Specific overexpression of IL-7 in the intestinal mucosa: The role in intestinal intraepithelial lymphocyte development

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 294, Issue 6, 2008, Pages

  Yang, Hua ^a,b,d   Madison, Blair ^b   Gumucio, Deborah L ^b   Teitelbaum, Daniel H ^b,c  

^a Xinqiao Hospital   (China)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN HOSPITALS   (United States)

^d THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Epithelial cells; Interleukin 7; Mouse; Transgenic

Indexed keywords

CD103 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; HERMES ANTIGEN; INTERLEUKIN 7; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; GENE OVEREXPRESSION; ILEUM; JEJUNUM; LAMINA PROPRIA; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMALL INTESTINE MUCOSA; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE; ANIMAL; CELL CULTURE; CYTOLOGY; INTESTINE MUCOSA; LYMPHOCYTE; METABOLISM; PHYSIOLOGY; UPREGULATION;

ANIMALS; CELLS, CULTURED; INTERLEUKIN-7; INTESTINAL MUCOSA; LYMPHOCYTES; MICE; UP-REGULATION;

EID: 48249115700     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00060.2008     Document Type: Article

References (53)

1. Armitage RJ, Namen AE, Sassenfeld HM, Grabstein KH. Regulation of human T cell proliferation by IL-7. J Immunol 144: 938-941, 1990.
2. Barnard JA, Beauchamp RD, Coffey RJ, Moses HL. Regulation of intestinal epithelial cell growth by transforming growth factor type beta. Proc Natl Acad Sci USA 86: 1578-1582, 1989.
3. Beagley KW, Husband AJ. Intraepithelial lymphocytes: origins, distribution, function. Crit Rev Immunol 18: 237-254, 1998.
4. Bhatia SK, Tygrett LT, Grabstein KH, Waldschmidt TJ. The effect of in vivo IL-7 deprivation on T cell maturation. J Exp Med 181: 1399-1409, 1995.
5. Boismenu R, Havran WL. Modulation of epithelial cell growth by intraepithelial gamma delta T cells. Science 266: 1253-1255, 1994.
6. Borger P, Kauffman HF, Postma DS, Vellenga E. IL-7 differentially modulates the expression of IFN-gamma and IL-4 in activated human T lymphocytes by transcriptional and post-transcriptional mechanisms. J Immunol 156: 1333-1338, 1996.
7. Eisenbraun MD, Mosley RL, Teitelbaum DH, Miller RA. Altered development of intestinal intraepithelial lymphocytes in P-glycoprotein- deficient mice. Dev Comp Immunol 24: 783-795, 2000.
8. Fujihashi K, Kawabata S, Hiroi T, Yamamoto M, McGhee JR, Nishikawa S, Kiyono H. Interleukin 2 (IL-2) and interleukin 7 (IL-7) reciprocally induce IL-7 and IL-2 receptors on gamma delta T cell receptor-positive intraepithelial lymphocytes. Proc Natl Acad Sci USA 93: 3613-3618, 1996.
9. Geiselhart LA, Humphries CA, Gregorio TA, Mou S, Subleski J, Komschlies KL. IL-7 administration alters the CD4:CD8 ratio, increases T cell numbers, and increases T cell function in the absence of activation. J Immunol 166: 3019-3027, 2001.
10. Guy-Grand D, Vassalli P. Gut intraepithelial T lymphocytes. Curr Opin Immunol 5: 247-252, 1993.
11. Hayday A, Theodoridis E, Ramsburg E, Shires J. Intraepithelial lymphocytes: exploring the Third Way in immunology. Nat Immunol 2: 997-1003, 2001.
12. He YW, Malek TR. The structure and function of gamma c-dependent cytokines and receptors: regulation of T lymphocyte development and homeostasis. Crit Rev Immunol 18: 503-524, 1998.
13. Howie D, Spencer J, Delord D, Pitzalis C, Wathen NC, Dogan A, Akbar A, Macdonald TT. Extrathymic T cell differentiation in the human intestine early in life. J Immunol 161: 5862-5872, 1998.
14. Jiang Y, McGee DW. Regulation of human lymphocyte IL-4 secretion by intestinal epithelial cell-derived interleukin-7 and transforming growth factor-beta. Clin Immunol Immunopathol 88: 287-296, 1998.
