MCL1 increases primitive thymocyte viability in female mice and promotes thymic expansion into adulthood

International Immunology

Volumn 23, Issue 10, 2011, Pages 647-659

  Gui, Jingang ^a   Morales, Amanda J ^a   Maxey, Sophie E ^a   Bessette, Katherine A ^b   Ratcliffe, Nora R ^b   Kelly, John A ^b   Craig, Ruth W ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b VA MEDICAL CENTER   (United States)

Author keywords

Double negative; Early T cell progenitor; MCL1; Radioresistance; Thymus; Viability

Indexed keywords

PROTEIN MCL 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL EXPANSION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; EARLY T CELL PROGENITOR; FEMALE; GAMMA IRRADIATION; GENE EXPRESSION; HEMATOPOIESIS; INVOLUTION; MALE; MOUSE; NONHUMAN; PRE T LYMPHOCYTE; PRIORITY JOURNAL; THYMOCYTE; THYMOPOIESIS; THYMUS; THYMUS ENLARGEMENT; WESTERN BLOTTING;

ANIMALS; CELL SURVIVAL; FEMALE; HUMANS; MALE; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-BCL-2; T-LYMPHOCYTES; THYMOCYTES; THYMUS GLAND; WHOLE-BODY IRRADIATION;

EID: 80053448448     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxr073     Document Type: Article

References (77)

