Smad and NFAT pathways cooperate to induce CD103 expression in human CD8 T lymphocytes

Journal of Immunology

Volumn 192, Issue 5, 2014, Pages 2471-2479

  Mokrani, M'Barka ^a,b,c   Klibi, Jihène ^a,b,c,h   Bluteau, Dominique ^d,i   Bismuth, Georges ^e,f,g   Mami Chouaib, Fathia ^a,b,c  

^a Unite Inst Natl de la S et de la Rech Med U753 Immunol des Tumeurs Humaines   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d Universite Paris Sud   (France)

^e INSTITUT COCHIN   (France)

^f CNRS   (France)

^g UNIVERSITÉ PARIS DESCARTES   (France)

^h INSTITUT PASTEUR   (France)

ⁱ SAINT LOUIS HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CD8+ T LYMPHOCYTE; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; GENETIC CODE; HUMAN; HUMAN CELL; ITGAE GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANTIGENS, CD; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; HEK293 CELLS; HUMANS; INTEGRIN ALPHA CHAINS; JURKAT CELLS; LUNG NEOPLASMS; NFATC TRANSCRIPTION FACTORS; RECEPTORS, ANTIGEN, T-CELL; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84896509142     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302192     Document Type: Article

References (56)

1. Le Floc'h, A., A. Jalil, I. Vergnon, B. Le Maux Chansac, V. Lazar, G. Bismuth, S. Chouaib, and F. Mami-Chouaib. 2007. Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J. Exp. Med. 204: 559-570.
2. Franciszkiewicz, K., A. Le Floc'h, A. Jalil, F. Vigant, T. Robert, I. Vergnon, A. Mackiewicz, K. Benihoud, P. Validire, S. Chouaib, et al. 2009. Intratumoral induction of CD103 triggers tumor-specific CTL function and CCR5-dependent T-cell retention. Cancer Res. 69: 6249-6255.
3. Le Floc'h, A., A. Jalil, K. Franciszkiewicz, P. Validire, I. Vergnon, and F. Mami-Chouaib. 2011. Minimal engagement of CD103 on cytotoxic T lymphocytes with an E-cadherin-Fc molecule triggers lytic granule polarization via a phospholipase Cgamma-dependent pathway. Cancer Res. 71: 328-338.
4. Franciszkiewicz, K., A. Le Floc'h, M. Boutet, I. Vergnon, A. Schmitt, and F. Mami-Chouaib. 2013. CD103 or LFA-1 engagement at the immune synapse between cytotoxic T cells and tumor cells promotes maturation and regulates T-cell effector functions. Cancer Res. 73: 617-628.
5. Springer, T. A. 1990. Adhesion receptors of the immune system. Nature 346: 425-434.
6. Hadley, G. A., S. T. Bartlett, C. S. Via, E. A. Rostapshova, and S. Moainie. 1997. The epithelial cell-specific integrin, CD103 (alpha E integrin), defines a novel subset of alloreactive CD8+ CTL J. Immunol. 159: 3748-3756.
7. Hadley, G. 2004. Role of integrin CD103 in promoting destruction of renal allografts by CD8 T cells. Am. J. Transplant. 4: 1026-1032.
8. Kinashi, T. 2005. Intracellular signalling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 5: 546-559.
9. Wong, W. K., H. Robertson, H. P. Carroll, S. Ali, and J. A. Kirby. 2003. Tubulitis in renal allograft rejection: role of transforming growth factor-beta and interleukin-15 in development and maintenance of CD103+ intraepithelial T cells. Transplantation 75: 505-514.
10. El-Asady, R., R. Yuan, K. Liu, D. Wang, R. E. Gress, P. J. Lucas, C. B. Drachenberg, and G. A. Hadley. 2005. TGF-beta-dependent CD103 expression by CD8(+) T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease. J. Exp. Med. 201: 1647-1657.
11. Luo, B. H., C. V. Carman, and T. A. Springer. 2007. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25: 619-647.
12. Zhou, S., H. Ueta, X. D. Xu, C. Shi, and K. Matsuno. 2008. Predominant donor CD103+CD8+ T cell infiltration into the gut epithelium during acute GvHD: a role of gut lymph nodes. Int. Immunol. 20: 385-394.
13. Liu, K., B. A. Anthony, M. M. Yearsly, M. Hamadani, A. Gaughan, J. J. Wang, S. M. Devine, and G. A. Hadley. 2011. CD103 deficiency prevents graft-versushost disease but spares graft-versus-tumor effects mediated by alloreactive CD8 T cells. PLoS One 6: e21968.
14. Kilshaw, P. J. 1999. Alpha E beta 7. Mol. Pathol. 52: 203-207.
15. Pauls, K., M. Schön, R. C. Kubitza, B. Homey, A. Wiesenborn, P. Lehmann, T. Ruzicka, C. M. Parker, and M. P. Schön. 2001. Role of integrin alphaE (CD103)beta7 for tissue-specific epidermal localization of CD8+ T lymphocytes. J. Invest. Dermatol. 117: 569-575.
