Scholar] [CrossRef] [PubMed]
- Silberhumer, G.R.; Brader, P.; Wong, J.; Serganova, I.S.; Gonen, M.; Gonzalez, S.J.; Blasberg, R.; Zamarin, D.; Fong, Y. Genetically engineered oncolytic newcastle disease virus effectively induces sustained remission of malignant pleural mesothelioma. Mol. Cancer Ther. 2010, 9, 2761–2769. [Google Scholar] [CrossRef]
- Heo, J.; Reid, T.; Ruo, L.; Breitbach, C.J.; Rose, S.; Bloomston, M.; Cho, M.; Lim, H.Y.; Chung, H.C.; Kim, C.W.; et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia jx-594 in liver cancer. Nat Med 2013, 19, 329–336. [Google Scholar] [CrossRef]
- Aoki, R.; Kawamura, T.; Goshima, F.; Ogawa, Y.; Nakae, S.; Nakao, A.; Moriishi, K.; Nishiyama, Y.; Shimada, S. Mast cells play a key role in host defense against herpes simplex virus infection through tnf-alpha and il-6 production. J. Invest. Dermatol. 2013, 133, 2170–2179. [Google Scholar] [CrossRef] [PubMed]
- Sun, Q.; Wang, D.; She, R.; Li, W.; Liu, S.; Han, D.; Wang, Y.; Ding, Y. Increased mast cell density during the infection with velogenic newcastle disease virus in chickens. Avian Pathol. 2008, 37, 579–585. [Google Scholar] [CrossRef] [PubMed]
- Fukuda, M.; Ushio, H.; Kawasaki, J.; Niyonsaba, F.; Takeuchi, M.; Baba, T.; Hiramatsu, K.; Okumura, K.; Ogawa, H. Expression and functional characterization of retinoic acid-inducible gene-i-like receptors of mast cells in response to viral infection. J. Innate. Immun. 2013, 5, 163–173. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Lai, Y.; Bernard, J.J.; Macleod, D.T.; Cogen, A.L.; Moss, B.; Di Nardo, A. Skin mast cells protect mice against vaccinia virus by triggering mast cell receptor s1pr2 and releasing antimicrobial peptides. J. Immunol. 2012, 188, 345–357. [Google Scholar] [CrossRef] [PubMed]
- Walsh, S.R.; Bastin, D.; Chen, L.; Nguyen, A.; Storbeck, C.J.; Lefebvre, C.; Stojdl, D.; Bramson, J.L.; Bell, J.C.; Wan, Y. Type i ifn blockade uncouples immunotherapy-induced antitumor immunity and autoimmune toxicity. J. Clin. Invest. 2019, 129, 518–530. [Google Scholar] [CrossRef] [PubMed]
- Jawdat, D.M.; Rowden, G.; Marshall, J.S. Mast cells have a pivotal role in tnf-independent lymph node hypertrophy and the mobilization of langerhans cells in response to bacterial peptidoglycan. J. Immunol. 2006, 177, 1755–1762. [Google Scholar] [CrossRef] [PubMed]
- Helby, J.; Bojesen, S.E.; Nielsen, S.F.; Nordestgaard, B.G. Ige and risk of cancer in 37 747 individuals from the general population. Ann. Oncol. 2015, 26, 1784–1790. [Google Scholar] [CrossRef] [PubMed]
- Jensen-Jarolim, E.; Achatz, G.; Turner, M.C.; Karagiannis, S.; Legrand, F.; Capron, M.; Penichet, M.L.; Rodriguez, J.A.; Siccardi, A.G.; Vangelista, L.; et al. Allergooncology: The role of ige-mediated allergy in cancer. Allergy 2008, 63, 1255–1266. [Google Scholar] [CrossRef]
- Nigro, E.A.; Brini, A.T.; Yenagi, V.A.; Ferreira, L.M.; Achatz-Straussberger, G.; Ambrosi, A.; Sanvito, F.; Soprana, E.; van Anken, E.; Achatz, G.; et al. Cutting edge: Ige plays an active role in tumor immunosurveillance in mice. J. Immunol. 2016, 197, 2583–2588. [Google Scholar] [CrossRef]