1. Hernandez, J. B., Newton, R. H. and Walsh, C. M. 2010. Life and death in the thymus-cell death signaling during T cell development. Curr. Opin. Cell Biol. 22:865.
2. Balciunaite, G., Ceredig, R. and Rolink, A. G. 2005. The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential. Blood 105:1930.
3. Min, H., Montecino-Rodriguez, E. and Dorshkind, K. 2004. Reduction in the developmental potential of intrathymic T cell progenitors with age. J. Immunol. 173:245.
4. Heng, T. S., Goldberg, G. L., Gray, D. H., Sutherland, J. S., Chidgey, A. P. and Boyd, R. L. 2005. Effects of castration on thymocyte development in two different models of thymic involution. J. Immunol. 175:2982.
5. Allman, D., Sambandam, A., Kim, S. et al. 2003. Thymopoiesis independent of common lymphoid progenitors. Nat. Immunol. 4:168.
6. Shortman, K. and Wu, L. 1996. Early T lymphocyte progenitors. Annu. Rev. Immunol. 14:29.
7. Benz, C., Martins, V. C., Radtke, F. and Bleul, C. C. 2008. The stream of precursors that colonizes the thymus proceeds selectively through the early T lineage precursor stage of T cell development. J. Exp. Med. 205:1187.
8. Akashi, K. 2009. Lymphoid lineage fate decision of hematopoietic stem cells. Ann. N. Y. Acad. Sci. 1176:18.
9. Saran, N., Lyszkiewicz, M., Pommerencke, J. et al. 2010. Multiple extrathymic precursors contribute to T-cell development with different kinetics. Blood 115:1137.
10. Dominguez-Gerpe, L. and Rey-Mendez, M. 2003. Evolution of the thymus size in response to physiological and random events throughout life. Microsc. Res. Tech. 62:464.
11. Maue, A. C., Yager, E. J., Swain, S. L., Woodland, D. L., Blackman, M. A. and Haynes, L. 2009. T-cell immunosenescence: lessons learned from mouse models of aging. Trends Immunol. 30:301.
12. Hale, J. S., Boursalian, T. E., Turk, G. L. and Fink, P. J. 2006. Thymic output in aged mice. Proc. Natl Acad. Sci. USA 103:8447.
13. Dorshkind, K. and Swain, S. 2009. Age-associated declines in immune system development and function: causes, consequences, and reversal. Curr. Opin. Immunol. 21:404.
14. Hollander, G. A., Krenger, W. and Blazar, B. R. 2010. Emerging strategies to boost thymic function. Curr. Opin. Pharmacol. 10:443.
15. Lee, D. K., Hakim, F. T. and Gress, R. E. 2010. The thymus and the immune system: layered levels of control. J. Thorac. Oncol. 5:S273.
16. Chidgey, A. P., Seach, N., Dudakov, J., Hammett, M. V. and Boyd, R. L. 2008. Strategies for reconstituting and boosting T cellbased immunity following haematopoietic stem cell transplantation: pre-clinical and clinical approaches. Semin. Immunopathol. 30:457.
17. Aspinall, R., Pido-Lopez, J., Imami, N. et al. 2007. Old rhesus macaques treated with interleukin-7 show increased TREC levels and respond well to influenza vaccination. Rejuvenation Res. 10:5-17.
18. Alpdogan, O., Muriglan, S. J., Eng, J. M. et al. 2003. IL-7 enhances peripheral T cell reconstitution after allogeneic hematopoietic stem cell transplantation. J. Clin. Invest. 112:1095.
19. Guimond, M., Leonard, W. J., Spolsk, R. et al. 2008. Thymic stromal lymphopoietin is not necessary or sufficient to mediate the thymopoietic effects of keratinocyte growth factor. Blood 111:969.
20. Williams, K. M., Lucas, P. J., Bare, C. V. et al. 2008. CCL25 increases thymopoiesis after androgen withdrawal. Blood 112:3255.
21. Goldberg, G. L., Dudakov, J. A., Reiseger, J. J. et al. 2010. Sex steroid ablation enhances immune reconstitution following cytotoxic antineoplastic therapy in young mice. J. Immunol. 184:6014.
22. Kelly, R. M., Highfill, S. L., Panoskaltsis-Mortari, A. et al. 2008. Keratinocyte growth factor and androgen blockade work in concert to protect against conditioning regimen-induced thymic epithelial damage and enhance T-cell reconstitution after murine bone marrow transplantation. Blood 111:5734.
23. Olsen, N. J. and Kovacs, W. J. 2011. Evidence that androgens modulate human thymic T cell output. J. Investig. Med. 59:32.
24. Hince, M., Sakkal, S., Vlahos, K., Dudakov, J., Boyd, R. and Chidgey, A. 2008. The role of sex steroids and gonadectomy in the control of thymic involution. Cell. Immunol. 252:122.
25. Penit, C. and Ezine, S. 1989. Cell proliferation and thymocyte subset reconstitution in sublethally irradiated mice: compared kinetics of endogenous and intrathymically transferred progenitors. Proc. Natl Acad. Sci. USA 86:5547.
