Sex steroid ablation enhances hematopoietic recovery following cytotoxic antineoplastic therapy in aged mice

Journal of Immunology

Volumn 183, Issue 11, 2009, Pages 7084-7094

  Dudakov, Jarrod A ^a   Goldberg, Gabrielle L ^a,b   Reiseger, Jessica J ^a   Vlahos, Katerina ^a   Chidgey, Ann P ^a   Boyd, Richard L ^a  

^a MONASH UNIVERSITY   (Australia)

^b BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; SEX HORMONE; ANTINEOPLASTIC AGENT;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BONE MARROW; CASTRATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; HEMATOPOIESIS; LYMPHOID PROGENITOR CELL; LYMPHOPOIESIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; THYMUS; AGING; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CYTOLOGY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; PHYSIOLOGY; T LYMPHOCYTE;

AGING; ANIMALS; ANTINEOPLASTIC AGENTS; BONE MARROW; BONE MARROW CELLS; CASTRATION; CYCLOPHOSPHAMIDE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GONADAL STEROID HORMONES; HEMATOPOIETIC STEM CELLS; LYMPHOPOIESIS; MALE; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES; THYMUS GLAND;

EID: 73349136289     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900196     Document Type: Article

References (79)

1. Mackall, C. L., T. A. Fleisher, M. R. Brown, I. T. Magrath, A. T. Shad, M. E. Horowitz, L. H. Wexler, M. A. Adde, L. L. McClure, and R. E. Gress. 1994. Lymphocyte depletion during treatment with intensive chemotherapy for cancer. Blood 84: 2221-2228. (Pubitemid 24296382)
2. Pizzo, P. A., M. Rubin, A. Freifeld, and T. J. Walsh. 1991. The child with cancer and infection. II. Nonbacterial infections. J Pediatr. 119: 845-857.
3. Mackall, C. L. 2000. T-cell immunodeficiency following cytotoxic antineoplastic therapy: a review. Stem Cells 18: 10-18.
4. Hakim, F. T., and R. E. Gress. 2005. Reconstitution of the lymphocyte compartment after lymphocyte depletion: a key issue in clinical immunology. Eur. J. Immunol. 35: 3099-3102.
5. Hakim, F. T., S. A. Memon, R. Cepeda, E. C. Jones, C. K. Chow, C. Kasten-Sportes, J. Odom, B. A. Vance, B. L. Christensen, C. L. Mackall, and R. E. Gress. 2005. Age-dependent incidence, time course, and consequences of thymic renewal in adults. J. Clin. Invest. 115: 930-939.
6. Miller, J. P., and D. Allman. 2003. The decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors. J. Immunol. 171: 2326-2330.
7. Min, H., E. Montecino-Rodriguez, and K. Dorshkind. 2006. Effects of aging on the common lymphoid progenitor to pro-B cell transition. J. Immunol. 176: 1007-1012. (Pubitemid 43099700)
8. Allman, D., and J. P. Miller. 2005. The aging of early B-cell precursors. Immunol. Rev. 205: 18-29.
9. Stephan, R. P., D. A. Lill-Elghanian, and P. L. Witte. 1997. Development of B cells in aged mice: decline in the ability of pro-B cells to respond to IL-7 but not to other growth factors. J. Immunol. 158: 1598-1609.
10. Ben-Yehuda, A., P. Szabo, R. Dyall, and M. E. Weksler. 1994. Bone marrow declines as a site of B-cell precursor differentiation with age: relationship to thymus involution. Proc. Natl. Acad. Sci. USA 91: 11988-11992.
11. Johnson, K. M., K. Owen, and P. L. Witte. 2002. Aging and developmental transitions in the B cell lineage. Int. Immunol. 14: 1313-1323.
12. Kline, G. H., T. A. Hayden, and N. R. Klinman. 1999. B cell maintenance in aged mice reflects both increased B cell longevity and decreased B cell generation. J. Immunol. 162: 3342-3349.
13. Szabo, P., S. Shen, W. Telford, and M. E. Weksler. 2003. Impaired rearrangement of IgH V to DJ segments in bone marrow Pro-B cells from old mice. Cell Immunol. 222: 78-87. (Pubitemid 36683127)
14. Kirman, I., K. Zhao, Y. Wang, P. Szabo, W. Telford, and M. E. Weksler. 1998. Increased apoptosis of bone marrow pre-B cells in old mice associated with their low number. Int. Immunol. 10: 1385-1392. (Pubitemid 28414344)
