The E3 ubiquitin ligase skp2 regulates neural differentiation independent from the cell cycle

Neural Development

Volumn 2, Issue 1, 2007, Pages

  Boix Perales, Hector ^a   Horan, Ian ^a   Wise, Helen ^a   Lin, Horng Ru ^b   Chuang, Li Chiou ^b   Yew, P Renee ^b   Philpott, Anna ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN; SKP2 PROTEIN, XENOPUS; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; XENOPUS PROTEIN;

ANIMAL; ANIMAL MODEL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE CELL; NEURAL TUBE; PHYSIOLOGY; PRENATAL DEVELOPMENT; STEM CELL; XENOPUS LAEVIS;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MODELS, ANIMAL; NEURAL TUBE; NEURONS; S-PHASE KINASE-ASSOCIATED PROTEINS; STEM CELLS; UBIQUITIN-PROTEIN LIGASES; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 38949123365     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-2-27     Document Type: Article

References (73)

1. Ubiquitin-mediated proteolysis: biological regulation via destruction. A Ciechanover A Orian AL Schwartz, Bioessays 2000 22 5 442 451 10.1002/(SICI)1521-1878(200005)22:5<442::AID-BIES63.0.CO;2-Q 10797484
2. Modes of regulation of ubiquitin-mediated protein degradation. D Kornitzer A Ciechanover, J Cell Physiol 2000 182 1 1 11 10.1002/(SICI)1097- 4652(200001)182:1<1::AID-JCP13.0.CO;2-V 10567911
3. The ubiquitin system. A Hershko A Ciechanover, Annu Rev Biochem 1998 67 425 479 10.1146/annurev.biochem.67.1.425 9759494
4. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. RM Feldman CC Correll KB Kaplan RJ Deshaies, Cell 1997 91 2 221 230 10.1016/S0092-8674(00)80404-3 9346239
5. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. D Skowyra KL Craig M Tyers SJ Elledge JW Harper, Cell 1997 91 2 209 219 10.1016/S0092-8674(00)80403-1 9346238
6. Cdc53 is a scaffold protein for multiple Cdc34/Skp1/F-box proteincomplexes that regulate cell division and methionine biosynthesis in yeast. EE Patton AR Willems D Sa L Kuras D Thomas KL Craig M Tyers, Genes Dev 1998 12 5 692 705 9499404
7. Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. T Kamura DM Koepp MN Conrad D Skowyra RJ Moreland O Iliopoulos WS Lane WG Kaelin Jr SJ Elledge RC Conaway, Science 1999 284 5414 657 661 10.1126/science.284.5414.657 10213691
8. ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. T Ohta JJ Michel AJ Schottelius Y Xiong, Mol Cell 1999 3 4 535 541 10.1016/S1097-2765(00)80482-7 10230407
9. Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. JH Seol RM Feldman W Zachariae A Shevchenko CC Correll S Lyapina Y Chi M Galova J Claypool S Sandmeyer, Genes Dev 1999 13 12 1614 1626 10385629
10. Interaction between ubiquitin-protein ligase SCFSKP2 and E2F-1 underlies the regulation of E2F-1 degradation. A Marti C Wirbelauer M Scheffner W Krek, Nat Cell Biol 1999 1 1 14 19 10.1038/8984 10559858
11. Skp2 regulates Myc protein stability and activity. SY Kim A Herbst KA Tworkowski SE Salghetti WP Tansey, Mol Cell 2003 11 5 1177 1188 10.1016/S1097-2765(03)00173-4 12769843
12. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. N von der Lehr S Johansson S Wu F Bahram A Castell C Cetinkaya P Hydbring I Weidung K Nakayama KI Nakayama, Mol Cell 2003 11 5 1189 1200 10.1016/S1097-2765(03)00193-X 12769844
13. Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21(CIP1/WAF1) and cyclin D proteins. ZK Yu JL Gervais H Zhang, Proc Natl Acad Sci USA 1998 95 19 11324 11329 9736735 10.1073/pnas.95.19.11324
14. Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. G Bornstein J Bloom D Sitry-Shevah K Nakayama M Pagano A Hershko, J Biol Chem 2003 278 28 25752 25757 10.1074/jbc.M301774200 12730199
15. Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication. K Nakayama H Nagahama YA Minamishima M Matsumoto I Nakamichi K Kitagawa M Shirane R Tsunematsu T Tsukiyama N Ishida, Embo J 2000 19 9 2069 2081 10790373 10.1093/emboj/19.9.2069
16. Cyclin E-CDK2 is a regulator of p27Kip1. RJ Sheaff M Groudine M Gordon JM Roberts BE Clurman, Genes Dev 1997 11 11 1464 1478 10.1101/gad.11.11.1464 9192873
17. Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. J Vlach S Hennecke B Amati, Embo J 1997 16 17 5334 5344 9311993 10.1093/emboj/16.17.5334
18. Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. A Montagnoli F Fiore E Eytan AC Carrano GF Draetta A Hershko M Pagano, Genes Dev 1999 13 9 1181 1189 10323868
19. Cell cycle control by Xenopus p28Kix1, a developmentally regulated inhibitor of cyclin-dependent kinases. W Shou WG Dunphy, Mol Biol Cell 1996 7 3 457 469 8868473
20. Cloning and characterization of the Xenopus cyclin-dependent kinase inhibitor p27XIC1. JY Su RE Rempel E Erikson JL Maller, Proc Natl Acad Sci USA 1995 92 22 10187 10191 7479751 10.1073/pnas.92.22.10187
21. Ubiquitination of cyclin-dependent kinase inhibitor, Xic1, is mediated by the Xenopus F-box protein xSkp2. HR Lin LC Chuang H Boix-Perales A Philpott PR Yew, Cell Cycle 2006 5 3 304 314 16410731
22. The cdk inhibitor p27Xic1 is required for differentiation of primary neurones in Xenopus. AE Vernon C Devine A Philpott, Development 2003 130 1 85 92 10.1242/dev.00193 12441293
23. Identification of neurogenin, a vertebrate neuronal determination gene. Q Ma C Kintner DJ Anderson, Cell 1996 87 1 43 52 10.1016/S0092-8674(00)81321-5 8858147
24. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. JE Lee SM Hollenberg L Snider DL Turner N Lipnick H Weintraub, Science 1995 268 5212 836 844 10.1126/science.7754368 7754368
25. Skp2-mediated degradation of p27 regulates progression into mitosis. K Nakayama H Nagahama YA Minamishima S Miyake N Ishida S Hatakeyama M Kitagawa S Iemura T Natsume KI Nakayama, Dev Cell 2004 6 5 661 672 10.1016/S1534-5807(04) 00131-5 15130491
26. A single cdk inhibitor, p27Xic1, functions beyond cell cycle regulation to promote muscle differentiation in Xenopus. AE Vernon A Philpott, Development 2003 130 1 71 83 10.1242/dev.00180 12441292
27. Intrinsic differences between the superficial and deep layers of the Xenopus ectoderm control primary neuronal differentiation. AD Chalmers D Welchman N Papalopulu, Dev Cell 2002 2 2 171 182 10.1016/S1534-5807(02)00113-2 11832243
28. Ubiquitination and degradation of the substrate recognition subunits of SCF ubiquitin-protein ligases. P Zhou PM Howley, Mol Cell 1998 2 5 571 580 10.1016/S1097-2765(00)80156-2 9844630
29. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. AC Carrano E Eytan A Hershko M Pagano, Nat Cell Biol 1999 1 4 193 199 10.1038/12013 10559916
30. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. H Sutterluty E Chatelain A Marti C Wirbelauer M Senften U Muller W Krek, Nat Cell Biol 1999 1 4 207 214 10.1038/12027 10559918
31. p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. LM Tsvetkov KH Yeh SJ Lee H Sun H Zhang, Curr Biol 1999 9 12 661 664 10.1016/S0960-9822(99)80290-5 10375532
32. Degradation of p57Kip2 mediated by SCFSkp2-dependent ubiquitylation. T Kamura T Hara S Kotoshiba M Yada N Ishida H Imaki S Hatakeyama K Nakayama KI Nakayama, Proc Natl Acad Sci USA 2003 100 18 10231 10236 12925736 10.1073/pnas.1831009100
33. Spatial and temporal patterns of cell division during early Xenopus embryogenesis. Y Saka JC Smith, Dev Biol 2001 229 2 307 318 10.1006/dbio.2000. 0101 11150237
34. Degradation of p27(Kip1) at the G(0)-G(1) transition mediated by a Skp2-independent ubiquitination pathway. T Hara T Kamura K Nakayama K Oshikawa S Hatakeyama, J Biol Chem 2001 276 52 48937 48943 10.1074/jbc.M107274200 11682478
35. Inverse relationship between Skp2 ubiquitin ligase and the cyclin dependent kinase inhibitor p27Kip1 in prostate cancer. O Ben-Izhak S Lahav-Baratz S Meretyk S Ben-Eliezer E Sabo M Dirnfeld S Cohen A Ciechanover, J Urol 2003 170 1 241 245 10.1097/01.ju.0000072113.34524.a7 12796697
36. S-phase kinase-associated protein 2 expression in laryngeal squamous cell carcinomas and its prognostic implications. Y Dong L Sui Y Watanabe K Sugimoto M Tokuda, Oncol Rep 2003 10 2 321 325 12579266
37. Immunohistochemical study of Skp2 and Jab1, two key molecules in the degradation of P27, in lung adenocarcinoma. A Goto T Niki S Moriyama N Funata H Moriyama Y Nishimura R Tsuchida JY Kato M Fukayama, Pathol Int 2004 54 9 675 681 10.1111/j.1440-1827.2004.01679.x 15363035
38. Role of the F-box protein Skp2 in lymphomagenesis. E Latres R Chiarle BA Schulman NP Pavletich A Pellicer G Inghirami M Pagano, Proc Natl Acad Sci USA 2001 98 5 2515 2520 11226270 10.1073/pnas.041475098
39. Defective cardiovascular development and elevated cyclin E and Notch proteins in mice lacking the Fbw7 F-box protein. MT Tetzlaff W Yu M Li P Zhang M Finegold K Mahon JW Harper RJ Schwartz SJ Elledge, Proc Natl Acad Sci USA 2004 101 10 3338 3345 14766969 10.1073/pnas.0307875101
40. Expression of Skp2, a p27(Kip1) ubiquitin ligase, in malignant lymphoma: correlation with p27(Kip1) and proliferation index. MS Lim A Adamson Z Lin B Perez-Ordonez RC Jordan S Tripp SL Perkins KS Elenitoba-Johnson, Blood 2002 100 8 2950 2956 10.1182/blood.V100.8.2950 12351407
41. The F-box protein SKP2 mediates androgen control of p27 stability in LNCaP human prostate cancer cells. L Lu H Schulz DA Wolf, BMC Cell Biol 2002 3 22 12188931 10.1186/1471-2121-3-22
42. Clinical and biological significance of S-phase kinase-associated protein 2 (Skp2) gene expression in gastric carcinoma: modulation of malignant phenotype by Skp2 overexpression, possibly via p27 proteolysis. TA Masuda H Inoue H Sonoda S Mine Y Yoshikawa K Nakayama K Nakayama M Mori, Cancer Res 2002 62 13 3819 3825 12097295