- Neuchrist, C.; Kornfehl, J.; Grasl, M.; Lassmann, H.; Kraft, D.; Ehrenberger, K.; Scheiner, O. Distribution of immunoglobulins in squamous cell carcinoma of the head and neck. Int. Arch. Allergy Immunol. 1994, 104, 97–100. [Google Scholar] [CrossRef]
- Fu, S.L.; Pierre, J.; Smith-Norowitz, T.A.; Hagler, M.; Bowne, W.; Pincus, M.R.; Mueller, C.M.; Zenilman, M.E.; Bluth, M.H. Immunoglobulin e antibodies from pancreatic cancer patients mediate antibody-dependent cell-mediated cytotoxicity against pancreatic cancer cells. Clin. Exp. Immunol. 2008, 153, 401–409. [Google Scholar] [CrossRef]
- Karagiannis, S.N.; Bracher, M.G.; Beavil, R.L.; Beavil, A.J.; Hunt, J.; McCloskey, N.; Thompson, R.G.; East, N.; Burke, F.; Sutton, B.J.; et al. Role of ige receptors in ige antibody-dependent cytotoxicity and phagocytosis of ovarian tumor cells by human monocytic cells. Cancer Immunol. Immunother. 2008, 57, 247–263. [Google Scholar] [CrossRef] [PubMed]
- Mommert, S.; Dittrich-Breiholz, O.; Stark, H.; Gutzmer, R.; Werfel, T. The histamine h4 receptor regulates chemokine production in human natural killer cells. Int. Arch. Allergy Immunol. 2015, 166, 225–230. [Google Scholar] [CrossRef] [PubMed]
- Damaj, B.B.; Becerra, C.B.; Esber, H.J.; Wen, Y.; Maghazachi, A.A. Functional expression of h4 histamine receptor in human natural killer cells, monocytes, and dendritic cells. J. Immunol. 2007, 179, 7907–7915. [Google Scholar] [CrossRef] [PubMed]
- Aydin, E.; Johansson, J.; Nazir, F.H.; Hellstrand, K.; Martner, A. Role of nox2-derived reactive oxygen species in nk cell-mediated control of murine melanoma metastasis. Cancer Immunol. Res. 2017, 5, 804–811. [Google Scholar] [CrossRef]
- Hansson, M.; Hermodsson, S.; Brune, M.; Mellqvist, U.H.; Naredi, P.; Betten, A.; Gehlsen, K.R.; Hellstrand, K. Histamine protects t cells and natural killer cells against oxidative stress. J. Interferon Cytokine Res. 1999, 19, 1135–1144. [Google Scholar] [CrossRef] [PubMed]
- Betten, A.; Dahlgren, C.; Hermodsson, S.; Hellstrand, K. Histamine inhibits neutrophil nadph oxidase activity triggered by the lipoxin a4 receptor-specific peptide agonist trp-lys-tyr-met-val-met. Scand. J. Immunol. 2003, 58, 321–326. [Google Scholar] [CrossRef] [PubMed]
- Johansson, M.; Henriksson, R.; Bergenheim, A.T.; Koskinen, L.O. Interleukin-2 and histamine in combination inhibit tumour growth and angiogenesis in malignant glioma. Br. J. Cancer 2000, 83, 826–832. [Google Scholar] [CrossRef] [PubMed]
- Cuapio, A.; Post, M.; Cerny-Reiterer, S.; Gleixner, K.V.; Stefanzl, G.; Basilio, J.; Herndlhofer, S.; Sperr, W.R.; Brons, N.H.; Casanova, E.; et al. Maintenance therapy with histamine plus il-2 induces a striking expansion of two cd56bright nk cell subpopulations in patients with acute myeloid leukemia and supports their activation. Oncotarget 2016, 7, 46466–46481. [Google Scholar] [CrossRef] [PubMed]
- Brune, M.; Castaigne, S.; Catalano, J.; Gehlsen, K.; Ho, A.D.; Hofmann, W.K.; Hogge, D.E.; Nilsson, B.; Or, R.; Romero, A.I.; et al. Improved leukemia-free survival after postconsolidation immunotherapy with histamine dihydrochloride and interleukin-2 in acute myeloid leukemia: Results of a randomized phase 3 trial. Blood 2006, 108, 88–96. [Google Scholar] [CrossRef] [PubMed]
