Interleukin-15-Dependent T-Cell-like Innate Intraepithelial Lymphocytes Develop in the Intestine and Transform into Lymphomas in Celiac Disease

Immunity

Volumn 45, Issue 3, 2016, Pages 610-625

  Ettersperger, Julien ^a,b   Montcuquet, Nicolas ^a,b   Malamut, Georgia ^a,b,c   Guegan, Nicolas ^a,b   Lopez Lastra, Silvia ^d,e   Gayraud, Ségolène ^a,b   Reimann, Christian ^b,e   Vidal, Elodie ^b   Cagnard, Nicolas ^b   Villarese, Patrick ^b   Andre Schmutz, Isabelle ^b,e   Gomes Domingues, Rita ^f   Godinho Silva, Cristina ^f   Veiga Fernandes, Henrique ^f   Lhermitte, Ludovic ^b   Asnafi, Vahid ^b   Macintyre, Elizabeth ^b   Cellier, Christophe ^a,b,c   Beldjord, Kheira ^b,g   Di Santo, James P ^d,e   Cerf Bensussan, Nadine ^a,b   Meresse, Bertrand ^a,b   more..

^a IMAGINE INSTITUTE   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^d INSTITUT PASTEUR   (France)

^e INSERM   (France)

^f INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^g UNIVERSITÉ PARIS DIDEROT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD34 ANTIGEN; GRANZYME B; INHIBITOR OF DIFFERENTIATION 2; INTERLEUKIN 15; JANUS KINASE 1; NOTCH1 RECEPTOR; STAT3 PROTEIN; GRANZYME;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELIAC DISEASE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GENE REARRANGEMENT; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTESTINE EPITHELIUM; INTESTINE LYMPHOMA; LYMPHOCYTE DIFFERENTIATION; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; SMALL INTESTINE; T LYMPHOCYTE; THYMUS; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; GENETIC TRANSCRIPTION; IMMUNOLOGY; INTESTINE; LYMPHOCYTE ACTIVATION; LYMPHOMA; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD3; CELIAC DISEASE; CELL DIFFERENTIATION; CELLS, CULTURED; GRANZYMES; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INTERLEUKIN-15; INTESTINES; LYMPHOCYTE ACTIVATION; LYMPHOMA; MICE; MICE, INBRED C57BL; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTE SUBSETS; TRANSCRIPTION, GENETIC;

EID: 84990890397     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.07.018     Document Type: Article

References (48)

