Tissue-Resident Innate and Innate-Like Lymphocyte Responses to Viral Infection
Abstract
:1. Introduction
2. Discussion
2.1. Innate Lymphoid Cells
2.2. Group 1 Innate Lymphoid Cells
2.3. Group 2 Innate Lymphoid Cells (ILC2)
2.4. Group 3 Innate Lymphoid Cells (ILC3)
2.5. Unconventional T Cells
2.6. Natural Killer/ Invariant Natural Killer T (NKT/iNKT) Cells
2.7. MAIT Cells
2.8. γδ T Cells
3. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Iwasaki, A.; Medzhitov, R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5, 987–995. [Google Scholar] [CrossRef] [PubMed]
- Fan, X.; Rudensky, A.Y. Hallmarks of Tissue-Resident Lymphocytes. Cell 2016, 164, 1198–1211. [Google Scholar] [CrossRef] [PubMed]
- Vivier, E.; Artis, D.; Colonna, M.; Diefenbach, A.; Di Santo, J.P.; Eberl, G.; Koyasu, S.; Locksley, R.M.; McKenzie, A.N.J.; Mebius, R.E.; et al. Innate Lymphoid Cells: 10 Years On. Cell 2018, 174, 1054–1066. [Google Scholar] [CrossRef] [PubMed]
- Godfrey, D.I.; Uldrich, A.P.; McCluskey, J.; Rossjohn, J.; Moody, D.B. The burgeoning family of unconventional T cells. Nat. Immunol. 2015, 16, 1114–1123. [Google Scholar] [CrossRef] [PubMed]
- Gasteiger, G.; Fan, X.; Dikiy, S.; Lee, S.Y.; Rudensky, A.Y. Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science 2015, 350, 981–985. [Google Scholar] [CrossRef] [PubMed]
- O’Sullivan, T.E.; Rapp, M.; Fan, X.; Weizman, O.-E.; Bhardwaj, P.; Adams, N.M.; Walzer, T.; Dannenberg, A.J.; Sun, J.C. Adipose-Resident Group 1 Innate Lymphoid Cells Promote Obesity-Associated Insulin Resistance. Immunity 2016, 45, 428–441. [Google Scholar] [CrossRef] [PubMed]
- Weizman, O.-E.; Adams, N.M.; Schuster, I.S.; Krishna, C.; Pritykin, Y.; Lau, C.; Degli-Esposti, M.A.; Leslie, C.S.; Sun, J.C.; O’Sullivan, T.E. ILC1 Confer Early Host Protection at Initial Sites of Viral Infection. Cell 2017, 171, 795–808. [Google Scholar] [CrossRef] [PubMed]
- Vashist, N.; Trittel, S.; Ebensen, T.; Chambers, B.J.; Guzmán, C.A.; Riese, P. Influenza-Activated ILC1s Contribute to Antiviral Immunity Partially Influenced by Differential GITR Expression. Front. Immunol. 2018, 9, 505. [Google Scholar] [CrossRef] [PubMed]
- Krueger, P.D.; Narayanan, S.; Surette, F.A.; Brown, M.G.; Sung, S.-S.J.; Hahn, Y.S. Murine liver-resident group 1 innate lymphoid cells regulate optimal priming of anti-viral CD8+ T cells. J. Leukoc. Biol. 2017, 101, 329–338. [Google Scholar] [CrossRef]
- Zhou, J.; Peng, H.; Li, K.; Qu, K.; Wang, B.; Wu, Y.; Ye, L.; Dong, Z.; Wei, H.; Sun, R.; et al. Liver-Resident NK Cells Control Antiviral Activity of Hepatic T Cells via the PD-1-PD-L1 Axis. Immunity 2019, 50, 403–417. [Google Scholar] [CrossRef]
- Duerr, C.U.; McCarthy, C.D.A.; Mindt, B.C.; Rubio, M.; Meli, A.P.; Pothlichet, J.; Eva, M.M.; Gauchat, J.-F.; Qureshi, S.T.; Mazer, B.D.; et al. Type I interferon restricts type 2 immunopathology through the regulation of group 2 innate lymphoid cells. Nat. Immunol. 2016, 17, 65–75. [Google Scholar] [CrossRef] [PubMed]
- Moro, K.; Kabata, H.; Tanabe, M.; Koga, S.; Takeno, N.; Mochizuki, M.; Fukunaga, K.; Asano, K.; Betsuyaku, T.; Koyasu, S. Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat. Immunol. 2016, 17, 76–86. [Google Scholar] [CrossRef] [PubMed]
