Loss of rho GDIα and resistance to tamoxifen via effects on estrogen receptor α

Journal of the National Cancer Institute

Volumn 103, Issue 7, 2011, Pages 538-552

  Barone, Ines ^a,d,e   Brusco, Lauren ^a,b   Gu, Guowei ^a   Selever, Jennifer ^a   Beyer, Amanda ^a   Covington, Kyle R ^a   Tsimelzon, Anna ^a   Wang, Tao ^a   Hilsenbeck, Susan G ^a   Chamness, Gary C ^a   And, Sebastiano ^d,e   Fuqua, Suzanne A W ^a,b,c  

^a Lester and Sue Smith Breast Center   (United States)

^b Department of Molecular and Cellular Biology ^*  (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d Centro Sanitario   (Italy)

^e UNIVERSITY OF CALABRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; P21 ACTIVATED KINASE 1; RHO GUANINE DISSOCIATION INHIBITOR ALPHA; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SERINE; TAMOXIFEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER RECURRENCE; CELL STRAIN MCF 7; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; CELL LINE, TUMOR; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; ESTROGEN ANTAGONISTS; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENOME-WIDE ASSOCIATION STUDY; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; HISTONE DEACETYLASES; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICE; MICE, NUDE; NEOPLASM RECURRENCE, LOCAL; ODDS RATIO; PHENOTYPE; PLASMIDS; PROTEIN ARRAY ANALYSIS; RANDOM ALLOCATION; REPRESSOR PROTEINS; RETROSPECTIVE STUDIES; RHO GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; SECONDARY PREVENTION; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SIGNAL TRANSDUCTION; TAMOXIFEN; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSPLANTATION, HETEROLOGOUS; TUMOR STEM CELL ASSAY;

EID: 79953853847     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djr058     Document Type: Article

References (68)

