Regulation of the adaptive immune system by innate lymphoid cells

Current Opinion in Immunology

Volumn 27, Issue 1, 2014, Pages 75-82

  Hepworth, Matthew R ^a   Sonnenberg, Gregory F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; GROUP 1 INNATE LYMPHOID CELL; GROUP 2 INNATE LYMPHOID CELL; GROUP 3 INNATE LYMPHOID CELL; HUMAN; IMMUNOMODULATION; IMMUNOREGULATION; INNATE IMMUNITY; LYMPHOCYTE; LYMPHOID TISSUE; NONHUMAN; REVIEW;

ADAPTIVE IMMUNITY; ANIMALS; HUMANS; IMMUNITY, INNATE; LYMPHOCYTES; LYMPHOID TISSUE;

EID: 84896804302     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2014.01.013     Document Type: Review

References (71)

1. Sonnenberg G.F., Artis D. Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease. Immunity 2012, 37:601-610.
2. Spits H., Di Santo J.P. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat Immunol 2011, 12:21-27.
3. Spits H., Artis D., Colonna M., Diefenbach A., Di Santo J.P., Eberl G., Koyasu S., Locksley R.M., McKenzie A.N., Mebius R.E., et al. Innate lymphoid cells-a proposal for uniform nomenclature. Nat Rev Immunol 2013, 13:145-149.
4. Sonnenberg G.F., Mjosberg J., Spits H., Artis D. SnapShot: innate lymphoid cells. Immunity 2013, 39. 622-622, e621.
5. Satoh-Takayama N., Lesjean-Pottier S., Vieira P., Sawa S., Eberl G., Vosshenrich C.A., Di Santo J.P. IL-7 and IL-15 independently program the differentiation of intestinal CD3-NKp46+ cell subsets from Id2-dependent precursors. J Exp Med 2010, 207:273-280.
6. Mielke L.A., Groom J.R., Rankin L.C., Seillet C., Masson F., Putoczki T., Belz G.T. TCF-1 controls ILC2 and NKp46+RORgammat+ innate lymphocyte differentiation and protection in intestinal inflammation. J Immunol 2013, 191:4383-4391.
7. Yang Q., Monticelli L.A., Saenz S.A., Chi A.W., Sonnenberg G.F., Tang J., De Obaldia M.E., Bailis W., Bryson J.L., Toscano K., et al. T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity 2013, 38:694-704.
8. Crellin N.K., Trifari S., Kaplan C.D., Satoh-Takayama N., Di Santo J.P., Spits H. Regulation of cytokine secretion in human CD127(+) LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 2010, 33:752-764.
9. Moro K., Yamada T., Tanabe M., Takeuchi T., Ikawa T., Kawamoto H., Furusawa J., Ohtani M., Fujii H., Koyasu S. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010, 463:540-544.
10. Bernink J.H., Peters C.P., Munneke M., Te Velde A.A., Meijer S.L., Weijer K., Hreggvidsdottir H.S., Heinsbroek S.E., Legrand N., Buskens C.J., et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol 2013, 14:221-229.
11. Fuchs A., Vermi W., Lee J.S., Lonardi S., Gilfillan S., Newberry R.D., Cella M., Colonna M. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-gamma-producing cells. Immunity 2013, 38:769-781.
12. Hoyler T., Klose C.S., Souabni A., Turqueti-Neves A., Pfeifer D., Rawlins E.L., Voehringer D., Busslinger M., Diefenbach A. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 2012, 37:634-648.
13. Neill D.R., Wong S.H., Bellosi A., Flynn R.J., Daly M., Langford T.K., Bucks C., Kane C.M., Fallon P.G., Pannell R., et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010, 464:1367-1370.
14. Price A.E., Liang H.E., Sullivan B.M., Reinhardt R.L., Eisley C.J., Erle D.J., Locksley R.M. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci U S A 2010, 107:11489-11494.
15. Sawa S., Cherrier M., Lochner M., Satoh-Takayama N., Fehling H.J., Langa F., Di Santo J.P., Eberl G. Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 2010, 330:665-669.
16. Sawa S., Lochner M., Satoh-Takayama N., Dulauroy S., Berard M., Kleinschek M., Cua D., Di Santo J.P., Eberl G. RORgammat+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol 2011, 12:320-326.
17. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., Sawa S., Lochner M., Rattis F., Mention J.J., Thiam K., Cerf-Bensussan N., Mandelboim O., et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 2008, 29:958-970.
18. Sonnenberg G.F., Monticelli L.A., Elloso M.M., Fouser L.A., Artis D. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 2011, 34:122-134.
19. Sonnenberg G.F., Monticelli L.A., Alenghat T., Fung T.C., Hutnick N.A., Kunisawa J., Shibata N., Grunberg S., Sinha R., Zahm A.M., et al. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 2012, 336:1321-1325.
20. Aujla S.J., Chan Y.R., Zheng M., Fei M., Askew D.J., Pociask D.A., Reinhart T.A., McAllister F., Edeal J., Gaus K., et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 2008, 14:275-281.
21. Cella M., Fuchs A., Vermi W., Facchetti F., Otero K., Lennerz J.K., Doherty J.M., Mills J.C., Colonna M. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009, 457:722-725.
22. Sonnenberg G.F., Fouser L.A., Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 2011, 12:383-390.
23. Basu R., O'Quinn D.B., Silberger D.J., Schoeb T.R., Fouser L., Ouyang W., Hatton R.D., Weaver C.T. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 2012, 37:1061-1075.
24. Klose C.S., Kiss E.A., Schwierzeck V., Ebert K., Hoyler T., d'Hargues Y., Goppert N., Croxford A.L., Waisman A., Tanriver Y., et al. A T-bet gradient controls the fate and function of CCR6-RORgammat+ innate lymphoid cells. Nature 2013, 494:261-265.
25. Sanos S.L., Bui V.L., Mortha A., Oberle K., Heners C., Johner C., Diefenbach A. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol 2009, 10:83-91.
26. Mebius R.E., Rennert P., Weissman I.L. Developing lymph nodes collect CD4+CD3- LTbeta+ cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 1997, 7:493-504.
27. Eberl G., Marmon S., Sunshine M.J., Rennert P.D., Choi Y., Littman D.R. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat Immunol 2004, 5:64-73.
28. van de Pavert S.A., Mebius R.E. New insights into the development of lymphoid tissues. Nat Rev Immunol 2010, 10:664-674.
29. White A., Carragher D., Parnell S., Msaki A., Perkins N., Lane P., Jenkinson E., Anderson G., Caamano J.H. Lymphotoxin a-dependent and -independent signals regulate stromal organizer cell homeostasis during lymph node organogenesis. Blood 2007, 110:1950-1959.
30. Vondenhoff M.F., Greuter M., Goverse G., Elewaut D., Dewint P., Ware C.F., Hoorweg K., Kraal G., Mebius R.E. LTbetaR signaling induces cytokine expression and up-regulates lymphangiogenic factors in lymph node anlagen. J Immunol 2009, 182:5439-5445.
31. Rennert P.D., James D., Mackay F., Browning J.L., Hochman P.S. Lymph node genesis is induced by signaling through the lymphotoxin beta receptor. Immunity 1998, 9:71-79.
32. Kim D., Mebius R.E., MacMicking J.D., Jung S., Cupedo T., Castellanos Y., Rho J., Wong B.R., Josien R., Kim N., et al. Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J Exp Med 2000, 192:1467-1478.
33. Kim M.Y., McConnell F.M., Gaspal F.M., White A., Glanville S.H., Bekiaris V., Walker L.S., Caamano J., Jenkinson E., Anderson G., et al. Function of CD4+CD3- cells in relation to B- and T-zone stroma in spleen. Blood 2007, 109:1602-1610.
34. Bouskra D., Brezillon C., Berard M., Werts C., Varona R., Boneca I.G., Eberl G. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008, 456:507-510.
35. Eberl G. Inducible lymphoid tissues in the adult gut: recapitulation of a fetal developmental pathway?. Nat Rev Immunol 2005, 5:413-420.
36. Tsuji M., Suzuki K., Kitamura H., Maruya M., Kinoshita K., Ivanov I.I., Itoh K., Littman D.R., Fagarasan S. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 2008, 29:261-271.
