SUMOylation of RhoGDIα is required for its repression of cyclin D1 expression and anchorage-independent growth of cancer cells

Molecular Oncology

Volumn 8, Issue 2, 2014, Pages 285-296

  Cao, Zipeng ^a,b   Li, Xueyong ^a   Li, Jingxia ^a   Kang, Beipei ^b   Chen, Jingyuan ^b   Luo, Wenjing ^b   Huang, Chuanshu ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Anchorage independent growth; Cyclin D1; Growth arrest; RhoGDI ; SUMOylation

Indexed keywords

CYCLIN D1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PROTEIN C JUN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 1; TRANSCRIPTION FACTOR AP 1; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ARTICLE; CANCER CELL; CELL CYCLE G0 PHASE; CELL CYCLE PROGRESSION; DOWN REGULATION; ENZYME INHIBITION; G1 PHASE CELL CYCLE CHECKPOINT; GROWTH INHIBITION; HUMAN; HUMAN CELL; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUMOYLATION; CANCER GROWTH; CONTROLLED STUDY; CYCLIN D1 GENE; ENZYME ACTIVATION; GENE; GENETIC TRANSCRIPTION; TRANSACTIVATION; TUMOR INVASION;

ANCHORAGE-INDEPENDENT GROWTH; CYCLIN D1; GROWTH ARREST; RHOGDIΑ; SUMOYLATION;

AMINO ACID SUBSTITUTION; CELL LINE, TUMOR; CYCLIN D1; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE SIGNALING SYSTEM; NEOPLASMS; POINT MUTATION; PROTO-ONCOGENE PROTEINS C-JUN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR ALPHA; SUMOYLATION; TRANSCRIPTION, GENETIC;

EID: 84894343455     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.11.006     Document Type: Article

References (81)