26. Penit, C. and Vasseur, F. 1988. Sequential events in thymocyte differentiation and thymus regeneration revealed by a combination of bromodeoxyuridine DNA labeling and antimitotic drug treatment. J. Immunol. 140:3315.
27. Bosco, N., Swee, L. K., Benard, A., Ceredig, R. and Rolink, A. 2010 Auto-reconstitution of the T-cell compartment by radioresistant hematopoietic cells following lethal irradiation and bone marrow transplantation. Exp. Hematol. 38:222.
28. Kozopas, K. M., Yang, T., Buchan, H. L., Zhou, P. and Craig, R. W. 1993 MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL-2. Proc. Natl Acad. Sci. USA 90:3516.
29. Opferman, J. T., Iwasaki, H., Ong, C. C. et al. 2005. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307:1101.
30. Opferman, J. T., Letai, A., Beard, C., Sorcinelli, M. D., Ong, C. C. and Korsmeyer, S. J. 2003. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426:671.
31. Craig, R. W. 2002. MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation, and tumorigenesis. Leukemia 16:444.
32. Dzhagalov, I., Dunkle, A. and He, Y. W. 2008. The anti-apoptotic Bcl-2 family member Mcl-1 promotes T lymphocyte survival at multiple stages. J. Immunol. 181:521.
33. Zhou, P., Qian, L., Bieszczad, C. K. et al. 1998. Mcl1 in transgenic mice promotes survival in a spectrum of hematopoietic cell types and immortalization in the myeloid lineage. Blood 92:3226.
34. Zhou, P., Xie, H., Qian, L. et al. 2001. MCL1 transgenic mice exhibit a high incidence of B cell lymphoma manifested as a spectrum of histologic subtypes. Blood 97:3902.
35. Zhou, P., Qian, L., Kozopas, K. M. and Craig, R. W. 1997. Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood 89:630.
36. Irla, M., Hugues, S., Gill, J. et al. 2008. Autoantigen-specific interactions with CD4+ thymocytes control mature medullary thymic epithelial cell cellularity. Immunity 29:451.
37. Sempowski, G. D., Gooding, M. E., Liao, H. X., Le, P. T. and Haynes, B. F. 2002. T cell receptor excision circle assessment of thymopoiesis in aging mice. Mol. Immunol. 38:841.
38. Rothaeusler, K. and Baumgarth, N. 2006. Evaluation of intranuclear BrdU detection procedures for use in multicolor flow cytometry. Cytometry A 69:249.
39. Gui, J., Zhu, X., Dohkan, J., Cheng, L., Barnes, P. F. and Su, D. M. 2007 The aged thymus shows normal recruitment of lymphohematopoietic progenitors but has defects in thymic epithelial cells. Int. Immunol. 19:1201.
40. Goldstein, A. 1964. Biostatistics, an Introductory Text. MacMillan Publishing Co., Inc., New York.
41. De Biasio, A., Vrana, J. A., Zhou, P. et al. 2007. N-terminal truncation of antiapoptotic MCL1, but not G2/M-induced phosphorylation, is associated with stabilization and abundant expression in tumor cells. J. Biol. Chem. 282:23919.
42. Rubtsov, A. V., Rubtsova, K., Kappler, J. W. and Marrack, P. 2010. Genetic and hormonal factors in female-biased autoimmunity. Autoimmun. Rev. 9:494.
43. Lustig, A., Carter, A., Bertak, D. et al. 2009. Transcriptome analysis of murine thymocytes reveals age-associated changes in thymic gene expression. Int. J. Med. Sci. 6:51.
44. Lustig, A., Weeraratna, A. T., Wood, W. W. et al. 2007. Transcriptome analysis of age-, gender- and diet-associated changes in murine thymus. Cell Immunol. 245:42.
45. Olsen, N. J., Olson, G., Viselli, S. M., Gu, X. and Kovacs, W. J. 2001 Androgen receptors in thymic epithelium modulate thymus size and thymocyte development. Endocrinology 142:1278.
46. Fujise, K., Zhang, D., Liu, J. and Yeh, E. T. 2000. Regulation of apoptosis and cell cycle progression by MCL1. Differential role of proliferating cell nuclear antigen. J. Biol. Chem. 275:39458.
47. Dulude, G., Cheynier, R., Gauchat, D. et al. 2008. The magnitude of thymic output is genetically determined through controlled intrathymic precursor T cell proliferation. J. Immunol. 181:7818.
48. Rothenberg, E. V., Moore, J. E. and Yui, M. A. 2008. Launching the T-cell-lineage developmental programme. Nat. Rev. Immunol. 8:9.
49. Gossens, K., Naus, S., Corbel, S. Y. et al. 2009. Thymic progenitor homing and lymphocyte homeostasis are linked via S1Pcontrolled expression of thymic P-selectin/CCL25. J. Exp. Med. 206:761.
50. Lee, P. P., Fitzpatrick, D. R., Beard, C. et al. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15:763.
51. Yang, C. Y., Lin, N. H., Lee, J. M. et al. 2009. Promoter knock-in mutations reveal a role of Mcl-1 in thymocyte-positive selection and tissue or cell lineage-specific regulation of Mcl-1 expression. J. Immunol. 182:2959.
