RhoC is an unexpected target of RhoGDI2 in prevention of lung colonization of bladder cancer

Molecular Cancer Research

Volumn 13, Issue 3, 2015, Pages 483-492

  Griner, Erin M ^a   Dancik, Garrett M ^b   Costello, James C ^c   Owens, Charles ^c   Guin, Sunny ^c   Edwards, Michael G ^d   Brautigan, David L ^a   Theodorescu, Dan ^c,e  

^a UNIVERSITY OF VIRGINIA   (United States)

^b EASTERN CONNECTICUT STATE UNIVERSITY   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIGEL; PROTEIN RHOC; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 2; TRANSCRIPTOME; UNCLASSIFIED DRUG; ARHGDIB PROTEIN, HUMAN; RAC1 PROTEIN, HUMAN; RHOC PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER CANCER; CANCER CELL; CANCER GROWTH; CANCER PREVENTION; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TUMOR INVASION; ANIMAL; BLADDER TUMOR; CANCER TRANSPLANTATION; CELL MOTION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; LUNG TUMOR; METABOLISM; PATHOLOGY; PROTEOMICS; SECONDARY;

MUS;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MICE; NEOPLASM TRANSPLANTATION; PROTEOMICS; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR BETA; URINARY BLADDER NEOPLASMS;

EID: 84928007454     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0420     Document Type: Article

References (40)

1. Hall A. Rho family GTPases. Biochem Soc Trans 2012;40:1378-82.
2. Rathinam R, Berrier A, Alahari SK. Role of Rho GTPases and their regulators in cancer progression. Front Biosci (Landmark Ed) 2011; 16:2561-71.
3. Ridley AJ. Rho A, RhoB and RhoC have different roles in cancer cell migration. J Microsc 2013;251:242-9.
4. 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.
5. Theodorescu D, Sapinoso LM, Conaway MR, Oxford G, Hampton GM, Frierson HF. Reduced expression of metastasis suppressor RhoGD12 is associated with decreased survival for patients with bladder cancer. Clin Cancer Res 2004;10:3800-6.
6. Ma L, Xu G, Sotnikova A, Szczepanowski M, Giefing M, Krause K, et al. Loss of expression of LyGDI (ARHGDIB), a rho GDP-dissociation inhibitor, in Hodgkin lymphoma. Br J Haematol 2007;139:217-23.
7. Niu H, Li H, Xu C, He P. Expression profile of RhoGDI2 in lung cancers and role of RhoGDI2 in lung cancer metastasis. Oncol Rep 2010;24:465-71.
8. Gildea JJ, Seraj MJ, Oxford G, Harding MA, Hampton GM, Moskaluk CA, et al. RhoGD12 is an invasion and metastasis suppressor gene in human cancer. Cancer Res 2002;62:6418-23.
9. Said N, Smith SC, Sanchez-Carbayo M, Theodorescu D. RhoGDI2 suppresses metastasis via reduction of versican expression and macrophage infiltration. J Clin Invest 2012;122:1503-18.
10. Titus B, Frierson HF, Conaway M, Ching K, Guise T, Chirgwin J, et al. Endothelin axis is a target of the lung metastasis suppressor gene RhoGD12. Cancer Res 2005;65:7320-7.
11. Said N, Smith S, Sanchez-Carbayo M, Theodorescu D. Tumor endothelin-1 enhances metastatic colonization of the lung in mouse xenograft models of bladder cancer. J Clin Invest 2011;121:132-47.
12. Wu Y, Moissogiu K, Wang H, Wang X, Frierson HF, Schwartz MA, et al. Src phosphorylation of RhoGDI2 regulates its metastasis suppressor function. Proc Natl Acad Sci U S A 2009;106:5807-12.
13. Gorvel JP, Chang TC, Boretto J, Azuma T, Chavrier P. Differential properties of D4/LyGDI versus RhoGDI: phosphorylation and rho GTPase selectivity. FEBS Lett 1998;422:269-73.
14. Scherle P, Behrens T, Staudt LM. LY-GDI, A GDP-dissociation inhibitor of the RhoA GTP-binding protein, is expressed preferentially in lymphocytes. Proc Natl Acad Sci U S A 1993;90:7568-72.
15. Moissoglu K, McRoberts KS, Meier JA, Theodorescu D, Schwartz MA. Rho GDP dissociation inhibitor 2 suppresses metastasis via unconventional regulation of RhoGTPases. Cancer Res 2009;69:2838-44.
16. Overdevest JB, Thomas S, Kristiansen G, Hansel DE, Smith SC, Theodorescu D. CD24 offers a therapeutic target for control of bladder cancer metastasis based on a requirement for lung colonization. Cancer Res 2011;71:3802-11.
17. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, Hinkle G, et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 2006;124:1283-98.
18. Nitz MD, Harding MA, Theodorescu D. Invasion and metastasis models for studying RhoGDI2 in bladder cancer. Methods Enzymol 2008; 439:219-33.
19. Sanchez-Carbayo M, Socci ND, Lozano J, Saint F, Cordon-Cardo C. Defining molecular profiles of poor outcome in patients with invasive bladder cancer using oligonucleotide microarrays. J Clin Oncol 2006;24:778-89.
20. Kim WJ, Kim EJ, Kim SK, Kim YJ, Ha YS, Jeong P, et al. Predictive value of progression-related gene classifier in primary non-muscle invasive bladder cancer. Mol Cancer 2010;9:3.
21. Miller JA, Cai C, Langfelder P, Geschwind DH, Kurian SM, Salomon DR, et al. Strategies for aggregating gene expression data: the collapseRows R function. BMC Bioinformatics 2011 12:322.
22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T))Method.Methods 2001;25:402-8.
23. Platko JV, Leonard DA, Adra CN, Shaw RJ, Cerione RA, Lim B. A single residue can modify target-binding affinity and activity of the functional domain of the Rho-subfamily GDP dissociation inhibitors. Proc Natl Acad Sci U S A 1995;92:2974-8.
24. Theodorescu D, Cornil I, Fernandez BJ, Kerbel RS. Overexpression of normal and mutated forms of HRAS induces orthotopic bladder invasion in a human transitional cell carcinoma. Proc Natl Acad Sci U S A 1990;87:9047-51.
25. Clark EA, Golub TR, Lander ES, Hynes RO. Genomic analysis of metastasis reveals an essential role for Rho C. Nature 2000;406:532-5.
26. Hakem A, Sanchez-Sweatman O, You-Ten A, Duncan G, Wakeham A, Khokha R, et al. RhoC is dispensable for embryogenesis and tumor initiation but essential for metastasis. Genes Dev 2005;19:1974-9.
27. IIIzumi M, Bandyopadhyay S, Pai SK, Watabe M, Hirota S, Hosobe S, et al. RhoC promotes metastasis via activation of the Pyk2 pathway in prostate cancer. Cancer Res 2008;68:7613-20.
28. Rosenthal DT, Zhang J, Bao L, Zhu L, Wu Z, Toy K, et al. RhoC impacts the metastatic potential and abundance of breast cancer stem cells. PLoS One 2012;7:e40979.
29. Ho TTG, Stultiens A, Dubail J, Lapiere CM, Nusgens BV, Colige AC, et al. RhoGDI alpha-dependent balance between RhoA and RhoC is a key regulator of cancer cell tumorigenesis. Mol Biol Cell 2011;22:3263-75.
30. Islam M, Lin G, Brenner JC, Pan Q, Merajver SD, Hou Y, et al. RhoC expression and head and neck cancer metastasis. Mol Cancer Res 2009;7:1771-80.
31. Unsal-Kacmaz K, Ragunathan S, Rosfjord E, Dann S, Upeslacis E, Grillo M, et al. The interaction of PKN3 with RhoC promotes malignant growth.Mol Oncol 2012;6:284-98.
32. Thomas S, Overdevest JB, Nitz MD, Williams PD, Owens CR, Sanchez- Carbayo M, et al. Src and Caveolin-1 reciprocally regulate metastasis via a common downstream signaling pathway in bladder cancer. Cancer Res 2011;71:832-41.
33. Kamai T, Tsujii T, Arai K, Takagi K, Asami H, Ito Y, et al. Significant association of Rho/ROCK pathwaywith invasion and metastasis of bladder cancer. Clin Cancer Res 2003;9:2632-41.
34. Rath N, Olson MF. Rho-associated kinases in tumorigenesis: re-considering ROCK inhibition for cancer therapy. EMBO Rep 2012;13:900-8.
35. Wheeler AP, Ridley AJ. Why three Rho proteins? Rho A, Rho B, Rho C, and cell motility. Exp Cell Res 2004;301:43-9.
36. Boulter E, Garcia-Mata R, Guilluy C, Dubash A, Rossi G, Brennwald PJ, et al. Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat Cell Biol 2010;12:477-U136.
37. Karantza V. Keratins in health and cancer: more than mere epithelial cell markers. Oncogene 2011;30:127-38.
38. Bluemke K, Bilkenroth U, Meye A, Fuessel S, Lautenschlaeger C, Goebel S, et al. Detection of circulating tumor cells in peripheral blood of patients with renal cell carcinoma correlates with prognosis. Cancer Epidemiol Biomarkers Prev 2009;18:2190-4.
39. Weckermann D, Polzer B, Ragg T, Blana A, Schlimok G, Arnholdt H, et al. Perioperative activation of disseminated tumor cells in bone marrow of patients with prostate cancer. J Clin Oncol 2009;27: 1549-56.
40. Lei T, Zhao X, Jin S, Meng Q, Zhou H, Zhang M. Discovery of potential bladder cancer biomarkers by comparative urine proteomics and analysis. Clin Genitourin Cancer 2013;11:56-62.