- Monticelli, L.A.; Sonnenberg, G.F.; Abt, M.C.; Alenghat, T.; Ziegler, C.G.K.; Doering, T.A.; Angelosanto, J.M.; Laidlaw, B.J.; Sathaliyawala, T.; Kubota, M.; et al. Innate lymphoid cells promote lung tissue homeostasis following acute influenza virus infection. Nat. Immunol. 2012, 30, 1045–1054. [Google Scholar]
- Arpaia, N.; Green, J.A.; Moltedo, B.; Arvey, A.; Hemmers, S.; Yuan, S.; Treuting, P.M.; Rudensky, A.Y. A Distinct Function of Regulatory T Cells in Tissue Protection. Cell 2015, 162, 1078–1089. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gorski, S.A.; Hahn, Y.S.; Braciale, T.J. Group 2 Innate Lymphoid Cell Production of IL-5 Is Regulated by NKT Cells during Influenza Virus Infection. PLoS Pathog. 2013, 9, e1003615. [Google Scholar] [CrossRef] [PubMed]
- Lai, D.; Tang, J.; Chen, L.; Fan, E.K.; Scott, M.J.; Li, Y.; Billiar, T.R.; Wilson, M.A.; Fang, X.; Shu, Q.; et al. Group 2 innate lymphoid cells protect lung endothelial cells from pyroptosis in sepsis. Cell Death Dis. 2018, 9, 369. [Google Scholar] [CrossRef] [Green Version]
- Rauber, S.; Luber, M.; Weber, S.; Maul, L.; Soare, A.; Wohlfahrt, T.; Lin, N.-Y.; Dietel, K.; Bozec, A.; Herrmann, M.; et al. Resolution of inflammation by interleukin-9-producing type 2 innate lymphoid cells. Nat. Med. 2017, 23, 938–944. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chang, Y.-J.; Kim, H.Y.; Albacker, L.A.; Baumgarth, N.; McKenzie, A.N.J.; Smith, D.E.; DeKruyff, R.H.; Umetsu, D.T. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat. Immunol. 2011, 12, 631–638. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jackson, D.J.; Makrinioti, H.; Rana, B.M.J.; Shamji, B.W.H.; Trujillo-Torralbo, M.-B.; Footitt, J.; del-Rosario, J.; Telcian, A.G.; Nikonova, A.; Zhu, J.; et al. IL-33–Dependent Type 2 Inflammation during Rhinovirus-induced Asthma Exacerbations In Vivo. Am. J. Respir. Crit. Care Med. 2014, 190, 1373–1382. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stier, M.T.; Bloodworth, M.H.; Toki, S.; Newcomb, D.C.; Goleniewska, K.; Boyd, K.L.; Quitalig, M.; Hotard, A.L.; Moore, M.L.; Hartert, T.V.; et al. Respiratory syncytial virus infection activates IL-13–producing group 2 innate lymphoid cells through thymic stromal lymphopoietin. J. Allergy Clin. Immunol. 2016, 138, 814–824. [Google Scholar] [CrossRef]
- Martinez-Gonzalez, I.; Mathä, L.; Steer, C.A.; Ghaedi, M.; Poon, G.F.T.; Takei, F. Allergen-Experienced Group 2 Innate Lymphoid Cells Acquire Memory-like Properties and Enhance Allergic Lung Inflammation. Immunity 2016, 45, 198–208. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Wang, W.; Zhao, C.; Wang, Y.; Wu, H.; Sun, X.; Guan, Y.; Zhang, Y. Prostaglandin E2 Inhibits Group 2 Innate Lymphoid Cell Activation and Allergic Airway Inflammation Through E-Prostanoid 4-Cyclic Adenosine Monophosphate Signaling. Front. Immunol. 2018, 9, 501. [Google Scholar] [CrossRef] [PubMed]
