Bcl-2 transgene expression promotes survival and reduces proliferation of CD3-CD4-CD8-T cell progenitors

International Immunology

Volumn 9, Issue 9, 1997, Pages 1291-1301

  O'Reilly, Lorraine A ^a   Harris, Alan W ^a   Strasser, Andreas ^a  

^a ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

Apoptosis; Cell cycle; Pro T cell; T lymphocyte development

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; HERMES ANTIGEN; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 7 RECEPTOR; PROTEIN BCL 2; STEM CELL FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ETIOLOGY; GENE EXPRESSION; GENE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL; T LYMPHOCYTE; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD3; ANTIGENS, CD4; ANTIGENS, CD8; CELL DIVISION; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENES, BCL-2; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, SCID; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTE SUBSETS; TRANSGENES;

EID: 0030879407     PISSN: 09538178     EISSN: None     Source Type: Journal    
DOI: 10.1093/intimm/9.9.1291     Document Type: Article

References (72)

1. von Boehmer, H. 1994. Positive selection of lymphocytes. Cell 76:219.
2. Shortrnan, K. and Wu, L. 1996 Early T lymphocyte progenitors. Annu. Rev. Immunol. 14:29.
3. Godfrey, D. I. and Zlotnik, A. 1993. Control points in early T-cell development. Immunol. Today 14:547.
4. Groettrup, M., Ungewiss, K., Azogui, O., Palacios, R., Owen, M. J., Mayday, A. C. and von Boehmer, H. 1993. A novel disulfidelinked heterodimer on pre-T cells consists of the T cell receptor β chain and a 33 kd glycoprotein. Cell 75:283.
5. Mombaerts, P., Clark, A. R., Rudnicki, M. A., lacomini, J., ltohara, S., Lafaille, J. J., Wang, L., Ichikawa, Y., Jaenisch, R., Hooper, M. L. and Tonegawa, S. 1992. Mutations in T-cell antigen receptor genes a and β block thymocyte development at different stages. Nature 360:225.
6. Mombaerts, P, Iacomini, J., Johnson, R. S., Herrup, K., Tonegawa, S. and Papaioannou, V. E. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869.
7. Shinkai, Y., Rathbun, G., Lam, K.-P., Oltz, E. M., Stewart, V., Mendelsohn, M., Charron, J., Datta, M., Young, F., Stall, A. M. and Alt, F. W. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangements. Cell 68:855.
8. Fehling, H. J., Krotkova, A., Saitnruf, C and Von Boehmer, H. 1995. Crucial role of the pre-T-cell receptor alpha gene in development of alpha-beta but not gamma-delta T cells. Nature 375:795.
9. Petrie, H. T., Livak, F., Schatz, D. G., Strasser, A., Crispe, N. I. and Shortman, K. 1993. Multiple rearangements in TCR-α chain genes maximize the production of useful thymocytes. J. Exp. Med. 178:615.
10. +) thymocytes in normal and genetically modified mice. J. Immunol. 154:5103.
11. Rodewald, H.-R., Kretzschmar, K., Swat, W. and Takeda, S. 1995. Intrathymically expressed c-kit ligand (stem cell factor) is a major factor driving expansion of very immature thymocytes in vivo. Immunity 3:313.
12. Mackarehtschian, K., Hardin, J. D., Moore, K. A., Boast, S., Goff, S. P and Lemischka, I. R. 1995. Targeted disruption of the flk2/flt3 gene leads to deficiencies in primitive hematopoietic progenitors. Immunity 3:147.
13. von Freeden-Jeffry, U., Vieira, P., Lucian, L. A., McNeil, T., Burdach, S, E. G. and Murray, R. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181:1519.
14. Peschon, J. J., Morrissey, P. J., Grabstein, K. H., Ramsdell, F. J., Maraskovsky, E., Gliniak, B. C., Park, L. S., Ziegler, S. F., Williams, D. E., Ware, C. B., Meyer, J. D. and Davison, B. L. 1994. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J. Exp. Med. 180:1955.
15. Egerton, M., Shortman, K, and Scollay, R. 1990. The kinetics of immature thymocyte development in vivo Int. Immunol. 2:501.
16. Surh, C. D. and Sprent, J. 1994. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:100.
17. Strasser, A. 1995. Life and death during lymphocyte development and function: evidence for two distinct killing mechanisms. Curr Opin. Immunol 7:228.
18. Kerr J. F. R., Wyllie, A. H, and Currie, A R. 1972 Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239.
19. Hengartner, M. O. and Horvitz, H. R. 1994. Programmed cell death in Caenorhabditis elegans. Curr Opin. Genet. Dev. 4:581.
20. Vaux, D. L and Strasser, A. 1996. The molecular biology of apoptosis. Proc. Natl Acad. Sci. USA 93:2239.
