Vγ4+γδT Cells Aggravate Severe H1N1 Influenza Virus Infection-Induced Acute Pulmonary Immunopathological Injury via Secreting Interleukin-17A

Frontiers in Immunology

Volumn 8, Issue , 2017, Pages

  Xue, Chunxue ^a   Wen, Mingjie ^b   Bao, Linlin ^c   Li, Hui ^d   Li, Fengdi ^c   Liu, Meng ^e   Lv, Qi ^c   An, Yunqing ^b   Zhang, Xulong ^b   Cao, Bin ^b,d  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

^d CHINA JAPAN FRIENDSHIP HOSPITAL   (China)

^e BEIJING HOSPITAL OF TRADITIONAL CHINESE MEDICINE AFFILIATED TO CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

A (H1N1) pdm09 virus; acute lung injury; influenza; interleukin 17A; NKG2D; T cell subsets

Indexed keywords

EID: 85050313803     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.01054     Document Type: Article

References (70)

1. Novel Swine-Origin Influenza AVIT Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, et al. Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med (2009) 360(25):2605–15.10.1056/NEJMoa090381019423869
2. Itoh Y, Shinya K, Kiso M, Watanabe T, Sakoda Y, Hatta M, et al. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature (2009) 460(7258):1021–5.10.1038/nature0826019672242
3. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science (2009) 325(5937):197–201.10.1126/science.117622519465683
4. Bai L, Gu L, Cao B, Zhai XL, Lu M, Lu Y, et al. Clinical features of pneumonia caused by 2009 influenza A(H1N1) virus in Beijing, China. Chest (2011) 139(5):1156–64.10.1378/chest.10-1036
5. Cao B, Li XW, Mao Y, Wang J, Lu HZ, Chen YS, et al. Clinical features of the initial cases of 2009 pandemic influenza A (H1N1) virus infection in China. N Engl J Med (2009) 361(26):2507–17.10.1056/NEJMoa090661220007555
6. Liu Q, Zhou YH, Yang ZQ. The cytokine storm of severe influenza and development of immunomodulatory therapy. Cell Mol Immunol (2016) 13(1):3–10.10.1038/cmi.2015.7426189369
7. Yang Y, Tang H. Aberrant coagulation causes a hyper-inflammatory response in severe influenza pneumonia. Cell Mol Immunol (2016) 13(4):432–42.10.1038/cmi.2016.127041635
8. To KK, Hung IF, Li IW, Lee KL, Koo CK, Yan WW, et al. Delayed clearance of viral load and marked cytokine activation in severe cases of pandemic H1N1 2009 influenza virus infection. Clin Infect Dis (2010) 50(6):850–9.10.1086/65058120136415
9. Song X, He X, Li X, Qian Y. The roles and functional mechanisms of interleukin-17 family cytokines in mucosal immunity. Cell Mol Immunol (2016) 13(4):418–31.10.1038/cmi.2015.10527018218
10. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol (2007) 25:821–52.10.1146/annurev.immunol.25.022106.14155717201677
11. Xu S, Cao X. Interleukin-17 and its expanding biological functions. Cell Mol Immunol (2010) 7(3):164–74.10.1038/cmi.2010.2120383173
12. Li C, Yang P, Sun Y, Li T, Wang C, Wang Z, et al. IL-17 response mediates acute lung injury induced by the 2009 pandemic influenza A (H1N1) virus. Cell Res (2012) 22(3):528–38.10.1038/cr.2011.16522025253
13. Crowe CR, Chen K, Pociask DA, Alcorn JF, Krivich C, Enelow RI, et al. Critical role of IL-17RA in immunopathology of influenza infection. J Immunol (2009) 183(8):5301–10.10.4049/jimmunol.090099519783685
14. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity (2009) 31(2):331–41.10.1016/j.immuni.2009.08.00119682929
15. Rachitskaya AV, Hansen AM, Horai R, Li Z, Villasmil R, Luger D, et al. Cutting edge: NKT cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J Immunol (2008) 180(8):5167–71.10.4049/jimmunol.180.8.516718390697
16. Hamada H, Garcia-Hernandez Mde L, Reome JB, Misra SK, Strutt TM, McKinstry KK, et al. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J Immunol (2009) 182(6):3469–81.10.4049/jimmunol.080181419265125
