Inhibition of S-phase kinase-associated protein 2 (Skp2) reprograms and converts diabetogenic T cells to Foxp3 + regulatory T cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 24, 2012, Pages 9493-9498

  Wang, Ding ^a   Qin, Hanjun ^a   Du, Weiting ^a   Shen, Yueh Wei ^a   Lee, Wen Hui ^a   Riggs, Arthur D ^a   Liu, Chih Pin ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Autoimmunity; Autoreactive cells; Type 1 diabetes

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; INTERLEUKIN 10; PROTEIN P21; PROTEIN P27; S PHASE KINASE ASSOCIATED PROTEIN 2; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CELL CYCLE REGULATION; CONTROLLED STUDY; DIABETES MELLITUS; DIABETOGENESIS; DOWN REGULATION; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOGENESIS; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; REGULATORY T LYMPHOCYTE;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; FORKHEAD TRANSCRIPTION FACTORS; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; S-PHASE KINASE-ASSOCIATED PROTEINS; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 84862170943     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1207293109     Document Type: Article

References (41)

1. + islet-specific T cell clone. Science 249:1433-1436.
2. Katz JD, Wang B, Haskins K, Benoist C, Mathis D (1993) Following a diabetogenic T cell from genesis through pathogenesis. Cell 74:1089-1100. (Pubitemid 23289465)
3. Sakaguchi S, Powrie F (2007) Emerging challenges in regulatory T cell function and biology. Science 317:627-629. (Pubitemid 47229955)
4. Vieira PL, et al. (2004) IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J Immunol 172:5986-5993. (Pubitemid 38621199)
5. + T cells during cure of colitis. J Immunol 177:5852-5860.
6. You S, et al. (2004) Presence of diabetes-inhibiting, glutamic acid decarboxylase-specific, IL-10-dependent regulatory T cells in naive nonobese diabetic mice. J Immunol 173:6777-6785. (Pubitemid 39541064)
7. + regulatory T cells for immunologic selftolerance and negative control of immune responses. Annu Rev Immunol 22:531-562.
8. Shevach EM (2004) Regulatory/suppressor T cells in health and disease. Arthritis Rheum 50:2721-2724.
9. O'Garra A, Vieira P (2004) Regulatory T cells and mechanisms of immune system control. Nat Med 10:801-805. (Pubitemid 39070850)
10. Qin H, et al. (2011) Killer cell Ig-like receptor (KIR) 3DL1 down-regulation enhances inhibition of type 1 diabetes by autoantigen-specific regulatory T cells. Proc Natl Acad Sci USA 108:2016-2021.
11. Carrano AC, Eytan E, Hershko A, Pagano M (1999) SKP2 is required for ubiquitinmediated degradation of the CDK inhibitor p27. Nat Cell Biol 1:193-199. (Pubitemid 129500937)
12. Yu ZK, Gervais JL, Zhang H (1998) Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21(CIP1/WAF1) and cyclin D proteins. Proc Natl Acad Sci USA 95:11324-11329.
13. Jackson PK, Eldridge AG (2002) The SCF ubiquitin ligase: An extended look. Mol Cell 9: 923-925. (Pubitemid 34626661)
14. Frescas D, Pagano M (2008) Deregulated proteolysis by the F-box proteins SKP2 and β-TrCP: Tipping the scales of cancer. Nat Rev Cancer 8:438-449. (Pubitemid 351744963)
15. Lisztwan J, et al. (1998) Association of human CUL-1 and ubiquitin-conjugating enzyme CDC34 with the F-box protein p45(SKP2): Evidence for evolutionary conservation in the subunit composition of the CDC34-SCF pathway. EMBO J 17:368-383. (Pubitemid 28045478)
16. Kamura T, et al. (2003) Degradation of p57Kip2 mediated by SCFSkp2-dependent ubiquitylation. Proc Natl Acad Sci USA 100:10231-10236. (Pubitemid 37071861)