37. Macpherson A.J. IgA adaptation to the presence of commensal bacteria in the intestine. Curr Top Microbiol Immunol 2006, 308:117-136.
38. Suzuki K., Fagarasan S. How host-bacterial interactions lead to IgA synthesis in the gut. Trends Immunol 2008, 29:523-531.
39. Tsuji M., Suzuki K., Kinoshita K., Fagarasan S. Dynamic interactions between bacteria and immune cells leading to intestinal IgA synthesis. Semin Immunol 2008, 20:59-66.
40. Kruglov A.A., Grivennikov S.I., Kuprash D.V., Winsauer C., Prepens S., Seleznik G.M., Eberl G., Littman D.R., Heikenwalder M., Tumanov A.V., et al. Nonredundant function of soluble LTalpha3 produced by innate lymphoid cells in intestinal homeostasis. Science 2013, 342:1243-1246.
41. Ota N., Wong K., Valdez P.A., Zheng Y., Crellin N.K., Diehl L., Ouyang W. IL-22 bridges the lymphotoxin pathway with the maintenance of colonic lymphoid structures during infection with Citrobacter rodentium. Nat Immunol 2011, 12:941-948.
42. Scandella E., Bolinger B., Lattmann E., Miller S., Favre S., Littman D.R., Finke D., Luther S.A., Junt T., Ludewig B. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat Immunol 2008, 9:667-675.
43. Gaboriau-Routhiau V., Rakotobe S., Lecuyer E., Mulder I., Lan A., Bridonneau C., Rochet V., Pisi A., De Paepe M., Brandi G., et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009, 31:677-689.
44. Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., Wei D., Goldfarb K.C., Santee C.A., Lynch S.V., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
45. Qiu J., Guo X., Chen Z.M., He L., Sonnenberg G.F., Artis D., Fu Y.X., Zhou L. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 2013, 39:386-399.
46. Cella M., Otero K., Colonna M. Expansion of human NK-22 cells with IL-7, IL-2, and IL-1beta reveals intrinsic functional plasticity. Proc Natl Acad Sci U S A 2010, 107:10961-10966.
47. Kim M.Y., Rossi S., Withers D., McConnell F., Toellner K.M., Gaspal F., Jenkinson E., Anderson G., Lane P.J. Heterogeneity of lymphoid tissue inducer cell populations present in embryonic and adult mouse lymphoid tissues. Immunology 2008, 124:166-174.
48. Withers D.R., Gaspal F.M., Mackley E.C., Marriott C.L., Ross E.A., Desanti G.E., Roberts N.A., White A.J., Flores-Langarica A., McConnell F.M., et al. Cutting edge: lymphoid tissue inducer cells maintain memory CD4 T cells within secondary lymphoid tissue. J Immunol 2012, 189:2094-2098.
49. Kim M.Y., Anderson G., White A., Jenkinson E., Arlt W., Martensson I.L., Erlandsson L., Lane P.J. OX40 ligand and CD30 ligand are expressed on adult but not neonatal CD4+CD3- inducer cells: evidence that IL-7 signals regulate CD30 ligand but not OX40 ligand expression. J Immunol 2005, 174:6686-6691.
50. Gaspal F.M., Kim M.Y., McConnell F.M., Raykundalia C., Bekiaris V., Lane P.J. Mice deficient in OX40 and CD30 signals lack memory antibody responses because of deficient CD4 T cell memory. J Immunol 2005, 174:3891-3896.
51. Kim M.Y., Gaspal F.M., Wiggett H.E., McConnell F.M., Gulbranson-Judge A., Raykundalia C., Walker L.S., Goodall M.D., Lane P.J. CD4(+)CD3(-) accessory cells costimulate primed CD4 T cells through OX40 and CD30 at sites where T cells collaborate with B cells. Immunity 2003, 18:643-654.
52. Withers D.R., Jaensson E., Gaspal F., McConnell F.M., Eksteen B., Anderson G., Agace W.W., Lane P.J. The survival of memory CD4+ T cells within the gut lamina propria requires OX40 and CD30 signals. J Immunol 2009, 183:5079-5084.
53. Hepworth M.R., Monticelli L.A., Fung T.C., Ziegler C.G., Grunberg S., Sinha R., Mantegazza A.R., Ma H.L., Crawford A., Angelosanto J.M., et al. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 2013, 498:113-117.
