ATP2A3 gene as an important player for resveratrol anticancer activity in breast cancer cells

Molecular Carcinogenesis

Volumn 56, Issue 7, 2017, Pages 1703-1711

  Izquierdo Torres, Eduardo ^a   Rodríguez, Gabriela ^a   Meneses Morales, Iván ^a   Zarain Herzberg, Angel ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

apoptosis; breast cancer cells; calcium; resveratrol; SERCA

Indexed keywords

CASPASE 3; KI 67 ANTIGEN; RESVERATROL; ANTINEOPLASTIC AGENT; ATP2A2 PROTEIN, HUMAN; ATP2A3 PROTEIN, HUMAN; CALCIUM; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SMALL INTERFERING RNA; STILBENE DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; ATP2A3 GENE; BREAST CANCER; CALCIUM TRANSPORT; CELL VIABILITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; MCF-7 CELL LINE; MDA-MB-231 CELL LINE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; UPREGULATION; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL PROLIFERATION; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL CULTURE;

ANTICARCINOGENIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CALCIUM; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; RNA, SMALL INTERFERING; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; STILBENES; TUMOR CELLS, CULTURED;

EID: 85013642734     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22625     Document Type: Article

References (60)

1. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: Dynamics, homeostasis and remodelling. Nature Rev Mol Cell Biol. 2003; 4:517–529.
2. Brini M, Carafoli E. Calcium pumps in health and disease. Physiol Rev. 2009; 89:1341–1378.
3. Arbabian A, Brouland JP, Gelebart P, et al. Endoplasmic reticulum calcium pumps and cancer. BioFactors. 2011; 37:139–149.
4. Roderick HL, Cook SJ. Ca2+ signalling checkpoints in cancer: Remodelling Ca2+ for cancer cell proliferation and survival. Nat Rev Cancer. 2008; 8:361–375.
5. Periasamy M, Kalyanasundaram A. SERCA pump isoforms: Their role in calcium transport and disease. Muscle Nerve. 2007; 35:430–442.
6. Korczak B, Zarain-Herzberg A, Brandl CJ, Ingles CJ, Green NM, MacLennan DH. Structure of the rabbit fast-twitch skeletal muscle Ca2+−ATPase gene. J Biol Chem. 1988; 263:4813–4819.
7. Zarain-Herzberg A, MacLennan DH, Periasamy M. Characterization of rabbit cardiac sarco(endo)plasmic reticulum Ca2(+)-ATPase gene. J Biol Chem. 1990; 265:4670–4677.
8. Kovacs T, Felfoldi F, Papp B, et al. All three splice variants of the human sarco/endoplasmic reticulum Ca2+−ATPase 3 gene are translated to proteins: A study of their co-expression in platelets and lymphoid cells. Biochem J. 2001; 358:559–568.
9. Martin V, Bredoux R, Corvazier E, et al. Three novel sarco/endoplasmic reticulum Ca2+−ATPase (SERCA) 3 isoforms. Expression, regulation, and function of the membranes of the SERCA3 family. J Biol. Chem. 2002; 277:24442–24452.
10. Endo Y, Uzawa K, Mochida Y, et al. Sarcoendoplasmic reticulum Ca(2+) ATPase type 2 downregulated in human oral squamous cell carcinoma. Int J Cancer. 2004; 110:225–231.
11. Gelebart P, Kovacs T, Brouland JP, et al. Expression of endomembrane calcium pumps in colon and gastric cancer cells. Induction of SERCA3 expression during differentiation. J Biol Chem. 2002; 277:26310–26320.
12. Pacifico F, Ulianich L, De Micheli S, et al. The expression of the sarco/endoplasmic reticulum Ca2 + −ATPases in thyroid and its down-regulation following neoplastic transformation. J Mol Endocrinol. 2003; 30:399–409.
13. Papp B, Brouland JP. Altered endoplasmic reticulum calcium pump expression during Breast tumorigenesis. Breast Cancer. 2011; 5:163–174.
14. Arbabian A, Brouland JP, Apati A, et al. Modulation of endoplasmic reticulum calcium pump expression during lung cancer cell differentiation. FEBS J. 2013; 280:5408–5418.
15. Ghoncheh M, Mirzaei M, Salehiniya H. Incidence and mortality of Breast cancer and their relationship with the human development index (HDI) in the world in 2012. Asian Pac J Cancer Prev. 2015; 16:8439–8443.
16. Duffy C, Perez K, Partridge A. Implications of phytoestrogen intake for breast cancer. CA Cancer J Clin. 2007; 57:260–277.
17. Rice S, Whitehead SA. Phytoestrogens and breast cancer-promoters or protectors? Endocr Relat Cancer. 2006; 13:995–1015.
18. Athar M, Back JH, Tang X, et al. Resveratrol: A review of preclinical studies for human cancer prevention. Toxicol Appl Pharmacol. 2007; 224:274–283.
19. Pozo-Guisado E, Alvarez-Barrientos A, Mulero-Navarro S, Santiago-Josefat B, Fernandez-Salguero PM. The antiproliferative activity of resveratrol results in apoptosis in MCF-7 but not in MDA-MB-231 human breast cancer cells: Cell-specific alteration of the cell cycle. Biochem Pharmacol. 2002; 64:1375–1386.
20. Li Y, Liu J, Liu X, et al. Resveratrol-induced cell inhibition of growth and apoptosis in MCF7 human breast cancer cells are associated with modulation of phosphorylated Akt and caspase-9. Appl Biochem Biotechnol. 2006; 135:181–192.
21. Leon-Galicia I, Diaz-Chavez J, Garcia-Villa E, et al. Resveratrol induces downregulation of DNA repair genes in MCF-7 human breast cancer cells. Eur J Cancer Prev. 2013; 22:11–20.
22. Tang HY, Shih A, Cao HJ, Davis FB, Davis PJ, Lin HY. Resveratrol-induced cyclooxygenase-2 facilitates p53-dependent apoptosis in human breast cancer cells. Mol Cancer Ther. 2006; 5:2034–2042.
23. Papoutsis AJ, Lamore SD, Wondrak GT, Selmin OI, Romagnolo DF. Resveratrol prevents epigenetic silencing of BRCA-1 by the aromatic hydrocarbon receptor in human breast cancer cells. J Nutr. 2010; 140:1607–1614.
24. Cai Y, Zhao L, Qin Y, Zhang M, He Y. Resveratrol inhibits proliferation and induces apoptosis of nasopharyngeal carcinoma cell line C666-1 through AMPK activation. Die Pharmazie. 2015; 70:399–403.
25. Chin YT, Hsieh MT, