Siah1/SIP regulates p27kip1 stability and cell migration under metabolic stress

Cell Cycle

Volumn 10, Issue 15, 2011, Pages 2592-2602

  Nagano, Yoshito ^a   Fukushima, Toru ^a,d   Okemoto, Kazuo ^a   Tanaka, Keiichiro ^a   Bowtell, David D L ^b,c   Ronai, Ze'ev A ^a   Reed, John C ^a   Matsuzawa, Shu Ichi ^a  

^a BURNHAM INSTITUTE   (United States)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

Cell migration; Glucose starvation; Siah1; SIP

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; PROTEIN; PROTEIN SIAH1; PROTEIN SIP; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; METABOLIC STRESS; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

EID: 79961116969     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.15.16912     Document Type: Article

References (56)

1. Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature 1994; 372:570-3; PMID: 7990932; DOI: 10.1038/372570a0.
2. Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 1994; 8:9-22; PMID: 8288131; DOI: 10.1101/gad.8.1.9.
3. 1 cyclin-Cdk protein kinase activity, is related to p21. Cell 1994; 78:67-74; PMID: 8033213; DOI: 10.1016/0092-8674(94)90573-8.
4. Kip1 for restriction point control of the fibroblast cell cycle. Science 1996; 272:877-80; PMID: 8629023; DOI: 10.1126/science.272.5263.877.
5. Kip1 expression is required for development and function of T cells. J Immunol 2001; 166:304-12; PMID: 11123306.
6. kip1 C-terminal scatter domain mediates Rac-dependent cell migration independent of cell cycle arrest functions. Mol Cell Biol 2003; 23:216-28; PMID: 12482975; DOI: 10.1128/MCB.23.1.216-28.2003.
7. Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev 2004; 18:862-76; PMID: 15078817; DOI: 10.1101/gad.1185504.
8. Kip1-deficient mice. Cell 1996; 85:733-44; PMID: 8646781; DOI: 10.1016/S0092-8674(00)81239-8.
9. Kip1. Cell 1996; 85:721-32; PMID: 8646780; DOI: 10.1016/S0092-8674(00)81238-6.
10. Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia and pituitary tumors. Cell 1996; 85:707-20; PMID: 8646779; DOI: 10.1016/S0092-8674(00)81237-4.
11. Slingerland J, Pagano M. Regulation of the cdk inhibitor p27 and its deregulation in cancer. J Cell Physiol 2000; 183:10-7; PMID: 10699961; DOI: 10.1002/(SICI)1097-4652(200004)183:1⟨10::AID-JCP2⟩3.0.CO;2-I.
12. Kip1: regulation and function of a haploinsufficient tumor suppressor and its misregulation in cancer. Exp Cell Res 2001; 264:148-68; PMID: 11237531; DOI: 10.1006/excr.2000. 5143.
13. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, Han K, et al. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat Med 2002; 8:1153-60; PMID: 12244302; DOI: 10.1038/nm761.
14. Kip1 at threonine 157 and modulation of its cellular localization. Nat Med 2002; 8:1145-52; PMID: 12244301; DOI: 10.1038/nm759.
15. Kip1 by PKB/Akt-mediated phosphorylation in breast cancer. Nat Med 2002; 8:1136-44; PMID: 12244303; DOI: 10.1038/nm762.
16. kip1 expression predicts poor prognosis in human ovarian cancer. Clin Cancer Res 2005; 11:632-7; PMID: 15701850.
17. Kip1 tumor suppressor functions as a cytoplasmic metastatic oncogene in melanoma. Cancer Res 2007; 67:9238-43; PMID: 17909030; DOI: 10.1158/0008-5472.CAN-07-1375.
18. Carrano AC, Eytan E, Hershko A, Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1999; 1:193-9; PMID: 10559916; DOI: 10.1038/12013.
19. Montagnoli A, Fiore F, Eytan E, Carrano AC, Draetta GF, Hershko A, et al. Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev 1999; 13:1181-9; PMID: 10323868; DOI: 10.1101/gad.13.9.1181.
20. Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol 1999; 1:207-14; PMID: 10559918; DOI: 10.1038/12027.
21. Bashir T, Pagan JK, Busino L, Pagano M. Phosphorylation of Ser72 is dispensable for Skp2 assembly into an active SCF ubiquitin ligase and its subcellular localization. Cell Cycle 2010; 9:971-4; PMID: 20160477; DOI: 10.4161/cc.9.5.10914.
22. Kip1 phosphorylation. Cell Cycle 2010; 9:2057-8; PMID: 20505330; DOI: 10.4161/cc.9.11.11927.
23. 1 and S phase. Nature 2001; 413:323-7; PMID: 11565035; DOI: 10.1038/35095083.
24. 1 phase. Nat Cell Biol 2004; 6:1229-35; PMID: 15531880; DOI: 10.1038/ncb1194.
25. kip1. EMBO J 2006; 25:5159-70; PMID: 17053782; DOI: 10.1038/sj.emboj.7601388.
26. Della NG, Senior PV, Bowtell DD. Isolation and characterisation of murine homologues of the Drosophila seven in absentia gene (sina). Development 1993; 117:1333-43; PMID: 8404535.
27. Hu G, Chung YL, Glover T, Valentine V, Look AT, Fearon ER. Characterization of human homologs of the Drosophila seven in absentia (sina) gene. Genomics 1997; 46:103-11; PMID: 9403064; DOI: 10.1006/geno.1997.4997.
28. Matsuzawa S, Takayama S, Froesch BA, Zapata JM, Reed JC. p53-inducible human homologue of Drosophila seven in absentia (Siah) inhibits cell growth: suppression by BAG-1. EMBO J 1998; 17:2736-47; PMID: 9582267; DOI: 10.1093/emboj/17.10.2736.
29. Reed JC, Ely K. Degrading Liaisons: Siah structure revealed. Nat Struct Biol 2002; 9:8-10; PMID: 11753426; DOI: 10.1038/nsb0102-8.
30. Matsuzawa SI, Reed JC. Siah-1, SIP and Ebi collaborate in a novel pathway for β-catenin degradation linked to p53 responses. Mol Cell 2001; 7:915-26; PMID: 11389839; DOI: 10.1016/S1097-2765(01)00242-8.
31. Filipek A, Kuznicki J. Molecular cloning and expression of a mouse brain cDNA encoding a novel protein target of calcyclin. J Neurochem 1998; 70:1793-8; PMID: 9572262; DOI: 10.1046/j.1471-4159.1998.70051793.x.
32. Filipek A, Jastrzebska B, Nowotny M, Kuznicki J. CacyBP/SIP, a calcyclin and Siah-1-interacting protein, binds EF-hand proteins of the S100 family. J Biol Chem 2002; 277:28848-52; PMID: 12042313; DOI: 10.1074/jbc.M203602200.
33. Matsuzawa S, Li C, Ni CZ, Takayama S, Reed JC, Ely KR. Structural analysis of Siah1 and its interactions with Siah-interacting protein (SIP). J Biol Chem 2003; 278:1837-40; PMID: 12421809; DOI: 10.1074/jbc.M210263200.
34. Santelli E, Leone M, Li C, Fukushima T, Preece NE, Olson AJ, et al. Structural analysis of Siah1-SIP interactions and insights into the assembly of an E3 ligase multiprotein complex. J Biol Chem 2005; 280:34278-87; PMID: 16085652; DOI: 10.1074/jbc.M506707200.
35. Amson RB, Nemani M, Roperch JP, Israeli D, Bougueleret L, Le Gall I, et al. Isolation of 10 differentially expressed cDNAs in p53-induced apoptosis: activation of the vertebrate homologue of the Drosphila seven in absentia gene. Proc Natl Acad Sci USA 1996; 93:3953-7; PMID: 8632996; DOI: 10.1073/pnas.93.9. 3953.
36. Iwai A, Marusawa H, Matsuzawa S, Fukushima T, Hijikata M, Reed JC, et al. Siah-1L, a novel transcript variant belonging to the human Siah family of proteins, regulates beta-catenin activity in a p53-dependent manner. Oncogene 2004; 23:7593-600; PMID: 15326481; DOI: 10.1038/sj.onc.1208016.
