RhoB deficiency in thymic medullary epithelium leads to early thymic atrophy

International Immunology

Volumn 23, Issue 10, 2011, Pages 593-600

  Bravo Nuevo, Arturo ^a,e   O'Donnell, Rebekah ^a   Rosendahl, Alexander ^b   Chung, Jae Hoon ^c   Benjamin, Laura E ^a   Odaka, Chikako ^d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b ASTRAZENECA R AND D   (Sweden)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^d NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^e LANKENAU INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Atrophy; RhoB; TGF ; Thymus

Indexed keywords

FIBRONECTIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CONTROLLED STUDY; EPITHELIUM; INVOLUTION; MALE; MOUSE; NONHUMAN; ORGAN WEIGHT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THYMIC MEDULLARY EPITHELIUM; THYMOCYTE; THYMUS; THYMUS ATROPHY;

ANIMALS; EPITHELIUM; FEMALE; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHOB GTP-BINDING PROTEIN; THYMUS GLAND; TRANSFORMING GROWTH FACTOR BETA;

EID: 80053452167     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxr064     Document Type: Article

References (58)

1. Jaffe, A. B. and Hall, A. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247.
2. Bokoch, G. M. 2005. Regulation of innate immunity by Rho GTPases. Trends Cell Biol. 15:163.
3. Wheeler, A. P. and Ridley, A. J. 2004. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp. Cell Res. 301:43.
4. Wennerberg, K. and Der, C. J. 2004. Rho-family GTPases: it's not only Rac and Rho. J. Cell Sci. 117:1301.
5. Du, W. and Prendergast, G. C. 1999. Geranylgeranylated RhoB mediates suppression of human tumor cell growth by farnesyltransferase inhibitors. Cancer Res. 59:5492.
6. Chen, Z., Sun, J., Pradines, A., Favre, G., Adnane, J. and Sebti, S. M. 2000 Both farnesylated and geranylgeranylated RhoB inhibit malignant transformation, induce apoptosis and suppress human tumor growth in nude mice. J. Biol. Chem. 275:17974.
7. Liu, A. X., Rane, N., Liu, J. P. and Prendergast, G. C. 2001. RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells. Mol. Cell. Biol. 21:6906.
8. Mazieres, J., Tillement, V., Allal, C. et al. 2005. Geranylgeranylated, but not farnesylated, RhoB suppresses Ras transformation of NIH-3T3 cells. Exp. Cell Res. 304:354.
9. Forget, M. A., Desrosiers, R. R., Moumdjian, M. et al. 2002. The expression of rho proteins decreases with human brain tumor progression: potential tumor markers. Clin. Exp. Metastasis. 19:9.
10. Adnane, J., Muro-Cacho, C., Mathews, L., Sebti, S. M. and Munoz-Antonia, T. 2002. Suppression of rho B expression in invasive carcinoma from head and neck cancer patients. Clin. Cancer Res. 8:2225.
11. Mazieres, J., Antonia, T., Daste, G. et al. 2004. Loss of RhoB expression in human lung cancer progression. Clin. Cancer Res. 10:2742.
12. Jiang, K., Delarue, F. L. and Sebti, S. M. 2004. EGFR, ErbB2 and Ras but not Src suppress RhoB expression while ectopic expression of RhoB antagonizes oncogene-mediated transformation. Oncogene 23:1136.
13. Canguilhem, B., Pradines, A., Baudouin, C. et al. 2005. RhoB protects human keratinocytes from UVB-induced apoptosis through epidermal growth factor receptor signaling. J. Biol. Chem. 280:43257.
14. Milia, J., Teyssier, F., Dalenc, F. et al. 2005. Farnesylated RhoB inhibits radiation-induced mitotic cell death and controls radiationinduced centrosome overduplication. Cell Death Differ. 12:492.
15. rho proteins. J. Cell Biol. 119:617.