17. Kuang DM, Peng C, Zhao Q, Wu Y, Zhu LY, Wang J, et al. Tumor-activated monocytes promote expansion of IL-17-producing CD8+ T cells in hepatocellular carcinoma patients. J Immunol (2010) 185(3):1544–9.10.4049/jimmunol.090409420581151
18. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med (2007) 13(2):139–45.10.1038/nm155117290272
19. Wu D, Wu P, Qiu F, Wei Q, Huang J. Human gammadelta T-cell subsets and their involvement in tumor immunity. Cell Mol Immunol (2017) 14(3):245–53.10.1038/cmi.2016.55
20. Patil RS, Bhat SA, Dar AA, Chiplunkar SV. The Jekyll and Hyde story of IL17-producing gammadelta T cells. Front Immunol (2015) 6:37.10.3389/fimmu.2015.00037
21. Lombes A, Durand A, Charvet C, Riviere M, Bonilla N, Auffray C, et al. Adaptive immune-like gamma/delta T lymphocytes share many common features with their alpha/beta T cell counterparts. J Immunol (2015) 195(4):1449–58.10.4049/jimmunol.1500375
22. Lockhart E, Green AM, Flynn JL. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol (2006) 177(7):4662–9.10.4049/jimmunol.177.7.466216982905
23. Hamada S, Umemura M, Shiono T, Tanaka K, Yahagi A, Begum MD, et al. IL-17A produced by gammadelta T cells plays a critical role in innate immunity against Listeria monocytogenes infection in the liver. J Immunol (2008) 181(5):3456–63.10.4049/jimmunol.181.5.345618714018
24. Papotto PH, Ribot JC, Silva-Santos B. IL-17+ gammadelta T cells as kick-starters of inflammation. Nat Immunol (2017) 18(6):604–11.10.1038/ni.3726
25. Munoz-Ruiz M, Sumaria N, Pennington DJ, Silva-Santos B. Thymic determinants of gammadelta T cell differentiation. Trends Immunol (2017) 38(5):336–44.10.1016/j.it.2017.01.007
26. Khairallah C, Dechanet-Merville J, Capone M. gammadelta T cell-mediated immunity to cytomegalovirus infection. Front Immunol (2017) 8:105.10.3389/fimmu.2017.00105
27. Qin G, Liu Y, Zheng J, Xiang Z, Ng IH, Malik Peiris JS, et al. Phenotypic and functional characterization of human gammadelta T-cell subsets in response to influenza A viruses. J Infect Dis (2012) 205(11):1646–53.10.1093/infdis/jis253
28. Li H, Xiang Z, Feng T, Li J, Liu Y, Fan Y, et al. Human Vgamma9Vdelta2-T cells efficiently kill influenza virus-infected lung alveolar epithelial cells. Cell Mol Immunol (2013) 10(2):159–64.10.1038/cmi.2012.70
29. Tu W, Zheng J, Liu Y, Sia SF, Liu M, Qin G, et al. The aminobisphosphonate pamidronate controls influenza pathogenesis by expanding a gammadelta T cell population in humanized mice. J Exp Med (2011) 208(7):1511–22.10.1084/jem.2011022621708931
30. Qin G, Mao H, Zheng J, Sia SF, Liu Y, Chan PL, et al. Phosphoantigen-expanded human gammadelta T cells display potent cytotoxicity against monocyte-derived macrophages infected with human and avian influenza viruses. J Infect Dis (2009) 200(6):858–65.10.1086/60541319656068
31. Okamoto Yoshida Y, Umemura M, Yahagi A, O’Brien RL, Ikuta K, Kishihara K, et al. Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung. J Immunol (2010) 184(8):4414–22.10.4049/jimmunol.0903332
32. Roark CL, French JD, Taylor MA, Bendele AM, Born WK, O’Brien RL. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gammadelta T cells. J Immunol (2007) 179(8):5576–83.10.4049/jimmunol.179.8.557617911645
33. Murdoch JR, Lloyd CM. Resolution of allergic airway inflammation and airway hyperreactivity is mediated by IL-17-producing {gamma}{delta}T cells. Am J Respir Crit Care Med (2010) 182(4):464–76.10.1164/rccm.200911-1775OC20413629
34. Murphy AG, O’Keeffe KM, Lalor SJ, Maher BM, Mills KH, McLoughlin RM. Staphylococcus aureus infection of mice expands a population of memory gammadelta T cells that are protective against subsequent infection. J Immunol (2014) 192(8):3697–708.10.4049/jimmunol.1303420
35. Huber SA, Graveline D, Newell MK, Born WK, O’Brien RL. V gamma 1+ T cells suppress and V gamma 4+ T cells promote susceptibility to coxsackievirus B3-induced myocarditis in mice. J Immunol (2000) 165(8):4174–81.10.4049/jimmunol.165.8.417411035049