37. Fiucci G, Beaucourt S, Duflaut D, Lespagnol A, Stumptner-Cuvelette P, Geant A, et al. Siah-1b is a direct transcriptional target of p53: identification of the functional p53 responsive element in the siah-1b promoter. Proc Natl Acad Sci USA 2004; 101:3510-5; Epub 2004 Feb 25.
38. Horikawa I, Fujita K, Harris CC. p53 governs telomere regulation feedback too, via TRF2. Aging (Albany NY) 2011; 3:26-32; PMID: 21266744.
39. 1 checkpoint. Immunity 2006; 24:29-39; PMID: 16413921; DOI: 10.1016/j.immuni.2005. 12.002.
40. House CM, Frew IJ, Huang HL, Wiche G, Traficante N, Nice E, et al. A binding motif for Siah ubiquitin ligase. Proc Natl Acad Sci USA 2003; 100:3101-6; PMID: 12626763; DOI: 10.1073/pnas.0534783100.
41. Kip1 drives cell motility in glioma cells. Cell Cycle 2010; 9:1231-40; PMID: 20404527; DOI: 10.4161/cc.9.7.11366.
42. See WL, Heinberg AR, Holland EC, Resh MD. p27 deficiency is associated with migration defects in PDGF-expressing gliomas in vivo. Cell Cycle 2010; 9:1562-7; PMID: 20404478; DOI: 10.4161/cc.9.8.11259.
43. Kip1 inhibits cancer cell motility, survival and tumorigenicity. Cancer Res 2006; 66:2162-72; PMID: 16489017; DOI: 10.1158/0008-5472.CAN-05-3304.
44. kip1 in restriction of breast cancer progression. Cancer Res 2007; 67:8032-42; PMID: 17804714; DOI: 10.1158/0008-5472.CAN-07-0083.
45. Kip1, increases its protein stability. J Biol Chem 2000; 275:25146-54; PMID: 10831586; DOI: 10.1074/jbc.M001144200.
46. Rodier G, Montagnoli A, Di Marcotullio L, Coulombe P, Draetta GF, Pagano M, et al. p27 cytoplasmic localization is regulated by phosphorylation on Ser10 and is not a prerequisite for its proteolysis. EMBO J 2001; 20:6672-82; PMID: 11726503; DOI: 10.1093/emboj/20.23.6672.
47. Besson A, Assoian RK, Roberts JM. Regulation of the cytoskeleton: an oncogenic function for CDK inhibitors? Nat Rev Cancer 2004; 4:948-55; PMID: 15573116; DOI: 10.1038/nrc1501.
48. Ning X, Sun S, Hong L, Liang J, Liu L, Han S, et al. Calcyclin-binding protein inhibits proliferation, tumorigenicity and invasion of gastric cancer. Mol Cancer Res 2007; 5:1254-62; PMID: 18171983; DOI: 10.1158/1541-7786.MCR-06- 0426.
49. Schneider G, Nieznanski K, Kilanczyk E, Bieganowski P, Kuznicki J, Filipek A. CacyBP/SIP interacts with tubulin in neuroblastoma NB2a cells and induces formation of globular tubulin assemblies. Biochim Biophys Acta 2007; 1773:1628-36.
50. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, et al. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 2005; 18:283-93; PMID: 15866171; DOI: 10.1016/j.molcel.2005.03.027.
51. Carling D. The AMP-activated protein kinase cascade - a unifying system for energy control. Trends Biochem Sci 2004; 29:18-24; PMID: 14729328; DOI: 10.1016/j.tibs.2003.11.005.
52. kip1 phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 2007; 9:218-24; PMID: 17237771; DOI: 10.1038/ncb1537.
53. Kip1. Cancer Res 2007; 67:10789-95; PMID: 18006823; DOI: 10.1158/0008-5472.CAN-07-2033.
54. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, et al. Cell migration: integrating signals from front to back. Science 2003; 302:1704-9; PMID: 14657486; DOI: 10.1126/science.1092053.
55. Khusial PR, Vadla B, Krishnan H, Ramlall TF, Shen Y, Ichikawa H, et al. Src activates Abl to augment Robo1 expression in order to promote tumor cell migration. Oncotarget 2010; 1:198-209; PMID: 21301049.
56. Wang L, Zhang J, Banerjee S, Barnes L, Sajja V, Liu Y, et al. Sumoylation of vimentin354 is associated with PIAS3 inhibition of glioma cell migration. Oncotarget 2010; 1:620-7; PMID: 21317457.