Differential roles of interleukin 15 mRNA isoforms generated by alternative splicing in immune responses in vivo

Journal of Experimental Medicine

Volumn 191, Issue 1, 2000, Pages 157-169

  Nishimura, Hitoshi ^a   Yajima, Toshiki ^a   Naiki, Yoshikazu ^a   Tsunobuchi, Hironaka ^a   Umemura, Masayuki ^a   Itano, Keiko ^a   Matsuguchi, Tetsuya ^a   Suzuki, Misao ^b   Ohashi, Pamela S ^c   Yoshikai, Yasunobu ^a  

^a NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KUMAMOTO UNIV SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

CD8 T cells; Memory T cells; Salmonella; Th1 Th2; Transgenic mice

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; COMPLEMENTARY DNA; GAMMA INTERFERON; INTERLEUKIN 15; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; T LYMPHOCYTE RECEPTOR;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EXON; IMMUNE RESPONSE; INFECTION RESISTANCE; INTERFERON PRODUCTION; MEMORY CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SALMONELLA; TRANSGENIC MOUSE;

ALTERNATIVE SPLICING; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOKINES; INTERLEUKIN-15; INTERLEUKIN-2; LYMPH NODES; MICE; MICE, TRANSGENIC; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SALMONELLA INFECTIONS, ANIMAL;

EID: 0034598370     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.1.157     Document Type: Article

References (59)