43. Elevated S-phase kinase-associated protein 2 protein expression in acute myelogenous leukemia: its association with constitutive phosphorylation of phosphatase and tensin homologue protein and poor prognosis. YH Min JW Cheong MH Lee JY Kim ST Lee JS Hahn YW Ko, Clin Cancer Res 2004 10 15 5123 5130 10.1158/1078-0432.CCR-04-0136 15297415
44. The expression of the F-box protein Skp2 is negatively associated with p27 expression in human pituitary tumors. M Musat M Korbonits M Pyle M Gueorguiev B Kola DG Morris M Powell C Dumitrache C Poiana AB Grossman, Pituitary 2002 5 4 235 242 10.1023/A:1025325832698 14558671
45. Skp2 protein expression in soft tissue sarcomas. AM Oliveira SH Okuno AG Nascimento RV Lloyd, J Clin Oncol 2003 21 4 722 727 10.1200/JCO.2003.05.112 12586812
46. Over-expression of p45(SKP2) in Kaposi's sarcoma correlates with higher tumor stage and extracutaneous involvement but is not directly related to p27(KIP1) down-regulation. RM Penin MT Fernandez-Figueras L Puig J Rex C Ferrandiz A Ariza, Mod Pathol 2002 15 11 1227 1235 10.1097/01.MP.0000036589. 99516.D6 12429803
47. Inverse relationship between p27/Kip.1 and the F-box protein Skp2 in human astrocytic gliomas by immunohistochemistry and Western blot. D Schiffer P Cavalla V Fiano C Ghimenti R Piva, Neurosci Lett 2002 328 2 125 128 10.1016/S0304-3940(02)00483-4 12133571
48. Skp2 overexpression is a prognostic factor in patients with ovarian adenocarcinoma. K Shigemasa L Gu TJ O'Brien K Ohama, Clin Cancer Res 2003 9 5 1756 1763 12738731
49. Expression of the F-box protein SKP2 induces hyperplasia, dysplasia, and low-grade carcinoma in the mouse prostate. EH Shim L Johnson HL Noh YJ Kim H Sun C Zeiss H Zhang, Cancer Res 2003 63 7 1583 1588 12670908
50. Oncogenic role of the ubiquitin ligase subunit Skp2 in human breast cancer. S Signoretti L Di Marcotullio A Richardson S Ramaswamy B Isaac M Rue F Monti M Loda M Pagano, J Clin Invest 2002 110 5 633 641 12208864 10.1172/JCI200215795
51. Elevated Skp2 protein expression in human prostate cancer: association with loss of the cyclin-dependent kinase inhibitor p27 and PTEN and with reduced recurrence-free survival. G Yang G Ayala A De Marzo W Tian A Frolov TM Wheeler TC Thompson JW Harper, Clin Cancer Res 2002 8 11 3419 3426 12429629
52. Down-regulation of SKP2 induces apoptosis in lung-cancer cells. S Yokoi K Yasui T Iizasa T Takahashi T Fujisawa J Inazawa, Cancer Sci 2003 94 4 344 349 10.1111/j.1349-7006.2003.tb01444.x 12824902
53. Amplification and overexpression of SKP2 are associated with metastasis of non-small-cell lung cancers to lymph nodes. S Yokoi K Yasui M Mori T Iizasa T Fujisawa J Inazawa, Am J Pathol 2004 165 1 175 180 15215173
54. A novel target gene, SKP2, within the 5p13 amplicon that is frequently detected in small cell lung cancers. S Yokoi K Yasui F Saito-Ohara K Koshikawa T Iizasa T Fujisawa T Terasaki A Horii T Takahashi S Hirohashi, Am J Pathol 2002 161 1 207 216 12107105
55. Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. LA Tintignac J Lagirand S Batonnet V Sirri MP Leibovitch SA Leibovitch, J Biol Chem 2005 280 4 2847 2856 10.1074/jbc.M411346200 15531760
