Reversion of RhoC GTPase-induced inflammatory breast cancer phenotype by treatment with a farnesyl transferase inhibitor

Molecular Cancer Therapeutics

Volumn 1, Issue 8, 2002, Pages 575-583

  Van Golen, Kenneth L ^a,b   Bao, LiWei ^a,b   DiVito, Melinda M ^a   Wu, ZhiFen ^a,b   Prendergast, George C ^c,d   Merajver, Sofia D ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c WISTAR INSTITUTE   (United States)

^d DUPONT COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [[2 [[2 [(2 AMINO 3 MERCAPTOPROPYL)AMINO] 3 METHYLPENTYL]OXY] 1 OXO 3 PHENYLPROPYL]AMINO] 4 (METHYLSULFONYL)BUTANOIC ACID ISOPROPYL ESTER; DRUG DERIVATIVE; ENZYME INHIBITOR; FARNESYL TRANS TRANSFERASE; METHIONINE; PHALLOIDIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOC PROTEIN, HUMAN; RHODAMINE; TRANSFERASE;

APOPTOSIS; ARTICLE; BREAST TUMOR; CELL CULTURE; CELL DIVISION; CELL LINE; CELL MOTION; DRUG ANTAGONISM; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; HUMAN; METABOLISM; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; WESTERN BLOTTING;

ALKYL AND ARYL TRANSFERASES; APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL DIVISION; CELL LINE, TRANSFORMED; CELL MOVEMENT; ENZYME INHIBITORS; FARNESYLTRANSTRANSFERASE; HUMANS; METHIONINE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; PHALLOIDINE; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHO GTP-BINDING PROTEINS; RHODAMINES; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0036599583     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Lee, B. J., and Tannenbaum, N. E. Inflammatory carcinoma of the breast: a report of twenty-eight cases from the breast clinic of Memorial Hospital. Surg. Gynecol. Obstet., 39: 580-595, 1924.
2. Kleer, C. G., van Golen, K. L., and Merajver, S. D. Molecular biology of breast cancer metastasis. Inflammatory breast cancer: clinical syndrome and molecular determinants. Breast Cancer Res., 2: 423-429, 2000. (Pubitemid 32223639)
3. Jaiyesimi, I. A., Buzdar, A. U., and Hortobagyi, G. Inflammatory breast cancer: a review. J. Clin. Oncol., 10: 1014-1024, 1992.
4. Beahrs, O., Henson, D., and Hutter, R. Manual for Staging of Cancer, pp. 145-150. Philadelphia, PA: Lippincott, Williams, and Wilkins, 1988.
5. van Golen, K. L., Davies, S., Wu, Z. F., Wang, Y., Bucana, C. D., Root, H., Chandrasekharappa, S., Strawderman, M., Ethier, S. P., and Merajver, S. D. A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC GTPase correlate with the inflammatory breast cancer phenotype. Clin. Cancer Res., 5: 2511-2519, 1999. (Pubitemid 29437336)
6. Ridley, A. J. The GTP-binding protein Rho. Int. J. Biochem. Cell Biol., 29: 1225-1229, 1997. (Pubitemid 28021707)
7. Esteve, P., Embade, N., Perona, R., Jimenez, B., del Peso, L., Leon, J., Arends, M., Miki, T., and Lacal, J. C. Rho-regulated signals induce apoptosis in vitro and in vivo by a p53-independent, but Bc12 dependent pathway. Oncogene, 17: 1855-1869, 1998. (Pubitemid 28482789)
8. Hall, A. Small GTP-binding proteins and the regulation of the cytoskeleton. Annu. Rev. Cell Biol., 10: 31-54, 1994. (Pubitemid 24372815)
9. Apenstrom, P. Effectors for the Rho GTPases. Curr. Opin. Cell Biol., 11: 95-102, 1999.
10. Nobes, C. D., and Hall, A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia and filopodia. Cell, 81: 53-62, 1995.
11. Takai, Y., Sasaki, T., and Matozaki, T. Small GTP-binding proteins. Physiol. Rev., 81: 153-208, 2001. (Pubitemid 32098004)
12. van Golen, K. L., Wu, Z. F., Qiao, X. T., Bao, L. W., and Merajver, S. D. RhoC GTPase, a novel transforming oncogene for human mammary epithelial cells that partially recapitulates the inflammatory breast cancer phenotype. Cancer Res., 60: 5832-5838, 2000.
13. van Golen, K. L., Wu, Z. F., Qiao, X. T., Bao, L. W., and Merajver, S. D. RhoC GTPase overexpression modulates induction of angiogenic factors in breast cells. Neoplasia (New York), 2: 418-425, 2000. (Pubitemid 32044787)
14. van Golen, K. L., Wu, Z. F., Bao, L. W., and Merajver, S. D. RhoC GTPase induces a motile and invasive phenotype in inflammatory breast cancer. Clin. Exp. Metastasis, 17: 745-745, 1999.