- Hernández, P.P.; Mahlakõiv, T.; Yang, I.; Schwierzeck, V.; Nguyen, N.; Guendel, F.; Gronke, K.; Ryffel, B.; Hölscher, C.; Dumoutier, L.; et al. Interferon-λ and interleukin 22 act synergistically for the induction of interferon-stimulated genes and control of rotavirus infection. Nat. Immunol. 2015, 16, 698–707. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.; Wang, X.; Liu, D.X.; Moroney-Rasmussen, T.; Lackner, A.A.; Veazey, R.S. IL-17-producing innate lymphoid cells are restricted to mucosal tissues and are depleted in SIV-infected macaques. Mucosal Immunol. 2012, 5, 658–669. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reeves, R.K.; Rajakumar, P.A.; Evans, T.I.; Connole, M.; Gillis, J.; Wong, F.E.; Kuzmichev, Y.V.; Carville, A.; Johnson, R.P. Gut inflammation and indoleamine deoxygenase inhibit IL-17 production and promote cytotoxic potential in NKp44+ mucosal NK cells during SIV infection. Blood 2011, 118, 3321–3330. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Richert-Spuhler, L.E.; Evans, T.I.; Gillis, J.; Connole, M.; Estes, J.D.; Keele, B.F.; Klatt, N.R.; Reeves, R.K. Hypercytotoxicity and Rapid Loss of NKp44+ Innate Lymphoid Cells during Acute SIV Infection. PLoS Pathog. 2014, 10, e1004551. [Google Scholar] [CrossRef]
- Mudd, J.C.; Busman-Sahay, K.; DiNapoli, S.R.; Lai, S.; Sheik, V.; Lisco, A.; Deleage, C.; Richardson, B.; Palesch, D.J.; Paiardini, M.; et al. Hallmarks of primate lentiviral immunodeficiency infection recapitulate loss of innate lymphoid cells. Nat. Commun. 2018, 9, 3967. [Google Scholar] [CrossRef]
- Rankin, L.C.; Girard-Madoux, M.J.H.; Seillet, C.; Mielke, L.A.; Kerdiles, Y.; Fenis, A.; Wieduwild, E.; Putoczki, T.; Mondot, S.; Lantz, O.; et al. Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat. Immunol. 2016, 17, 179–186. [Google Scholar] [CrossRef]
- Jie, Z.; Liang, Y.; Hou, L.; Dong, C.; Iwakura, Y.; Soong, L.; Cong, Y.; Sun, J. Intrahepatic Innate Lymphoid Cells Secrete IL-17A and IL-17F That Are Crucial for T Cell Priming in Viral Infection. J. Immunol. 2014, 192, 3289–3300. [Google Scholar] [CrossRef] [Green Version]
- Zhao, J.; Zhang, Z.; Luan, Y.; Zou, Z.; Sun, Y.; Li, Y.; Jin, L.; Zhou, C.; Fu, J.; Gao, B.; et al. Pathological functions of interleukin-22 in chronic liver inflammation and fibrosis with hepatitis B virus infection by promoting T helper 17 cell recruitment. Hepatology 2014, 59, 1331–1342. [Google Scholar] [CrossRef]
- Wang, Q.; Zhou, J.; Zhang, B.; Tian, Z.; Tang, J.; Zheng, Y.; Huang, Z.; Tian, Y.; Jia, Z.; Tang, Y.; et al. Hepatitis B Virus Induces IL-23 Production in Antigen Presenting Cells and Causes Liver Damage via the IL-23/IL-17 Axis. PLoS Pathog. 2013, 9, e1003410. [Google Scholar] [CrossRef]
- Taube, C.; Tertilt, C.; Gyülveszi, G.; Dehzad, N.; Kreymborg, K.; Schneeweiss, K.; Michel, E.; Reuter, S.; Renauld, J.-C.; Arnold-Schild, D.; et al. IL-22 Is Produced by Innate Lymphoid Cells and Limits Inflammation in Allergic Airway Disease. PLoS ONE 2011, 6, e21799. [Google Scholar] [CrossRef]
- Wingender, G.; Krebs, P.; Beutler, B.; Kronenberg, M. Antigen-Specific Cytotoxicity by Invariant NKT Cells In Vivo Is CD95/CD178-Dependent and Is Correlated with Antigenic Potency. J. Immunol. 2010, 185, 2721–2729. [Google Scholar] [CrossRef]
