Thymic rejuvenation and aging

Current Opinion in Immunology

Volumn 25, Issue 4, 2013, Pages 516-522

  Ventevogel, Melissa S ^a   Sempowski, Gregory D ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEMTUZUMAB; ANDROGEN RECEPTOR; CD4 ANTIGEN; CD8 ANTIGEN; ESTROGEN; FOLLITROPIN; GHRELIN; GONADORELIN DERIVATIVE; INTERLEUKIN 22; INTERLEUKIN 7; KERATINOCYTE GROWTH FACTOR; LEUPRORELIN; LUTEINIZING HORMONE; PALIFERMIN; RECOMBINANT GROWTH HORMONE; SEX HORMONE; TESTOSTERONE;

AGING; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CASTRATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CHRONIC GRAFT VERSUS HOST DISEASE; CLINICAL TRIAL (TOPIC); DISEASE ASSOCIATION; HEMATOLOGIC MALIGNANCY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNOSTIMULATION; INVOLUTION; IONIZING RADIATION; LYMPHOID TISSUE; MALIGNANT NEOPLASTIC DISEASE; MORBIDITY; MORTALITY; MULTIPLE SCLEROSIS; NONHUMAN; OPPORTUNISTIC INFECTION; PROTEIN EXPRESSION; PULSATILE DRUG RELEASE; RADIATION EXPOSURE; REJUVENATION; REVIEW; STEM CELL TRANSPLANTATION; T LYMPHOCYTE; THYMUS FUNCTION; TISSUE REGENERATION;

AGING; ANIMALS; CYTOKINES; GROWTH HORMONE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; REJUVENATION; THYMUS GLAND;

EID: 84884166992     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2013.06.002     Document Type: Review

References (67)