- McAlpine, S.M.; Issekutz, T.B.; Marshall, J.S. Virus stimulation of human mast cells results in the recruitment of cd56(+) t cells by a mechanism dependent on ccr5 ligands. FASEB J. 2012, 26, 1280–1289. [Google Scholar] [CrossRef] [PubMed]
- Becker, Y. Respiratory syncytial virus (rsv) evades the human adaptive immune system by skewing the th1/th2 cytokine balance toward increased levels of th2 cytokines and ige, markers of allergy--a review. Virus Genes 2006, 33, 235–252. [Google Scholar] [CrossRef] [PubMed]
- Sigurs, N.; Bjarnason, R.; Sigurbergsson, F.; Kjellman, B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am. J. Respir. Crit. Care Med. 2000, 161, 1501–1507. [Google Scholar] [CrossRef] [PubMed]
- Jackson, D.J.; Gangnon, R.E.; Evans, M.D.; Roberg, K.A.; Anderson, E.L.; Pappas, T.E.; Printz, M.C.; Lee, W.M.; Shult, P.A.; Reisdorf, E.; et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am. J. Respir. Crit. Care Med. 2008, 178, 667–672. [Google Scholar] [CrossRef] [PubMed]
- Dakhama, A.; Lee, Y.M.; Ohnishi, H.; Jing, X.; Balhorn, A.; Takeda, K.; Gelfand, E.W. Virus-specific ige enhances airway responsiveness on reinfection with respiratory syncytial virus in newborn mice. J. Allergy Clin. Immunol. 2009, 123, 138–145.e5. [Google Scholar] [CrossRef] [PubMed]
- Kimman, T.G.; Terpstra, G.K.; Daha, M.R.; Westenbrink, F. Pathogenesis of naturally acquired bovine respiratory syncytial virus infection in calves: Evidence for the involvement of complement and mast cell mediators. Am. J. Vet. Res. 1989, 50, 694–700. [Google Scholar] [PubMed]
- Everard, M.L.; Fox, G.; Walls, A.F.; Quint, D.; Fifield, R.; Walters, C.; Swarbrick, A.; Milner, A.D. Tryptase and ige concentrations in the respiratory tract of infants with acute bronchiolitis. Arch. Dis. Child 1995, 72, 64–69. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Oymar, K.; Halvorsen, T.; Aksnes, L. Mast cell activation and leukotriene secretion in wheezing infants. Relation to respiratory syncytial virus and outcome. Pediatr. Allergy Immunol. 2006, 17, 37–42. [Google Scholar] [CrossRef] [PubMed]
- Al-Afif, A.; Alyazidi, R.; Oldford, S.A.; Huang, Y.Y.; King, C.A.; Marr, N.; Haidl, I.D.; Anderson, R.; Marshall, J.S. Respiratory syncytial virus infection of primary human mast cells induces the selective production of type i interferons, cxcl10, and ccl4. J. Allergy Clin. Immunol. 2015, 136, 1346–1354.e1. [Google Scholar] [CrossRef] [PubMed]
- Peritt, D.; Robertson, S.; Gri, G.; Showe, L.; Aste-Amezaga, M.; Trinchieri, G. Differentiation of human nk cells into nk1 and nk2 subsets. J. Immunol. 1998, 161, 5821–5824. [Google Scholar] [PubMed]
- Kaiko, G.E.; Phipps, S.; Angkasekwinai, P.; Dong, C.; Foster, P.S. Nk cell deficiency predisposes to viral-induced th2-type allergic inflammation via epithelial-derived il-25. J. Immunol. 2010, 185, 4681–4690. [Google Scholar] [CrossRef] [PubMed]
- Ple, C.; Barrier, M.; Amniai, L.; Marquillies, P.; Bertout, J.; Tsicopoulos, A.; Walzer, T.; Lassalle, P.; Duez, C. Natural killer cells accumulate in lung-draining lymph nodes and regulate airway eosinophilia in a murine model of asthma. Scand. J. Immunol. 2010, 72, 118–127. [Google Scholar] [CrossRef] [PubMed]
- Wingett, D.; Nielson, C.P. Divergence in nk cell and cyclic amp regulation of t cell cd40l expression in asthmatic subjects. J. Leukoc. Biol. 2003, 74, 531–541. [Google Scholar] [CrossRef] [PubMed]