1. Hortobagyi GN, De la Garza Salazar J, Pritchard K, et al. The global breast cancer burden: variations in epidemiology and survival. Clin Breast Cancer. 2005;6(5):391-401. (Pubitemid 43078894)
2. Dowsett M, Martin LA, Smith I, Johnston S. Mechanisms of resistance to aromatase inhibitors. J Steroid Biochem Mol Biol. 2005;95(1-5): 167-172. (Pubitemid 41137307)
3. Saphner T, Tormey DC, Gray R. Annual hazard rates of recurrence for breast cancer after primary therapy. J Clin Oncol. 1996;14(10):2738-2746. (Pubitemid 26329660)
4. Hull DF, Clark GM, Osborne CK, Chamness GC, Knight WAI, McGuire WL. Multiple estrogen receptor assays in human breast cancer. Cancer Res. 1983;43(1):413-416. (Pubitemid 13172851)
5. Knowlden JM, Hutcheson IR, Jones HE, et al. Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology. 2003;144(3):1032-1044. (Pubitemid 36262870)
6. Herynk MH, Fuqua SA. Estrogen receptors in resistance to hormone therapy. Adv Exp Med Biol. 2007;608:130-143.
7. Yang J, Mani SA, Donaher JL, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117(7):927-939. (Pubitemid 38798858)
8. Gildea JJ, Seraj MJ, Oxford G, et al. RhoGDI2 is an invasion and metastasis suppressor gene in human cancer. Cancer Res. 2002;62(22): 6418-6423. (Pubitemid 35364098)
9. Vaidya KS, Welch DR. Metastasis suppressors and their roles in breast carcinoma. J Mammary Gland Biol Neoplasia. 2007;12(2-3):175-190. (Pubitemid 47215435)
10. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature. 2002;420(6916):629-635. (Pubitemid 36764489)
11. Lin M, Van Golen KL. Rho-regulatory proteins in breast cancer cell mo-tility and invasion. Breast Cancer Res Treat. 2004;84(1):49-60. (Pubitemid 38388860)
12. Jiang WG, Watkins G, Lane J, et al. Prognostic value of rho GTPases and rho guanine nucleotide dissociation inhibitors in human breast cancers. Clin Cancer Res. 2003;9(17):6432-6440. (Pubitemid 38031830)
13. Cui Y, Zhang M, Pestell R, Curran EM, Welshons WV, Fuqua SAW. Phosphorylation of estrogen receptor a blocks its acetylation and regulates estrogen sensitivity. Cancer Res. 2004;64(24):9199-9208. (Pubitemid 39665536)
14. Cui Y, Parra I, Zhang M, et al. Elevated expression of mitogen-activated protein kinase phosphatase 3 in breast tumors: a mechanism of tamoxifen resistance. Cancer Res. 2006;66(11):5950-5959. (Pubitemid 43927151)
15. Fuqua SAW, Wiltschke C, Zhang QX, et al. A hypersensitive estrogen receptor-a mutation in premalignant breast lesions. Cancer Res. 2000;60(15):4026-4029. (Pubitemid 30636577)
16. Herman ME, Katzenellenbogen BS. Response-specifc antiestrogen resistance in a newly characterized MCF-7 human breast cancer cell line resulting from long-term exposure to trans-hydroxytamoxifen. J Steroid Biochem Mol Biol. 1996;59(2):121-134. (Pubitemid 27036264)
17. Nishitani J, Nishinaka T, Cheng CH, Rong W, Yokoyama KK, Chiu R. Recruitment of the retinoblastoma protein to c-Jun enhances transcription activity mediated through the AP-1 binding site. J Biol Chem. 1999; 274(9):5454-5461. (Pubitemid 29109191)
18. Osborne CK, Coronado-Heinsohn EB, Hilsenbeck SG, McCue BL, Wakeling AE, McClelland RA. Comparison of the effects of a pure steroi-dal antiestrogen with those of tamoxifen in a model of human breast cancer. J Natl Cancer Inst. 1995;87(10):746-750.
19. Holm S. A simple sequentially rejective multiple test procedure. Scand J Stat. 1979;6(2):65-70.
20. Team RDC. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2008.
21. Loi S, Haibe-Kains B, Desmedt C, et al. Defnition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J Clin Oncol. 2007;25(10):1239-1246. (Pubitemid 46640570)
22. De Amicis F, Thirugnansampanthan J, Cui Y, et al. Androgen receptor overexpression induces tamoxifen resistance in human breast cancer cells. Breast Cancer Res Treat. 2009;89(9):4037-4041.
23. Harrell JC, Dye WW, Allred DC, et al. Estrogen receptor positive breast cancer metastasis: altered hormonal sensitivity and tumor aggressiveness in lymphatic vessels and lymph nodes. Cancer Res. 2006;66(18): 9308-9315. (Pubitemid 44521153)
24. Dauvois S, Danielian PS, White R, Parker MG. Antiestrogen ICI 164,384 reduces cellular estrogen receptor content by increasing its turnover. Proc Natl Acad Sci USA. 1992;89(9):4037-4041.
25. Karnoub AE, Symons M, Campbell SL, Der CJ. Molecular basis for Rho GTPase signaling specifcity. Breast Cancer Res Treat. 2004;84(1):61-71. (Pubitemid 38388861)
