Pharmacological induction of cell surface GRP78 contributes to apoptosis in triple negative breast cancer cells

Oncotarget

Volumn 5, Issue 22, 2014, Pages 11452-11463

  Raiter, Annat ^a   Yerushalmi, Rinat ^b   Hardy, Britta ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b RABIN MEDICAL CENTER   (Israel)

Author keywords

Apoptosis; Drug induced cell surface GRP78; Triple negative breast cancer cells

Indexed keywords

CASPASE 3; CYTOCHROME C; DOCETAXEL; DOXORUBICIN; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; TUNICAMYCIN; HEAT SHOCK PROTEIN; MOLECULAR CHAPERONE GRP78;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER CELL LINE; CANCER INHIBITION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PROTEIN EXPRESSION; PROTEIN SECRETION; RECEPTOR BLOCKING; TRIPLE NEGATIVE BREAST CANCER; TUMOR VOLUME; UPREGULATION; ANIMAL; CELL MEMBRANE; CELL SEPARATION; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; SIGNAL TRANSDUCTION; TUMOR CELL LINE; UNFOLDED PROTEIN RESPONSE;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL MEMBRANE; CELL SEPARATION; DOXORUBICIN; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAT-SHOCK PROTEINS; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP; TRIPLE NEGATIVE BREAST NEOPLASMS; TUNICAMYCIN; UNFOLDED PROTEIN RESPONSE;

EID: 84917737300     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2576     Document Type: Article

