Glucose-regulated protein 78 controls cross-talk between apoptosis and autophagy to determine antiestrogen responsiveness

Cancer Research

Volumn 72, Issue 13, 2012, Pages 3337-3349

  Cook, Katherine L ^a   Shajahan, Ayesha N ^a   Wärri, Anni ^a   Jin, Lu ^a   Hilakivi Clarke, Leena A ^a   Clarke, Robert ^a  

^a GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; AFIMOXIFENE; ANTIESTROGEN; BECLIN 1; CASPASE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; FULVESTRANT; GLUCOSE REGULATED PROTEIN 78; MAMMALIAN TARGET OF RAPAMYCIN; TAMOXIFEN; TUBERIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER TISSUE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG RESPONSE; DRUG SENSITIVITY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; AUTOPHAGY; ESTROGEN RECEPTOR MODULATORS; FEMALE; HEAT-SHOCK PROTEINS; HUMANS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84863570015     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-0269     Document Type: Article

References (44)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
2. Clarke R, Leonessa F, Welch JN, Skaar TC. Cellular and molecular pharmacology of antiestrogen action and resistance. Pharmacol Rev 2001;76:25-71. (Pubitemid 32173107)
3. Clarke M, Collins R, Davies C, Godwin J, Gray R, Peto R. Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet 1998;351:1451-67. (Pubitemid 28227036)
4. Riggins RB, Bouton AH, Liu MC, Clarke R. Antiestrogens, aromatase inhibitors, and apoptosis in breast cancer. Vitam Horm 2005;71:201-37. (Pubitemid 43631307)
5. Clarke R, Cook KL, Hu R, Facey CO, Tavassoly I, Schwartz JL, et al. Endoplasmic reticulum stress, the unfolded protein response, autophagy, and the integrated regulation of breast cancer cell fate. Cancer Res 2012;72:1321-31.
6. Cook KL, Shajahan AN, Clarke R. Autophagy and endocrine resistance in breast cancer. Expert Rev Anticancer Ther 2011;11:1283-94.
7. Clarke R, Shajahan AN, Riggins RB, Cho Y, Crawford A, Xuan JH, et al. Gene network signaling in hormone responsiveness modifies apoptosis and autophagy in breast cancer cells. J Steroid Biochem Mol Biol 2009;114:8-20.
8. Samaddar JS, Gaddy VT, Duplantier J, Thandavan SP, Shah M, Smith MJ, et al. A role for macroautophagy in protection against 4-hydroxytamoxifen-induced cell death and the development of antiestrogen resistance. Mol Cancer Ther 2008;7:2977-87.
9. Schoenlein PV, Periyasamy-Thandavan S, Samaddar JS, Jackson WH, Barrett JT. Autophagy facilitates the progression of ER alphapositive breast cancer cells to antiestrogen resistance. Autophagy 2009;5:400-3.
10. Scriven P, Coulson S, Haines R, Balasubramanian S, Cross S, Wyld L. Activation and clinical significance of the unfolded protein response in breast cancer. Br J Cancer 2009;101:1692-8.
11. Gomez BP, Riggins RB, Shajahan AN, Klimach U, Wang A, Crawford AC, et al. Human X-box binding protein-1 confers both estrogen independence and antiestrogen resistance in breast cancer cell lines. FASEB J 2007;21:4013-27. (Pubitemid 350232358)
12. Verfaillie T, Garg AD, Agostinis P. Targeting ER stress induced apoptosis and inflammation in cancer. Cancer Lett. 2010 Aug 21. [Epub ahead of print].
13. Fernandez PM, Tabbara SO, Jacobs LK, Manning FC, Tsangaris TN, Schwartz AM. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Res Treat 2000;59:15-26. (Pubitemid 30153894)
14. Gazit G, Lu J, Lee AS. De-regulation of GRP stress protein expression in human breast cancer cell lines. Breast Cancer Res Treat 1999;54:135-46. (Pubitemid 29295316)
15. Baumeister P, Dong D, Fu Y, Lee AS. Transcriptional induction of GRP78/BiP by histone deacetylase inhibitors and resistance to histone deacetylase inhibitor-induced apoptosis. Mol Cancer Ther 2009;8:1086-94.
16. Chen TC. GRP78/BiP modulation of GRP78/BiP in altering sensitivity to chemotherapy. Methods Enzymol 2011;491:25-36.
17. Verfaillie T, Salazar M, Velasco G, Agostinis P. Linking ER stress to autophagy: potential implications for cancer therapy. Int J Cell Biol 2010;2010:930509.
18. Fu Y, Li J, Lee AS. GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Res 2007;67:3734-40. (Pubitemid 46762159)
19. Zhou H, Zhang Y, Fu Y, Chan L, Lee AS. A novel mechanism of anti-apoptotic function of 78 kDa glucose-regulated protein (GRP78), an endocrine resistance factor in breast cancer, through release of B-cell lymphoma 2 (BCL-2) from BCL-2-interacting killer (BIK). J Biol Chem 2011;286:25687-96.
20. Butler WB, Berlinski PJ, Hillman RM, Kelsey WH, Toenniges MM. Relation of in vitro properties to tumorigenicity for a series of sublines of the human breast cancer cell line MCF-7. Cancer Res 1986;46:6339-48. (Pubitemid 17221781)
21. Butler WB, Fontana JA. Responses to retinoic acid of tamoxifen-sensitive and -resistant sublines of human breast cancer cell line MCF-7. Cancer Res 1992;52:6164-7.