16. C uburu, N., B. S. Graham, C. B. Buck, R. C. Kines, Y. Y. Pang, P. M. Day, D. R. Lowy, and J. T. Schiller. 2012. Intravaginal immunization with HPV vectors induces tissue-resident CD8+ T cell responses. J. Clin. Invest. 122: 4606-4620.
17. Sung, S. S., S. M. Fu, C. E. Rose, Jr., F. Gaskin, S. T. Ju, and S. R. Beaty. 2006. A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J. Immunol. 176: 2161-2172.
18. Annacker, O., J. L. Coombes, V. Malmstrom, H. H. Uhlig, T. Bourne, B. Johansson-Lindbom, W. W. Agace, C. M. Parker, and F. Powrie. 2005. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 202: 1051-1061.
19. Rao, P. E., A. L. Petrone, and P. D. Ponath. 2005. Differentiation and expansion of T cells with regulatory function from human peripheral lymphocytes by stimulation in the presence of TGF-beta. J. Immunol. 174: 1446-1455.
20. Cresswell, J., W. K. Wong, M. J. Henry, H. Robertson, D. E. Neal, and J. A. Kirby. 2002. Adhesion of lymphocytes to bladder cancer cells: the role of the alpha(E)beta(7) integrin. Cancer Immunol. Immunother. 51: 483-491.
21. Quinn, E., N. Hawkins, Y. L. Yip, C. Suter, and R. Ward. 2003. CD103+ intraepithelial lymphocytes-A unique population in microsatellite unstable sporadic colorectal cancer. Eur. J. Cancer 39: 469-475.
22. French, J. J., J. Cresswell, W. K. Wong, K. Seymour, R. M. Charnley, and J. A. Kirby. 2002. T cell adhesion and cytolysis of pancreatic cancer cells: a role for E-cadherin in immunotherapy? Br. J. Cancer 87: 1034-1041.
23. Webb, J. R., D. A. Wick, J. S. Nielsen, E. Tran, K. Milne, E. McMurtrie, and B. H. Nelson. 2010. Profound elevation of CD8+ T cells expressing the intraepithelial lymphocyte marker CD103 (alphaE/beta7 integrin) in high-grade serous ovarian cancer. Gynecol. Oncol. 118: 228-236.
24. Andrew, D. P., L. S. Rott, P. J. Kilshaw, and E. C. Butcher. 1996. Distribution of alpha 4 beta 7 and alpha E beta 7 integrins on thymocytes, intestinal epithelial lymphocytes and peripheral lymphocytes. Eur. J. Immunol. 26: 897-905.
25. Kilshaw, P. J., and J. M. Higgins. 2002. Alpha E: no more rejection? J. Exp. Med. 196: 873-875.
26. Masson, F., T. Calzascia, W. Di Berardino-Besson, N. De Tribolet, P. Y. Dietrich, and P. R. Walker. 2007. Brain microenvironment promotes the final functional maturation of tumor-specific effector CD8+ T cells. J. Immunol. 179: 845-853.
27. Ling, K. L., N. Dulphy, P. Bahl, M. Salio, K. Maskell, J. Piris, B. F. Warren, B. D. George, N. J. Mortensen, and V. Cerundolo. 2007. Modulation of CD103 expression on human colon carcinoma-specific CTL. J. Immunol. 178: 2908-2915.
28. Teraki, Y., and T. Shiohara. 2002. Preferential expression of alphaEbeta7 integrin (CD103) on CD8+ T cells in the psoriatic epidermis: regulation by interleukins 4 and 12 and transforming growth factor-beta. Br. J. Dermatol. 147: 1118-1126.
29. Lucas, P. J., S. J. Kim, S. J. Melby, and R. E. Gress. 2000. Disruption of T cell homeostasis in mice expressing a T cell-specific dominant negative transforming growth factor beta II receptor. J. Exp. Med. 191: 1187-1196.
30. Wang, D., R. Yuan, Y. Feng, R. El-Asady, D. L. Farber, R. E. Gress, P. J. Lucas, and G. A. Hadley. 2004. Regulation of CD103 expression by CD8+ T cells responding to renal allografts. J. Immunol. 172: 214-221.
31. Parker, C. M., K. L. Cepek, G. J. Russell, S. K. Shaw, D. N. Posnett, R. Schwarting, and M. B. Brenner. 1992. A family of beta 7 integrins on human mucosal lymphocytes. Proc. Natl. Acad. Sci. USA 89: 1924-1928.
32. Kilshaw, P. J., and S. J. Murant. 1990. A new surface antigen on intraepithelial lymphocytes in the intestine. Eur. J. Immunol. 20: 2201-2207.
33. Lim, S. P., E. Leung, and G. W. Krissansen. 1998. The beta7 integrin gene (Itgb-7) promoter is responsive to TGF-beta1: defining control regions. Immunogenetics 48: 184-195.
34. Robinson, P. W., S. J. Green, C. Carter, J. Coadwell, and P. J. Kilshaw. 2001. Studies on transcriptional regulation of the mucosal T-cell integrin alphaEbeta7 (CD103). Immunology 103: 146-154.
