Overexpression of RhoH permits to bypass the Pre-TCR checkpoint

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Tamehiro, Norimasa ^a   Oda, Hiroyo ^a   Shirai, Mutsunori ^b   Suzuki, Harumi ^a  

^a NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^b YAMAGUCHI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

REGULATOR PROTEIN; RHOH PROTEIN; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG; LYMPHOCYTE ANTIGEN RECEPTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOH PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4 CD8 RATIO; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE REARRANGEMENT; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TCR BETA GENE; THYMOCYTE; THYMUS; TRANSGENICS; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL CYCLE CHECKPOINT; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PHYSIOLOGY; T LYMPHOCYTE; T LYMPHOCYTE RECEPTOR GENE; TRANSGENIC MOUSE; UPREGULATION;

MUS;

ANIMALS; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, T-CELL RECEPTOR; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RHO GTP-BINDING PROTEINS; T-LYMPHOCYTES; THYMUS GLAND; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84938310616     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131047     Document Type: Article

References (45)

1. Gascoigne NRJ, Palmer E. Signaling in thymic selection. Current Opinion in Immunology. 2011; 23 (2):207-12. doi: 10.1016/j.coi.2010.12.017 PMID: 21242076
2. Chakraborty AK, Weiss A. Insights into the initiation of TCR signaling. Nature Immunology. 2014; 15 (9):798-807. doi: 10.1038/ni.2940 PMID: 25137454
3. Cleverley S, Henning S, Cantrell D. Inhibition of Rho at different stages of thymocyte development gives different perspectives on Rho function. Current Biology. 1999; 9(12):657-60. PMID: 10375531
4. Gu Y, Chae HD, Siefring JE, Jasti AC, Hildeman DA, Williams DA. RhoH GTPase recruits and activates Zap70 required for T cell receptor signaling and thymocyte development. Nature Immunology. 2006; 7 (11):1182-90. PMID: 17028588
5. Dorn T, Kuhn U, Bungartz G, Stiller S, Bauer M, Ellwart J, et al. RhoH is important for positive thymocyte selection and T-cell receptor signaling. Blood. 2007; 109(6):2346-55. PMID: 17119112
6. Chae HD, Siefring JE, Hildeman DA, Gu Y, Williams DA. RhoH regulates subcellular localization of ZAP-70 and lck in T cell receptor signaling. Plos One. 2010; 5(11).
7. Wang H, Zeng X, Fan ZG, Lim B. RhoH modulates pre-TCR and TCR signalling by regulating LCK. Cellular Signalling. 2011; 23(1):249-58. doi: 10.1016/j.cellsig.2010.09.009 PMID: 20851766
8. Oda H, Fujimoto M, Patrick MS, Chida D, Sato Y, Azuma Y, et al. RhoH Plays Critical Roles in Fc epsilon RI-Dependent Signal Transduction in Mast Cells. Journal of Immunology. 2009; 182(2):957-62. PMID: 19124738
9. Troeger A, Chae HD, Senturk M, Wood J, Williams DA. A unique carboxyl-terminal insert domain in the hematopoietic-specific GTPase-deficient Rho GTPase RhoH regulates post-translational processing. Journal of Biological Chemistry. 2013; 288(51):36451-62. doi: 10.1074/jbc.M113.505727 PMID: 24189071
10. Oda H, Tamehiro N, Patrick MS, Hayakawa K, Suzuki H. Differential requirement for RhoH in development of TCR alpha beta CD8 alpha alpha IELs and other types of T cells. Immunology Letters. 2013; 151(1-2):1-9. doi: 10.1016/j.imlet.2013.02.007 PMID: 23499578
11. Danska JS, Pflumio F, Williams CJ, Huner O, Dick JE, Guidos CJ. Rescue of T-cell-specific V(D)J recombination in scid mice by DNA-damaging agents. Science. 1994; 266(5184):450-5. PMID: 7524150
12. Zunigapflucker JC, Jiang D, Schwartzberg PL, Lenardo MJ. Sublethal gamma-radiation induces differentiation of CD4+/CD8+ thymocytes without T-cell receptor-beta rearrangement in recombinase activation gene 2-/- mice. Journal of Experimental Medicine. 1994; 180(4):1517-21. PMID: 7931082