1. Carnevalli, L.S., Scognamiglio, R., Cabezas-Wallscheid, N., Rahmig, S., Laurenti, E., Masuda, K., Jöckel, L., Kuck, A., Sujer, S., Polykratis, A., et al. Improved HSC reconstitution and protection from inflammatory stress and chemotherapy in mice lacking granzyme B. J. Exp. Med. 211 (2014), 769–779.
2. Cellier, C., Patey, N., Mauvieux, L., Jabri, B., Delabesse, E., Cervoni, J.P., Burtin, M.L., Guy-Grand, D., Bouhnik, Y., Modigliani, R., et al. Abnormal intestinal intraepithelial lymphocytes in refractory sprue. Gastroenterology 114 (1998), 471–481.
3. Cepek, K.L., Parker, C.M., Madara, J.L., Brenner, M.B., Integrin alpha E beta 7 mediates adhesion of T lymphocytes to epithelial cells. J. Immunol. 150 (1993), 3459–3470.
4. Chea, S., Perchet, T., Petit, M., Verrier, T., Guy-Grand, D., Banchi, E.G., Vosshenrich, C.A., Di Santo, J.P., Cumano, A., Golub, R., Notch signaling in group 3 innate lymphoid cells modulates their plasticity. Sci. Signal., 9, 2016, ra45.
5. Crescenzo, R., Abate, F., Lasorsa, E., Tabbo’, F., Gaudiano, M., Chiesa, N., Di Giacomo, F., Spaccarotella, E., Barbarossa, L., Ercole, E., et al., European T-Cell Lymphoma Study Group, T-Cell Project: Prospective Collection of Data in Patients with Peripheral T-Cell Lymphoma and the AIRC 5xMille Consortium “Genetics-Driven Targeted Management of Lymphoid Malignancies”. Convergent mutations and kinase fusions lead to oncogenic STAT3 activation in anaplastic large cell lymphoma. Cancer Cell 27 (2015), 516–532.
6. De Obaldia, M.E., Bhandoola, A., Transcriptional regulation of innate and adaptive lymphocyte lineages. Annu. Rev. Immunol. 33 (2015), 607–642.
7. De Smedt, M., Taghon, T., Van de Walle, I., De Smet, G., Leclercq, G., Plum, J., Notch signaling induces cytoplasmic CD3 epsilon expression in human differentiating NK cells. Blood 110 (2007), 2696–2703.
8. Eiras, P., Leon, F., Camarero, C., Lombardia, M., Roldan, E., Bootello, A., Roy, G., Intestinal intraepithelial lymphocytes contain a CD3- CD7+ subset expressing natural killer markers and a singular pattern of adhesion molecules. Scand. J. Immunol. 52 (2000), 1–6.
9. Fronková, E., Krejcí, O., Kalina, T., Horváth, O., Trka, J., Hrusák, O., Lymphoid differentiation pathways can be traced by TCR delta rearrangements. J. Immunol. 175 (2005), 2495–2500.
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 38 (2013), 769–781.
11. Gordy, L.E., Bezbradica, J.S., Flyak, A.I., Spencer, C.T., Dunkle, A., Sun, J., Stanic, A.K., Boothby, M.R., He, Y.W., Zhao, Z., et al. IL-15 regulates homeostasis and terminal maturation of NKT cells. J. Immunol. 187 (2011), 6335–6345.
12. Guy-Grand, D., Cuénod-Jabri, B., Malassis-Seris, M., Selz, F., Vassalli, P., Complexity of the mouse gut T cell immune system: identification of two distinct natural killer T cell intraepithelial lineages. Eur. J. Immunol. 26 (1996), 2248–2256.
13. Howie, D., Spencer, J., DeLord, D., Pitzalis, C., Wathen, N.C., Dogan, A., Akbar, A., MacDonald, T.T., Extrathymic T cell differentiation in the human intestine early in life. J. Immunol. 161 (1998), 5862–5872.
14. Jarry, A., Cerf-Bensussan, N., Brousse, N., Selz, F., Guy-Grand, D., Subsets of CD3+ (T cell receptor alpha/beta or gamma/delta) and CD3- lymphocytes isolated from normal human gut epithelium display phenotypical features different from their counterparts in peripheral blood. Eur. J. Immunol. 20 (1990), 1097–1103.
15. 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 157 (2014), 340–356.