1. Assoian R.K., Klein E.A. Growth control by intracellular tension and extracellular stiffness. Trends Cell Biol. 2008, 18:347-352.
2. Assoian R.K., Schwartz M.A. Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. Curr. Opin. Genet. Dev. 2001, 11:48-53.
3. Balmanno K., Cook S.J. Sustained MAP kinase activation is required for the expression of cyclin D1, p21Cip1 and a subset of AP-1 proteins in CCL39 cells. Oncogene 1999, 18:3085-3097.
4. Bohmer R.M., Scharf E., Assoian R.K. Cytoskeletal integrity is required throughout the mitogen stimulation phase of the cell cycle and mediates the anchorage-dependent expression of cyclin D1. Mol. Biol. Cell 1996, 7:101-111.
5. Coleman M.L., Marshall C.J., Olson M.F. RAS and RHO GTPases in G1-phase cell-cycle regulation. Nat. Rev. Mol. Cell Biol. 2004, 5:355-366.
6. Cook S.J., Aziz N., McMahon M. The repertoire of fos and jun proteins expressed during the G1 phase of the cell cycle is determined by the duration of mitogen-activated protein kinase activation. Mol. Cell. Biol. 1999, 19:330-341.
7. Croft D.R., Olson M.F. The Rho GTPase effector ROCK regulates cyclin A, cyclin D1, and p27Kip1 levels by distinct mechanisms. Mol. Cell. Biol. 2006, 26:4612-4627.
8. Dadke S., Cotteret S., Yip S.C., Jaffer Z.M., Haj F., Ivanov A., Rauscher F., Shuai K., Ng T., Neel B.G., Chernoff J. Regulation of protein tyrosine phosphatase 1B by sumoylation. Nat. Cell Biol. 2007, 9:80-85.
9. DerMardirossian C., Bokoch G.M. GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol. 2005, 15:356-363.
10. Desterro J.M., Rodriguez M.S., Hay R.T. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell 1998, 2:233-239.
11. Dovas A., Couchman J.R. RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochem. J. 2005, 390:1-9.
12. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
13. Fang J.Y., Richardson B.C. The MAPK signalling pathways and colorectal cancer. Lancet Oncol. 2005, 6:322-327.
14. Fang Y., Yu Y., Hou Q., Zheng X., Zhang M., Zhang D., Li J., Wu X.R., Huang C. The Chinese herb isolate isorhapontigenin induces apoptosis in human cancer cells by down-regulating overexpression of antiapoptotic protein XIAP. J.Biol. Chem. 2012, 287:35234-35243.
15. Faure J., Dagher M.C. Interactions between Rho GTPases and Rho GDP dissociation inhibitor (Rho-GDI). Biochimie 2001, 83:409-414.
16. Garcia-Mata R., Boulter E., Burridge K. The 'invisible hand': regulation of RHO GTPases by RHOGDIs. Nat. Rev. Mol. Cell Biol. 2011, 12:493-504.
17. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
18. Gill G. Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 2005, 15:536-541.
19. Gillett C., Smith P., Gregory W., Richards M., Millis R., Peters G., Barnes D. Cyclin D1 and prognosis in human breast cancer. Int. J. Cancer 1996, 69:92-99.
20. Harding M.A., Theodorescu D. RhoGDI signaling provides targets for cancer therapy. Eur. J. Cancer 2010, 46:1252-1259.
21. Hatzivassiliou G., Song K., Yen I., Brandhuber B.J., Anderson D.J., Alvarado R., Ludlam M.J., Stokoe D., Gloor S.L., Vigers G., et al. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 2010, 464:431-435.
22. Heidorn S.J., Milagre C., Whittaker S., Nourry A., Niculescu-Duvas I., Dhomen N., Hussain J., Reis-Filho J.S., Springer C.J., Pritchard C., Marais R. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 2010, 140:209-221.
23. Hirai A., Nakamura S., Noguchi Y., Yasuda T., Kitagawa M., Tatsuno I., Oeda T., Tahara K., Terano T., Narumiya S., et al. Geranylgeranylated rho small GTPase(s) are essential for the degradation of p27Kip1 and facilitate the progression from G1 to S phase in growth-stimulated rat FRTL-5 cells. J.Biol. Chem. 1997, 272:13-16.
24. Hoffman G.R., Nassar N., Cerione R.A. Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell 2000, 100:345-356.
25. Hu W., Bellone C.J., Baldassare J.J. RhoA stimulates p27(Kip) degradation through its regulation of cyclin E/CDK2 activity. J.Biol. Chem. 1999, 274:3396-3401.
26. Huang C., Ma W.Y., Dawson M.I., Rincon M., Flavell R.A., Dong Z. Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid. Proc. Natl. Acad. Sci. U S A 1997, 94:5826-5830.
27. Huang C., Ma W.Y., Dong Z. The extracellular-signal-regulated protein kinases (Erks) are required for UV-induced AP-1 activation in JB6 cells. Oncogene 1999, 18:2828-2835.
28. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 2004, 73:355-382.
29. King A.J., Sun H., Diaz B., Barnard D., Miao W., Bagrodia S., Marshall M.S. The protein kinase Pak3 positively regulates Raf-1 activity through phosphorylation of serine 338. Nature 1998, 396:180-183.
30. Klein E.A., Assoian R.K. Transcriptional regulation of the cyclin D1 gene at a glance. J.Cell Sci. 2008, 121:3853-3857.