13. Newton K, Harris AW, Strasser A. FADD/MORT1 regulates the pre-TCR checkpoint and can function as a tumour suppressor. Embo Journal. 2000; 19(5):931-41. PMID: 10698935
14. Guidos CJ, Williams CJ, Grandal I, Knowles G, Huang MTF, Danska JS. V(D)J recombination activates a p53-dependent DNA damage checkpoint in scid lymphocyte precursors. Genes & Development. 1996; 10(16):2038-54.
15. Shinkai Y, Alt FW. CD3-epsilon-mediated signals rescue the development of CD4+ CD8+ thymocytes in RAG-2(-/-) mice in the absence of TCR beta-chain expression. International Immunology. 1994; 6 (7):995-1001. PMID: 7947468
16. Mombaerts P, Anderson SJ, Perlmutter RM, Mak TW, Tonegawa S. An activated lck transgene promotes thymocyte development in RAG-1 mutant mice. Immunity. 1994; 1(4):261-7. PMID: WOS: A1994PK16600003.
17. Norment AM, Forbush KA, Nguyen N, Malissen M, Perlmutter RM. Replacement of pre-T cell receptor signaling functions by the CD4 coreceptor. Journal of Experimental Medicine. 1997; 185(1):121-30. PMID: 8996248
18. Swat W, Shinkai Y, Cheng HL, Davidson L, Alt FW. Activated ras signals differentiation and expansion of CD4+8+ thymocytes. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93(10):4683-7. PMID: 8643464
19. Gomez M, Tybulewicz V, Cantrell DA. Control of pre-T cell proliferation and differentiation by the GTPase Rac-I. Nature Immunology. 2000; 1(4):348-52. PMID: 11017108
20. Lake RA, Wotton D, Owen MJ. A 3' Transcriptional enhancer regulates tissue-specific expression of the human CD2 gene. Embo Journal. 1990; 9(10):3129-36. PMID: 2209539
21. Zhumabekov T, Corbella P, Tolaini M, Kioussis D. Improved version of human CD2 minigene mice. Journal of Immunological Methods. 1995; 185(1):133-40. PMID: 7665895
22. Wada H, Masuda K, Satoh R, Kakugawa K, Ikawa T, Katsura Y, et al. Adult T-cell progenitors retain myeloid potential. Nature. 2008; 452(7188):768-U10. doi: 10.1038/nature06839 PMID: 18401412
23. Stritesky GL, Xing Y, Erickson JR, Kalekar LA, Wang XD, Mueller DL, et al. Murine thymic selection quantified using a unique method to capture deleted T cells. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(12):4679-84. doi: 10.1073/pnas.1217532110 PMID: 23487759
24. Azzam HS, Grinberg A, Lui K, Shen H, Shores EW, Love PE. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. Journal of Experimental Medicine. 1998; 188 (12):2301-11. PMID: 9858516
25. Rodewald HR, Awad K, Moingeon P, Dadamio L, Rabinowitz D, Shinkai Y, et al. Fc-gamma-RII/III and CD2 expression mark distinct subpopulations of immature CD4-CD8-mutine thymocytes in vivo developmental kinetics and T-cell receptor beta-chain rearrangement status. Journal of Experimental Medicine. 1993; 177(4):1079-92. PMID: 8096236
26. Li XY, Bu X, Lu BF, Avraham H, Flavell RA, Lim B. The hematopoiesis-specific GTP-binding protein RhoH is GTPase deficient and modulates activities of other Rho GTPases by an inhibitory function. Molecular and Cellular Biology. 2002; 22(4):1158-71. PMID: 11809807
27. Chae H-D, Lee KE, Williams DA, Gu Y. Cross-talk between RhoH and Rac1 in regulation of actin cytoskeleton and chemotaxis of hematopoietic progenitor cells. Blood. 2008; 111(5):2597-605. PMID: 18089848
28. Abraham KM, Levin SD, Marth JD, Forbush KA, Perlmutter RM. Thymic tumorigenesis induced by overexpression of p56lck. Proceedings of the National Academy of Sciences of the United States of America. 1991; 88(9):3977-81. PMID: 1708890
29. Anderson SJ, Abraham KM, Nakayama T, Singer A, Perlmutter RM. Inhibition of T-cell receptor beta-chain gene rearrangement by overexpression of the nonreceptor protein tyrosine kinase-p56lck. Embo Journal. 1992; 11(13):4877-86. PMID: 1334460