16. Koch, U., Fiorini, E., Benedito, R., Besseyrias, V., Schuster-Gossler, K., Pierres, M., Manley, N.R., Duarte, A., Macdonald, H.R., Radtke, F., Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J. Exp. Med. 205 (2008), 2515–2523.
17. Koskela, H.L., Eldfors, S., Ellonen, P., van Adrichem, A.J., Kuusanmäki, H., Andersson, E.I., Lagström, S., Clemente, M.J., Olson, T., Jalkanen, S.E., et al. Somatic STAT3 mutations in large granular lymphocytic leukemia. N. Engl. J. Med. 366 (2012), 1905–1913.
18. Lambolez, F., Azogui, O., Joret, A.M., Garcia, C., von Boehmer, H., Di Santo, J., Ezine, S., Rocha, B., Characterization of T cell differentiation in the murine gut. J. Exp. Med. 195 (2002), 437–449.
19. León, F., Roldán, E., Sanchez, L., Camarero, C., Bootello, A., Roy, G., Human small-intestinal epithelium contains functional natural killer lymphocytes. Gastroenterology 125 (2003), 345–356.
20. Lin, T., Matsuzaki, G., Yoshida, H., Kobayashi, N., Kenai, H., Omoto, K., Nomoto, K., CD3-CD8+ intestinal intraepithelial lymphocytes (IEL) and the extrathymic development of IEL. Eur. J. Immunol. 24 (1994), 1080–1087.
21. Loeb, C.R., Harris, J.L., Craik, C.S., Granzyme B proteolyzes receptors important to proliferation and survival, tipping the balance toward apoptosis. J. Biol. Chem. 281 (2006), 28326–28335.
22. Malamut, G., El Machhour, R., Montcuquet, N., Martin-Lannerée, S., Dusanter-Fourt, I., Verkarre, V., Mention, J.J., Rahmi, G., Kiyono, H., Butz, E.A., et al. IL-15 triggers an antiapoptotic pathway in human intraepithelial lymphocytes that is a potential new target in celiac disease-associated inflammation and lymphomagenesis. J. Clin. Invest. 120 (2010), 2131–2143.
23. Malamut, G., Meresse, B., Cellier, C., Cerf-Bensussan, N., Refractory celiac disease: from bench to bedside. Semin. Immunopathol. 34 (2012), 601–613.
24. Mayans, S., Stepniak, D., Palida, S.F., Larange, A., Dreux, J., Arlian, B.M., Shinnakasu, R., Kronenberg, M., Cheroutre, H., Lambolez, F., αβT cell receptors expressed by CD4(-)CD8αβ(-) intraepithelial T cells drive their fate into a unique lineage with unusual MHC reactivities. Immunity 41 (2014), 207–218.
25. McDonald, B.D., Bunker, J.J., Ishizuka, I.E., Jabri, B., Bendelac, A., Elevated T cell receptor signaling identifies a thymic precursor to the TCRαβ(+)CD4(-)CD8β(-) intraepithelial lymphocyte lineage. Immunity 41 (2014), 219–229.
26. McKenzie, A.N., Spits, H., Eberl, G., Innate lymphoid cells in inflammation and immunity. Immunity 41 (2014), 366–374.
27. Mention, J.J., Ben Ahmed, M., Bègue, B., Barbe, U., Verkarre, V., Asnafi, V., Colombel, J.F., Cugnenc, P.H., Ruemmele, F.M., McIntyre, E., et al. Interleukin 15: a key to disrupted intraepithelial lymphocyte homeostasis and lymphomagenesis in celiac disease. Gastroenterology 125 (2003), 730–745.
28. Meresse, B., Malamut, G., Cerf-Bensussan, N., Celiac disease: an immunological jigsaw. Immunity 36 (2012), 907–919.
29. Park, Y., Moon, S.J., Lee, S.W., Lineage re-commitment of CD4CD8αα intraepithelial lymphocytes in the gut. BMB Rep. 49 (2016), 11–17.
30. Peaudecerf, L., dos Santos, P.R., Boudil, A., Ezine, S., Pardigon, N., Rocha, B., The role of the gut as a primary lymphoid organ: CD8alphaalpha intraepithelial T lymphocytes in euthymic mice derive from very immature CD44+ thymocyte precursors. Mucosal Immunol. 4 (2011), 93–101.
31. Radtke, F., Fasnacht, N., Macdonald, H.R., Notch signaling in the immune system. Immunity 32 (2010), 14–27.