- Mathias, C.B.; Guernsey, L.A.; Zammit, D.; Brammer, C.; Wu, C.A.; Thrall, R.S.; Aguila, H.L. Pro-inflammatory role of natural killer cells in the development of allergic airway disease. Clin. Exp. Allergy 2014, 44, 589–601. [Google Scholar] [CrossRef] [PubMed]
- Wei, H.; Zhang, J.; Xiao, W.; Feng, J.; Sun, R.; Tian, Z. Involvement of human natural killer cells in asthma pathogenesis: Natural killer 2 cells in type 2 cytokine predominance. J. Allergy Clin. Immunol. 2005, 115, 841–847. [Google Scholar] [CrossRef] [PubMed]
- Aktas, E.; Akdis, M.; Bilgic, S.; Disch, R.; Falk, C.S.; Blaser, K.; Akdis, C.; Deniz, G. Different natural killer (nk) receptor expression and immunoglobulin e (ige) regulation by nk1 and nk2 cells. Clin. Exp. Immunol. 2005, 140, 301–309. [Google Scholar] [CrossRef]
- Mesdaghi, M.; Vodjgani, M.; Salehi, E.; Hadjati, J.; Sarrafnejad, A.; Bidad, K.; Berjisian, F. Natural killer cells in allergic rhinitis patients and nonatopic controls. Int. Arch. Allergy Immunol. 2010, 153, 234–238. [Google Scholar] [CrossRef]
- Raundhal, M.; Morse, C.; Khare, A.; Oriss, T.B.; Milosevic, J.; Trudeau, J.; Huff, R.; Pilewski, J.; Holguin, F.; Kolls, J.; et al. High ifn-gamma and low slpi mark severe asthma in mice and humans. J. Clin. Invest. 2015, 125, 3037–3050. [Google Scholar] [CrossRef]
- Krishnan, V.; Diette, G.B.; Rand, C.S.; Bilderback, A.L.; Merriman, B.; Hansel, N.N.; Krishnan, J.A. Mortality in patients hospitalized for asthma exacerbations in the united states. Am. J. Respir. Crit. Care Med. 2006, 174, 633–638. [Google Scholar] [CrossRef]
- Busse, W.W.; Lemanske, R.F., Jr.; Gern, J.E. Role of viral respiratory infections in asthma and asthma exacerbations. Lancet 2010, 376, 826–834. [Google Scholar] [CrossRef]
- Edwards, M.R.; Regamey, N.; Vareille, M.; Kieninger, E.; Gupta, A.; Shoemark, A.; Saglani, S.; Sykes, A.; Macintyre, J.; Davies, J.; et al. Impaired innate interferon induction in severe therapy resistant atopic asthmatic children. Mucosal. Immunol. 2013, 6, 797–806. [Google Scholar] [CrossRef]
- Dunican, E.M.; Fahy, J.V. The role of type 2 inflammation in the pathogenesis of asthma exacerbations. Ann. Am. Thorac. Soc. 2015, 12 Suppl 2, S144–149. [Google Scholar]
- Tel, J.; Torensma, R.; Figdor, C.G.; de Vries, I.J. Il-4 and il-13 alter plasmacytoid dendritic cell responsiveness to cpg DNA and herpes simplex virus-1. J. Invest. Dermatol. 2011, 131, 900–906. [Google Scholar] [CrossRef] [PubMed]
- Moriwaki, A.; Matsumoto, K.; Matsunaga, Y.; Fukuyama, S.; Matsumoto, T.; Kan-o, K.; Noda, N.; Asai, Y.; Nakanishi, Y.; Inoue, H. Il-13 suppresses double-stranded rna-induced ifn-lambda production in lung cells. Biochem. Biophys. Res. Commun. 2011, 404, 922–927. [Google Scholar] [CrossRef] [PubMed]
- Contoli, M.; Ito, K.; Padovani, A.; Poletti, D.; Marku, B.; Edwards, M.R.; Stanciu, L.A.; Gnesini, G.; Pastore, A.; Spanevello, A.; et al. Th2 cytokines impair innate immune responses to rhinovirus in respiratory epithelial cells. Allergy 2015, 70, 910–920. [Google Scholar] [CrossRef] [PubMed]
