ARHGAP21 is a RhoGAP for RhoA and RhoC with a role in proliferation and migration of prostate adenocarcinoma cells

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 2, 2013, Pages 365-374

  Lazarini, Mariana ^a   Traina, Fabiola ^a   Machado Neto, João A ^a   Barcellos, Karin S A ^a   Moreira, Yuri B ^b   Brandão, Marcelo M ^b   Verjovski Almeida, Sergio ^b   Ridley, Anne J ^c   Saad, Sara T Olalla ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

ARHGAP21; Endothelin 1; PC3; Prostate adenocarcinoma; RhoA; RhoC

Indexed keywords

ENDOTHELIN 1; FIBRONECTIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN ARHGAP21; PROTEIN RHOC; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CARCINOMA CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL GROWTH; CELL INTERACTION; CELL MIGRATION; CELL NUCLEUS; CELL PROLIFERATION; CELL STRAIN LNCAP; CELL STRUCTURE; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; SIGNAL TRANSDUCTION;

ADENOCARCINOMA; BASE SEQUENCE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DNA PRIMERS; GENE SILENCING; GTPASE-ACTIVATING PROTEINS; HUMANS; IN SITU NICK-END LABELING; MALE; PROSTATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84871807496     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.11.010     Document Type: Article

References (58)