- Vincent, M.S.; Leslie, D.S.; Gumperz, J.E.; Xiong, X.; Grant, E.P.; Brenner, M.B. CD1-dependent dendritic cell instruction. Nat. Immunol. 2002, 3, 1163–1168. [Google Scholar] [CrossRef]
- Carreño, L.J.; Kharkwal, S.S.; Porcelli, S.A. Optimizing NKT cell ligands as vaccine adjuvants. Immunotherapy 2014, 6, 309–320. [Google Scholar] [CrossRef] [Green Version]
- De Santo, C.; Salio, M.; Masri, S.H.; Lee, L.Y.-H.; Dong, T.; Speak, A.O.; Porubsky, S.; Booth, S.; Veerapen, N.; Besra, G.S.; et al. Invariant NKT cells reduce the immunosuppressive activity of influenza A virus–induced myeloid-derived suppressor cells in mice and humans. J. Clin. Investig. 2008, 118, 4036–4048. [Google Scholar] [CrossRef] [Green Version]
- Johnson, T.R.; Hong, S.; Van Kaer, L.; Koezuka, Y.; Graham, B.S. NK T Cells Contribute to Expansion of CD8+ T Cells and Amplification of Antiviral Immune Responses to Respiratory Syncytial Virus. J. Virol. 2002, 76, 4294–4303. [Google Scholar] [CrossRef]
- Sanchez, D.J.; Gumperz, J.E.; Ganem, D. Regulation of CD1d expression and function by a herpesvirus infection. J. Clin. Investig. 2005, 115, 1369–1378. [Google Scholar] [CrossRef] [Green Version]
- Rao, P.; Pham, H.T.; Kulkarni, A.; Yang, Y.; Liu, X.; Knipe, D.M.; Cresswell, P.; Yuan, W. Herpes Simplex Virus 1 Glycoprotein B and US3 Collaborate To Inhibit CD1d Antigen Presentation and NKT Cell Function. J. Virol. 2011, 85, 8093–8104. [Google Scholar] [CrossRef]
- Webb, T.J.R.; Litavecz, R.A.; Khan, M.A.; Du, W.; Gervay-Hague, J.; Renukaradhya, G.J.; Brutkiewicz, R.R. Inhibition of CD1d1-mediated antigen presentation by the vaccinia virus B1R and H5R molecules. Eur. J. Immunol. 2006, 36, 2595–2600. [Google Scholar] [CrossRef] [Green Version]
- Miura, S.; Kawana, K.; Schust, D.J.; Fujii, T.; Yokoyama, T.; Iwasawa, Y.; Nagamatsu, T.; Adachi, K.; Tomio, A.; Tomio, K.; et al. CD1d, a Sentinel Molecule Bridging Innate and Adaptive Immunity, Is Downregulated by the Human Papillomavirus (HPV) E5 Protein: A Possible Mechanism for Immune Evasion by HPV. J. Virol. 2010, 84, 11614–11623. [Google Scholar] [CrossRef]
- Chen, N.; McCarthy, C.; Drakesmith, H.; Li, D.; Cerundolo, V.; McMichael, A.J.; Screaton, G.R.; Xu, X.-N. HIV-1 down-regulates the expression of CD1d via Nef. Eur. J. Immunol. 2006, 36, 278–286. [Google Scholar] [CrossRef] [Green Version]
- van Dommelen, S.L.H.; Tabarias, H.A.; Smyth, M.J.; Degli-Esposti, M.A. Activation of Natural Killer (NK) T Cells during Murine Cytomegalovirus Infection Enhances the Antiviral Response Mediated by NK Cells. J. Virol. 2003, 77, 1877–1884. [Google Scholar] [CrossRef] [Green Version]
- Guillonneau, C.; Mintern, J.D.; Hubert, F.-X.; Hurt, A.C.; Besra, G.S.; Porcelli, S.; Barr, I.G.; Doherty, P.C.; Godfrey, D.I.; Turner, S.J. Combined NKT cell activation and influenza virus vaccination boosts memory CTL generation and protective immunity. Proc. Natl. Acad. Sci. USA 2009, 106, 3330–3335. [Google Scholar] [CrossRef] [Green Version]
- Ko, S.-Y.; Ko, H.-J.; Chang, W.-S.; Park, S.-H.; Kweon, M.-N.; Kang, C.-Y. α-Galactosylceramide Can Act As a Nasal Vaccine Adjuvant Inducing Protective Immune Responses against Viral Infection and Tumor. J. Immunol. 2005, 175, 3309–3317. [Google Scholar] [CrossRef]
