RBX1/ROC1 disruption results in early embryonic lethality due to proliferation failure, partially rescued by simultaneous loss of p27

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

Volumn 106, Issue 15, 2009, Pages 6203-6208

  Tan, Mingjia ^a   Davis, Shannon W ^b   Saunders, Thomas L ^b   Zhu, Yuan ^b   Sun, Yi ^a  

^a UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Growth suppression; Protein degradation; SCF E3 ubiquitin ligase

Indexed keywords

PROTEIN DERIVATIVE; PROTEIN P27; REGULATOR OF CULLINS 1; RING BOX PROTEIN 1; UNCLASSIFIED DRUG; CARRIER PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1B; RBX1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL GROWTH; CELL PROLIFERATION; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FIBROBLAST; GENE; HETEROZYGOTE; IN VIVO STUDY; LETHALITY; LIFESPAN; MALE; MOUSE; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; ANIMAL; ANIMAL EMBRYO; CELL LINE; CYTOLOGY; EMBRYO DEATH; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; MUTATION; PATHOLOGY; PRENATAL DEVELOPMENT; TIME; TRANSGENIC MOUSE;

MUS;

ANIMALS; CARRIER PROTEINS; CELL LINE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P27; EMBRYO LOSS; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; MALE; MICE; MICE, TRANSGENIC; MUTATION; TIME FACTORS;

EID: 65549122047     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0812425106     Document Type: Article

References (42)