- Jordan, W.J.; Eskdale, J.; Srinivas, S.; Pekarek, V.; Kelner, D.; Rodia, M.; Gallagher, G. Human interferon lambda-1 (ifn-lambda1/il-29) modulates the th1/th2 response. Genes Immun. 2007, 8, 254–261. [Google Scholar] [CrossRef]
- Huber, J.P.; Ramos, H.J.; Gill, M.A.; Farrar, J.D. Cutting edge: Type i ifn reverses human th2 commitment and stability by suppressing gata3. J. Immunol. 2010, 185, 813–817. [Google Scholar] [CrossRef]
- Djukanovic, R.; Harrison, T.; Johnston, S.L.; Gabbay, F.; Wark, P.; Thomson, N.C.; Niven, R.; Singh, D.; Reddel, H.K.; Davies, D.E.; et al. The effect of inhaled ifn-beta on worsening of asthma symptoms caused by viral infections. A randomized trial. Am. J. Respir. Crit. Care Med. 2014, 190, 145–154. [Google Scholar] [CrossRef] [PubMed]
- Cerboni, C.; Zingoni, A.; Cippitelli, M.; Piccoli, M.; Frati, L.; Santoni, A. Antigen-activated human t lymphocytes express cell-surface nkg2d ligands via an atm/atr-dependent mechanism and become susceptible to autologous nk- cell lysis. Blood 2007, 110, 606–615. [Google Scholar] [CrossRef] [PubMed]
Tumor | Role | Biological Action or Clinical Observation |
---|---|---|
Pancreatic adenocarcinoma [41] * Prostate [42] | Pro-tumorigenic | Angiogenesis via VEGF production |
Colorectal cancer [43] Lung adenocarcinoma [44] Melanoma [45] Gastric cancer [46] | Pro-tumorigenic | Angiogenesis |
Renal carcinoma [47] | Pro-tumorigenic | Impair anti-tumoral responses via IL-10 and TGF-β production |
Muscle invasive bladder cancer [48] | Pro-tumorigenic | Negative correlation between TIMC numbers and patient survival |
Hepatocellular cancer [49] * Gastric cancer [50] | Pro-tumorigenic | IL-17 expression |
* Hepatocarcinoma [51] * Colon cancer [52] | Pro-tumorigenic | Recruitment of MDSC Increase the suppressive role of MDSC via IFN-γ and NO production |
* Skin carcinogenesis [53] | Anti-tumorigenic | Recruitment of effector immune cells to the tumor site |
Breast cancer [54] | Anti-tumorigenic | Presence of mast cells is a good prognosis marker |
Renal cell carcinoma [55] | Anti-tumorigenic | Positive correlation between TIMC numbers and patient survival |
Esophageal squamous cell carcinoma [56] | Anti-tumorigenic | Negative correlation between IL-17+ mast cells and tumor invasion |
Ovarian cancer [57] | Anti-tumorigenic | Mast cell infiltration in tumors with high vessel density was associated with improved survival |
B cell lymphoma [58] Pleural mesothelioma [59] | Anti-tumorigenic | TIMC associated to favorable clinical outcome |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Portales-Cervantes, L.; Dawod, B.; Marshall, J.S. Mast Cells and Natural Killer Cells—A Potentially Critical Interaction. Viruses 2019, 11, 514. https://doi.org/10.3390/v11060514
Portales-Cervantes L, Dawod B, Marshall JS. Mast Cells and Natural Killer Cells—A Potentially Critical Interaction. Viruses. 2019; 11(6):514. https://doi.org/10.3390/v11060514
Chicago/Turabian StylePortales-Cervantes, Liliana, Bassel Dawod, and Jean S. Marshall. 2019. "Mast Cells and Natural Killer Cells—A Potentially Critical Interaction" Viruses 11, no. 6: 514. https://doi.org/10.3390/v11060514
APA StylePortales-Cervantes, L., Dawod, B., & Marshall, J. S. (2019). Mast Cells and Natural Killer Cells—A Potentially Critical Interaction. Viruses, 11(6), 514. https://doi.org/10.3390/v11060514