22. Brunner N, Boulay V, Fojo A, Freter CE, Lippman ME, Clarke R. Acquisition of hormone-independent growth in MCF-7 cells is accompanied by increased expression of estrogen-regulated genes but without detectable DNA amplifications. Cancer Res 1993;53:283-90. (Pubitemid 23031838)
23. Brunner N, Boysen B, Jirus S, Skaar TC, Holst-Hansen C, Lippman J, et al. MCF7/LCC9: an antiestrogen-resistant MCF-7 variant in which acquired resistance to the steroidal antiestrogen ICI 182,780 confers an early cross-resistance to the nonsteroidal antiestrogen tamoxifen. Cancer Res 1997;57:3486-93. (Pubitemid 27355496)
24. Romanelli S, Perego P, Pratesi G, Carenini N, Tortoreto M, Zunino F. In vitro and in vivo interaction between cisplatin and topotecan in ovarian carcinoma systems. Cancer Chemother Pharmacol 1998;41:385-90. (Pubitemid 28095754)
25. Kelber JA, Panopoulos AD, Shani G, Booker EC, Belmonte JC, Vale WW, et al. Blockade of Cripto binding to cell surface GRP78 inhibits oncogenic Cripto signaling via MAPK/PI3K and Smad2/3 pathways. Oncogene 2009;28:2324-36.
26. Shani G, Fischer WH, Justice NJ, Kelber JA, Vale W, Gray PC. GRP78 and Cripto form a complex at the cell surface and collaborate to inhibit transforming growth factor beta signaling and enhance cell growth. Mol Cell Biol 2008;28:666-77.
27. Davidson DJ, Haskell C, Majest S, Kherzai A, Egan DA, Walter KA, et al. Kringle 5 of human plasminogen induces apoptosis of endothelial and tumor cells through surface-expressed glucose-regulated protein 78. Cancer Res 2005;65:4663-72. (Pubitemid 40740802)
28. Philippova M, Ivanov D, Joshi MB, Kyriakakis E, Rupp K, Afonyushkin T, et al. Identification of proteins associating with glycosylphosphatidylinositol- anchored T-cadherin on the surface of vascular endothelial cells: role for Grp78/BiP in T-cadherin-dependent cell survival. Mol Cell Biol 2008;28:4004-17. (Pubitemid 351812986)
29. Crawford AC, Riggins RB, Shajahan AN, Zwart A, Clarke R. Coinhibition of BCL-W and BCL2 restores antiestrogen sensitivity through BECN1 and promotes an autophagy-associated necrosis. PLoS One 2010;5:e8604.
30. Dong D, Stapleton C, Luo B, Xiong S, Ye W, Zhang Y, et al. A critical role for GRP78/BiP in the tumor microenvironment for neovascularization during tumor growth and metastasis. Cancer Res 2011;71:2848-57.
31. Ingle J, Suman V, Rowland K. Fulvestrant in women with advanced breast cancer after progression on prior aromatase inhibitor therapy: North Central Cancer Treatment Trial Group Number N0032. J Clin Oncol 2006;24:1052-6. (Pubitemid 46638801)
32. Perey L, Paridaens R, Hawle H. Clinical benefit of fulvestrant in postmenopausal women with advanced breast cancer and primary or acquired resistance to aromatase inhibitors: final results of phase II Swiss Group for Clinical Cancer Research Trial (SAKK 21/00). Annu Oncol 2007;18:64-9. (Pubitemid 46152501)
33. Clarke R, Brunner N. Acquired estrogen independence and antiestrogen resistance in breast cancer: estrogen receptor driven phenotypes? Trends Endocrinol Metab 1996;7:291-300.
34. Li J, Ni M, Lee B, Barron E, Hinton DR, Lee AS. The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ 2008;15:1460-71.
35. Guzel E, Basar M, Ocak N, Arici A, Kayisli UA. Bidirectional interaction between unfolded-protein-response key protein HSPA5 and estrogen signaling in human endometrium. Biol Reprod 2011;85:121-7.
36. Kuske B, Naughton C, Moore K, MacLeod K, Miller W, Clarke R, et al. Endocrine therapy resistance can be associated with high estrogen receptor-α (ERα) expression and reduced ERα phosphorylation in breast cancer models. Endocr Relat Cancer 2006;13:1121-33. (Pubitemid 46212567)
37. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 2003;278:20915-24. (Pubitemid 36806399)
38. Tu YF, Kaipparettu BA, Ma Y, Wong LJ. Mitochondria of highly metastatic breast cancer cell line MDA-MB-231 exhibits increased autophagic properties. Biochim Biophys Acta 2011;1807:1125-32.
39. He CC, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009;43:67-93.
40. Bennett HL, Fleming JT, O'Prey J, Ryan KM, Leung HY. Androgens modulate autophagy and cell death via regulation of the endoplasmic reticulum chaperone glucose-regulated protein 78/BiP in prostate cancer cells. Cell Death Dis 2010;1:e72.
41. Noda T, Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 1998;273:3963-6. (Pubitemid 28103257)
42. Ozcan U, Ozcan L, Yilmaz E, Duvel K, Sahin M, Manning BD, et al. Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol Cell 2008;29:541-51. (Pubitemid 351384644)
43. Nakajima S, Hiramatsu N, Hayakawa K, Saito Y, Kato H, Huang T, et al. Selective abrogation of BiP/GRP78 blunts activation of NF-kappaB through the ATF6 branch of the UPR: involvement of C/EBPbeta and mTOR-dependent dephosphorylation of Akt. Mol Cell Biol 2011;31:1710-8.
44. Dickson R, Lippman M. Estrogenic regulation of growth and polypeptide growth factor secretion in human breast carcinoma. Endocrine Rev 1987;8:29-43.