56. Skp2 is oncogenic and overexpressed in human cancers. M Gstaiger R Jordan M Lim C Catzavelos J Mestan J Slingerland W Krek, Proc Natl Acad Sci USA 2001 98 9 5043 5048 11309491 10.1073/pnas.081474898
57. G1/S phase cyclin-dependent kinase overexpression perturbs early development and delays tissue-specific differentiation in Xenopus. L Richard-Parpaillon RA Cosgrove C Devine AE Vernon A Philpott, Development 2004 131 11 2577 2586 10.1242/dev.01121 15115752
58. Early neurogenesis in Xenopus: the spatio-temporal pattern of proliferation and cell lineages in the embryonic spinal cord. V Hartenstein, Neuron 1989 3 4 399 411 10.1016/0896-6273(89)90200-6 2642003
59. p107 inhibits G1 to S phase progression by down-regulating expression of the F-box protein Skp2. G Rodier C Makris P Coulombe A Scime K Nakayama KI Nakayama S Meloche, J Cell Biol 2005 168 1 55 66 10.1083/jcb.200404146 15631990
60. E2F-Rb complexes regulating transcription of genes important for differentiation and development. M Korenjak A Brehm, Curr Opin Genet Dev 2005 15 5 520 527 10.1016/j.gde.2005.07.001 16081278
61. E2F and its developmental regulation in Xenopus laevis. A Philpott SH Friend, Mol Cell Biol 1994 14 7 5000 5009 8007993
62. Cell cycling and differentiation do not require the retinoblastoma protein during early Xenopus development. RA Cosgrove A Philpott, Dev Biol 2007 303 1 311 324 10.1016/j.ydbio.2006.11.015 17188261
63. The protooncogene c-myc is an essential regulator of neural crest formation in xenopus. A Bellmeyer J Krase J Lindgren C LaBonne, Dev Cell 2003 4 6 827 839 10.1016/S1534-5807(03)00160-6 12791268
64. Complete inhibition of Cdk/cyclin by one molecule of p21(Cip1). L Hengst U Gopfert HA Lashuel SI Reed, Genes Dev 1998 12 24 3882 3888 9869641
65. XNGNR1-dependent neurogenesis mediates early neural cell death. W Yeo J Gautier, Mech Dev 2005 122 5 635 644 10.1016/j.mod.2004.12.010 15817221
66. Cytoplasmic ubiquitin ligase KPC regulates proteolysis of p27(Kip1) at G1 phase. T Kamura T Hara M Matsumoto N Ishida F Okumura S Hatakeyama M Yoshida K Nakayama KI Nakayama, Nat Cell Biol 2004 6 12 1229 1235 10.1038/ncb1194 15531880
67. Proteolysis and DNA replication: the CDC34 requirement in the Xenopus egg cell cycle. PR Yew MW Kirschner, Science 1997 277 5332 1672 1676 10.1126/science.277.5332.1672 9287222
68. Tumour suppression: putting on the brakes. H Harris, Nature 2004 427 6971 201 10.1038/427201a 14724616
69. In situ hybridization: an improved whole-mount method for Xenopus embryos. RM Harland, Methods Cell Biol 1991 36 685 695 1811161
70. Notch targets the Cdk inhibitor Xic1 to regulate differentiation but not the cell cycle in neurons. AE Vernon M Movassagh I Horan H Wise S Ohnuma A Philpott, EMBO Rep 2006 7 6 643 648 16648822
71. Localization of a nervous system-specific class II beta-tubulin gene in Xenopus laevis embryos by whole-mount in situ hybridization. R Oschwald K Richter H Grunz, Int J Dev Biol 1991 35 4 399 405 1801865
72. Early Development of Xenopus laevis. HL Sive RM Grainger RM Harland, Cold Spring Harbour Laboratory Press 2000
73. Nonradioactive in situ hybridization to xenopus tissue sections. K Butler AM Zorn JB Gurdon, Methods 2001 23 4 303 312 10.1006/meth.2000.1142 11316431