31. Kotaja N., Karvonen U., Janne O.A., Palvimo J.J. PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol. 2002, 22:5222-5234.
32. Krens S.F., Spaink H.P., Snaar-Jagalska B.E. Functions of the MAPK family in vertebrate-development. FEBS Lett. 2006, 580:4984-4990.
33. Kubota Y., O'Grady P., Saito H., Takekawa M. Oncogenic Ras abrogates MEK SUMOylation that suppresses the ERK pathway and cell transformation. Nat. Cell Biol. 2011, 13:282-291.
34. Leng J., Klemke R.L., Reddy A.C., Cheresh D.A. Potentiation of cell migration by adhesion-dependent cooperative signals from the GTPase Rac and Raf kinase. J.Biol. Chem. 1999, 274:37855-37861.
35. Li W., Chong H., Guan K.L. Function of the Rho family GTPases in Ras-stimulated Raf activation. J.Biol. Chem. 2001, 276:34728-34737.
36. Li J., Chen H., Tang M.S., Shi X., Amin S., Desai D., Costa M., Huang C. PI-3K and Akt are mediators of AP-1 induction by 5-MCDE in mouse epidermal Cl41 cells. J.Cell Biol. 2004, 165:77-86.
37. Liberto M., Cobrinik D., Minden A. Rho regulates p21(CIP1), cyclin D1, and checkpoint control in mammary epithelial cells. Oncogene 2002, 21:1590-1599.
38. Liu J., Zhang D., Luo W., Yu Y., Yu J., Li J., Zhang X., Zhang B., Chen J., Wu X.R., et al. X-linked inhibitor of apoptosis protein (XIAP) mediates cancer cell motility via Rho GDP dissociation inhibitor (RhoGDI)-dependent regulation of the cytoskeleton. J.Biol. Chem. 2011, 286:15630-15640.
39. Liu J., Zhang D., Luo W., Yu J., Li J., Yu Y., Zhang X., Chen J., Wu X.R., Huang C. E3 ligase activity of XIAP RING domain is required for XIAP-mediated cancer cell migration, but not for its RhoGDI binding activity. PloS One 2012, 7:e35682.
40. Lu Q., Longo F.M., Zhou H., Massa S.M., Chen Y.H. Signaling through Rho GTPase pathway as viable drug target. Curr. Med. Chem. 2009, 16:1355-1365.
41. Luo W., Liu J., Li J., Zhang D., Liu M., Addo J.K., Patil S., Zhang L., Yu J., Buolamwini J.K., et al. Anti-cancer effects of JKA97 are associated with its induction of cell apoptosis via a Bax-dependent and p53-independent pathway. J.Biol. Chem. 2008, 283:8624-8633.
42. Malumbres M., Barbacid M. RAS oncogenes: the first 30 years. Nat. Rev. Cancer 2003, 3:459-465.
43. Melchior F. SUMO - nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 2000, 16:591-626.
44. Moissoglu K., McRoberts K.S., Meier J.A., Theodorescu D., Schwartz M.A. Rho GDP dissociation inhibitor 2 suppresses metastasis via unconventional regulation of RhoGTPases. Cancer Res. 2009, 69:2838-2844.
45. Molenaar J.J., Ebus M.E., Koster J., van Sluis P., van Noesel C.J., Versteeg R., Caron H.N. Cyclin D1 and CDK4 activity contribute to the undifferentiated phenotype in neuroblastoma. Cancer Res. 2008, 68:2599-2609.
46. Muller S., Hoege C., Pyrowolakis G., Jentsch S. SUMO, ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell Biol. 2001, 2:202-210.
47. Muller S., Ledl A., Schmidt D. SUMO: a regulator of gene expression and genome integrity. Oncogene 2004, 23:1998-2008.
48. Musgrove E.A. Cyclins: roles in mitogenic signaling and oncogenic transformation. Growth Factors 2006, 24:13-19.
49. Olson M.F., Paterson H.F., Marshall C.J. Signals from Ras and Rho GTPases interact to regulate expression of p21Waf1/Cip1. Nature 1998, 394:295-299.
50. Ouyang W., Ma Q., Li J., Zhang D., Liu Z.G., Rustgi A.K., Huang C. Cyclin D1 induction through IkappaB kinase beta/nuclear factor-kappaB pathway is responsible for arsenite-induced increased cell cycle G1-S phase transition in human keratinocytes. Cancer Res. 2005, 65:9287-9293.
51. Ouyang W., Luo W., Zhang D., Jian J., Ma Q., Li J., Shi X., Chen J., Gao J., Huang C. PI-3K/Akt pathway-dependent cyclin D1 expression is responsible for arsenite-induced human keratinocyte transformation. Environ. Health Perspect. 2008, 116:1-6.
52. Park E.R., Eblen S.T., Catling A.D. MEK1 activation by PAK: a novel mechanism. Cell. Signal. 2007, 19:1488-1496.
53. Park J., Kim K., Lee E.J., Seo Y.J., Lim S.N., Park K., Rho S.B., Lee S.H., Lee J.H. Elevated level of SUMOylated IRF-1 in tumor cells interferes with IRF-1-mediated apoptosis. Proc. Natl. Acad. Sci. U S A 2007, 104:17028-17033.
54. Porter K.E., Turner N.A., O'Regan D.J., Balmforth A.J., Ball S.G. Simvastatin reduces human atrial myofibroblast proliferation independently of cholesterol lowering via inhibition of RhoA. Cardiovasc. Res. 2004, 61:745-755.
55. Rajakulendran T., Sahmi M., Lefrancois M., Sicheri F., Therrien M. A dimerization-dependent mechanism drives RAF catalytic activation. Nature 2009, 461:542-545.
56. Ramakrishnan M., Musa N.L., Li J., Liu P.T., Pestell R.G., Hershenson M.B. Catalytic activation of extracellular signal-regulated kinases induces cyclin D1 expression in primary tracheal myocytes. Am. J. Respir. Cell Mol. Biol. 1998, 18:736-740.