52. Campbell, K. J., Bath, M. L., Turner, M. L. et al. 2010. Elevated Mcl-1 perturbs lymphopoiesis, promotes transformation of hematopoietic stem/progenitor cells, and enhances drug resistance. Blood 116:3197.
53. Ogilvy, S., Metcalf, D., Print, C. G., Bath, M. L., Harris, A. W. and Adams, J. M. 1999. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc. Natl Acad. Sci. USA 96:14943.
54. Min, H., Montecino-Rodriguez, E. and Dorshkind, K. 2005. Effects of aging on early B- and T-cell development. Immunol. Rev. 205:7.
55. Sutherland, J. S., Goldberg, G. L., Hammett, M. V. et al. 2005. Activation of thymic regeneration in mice and humans following androgen blockade. J. Immunol. 175:2741.
56. Rossi, F. M., Corbel, S. Y., Merzaban, J. S. et al. 2011. Recruitment of adult thymic progenitors is regulated by P-selectin and its ligand PSGL-1. Nat. Immunol. 6:626.
57. Shen, H., Yu, H., Liang, P. H. et al. 2011. Bid is a positive regulator for donor-derived lymphoid cell regeneration in gamma-irradiated recipients. Exp. Hematol. 39:947.
58. van Ewijk, W., Hollander, G., Terhorst, C. and Wang, B. 2000. Stepwise development of thymic microenvironments in vivo is regulated by thymocyte subsets. Development 127:1583.
59. Shakib, S., Desanti, G. E., Jenkinson, W. E., Parnell, S. M., Jenkinson, E. J. and Anderson, G. 2009. Checkpoints in the development of thymic cortical epithelial cells. J. Immunol. 182:130.
60. Roberts, N. A., Desanti, G. E., Withers, D. R. et al. 2009. Absence of thymus crosstalk in the fetus does not preclude hematopoietic induction of a functional thymus in the adult. Eur. J. Immunol. 39:2395.
61. Jenkinson, W. E., Bacon, A., White, A. J., Anderson, G. and Jenkinson, E. J. 2008. An epithelial progenitor pool regulates thymus growth. J. Immunol. 181:6101.
62. Strasser, A., Harris, A. W. and Cory, S. 1991. bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 67:889.
63. 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.
64. Zhang, N., Hartig, H., Dzhagalov, I., Draper, D. and He, Y. W. 2005 The role of apoptosis in the development and function of T lymphocytes. Cell Res. 15:749.
65. Opferman, J. T. 2008. Apoptosis in the development of the immune system. Cell Death Differ. 15:234.
66. von Freeden-Jeffry, U., Solvason, N., Howard, M. and Murray, R. 1997 The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity 7:147.
67. Kondo, M., Akashi, K., Dome, J., Sugamura, K. and Weissman, I. L. 1997 Bcl-2 rescues T lymphopoiesis, but not B or NK cell development, in common gamma chain-deficient mice. Immunity 7:155.
68. Maraskovsky, E., O'Reilly, L. A., Teepe, M., Corcoran, L. M., Peschon, J. J. and Strasser, A. 1997. Bcl-2 can rescue T lymphocyte development in interleukin-7 receptor-deficient mice but not in mutant rag-1-/- mice. Cell 89:1011.
69. Veis, D. J., Sorenson, C. M., Shutter, J. R. and Korsmeyer, S. J. 1993 Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75:229.
70. Kelly, P. N., White, M. J., Goschnick, M. W. et al. 2010. Individual and overlapping roles of BH3-only proteins Bim and Bad in apoptosis of lymphocytes and platelets and in suppression of thymic lymphoma development. Cell Death Differ. 17:1655.
71. Biswas, S., Shi, Q., Matise, L., Cleveland, S., Dave, U. and Zinkel, S. 2010 A role for proapoptotic Bax and Bak in T-cell differentiation and transformation. Blood 116:5237.
72. Rathmell, J. C., Lindsten, T., Zong, W. X., Cinalli, R. M. and Thompson, C. B. 2002. Deficiency in Bak and Bax perturbs thymic selection and lymphoid homeostasis. Nat. Immunol. 3:932.
73. Wei, M. C., Zong, W. X., Cheng, E. H. et al. 2001. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727.
74. Pellegrini, M., Bouillet, P., Robati, M., Belz, G. T., Davey, G. M. and Strasser, A. 2004. Loss of Bim increases T cell production and function in interleukin 7 receptor-deficient mice. J. Exp. Med. 200:1189.
75. Bouillet, P., Purton, J. F., Godfrey, D. I. et al. 2002. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature 415:922.
76. Arbour, N., Vanderluit, J. L., Le Grand, J. N. et al. 2008. Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J. Neurosci. 28:6068.
77. Sitailo, L. A., Jerome-Morais, A. and Denning, M. F. 2009. Mcl-1 functions as major epidermal survival protein required for proper keratinocyte differentiation. J. Invest. Dermatol. 129:1351.