15. Yu, W., H. Nagaoka, M. Jankovic, Z. Misulovin, H. Suh, A. Rolink, F. Melchers, E. Meffre, and M. C. Nussenzweig. 1999. Continued RAG expression in late stages of B cell development and no apparent re-induction after immunization. Nature 400: 682-687. (Pubitemid 129516184)
16. Allman, D., and J. P. Miller. 2005. B cell development and receptor diversity during aging. Curr. Opin. Immunol. 17: 463-467. (Pubitemid 41207947)
17. Weksler, M. E., M. Goodhardt, and P. Szabo. 2002. The effect of age on B cell development and humoral immunity. Springer Semin. Immunopathol. 24: 35-52.
18. Weksler, M. E., and P. Szabo. 2000. The effect of age on the B-cell repertoire. J Clin. Immunol. 20: 240-249.
19. Gibson, K. L., Y. C. Wu, Y. Barnett, O. Duggan, R. Vaughan, E. Kondeatis, B. O. Nilsson, A. Wikby, D. Kipling, and D. K. Dunn-Walters. 2009. B-cell diversity decreases in old age and is correlated with poor health status. Aging Cell 8: 18-25.
20. Siegrist, C.-A., and R. Aspinall. 2009. B-cell responses to vaccination at the extremes of age. Nat. Rev. Immunol. 9: 185-194.
21. George, A. J., and M. A. Ritter. 1996. Thymic involution with ageing: obsolescence or good housekeeping? Immunol. Today. 17: 267-272.
22. Aspinall, R., and D. Andrew. 2000. Thymic involution in aging. J Clin. Immunol. 20: 250-256.
23. Douek, D. C., R. D. McFarland, P. H. Keiser, E. A. Gage, J. M. Massey, B. F. Haynes, M. A. Polis, A. T. Haase, M. B. Feinberg, J. L. Sullivan, et al. 1998. Changes in thymic function with age and during the treatment of HIV infection. Nature 396: 690-695.
24. Sutherland, J. S., G. L. Goldberg, M. V. Hammett, A. P. Uldrich, S. P. Berzins, T. S. Heng, B. R. Blazar, J. L. Millar, M. A. Malin, A. P. Chidgey, and R. L. Boyd. 2005. Activation of thymic regeneration in mice and humans following androgen blockade. J. Immunol. 175: 2741-2753.
25. Berzins, S. P., A. P. Uldrich, J. S. Sutherland, J. Gill, J. F. Miller, D. I. Godfrey, and R. L. Boyd. 2002. Thymic regeneration: teaching an old immune system new tricks. Trends Mol. Med. 8: 469-476.
26. Mosley, R. L., M. M. Koker, and R. A. Miller. 1998. Idiosyncratic alterations of TCR size distributions affecting both CD4 and CD8 T cell subsets in aging mice. Cell Immunol. 189: 10-18.
27. LeMaoult, J., I. Messaoudi, J. S. Manavalan, H. Potvin, D. Nikolich-Zugich, R. Dyall, P. Szabo, M. E. Weksler, and J. Nikolich-Zugich. 2000. Age-related dysregulation in CD8 T cell homeostasis: kinetics of a diversity loss. J. Immunol. 165: 2367-2373.
28. Dorshkind, K., E. Montecino-Rodriguez, and R. A. J. Signer. 2009. The ageing immune system: is it ever too old to become young again? Nat. Rev. Immunol. 9: 57-62.
29. Haynes, L., and S. L. Swain. 2006. Why Aging T Cells Fail: Implications for Vaccination. Immunity 24: 663-666. (Pubitemid 43867372)
30. Nikolich-Zugich, J. 2008. Ageing and life-long maintenance of T-cell subsets in the face of latent persistent infections. Nat. Rev. Immunol. 8: 512-522. (Pubitemid 351913675)
31. Effros, R. B. 2007. Role of T lymphocyte replicative senescence in vaccine efficacy. Vaccine 25: 599-604.
32. Haynes, L., and A. C. Maue. 2009. Effects of aging on T cell function. Curr. Opin. Immunol. 21: 414-417.
33. Brock, N. 1996. The history of the oxazaphosphorine cytostatics. Cancer. 78: 542-547.
34. Zitvogel, L., L. Apetoh, F. Ghiringhelli, and G. Kroemer. 2008. Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol. 8: 59-73.
35. + T-lymphocyte regeneration after intensive chemotherapy. N. Engl. J. Med. 332: 143-149.
36. Storek, J., R. P. Witherspoon, and R. Storb. 1995. T cell reconstitution after bone marrow transplantation into adult patients does not resemble T cell development in early life. Bone Marrow Transplant. 16: 413-425.
37. Weinberg, K., G. Annett, A. Kashyap, C. Lenarsky, S. J. Forman, and R. Parkman. 1995. The effect of thymic function on immunocompetence following bone marrow transplantation. Biol. Blood Marrow Transplant. 1: 18-23.