References (61)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61:69-90.
2. DeSantis C, Siegel R, Bandi P, Jemal A. Breast cancer statistics, 2011. CA Cancer J Clin. 2011; 61:409-418.
3. Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D. Molecular portraits of human breast tumours. Nature. 2000; 406:747-752.
4. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001; 98:10869-10874.
5. Sotiriou C, Neo SY, McShane LM, Korn EL, Long PM, Jazaeri A, Martiat P, Fox SB, Harris AL, Liu ET. Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci U S A. 2003; 100:10393-10398.
6. Guedj M, Marisa L, de Reynies A, Orsetti B, Schiappa R, Bibeau F, MacGrogan G, Lerebours F, Finetti P, Longy M, Bertheau P, Bertrand F, Bonnet F, et al. A refined molecular taxonomy of breast cancer. Oncogene. 2012; 31:1196-1206.
7. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, Lickley LA, Rawlinson E, Sun P, Narod SA. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007; 13:4429-4434.
8. Chen JQ, Russo J. ER alpha-negative and triple negative breast cancer: molecular features and potential therapeutic approaches. Biochim Biophys Acta. 2009; 1796:162-175.
9. Mayer IA, Abramson VG, Lehmann BD, Pietenpol JA. New Strategies for Triple-Negative Breast Cancer Deciphering the Heterogeneity. Clin Cancer Res. 2014; 20:782-790.
10. Lee AS. Mammalian stress response: induction of the glucose-regulated protein family. Curr. Opin. Cell Biol. 1992; 4:267-273.
11. Haas IG. BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia. 1994; 50:1012-20.
12. Ni M, Zhang Y, Lee AS. Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signaling and therapeutic targeting. Biochem. J. 2011; 434:181-188.
13. Fu Y, Lee AS. Glucose Regulated Proteins in Cancer Progression, Drug Resistance and Immunotherapy. Cancer Biology & Therapy. 2006; 5:741-744.
14. 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; 67:3734-3740.
15. Shuda M, Kondoh N, Imazeki N, Tanaka K, Okada T, Mori K, Hada A, Arai M, Wakatsuki T, Matsubara O, Yamamoto N, Yamamoto M. Activation of the ATF6, XBP1 and grp78 genes in human hepatocellular carcinoma: a possible involvement of the ER stress pathway in hepatocarcinogenesis. J Hepatol. 2003; 38:605-614.
16. Kim R, Emi M, Tanabe K, Murakami S. Role of the unfolded protein response in cell death. Apoptosis. 2006; 11:5-13.
17. Lee AS. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res. 2007; 67:496-499.
18. Schwarze S, Rangnekar VM. Targeting plasma membrane GRP78 for cancer growth inhibition. Cancer Biology & Therapy. 2010; 9:153-155.
19. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 2005; 24:1243-1255.
20. Berger CL, Dong Z, Hanlon D, Bisaccia E, Edelson RL. A lymphocyte cell surface heat shock protein homologous to the endoplasmic reticulum chaperone, immunoglobulin heavy chain binding protein BIP. Int. J. Cancer. 1997; 71:1077-1085.
21. Xiao G, Chung TF, Pyun HY, Fine RE, Johnson RJ. KDEL proteins are found on the surface of NG108-NG115 cells. Brain Res. Mol. Brain Res. 1999; 72:121-128.
22. Shin BK, Wang H, Yim AM, Le Naour F, Brichory F, Jang JH, Zhao R, Puravs E, Tra J, Michael CW, Misek DE, Hanash SM. Global profiling of the cell surface proteome of cancer cells uncovers an abundance of proteins with chaperone function. J. Biol. Chem. 2003; 278:7607-7616.
23. Misra UK, Gonzalez-Gronow M, Gawdi G, Wang F, Pizzo SV. A novel receptor function for the heat shock protein Grp78: silencing of Grp78 gene expression attenuates α2M*-induced signalling. Cell. Signalling. 2004; 16:929-938.
24. Liu Y, Steiniger SC, Kim Y, Kaufmann GF, Felding-Habermann B, Janda KD. Mechanistic studies of a peptidic GRP78 ligand for cancer cell-specific drug delivery. Mol. Pharm. 2007; 4:435-447.
25. Jakobsen CG, Rasmussen N, Laenkholm AV, Ditzel HJ. Phage display derived human monoclonal antibodies isolated by binding to the surface of live primary breast cancer cells recognize GRP78. Cancer Res. 2007; 67:9507-9517.
26. Rauschert N, Brandlein S, Holzinger E, Hensel F, Muller-Hermelink HK, Vollmers HP. A new tumor-specific variant of GRP78 as target for antibody-based therapy. Lab. Invest. 2008; 88:375-386.
27. Lee E, Nichols P, Groshen S, Spicer D, Lee AS. GRP78 as potential predictor for breast cancer response to adjuvant taxane therapy. Int. J. Cancer. 2011; 128:726-731.
28. 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; 278:20915-20924.
29. Thomas S, Sharma N, Gonzalez R, Pao P-W, Hofman FM, Chen TC, Louies SG, Pirrung MC, Schontal AS. Repositioning of Verrucosidin, a Purported Inhibitor of Chaperone Protein GRP78, as an Inhibitor of Mitochondrial Electron Transport Chain Complex I. PLoS ONE. 2013; 8:e65695. doi:10.1371/journal.
30. Singha PK, Pandeswara S, Venkatachalam MA, Saikumar P. Manumycin A inhibits triple-negative breast cancer growth through LC3-mediated cytoplasmic vacuolation death. Cell Death and Disease. 2013; 4:e457. doi:10.1038.
31. Mudvari P, Ohshiro K, Nair V, Horvath A, Kumar R. Genomic Insights into Triple-Negative and HER2-Positive Breast Cancers Using Isogenic Model Systems. PLoS ONE. 2013; 8:e74993.
32. Hardy B, Raiter A, Yakimov M, Vilkin A, Niv Y. Colon cancer cells expressing cell surface GRP78 as a marker for reduced tumorigenicity. Cell Oncol. 2012; 35:345-354.
33. de Ruijter TC, Veeck J, de Hoon JP, van Engeland M, Tjan-Heijnen VC. Characteristics of triple-negative breast cancer. J Cancer Res Clin Oncol. 2011; 137:183-192.
34. Reddy KB. Triple-negative breast cancers: an updated review on treatment options. Curr Oncol. 2011; 18:e173-9.