15. Geyer, M., and Wittinghofer, A. GEFs, GAPs, GDIs and effectors: taking a closer (3D) look at the regulation of Ras-related GTP-binding proteins. Curr. Opin. Struct. Biol., 7: 786-792, 1997. (Pubitemid 28025104)
16. Prokopenko, S. N., Saint, R., and Bellen, H. J. Untying the Gordian knot of cytokinesis. Role of small G proteins and their regulators. J. Cell Biol., 148: 843-848, 2000.
17. Seabra, M. C. Membrane association and targeting of prenylated Ras-like GTPases. Cell. Signalling, 10: 167-172, 1998. (Pubitemid 28156067)
18. Kirschmeier, P. T., Whyte, D., Wilson, O., Bishop, W. R., and Pai, J. K. In vivo prenylation analysis of Ras and Rho proteins. Methods Enzymol., 332: 115-127, 2001. (Pubitemid 32275376)
19. Adamson, P., Marshall, C. J., Hall, A., and Tilbrook, P. A. Posttranslational modifications of p21rho proteins. J. Biol. Chem., 267: 20033-20038, 1992.
20. Sinensky, M. Recent advances in the study of prenylated proteins. Biochim. Biophys. Acta., 1484: 93-106, 2000. (Pubitemid 30175960)
21. Bishop, A. L., and Hall, A. Rho GTPases and their effector proteins. Biochem. J., 348 Pt 2: 241-255, 2000. (Pubitemid 30345195)
22. Verbeke, G., and Molenberghs, G. Linear mixed models in practice: an SAS-oriented approach. New York, NY: Springer-Verlag, 1997.
23. Zohn, I. M., Campbell, S. L., Khosravi-Far, R., Rossman, K. L., and Der, C. J. Rho family proteins and Ras transformation: the RHOad less traveled gets congested. Oncogene, 17: 1415-1438, 1998. (Pubitemid 28458410)
24. Gamblin, S. J., and Smerdon, S. J. GTPase-activating proteins and their complexes. Curr. Opin. Struct. Biol., 8: 195-201, 1998. (Pubitemid 28221051)
25. Olofsson, B. Rho guanine dissociation inhibitors: pivotal molecules in cellular signalling. Cell. Signalling, 11: 545-554, 1999. (Pubitemid 29255886)
26. Ethier, S. P., Kokeny, K. E., Ridings, J. W., and Dilts, C. A. erbB family receptor expression and growth regulation in a newly isolated human breast cancer cell line. Cancer Res., 56: 899-907, 1996. (Pubitemid 26055484)
27. Ethier, S. P. Human breast cancer cell lines as models of growth regulation and disease progression. J. Mammary Gland Biol. Neoplasia, 1: 111-121, 1996.
28. Sartor, C. I., Dziubinski, M. L., Yu, C. L., Jove, R., and Ethier, S. P. Role of epidermal growth factor receptor and STAT-3 activation in autonomous proliferation of SUM-102PT human breast cancer cells. Cancer Res., 57: 978-987, 1997. (Pubitemid 27098027)
29. Band, V., Zajchowski, D., Kulesa, V., and Sager, R. Human papilloma virus DNAs immortalize normal human mammary epithelial cells and reduce their growth factor requirements. Proc. Natl. Acad. Sci. USA, 87: 463-467, 1990.
30. Lebowitz, P. F., Davide, J. P., and Prendergast, G. C. Evidence that farnesyltransferase inhibitors suppress Ras transformation by interfering with Rho activity. Mol. Cell. Biol., 15: 6613-6622, 1995.
31. Du, W., Liu, A., and Prendergast, G. C. Activation of the PI3'K-AKT pathway masks the proapoptotic effects of farnesyltransferase inhibitors. Cancer Res., 59: 4208-4212, 1999. (Pubitemid 29418727)
32. Liu, A., Du, W., Liu, J. P., Jessell, T. M., and Prendergast, G. C. RhoB alteration is necessary for apoptotic and antineoplastic responses to farnesyltransferase inhibitors. Mol. Cell. Biol., 20: 6105-6113, 2000. (Pubitemid 30613058)
33. Kleer, C. G., van Golen, K. L., Zhang, Y., Wu, Z. F., Rubin, M. A., and Merajver, S. D. Characterization of RhoC expression in benign and malignant breast disease: a potential new marker for small breast carcinomas with metastatic potential. Am. J. Pathol., 160: 579-84, 2002. (Pubitemid 34160335)
34. Zondag, G. C. M., Evers, E. E., ten Klooster, J. P., Janssen, L., van der Kammen, R. A., and Collard, J. G. Oncogenic Ras downregulates Rac activity, which leads to increased Rho activity and epithelial-mesenchymal transition. J. Cell Biol., 149: 775-782, 2000.