1. Tagaya, Y., R.N. Bamford, A. DeFilippis, and T.A. Waldmann. 1996. IL-15: a pleiotropic cytokine with diverse receptor/signaling pathways whose expression is controlled at multiple levels. Immunity. 4:329-336.
2. Waldmann, T.A., Y. Tagaya, and R.N. Bamford. 1998. Interleukin-2, interleukin-15, and their receptors. Int. Rev. Immunol. 16:205-226.
3. Waldmann, T.A., and Y. Tagaya. 1999. The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu. Rev. Immunol. 17:19-49.
4. Grabstein, K.H., J. Eisenmann, K. Shanebeck, C. Rauch, S. Srinivasan, V. Fung, C. Beers, J. Richardson, M.A. Schoenborn, M. Ahdieh, et al. 1994. Cloning of a T-cell growth factor that interacts with the β chain of the interleukin-2 receptor. Science. 246:965-968.
5. Bamford, R.N., A.P. Battiata, J.D. Burton, H. Sharma, and T.A. Waldmann. 1996. IL-15/T production by the adult T-cell leukemia cell line HuT-102 is associated with an HTLV-I-R/IL-15 fusion message that lacks many upstream AUGs that normally attenuate IL-15 mRNA translation. Proc. Natl. Acad. Sci. USA. 93:2897-2902.
6. Carson, W.E., T.A. Fehniger, S. Halder, K. Eckhert, M.J. Lindemann, C.F. Lai, C.M. Croce, H. Baumann, and M.A. Caligiuri. 1997. A potential role of interleukin-15 in the regulation of human natural killer cell survival. J. Clin. Invest. 99:937-943.
7. Inagaki-Ohara, K., H. Nishimura, A. Mitani, and Y. Yoshikai. 1997. Interleukin-15 preferentially promotes the growth of intestinal intraepithelial lymphocytes bearing γδ T cell receptor in mice. Eur. J. Immunol. 27:2885-2891.
8. + intestinal intraepithelial lymphocytes. J. Immunol. 162: 1896-1903.
9. Ogasawara, K., S. Hida, N. Azimi, Y. Tagaya, T. Sato, Y. Yokochi-Fukuda, T.A. Waldmann, T. Taniguchi, and S. Taki. 1998. Requirement for IRF-1 in the microenvironment supporting development of natural killer cells. Nature. 391:700-703.
10. + T) cells, natural killer cells, and intestinal intraepithelial T cells. J. Exp. Med. 187:967-972.
11. Lodolce, J.P., D.I., Boone, S. Chai, R.E. Swain, T. Dassopoulos, S. Trettin, and A. Ma. 1998. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation, Immunity. 9:669-676.
12. Alleva, D.G., S.B. Kaser, M.A. Monroy, M.J. Fenton, and D.I. Beller. 1997. IL-15 functions as a potent autocrine regulator of macrophage proinflammatory cytokine production. J. Immunol. 159:2941-2951.
13. Tagaya, Y., J.D. Burton, Y. Miyamoto, and T.A. Waldmann. 1996. Identification of a novel receptor/signal transduction pathway for IL-15/T in mast cells. EMBO (Eur. Mol. Biol. Organ.) J. 15:4928-4939.
14. Carson, W.E., J.G. Giri, M.J. Lindemann, M.L. Linett, M. Ahdieh, R. Paxton, D. Anderson, J. Eisenmann, K. Grabstein, and M.A. Caligiuri. 1994. Interleukin (IL)-15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J. Exp. Med. 180:1395-1403.
15. Armitage, R.J., B.M. Macduff, J. Eisennian, R. Paxton, and K.H. Grabstein. 1995. IL-15 has stipulatory activity for the induction of B cell proliferation and differentiation. J. Immunol. 154:483-490.
16. + T cell-mediated immunity against Toxoplasma gondii infection in mice. J. Immunol. 157:2103-2108.
17. Mody, C.H., J.C.L. Spurrell, and C.J. Wood. 1998. Interleukin-15 induces antimicrobial activity after release by Cryptococcus neoformans-stimulated monocytes. J. Infect. Dis. 178: 803-814.
18. Vazquez, N., T.J. Walsh, D. Friedman, S.J. Chanock, and C.A. Lyman. 1998. Interleukin-15 augments superoxide production and microbicidal activity of human monocytes against Candida albicans. Infect. Immun. 66:145-150.
19. Nishimura, H., K. Hiromatsu, N. Kobayashi, K. Grabstein, K. Paxton, K. Sugamura, J.A. Bluestone, and Y. Yoshikai. 1996. IL-15 is a novel growth factor for murine γδ T cells induced by Salmonella infection. J. Immunol. 156:663-669.
20. Takano, M., H. Nishimura, Y. Kimura, Y. Mokuno, J. Washizu, S. Itohara, Y. Nimura, and Y. Yoshikai. 1998. Protective roles of γδ T cells and interleukin-15 in Escherichia coli infection in mice. Infect. Immun. 66:3270-3278.
21. Hirose, K., H. Suzuki, H. Nishimura, A. Mitani, J. Washizu, T. Matsuguchi, and Y. Yoshikai. 1998. Interleukin-15 may be responsible for early activation of intestinal intraepithelial lymphocytes after oral infection with Listeria monocytogenes in rat. Infect. Immun. 66:5677-5683.
22. Doherty, T.M., R.A. Seder, and A. Sher. 1996. Induction and regulation of IL-15 expression in murine macrophages. J. Immunol. 156:735-741.
23. Jullien, D., P.A. Sieling, K. Uyemura, N.D. Mar, T.H. Rea, and R.L. Modlin. 1997. IL-15, an immunomodulator of T cell responses in intracellular infection. J. Immunol. 158:800-806.
24. Chehimi. J., J.D. Marshall, O. Salvucci, I. Frank, S. Chehimi, S. Kawecki, D. Bacheller, S. Rifat, and S. Chouaib. 1997. IL-15 enhances immune functions during HIV infection. J. Immunol. 158:5978-5987.
25. Flamand, L., I. Stefanescu, and J. Menezes. 1996. Human herpesvirus-6 enhances natural killer cell cytotoxicity via IL-15. J. Clin. Invest. 97:1373-1381.
26. Atedzoe, B.N., A. Ahmad, and J. Menezes. 1997. Enhancement of natural killer cell cytotoxicity by the human herpesvirus-7 via IL-15 induction. J. Immunol. 159:4966-4972.
27. Kakumu, S., A. Okumura, T. Ishikawa, M. Yano, A. Enomoto, H. Nishimura, K. Yoshioka, and Y. Yoshikai. 1997. Serum levels of IL-10, IL-15 and soluble tumor necrosis factor-alpha (TNF-alpha) receptors in type C chronic liver disease. Clin. Exp. Immunol. 109:458-463.
