Human RORγt+CD34+ cells are lineage-specified progenitors of group 3 RORγt+ innate lymphoid cells

Immunity

Volumn 41, Issue 6, 2014, Pages 988-1000

  Montaldo, Elisa ^a,b   Teixeira Alves, Luiz Gustavo ^c   Glatzer, Timor ^c   Durek, Pawel ^c   Stervbo, Ulrik ^c   Hamann, Wiebke ^c   Babic, Marina ^c,d   Paclik, Daniela ^c   Stölzel, Katharina ^e   Gröne, Jörn ^e   Lozza, Laura ^f   Juelke, Kerstin ^c,e   Matzmohr, Nadine ^e   Loiacono, Fabrizio ^g   Petronelli, Francesca ^g   Huntington, Nicholas David ^h   Moretta, Lorenzo ^g   Mingari, Maria Cristina ^a,b   Romagnani, Chiara ^c  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c POTSDAM INSTITUTE FOR CLIMATE IMPACT RESEARCH PIK   (Germany)

^d UNIVERSITY OF RIJEKA   (Croatia)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^f MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^g G GASLINI INSTITUTE   (Italy)

^h UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; RETINOID RELATED ORPHAN RECEPTOR GAMMA;

ADULT; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; GENETICS; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE; LYMPHOCYTE; METABOLISM; MICROARRAY ANALYSIS; NATURAL KILLER CELL; PALATINE TONSIL; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADULT; ANTIGENS, CD34; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNITY, INNATE; INTERLEUKINS; INTESTINES; KILLER CELLS, NATURAL; LYMPHOCYTES; MICROARRAY ANALYSIS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; PALATINE TONSIL; SIGNAL TRANSDUCTION;

EID: 84918529869     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2014.11.010     Document Type: Article

References (54)