1. Marodon G., Klatzmann D. In situ transduction of stromal cells and thymocytes upon intrathymic injection of lentiviral vectors. BMC Immunol 2004, 5:18.
2. Nishino M., Ashiku S.K., Kocher O.N., Thurer R.L., Boiselle P.M., Hatabu H. The thymus: a comprehensive review. Radiographics 2006, 26:335-348.
3. Klein L., Kyewski B. Self-antigen presentation by thymic stromal cells: a subtle division of labor. Curr Opin Immunol 2000, 12:179-186.
4. Hale L.P. Histologic and molecular assessment of human thymus. Ann Diagn Pathol 2004, 8:50-60.
5. Gruver A.L., Hudson L.L., Sempowski G.D. Immunosenescence of ageing. J Pathol 2007, 211:144-156.
6. Sempowski G.D., Hale L.P., Sundy J.S., Massey J.M., Koup R.A., Douek D.C., Patel D.D., Haynes B.F. Leukemia inhibitory factor, oncostatin M, IL-6, and stem cell factor mRNA expression in human thymus increases with age and is associated with thymic atrophy. J Immunol 2000, 164:2180-2187.
7. Lynch H.E., Goldberg G.L., Chidgey A., Van den Brink M.R., Boyd R., Sempowski G.D. Thymic involution and immune reconstitution. Trends Immunol 2009, 30:366-373.
8. Shanley D.P., Aw D., Manley N.R., Palmer D.B. An evolutionary perspective on the mechanisms of immunosenescence. Trends Immunol 2009, 30:374-381.
9. Dowling M.R., Hodgkin P.D. Why does the thymus involute? A selection-based hypothesis. Trends Immunol 2009, 30:295-300.
10. Sempowski G.D., Gooding M.E., Liao H.X., Le P.T., Haynes B.F. T cell receptor excision circle assessment of thymopoiesis in aging mice. Mol Immunol 2002, 38:841-848.
11. Dudakov J.A., van den Brink M.R. Greater than the sum of their parts: combination strategies for immune regeneration following allogeneic hematopoietic stem cell transplantation. Best Pract Res Clin Haematol 2011, 24:467-476.
12. Chinn I.K., Blackburn C.C., Manley N.R., Sempowski G.D. Changes in primary lymphoid organs with aging. Semin Immunol 2012, 24:309-320.
13. Gordon J., Manley N.R. Mechanisms of thymus organogenesis and morphogenesis. Development 2011, 138:3865-3878.
14. Lind E.F., Prockop S.E., Porritt H.E., Petrie H.T. Mapping precursor movement through the postnatal thymus reveals specific microenvironments supporting defined stages of early lymphoid development. J Exp Med 2001, 194:127-134.
15. Prockop S.E., Palencia S., Ryan C.M., Gordon K., Gray D., Petrie H.T. Stromal cells provide the matrix for migration of early lymphoid progenitors through the thymic cortex. J Immunol 2002, 169:4354-4361.
16. Anderson G., Jenkinson E.J., Moore N.C., Owen J.J. MHC class II-positive epithelium and mesenchyme cells are both required for T-cell development in the thymus. Nature 1993, 362:70-73.
17. Zuniga-Pflucker J.C. T-cell development made simple. Nat Rev Immunol 2004, 4:67-72.
18. Greenstein B.D., Fitzpatrick F.T., Adcock I.M., Kendall M.D., Wheeler M.J. Reappearance of the thymus in old rats after orchidectomy: inhibition of regeneration by testosterone. J Endocrinol 1986, 110:417-422.
19. Greenstein B.D., Fitzpatrick F.T., Kendall M.D., Wheeler M.J. Regeneration of the thymus in old male rats treated with a stable analogue of LHRH. J Endocrinol 1987, 112:345-350.
20. Heng T.S., Goldberg G.L., Gray D.H., Sutherland J.S., Chidgey A.P., Boyd R.L. Effects of castration on thymocyte development in two different models of thymic involution. J Immunol 2005, 175:2982-2993.
21. Windmill K.F., Lee V.W. Effects of castration on the lymphocytes of the thymus, spleen and lymph nodes. Tissue Cell 1998, 30:104-111.
22. Windmill K.F., Meade B.J., Lee V.W. Effect of prepubertal gonadectomy and sex steroid treatment on the growth and lymphocyte populations of the rat thymus. Reprod Fertil Dev 1993, 5:73-81.
23. Sutherland J.S., Goldberg G.L., Hammett M.V., Uldrich A.P., Berzins S.P., Heng T.S., Blazar B.R., Millar J.L., Malin M.A., Chidgey A.P., et al. Activation of thymic regeneration in mice and humans following androgen blockade. J Immunol 2005, 175:2741-2753.
24. Dudakov J.A., Goldberg G.L., Reiseger J.J., Chidgey A.P., Boyd R.L. Withdrawal of sex steroids reverses age- and chemotherapy-related defects in bone marrow lymphopoiesis. J Immunol 2009, 182:6247-6260.
25. Dudakov J.A., Goldberg G.L., Reiseger J.J., Vlahos K., Chidgey A.P., Boyd R.L. Sex steroid ablation enhances hematopoietic recovery following cytotoxic antineoplastic therapy in aged mice. J Immunol 2009, 183:7084-7094.