21. Cory, S. 1995. Regulation of lymphocyte survival by the BCL-2 gene family. Annu. Rev. Immunol. 13:513.
22. Korsmeyer, S. J. 1995. Regulators of cell death. Trends Genet. 11:101
23. + stage during positive selection and promotes thymocyte differentiation at several control points. Immunity 1:197.
24. Strasser, A., Harris, A. W., Von Boehmer, H. and Cory, S. 1994. Positive and negative selection of T cells in T cell receptor transgenic mice expressing a bcl-2 transgene. Proc. Natl Acad. Sci. USA 91:1376.
25. Sentman, C. L., Shutter, J. R., Hockenbery, D., Kanagawa, O. and Korsmeyer, S. J 1991. bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 67:879
26. Strasser, A., Harris, A. W. and Cory, S. 1991. Bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 67:889.
27. Mazel, S., Burtrum, D. and Petrie, H. T. 1996 Regulation of cell division cycle progression by bcl-2 expression: a potential mechanism for inhibition of programmed cell death. J. Exp. Med. 183:2219.
28. Borner, C. 1996. Diminished cell proliferation associated with the death-protective activity of Bcl-2. J. Biol. Chem. 271:12695.
29. Linette, G. P., Li, Y., Roth, K. and Korsmeyer, S. J. 1996. Cross talk between cell death and cell cycle progression: BCL-2 regulates NFAT-mediated activation. Proc. Natl Acad. Sci. USA 93:9545.
30. O'Reilly, L., Huang, D. C. S. and Strasser, A. 1996. The cell death inhibitor Bcl-2 and its homologues influence control of cell cycle entry. EMBO J. 15:6979.
31. Brady, H. J. M., Gil-Gómez, G., Kirberg, J, and Berns, A. J. M. 1996. Baxa perturbs T cell development and affects cell cycle entry of T cells. EMBO J. 15:6991.
32. Strasser, A., Harris. A, W., Vaux. D L., Webb, E, Bath, M, L., Adams, J. M and Cory, S. 1990. Abnormalities of the immune system induced by dysregulated bcl-2 expression in transgenic mice. Curr. Top. Microbiol Immunol 166:175.
33. Bosma, G. C., Custer, R. P. and Bcsma, M. J 1983. A severe combined immunodeficiency mutation in the mouse. Nature 301:527.
34. Strasser, A., Harris, A. W., Corcoran, L. M. and Cory, S, 1994. bcl-2 expression promotes B but not T lymphoid development in seid mice. Nature 368:457.
35. von Boehmer, H. 1990. Developmental biology of T cells in T cell-receptor transgenic mice. Annu. Rev. Immunol. 8:531.
36. Strasser, A., Harris, A. W., Huang, D. C. S., Krammer, P. H. and Cory, S, 1995. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 14:6136.
37. Förster, I., Vieira, P. and Rajewsky, K. 1989. Flow cytometric analysis of cell proliferation dynamics in the B cell compartment of the mouse. Int. Immunol. 1:321.
38. Fulcher, D A. and Basten, A. 1994 Reduced life span of anergic self-reactive B cells in a double-transgenic model. J. Exp. Med. 179:125.
39. Wu, L., Scollay, R., Egerton, M., Pearse, M., Spangrude, G. J. and Shortman, K. 1991. CD4 expressed on earliest T-lineage precursor cells in the adult murine thymus Nature 349:71.
40. Strasser, A. 1995. Bcl-2 and p53 interactions in apoptosis and cancer therapy. J. NIH Res. 7:48.
41. Pezzella, F., Tse, A. G. D., Cordell, J. L., Pulford, K. A. R., Gatter, K. C. and Mason, D. Y. 1990. Expression of the bcl-2 oncogene protein is not specific for the 14;18 chromosomal translocation. Am. J. Pathol 137:225.
42. Godfrey, D. I., Zlotnik, A. and Suda, T. 1992. Phenotypical and functional characterization of c-kit expression during intrathymic T cell development. J. Immunol. 149:2281.
43. Kishi, H., Borgulya, P., Scott, B., Karjalainen, K., Traunecker, A., Kaufman, J. and von Boehmer, H. 1991. Surface expression of the beta T cell receptor (TCR) chain in the absence of other TCR or CD3 proteins on immature T cells. EMBO J. 10:93.
44. Shinkai, Y., Koyasu, S., Nakayama, K.-I., Murphy, K. M., Loh, C. Y., Reinherz, E. L. and Alt, F. W. 1993. Restoration of T cell development in RAG-2-deficient mice by functional TCR transgenes. Science 259:822.
45. Cory, S., Strasser, A., Jacks, T., Corcoran, L. M., Metz, T., Harris, A. W. and Adams, J. M. 1994. Enhanced cell survival and tumorigenesis. Cold Spring Harbor Symp. Quant. Biol. 59:365.
46. Vairo, G., Innes, K. M. and Adams, J. M. 1996, Bcl-2 has a cell cycle inhibitory function separable from its enhancement of cell survival. Oncogene 13:1511.
47. Veis, D. J., Sentman, C. L., Bach, E, A. and Korsmeyer, S. J. 1993, Expression of the Bcl-2 protein in murine and human thymocytes and in peripheral T lymphocytes. J Immunol. 151:2546.