- Artiaga, B.L.; Yang, G.; Hackmann, T.J.; Liu, Q.; Richt, J.A.; Salek-Ardakani, S.; Castleman, W.L.; Lednicky, J.A.; Driver, J.P. α-Galactosylceramide protects swine against influenza infection when administered as a vaccine adjuvant. Sci. Rep. 2016, 6, 23593. [Google Scholar] [CrossRef] [Green Version]
- Veldt, B.J.; van der Vliet, H.J.J.; von Blomberg, B.M.E.; van Vlierberghe, H.; Gerken, G.; Nishi, N.; Hayashi, K.; Scheper, R.J.; de Knegt, R.J.; van den Eertwegh, A.J.M.; et al. Randomized placebo controlled phase I/II trial of α-galactosylceramide for the treatment of chronic hepatitis C. J. Hepatol. 2007, 47, 356–365. [Google Scholar] [CrossRef]
- Woltman, A.M.; ter Borg, M.; Binda, R.; Sprengers, D.; von Blomberg, B.M.; Scheper, R.; Hayashi, K.; Nishi, N.; Boonstra, A.; van der Molen, R.; et al. α-Galactosylceramide in chronic hepatitis B infection: Results from a randomized placebo-controlled Phase I/II trial. Antivir. Ther. 2009, 14, 809–818. [Google Scholar] [CrossRef]
- Treiner, E.; Duban, L.; Bahram, S.; Radosavljevic, M.; Wanner, V.; Tilloy, F.; Affaticati, P.; Gilfillan, S.; Lantz, O. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 2003, 422, 164–169. [Google Scholar] [CrossRef]
- Gold, M.C.; Cerri, S.; Smyk-Pearson, S.; Cansler, M.E.; Vogt, T.M.; Delepine, J.; Winata, E.; Swarbrick, G.M.; Chua, W.-J.; Yu, Y.Y.L.; et al. Human Mucosal Associated Invariant T Cells Detect Bacterially Infected Cells. PLoS Biol. 2010, 8, e1000407. [Google Scholar] [CrossRef]
- Le Bourhis, L.; Martin, E.; Péguillet, I.; Guihot, A.; Froux, N.; Coré, M.; Lévy, E.; Dusseaux, M.; Meyssonnier, V.; Premel, V.; et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 2010, 11, 701–708. [Google Scholar] [CrossRef] [Green Version]
- Gold, M.C.; McLaren, J.E.; Reistetter, J.A.; Smyk-Pearson, S.; Ladell, K.; Swarbrick, G.M.; Yu, Y.Y.L.; Hansen, T.H.; Lund, O.; Nielsen, M.; et al. MR1-restricted MAIT cells display ligand discrimination and pathogen selectivity through distinct T cell receptor usage. J. Exp. Med. 2014, 211, 1601–1610. [Google Scholar] [CrossRef]
- Ussher, J.E.; Klenerman, P.; Willberg, C.B. Mucosal-Associated Invariant T-Cells: New Players in Anti-Bacterial Immunity. Front. Immunol. 2014, 5, 450. [Google Scholar] [CrossRef]
- Bennett, M.S.; Trivedi, S.; Iyer, A.S.; Hale, J.S.; Leung, D.T. Human mucosal-associated invariant T (MAIT) cells possess capacity for B cell help. J. Leukoc. Biol. 2017, 102, 1261–1269. [Google Scholar] [CrossRef]
- Ussher, J.E.; Bilton, M.; Attwod, E.; Shadwell, J.; Richardson, R.; de Lara, C.; Mettke, E.; Kurioka, A.; Hansen, T.H.; Klenerman, P.; et al. CD161++ CD8+ T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner: Innate immunity. Eur. J. Immunol. 2014, 44, 195–203. [Google Scholar] [CrossRef]
- van Wilgenburg, B.; Scherwitzl, I.; Hutchinson, E.C.; Leng, T.; Kurioka, A.; Kulicke, C.; de Lara, C.; Cole, S.; Vasanawathana, S.; Limpitikul, W.; et al. MAIT cells are activated during human viral infections. Nat. Commun. 2016, 7, 11653. [Google Scholar] [CrossRef] [Green Version]