26. Goldberg G.L., Alpdogan O., Muriglan S.J., Hammett M.V., Milton M.K., Eng J.M., Hubbard V.M., Kochman A., Willis L.M., Greenberg A.S., et al. Enhanced immune reconstitution by sex steroid ablation following allogeneic hemopoietic stem cell transplantation. J Immunol 2007, 178:7473-7484.
27. Goldberg G.L., Dudakov J.A., Reiseger J.J., Seach N., Ueno T., Vlahos K., Hammett M.V., Young L.F., Heng T.S., Boyd R.L., et al. Sex steroid ablation enhances immune reconstitution following cytotoxic antineoplastic therapy in young mice. J Immunol 2010, 184:6014-6024.
28. Goldberg G.L., Sutherland J.S., Hammet M.V., Milton M.K., Heng T.S., Chidgey A.P., Boyd R.L. Sex steroid ablation enhances lymphoid recovery following autologous hematopoietic stem cell transplantation. Transplantation 2005, 80:1604-1613.
29. Blackburn C.C., Augustine C.L., Li R., Harvey R.P., Malin M.A., Boyd R.L., Miller J.F., Morahan G. The nu gene acts cell-autonomously and is required for differentiation of thymic epithelial progenitors. Proc Natl Acad Sci USA 1996, 93:5742-5746.
30. Kendall M.D., Fitzpatrick F.T., Greenstein B.D., Khoylou F., Safieh B., Hamblin A. Reversal of ageing changes in the thymus of rats by chemical or surgical castration. Cell Tissue Res 1990, 261:555-564.
31. Rao L.V., Cleveland R.P., Kimmel R.J., Ataya K.M. Gonadotropin-releasing hormone agonist influences absolute levels of lymphocyte subsets in vivo in male mice. Immunol Cell Biol 1996, 74:134-143.
32. Grossman C.J., Nathan P., Taylor B.B., Sholiton L.J. Rat thymic dihydrotestosterone receptor: preparation, location and physiochemical properties. Steroids 1979, 34:539-553.
33. Grossman C.J., Sholiton L.J., Blaha G.C., Nathan P. Rat thymic estrogen receptor-II. Physiological properties. J Steroid Biochem 1979, 11:1241-1246.
34. Grossman C.J., Sholiton L.J., Nathan P. Rat thymic estrogen receptor-I. Preparation, location and physiochemical properties. J Steroid Biochem 1979, 11:1233-1240.
35. McCruden A.B., Stimson W.H. Androgen binding cytosol receptors in the rat thymus: physicochemical properties, specificity and localisation. Thymus 1981, 3:105-117.
36. Viselli S.M., Stanziale S., Shults K., Kovacs W.J., Olsen N.J. Castration alters peripheral immune function in normal male mice. Immunology 1995, 84:337-342.
37. Olsen N.J., Olson G., Viselli S.M., Gu X., Kovacs W.J. Androgen receptors in thymic epithelium modulate thymus size and thymocyte development. Endocrinology 2001, 142:1278-1283.
38. Fitzpatrick F.T., Kendall M.D., Wheeler M.J., Adcock I.M., Greenstein B.D. Reappearance of thymus of ageing rats after orchidectomy. J Endocrinol 1985, 106:R17-R19.
39. Goldberg G.L., King C.G., Nejat R.A., Suh D.Y., Smith O.M., Bretz J.C., Samstein R.M., Dudakov J.A., Chidgey A.P., Chen-Kiang S., et al. Luteinizing hormone-releasing hormone enhances T cell recovery following allogeneic bone marrow transplantation. J Immunol 2009, 182:5846-5854.
40. Le P.T., Lazorick S., Whichard L.P., Yang Y.C., Clark S.C., Haynes B.F., Singer K.H. Human thymic epithelial cells produce IL-6, granulocyte-monocyte-CSF, and leukemia inhibitory factor. J Immunol 1990, 145:3310-3315.
41. Le P.T., Tuck D.T., Dinarello C.A., Haynes B.F., Singer K.H. Human thymic epithelial cells produce interleukin 1. J Immunol 1987, 138:2520-2526.
42. Le P.T., Kurtzberg J., Brandt S.J., Niedel J.E., Haynes B.F., Singer K.H. Human thymic epithelial cells produce granulocyte and macrophage colony-stimulating factors. J Immunol 1988, 141:1211-1217.
43. Galy A.H., de Waal Malefyt R., Barcena A., Peterson S.M., Spits H. Untransfected and SV40-transfected fetal and postnatal human thymic stromal cells. Analysis of phenotype, cytokine gene expression and cytokine production. Thymus 1993, 22:13-33.
44. Morrissey P.J., McKenna H., Widmer M.B., Braddy S., Voice R., Charrier K., Williams D.E., Watson J.D. Steel factor (c-kit ligand) stimulates the in vitro growth of immature CD3-/CD4-/CD8- thymocytes: synergy with IL-7. Cell Immunol 1994, 157:118-131.
45. von Freeden-Jeffry U., Solvason N., Howard M., Murray R. The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity 1997, 7:147-154.
46. Goodwin R.G., Friend D., Ziegler S.F., Jerzy R., Falk B.A., Gimpel S., Cosman D., Dower S.K., March C.J., Namen A.E., et al. Cloning of the human and murine interleukin-7 receptors: demonstration of a soluble form and homology to a new receptor superfamily. Cell 1990, 60:941-951.