35. Evers, E. E., van der Kammen, R. A., ten Klooster, J. P., and Collard, J. G. Rho-like GTPases in tumor cell invasion. Methods Enzymol., 325: 403-415, 2000.
36. Albrecht-Buehler, G. The phagokinetic tracks of 3T3 cells. Cell, 11: 395-404, 1977.
37. van Golen, K. L., Risin, S., Staroselsky, A., Berger, D., Tainsky, M. A., Pathak, S., and Price, J. E. Predominance of the metastatic phenotype in hybrids formed by fusion of mouse and human melanoma clones. Clin. Exp. Metastasis, 14: 95-106, 1996. (Pubitemid 26074273)
38. Darzynkiewicz, Z., Juan, G., Li, X., Gorczyca, W., Murakami, T., and Traganos, F. Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry, 27: 1-20, 1997. (Pubitemid 27059777)
39. 1 arrest in B-cell hybridomas by interleukin-6 is not accompanied by altered expression of immediate early response genes. J. Cell Physiol., 145: 564-574, 1990.
40. MacPherson, I., and Montangnier, L. Agar suspension culture for the selective assay of cells transformed by polyoma virus. Virology, 23: 291-294, 1964.
41. Santner, S. J., Dawson, P. J., Tait, L., Soule, H. D., Eliason, J., Mohamed, A. N., Wolman, S. R., Heppner, G. H., and Miller, F. R. Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells. Breast Cancer Res. Treat., 65: 101-110, 2001. (Pubitemid 32193613)
42. Du, W., Lebowitz, P. F., and Prendergast, G. C. Cell growth inhibition by farnesyltransferase inhibitors is mediated by gain of geranylgeranylated RhoB. Mol. Cell. Biol., 19: 1831-1840, 1999. (Pubitemid 29098241)
43. Liu, A., and Prendergast, G. C. Geranylgeranylated RhoB is sufficient to mediate tissue-specific suppression of Akt kinase activity by farnesyltransferase inhibitors. FEBS Lett., 24114: 1-4, 2000.
44. Garcia, A. M., Rowell, C., Ackermann, K., Kowalczyk, J. J., and Lewis, M. D. Peptidomimetic inhibitors of Ras farnesylation and function in whole cells. J. Biol. Chem., 268: 18415-18418, 1993. (Pubitemid 23273764)
45. James, G. L., Goldstein, J. L., Brown, M. S., Rawson, T. E., Somers, T. C., McDowell, R. S., Crowley, C. W., Lucas, B. K., Levinson, A. D., and Marsters, J. C., Jr. Benzodiazepine peptidomimetics: potent inhibitors of Ras farnesylation in animal cells. Science (Wash. DC), 260: 1937-1942, 1993. (Pubitemid 23258274)
46. Kohl, N. E., Mosser, S. D., deSolms, S. J., Giuliani, E. A., Pompliano, D. L., Graham, S. L., Smith, R. L., Scolnick, E. M., Oliff, A., and Gibbs, J. B. Selective inhibition of ras-dependent transformation by a farnesyltransferase inhibitor. Science (Wash. DC), 260: 1934-1937, 1993. (Pubitemid 23258273)
47. Rowinsky, E. K., Windle, J. J., and Von Hoff, D. D. Ras protein farnesyltransferase: a strategic target for anticancer therapeutic development. J. Clin. Oncol., 17: 3631-3652, 1999. (Pubitemid 29517936)
48. Cohen, L. H., Pieterman, E., van Leeuwen, R. E., Overhand, M., Burm, B. E., van der Marel, G. A., and van Boom, J. H. Inhibitors of prenylation of Ras and other G-proteins and their application as therapeutics. Biochem. Pharmacol., 60: 1061-1068, 2000.
49. Mondal, M. S., Wang, Z., Seeds, A. M., and Rando, R. R. The specific binding of small molecule isoprenoids to rhoGDP dissociation inhibitor (rhoGDI). Biochemistry, 39: 406-412, 2000. (Pubitemid 30056476)
50. Hancock, J. F., Magee, A. I., Childs, J. E., and Marshall, C. J. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell, 57: 1167-1177, 1989. (Pubitemid 19169813)
51. Hancock, J. F., Cadwallader, K., Paterson, H., and Marshall, C. J. A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO J., 10: 4033-4039, 1991. (Pubitemid 21905433)
52. Lai, R. K., Perez-Sala, D., Canada, F. J., and Rando, R. R. The - subunit of transducin is farnesylated. Proc. Natl. Acad. Sci. USA, 87: 7673-7677, 1990.