1. Anthony D.F., Sin Y.Y., Vadrevu S., Advant N., Day J.P., Byrne A.M., Lynch M.J., Milligan G., Houslay M.D., Baillie G.S. beta-Arrestin 1 inhibits the GTPase-activating protein function of ARHGAP21, promoting activation of RhoA following angiotensin II type 1A receptor stimulation. Mol. Cell. Biol. 2011, 31:1066-1075.
2. Basseres D.S., Tizzei E.V., Duarte A.A., Costa F.F., Saad S.T. ARHGAP10, a novel human gene coding for a potentially cytoskeletal Rho-GTPase activating protein. Biochem. Biophys. Res. Commun. 2002, 294:579-585.
3. Borges L., Bigarella C.L., Baratti M.O., Crosara-Alberto D.P., Joazeiro P.P., Franchini K.G., Costa F.F., Saad S.T. ARHGAP21 associates with FAK and PKCzeta and is redistributed after cardiac pressure overload. Biochem. Biophys. Res. Commun. 2008, 374:641-646.
4. Vega F.M., Ridley A.J. Rho GTPases in cancer cell biology. FEBS Lett. 2008, 582:2093-2101.
5. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
6. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 2005, 21:247-269.
7. Hakem A., Sanchez-Sweatman O., You-Ten A., Duncan G., Wakeham A., Khokha R., Mak T.W. RhoC is dispensable for embryogenesis and tumor initiation but essential for metastasis. Genes Dev. 2005, 19:1974-1979.
8. Bishop A.L., Hall A. Rho GTPases and their effector proteins. Biochem. J. 2000, 348(Pt. 2):241-255.
9. Sousa S., Cabanes D., Archambaud C., Colland F., Lemichez E., Popoff M., Boisson-Dupuis S., Gouin E., Lecuit M., Legrain P., Cossart P. ARHGAP10 is necessary for alpha-catenin recruitment at adherens junctions and for Listeria invasion. Nat. Cell Biol. 2005, 7:954-960.
10. Dubois T., Paleotti O., Mironov A.A., Fraisier V., Stradal T.E., De Matteis M.A., Franco M., Chavrier P. Golgi-localized GAP for Cdc42 functions downstream of ARF1 to control Arp2/3 complex and F-actin dynamics. Nat. Cell Biol. 2005, 7:353-364.
11. Bigarella C.L., Borges L., Costa F.F., Saad S.T. ARHGAP21 modulates FAK activity and impairs glioblastoma cell migration. Biochim. Biophys. Acta 2009, 1793:806-816.
12. Dubois T., Chavrier P. ARHGAP10, a novel RhoGAP at the cross-road between ARF1 and Cdc42 pathways, regulates Arp2/3 complex and actin dynamics on Golgi membranes. Med. Sci. (Paris) 2005, 21:692-694.
13. Wang S., Li H., Chen Y., Wei H., Gao G.F., Liu H., Huang S., Chen J.L. Transport of influenza A virus neuraminidase (NA) to host cell surface is regulated by ARHGAP21 and Cdc42. J. Biol. Chem. 2012, 287:9804-9816.
14. Carles A., Millon R., Cromer A., Ganguli G., Lemaire F., Young J., Wasylyk C., Muller D., Schultz I., Rabouel Y., Dembele D., Zhao C., Marchal P., Ducray C., Bracco L., Abecassis J., Poch O., Wasylyk B. Head and neck squamous cell carcinoma transcriptome analysis by comprehensive validated differential display. Oncogene 2006, 25:1821-1831.
15. Liao Y.C., Lo S.H. Deleted in liver cancer-1 (DLC-1): a tumor suppressor not just for liver. Int. J. Biochem. Cell Biol. 2008, 40:843-847.
16. Durkin M.E., Ullmannova V., Guan M., Popescu N.C. Deleted in liver cancer 3 (DLC-3), a novel Rho GTPase-activating protein, is downregulated in cancer and inhibits tumor cell growth. Oncogene 2007, 26:4580-4589.
17. Gen Y., Yasui K., Zen K., Nakajima T., Tsuji K., Endo M., Mitsuyoshi H., Minami M., Itoh Y., Tanaka S., Taniwaki M., Arii S., Okanoue T., Yoshikawa T. A novel amplification target, ARHGAP5, promotes cell spreading and migration by negatively regulating RhoA in Huh-7 hepatocellular carcinoma cells. Cancer Lett. 2009, 275:27-34.
18. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J. Clin. 2011, 61:69-90.
19. Shen M.M., Abate-Shen C. Molecular genetics of prostate cancer: new prospects for old challenges. Genes Dev. 2010, 24:1967-2000.
20. Chiao J.W., Moonga B.S., Yang Y.M., Kancherla R., Mittelman A., Wu-Wong J.R., Ahmed T. Endothelin-1 from prostate cancer cells is enhanced by bone contact which blocks osteoclastic bone resorption. Br. J. Cancer 2000, 83:360-365.
21. Lopergolo A., Zaffaroni N. Biomolecular markers of outcome prediction in prostate cancer. Cancer 2009, 115:3058-3067.
22. Vega F.M., Fruhwirth G., Ng T., Ridley A.J. RhoA and RhoC have distinct roles in migration and invasion by acting through different targets. J. Cell Biol. 2011, 193:655-665.
23. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
24. Takesono A., Heasman S.J., Wojciak-Stothard B., Garg R., Ridley A.J. Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells. PLoS One 2010, 5:e8774.
25. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5116-5121.
26. Gotz S., Garcia-Gomez J.M., Terol J., Williams T.D., Nagaraj S.H., Nueda M.J., Robles M., Talon M., Dopazo J., Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008, 36:3420-3435.
27. van Zijl F., Krupitza G., Mikulits W. Initial steps of metastasis: cell invasion and endothelial transmigration. Mutat. Res. 2011, 728:23-34.
28. Reymond N., Riou P., Ridley A.J. Rho GTPases and cancer cell transendothelial migration. Methods Mol. Biol. 2012, 827:123-142.
29. Xie S., Zhu M., Lv G., Zhang Q., Wang G. The role of RhoC in the proliferation and apoptosis of hepatocellular carcinoma cells. Med. Oncol. 2012, 29:1802-1809.
30. Faried A., Faried L.S., Kimura H., Nakajima M., Sohda M., Miyazaki T., Kato H., Usman N., Kuwano H. RhoA and RhoC proteins promote both cell proliferation and cell invasion of human oesophageal squamous cell carcinoma cell lines in vitro and in vivo. Eur. J. Cancer 2006, 42:1455-1465.
31. Wang L., Yang L., Luo Y., Zheng Y. A novel strategy for specifically down-regulating individual Rho GTPase activity in tumor cells. J. Biol. Chem. 2003, 278:44617-44625.
32. Bagnato A., Loizidou M., Pflug B.R., Curwen J., Growcott J. Role of the endothelin axis and its antagonists in the treatment of cancer. Br. J. Pharmacol. 2011, 163:220-233.
33. Papsidero L.D., Kuriyama M., Wang M.C., Horoszewicz J., Leong S.S., Valenzuela L., Murphy G.P., Chu T.M. Prostate antigen: a marker for human prostate epithelial cells. J. Natl. Cancer Inst. 1981, 66:37-42.
34. Araki S., Omori Y., Lyn D., Singh R.K., Meinbach D.M., Sandman Y., Lokeshwar V.B., Lokeshwar B.L. Interleukin-8 is a molecular determinant of androgen independence and progression in prostate cancer. Cancer Res. 2007, 67:6854-6862.
35. Saleem M., Adhami V.M., Zhong W., Longley B.J., Lin C.Y., Dickson R.B., Reagan-Shaw S., Jarrard D.F., Mukhtar H. A novel biomarker for staging human prostate adenocarcinoma: overexpression of matriptase with concomitant loss of its inhibitor, hepatocyte growth factor activator inhibitor-1. Cancer Epidemiol. Biomarkers Prev. 2006, 15:217-227.
36. Laidler P., Dulinska J., Lekka M., Lekki J. Expression of prostate specific membrane antigen in androgen-independent prostate cancer cell line PC-3. Arch. Biochem. Biophys. 2005, 435:1-14.
37. Banerjee A.G., Liu J., Yuan Y., Gopalakrishnan V.K., Johansson S.L., Dinda A.K., Gupta N.P., Trevino L., Vishwanatha J.K. Expression of biomarkers modulating prostate cancer angiogenesis: differential expression of annexin II in prostate carcinomas from India and USA. Mol. Cancer 2003, 2:34.
38. Dozmorov M.G., Hurst R.E., Culkin D.J., Kropp B.P., Frank M.B., Osban J., Penning T.M., Lin H.K. Unique patterns of molecular profiling between human prostate cancer LNCaP and PC-3 cells. Prostate 2009, 69:1077-1090.
39. Kaibuchi K., Kuroda S., Amano M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 1999, 68:459-486.
40. Sahai E., Marshall C.J. ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat. Cell Biol. 2002, 4:408-415.
41. Simpson K.J., Dugan A.S., Mercurio A.M. Functional analysis of the contribution of RhoA and RhoC GTPases to invasive breast carcinoma. Cancer Res. 2004, 64:8694-8701.
42. Dietrich K.A., Schwarz R., Liska M., Grass S., Menke A., Meister M., Kierschke G., Langle C., Genze F., Giehl K. Specific induction of migration and invasion of pancreatic carcinoma cells by RhoC, which differs from RhoA in its localisation and activity. Biol. Chem. 2009, 390:1063-1077.
43. Bellovin D.I., Simpson K.J., Danilov T., Maynard E., Rimm D.L., Oettgen P., Mercurio A.M. Reciprocal regulation of RhoA and RhoC characterizes the EMT and identifies RhoC as a prognostic marker of colon carcinoma. Oncogene 2006, 25:6959-6967.
44. Schmidt A., Hall A. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 2002, 16:1587-1609.
45. Bustos R.I., Forget M.A., Settleman J.E., Hansen S.H. Coordination of Rho and Rac GTPase function via p190B RhoGAP. Curr. Biol. 2008, 18:1606-1611.
46. Xu H., Eleswarapu S., Geiger H., Szczur K., Daria D., Zheng Y., Settleman J., Srour E.F., Williams D.A., Filippi M.D. Loss of the Rho GTPase activating protein p190-B enhances hematopoietic stem cell engraftment potential. Blood 2009, 114:3557-3566.
47. Tatsis N., Lannigan D.A., Macara I.G. The function of the p190 Rho GTPase-activating protein is controlled by its N-terminal GTP binding domain. J. Biol. Chem. 1998, 273:34631-34638.
48. Arthur W.T., Burridge K. RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol. Biol. Cell 2001, 12:2711-2720.
49. Kawanabe Y., Nauli S.M. Endothelin. Cell. Mol. Life Sci. 2011, 68:195-203.
50. Nelson J., Bagnato A., Battistini B., Nisen P. The endothelin axis: emerging role in cancer. Nat. Rev. Cancer 2003, 3:110-116.
51. Nelson J.B., Hedican S.P., George D.J., Reddi A.H., Piantadosi S., Eisenberger M.A., Simons J.W. Identification of endothelin-1 in the pathophysiology of metastatic adenocarcinoma of the prostate. Nat. Med. 1995, 1:944-949.
52. Kopetz E.S., Nelson J.B., Carducci M.A. Endothelin-1 as a target for therapeutic intervention in prostate cancer. Invest. New Drugs 2002, 20:173-182.
53. Carducci M.A., Padley R.J., Breul J., Vogelzang N.J., Zonnenberg B.A., Daliani D.D., Schulman C.C., Nabulsi A.A., Humerickhouse R.A., Weinberg M.A., Schmitt J.L., Nelson J.B. Effect of endothelin-A receptor blockade with atrasentan on tumor progression in men with hormone-refractory prostate cancer: a randomized, phase II, placebo-controlled trial. J. Clin. Oncol. 2003, 21:679-689.
54. Michaelson M.D., Kaufman D.S., Kantoff P., Oh W.K., Smith M.R. Randomized phase II study of atrasentan alone or in combination with zoledronic acid in men with metastatic prostate cancer. Cancer 2006, 107:530-535.
55. Nelson J.B. Endothelin inhibition: novel therapy for prostate cancer. J. Urol. 2003, 170:S65-S67. (discussion S67-68).
56. Lagares D., Busnadiego O., Garcia-Fernandez R.A., Lamas S., Rodriguez-Pascual F. Adenoviral gene transfer of ET-1 in the lung induces pulmonary fibrosis through FAK activation. Am. J. Respir. Cell Mol. Biol. 2012, 47:834-842.
57. Mori K., Amano M., Takefuji M., Kato K., Morita Y., Nishioka T., Matsuura Y., Murohara T., Kaibuchi K. Rho-kinase contributes to sustained RhoA activation through phosphorylation of p190A RhoGAP. J. Biol. Chem. 2009, 284:5067-5076.
58. Rosano L., Cianfrocca R., Masi S., Spinella F., Di Castro V., Biroccio A., Salvati E., Nicotra M.R., Natali P.G., Bagnato A. Beta-arrestin links endothelin A receptor to beta-catenin signaling to induce ovarian cancer cell invasion and metastasis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2806-2811.