Transforming Growth Factor-β Signaling Guides the Differentiation of Innate Lymphoid Cells in Salivary Glands

Immunity

Volumn 44, Issue 5, 2016, Pages 1127-1139

  Cortez, Victor S ^a   Cervantes Barragan, Luisa ^a   Robinette, Michelle L ^a   Bando, Jennifer K ^a   Wang, Yaming ^a   Geiger, Theresa L ^b   Gilfillan, Susan ^a   Fuchs, Anja ^a   Vivier, Eric ^c   Sun, Joe C ^b   Cella, Marina ^a   Colonna, Marco ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

Development; Innate lymphoid cells; Salivary gland; Signaling; TGF ; Transcription factors

Indexed keywords

5' NUCLEOTIDASE; ALPHA1 INTEGRIN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; SMAD4 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EOMES; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; EOMES PROTEIN, MOUSE; LY ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; NCR1 PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; SMAD4 PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EOMES GENE; FEMALE; GENE; GENE DELETION; GENOME IMPRINTING; INTRACELLULAR SIGNALING; LYMPHOID CELL; MICROARRAY ANALYSIS; MICROENVIRONMENT; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALIVARY GLAND; TGFBR2 GENE; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; LYMPHOCYTE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIGENS, LY; CELL DIFFERENTIATION; CELLULAR MICROENVIRONMENT; GENE EXPRESSION PROFILING; IMMUNITY, INNATE; KILLER CELLS, NATURAL; LYMPHOCYTES; MAP KINASE KINASE 4; MICE; MICE, KNOCKOUT; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SALIVARY GLANDS; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; T-BOX DOMAIN PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84964828817     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.03.007     Document Type: Article

References (44)

1. Atarashi K., Tanoue T., Oshima K., Suda W., Nagano Y., Nishikawa H., Fukuda S., Saito T., Narushima S., Hase K., et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013, 500:232-236.
2. Constantinides M.G., McDonald B.D., Verhoef P.A., Bendelac A. A committed precursor to innate lymphoid cells. Nature 2014, 508:397-401.
3. Cortez V.S., Fuchs A., Cella M., Gilfillan S., Colonna M. Cutting edge: Salivary gland NK cells develop independently of Nfil3 in steady-state. J. Immunol. 2014, 192:4487-4491.
4. Curotto de Lafaille M.A., Lafaille J.J. CD4(+) regulatory T cells in autoimmunity and allergy. Curr. Opin. Immunol. 2002, 14:771-778.
5. Daussy C., Faure F., Mayol K., Viel S., Gasteiger G., Charrier E., Bienvenu J., Henry T., Debien E., Hasan U.A., et al. T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J. Exp. Med. 2014, 211:563-577.
6. Deaglio S., Robson S.C. Ectonucleotidases as regulators of purinergic signaling in thrombosis, inflammation, and immunity. Adv. Pharmacol. 2011, 61:301-332.
7. Diefenbach A., Colonna M., Koyasu S. Development, differentiation, and diversity of innate lymphoid cells. Immunity 2014, 41:354-365.
8. Eberl G., Colonna M., Di Santo J.P., McKenzie A.N. Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science 2015, 348:aaa6566.
9. Ebihara T., Song C., Ryu S.H., Plougastel-Douglas B., Yang L., Levanon D., Groner Y., Bern M.D., Stappenbeck T.S., Colonna M., et al. Runx3 specifies lineage commitment of innate lymphoid cells. Nat. Immunol. 2015, 16:1124-1133.
10. 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.
11. 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.
12. Glimcher L.H., Townsend M.J., Sullivan B.M., Lord G.M. Recent developments in the transcriptional regulation of cytolytic effector cells. Nat. Rev. Immunol. 2004, 4:900-911.
13. Gordon S.M., Chaix J., Rupp L.J., Wu J., Madera S., Sun J.C., Lindsten T., Reiner S.L. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 2012, 36:55-67.
14. Hu Y., Lee Y.T., Kaech S.M., Garvy B., Cauley L.S. Smad4 promotes differentiation of effector and circulating memory CD8 T cells but is dispensable for tissue-resident memory CD8 T cells. J. Immunol. 2015, 194:2407-2414.
15. Huser C.A., Pringle M.A., Heath V.J., Bell A.K., Kendrick H., Smalley M.J., Crighton D., Ryan K.M., Gusterson B.A., Stein T. TSC-22D1 isoforms have opposing roles in mammary epithelial cell survival. Cell Death Differ. 2010, 17:304-315.
16. Ichiyama K., Sekiya T., Inoue N., Tamiya T., Kashiwagi I., Kimura A., Morita R., Muto G., Shichita T., Takahashi R., Yoshimura A. Transcription factor Smad-independent T helper 17 cell induction by transforming-growth factor-β is mediated by suppression of eomesodermin. Immunity 2011, 34:741-754.
17. Jaskoll T., Melnick M. Submandibular gland morphogenesis: stage-specific expression of TGF-alpha/EGF, IGF, TGF-beta, TNF, and IL-6 signal transduction in normal embryonic mice and the phenotypic effects of TGF-beta2, TGF-beta3, and EGF-r null mutations. Anat. Rec. 1999, 256:252-268.
18. 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.
19. Larsen M., Yamada K.M., Musselmann K. Systems analysis of salivary gland development and disease. Wiley Interdiscip. Rev. Syst. Biol. Med. 2010, 2:670-682.
20. Lourenço S.V., Uyekita S.H., Lima D.M., Soares F.A. Developing human minor salivary glands: morphological parallel relation between the expression of TGF-beta isoforms and cytoskeletal markers of glandular maturation. Virchows Arch. 2008, 452:427-434.
21. Mackay L.K., Rahimpour A., Ma J.Z., Collins N., Stock A.T., Hafon M.L., Vega-Ramos J., Lauzurica P., Mueller S.N., Stefanovic T., et al. The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat. Immunol. 2013, 14:1294-1301.
22. Marcoe J.P., Lim J.R., Schaubert K.L., Fodil-Cornu N., Matka M., McCubbrey A.L., Farr A.R., Vidal S.M., Laouar Y. TGF-β is responsible for NK cell immaturity during ontogeny and increased susceptibility to infection during mouse infancy. Nat. Immunol. 2012, 13:843-850.
23. Martin M., Lefaix J., Delanian S. TGF-beta1 and radiation fibrosis: a master switch and a specific therapeutic target?. Int. J. Radiat. Oncol. Biol. Phys. 2000, 47:277-290.
24. Massagué J. TGFβ signalling in context. Nat. Rev. Mol. Cell Biol. 2012, 13:616-630.
25. Meharra E.J., Schön M., Hassett D., Parker C., Havran W., Gardner H. Reduced gut intraepithelial lymphocytes in VLA1 null mice. Cell. Immunol. 2000, 201:1-5.
26. Mueller S.N., Mackay L.K. Tissue-resident memory T cells: local specialists in immune defence. Nat. Rev. Immunol. 2016, 16:79-89.
27. Narni-Mancinelli E., Chaix J., Fenis A., Kerdiles Y.M., Yessaad N., Reynders A., Gregoire C., Luche H., Ugolini S., Tomasello E., et al. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA 2011, 108:18324-18329.
28. Peng H., Jiang X., Chen Y., Sojka D.K., Wei H., Gao X., Sun R., Yokoyama W.M., Tian Z. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 2013, 123:1444-1456.
29. Rijal S., Fleming S., Cummings N., Rynkiewicz N.K., Ooms L.M., Nguyen N.Y., Teh T.C., Avery S., McManus J.F., Papenfuss A.T., et al. Inositol polyphosphate 4-phosphatase II (INPP4B) is associated with chemoresistance and poor outcome in AML. Blood 2015, 125:2815-2824.
30. Robinette M.L., Fuchs A., Cortez V.S., Lee J.S., Wang Y., Durum S.K., Gilfillan S., Colonna M. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 2015, 16:306-317. Immunological Genome Consortium.
31. Robinson P.W., Green S.J., Carter C., Coadwell J., Kilshaw P.J. Studies on transcriptional regulation of the mucosal T-cell integrin alphaEbeta7 (CD103). Immunology 2001, 103:146-154.
32. Schenkel J.M., Masopust D. Tissue-resident memory T cells. Immunity 2014, 41:886-897.
33. Schuster I.S., Wikstrom M.E., Brizard G., Coudert J.D., Estcourt M.J., Manzur M., O'Reilly L.A., Smyth M.J., Trapani J.A., Hill G.R., et al. TRAIL+ NK cells control CD4+ T cell responses during chronic viral infection to limit autoimmunity. Immunity 2014, 41:646-656.
34. Seillet C., Huntington N.D., Gangatirkar P., Axelsson E., Minnich M., Brady H.J., Busslinger M., Smyth M.J., Belz G.T., Carotta S. Differential requirement for Nfil3 during NK cell development. J. Immunol. 2014, 192:2667-2676.
35. Shiow L.R., Rosen D.B., Brdicková N., Xu Y., An J., Lanier L.L., Cyster J.G., Matloubian M. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 2006, 440:540-544.
36. Skon C.N., Lee J.Y., Anderson K.G., Masopust D., Hogquist K.A., Jameson S.C. Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat. Immunol. 2013, 14:1285-1293.
37. 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.
38. Tessmer M.S., Reilly E.C., Brossay L. Salivary gland NK cells are phenotypically and functionally unique. PLoS Pathog. 2011, 7:e1001254.
39. Tindemans I., Serafini N., Di Santo J.P., Hendriks R.W. GATA-3 function in innate and adaptive immunity. Immunity 2014, 41:191-206.
40. Xu W., Domingues R.G., Fonseca-Pereira D., Ferreira M., Ribeiro H., Lopez-Lastra S., Motomura Y., Moreira-Santos L., Bihl F., Braud V., et al. NFIL3 orchestrates the emergence of common helper innate lymphoid cell precursors. Cell Rep. 2015, 10:2043-2054.
41. Yagi R., Zhong C., Northrup D.L., Yu F., Bouladoux N., Spencer S., Hu G., Barron L., Sharma S., Nakayama T., et al. The transcription factor GATA3 is critical for the development of all IL-7Rα-expressing innate lymphoid cells. Immunity 2014, 40:378-388.
42. Yu X., Wang Y., Deng M., Li Y., Ruhn K.A., Zhang C.C., Hooper L.V. The basic leucine zipper transcription factor NFIL3 directs the development of a common innate lymphoid cell precursor. eLife 2014, 3:3.
43. Zhang Y.E. Non-Smad pathways in TGF-beta signaling. Cell Res. 2009, 19:128-139.
44. Zhang N., Bevan M.J. Transforming growth factor-β signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity 2013, 39:687-696.