53. Rando, R. R. Chemical biology of protein isoprenylation/methylation. Biochim. Biophys. Acta, 1300: 5-16, 1996. (Pubitemid 26103894)
54. Zhang, B., Zhang, Y., Collins, C. C., Johnson, D. I., and Zheng, Y. A built-in arginine finger triggers the self-stimulatory GTPase-activating activity of rho family GTPases. J. Biol. Chem., 274: 2609-2612, 1999. (Pubitemid 29075336)
55. Zhang, B., and Zheng, Y. Negative regulation of Rho family GTPases Cdc42 and Rac2 by homodimer formation. J. Biol. Chem., 273: 25728-25733, 1998. (Pubitemid 28475796)
56. Omer, C. A., Chen, Z., Diehl, R. E., Conner, M. W., Chen, H. Y., Trumbauer, M. E., Gopal-Truter, S., Seeburger, G., Bhimnathwala, H., Abrams, M. T., Davide, J. P., Ellis, M. S., Gibbs, J. B., Greenberg, I., Hamilton, K., Koblan, K. S., Kral, A. M., Liu, D., Lobell, R. B., Miller, P. J., Mosser, S. D., O'Neill, T. J., Rands, E., Schaber, M. D., Senderak, E. T., Oliff, A., and Kohl, N. E. Mouse mammary tumor virus-Ki-rasB transgenic mice develop mammary carcinomas that can be growth-inhibited by a farnesyl:protein transferase inhibitor. Cancer Res., 60: 2680-2688, 2000. (Pubitemid 30318244)
57. Prendergast, G. C., Davide, J. P., deSolms, S. J., Giuliani, E. A., Graham, S. L., Gibbs, J. B., Oliff, A., and Kohl, N. E. Farnesyltransferase inhibition causes morphological reversion of ras-transformed cells by a complex mechanism that involves regulation of the actin cytoskeleton. Mol. Cell. Biol., 14: 4193-4202, 1994.
58. Prendergast, G. C., Khosravi-Far, R., Solski, P. A., Kurzawa, H., Lebowitz, P. F., and Der, C. J. Critical role of Rho in cell transformation by oncogenic Ras. Oncogene, 10: 2289-2296, 1995.
59. Prendergast, G. C., and Oliff, A. Farnesyltransferase inhibitors: antineoplastic properties, mechanisms of action, and clinical prospects. Semin. Cancer Biol., 10: 443-452, 2000. (Pubitemid 32181914)
60. Lebowitz, P. F., Casey, P. J., Prendergast, G. C., and Thissen, J. A. Farnesyltransferase inhibitors alter the prenylation and growth-stimulating function of RhoB. J. Biol. Chem., 272: 15591-15594, 1997. (Pubitemid 27265524)
61. Lebowitz, P. F., and Prendergast, G. C. Non-Ras targets of farnesyltransferase inhibitors: focus on Rho. Oncogene, 17: 1439-1445, 1998. (Pubitemid 28458411)
62. Zalcman, G., Closson, V., Linares-Cruz, G., Lerebours, F., Honore, N., Tavitian, A., and Olofsson, B. Regulation of Ras-related RhoB protein expression during the cell cycle. Oncogene, 10: 1935-1945, 1995.
63. Prendergast, G. C. Farnesyltransferase inhibitors define a role for RhoB in controlling neoplastic pathophysiology. Histol. Histopathol., 16: 269-275, 2001. (Pubitemid 32094043)
64. Leung, T., Chen, X., Manser, E., and Lim, L. The p160 RhoA-binding kinase ROKα is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol., 16: 5313-5327, 1996. (Pubitemid 26315050)
65. Michaelson, D., Silletti, J., Murphy, G., D'Eustachio, P., Rush, M., and Philips, M. R. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J. Cell. Biol., 152: 111-126, 2001. (Pubitemid 32102441)
66. Gelb, M. H. Protein prenylation, et cetera: signal transduction in two dimensions. Science (Wash. DC), 275: 1750-1751, 1997. (Pubitemid 27136701)
67. Glomset, J. A., and Farnsworth, C. C. Role of protein modification reactions in programming interactions between ras-related GTPases and cell membranes. Annu. Rev. Cell Biol., 10: 181-205, 1994. (Pubitemid 24372820)
68. Suwa, H., Ohshio, G., Imamura, T., Watanabe, G., Arii, S., Imamura, M., Narumiya, S., Hiai, H., and Fukumoto, M. Overexpression of the rhoC gene correlates with progression of ductal adenocarcinoma of the pancreas. Br. J. Cancer, 77: 147-152, 1998. (Pubitemid 28029787)
69. Clark, E. A., Golub, T. R., Lander, E. S., and Hynes, R. O. Genomic analysis of metastasis reveals an essential role for RhoC. Nature (Lond.), 406: 532-535, 2000. (Pubitemid 30625739)