- Paquin-Proulx, D.; Avelino-Silva, V.I.; Santos, B.A.N.; Silveira Barsotti, N.; Siroma, F.; Fernandes Ramos, J.; Coracini Tonacio, A.; Song, A.; Maestri, A.; Barros Cerqueira, N.; et al. MAIT cells are activated in acute Dengue virus infection and after in vitro Zika virus infection. PLoS Negl. Trop. Dis. 2018, 12, e0006154. [Google Scholar] [CrossRef]
- van Wilgenburg, B.; Loh, L.; Chen, Z.; Pediongco, T.J.; Wang, H.; Shi, M.; Zhao, Z.; Koutsakos, M.; Nüssing, S.; Sant, S.; et al. MAIT cells contribute to protection against lethal influenza infection in vivo. Nat. Commun. 2018, 9, 4706. [Google Scholar] [CrossRef]
- Leeansyah, E.; Ganesh, A.; Quigley, M.F.; Sonnerborg, A.; Andersson, J.; Hunt, P.W.; Somsouk, M.; Deeks, S.G.; Martin, J.N.; Moll, M.; et al. Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 2013, 121, 1124–1135. [Google Scholar] [CrossRef]
- Fernandez, C.S.; Amarasena, T.; Kelleher, A.D.; Rossjohn, J.; McCluskey, J.; Godfrey, D.I.; Kent, S.J. MAIT cells are depleted early but retain functional cytokine expression in HIV infection. Immunol. Cell Biol. 2015, 93, 177–188. [Google Scholar] [CrossRef]
- Leeansyah, E.; Svärd, J.; Dias, J.; Buggert, M.; Nyström, J.; Quigley, M.F.; Moll, M.; Sönnerborg, A.; Nowak, P.; Sandberg, J.K. Arming of MAIT Cell Cytolytic Antimicrobial Activity Is Induced by IL-7 and Defective in HIV-1 Infection. PLoS Pathog. 2015, 11, e1005072. [Google Scholar] [CrossRef]
- Robinette, M.L.; Bando, J.K.; Song, W.; Ulland, T.K.; Gilfillan, S.; Colonna, M. IL-15 sustains IL-7R-independent ILC2 and ILC3 development. Nat. Commun. 2017, 8, 14601. [Google Scholar] [CrossRef] [Green Version]
- Pang, T.; Cardosa, M.J.; Guzman, M.G. Of cascades and perfect storms: The immunopathogenesis of dengue haemorrhagic fever-dengue shock syndrome (DHF/DSS). Immunol. Cell Biol. 2007, 85, 43–45. [Google Scholar] [CrossRef]
- Wang, S.; Le, T.Q.; Kurihara, N.; Chida, J.; Cisse, Y.; Yano, M.; Kido, H. Influenza Virus–Cytokine-Protease Cycle in the Pathogenesis of Vascular Hyperpermeability in Severe Influenza. J. Infect. Dis. 2010, 202, 991–1001. [Google Scholar] [CrossRef]
- Latha, T.S.; Reddy, M.C.; Durbaka, P.V.R.; Rachamallu, A.; Pallu, R.; Lomada, D. γδ T Cell-Mediated Immune Responses in Disease and Therapy. Front. Immunol. 2014, 5, 571. [Google Scholar] [CrossRef]
- Chien, Y.; Meyer, C.; Bonneville, M. γδ T Cells: First Line of Defense and Beyond. Annu. Rev. Immunol. 2014, 32, 121–155. [Google Scholar] [CrossRef]
- Uldrich, A.P.; Le Nours, J.; Pellicci, D.G.; Gherardin, N.A.; McPherson, K.G.; Lim, R.T.; Patel, O.; Beddoe, T.; Gras, S.; Rossjohn, J.; et al. CD1d-lipid antigen recognition by the γδ TCR. Nat. Immunol. 2013, 14, 1137–1145. [Google Scholar] [CrossRef]
- Long, K.M.; Ferris, M.T.; Whitmore, A.C.; Montgomery, S.A.; Thurlow, L.R.; McGee, C.E.; Rodriguez, C.A.; Lim, J.K.; Heise, M.T. γδ T Cells Play a Protective Role in Chikungunya Virus-Induced Disease. J. Virol. 2016, 90, 433–443. [Google Scholar] [CrossRef]
- Simonian, P.L.; Roark, C.L.; Diaz del Valle, F.; Palmer, B.E.; Douglas, I.S.; Ikuta, K.; Born, W.K.; O’Brien, R.L.; Fontenot, A.P. Regulatory Role of T Cells in the Recruitment of CD4+ and CD8+ T Cells to Lung and Subsequent Pulmonary Fibrosis. J. Immunol. 2006, 177, 4436–4443. [Google Scholar] [CrossRef]