30. Cimbro R, Vassena L, Arthos J, Cicala C, Kehrl JH, Park C, et al. IL-7 induces expression and activation of integrin alpha 4 beta 7 promoting naive T-cell homing to the intestinal mucosa. Blood. 2012; 120 (13):2610-9. PMID: 22896005
31. Sportes C, Hakim FT, Memon SA, Zhang H, Chua KS, Brown MR, et al. Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. Journal of Experimental Medicine. 2008; 205(7):1701-14. doi: 10.1084/jem.20071681 PMID: 18573906
32. Crequer A, Troeger A, Patin E, Ma CS, Picard C, Pedergnana V, et al. Human RHOH deficiency causes T cell defects and susceptibility to EV-HPV infections. Journal of Clinical Investigation. 2012; 122 (9):3239-47. doi: 10.1172/JCI62949 PMID: 22850876
33. Bogue MA, Zhu CM, AguilarCordova E, Donehower LA, Roth DB. p53 is required for both radiationinduced differentiation and rescue of V(D)J rearrangement in scid mouse thymocytes. Genes & Development. 1996; 10(5):553-65.
34. Murphy WJ, Durum SK, Anver MR, Ferris DK, McVicar DW, Oshea JJ, et al. Induction of T-cell differentiation and lymphomagenesis in the thymus of mice with severe combined immune-deficiency (scid). Journal of Immunology. 1994; 153(3):1004-14. PMID: 7913108
35. Guidos CJ, Williams CJ, Wu GE, Paige CJ, Danska JS. Development of CD4+ CD8+ thymocytes in RAG-deficient mice through a T-cell receptor-beta chain-independent pathway. Journal of Experimental Medicine. 1995; 181(3):1187-95. PMID: 7869035
36. Nacht M, Strasser A, Chan YR, Harris AW, Schlissel M, Bronson R, et al. Mutations in the p53 and SCID genes cooperate in tumorigenesis. Genes & Development. 1996; 10(16):2055-66.
37. Di JA, Lenardo MJ, ZunigaPflucker JC. p53 prevents maturation to the CD4+CD8+ stage of thymocyte differentiation in the absence of T cell receptor rearrangement. Journal of Experimental Medicine. 1996; 183(4):1923-8. PMID: 8666950
38. Haks MC, Krimpenfort P, van den Brakel JHN, Kruisbeek AM. Pre-TCR signaling and inactivation of p53 induces crucial cell survival pathways in pre-T cells. Immunity. 1999; 11(1):91-101. PMID: 10435582
39. Norment AM, Bogatzki LY, Klinger M, Ojala EW, Bevan MJ, Kay RJ. Transgenic expression of RasGRP1 induces the maturation of double-negative thymocytes and enhances the production of CD8 single-positive thymocytes. Journal of Immunology. 2003; 170(3):1141-9.
40. Williams JA, Hathcock KS, Klug D, Harada Y, Choudhury B, Allison JP, et al. Regulated costimulation in the thymus is critical for T cell development: Dysregulated CD28 costimulation can bypass the pre- TCR checkpoint. Journal of Immunology. 2005; 175(7):4199-207. PMID: 16177059
41. Leduc I, Karsunky H, Mathieu N, Schmidt T, Verthuy C, Ferrier P, et al. The Pim-1 kinase stimulates maturation of TCR beta-deficient T cell progenitors: implications for the mechanism of Pim-1 action. International Immunology. 2000; 12(10):1389-96. PMID: 11007756
42. Miyazaki T. Two distinct steps during thymocyte maturation from CD4-CD8- to CD4+CD8+ distinguished in the early growth response (Egr)-1 transgenic mice with a recombinase-activating gene-deficient background. Journal of Experimental Medicine. 1997; 186(6):877-85. PMID: 9294142
43. Koltsova EK, Ciofani M, Benezra R, Miyazaki T, Clipstone N, Zuniga-Pflucker JC, et al. Early growth response 1 and NF-ATc1 act in concert to promote thymocyte development beyond the beta-Selection checkpoint. Journal of Immunology. 2007; 179(7):4694-703. PMID: 17878368
44. Xi HK, Kersh GJ. Early growth response gene 3 regulates thymocyte proliferation during the transition from CD4-CD8- to CD4+CD8+. Journal of Immunology. 2004; 172(2):964-71. PMID: 14707069
45. Merck E, Lees RK, Voyle RB, Held W, MacDonald HR. Ly49D-mediated ITAM signaling in immature thymocytes impairs development by bypassing the pre-TCR checkpoint. Journal of Immunology. 2011; 187(1):110-7. doi: 10.4049/jimmunol.1002755 PMID: 21632721