32. Reinecker, H.C., MacDermott, R.P., Mirau, S., Dignass, A., Podolsky, D.K., Intestinal epithelial cells both express and respond to interleukin 15. Gastroenterology 111 (1996), 1706–1713.
33. Rocha, B., Vassalli, P., Guy-Grand, D., Thymic and extrathymic origins of gut intraepithelial lymphocyte populations in mice. J. Exp. Med. 180 (1994), 681–686.
34. Rothenberg, E.V., Zhang, J., Li, L., Multilayered specification of the T-cell lineage fate. Immunol. Rev. 238 (2010), 150–168.
35. Schmitz, F., Tjon, J.M., Lai, Y., Thompson, A., Kooy-Winkelaar, Y., Lemmers, R.J., Verspaget, H.W., Mearin, M.L., Staal, F.J., Schreurs, M.W., et al. Identification of a potential physiological precursor of aberrant cells in refractory coeliac disease type II. Gut 62 (2013), 509–519.
36. Schmitz, F., Kooy-Winkelaar, Y., Wiekmeijer, A.S., Brugman, M.H., Mearin, M.L., Mulder, C., Chuva de Sousa Lopes, S., Mummery, C.L., Staal, F.J., van Bergen, J., Koning, F., The composition and differentiation potential of the duodenal intraepithelial innate lymphocyte compartment is altered in coeliac disease. Gut 65 (2016), 1269–1278.
37. Schotte, R., Dontje, W., Nagasawa, M., Yasuda, Y., Bakker, A.Q., Spits, H., Blom, B., Synergy between IL-15 and Id2 promotes the expansion of human NK progenitor cells, which can be counteracted by the E protein HEB required to drive T cell development. J. Immunol. 184 (2010), 6670–6679.
38. Schröder, N., Gossler, A., Expression of Notch pathway components in fetal and adult mouse small intestine. Gene Expr. Patterns 2 (2002), 247–250.
39. Schulthess, J., Meresse, B., Ramiro-Puig, E., Montcuquet, N., Darche, S., Bègue, B., Ruemmele, F., Combadière, C., Di Santo, J.P., Buzoni-Gatel, D., Cerf-Bensussan, N., Interleukin-15-dependent NKp46+ innate lymphoid cells control intestinal inflammation by recruiting inflammatory monocytes. Immunity 37 (2012), 108–121.
40. Serafini, N., Vosshenrich, C.A., Di Santo, J.P., Transcriptional regulation of innate lymphoid cell fate. Nat. Rev. Immunol. 15 (2015), 415–428.
41. Six, E.M., Bonhomme, D., Monteiro, M., Beldjord, K., Jurkowska, M., Cordier-Garcia, C., Garrigue, A., Dal Cortivo, L., Rocha, B., Fischer, A., et al. A human postnatal lymphoid progenitor capable of circulating and seeding the thymus. J. Exp. Med. 204 (2007), 3085–3093.
42. 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. 13 (2013), 145–149.
43. Tack, G.J., van Wanrooij, R.L., Langerak, A.W., Tjon, J.M., von Blomberg, B.M., Heideman, D.A., van Bergen, J., Koning, F., Bouma, G., Mulder, C.J., Schreurs, M.W., Origin and immunophenotype of aberrant IEL in RCDII patients. Mol. Immunol. 50 (2012), 262–270.
44. van Dongen, J.J., Langerak, A.W., Brüggemann, M., Evans, P.A., Hummel, M., Lavender, F.L., Delabesse, E., Davi, F., Schuuring, E., García-Sanz, R., et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia 17 (2003), 2257–2317.
45. + innate-type lymphocytes in the intestinal epithelium mediate mucosal immunity. Immunity 41 (2014), 451–464.
46. van Tetering, G., Bovenschen, N., Meeldijk, J., van Diest, P.J., Vooijs, M., Cleavage of Notch1 by granzyme B disables its transcriptional activity. Biochem. J. 437 (2011), 313–322.
47. Vosshenrich, C.A., Di Santo, J.P., Developmental programming of natural killer and innate lymphoid cells. Curr. Opin. Immunol. 25 (2013), 130–138.
48. Wakabayashi, Y., Watanabe, H., Inoue, J., Takeda, N., Sakata, J., Mishima, Y., Hitomi, J., Yamamoto, T., Utsuyama, M., Niwa, O., et al. Bcl11b is required for differentiation and survival of alphabeta T lymphocytes. Nat. Immunol. 4 (2003), 533–539.