35. Dorothée, G., I. Vergnon, F. El Hage, B. Le Maux Chansac, V. Ferrand, Y. Lécluse, P. Opolon, S. Chouaib, G. Bismuth, and F. Mami-Chouaib. 2005. In situ sensory adaptation of tumor-infiltrating T lymphocytes to peptide-MHC levels elicits strong antitumor reactivity. J. Immunol. 174: 6888-6897.
36. Echchakir, H., F. Mami-Chouaib, I. Vergnon, J. F. Baurain, V. Karanikas, S. Chouaib, and P. G. Coulie. 2001. A point mutation in the alpha-Actinin-4 gene generates an antigenic peptide recognized by autologous cytolytic T lymphocytes on a human lung carcinoma. Cancer Res. 61: 4078-4083.
37. Shi, Y., and J. Massagué. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
38. Massagué, J. 1998. TGF-beta signal transduction. Annu. Rev. Biochem. 67: 753-791.
39. Verschueren, K., and D. Huylebroeck. 1999. Remarkable versatility of Smad proteins in the nucleus of transforming growth factor-beta activated cells. Cytokine Growth Factor Rev. 10: 187-199.
40. Park, J., N. R. Yaseen, P. G. Hogan, A. Rao, and S. Sharma. 1995. Phosphorylation of the transcription factor NFATp inhibits its DNA binding activity in cyclosporin A-treated human B and T cells. J. Biol. Chem. 270: 20653-20659.
41. Thomas, D. A., and J. Massagué. 2005. TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 8: 369-380.
42. Takimoto, T., Y. Wakabayashi, T. Sekiya, N. Inoue, R. Morita, K. Ichiyama, R. Takahashi, M. Asakawa, G. Muto, T. Mori, et al. 2010. Smad2 and Smad3 are redundantly essential for the TGF-beta-mediated regulation of regulatory T plasticity and Th1 development. J. Immunol. 185: 842-855.
43. Cornwell, R. D., K. A. Gollahon, and D. D. Hickstein. 1993. Description of the leukocyte function-Associated antigen 1 (LFA-1 or CD11a) promoter. Proc. Natl. Acad. Sci. USA 90: 4221-4225.
44. Nueda, A., M. López-Cabrera, A. Vara, and A. L. Corbí. 1993. Characterization of the CD11a (alpha L, LFA-1 alpha) integrin gene promoter. J. Biol. Chem. 268: 19305-19311.
45. Zutter, M. M., S. A. Santoro, A. S. Painter, Y. L. Tsung, and A. Gafford. 1994. The human alpha 2 integrin gene promoter: identification of positive and negative regulatory elements important for cell-type and developmentally restricted gene expression. J. Biol. Chem. 269: 463-469.
46. Lin, C. S., Y. Chen, T. Huynh, and R. Kramer. 1997. Identification of the human alpha6 integrin gene promoter. DNA Cell Biol. 16: 929-937.
47. Córbi, A. L., and C. Lopéz-Rodríguez. 1997. CD11c integrin gene promoter activity during myeloid differentiation. Leuk. Lymphoma 25: 415-425.
48. Hanai, J., L. F. Chen, T. Kanno, N. Ohtani-Fujita, W. Y. Kim, W. H. Guo, T. Imamura, Y. Ishidou, M. Fukuchi, M. J. Shi, et al. 1999. Interaction and functional cooperation of PEBP2/CBF with Smads: synergistic induction of the immunoglobulin germline Calpha promoter. J. Biol. Chem. 274: 31577-31582.
49. Zaidi, S. K., A. J. Sullivan, A. J. Van Wijnen, J. L. Stein, G. S. Stein, and J. B. Lian. 2002. Integration of Runx and Smad regulatory signals at transcriptionally active subnuclear sites. Proc. Natl. Acad. Sci. USA 99: 8048-8053.
50. Miyazono, K., S. Maeda, and T. Imamura. 2004. Coordinate regulation of cell growth and differentiation by TGF-beta superfamily and Runx proteins. Oncogene 23: 4232-4237.
51. Blyth, K., E. R. Cameron, and J. C. Neil. 2005. The RUNX genes: gain or loss of function in cancer. Nat. Rev. Cancer 5: 376-387.
52. Grueter, B., M. Petter, T. Egawa, K. Laule-Kilian, C. J. Aldrian, A. Wuerch, Y. Ludwig, H. Fukuyama, H. Wardemann, R. Waldschuetz, et al. 2005. Runx3 regulates integrin alpha E/CD103 and CD4 expression during development of CD42/CD8+ T cells. J. Immunol. 175: 1694-1705.
53. Tone, Y., K. Furuuchi, Y. Kojima, M. L. Tykocinski, M. I. Greene, and M. Tone. 2008. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat. Immunol. 9: 194-202.
54. Zou, W. 2006. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 6: 295-307.
55. Suffia, I., S. K. Reckling, G. Salay, and Y. Belkaid. 2005. A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. J. Immunol. 174: 5444-5455.
56. Wagner, N., J. Löhler, E. J. Kunkel, K. Ley, E. Leung, G. Krissansen, K. Rajewsky, and W. Müller. 1996. Critical role for beta7 integrins in formation of the gut-Associated lymphoid tissue. Nature 382: 366-370.