- Barcy, S.; De Rosa, S.C.; Vieira, J.; Diem, K.; Ikoma, M.; Casper, C.; Corey, L. γδ+ T Cells Involvement in Viral Immune Control of Chronic Human Herpesvirus 8 Infection. J. Immunol. 2008, 180, 3417–3425. [Google Scholar] [CrossRef]
- Ravens, S.; Schultze-Florey, C.; Raha, S.; Sandrock, I.; Drenker, M.; Oberdörfer, L.; Reinhardt, A.; Ravens, I.; Beck, M.; Geffers, R.; et al. Human γδ T cells are quickly reconstituted after stem-cell transplantation and show adaptive clonal expansion in response to viral infection. Nat. Immunol. 2017, 18, 393–401. [Google Scholar] [CrossRef] [PubMed]
- Selin, L.K.; Santolucito, P.A.; Pinto, A.K.; Szomolanyi-Tsuda, E.; Welsh, R.M. Innate Immunity to Viruses: Control of Vaccinia Virus Infection by T Cells. J. Immunol. 2001, 166, 6784–6794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, T.; Gao, Y.; Scully, E.; Davis, C.T.; Anderson, J.F.; Welte, T.; Ledizet, M.; Koski, R.; Madri, J.A.; Barrett, A.; et al. T Cells Facilitate Adaptive Immunity against West Nile Virus Infection in Mice. J. Immunol. 2006, 177, 1825–1832. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agrati, C.; Alonzi, T.; De Santis, R.; Castilletti, C.; Abbate, I.; Capobianchi, M.R.; D’Offizi, G.; Siepi, F.; Fimia, G.M.; Tripodi, M.; et al. Activation of Vγ9Vδ2 T cells by non-peptidic antigens induces the inhibition of subgenomic HCV replication. Int. Immunol. 2006, 18, 11–18. [Google Scholar] [CrossRef] [PubMed]
- Qin, G.; Liu, Y.; Zheng, J.; Ng, I.H.Y.; Xiang, Z.; Lam, K.-T.; Mao, H.; Li, H.; Peiris, J.S.M.; Lau, Y.-L.; et al. Type 1 Responses of Human V 9V 2 T Cells to Influenza A Viruses. J. Virol. 2011, 85, 10109–10116. [Google Scholar] [CrossRef] [PubMed]
- Djaoud, Z.; Guethlein, L.A.; Horowitz, A.; Azzi, T.; Nemat-Gorgani, N.; Olive, D.; Nadal, D.; Norman, P.J.; Münz, C.; Parham, P. Two alternate strategies for innate immunity to Epstein-Barr virus: One using NK cells and the other NK cells and γδ T cells. J. Exp. Med. 2017, 214, 1827–1841. [Google Scholar] [CrossRef] [Green Version]
- Chen, M.; Zhang, D.; Zhen, W.; Shi, Q.; Liu, Y.; Ling, N.; Peng, M.; Tang, K.; Hu, P.; Hu, H.; et al. Characteristics of Circulating T Cell Receptor γδ T Cells from Individuals Chronically Infected with Hepatitis B Virus (HBV): An Association between Vδ2 Subtype and Chronic HBV Infection. J. Infect. Dis. 2008, 198, 1643–1650. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khairallah, C.; Netzer, S.; Villacreces, A.; Juzan, M.; Rousseau, B.; Dulanto, S.; Giese, A.; Costet, P.; Praloran, V.; Moreau, J.-F.; et al. γδ T Cells Confer Protection against Murine Cytomegalovirus (MCMV). PLoS Pathog. 2015, 11, e1004702. [Google Scholar] [CrossRef] [PubMed]
- Sell, S.; Dietz, M.; Schneider, A.; Holtappels, R.; Mach, M.; Winkler, T.H. Control of Murine Cytomegalovirus Infection by γδ T Cells. PLoS Pathog. 2015, 11, e1004481. [Google Scholar] [CrossRef]