57. Sahai E., Marshall C.J. RHO-GTPases and cancer. Nat. Rev. Cancer 2002, 2:133-142.
58. Sanchez-Mora N., Presmanes M.C., Monroy V., Moreno N., Lara-Martinez J.M., Aladro M.H., Alvarez-Fernandez E. Micropapillary lung adenocarcinoma: a distinctive histologic subtype with prognostic significance: case series. Hum. Pathol. 2008, 39:324-330.
59. Sasaki T., Takai Y. The Rho small G protein family-Rho GDI system as a temporal and spatial determinant for cytoskeletal control. Biochem. Biophys. Res. Commun. 1998, 245:641-645.
60. Schubbert S., Shannon K., Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer 2007, 7:295-308.
61. Sherr C.J. G1 phase progression: cycling on cue. Cell 1994, 79:551-555.
62. Snyder J.T., Worthylake D.K., Rossman K.L., Betts L., Pruitt W.M., Siderovski D.P., Der C.J., Sondek J. Structural basis for the selective activation of Rho GTPases by Dbl exchange factors. Nat. Struct. Biol. 2002, 9:468-475.
63. Sobko A., Ma H., Firtel R.A. Regulated SUMOylation and ubiquitination of DdMEK1 is required for proper chemotaxis. Dev. Cell 2002, 2:745-756.
64. Song L., Li J., Zhang D., Liu Z.G., Ye J., Zhan Q., Shen H.M., Whiteman M., Huang C. IKKbeta programs to turn on the GADD45alpha-MKK4-JNK apoptotic cascade specifically via p50 NF-kappaB in arsenite response. J.Cell Biol. 2006, 175:607-617.
65. Song L., Li J., Ye J., Yu G., Ding J., Zhang D., Ouyang W., Dong Z., Kim S.O., Huang C. p85alpha acts as a novel signal transducer for mediation of cellular apoptotic response to UV radiation. Mol. Cell. Biol. 2007, 27:2713-2731.
66. Stacey D.W. Cyclin D1 serves as a cell cycle regulatory switch in actively proliferating cells. Curr. Opin. Cell Biol. 2003, 15:158-163.
67. Swant J.D., Rendon B.E., Symons M., Mitchell R.A. Rho GTPase-dependent signaling is required for macrophage migration inhibitory factor-mediated expression of cyclin D1. J.Biol. Chem. 2005, 280:23066-23072.
68. Talarmin H., Rescan C., Cariou S., Glaise D., Zanninelli G., Bilodeau M., Loyer P., Guguen-Guillouzo C., Baffet G. The mitogen-activated protein kinase kinase/extracellular signal-regulated kinase cascade activation is a key signalling pathway involved in the regulation of G(1) phase progression in proliferating hepatocytes. Mol. Cell. Biol. 1999, 19:6003-6011.
69. Tanaka T., Tatsuno I., Noguchi Y., Uchida D., Oeda T., Narumiya S., Yasuda T., Higashi H., Kitagawa M., Nakayama K., et al. Activation of cyclin-dependent kinase 2 (Cdk2) in growth-stimulated rat astrocytes. Geranylgeranylated Rho small GTPase(s) are essential for the induction of cyclin E gene expression. J.Biol. Chem. 1998, 273:26772-26778.
70. Tzima E. Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. Circ. Res. 2006, 98:176-185.
71. Van Aelst L., D'Souza-Schorey C. Rho GTPases and signaling networks. Genes Dev. 1997, 11:2295-2322.
72. Vega F.M., Ridley A.J. Rho GTPases in cancer cell biology. FEBS Lett. 2008, 582:2093-2101.
73. Wang Z., Thurmond D.C. Differential phosphorylation of RhoGDI mediates the distinct cycling of Cdc42 and Rac1 to regulate second-phase insulin secretion. J.Biol. Chem. 2010, 285:6186-6197.
74. Wang J., Ouyang W., Li J., Wei L., Ma Q., Zhang Z., Tong Q., He J., Huang C. Loss of tumor suppressor p53 decreases PTEN expression and enhances signaling pathways leading to activation of activator protein 1 and nuclear factor kappaB induced by UV radiation. Cancer Res. 2005, 65:6601-6611.
75. Watanabe G., Lee R.J., Albanese C., Rainey W.E., Batlle D., Pestell R.G. Angiotensin II activation of cyclin D1-dependent kinase activity. J.Biol. Chem. 1996, 271:22570-22577.
76. Welsh C.F., Roovers K., Villanueva J., Liu Y., Schwartz M.A., Assoian R.K. Timing of cyclin D1 expression within G1 phase is controlled by Rho. Nat. Cell Biol. 2001, 3:950-957.
77. Yamamoto M., Tamakawa S., Yoshie M., Yaginuma Y., Ogawa K. Neoplastic hepatocyte growth associated with cyclin D1 redistribution from the cytoplasm to the nucleus in mouse hepatocarcinogenesis. Mol. Carcinog. 2006, 45:901-913.
78. Young A., Lyons J., Miller A.L., Phan V.T., Alarcon I.R., McCormick F. Ras signaling and therapies. Adv. Cancer Res. 2009, 102:1-17.
79. Yu J., Zhang D., Liu J., Li J., Yu Y., Wu X.R., Huang C. RhoGDI SUMOylation at Lys-138 increases its binding activity to Rho GTPase and its inhibiting cancer cell motility. J.Biol. Chem. 2012, 287:13752-13760.
80. Zhang D., Song L., Li J., Wu K., Huang C. Coordination of JNK1 and JNK2 is critical for GADD45alpha induction and its mediated cell apoptosis in arsenite responses. J.Biol. Chem. 2006, 281:34113-34123.
81. Zhang J., Ouyang W., Li J., Zhang D., Yu Y., Wang Y., Li X., Huang C. Suberoylanilide hydroxamic acid (SAHA) inhibits EGF-induced cell transformation via reduction of cyclin D1 mRNA stability. Toxicol. Appl. Pharmacol. 2012, 263:218-224.