17. Tedesco D, Lukas J, Reed SI (2002) The pRb-related protein p130 is regulated by phosphorylation-dependent proteolysis via the protein-ubiquitin ligase SCF(Skp2). Genes Dev 16:2946-2957. (Pubitemid 35334742)
18. Lyapina SA, Correll CC, Kipreos ET, Deshaies RJ (1998) Human CUL1 forms an evolutionarily conserved ubiquitin ligase complex (SCF) with SKP1 and an F-box protein. Proc Natl Acad Sci USA 95:7451-7456. (Pubitemid 28293273)
19. Nakayama K, et al. (2000) Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication. EMBO J 19: 2069-2081. (Pubitemid 30237582)
20. Kang-Decker N, et al. (2004) Loss of CBP causes T cell lymphomagenesis in synergy with p27Kip1 insufficiency. Cancer Cell 5:177-189. (Pubitemid 38283803)
21. Latres E, et al. (2001) Role of the F-box protein Skp2 in lymphomagenesis. Proc Natl Acad Sci USA 98:2515-2520. (Pubitemid 32209513)
22. Zuo T, et al. (2007) FOXP3 is a novel transcriptional repressor for the breast cancer oncogene SKP2. J Clin Invest 117:3765-3773. (Pubitemid 350224087)
23. + regulatory T cells prevent type 1 diabetes preceded by dendritic cell-dominant invasive insulitis by affecting chemotaxis and local invasiveness of dendritic cells. J Immunol 185:2493-2501.
24. + T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J Exp Med 199:1479-1489.
25. + regulatory T cells during autoimmune diabetes. J Exp Med 201:1333-1346.
26. + regulatory T cells are highly susceptible to CD95 ligand- but not to TCR-mediated cell death. J Immunol 175:32-36.
27. Krammer PH (2000) CD95's deadly mission in the immune system. Nature 407: 789-795.
28. Kerdiles YM, et al. (2010) Foxo transcription factors control regulatory T cell development and function. Immunity 33:890-904.
29. + regulatory T cells. Nat Immunol 11:618-627.
30. Ouyang W, Beckett O, Flavell RA, Li MO (2009) An essential role of the Forkhead-box transcription factor Foxo1 in control of T cell homeostasis and tolerance. Immunity 30: 358-371.
31. Medema RH, Kops GJ, Bos JL, Burgering BM (2000) AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404: 782-787. (Pubitemid 30212408)
32. Seoane J, Le HV, Shen L, Anderson SA, Massagué J (2004) Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117:211-223. (Pubitemid 38496241)
33. Tran H, Brunet A, Griffith EC, Greenberg ME (2003) The many forks in FOXO's road. Sci STKE 2003:RE5.
34. Cardozo T, Pagano M (2004) The SCF ubiquitin ligase: Insights into a molecular machine. Nat Rev Mol Cell Biol 5:739-751. (Pubitemid 39208183)
35. Huang H, et al. (2005) Skp2 inhibits FOXO1 in tumor suppression through ubiquitinmediated degradation. Proc Natl Acad Sci USA 102:1649-1654. (Pubitemid 40209222)
36. Korn T, et al. (2007) Myelin-specific re\gulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat Med 13:423-431. (Pubitemid 46559831)
37. Chen C, Lee WH, Yun P, Snow P, Liu CP (2003) Induction of autoantigen-specific Th2 and Tr1 regulatory T cells and modulation of autoimmune diabetes. J Immunol 171: 733-744. (Pubitemid 36871383)
38. You S, et al. (2003) Detection and characterization of T cells specific for BDC2.5 T cell-stimulating peptides. J Immunol 170:4011-4020. (Pubitemid 36428162)
39. Chen C, Lee WH, Zhong L, Liu CP (2006) Regulatory T cells can mediate their function through the stimulation of APCs to produce immunosuppressive nitric oxide. J Immunol 176:3449-3460. (Pubitemid 43363992)
40. Chen C, Liu CP (2009) Regulatory function of a novel population of mouse autoantigen-specific Foxp3 regulatory T cells depends on IFN-γ, NO, and contact with target cells. PLoS ONE 4:e7863.
41. Ortiz S, et al. (2010) Comparative analyses of differentially induced T-cell receptor-mediated phosphorylation pathways in T lymphoma cells. Exp Biol Med (Maywood) 235:1450-1463.