- Bhatnagar, N.; Girard, P.-M.; Lopez-Gonzalez, M.; Didier, C.; Collias, L.; Jung, C.; Bollens, D.; Duvivier, C.; Von Platen, C.; Scott-Algara, D.; et al. Potential Role of Vδ2+ γδ T Cells in Regulation of Immune Activation in Primary HIV Infection. Front. Immunol. 2017, 8, 1189. [Google Scholar] [CrossRef]
- Olson, G.S.; Moore, S.W.; Richter, J.M.; Garber, J.J.; Bowman, B.A.; Rawlings, C.A.; Flagg, M.; Corleis, B.; Kwon, D.S. Increased frequency of systemic pro-inflammatory Vδ1+ γδ T cells in HIV elite controllers correlates with gut viral load. Sci. Rep. 2018, 8, 16471. [Google Scholar] [CrossRef] [PubMed]
- Tu, W.; Zheng, J.; Liu, Y.; Sia, S.F.; Liu, M.; Qin, G.; Ng, I.H.Y.; Xiang, Z.; Lam, K.-T.; Peiris, J.S.M.; et al. The aminobisphosphonate pamidronate controls influenza pathogenesis by expanding a γδ T cell population in humanized mice. J. Exp. Med. 2011, 208, 1511–1522. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Cell Type | Virus | Protection or Pathogenesis | Genetic Evidence * | Redundancy | Reference |
---|---|---|---|---|---|
ILC1 | MCMV | Protection | Yes | No | [7] |
ILC1 | Influenza A (H1N1) | Protection | No | ? | [8] |
ILC1 | Adenovirus, LCMV | Protection | No | ? | [9,10] |
ILC2 | Influenza A (H1N1) | Pathogenesis | No | ? | [11] |
ILC2 | Influenza A (H1N1) | Protection | No | ? | [13] |
ILC2 | Influenza A (H1N1) | Protection | No | ? | [15] |
ILC2 | Influenza A (H3N1) | Pathogenesis | No | ? | [18] |
ILC2 | Rhinovirus | Pathogenesis | No | ? | [19] |
ILC2 | RSV | Pathogenesis | No | ? | [20] |
ILC3 | Rotavirus | Protection | No | ? | [23] |
ILC3 | SIV | Protection | No | ? | [24,25,26] |
ILC3 | Adenovirus, LCMV | Pathogenesis | No | ? | [29] |
ILC3 | Chronic HBV | Pathogenesis | No | ? | [30,31] |
iNKT | Influenza A (PR8) | Protection | Yes | No | [36] |
iNKT | RSV | Protection | No | ? | [37] |
iNKT | MCMV | Protection | Yes | Yes | [43] |
iNKT | Influenza A | Protection | No | ? | [44,45] |
iNKT | Influenza A (H1N1) | Protection | No | ? | [46] |
iNKT | Chronic HBV, HCV | Neither | No | ? | [47,48] |
MAIT | Dengue, HCV, Influenza | Both | No | ? | [56] |
MAIT | Influenza A (H1N1) | Protection | Yes | No | [58] |
MAIT | HIV | Protection | No | ? | [61] |
γδ | HHV | Protection | No | ? | [70,71] |
γδ | Vaccinia, West Nile | Protection | Yes | No | [72,73] |
γδ | MCMV | Protection | Yes | Yes | [78,79] |
γδ | HIV | Pathogenesis | No | ? | [81] |
γδ | Influenza A (H1N1, H5N1) | Protection | Yes | No | [82] |
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Hildreth, A.D.; O’Sullivan, T.E. Tissue-Resident Innate and Innate-Like Lymphocyte Responses to Viral Infection. Viruses 2019, 11, 272. https://doi.org/10.3390/v11030272
Hildreth AD, O’Sullivan TE. Tissue-Resident Innate and Innate-Like Lymphocyte Responses to Viral Infection. Viruses. 2019; 11(3):272. https://doi.org/10.3390/v11030272
Chicago/Turabian StyleHildreth, Andrew D., and Timothy E. O’Sullivan. 2019. "Tissue-Resident Innate and Innate-Like Lymphocyte Responses to Viral Infection" Viruses 11, no. 3: 272. https://doi.org/10.3390/v11030272
APA StyleHildreth, A. D., & O’Sullivan, T. E. (2019). Tissue-Resident Innate and Innate-Like Lymphocyte Responses to Viral Infection. Viruses, 11(3), 272. https://doi.org/10.3390/v11030272