1. Ahn Y.O., Blazar B.R., Miller J.S., Verneris M.R. Lineage relationships of human interleukin-22-producing CD56+ RORγt+ innate lymphoid cells and conventional natural killer cells. Blood 2013, 121:2234-2243.
2. 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.
3. Brucklacher-Waldert V., Stuerner K., Kolster M., Wolthausen J., Tolosa E. Phenotypical and functional characterization of T helper 17 cells in multiple sclerosis. Brain 2009, 132:3329-3341.
4. Buonocore S., Ahern P.P., Uhlig H.H., Ivanov I.I., Littman D.R., Maloy K.J., Powrie F. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 2010, 464:1371-1375.
5. Carotta S., Pang S.H., Nutt S.L., Belz G.T. Identification of the earliest NK-cell precursor in the mouse BM. Blood 2011, 117:5449-5452.
6. Cella M., Fuchs A., Vermi W., Facchetti F., Otero K., Lennerz J.K.M., 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.
7. 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. USA 2010, 107:10961-10966.
8. Chang S.H., Reynolds J.M., Pappu B.P., Chen G., Martinez G.J., Dong C. Interleukin-17C promotes Th17 cell responses and autoimmune disease via interleukin-17 receptor E. Immunity 2011, 35:611-621.
9. Chappaz S., Gärtner C., Rodewald H.R., Finke D. Kit ligand and Il7 differentially regulate Peyer's patch and lymph node development. J.Immunol. 2010, 185:3514-3519.
10. Cherrier M., Eberl G. The development of LTi cells. Curr. Opin. Immunol. 2012, 24:178-183.
11. Cherrier M., Sawa S., Eberl G. Notch, Id2, and RORγt sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J.Exp. Med. 2012, 209:729-740.
12. Constantinides M.G., McDonald B.D., Verhoef P.A., Bendelac A. A committed precursor to innate lymphoid cells. Nature 2014, 508:397-401.
13. Crellin N.K., Trifari S., Kaplan C.D., Cupedo T., Spits H. Human NKp44+IL-22+ cells and LTi-like cells constitute a stable RORC+ lineage distinct from conventional natural killer cells. J.Exp. Med. 2010, 207:281-290.
14. Cupedo T., Crellin N.K., Papazian N., Rombouts E.J., Weijer K., Grogan J.L., Fibbe W.E., Cornelissen J.J., Spits H. Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat. Immunol. 2009, 10:66-74.
15. Eberl G., Littman D.R. Thymic origin of intestinal alphabeta Tcells revealed by fate mapping of RORgammat+ cells. Science 2004, 305:248-251.
16. Fathman J.W., Bhattacharya D., Inlay M.A., Seita J., Karsunky H., Weissman I.L. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood 2011, 118:5439-5447.
17. Freud A.G., Becknell B., Roychowdhury S., Mao H.C., Ferketich A.K., Nuovo G.J., Hughes T.L., Marburger T.B., Sung J., Baiocchi R.A., et al. A human CD34(+) subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity 2005, 22:295-304.
18. Freud A.G., Yokohama A., Becknell B., Lee M.T., Mao H.C., Ferketich A.K., Caligiuri M.A. Evidence for discrete stages of human natural killer cell differentiation invivo. J.Exp. Med. 2006, 203:1033-1043.
19. 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-γ-producing cells. Immunity 2013, 38:769-781.
20. Geremia A., Arancibia-Cárcamo C.V., Fleming M.P.P., Rust N., Singh B., Mortensen N.J., Travis S.P.L., Powrie F. IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J.Exp. Med. 2011, 208:1127-1133.
21. + innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44. Immunity 2013, 38:1223-1235.
22. Hoorweg K., Peters C.P., Cornelissen F., Aparicio-Domingo P., Papazian N., Kazemier G., Mjösberg J.M., Spits H., Cupedo T. Functional differences between human NKp44(-) and NKp44(+) RORC(+) innate lymphoid cells. Front. Immunol. 2012, 3:72.
23. Hughes T., Becknell B., McClory S., Briercheck E., Freud A.G., Zhang X., Mao H., Nuovo G., Yu J., Caligiuri M.A. Stage 3 immature human natural killer cells found in secondary lymphoid tissue constitutively and selectively express the TH 17 cytokine interleukin-22. Blood 2009, 113:4008-4010.
24. Hughes T., Becknell B., Freud A.G., McClory S., Briercheck E., Yu J., Mao C., Giovenzana C., Nuovo G., Wei L., et al. Interleukin-1beta selectively expands and sustains interleukin-22+ immature human natural killer cells in secondary lymphoid tissue. Immunity 2010, 32:803-814.
25. Hughes T., Briercheck E.L., Freud A.G., Trotta R., McClory S., Scoville S.D., Keller K., Deng Y., Cole J., Harrison N., et al. The transcription factor AHR prevents the differentiation of a stage 3 innate lymphoid cell subset to natural killer cells. Cell Rep. 2014, 8:150-162.
26. Kiss E.A., Vonarbourg C., Kopfmann S., Hobeika E., Finke D., Esser C., Diefenbach A. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 2011, 334:1561-1565.
27. Klose C.S., Kiss E.A., Schwierzeck V., Ebert K., Hoyler T., d'Hargues Y., Göppert N., Croxford A.L., Waisman A., Tanriver Y., Diefenbach A. A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 2013, 494:261-265.
28. Klose C.S., Flach M., Möhle L., Rogell L., Hoyler T., Ebert K., Fabiunke C., Pfeifer D., Sexl V., Fonseca-Pereira D., et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 2014, 157:340-356.
29. Lee J.S., Cella M., McDonald K.G., Garlanda C., Kennedy G.D., Nukaya M., Mantovani A., Kopan R., Bradfield C.A., Newberry R.D., Colonna M. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 2012, 13:144-151.