36. Xu L, Bao L, Zhou J, Wang D, Deng W, Lv Q, et al. Genomic polymorphism of the pandemic A (H1N1) influenza viruses correlates with viral replication, virulence, and pathogenicity in vitro and in vivo. PLoS One (2011) 6(6):e20698.10.1371/journal.pone.002069821698272
37. van der Heyde HC, Elloso MM, Chang WL, Kaplan M, Manning DD, Weidanz WP. Gamma delta T cells function in cell-mediated immunity to acute blood-stage Plasmodium chabaudi adami malaria. J Immunol (1995) 154(8):3985–90.7706737
38. Hiromatsu K, Yoshikai Y, Matsuzaki G, Ohga S, Muramori K, Matsumoto K, et al. A protective role of gamma/delta T cells in primary infection with Listeria monocytogenes in mice. J Exp Med (1992) 175(1):49–56.10.1084/jem.175.1.491530961
39. Lu X, Ding ZC, Cao Y, Liu C, Habtetsion T, Yu M, et al. Alkylating agent melphalan augments the efficacy of adoptive immunotherapy using tumor-specific CD4+ T cells. J Immunol (2015) 194(4):2011–21.10.4049/jimmunol.140189425560408
40. Liu B, Zhang X, Deng W, Liu J, Li H, Wen M, et al. Severe influenza A(H1N1)pdm09 infection induces thymic atrophy through activating innate CD8(+)CD44(hi) T cells by upregulating IFN-gamma. Cell Death Dis (2014) 5:e1440.10.1038/cddis.2014.323
41. Kisielow J, Kopf M. The origin and fate of gamma delta T cell subsets. Curr Opin Immunol (2013) 25(2):181–8.10.1016/j.coi.2013.03.002
42. Born WK, Yin Z, Hahn YS, Sun D, O’Brien RL. Analysis of gamma delta T cell functions in the mouse. J Immunol (2010) 184(8):4055–61.10.4049/jimmunol.090367920368285
43. Qin G, Liu Y, Zheng J, Ng IH, Xiang Z, Lam KT, et al. Type 1 responses of human Vgamma9Vdelta2 T cells to influenza A viruses. J Virol (2011) 85(19):10109–16.10.1128/JVI.05341-11
44. Chien YH, Meyer C, Bonneville M. gammadelta T cells: first line of defense and beyond. Annu Rev Immunol (2014) 32:121–55.10.1146/annurev-immunol-032713-120216
45. Schmolka N, Serre K, Grosso AR, Rei M, Pennington DJ, Gomes AQ, et al. Epigenetic and transcriptional signatures of stable versus plastic differentiation of proinflammatory gammadelta T cell subsets. Nat Immunol (2013) 14(10):1093–100.10.1038/ni.2702
46. Rincon-Orozco B, Kunzmann V, Wrobel P, Kabelitz D, Steinle A, Herrmann T. Activation of V gamma 9V delta 2 T cells by NKG2D. J Immunol (2005) 175(4):2144–51.10.4049/jimmunol.175.4.214416081780
47. Guerin C, Reignier J, Richard JC, Beuret P, Gacouin A, Boulain T, et al. Prone positioning in severe acute respiratory distress syndrome. N Engl J Med (2013) 368(23):2159–68.10.1056/NEJMoa121410323688302
48. Teijaro JR, Walsh KB, Cahalan S, Fremgen DM, Roberts E, Scott F, et al. Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell (2011) 146(6):980–91.10.1016/j.cell.2011.08.01521925319
49. Hayday AC. [gamma][delta] cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol (2000) 18:975–1026.10.1146/annurev.immunol.18.1.97510837080
50. Ravens S, Schultze-Florey C, Raha S, Sandrock I, Drenker M, Oberdorfer L, et al. Human gammadelta T cells are quickly reconstituted after stem-cell transplantation and show adaptive clonal expansion in response to viral infection. Nat Immunol (2017) 18(4):393–401.10.1038/ni.3686
51. Meng Z, Wang J, Yuan Y, Cao G, Fan S, Gao C, et al. gammadelta T cells are indispensable for interleukin-23-mediated protection against concanavalin A-induced hepatitis in hepatitis B virus transgenic mice. Immunology (2017) 151(1):43–55.10.1111/imm.12712
52. Tuero I, Venzon D, Robert-Guroff M. Mucosal and systemic gammadelta+ T cells associated with control of simian immunodeficiency virus infection. J Immunol (2016) 197(12):4686–95.10.4049/jimmunol.1600579