26. Rayala SK, Molli PR, Kumar R. Nuclear p21-activated kinase 1 in breast cancer packs off tamoxifen sensitivity. Cancer Res. 2006;66(12): 5985-5988.
27. Wang RA, Mazumdar A, Vadlamudi RK, Kumar R. P21-activated kinase-1 phosphorylates and transactivates estrogen receptor-alpha and promotes hyperplasia in mammary epithelium. EMBO J. 2002;21(20): 5437-5447. (Pubitemid 35231023)
28. Rayala SK, Talukder AH, Balasenthil S, et al. P21-activated kinase 1 regulation of estrogen receptor-alpha activation involves serine 305 activation linked with serine 118 phosphorylation. Cancer Res. 2006;66(3):1694-1701. (Pubitemid 43259954)
29. Michalides R, Griekspoor A, Balkenende A, et al. Tamoxifen resistance by a conformational arrest of the estrogen receptor alpha after PKA activation in breast cancer. Cancer Cell. 2004;5(6):597-605. (Pubitemid 38748921)
30. Holm C, Kok M, Michalides R, et al. Phosphorylation of the oestrogen receptor alpha at serine 305 and prediction of tamoxifen resistance in breast cancer. J Pathol. 2009;217(3):372-379.
31. Chen D, Washbrook E, Sarwar N, et al. Phosphorylation of human estrogen receptor alpha at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specifc antisera. Oncogene. 2002;21(32): 4921-4931.
32. El Marzouk S, Schultz-Norton JR, Likhite VS, McLeod IX, Yates JR, Nardulli AM. Rho GDP dissociation inhibitor alpha interacts with estrogen receptor alpha and infuences estrogen responsiveness. J Mol Endocrinol. 2007;39(4):249-259. (Pubitemid 350047646)
33. Su LF, Knoblauch R, Garabedian MJ. Rho GTPases as modulators of the estrogen receptor transcriptional response. J Biol Chem. 2001;276(5): 3231-3237.
34. Nawaz Z, Lonard DM, Dennis AP, Smith CL, O'Malley BW. Proteasome-dependent degradation of the human estrogen receptor. Biochemistry. 1999;96(5):1858-1862. (Pubitemid 29117832)
35. Kayser K, Biechele U, Kayser G, et al. Pulmonary metastases of breast carcinomas: ligandohistochemical, nuclear, and structural analysis of primary and metastatic tumors with emphasis on period of occurrence of metastases and survival. J Surg Oncol. 1998;69(3):137-146. (Pubitemid 28549888)
36. Lin M, Van Golen KL. Rho-regulatory proteins in breast cancer cell mo-tility and invasion. Breast Cancer Res Treat. 2004;84(1):49-60. (Pubitemid 38388860)
37. Jo M, Thomas KS, Somlyo AV, Somlyo AP, Gonias SL. Cooperativity between the Ras-ERK and Rho-Rho kinase pathways in urokinase-type plasminogen activator-stimulated cell migration. J Biol Chem. 2002;277(14):12479-12485. (Pubitemid 34952823)
38. Nakshatri H, Bhat-Nakshatri P, Martin DA, Goulet RJ, Sledge GW. Constitutive activation of NF-kappaB during progression of breast cancer to hormone-independent growth. Mol Cell Biol. 1997;17(7): 3629-3639. (Pubitemid 27281838)
39. Burbelo P, Wellstein A, Pestell RG. Altered Rho GTPase signaling pathways in breast cancer cells. Breast Cancer Res Treat. 2004;84(1): 43-48. (Pubitemid 38388859)
40. Planas-Silva MD, Waltz PK. Estrogen promotes reversible epithelial-to-mesenchymal-like transition and collective motility in MCF-7 breast cancer cells. J Steroid Biochem Mol Biol. 2007;104(1-2):11-21. (Pubitemid 46412987)
41. Kumar R. Another tie that binds the MTA family to breast cancer. Cell. 2003;113(2):142-143. (Pubitemid 36514965)
42. Cui Y, Niu A, Pestell R, et al. Metastasis-associated protein 2 is a repressor of estrogen receptor alpha whose overexpression leads to estrogen-independent growth of human breast cancer cells. Mol Endocrinol. 2006; 20(9):2020-2035. (Pubitemid 44286702)
43. Nicolini A, Giardino R, Carpi A, et al. Metastatic breast cancer: an updating. Biomed Pharmacother. 2006;60(9):548-556.
44. Robertson J. Oestrogen receptor: a stable phenotype in breast cancer. Br J Cancer. 1996;73(1):5-12. (Pubitemid 26026252)
45. Gutierrez MC, Detre S, Johnston S, et al. Molecular changes in tamoxifen-resistant breast cancer: relationship between estrogen receptor, HER-2, and p38 mitogen-activated protein kinase. J Clin Oncol. 2005;23(11): 2469-2476. (Pubitemid 47050837)
46. Shou J, Massarweh S, Osborne CK, et al. Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/ HER2-positive breast cancer. J Natl Cancer Inst. 2004;96(12): 926-935. (Pubitemid 38868139)