30. Luci C., Reynders A., Ivanov I.I., Cognet C., Chiche L., Chasson L., Hardwigsen J., Anguiano E., Banchereau J., Chaussabel D., et al. Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 2009, 10:75-82.
31. Mebius R.E., Miyamoto T., Christensen J., Domen J., Cupedo T., Weissman I.L., Akashi K. The fetal liver counterpart of adult common lymphoid progenitors gives rise to all lymphoid lineages, CD45+CD4+CD3- cells, as well as macrophages. J.Immunol. 2001, 166:6593-6601.
32. Miller J.S., Alley K.A., McGlave P. Differentiation of natural killer (NK) cells from human primitive marrow progenitors in a stroma-based long-term culture system: identification of a CD34+7+ NK progenitor. Blood 1994, 83:2594-2601.
33. Montaldo E., Vitale C., Cottalasso F., Conte R., Glatzer T., Ambrosini P., Moretta L., Mingari M.C. Human NK cells at early stages of differentiation produce CXCL8 and express CD161 molecule that functions as an activating receptor. Blood 2012, 119:3987-3996.
34. Possot C., Schmutz S., Chea S., Boucontet L., Louise A., Cumano A., Golub R. Notch signaling is necessary for adult, but not fetal, development of RORγt(+) innate lymphoid cells. Nat. Immunol. 2011, 12:949-958.
35. Qiu J., Heller J.J., Guo X., Chen Z.M., Fish K., Fu Y.X., Zhou L. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 2012, 36:92-104.
36. Ramesh R., Kozhaya L., McKevitt K., Djuretic I.M., Carlson T.J., Quintero M.A., McCauley J.L., Abreu M.T., Unutmaz D., Sundrud M.S. Pro-inflammatory human Th17 cells selectively express P-glycoprotein and are refractory to glucocorticoids. J.Exp. Med. 2014, 211:89-104.
37. Rankin L.C., Groom J.R., Chopin M., Herold M.J., Walker J.A., Mielke L.A., McKenzie A.N., Carotta S., Nutt S.L., Belz G.T. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat. Immunol. 2013, 14:389-395.
38. Rosmaraki E.E., Douagi I., Roth C., Colucci F., Cumano A., Di Santo J.P. Identification of committed NK cell progenitors in adult murine bone marrow. Eur. J. Immunol. 2001, 31:1900-1909.
39. 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.
40. Santarlasci V., Maggi L., Capone M., Querci V., Beltrame L., Cavalieri D., D'Aiuto E., Cimaz R., Nebbioso A., Liotta F., et al. Rarity of human T helper 17 cells is due to retinoic acid orphan receptor-dependent mechanisms that limit their expansion. Immunity 2012, 36:201-214.
41. Satoh-Takayama N., Vosshenrich C.A.J., 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.
42. 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.
43. Sawa S., Lochner M., Satoh-Takayama N., Dulauroy S., Bérard M., Kleinschek M., Cua D., Di Santo J.P., Eberl G. RORγt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 2011, 12:320-326.
44. Sciumé G., Hirahara K., Takahashi H., Laurence A., Villarino A.V., Singleton K.L., Spencer S.P., Wilhelm C., Poholek A.C., Vahedi G., et al. Distinct requirements for T-bet in gut innate lymphoid cells. J.Exp. Med. 2012, 209:2331-2338.
45. Sivori S., Vitale M., Morelli L., Sanseverino L., Augugliaro R., Bottino C., Moretta L., Moretta A. p46, a novel natural killer cell-specific surface molecule that mediates cell activation. J.Exp. Med. 1997, 186:1129-1136.
46. Spits H., Cupedo T. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 2012, 30:647-675.
47. Spits H., 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-a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013, 13:145-149.
48. Sun Z., Unutmaz D., Zou Y.R., Sunshine M.J., Pierani A., Brenner-Morton S., Mebius R.E., Littman D.R. Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 2000, 288:2369-2373.
49. Tachibana M., Tenno M., Tezuka C., Sugiyama M., Yoshida H., Taniuchi I. Runx1/Cbfβ2 complexes are required for lymphoid tissue inducer cell differentiation at two developmental stages. J.Immunol. 2011, 186:1450-1457.
50. Tang Q., Ahn Y.O., Southern P., Blazar B.R., Miller J.S., Verneris M.R. Development of IL-22-producing NK lineage cells from umbilical cord blood hematopoietic stem cells in the absence of secondary lymphoid tissue. Blood 2011, 117:4052-4055.
51. Toren A., Bielorai B., Jacob-Hirsch J., Fisher T., Kreiser D., Moran O., Zeligson S., Givol D., Yitzhaky A., Itskovitz-Eldor J., et al. CD133-positive hematopoietic stem cell "stemness" genes contain many genes mutated or abnormally expressed in leukemia. Stem Cells 2005, 23:1142-1153.
52. Veldhoen M., Hirota K., Christensen J., O'Garra A., Stockinger B. Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 Tcells. J.Exp. Med. 2009, 206:43-49.
53. Vitale M., Bottino C., Sivori S., Sanseverino L., Castriconi R., Marcenaro E., Augugliaro R., Moretta L., Moretta A. NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J.Exp. Med. 1998, 187:2065-2072.
54. Yoshida H., Kawamoto H., Santee S.M., Hashi H., Honda K., Nishikawa S., Ware C.F., Katsura Y., Nishikawa S.I. Expression of alpha(4)beta(7) integrin defines a distinct pathway of lymphoid progenitors committed to Tcells, fetal intestinal lymphotoxin producer, NK, and dendritic cells. J.Immunol. 2001, 167:2511-2521.