48. Gratiot-Deans, J., Merino, R., Nunez, G. and Turka, L. A. 1994. Bcl-2 expression during T-cell development: early loss and ate return occur at specific stages of commitment to differentiation and survival. Proc. Natl Acad. Sci. USA 91:10685,
49. Veis, D. J., Sorenson, C. M., Shutter, J. R. and Korsmeyer, S, J. 1993. Bcl-2-deficient mice demonstrate fulminant lyrnphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75:229.
50. Nakayama, K.-I., Nakayama, K., Izumi, N., Kulda, K., Shinkai, Y., Louie, M, C., Fields, L. E., Lucas, P. J., Stewart V., Alt, F. W. and Loh, D. Y. 1993. Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science 261:1884.
51. Nakayama, K.-I., Nakayama, K., Dustin, L. B. and Loh, D. Y. 1995. T-B cell interaction inhibits spontaneous apoptosis of mature lymphocytes in Bcl-2-deficient mice. J. Exp. Med. 182:1101.
52. Vanhaesebroeck, B., Reed, J. C., de Valck, D., Grooten, J., Miyashita, T., Tanaka, S., Beyaert, R., van Roy, F. and Fiers, W. 1993. Effect of bcl-2 proto-oncogene expression on cellular sensitivity to tumor necrosis factor-mediated cytotoxicity. Oncogene 8:1075.
53. Memon, S. A., Moreno, M. B., Petrak, D. and Zacharchuk, C. M. 1995. Bcl-2 blocks glucocorticoid- but not Fas- or activation-induced apoptosis in a T cell hybridoma. J. Immunol. 115:4644.
54. Chinnaiyan, A. M., Orth, K., O'Rourke, K., Duan H., Poirier, G. G. and Dixit, V. M. 1996 Molecular ordering of the cel death pathway. J. Biol. Chem. 271:4573.
55. O'Reilly, L. A., Harris, A. W., Tarlinton, D. M., Corcoran, L. M. and Strasser, A. 1997. Expression of a bcl-2 transgene reduces proliferation and slows turnover of developing B cells in vivo. J. Immunol., in press.
56. Motoyama, N., Wang, F. P., Roth, K. A., Sawa. H., Nakayama, K., Nakayama, K., Negishi, I., Senju, S., Zhang, Q., Fujii, S. and Loh, D. Y. 1995. Massive cell death of immature hematopoietic cells and neurons in Bcl-x deficient mice. Science 267:1506.
57. Vaux, D. L., Haecker, G. and Strasser, A. 1994. An evolutionary perspective on apoptosis. Cell 76:777.
58. Shaham, S. and Horvitz, H. R. 1996. Developing Caenorhabditis elegans neurons may contain both cell-death protective and killer activities. Genes Dev. 10:578.
59. Kumar, S. and Lavin, M. F. 1996. The ICE family of cysteine proteases as effectors of cell death. Cell Death Different. 3:255.
60. Huang, D, C. S., O'Reilly, L, A., Strasser, A. and Cory, S. 1997. The anti-apoptosis function of Bcl-2 can be genetically separated from its inhibitory effect on cell cycle entry EMBO J., in press.
61. Theodorakis, P., D'Sa-Eipper, C., Subramanian, T. and Chinnadurai, G. 1996. Unmasking of a proliferation-restraining activity of the anti-apoptosis protein EBV BHRF1. Oncogene 12:1707.
62. Uhlmann, E. J., D'Sa-Eipper, C., Subramanian, T., Wagner, A. J., Hay, N. and Chinnadurai, G. 1996. Deletion of a nonconserved region of Bcl-2 confers a novel gain of function: suppression of apoptosis with concomitant cell proliferation. Cancer Res. 56:2506.
63. White, E. 1996. Life, death, and the pursuit of apoptosis. Genes Dev. 10:1.
64. L. Nature 379:554.
65. Borner, C., Martinou, I., Mattmann, C., Irmler, M., Schaerer E., Martinou, J.-C. and Tschopp, J. 1994. The protein bcl-2α does not require membrane attachment, but two conserved domains to suppress apoptosis. J. Cell Biol. 126:1059.
66. Oltvai, Z. N. and Korsmeyer, S. J. 1994. Checkpoints of dueling dimers foil death wishes. Cell 79:189.
67. McDonnell, T. J. and Korsmeyer, S. J. 1991. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14;18). Nature 349:254.
68. μ-bcl-2 transgene facilitates spontaneous transformation of early pre-B and immunoglobu in-secreting cells but not T cells, Oncogene 8:1.
69. Linette, G. P., Hess, J. L., Sentman, C. L. and Korsmeyer. S. J. 1995. Peripheral T-cell lymphoma in lckpr-bcl-2 transgenic mice. Blood 86:1255.
70. Cleary, M. and Rosenberg, S. A. 1990. The bcl-2 gene, follicular lymphoma, and Hodgkin's disease. J. Natl Cancer Inst. 82:808.
71. Strasser, A., Harris, A. W., Bath, M. L. and Gory, S. 1990. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 348:331.
72. Acton, D., Domen, J., Jacobs, H., Vlaar, M., Korsmeyer, S. and Berns, A. 1992. Collaboration of PIM-1 and BCL-2 in lymphomagenesis. Curr. Top. Microbiol Immunol. 182:293.