38. + T-cell regenerative pathways result in prolonged T-cell subset imbalance after intensive chemotherapy. Blood 89: 3700-3707.
39. + subset reveals multiple homeostatic T-cell compartments with distinct implications for immune competence. Immunology 106: 27-37.
40. Sfikakis, P. P., G. M. Gourgoulis, L. A. Moulopoulos, G. Kouvatseas, A. N. Theofilopoulos, and M. A. Dimopoulos. 2005. Age-related thymic activity in adults following chemotherapy-induced lymphopenia. Eur J. Clin. Invest. 35: 380-387.
41. Balducci, L., H. Al-Halawani, V. Charu, J. Tam, S. Shahin, L. Dreiling, and W. B. Ershler. 2007. Elderly cancer patients receiving chemotherapy benefit from first-cycle pegfilgrastim. Oncologist 12: 1416-1424.
42. Balducci, L. 2003. Myelosuppression and its consequences in elderly patients with cancer. Oncology 17: 27-32. (Pubitemid 37493953)
43. Li, F., F. Jin, A. Freitas, P. Szabo, and M. E. Weksler. 2001. Impaired regeneration of the peripheral B cell repertoire from bone marrow following lymphopenia in old mice. Eur. J. Immunol. 31: 500-505. (Pubitemid 32166605)
44. Gardner, R. V., E. McKinnon, and C. M. Astle. 2001. Analysis of the stem cell sparing properties of cyclophosphamide. Eur J Haematol. 67: 14-22. (Pubitemid 32769810)
45. Gardner, R. V., R. Begue, and E. McKinnon. 2001. The effect of granulocytemacrophage colony-stimulating factor (GM-CSF) on primitive hematopoietic stem cell (PHSC) function and numbers, after chemotherapy. Exp. Hematol. 29: 1053-1059.
46. Offner, F., T. Kerre, M. De Smedt, and J. Plum. 1999. Bone marrow CD34 cells generate fewer T cells in vitro with increasing age and following chemotherapy. Br. J. Haematol. 104: 801-808. (Pubitemid 29143501)
47. Clutter, S. D., J. E. Fortney, and L. F. Gibson. 2006. Chemotherapy disrupts activity of translational regulatory proteins in bone marrow stromal cells. Exp. Hematol. 34: 1522-1531.
48. Olsen, N. J., X. Gu, and W. J. Kovacs. 2001. Bone marrow stromal cells mediate androgenic suppression of B lymphocyte development. J. Clin. Invest. 108: 1697-1704.
49. Olsen, N. J., and W. J. Kovacs. 1996. Gonadal steroids and immunity. Endocr. Rev. 17: 369-384.
50. Olsen, N. J., and W. J. Kovacs. 2001. Effects of androgens on T and B lymphocyte development. Immunol. Res. 23: 281-288.
51. Kincade, P. W., K. L. Medina, and G. Smithson. 1994. Sex hormones as negative regulators of lymphopoiesis. Immunol. Rev. 137: 119-134.
52. Gray, D. H., T. Ueno, A. P. Chidgey, M. Malin, G. L. Goldberg, Y. Takahama, and R. L. Boyd. 2005. Controlling the thymic microenvironment. Curr. Opin. Immunol. 17: 137-143.
53. Fitzpatrick, F. T., M. D. Kendall, M. J. Wheeler, I. M. Adcock, and B. D. Greenstein. 1985. Reappearance of thymus of ageing rats after orchidectomy. J Endocrinol. 106: R17-R19.
54. Greenstein, B. D., F. T. Fitzpatrick, I. M. Adcock, M. D. Kendall, and M. J. Wheeler. 1986. Reappearance of the thymus in old rats after orchidectomy: inhibition of regeneration by testosterone. J. Endocrinol. 110: 417-422.
55. Dudakov, J. A., G. L. Goldberg, J. J. Reiseger, A. P. Chidgey, and R. L. Boyd. 2009. Withdrawal of sex steroids reverses age- and chemotherapy-related defects in bone marrow lymphopoiesis. J. Immunol. 182: 6247-6260.
56. Goldberg, G. L., O. Alpdogan, S. J. Muriglan, M. V. Hammett, M. K. Milton, J. M. Eng, V. M. Hubbard, A. Kochman, L. M. Willis, A. S. Greenberg, et al. 2007. Enhanced immune reconstitution by sex steroid ablation following allogeneic hemopoietic stem cell transplantation. J. Immunol. 178: 7473-7484.
57. Goldberg, G. L., J. S. Sutherland, M. V. Hammet, M. K. Milton, T. S. Heng, A. P. Chidgey, and R. L. Boyd. 2005. Sex steroid ablation enhances lymphoid recovery following autologous hematopoietic stem cell transplantation. Transplantation 80: 1604-1613.