35. Issa A, Gill JW, Heideman MR, Sahin O, Wiemann S, Dey JH, Hynes NE. Combinatorial targeting of FGF and ErbB receptors blocks growth and metastatic spread of breast cancer models. Breast Cancer Research. 2013; 15:R8.
36. Xue M, Ge Y, Zhang J, Wang Q, Hou L, Liu Y, Sun L, Li Q. Anticancer Properties and Mechanisms of Fucoidan on Mouse Breast Cancer In Vitro and In Vivo. PLoS ONE. 2012; 7:e43483.
37. Lal S, Mahajan A, WN, Chowbay B. Pharmacogenetics of Target Genes Across Doxorubicin Disposition Pathway: A Review. Current Drug Metabolism. 2010; 11:115-128.
38. Kim SJ, Park KM, Kim N, Yeom IY. Doxorubicin prevents endoplasmic reticulum stress-induced apoptosis. Biochemical and Biophysical Research Communications. 2006; 339:463-468.
39. Lai HC, Yeh YC, Ting CT, Lee WL, Lee HW, Wang LC, Wang KY, Lai HC, Wu A, Liu TJ. Doxycycline suppresses doxorubicin induced oxidative stress and cellular apoptosis in mouse hearts. Eur J Pharmacol. 2010; 644:176-187.
40. Lu M, Merali S, Gordon R, Jiang J, Li Y, Mandeli J, Duan X, Fallon J, Holland JF. Prevention of Doxorubicin Cardiopathic Changes by a Benzyl Styryl Sulfone in Mice. Genes and Cancer. 2011; 2:985-992.
41. Schonthal AH. Endoplasmic Reticulum Stress: Its Role in Disease and Novel Prospects for Therapy Hindawi Publishing Corporation Scientifica Volume 2012, Article ID 857516, http://dx.doi.org/10.6064/2012/857516.
42. Ma H, Miao X, Ma Q, Zheng W, Zhou H, Jia L. Functional Roles of Glycogene and N-Glycan in Multidrug Resistance of Human Breast Cancer Cells. IUBMB Life. 2013; 65:409-422.
43. Li Z, Wang Y, Wu H, Zhang L, Yang P, Li Z. GRP78 enhances the glutamine metabolism to support cell survival from glucose deficiency by modulating the β-catenin signaling. Oncotarget. 2014; 5:5369-5380.
44. Zheng YZ, Cao ZG, Hu X, Shao ZM. The endoplasmic reticulum stress markers GRP78 and CHOP predict disease-free survival and responsiveness to chemotherapy in breast cancer. Breast Cancer Res Treat. 2014; 145:349-358.
45. Hsu WM, Hsieh FJ, Jeng YM, Kuo ML, Tsao PN, Lee H, Lin MT, Lai HS, Chen CN, Lai DM, Chen WJ. GRP78 expression correlates with histologic differentiation and favorable prognosis in neuroblastic tumors. Int J Cancer. 2005; 113:920-927.
46. Uramoto H, Sugio K, Oyama T, Nakata S, Ono K, Yoshimastu T, Morita M, Yasumoto K. Expression of endoplasmic reticulum molecular chaperone Grp78 in human lung cancer and its clinical significance. Lung Cancer. 2005 Jul; 49:55-62.
47. Bao L, Haque A, Jackson K, Hazari S, Moroz K, Jetly R, Dash R. Increased Expression of P-Glycoprotein Is Associated with Doxorubicin Chemoresistance in the Metastatic 4T1 Breast Cancer Model. Am J Pathol. 2011; 178:838-852.
48. Dricu A, Carlberg M, Wang M, Larsson O. Inhibition of N-linked Glycosylation Using Tunicamycin Causes Cell Death in Malignant Cells: Role of Down-Regulation of the Insulin-like Growth Factor 1 Receptor in Induction of Apoptosis. Cancer Research. 1997; 57:543-548.
49. Goldenberg-Cohen N, Raiter A, Gaydar V, Dratviman-Storobinsky O, Goldstein T, Weizman A, Hardy B. Peptide-binding GRP78 protects neurons from hypoxia-induced apoptosis. Apoptosis. 2012; 17:278-288.
50. Abu-Qare AW, Abou-Donia MB. Biomarkers of apoptosis: release of cytochrome c, activation of caspase 3, induction of 8 hydroxy-2'deoxyguanosine, increased 3 nitrotyrosine and alteration of p53 gene. J. Toxicol. Environ. Health B Crit. Rev. 2001; 4:313-332.
51. Campos CB, Paim BA, Cosso RG, Castilho RF, Rottenberg H, Vercesi AE. Method for monitoring of mitochondrial cytochrome c release during cell death: Immunodetection of cytochrome c by flow cytometry after selective permeabilization of the plasma membrane Cytometry A. 2006; 69:515-523.
52. Nakamura S, Takizawa H, Shimazawa M, Hashimoto Y, Sugitani S, Tsuruma K, Hara H. Mild Endoplasmic Reticulum Stress Promotes Retinal Neovascularization via Induction of BiP/GRP78. PLoS ONE. 2013; 8:e60517.
53. Axel H. Schonthal. Pharmacological targeting of endoplasmic reticulum stress signaling in cancer. Biochemical Pharmacology. 2013; 85:653-666.
54. Kandala PK, Srivastava SK. Regulation of macroautophagy in ovarian cancer cells in vitro and in vivo by controlling Glucose regulatory protein 78 and AMPK. Oncotarget. 2012; 3:435-449.
55. Misra UK, Pizzo SV. Ligation of cell surface GRP78 with antibody directed against the COOH-terminal domain of GRP78 suppresses Ras/MAPK and PI 3-kinase/AKT signaling while promoting caspase activation in human prostate cancer cells. Cancer Biol. Ther. 2010; 9:142-152.
56. Deally CM, Weiberg LE, Singal PK. Subcellular effects of adriamycin in the heart: a concise review. J Mol Cell Cardiol. 1987; 19:817-828.
57. Mintz PJ, Kim J, Do KA, Wang X, Zinner RG, Cristofanilli M, Arap MA, Hong WK, Troncoso P, Logothetis CJ, Pasqualini R, Arap W. Fingerprinting the circulating repertoire of antibodies from cancer patients. Nat Biotechnol. 2003; 21:57-63.
58. Gonzalez-Gronow M, Cuchacovich M, Llanos C, Urzua C, Gawdi G, Pizzo SV. Prostate cancer cell proliferation in vitro is modulated by antibodies against glucose-regulated protein 78 isolated from patient serum. Cancer Res. 2006; 66:11424-11431.
59. Taylor DD, Gercel-Taylor C, Parker LP. Patient derived tumor reactive antibodies as diagnostic markers for ovarian cancer. Gynecol Oncol. 2009; 115:112-120.
60. Raiter A, Vilkin A, Gingold R, Levi Z, Halpern M, Niv Y, Hardy B. The presence of anti-GRP78 antibodies in the serum of patients with colorectal carcinoma: a potential biomarker for early cancer detection.
61. Defresne F, Bouzin C, Guilbaud C, Dieu M, Delaive E, Michiels C, Raes M, Feron O. Anticancer treatments and angiogenesis on the seric titer of autoantibody used as tumor and metastasis biomarker. Neoplasia. 2010; 12:562-570