53. Zheng J, Liu Y, Lau YL, Tu W. gammadelta-T cells: an unpolished sword in human anti-infection immunity. Cell Mol Immunol (2013) 10(1):50–7.10.1038/cmi.2012.43
54. Glatzel A, Wesch D, Schiemann F, Brandt E, Janssen O, Kabelitz D. Patterns of chemokine receptor expression on peripheral blood gamma delta T lymphocytes: strong expression of CCR5 is a selective feature of V delta 2/V gamma 9 gamma delta T cells. J Immunol (2002) 168(10):4920–9.10.4049/jimmunol.168.10.492011994442
55. Costa MF, de Negreiros CB, Bornstein VU, Valente RH, Mengel J, Henriques M, et al. Murine IL-17+ Vgamma4 T lymphocytes accumulate in the lungs and play a protective role during severe sepsis. BMC Immunol (2015) 16:36.10.1186/s12865-015-0098-8
56. Hayday AC. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity (2009) 31(2):184–96.10.1016/j.immuni.2009.08.00619699170
57. Iwakura Y, Ishigame H, Saijo S, Nakae S. Functional specialization of interleukin-17 family members. Immunity (2011) 34(2):149–62.10.1016/j.immuni.2011.02.01221349428
58. Korn T, Petermann F. Development and function of interleukin 17-producing gammadelta T cells. Ann N Y Acad Sci (2012) 1247:34–45.10.1111/j.1749-6632.2011.06355.x
59. Huang J, Meng S, Hong S, Lin X, Jin W, Dong C. IL-17C is required for lethal inflammation during systemic fungal infection. Cell Mol Immunol (2016) 13(4):474–83.10.1038/cmi.2015.5626166766
60. Wang J, Li F, Wei H, Lian ZX, Sun R, Tian Z. Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation. J Exp Med (2014) 211(12):2397–410.10.1084/jem.2014062525366965
61. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity (2009) 31(2):321–30.10.1016/j.immuni.2009.06.02019682928
62. Ma Y, Aymeric L, Locher C, Mattarollo SR, Delahaye NF, Pereira P, et al. Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. J Exp Med (2011) 208(3):491–503.10.1084/jem.2010026921383056
63. He W, Hao J, Dong S, Gao Y, Tao J, Chi H, et al. Naturally activated V gamma 4 gamma delta T cells play a protective role in tumor immunity through expression of eomesodermin. J Immunol (2010) 185(1):126–33.10.4049/jimmunol.090376720525896
64. Matsuzaki G, Yamada H, Kishihara K, Yoshikai Y, Nomoto K. Mechanism of murine Vgamma1+ gamma delta T cell-mediated innate immune response against Listeria monocytogenes infection. Eur J Immunol (2002) 32(4):928–35.10.1002/1521-4141(200204)32:4<928::AID-IMMU928>3.3.CO;2-911920558
65. Dong P, Zhang S, Cai M, Kang N, Hu Y, Cui L, et al. Global characterization of differential gene expression profiles in mouse Vgamma1+ and Vgamma4+ gammadelta T cells. PLoS One (2014) 9(11):e112964.10.1371/journal.pone.0112964
66. Alexander AA, Maniar A, Cummings JS, Hebbeler AM, Schulze DH, Gastman BR, et al. Isopentenyl pyrophosphate-activated CD56+ {gamma}{delta} T lymphocytes display potent antitumor activity toward human squamous cell carcinoma. Clin Cancer Res (2008) 14(13):4232–40.10.1158/1078-0432.CCR-07-491218594005
67. Wrobel P, Shojaei H, Schittek B, Gieseler F, Wollenberg B, Kalthoff H, et al. Lysis of a broad range of epithelial tumour cells by human gamma delta T cells: involvement of NKG2D ligands and T-cell receptor- versus NKG2D-dependent recognition. Scand J Immunol (2007) 66(2–3):320–8.10.1111/j.1365-3083.2007.01963.x17635809
68. Dalton JE, Howell G, Pearson J, Scott P, Carding SR. Fas-Fas ligand interactions are essential for the binding to and killing of activated macrophages by gamma delta T cells. J Immunol (2004) 173(6):3660–7.10.4049/jimmunol.173.6.366015356111
69. Peterman GM, Spencer C, Sperling AI, Bluestone JA. Role of gamma delta T cells in murine collagen-induced arthritis. J Immunol (1993) 151(11):6546–58.8245484
70. Nian H, Shao H, Zhang G, Born WK, O’Brien RL, Kaplan HJ, et al. Regulatory effect of gammadelta T cells on IL-17+ uveitogenic T cells. Invest Ophthalmol Vis Sci (2010) 51(9):4661–7.10.1167/iovs.09-504520375337