58. Goldberg, G. L., C. G. King, R. A. Nejat, D. Y. Suh, O. M. Smith, J. C. Bretz, R. M. Samstein, J. A. Dudakov, A. P. Chidgey, S. Chen-Kiang, et al. 2009. Luteinizing hormone-releasing hormone enhances T cell recovery following allogeneic bone marrow transplantation. J. Immunol. 182: 5846-5854.
59. Heng, T. S., G. L. Goldberg, D. H. Gray, J. S. Sutherland, A. P. Chidgey, and R. L. Boyd. 2005. Effects of castration on thymocyte development in two different models of thymic involution. J. Immunol. 175: 2982-2993.
60. Porritt, H. E., L. L. Rumfelt, S. Tabrizifard, T. M. Schmitt, J. C. Zuniga-Pflucker, and H. T. Petrie. 2004. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 20: 735-745.
61. + stem cell compartment is accompanied by loss of self-renewal capacity. Immunity 15: 659-669.
62. Osawa, M., K. Hanada, H. Hamada, and H. Nakauchi. 1996. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273: 242-245. (Pubitemid 26285891)
63. Morrison, S. J., A. M. Wandycz, H. D. Hemmati, D. E. Wright, and I. L. Weissman. 1997. Identification of a lineage of multipotent hematopoietic progenitors. Development 124: 1929-1939.
64. - short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood 105: 2717-2723.
65. Igarashi, H., S. C. Gregory, T. Yokota, N. Sakaguchi, and P. W. Kincade. 2002. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 17: 117-130. (Pubitemid 35245955)
66. Adolfsson, J., R. Mansson, N. Buza-Vidas, A. Hultquist, K. Liuba, C. T. Jensen, D. Bryder, L. Yang, O. J. Borge, L. A. Thoren, et al. 2005. Identification of Flt3+ lympho-myeloid stem cells lacking erythromegakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121: 295-306.
67. + lymphoid-restricted bone marrow cells with T precursor potential. Nat. Immunol. 4: 866-873.
68. - hematopoietic progenitor with potent lymphoid and myeloid developmental potential. Eur. J. Immunol. 35: 2019-2030.
69. Shand, J. C., P. J. Mansky, M. V. Brown, T. A. Fleisher, and C. L. Mackall. 2006. Adolescents and young adults successfully restore lymphocyte homeostasis after intensive T-cell depleting therapy for cancer. Br. J. Haematol. 135: 270-271.
70. Cavenagh, J. D., T. M. Milne, M. G. Macey, and A. C. Newland. 1997. Thymic function in adults: evidence derived from immune recovery patterns following myeloablative chemotherapy and stem cell infusion. Br. J. Haematol. 97: 673-676.
71. Krueger, A., and H. von Boehmer. 2007. Identification of a T lineage-committed progenitor in adult blood. Immunity 26: 105-116.
72. Maillard, I., B. A. Schwarz, A. Sambandam, T. Fang, O. Shestova, L. Xu, A. Bhandoola, and W. S. Pear. 2006. Notch-dependent T-lineage commitment occurs at extrathymic sites following bone marrow transplantation. Blood 107: 3511-3519.
73. Morrison, S. J., D. E. Wright, and I. L. Weissman. 1997. Cyclophosphamide/granulocyte colony-stimulating factor induces hematopoietic stem cells to proliferate prior to mobilization. Proc. Natl. Acad. Sci. USA 94: 1908-1913.
74. Benten, W. P., M. Lieberherr, G. Giese, C. Wrehlke, O. Stamm, C. E. Sekeris, H. Mossmann, and F. Wunderlich. 1999. Functional testosterone receptors in plasma membranes of T cells. FASEB J. 13: 123-133.
75. McMurray, R. W., S. Suwannaroj, K. Ndebele, and J. K. Jenkins. 2001. Differential effects of sex steroids on T and B cells: modulation of cell cycle phase distribution, apoptosis and bcl-2 protein levels. Pathobiology 69: 44-58.
76. Olsen, N. J., S. M. Viselli, J. Fan, and W. J. Kovacs. 1998. Androgens accelerate thymocyte apoptosis. Endocrinology 139: 748-752.
77. + regulatory T cells is indexed to the number of IL-2-producing cells. J. Immunol. 177: 192-200.
78. Olsen, N. J., G. Olson, S. M. Viselli, X. Gu, and W. J. Kovacs. 2001. Androgen receptors in thymic epithelium modulate thymus size and thymocyte development. Endocrinology 142: 1278-1283.
79. Williams, K. M., P. J. Lucas, C. V. Bare, J. Wang, Y. W. Chu, E. Tayler, V. Kapoor, and R. E. Gress. 2008. CCL25 increases thymopoiesis after androgen withdrawal. Blood 112: 3255-3263.