16. Michaelson, D., Silletti, J., Murphy, G., D'Eustachio, P., Rush, M. and Philips, M. R. 2001. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J. Cell Biol. 152:111.
17. Wherlock, M., Gampel, A., Futter, C. and Mellor, H. 2004. Farnesyltransferase inhibitors disrupt EGF receptor traffic through modulation of the RhoB GTPase. J. Cell Sci. 117:3221.
18. Gampel, A., Parker, P. J. and Mellor, H. 1999. Regulation of epidermal growth factor receptor traffic by the small GTPase RhoB. Curr. Biol. 9:955.
19. Adini, I., Rabinowitz, I., Sun, J. F., Prendergast, G. C. and Benjamin, L. E. 2003. RhoB controls Akt trafficking and stagespecific survival of endothelial cells during vascular development. Genes Dev. 17:2721.
20. Liu, A. X., Rane, N., Liu, J. P. and Prendergast, G. C. 2001. RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells. Mol. Cell. Biol. 21:6906.
21. Wheeler, A. P. and Ridley, A. J. 2007. RhoB affects macrophage adhesion, integrin expression and migration. Exp. Cell. Res. 313:3505.
22. Aspinall, R., Andrew, D. and Pido-Lopez, J. 2002. Age-associated changes in thymopoiesis. Springer Semin. Immunopathol. 24:87.
23. Taub, D. D. and Longo, D. L. 2005. Insights into thymic aging and regeneration. Immunol. Rev. 205:72.
24. Tosi, P., Kraft, R., Luzi, P. et al. 1982. Involution pattern of the human thymus. I. Size of the cortical area as a function of age. Clin. Exp. Immunol. 47:497.
25. Clarke, A. G. and Kendall, M. D. 1989. Histological changes in the thymus during mouse pregnancy. Thymus 14:65.
26. Barr, I. G., Khalid, B. A., Pearce, P. et al. 1982. Dihydrotestosterone and estradiol deplete corticosensitive thymocytes lacking in receptors for these hormones. J. Immunol. 128:2825.
27. 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.
28. Olsen, N. J., Zhou, P., Ong, H. and Kovacs, W. J. 1993. Testosterone induces expression of transforming growth factorbeta in the murine thymus. J. Steroid Biochem. Mol. Biol. 45:327.
29. Sempowski, G. D., Hale, L. P., Sundy, J. S. et al. 2000. 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. 164:2180.
30. Kumar, R., Langer, J. C. and Snoeck, H. W. 2006. Transforming growth factor-beta2 is involved in quantitative genetic variation in thymic involution. Blood 107:1974.
31. Aspinall, R. and Andrew, D. 2002. Age-associated thymic atrophy is linked to a decline in IL-7 production. Exp. Gerontol. 37:455.
32. Tyan, M. L. 1977. Age-related decrease in mouse T progenitors. J. Immunol. 118:846.
33. Eren, R., Globerson, A., Abel, L. and Zharhary, D. 1990. Quantitative analysis of bone marrow thymic progenitors in young and aged mice. Cell. Immunol. 127:238.
34. Min, H., Montecino-Rodriquez, E. and Dorshkind, K. 2004. Reduction in the developmental potential of intrathymic T cell progenitors with age. J. Immunol. 173:245.
35. Aspinall, R. 1997. Age-associated thymic atrophy in the mouse is due to a deficiency affecting rearrangement of the TCR during intrathymic T cell development. J. Immunol. 158:3037.
36. Farr, A. G., Dooley, J. L. and Erickson, M. 2002. Organization of thymic medullary epithelial heterogeneity: implications for mechanisms of epithelial differentiation. Immunol. Rev. 189:20.
37. 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.
38. Gray, D. H., Seach, N., Ueno, T. et al. 2006. Developmental kinetics, turnover, and stimulatory capacity of thymic epithelial cells. Blood 108:3777.
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. Odaka, C. 2009. Localization of mesenchymal cells in adult mouse thymus: their abnormal distribution in mice with disorganization of thymic medullary epithelium. J. Histochem. Cytochem. 57:373.
41. Rosendahl, A., Speletas, M., Leandersson, K., Ivars, F. and Sideras, P. 2003. Transforming growth factor-beta- and Activin-Smad signaling pathways are activated at distinct maturation stages of the thymopoeisis. Int. Immunol. 15:1401.
42. Pazirandeh, A., Jondal, M. and Okret, S. 2004. Glucocorticoids delay age-associated thymic involution through directly affecting the thymocytes. Endocrinology 145:2392.
43. Govinden, R. and Bhoola, K. D. 2003. Genealogy, expression, and cellular function of transforming growth factor-beta. Pharmacol. Ther. 98:257.
44. Massagué, J. 2000. How cells read TGF-beta signals. Nat. Rev. Mol. Cell. Biol. 1:169.
45. Adnane, J., Seijo, E., Chen, Z. et al. 2002. RhoB, not RhoA, represses the transcription of the transforming growth factor beta type II receptor by a mechanism involving activator protein 1. J. Biol. Chem. 277:8500.
46. Engel, M. E., Datta, P. K. and Moses, H. L. 1998. RhoB is stabilized by transforming growth factor beta and antagonizes transcriptional activation. J. Biol. Chem. 273:9921.
47. Ignotz, R. A., Endo, T. and Massagué, J. 1987. Regulation of fibronectin and type I collagen mRNA levels by transforming growth factor-beta. J. Biol. Chem. 262:6443.
48. Raghow, R., Postlethwaite, A. E., Keski-Oja, J., Moses, H. L. and Kang, A. H. 1987. Transforming growth factor-beta increases steady state levels of type I procollagen and fibronectin messenger RNAs posttranscriptionally in cultured human dermal fibroblasts. J. Clin. Invest. 79:1285.
49. Lannes-Vieira, J., Dardenne, M. and Savino, W. 1991. Extracellular matrix components of the mouse thymus microenvironment: ontogenetic studies and modulation by glucocorticoid hormones. J. Histochem. Cytochem. 9:1539.
50. Aw, D., Silva, A. B., Maddick, M., von Zglinicki, T. and Palmer, D. B. 2008. Architectural changes in the thymus of aging mice. Aging Cell 7:158.
51. Henderson, D. J., Ybot-Gonzalez, P. and Copp, A. J. 2000. RhoB is expressed in migrating neural crest and endocardial cushions of the developing mouse embryo. Mech. Dev. 95:211.
52. Maddala, R., Peng, Y. W. and Rao, P. V. 2001. Selective expression of the small GTPase RhoB in the early developing mouse lens. Dev. Dyn. 222:534.
53. Crema, V. O., Fossati, A. C., Hamassaki, D. E. and Santos, M. F. [2008] Distribution of small Rho GTPases in the developing rat submandibular gland. J. Mol. Histol. 39:519.
54. Mazieres, J., Antonia, T., Daste, G. et al. 2004. Loss of RhoB expression in human lung cancer progression. Clin. Cancer Res. 10:2742.
55. Hauri-Hohl, M. M., Zuklys, S., Keller, M. P. et al. 2008. TGF-beta signaling in thymic epithelial cells regulates thymic involution and postirradiation reconstitution. Blood 112:626.
56. Elcüman, E. A. and Akay, M. T. 1998. Age-dependent immunolocalization of fibronectin and histological changes in the thymus of rats. Vet. Res. Commun. 22:525.
57. Yoon, Y. S., Choo, J. H., Yoo, T., Kang, K. and Chung, J. H. 2007. RhoB is epigenetically regulated in an age- and tissue-specific manner. Biochem. Biophys. Res. Commun. 362:164.
58. Phillips, J. A., Brondstetter, T. I., English, C. A., Lee, H. E., Virts, E. L. and Thoman, M. L. 2004. IL-7 gene therapy in aging restores early thymopoiesis without reversing involution. J. Immunol. 173:4867.