54. Korn L.L., Thomas H.H., Hubbeling H.G., Spencer S.P., Sinha R., Simkins H.M.A., Salzman N.H., Bushman F.D., Laufer T.M. Conventional CD4+ T cells regulate IL-22-producing intestinal innate lymphoid cells. Mucosal Immunol 2014, 10.1038/mi.2013.121.
55. Mabbott N.A., Donaldson D.S., Ohno H., Williams I.R., Mahajan A. Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol 2013, 6:666-677.
56. Gray E.E., Friend S., Suzuki K., Phan T.G., Cyster J.G. Subcapsular sinus macrophage fragmentation and CD169+ bleb acquisition by closely associated IL-17-committed innate-like lymphocytes. PLoS ONE 2012, 7:e38258.
57. Monticelli L.A., Sonnenberg G.F., Abt M.C., Alenghat T., Ziegler C.G., Doering T.A., Angelosanto J.M., Laidlaw B.J., Yang C.Y., Sathaliyawala T., et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol 2011, 12:1045-1054.
58. Mirchandani A.S., Besnard A.-G., Yip E., Scott C., Bain C.C., Cerovic V., Salmond R.J., Liew F.Y. Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J. Immunol. 2014, 10.4049/jimmunol.1300974.
59. Kim B.S., Siracusa M.C., Saenz S.A., Noti M., Monticelli L.A., Sonnenberg G.F., Hepworth M.R., Van Voorhees A.S., Comeau M.R., Artis D. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci Transl Med 2013, 5:170ra116.
60. Narni-Mancinelli E., Jaeger B.N., Bernat C., Fenis A., Kung S., De Gassart A., Mahmood S., Gut M., Heath S.C., Estelle J., et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 2012, 335:344-348.
61. Ghadially H., Horani A., Glasner A., Elboim M., Gazit R., Shoseyov D., Mandelboim O. NKp46 regulates allergic responses. Eur J Immunol 2013.
62. Lu L., Ikizawa K., Hu D., Werneck M.B., Wucherpfennig K.W., Cantor H. Regulation of activated CD4+ T cells by NK cells via the Qa-1-NKG2A inhibitory pathway. Immunity 2007, 26:593-604.
63. Waggoner S.N., Cornberg M., Selin L.K., Welsh R.M. Natural killer cells act as rheostats modulating antiviral T cells. Nature 2011, 481:394-398.
64. Kim C.J., Nazli A., Rojas O.L., Chege D., Alidina Z., Huibner S., Mujib S., Benko E., Kovacs C., Shin L.Y., et al. A role for mucosal IL-22 production and Th22 cells in HIV-associated mucosal immunopathogenesis. Mucosal Immunol 2012, 5:670-680.
65. 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.
66. Klatt N.R., Estes J.D., Sun X., Ortiz A.M., Barber J.S., Harris L.D., Cervasi B., Yokomizo L.K., Pan L., Vinton C.L., et al. Loss of mucosal CD103+ DCs and IL-17+ and IL-22+ lymphocytes is associated with mucosal damage in SIV infection. Mucosal Immunol 2012, 5:646-657.
67. Geremia A., Arancibia-Carcamo C.V., Fleming M.P., Rust N., Singh B., Mortensen N.J., Travis S.P., Powrie F. IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J Exp Med 2011, 208:1127-1133.
68. Perry J.S., Han S., Xu Q., Herman M.L., Kennedy L.B., Csako G., Bielekova B. Inhibition of LTi cell development by CD25 blockade is associated with decreased intrathecal inflammation in multiple sclerosis. Sci Transl Med 2012, 4:145ra106.
69. Mjosberg J.M., Trifari S., Crellin N.K., Peters C.P., van Drunen C.M., Piet B., Fokkens W.J., Cupedo T., Spits H. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol 2011, 12:1055-1062.
70. Takayama T., Kamada N., Chinen H., Okamoto S., Kitazume M.T., Chang J., Matuzaki Y., Suzuki S., Sugita A., Koganei K., et al. Imbalance of NKp44(+)NKp46(-) and NKp44(-)NKp46(+) natural killer cells in the intestinal mucosa of patients with Crohn's disease. Gastroenterology 2010, 139:882-892. 892 e881-e883.
71. Ciccia F., Accardo-Palumbo A., Alessandro R., Rizzo A., Principe S., Peralta S., Raiata F., Giardina A., De Leo G., Triolo G. Interleukin-22 and interleukin-22-producing NKp44+ natural killer cells in subclinical gut inflammation in ankylosing spondylitis. Arthritis Rheum 2012, 64:1869-1878.