47. Schluns K.S., Kieper W.C., Jameson S.C., Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 2000, 1:426-432.
48. Rosenberg S.A., Sportes C., Ahmadzadeh M., Fry T.J., Ngo L.T., Schwarz S.L., Stetler-Stevenson M., Morton K.E., Mavroukakis S.A., Morre M., et al. IL-7 administration to humans leads to expansion of CD8+ and CD4+ cells but a relative decrease of CD4+ T-regulatory cells. J Immunother 2006, 29:313-319.
49. Revest J.M., Suniara R.K., Kerr K., Owen J.J., Dickson C. Development of the thymus requires signaling through the fibroblast growth factor receptor R2-IIIb. J Immunol 2001, 167:1954-1961.
50. Suniara R.K., Jenkinson E.J., Owen J.J. An essential role for thymic mesenchyme in early T cell development. J Exp Med 2000, 191:1051-1056.
51. Erickson M., Morkowski S., Lehar S., Gillard G., Beers C., Dooley J., Rubin J.S., Rudensky A., Farr A.G. Regulation of thymic epithelium by keratinocyte growth factor. Blood 2002, 100:3269-3278.
52. Rossi S., Blazar B.R., Farrell C.L., Danilenko D.M., Lacey D.L., Weinberg K.I., Krenger W., Hollander G.A. Keratinocyte growth factor preserves normal thymopoiesis and thymic microenvironment during experimental graft-versus-host disease. Blood 2002, 100:682-691.
53. Rossi S.W., Jeker L.T., Ueno T., Kuse S., Keller M.P., Zuklys S., Gudkov A.V., Takahama Y., Krenger W., Blazar B.R., et al. Keratinocyte growth factor (KGF) enhances postnatal T-cell development via enhancements in proliferation and function of thymic epithelial cells. Blood 2007.
54. Dooley J., Erickson M., Larochelle W.J., Gillard G.O., Farr A.G. FGFR2IIIb signaling regulates thymic epithelial differentiation. Dev Dyn 2007, 236:3459-3471.
55. Alpdogan O., Hubbard V.M., Smith O.M., Patel N., Lu S., Goldberg G.L., Gray D.H., Feinman J., Kochman A.A., Eng J.M., et al. Keratinocyte growth factor (KGF) is required for postnatal thymic regeneration. Blood 2006, 107:2453-2460.
56. Min D., Panoskaltsis-Mortari A., Kuro O.M., Hollander G.A., Blazar B.R., Weinberg K.I. Sustained thymopoiesis and improvement in functional immunity induced by exogenous KGF administration in murine models of aging. Blood 2007, 109:2529-2537.
57. Min D., Panoskaltsis-Mortari A., Kuro-o M., Holländer G.A., Blazar B.R., Weinberg K.I. Sustained thymopoiesis and improvement in functional immunity induced by exogenous KGF administration in murine models of aging. Blood 2007, 109:2529-2537.
58. Brand S., Beigel F., Olszak T., Zitzmann K., Eichhorst S.T., Otte J.M., Diepolder H., Marquardt A., Jagla W., Popp A., et al. IL-22 is increased in active Crohn's disease and promotes proinflammatory gene expression and intestinal epithelial cell migration. Am J Physiol Gastrointest Liver Physiol 2006, 290:G827-G838.
59. Dudakov J.A., Hanash A.M., Jenq R.R., Young L.F., Ghosh A., Singer N.V., West M.L., Smith O.M., Holland A.M., Tsai J.J., et al. Interleukin-22 drives endogenous thymic regeneration in mice. Science 2012, 336:91-95.
60. Heng T.S., Chidgey A.P., Boyd R.L. Getting back at nature: understanding thymic development and overcoming its atrophy. Curr Opin Pharmacol 2010, 10:425-433.
61. Taub D.D., Murphy W.J., Longo D.L. Rejuvenation of the aging thymus: growth hormone-mediated and ghrelin-mediated signaling pathways. Curr Opin Pharmacol 2010, 10:408-424.
62. Welniak L.A., Sun R., Murphy W.J. The role of growth hormone in T-cell development and reconstitution. J Leukoc Biol 2002, 71:381-387.
63. Goldberg G.L., Zakrzewski J.L., Perales M.A., van den Brink M.R. Clinical strategies to enhance T cell reconstitution. Semin Immunol 2007, 19:289-296.
64. Tian Z.G., Woody M.A., Sun R., Welniak L.A., Raziuddin A., Funakoshi S., Tsarfaty G., Longo D.L., Murphy W.J. Recombinant human growth hormone promotes hematopoietic reconstitution after syngeneic bone marrow transplantation in mice. Stem Cells 1998, 16:193-199.
65. Murphy W.J., Longo D.L. Growth hormone as an immunomodulating therapeutic agent. Immunol Today 2000, 21:211-213.
66. Hudson L.L., Louise Markert M., Devlin B.H., Haynes B.F., Sempowski G.D. Human T cell reconstitution in DiGeorge syndrome and HIV-1 infection. Semin Immunol 2007, 19:297-309.
67. Dixit V.D., Yang H., Sun Y., Weeraratna A.T., Youm Y.H., Smith R.G., Taub D.D. Ghrelin promotes thymopoiesis during aging. J Clin Invest 2007, 117:2778-2790.