1. Bai C, et al. (1996) SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263-274.
2. Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209-219.
3. Ohta T, Michel JJ, Schottelius AJ, Xiong Y (1999) ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol Cell 3:535-541.
4. Kamura T, Conrad MN, Yan Q, Conaway RC, Conaway JW (1999) The Rbx1 subunit of SCF and VHL E3 ubiquitin ligase activates Rub1 modification of cullins Cdc53 and Cul2. Genes Dev 13:2928-2933.
5. Tan P, et al. (1999) Recruitment of a ROC1-CUL1 ubiquitin ligase by Skp1 and HOS to catalyze the ubiquitination of IkBa. Mol Cell 3:527-533.
6. Seol JH, et al. (1999) Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev 13:1614-1626.
7. Willems AR, Schwab M, Tyers M (2004) A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695:133-170.
8. Zheng N, et al. (2002) Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416:703-709.
9. Wu K, et al. (2000) The SCF(HOS/beta-TRCP)-ROC1 E3 ubiquitin ligase utilizes two distinct domains within CUL1 for substrate targeting and ubiquitin ligation. Mol Cell Biol 20:1382-1393.
10. Nakayama KI, Nakayama K (2005) Regulation of the cell cycle by SCF-type ubiquitin ligases. Semin Cell Dev Biol 16:323-333.
11. Nakayama KI, Nakayama K (2006) Ubiquitin ligases: Cell-cycle control and cancer. Nat Rev Cancer 6:369-381.
12. Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6:9-20.
13. Morimoto M, Nishida T, Nagayama Y, Yasuda H (2003) Nedd8-modification of Cul1 is promoted by Roc1 as a Nedd8-E3 ligase and regulates its stability. Biochem Biophys Res Commun 301:392-398.
14. Pan ZQ, Kentsis A, Dias DC, Yamoah K, Wu K (2004) Nedd8 on cullin: Building an expressway to protein destruction. Oncogene 23:1985-1997.
15. Sun Y, Tan M, Duan H, Swaroop M (2001) SAG/ROC/Rbx/Hrt, a zinc RING finger gene family: Molecular cloning, biochemical properties, and biological functions. Antioxid Redox Signal 3:635-650.
16. Gu Q, Tan M, Sun Y (2007) SAG/ROC2/Rbx2 is a novel activator protein-1 target that promotes c-Jun degradation and inhibits 12-O-tetradecanoylphorbol- 13-acetate-induced neoplastic transformation. Cancer Res 67:3616-3625.
17. Kamura T, et al. (2004) VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes Dev 18:3055-3065.
18. Hakem R, et al. (1996) The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85:1009-1023.
19. Carrano AC, Eytan E, Hershko A, Pagano M (1999) SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1:193-199.
20. Tsvetkov LM, Yeh K-H, Lee S-J, Sun H, Zhang H (1999) p27kip1ubiquitination and degradation is regulated by the SCFskp2 complex through phosphorylated Thr187 in p27. Cur Biol 9:661-664.
21. Sutterluty H, et al. (1999) p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol 1:207-214.
22. Noureddine MA, Donaldson TD, Thacker SA, Duronio RJ (2002) Drosophila Roc1a encodes a RING-H2 protein with a unique function in processing the Hh signal transducer Ci by the SCF E3 ubiquitin ligase. Dev Cell 2:757-770.
23. Sherr CJ, Roberts JM (1999) CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev 13:1501-1512.
24. Fero ML, et al. (1996) A syndrome of multiorgan hyperplasia with features of gigan-tism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85:733-744.
25. Kiyokawa H, et al. (1996) Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85:721-732.
26. Nakayama K, et al. (1996) Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85:707-720.
27. Perin JP, et al. (1999) Genomic organization and expression of the ubiquitin-proteasome complex-associated protein Rbx1/ROC1/Hrt1. Cell Mol Biol 45:1131-1137.
28. Sherr CJ, Roberts JM (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9:1149-1163.
29. Ciemerych MA, Yu Q, Szczepanska K, Sicinski P (2008) CDK4 activity in mouse embryos expressing a single D-type cyclin. Int J Dev Biol 52:299-305.
30. Nagahama H, Hatakeyama S, Nakayama K, Nagata M, Tomita K (2001) Spatial and temporal expression patterns of the cyclin-dependent kinase (CDK) inhibitors p27Kip1 and p57Kip2 during mouse development. Anat Embryol 203:77-87.
31. Swaroop M, et al. (2000) Yeast homolog of human SAG/ROC2/Rbx2/Hrt2 is essential for cell growth, but not for germination: Chip profiling implicates its role in cell cycle regulation. Oncogene 19:2855-2866.
32. Sasagawa Y, Urano T, Kohara Y, Takahashi H, Higashitani A (2003) Caenorhabditis elegans RBX1 is essential for meiosis, mitotic chromosomal condensation and segregation, and cytokinesis. Genes Cells 8:857-872.
33. Dealy MJ, et al. (1999) Loss of Cul1 results in early embryonic lethality and dysregula-tion of cyclin E. Nat Genet 23:245-248.
34. Singer JD, Gurian-West M, Clurman B, Roberts JM (1999) Cullin-3 targets cyclin E for ubiquitination and controls S phase in mammalian cells. Genes Dev 13:2375-2387.
35. Li B, Ruiz JC, Chun KT (2002) CUL-4A is critical for early embryonic development. Mol Cell Biol 22:4997-5005.
36. Arai T, et al. (2003) Targeted disruption of p185/Cul7 gene results in abnormal vascular morphogenesis. Proc Natl Acad Sci USA 100:9855-9860.
37. 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.
38. Hakem R, de la Pompa JL, Elia A, Potter J, Mak TW (1997) Partial rescue of Brca1 (5-6) early embryonic lethality by p53 or p21 null mutation. Nat Genet 16:298-302.
39. Donaldson TD, Noureddine MA, Reynolds PJ, Bradford W, Duronio RJ (2004) (2004) Targeted disruption of Drosophila Roc1b reveals functional differences in the Roc subunit of Cullin-dependent E3 ubiquitin ligases. Mol Biol Cell 15:4892-4903.
40. Nagy A, Gertsenstein M, Vintersten K, Behringer R (2003) Manipulating the Mouse Embryo: A Laboratory Manual (Cold Spring Harbor Lab Press, New York).
41. Hughes ED, et al. (2007) Genetic variation in C57BL/6 ES cell lines and genetic instability in the Bruce4 C57BL/6 ES cell line. Mamm Genome 18:549-558.
42. Duan H, et al. (1999) SAG, a novel zinc RING finger protein that protects cells from apoptosis induced by redox agents. Mol Cell Biol 19:3145-3155.