28. McInnes, I.B., J. Al-Mughales, M. Field, B.P. Leung, F.-P. Huang, R. Dixon, R.D. Sturrock, P.C. Wilkinson, and F.Y. Liew. 1996. The role of interleukin 15 in T-cell migration and activation in rheumatoid arthritis. Nat. Med. 2:175-182.
29. McInnes, I.B., B.P., Leung, R.D. Sturrock, M. Field, and F.Y. Liew. 1997. Interleukin-15 meidates T cell-dependent regulation of tumor necrosis factor-α production in rheumatoid arthritis, Nat. Med. 3:189-195.
30. Kirman, I., and O.H. Nielsen. 1996. Increased numbers of interlcukin-15-expressing cells in active ulcerative colitis. Am. J. Gastroenteorl. 91:1789-1794.
31. Sakai, T., K. Kusugami, H. Nishimura, T. Ando, T. Yamaguchi, M. Ohsuga, K. Ina, A. Enomoto, Y. Kimura, and Y. Yoshikai. 1998. Interleukin 15 activity in the rectal mucosa of inflammatory bowel disease. Gastroenterology. 114: 1237-1243.
32. Gamero, A.M., D. Ussery, D.S. Reintgen, C.A. Puleo, and J.Y. Djeu. 1995. Interleukin 15 induction of lymphokine-activated killer cell function against autologous tumor cells in melanoma patient lymphocytes by a CD18-dependent, perforin-related mechanism, Cancer Res. 55:4988-4994.
33. Kimura, K., H. Nishimura, K. Hirose, T. Matsuguchi, Y. Nimura, and Y. Yoshikai. 1999. Immunogene therapy of murine fibrosarcoma using IL.-15 gene with high translation efficiency. Eur. J. Immunol. 29:1532-1542.
34. Nishimura, H., J. Washizu, N. Nakamura, A. Enomoto, and Y. Yoshikai. 1998. Translational efficiency is up-regulated by alternative exon in murine IL-15 mRNA. J. Immunol. 160: 936-942.
35. Meazza, R., S. Verdiani, R. Biassoni, M. Coppolecchia, A. Gaggero, A. Orengo, M.P. Colombo, B. Azzarone, and S. Ferrini. 1996. Identification of a novel interleukin-15 (IL-15) transcript isoform generated by alternative splicing in human small cell lung cancer cell lines. Oncogene. 12:2187-2192.
36. Onu, A., T. Pohl, H. Krause, and S. Bulfone-Paus. 1997. Regulation of IL-1.5 secretion via the leader peptide of two IL-15 isoform. J. Immunol. 158:255-262.
37. Tagaya, Y., G. Kurys, T.A. Thies, J.M. Losi, N. Azimi, J.A. Hanover, R.N. Bamford, and T.A. Waldmann. 1997. Generation oF secretable and non-secretable interleukin 15 isoforms through alternate usage of signal peptides. Proc. Natl. Acad. Sci. USA. 94:14444-14449.
38. Bamford, R.N., A.P. DeFilippis, N. Azimi, G. Kurys, and T.A. Waldmann. 1998. The 5′ untranslated region, signal peptide, and the cording sequence of the carboxyl terminus of IL-15 participate in its multifaceted translational control. J. Immunol. 160:4418-4426.
39. Anderson, D.M., L. Johnson, M.B. Glaccum, N.G. Copeland, D.J. Gilbert, N.A. Jenkins, V. Valentine, M.N. Kirstein, D.N. Shapiro, S. Morris, et al. 1995. Chromosomal assignment and genomic structure of II 15. Genomics. 25: 701-706.
40. Emoto, M., H. Danbara, and Y. Yoshikai. 1992. Induction of γ/δ T cells in murine salmonellosis by an avirulent but not a virulent strain of Salmonella choleraesus. J. Exp. Med. 176: 363-372.
41. + T cells. J. Exp. Med. 188:103-117
42. Bachmann, M.F., A. Gallimore, S. Linkert, V. Cerundolo, A. Lanzavecchia, M. Kopf, and A. Viola. 1999. Developmental regulation of lck targeting to the CD8 coreceptor controls signaling in naive and memory T cells. J. Exp. Med. 189: 1521-1529.
43. + T cells in vivo by IL-15. Immunity. 8:591-599.
44. + T cells producing IL-4 may be involved in the increased susceptibility of mice with the beige mutation during salmonella infection. J. Immunol 158: 2268-2277.
45. Doherty, P.C., W. Allan, M. Eichelberger, and S.R. Carding. 1992. Roles of alpha beta and gamma delta T cell subsets in viral immunity. Annu. Rev. Immunnol. 10:123-151.
46. Ahmed, R., and D. Gray. 1996. Immunological memory and protective immunity: understanding their relation. Science: 272:54-00.
47. Zinkernagel, R.M., M.F. Bachmann, T.M. Kundig, S. Oehen, H. Pircher, and H. Hengartner. 1996. On immunological memory. Annu. Rev. Immunol. 14:333-367.
48. Tough, D.F., P. Borrow, and J. Sprent. 1996. Induction of bystander T cell proliferation by virus and type I interferon in vivo. Science. 272:1947-1950.
49. Ehl, S., J. Hombach, P. Aichele, H. Hengartner, and R. Zinkemagel. 1997. Bystander activation of cytotoxic T cells: studies on the mechanism and evaluation of in vivo significance in a transgenic mouse model. J. Exp. Med. 185:1241-1251.
50. Zarozinski, C.C., and R.M. Welsh. 1997. Minimal bystander activation of CD8 T cells during the virus-induced polyclonal T cell response. J. Exp. Med. 185:1629-1639.
51. + T cells during an acute virus infection. Immunity. 8:167-175.
52. Murali-Krishna, K., J.D. Altman, M. Suresh, D.J.D. Sourdive, A.J. Zajac, J.D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity. 8:177-187.
53. Kaufmann, S.H.E. 1993. Immunity to intracellular bacteria. Annu. Rev. Immunol. 11:129-157.
54. Ramarathinam, L., D.W. Niesel, and G.R. Klimpel. 1993. Salmonella typhimurium induces IFN-γ production in murine splenocytes. J. Immunol. 150:3973-3979.
55. + T cell responses: the alternative approaches. Annu. Rev. Immunol. 15:297-322.
56. Murphy, K.M. 1998. T lymphocyte differentiation in the periphery. Curr. Opin. Immunol. 10:226-232.
57. Green, M.R. 1991. Biochemical mechanisms of constitutive and regulated pre-mRNA splicing. Annu. Rev. Cell Biol. 7:559-571.
58. Padgett, R.A., P.J. Graboswi, M.M. Konarska, S. Seiler, and P.A. Sharp. 1986. Splicing of messenger RNA precursor. Annu. Rev. Biochem. 55:1119-1133.
59. Smith, C.W., J.G. Patton, and B. Nadal-Ginard. 1989. Alternative splicing in the control of gene expression, Annu. Rev. Genet. 23:527-545.