15. Kenai H, Matsuzaki G, Nakamura T, Yoshikai Y, Nomoto K. Thymus-derived cytokine(s) including interleukin-7 induce increase of T cell receptor αβ+ CD4-CD8- T cells which are extrathymically differentiated in athymic nude mice. Eur J Immunol 23: 1818-1825, 1993.
16. Kiristioglu I, Antony P, Fan Y, Forbush B, Mosley RL, Yang H, Teitelbaum DH. Total parenteral nutrition-associated changes in mouse intestinal intraepithelial lymphocytes. Dig Dis Sci 47: 1147-1157, 2002.
17. Kiristioglu I, Teitelbaum DH. Alteration of the intestinal intraepithelial lymphocytes during total parenteral nutrition. J Surg Res 79: 91-96, 1998.
18. Laky K, Lefrancois L, Lingenheld EG, Puddington L. Enterocyte expression of interleukin 7 induces development of gamma delta T cells and Peyer's patches. J Exp Med 191: 1569-1580, 2000.
19. Laouar Y, Crispe IN, Flavell RA. Overexpression of IL-7R alpha provides a competitive advantage during early T-cell development. Blood 103: 1985-1994, 2004.
20. Li J, Kudsk KA, Gocinski B, Dent D, Glezer J, Langkamp-Henken B. Effects of parenteral and enteral nutrition on gut-associated lymphoid tissue. J Trauma 39: 44-52, 1995.
21. Lin T, Matsuzaki G, Yoshida H, Kenai H, Omoto K, Umesue M, Singaram C, Nomoto K. Thymus ontogeny and the development of TCR alpha beta intestinal intraepithelial lymphocytes. Cell Immunol 171: 132-139, 1996.
22. Madison BB, Braunstein K, Kuizon E, Portman K, Qiao XT, Gumucio DL. Epithelial hedgehog signals pattern the intestinal crypt-villus axis. Development 132: 279-289, 2005.
23. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 277: 33275-33283, 2002.
24. Maki K, Sunaga S, Komagata Y, Kodaira Y, Mabuchi A, Karasuyama H, Yokomuro K, Miyazaki JI, Ikuta K. Interleukin 7 receptor-deficient mice lack gammadelta T cells. Proc Natl Acad Sci USA 93: 7172-7177, 1996.
25. Maunoury R, Robine S, Pringault E, Leonard N, Gaillard JA, Louvard D. Developmental regulation of villin gene expression in the epithelial cell lineages of mouse digestive and urogenital tracts. Development 115: 717-728, 1992.
26. Miller RA. Age-related changes in T cell surface markers: a longitudinal analysis in genetically heterogeneous mice. Mech Ageing Dev 96: 181-196, 1997.
27. Pinto D, Robine S, Jaisser F, El Marjou FE, Louvard D. Regulatory sequences of the mouse villin gene that efficiently drive transgenic expression in immature and differentiated epithelial cells of small and large intestines. J Biol Chem 274: 6476-6482, 1999.
28. Porter BO, Malek TR. Thymic and intestinal intraepithelial T lymphocyte development are each regulated by the gammac-dependent cytokines IL-2, IL-7, and IL-15. Semin Immunol 12: 465-474, 2000.
29. Rocha B, Vassalli P, Guy-Grand D. Thymic and extrathymic origins of gut intraepithelial lymphocyte populations in mice. J Exp Med 180: 681-686, 1994.
30. Rubin J, Osada H, Finch P. Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc Natl Acad Sci USA 806: 802-906, 1989.
31. Sillett HK, Southgate J, Howdle PD, Trejdosiewicz LK. Expression of activation and costimulatory elements by human intestinal intraepithelial lymphocytes. Scand J Immunol 50: 52-60, 1999.
32. Sudo T, Nishikawa S, Ohno N, Akiyama N, Tamakoshi M, Yoshida H. Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc Natl Acad Sci USA 90: 9125-9129, 1993.
33. Suzuki K, Oida T, Hamada H, Hitotsumatsu O, Watanabe M, Hibi T, Yamamoto H, Kubota E, Kaminogawa S, Ishikawa H. Gut cryptopatches: direct evidence of extrathymic anatomical sites for intestinal T lymphopoiesis. Immunity 13: 691-702, 2000.
34. Tan JT, Dudl E, LeRoy E, Murray R, Sprent J, Weinberg KI, Surh CD. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci USA 98: 8732-8737, 2001.
35. Thomis DC, Gurniak CB, Tivol E, Sharpe AH, Berg LJ. Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science 270: 794-797, 1995.
36. Tough DF, Sprent J. Turnover of naive- and memory-phenotype T cells. J Exp Med 179: 1127-1135, 1994.
37. Watanabe M, Ueno Y, Yajima T, Iwao Y, Tsuchiya M, Ishikawa H, Aiso S, Hibi T, Ishii H. Interleukin 7 is produced by human intestinal epithelial cells and regulates the proliferation of intestinal mucosal lymphocytes. J Clin Invest 95: 2945-2953, 1995.
38. Watanabe M, Ueno Y, Yajima T, Okamoto S, Hayashi T, Yamazaki M, Iwao Y, Ishii H, Habu S, Uehira M, Nishimoto H, Ishikawa H, Hata J, Hibi T. Interleukin 7 transgenic mice develop chronic colitis with decreased interleukin 7 protein accumulation in the colonic mucosa. J Exp Med 187: 389-402, 1998.
39. Watanabe M, Yamazaki M, Okamoto R, Ohoka S, Araki A, Nakamura T, Kanai T. Therapeutic approaches to chronic intestinal inflammation by specific targeting of mucosal IL-7/IL-7R signal pathway. Curr Drug Targets Inflamm Allergy 2: 119-123, 2003.
40. Weissenbach M, Clahsen T, Weber C, Spitzer D, Wirth D, Vestweber D, Heinrich PC, Schaper F. Interleukin-6 is a direct mediator of T cell migration. Eur J Immunol 34: 2895-2906, 2004.
41. Welch PA, Namen AE, Goodwin RG, Armitage R, Cooper MD. Human IL-7: a novel T cell growth factor. J Immunol 143: 3562-3567, 1989.
42. Witkowski J, Miller R. Increased function of P-glycoprotein in T lymphocyte subsets of aging mice. J Immunol 150: 1296-1306, 1993.
43. Yada S, Nukina H, Kishihara K, Takamura N, Yoshida H, Inagaki-Ohara K, Nomoto K, Lin T. IL-7 prevents both caspase-dependent and -independent pathways that lead to the spontaneous apoptosis of i-EIL. Cell Immunol 208: 88-95, 2001.
44. Yamazaki M, Yajima T, Tanabe M, Fukui K, Okada E, Okamoto R, Oshima S, Nakamura T, Kanai T, Uehira M, Takeuchi T, Ishikawa H, Hibi T, Watanabe M. Mucosal T cells expressing high levels of IL-7 receptor are potential targets for treatment of chronic colitis. J Immunol 171: 1556-1563, 2003.
45. Yang H, Antony PA, Wildhaber BE, Teitelbaum DH. Intestinal intraepithelial lymphocyte gammadelta-T cell-derived keratinocyte growth factor modulates epithelial growth in the mouse. J Immunol 172: 4151-4158, 2004.
46. Yang H, Fan Y, Teitelbaum DH. Intraepithelial lymphocyte-derived interferon-gamma evokes enterocyte apoptosis with parenteral nutrition in mice. Am J Physiol Gastrointest Liver Physiol 284: G629-G637, 2003.
47. Yang H, Finaly R, Teitelbaum DH. Alteration in epithelial permeability and ion transport in a mouse model of total parenteral nutrition. Crit Care Med 31: 1118-1125, 2003.
48. Yang H, Kiristioglu I, Fan Y, Forbush B, Bishop DK, Antony PA, Zhou H, Teitelbaum DH. Interferon-gamma expression by intraepithelial lymphocytes results in a loss of epithelial barrier function in a mouse model of total parenteral nutrition. Ann Surg 236: 226-234, 2002.
49. Yang H, Spencer AU, Teitelbaum DH. Interleukin-7 administration alters intestinal intraepithelial lymphocyte phenotype and function in vivo. Cytokine 31: 419-428, 2005.
50. Yang H, Sun X, Haxhija EQ, Teitelbaum DH. Intestinal epithelial cell-derived interleukin-7: a mechanism for the alteration of intraepithelial lymphocytes in a mouse model of total parenteral nutrition. Am J Physiol Gastrointest Liver Physiol 292: G84-G91, 2007.
51. Yang H, Teitelbaum DH. Novel agents in the treatment of intestinal failure: humoral factors. Gastroenterology 130: S117-S121, 2006.
52. Yang H, Wildhaber B, Tazuke Y, Teitelbaum DH. 2002 Harry M. Vars Research Award. Keratinocyte growth factor stimulates the recovery of epithelial structure and function in a mouse model of total parenteral nutrition. JPEN J Parenter Enteral Nutr 26: 333-340; discussion 340-341, 2002.
53. Yang H, Wildhaber BE, Teitelbaum DH. Decline in intestinal epithelial cell-derived IL-7: a mechanism for the alteration of intraepithelial lymphocytes in a mouse model of total parenteral nutrition (Abstract). Gastroenterology 126: A-126, 2004.