47. Creighton CJ, Hilger AM, Murthy S, Rae JM, Chinnaiyan AM, El-Ashry D. Activation of mitogen-activated protein kinase in estrogen receptor alpha-positive breast cancer cells in vitro induces an in vivo molecular phenotype of estrogen receptor alpha-negative human breast tumors. Cancer Res. 2006;66(7):3903-3911.
48. El-Ashry D, Miller D, Kharbanda S, Lippman M, Kern F. Constitutive Raf-1 kinase activity in breast cancer cells induces both estrogen-independent growth and apoptosis. Oncogene. 1997;15(4):423-435. (Pubitemid 27370992)
49. Iorns E, Turner NC, Elliott R, et al. Identifcation of CDK10 as an important determinant of resistance to endocrine therapy for breast cancer. Cancer Cell. 2008;13(2):91-104. (Pubitemid 351163160)
50. Bedard PL, Freedman OC, Howell A, Clemons M. Overcoming endocrine resistance in breast cancer: are signal transduction inhibitors the answer? Breast Cancer Res Treat. 2008;108(3):307-317. (Pubitemid 351431070)
51. Schmitz AA, Govek EE, Bottner B, Van Aelst L. Rho GTPases: signaling, migration, and invasion. Exp Cell Res. 2000;261(1):1-12.
52. Albright CD, Carter CA, Kaufman DG. Tamoxifen alters the localization of F-actin and alpha 5/beta 1-integrin fbronectin receptors in human en-dometrial stromal cells and carcinoma cells. Pathobiology. 1997;65(4): 177-183. (Pubitemid 27472522)
53. Cai D, Iyer A, Felekkis KN, et al. AND-34/BCAR3, a GDP exchange factor whose overexpression confers antiestrogen resistance, activates Rac, PAK1, and the cyclin D1 promoter. Cancer Res. 2003;63(20): 6802-6808. (Pubitemid 37322962)
54. Ma XJ, Wang Z, Ryan PD, et al. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell. 2004;5(6):607-616. (Pubitemid 38748922)
55. Jansen MP, Foekens JA, Van Staveren IL, et al. Molecular classifcation of tamoxifen-resistant breast carcinomas by gene expression profling. J Clin Oncol. 2005;23(4):732-740. (Pubitemid 46224172)
56. Chanrion M, Negre V, Fontaine H, et al. A gene expression signature that can predict the recurrence of tamoxifen-treated primary breast cancer. Clin Cancer Res. 2008;14(6):1744-1752. (Pubitemid 351469459)
57. Kok M, Linn SC, Van Laar RK, et al. Comparison of gene expression profles predicting progression in breast cancer patients treated with ta-moxifen. Breast Cancer Res Treat. 2009;113(2):275-283.
58. Holm C, Rayala S, Jirstrom K, Stal O, Kumar R, Landberg G. Association between Pak1 expression and subcellular localization and tamoxifen resistance in breast cancer patients. J Natl Cancer Inst. 2006;98(10):671-680. (Pubitemid 43821785)
59. Barone I, Cui Y, Herynk MH, et al. Expression of the K303R estrogen receptor-alpha breast cancer mutation induces resistance to an aromatase inhibitor via addiction to the PI3K/Akt kinase pathway. Cancer Res. 2009;69(11):4724-4732.
60. Giordano C, Cui Y, Barone I, et al. Growth factor-induced resistance to tamoxifen is associated with a mutation of estrogen receptor alpha and its phosphorylation at serine 305. Breast Cancer Res Treat. 2010;19(1): 71-85.
61. Barone I, Iacopetta D, Covington KR, et al. Phosphorylation of the mutant K303R estrogen receptor alpha at serine 305 affects aromatase inhibitor sensitivity. Oncogene. 2010;29(16):2404-2414.
62. Cui Y, Zhang M, Pestell R, Fuqua SAW. Phosphorylation of estrogen receptor a blocks its acetylation and regulates estrogen sensitivity. Cancer Res. 2004;64(24):9199-9208. (Pubitemid 39665536)
63. Ma Y, Fan S, Hu C, et al. BRCA1 regulates acetylation and ubiquitination of estrogen receptor alpha. Mol Endocrinol. 2010;24(1):76-90.
64. Talukder AH, Meng Q, Kumar R. CRIPak, a novel endogenous Pak1 inhibitor. Oncogene. 2006;25(9):1311-1319. (Pubitemid 43336459)
65. Theodorescu D, Sapinoso LM, Conaway MR, Oxford G, Hampton GM, Frierson HF Jr. Reduced expression of metastasis suppressor RhoGDI2 is associated with decreased survival for patients with bladder cancer. Clin Cancer Res. 2004;10(11):3800-3806. (Pubitemid 38697615)
66. Titus B, Frierson HF Jr, Conaway M, et al. Endothelin axis is a target of the lung metastasis suppressor gene RhoGDI2. Cancer Res. 2005;65(16): 7320-7327. (Pubitemid 41161264)
67. Wu Y, McRoberts K, Berr SS, Frierson HF Jr, Conaway M, Theodorescu D. Neuromedin U is regulated by the metastasis suppressor RhoGDI2 and is a novel promoter of tumor formation, lung metastasis and cancer ca-chexia. Oncogene. 2007;26(5):765-773. (Pubitemid 46204255)
68. Manavathi B, Singh K, Kumar R. MTA family of coregulators in nuclear receptor biology and pathology. Nucl Recept Signal. 2007;5:e010.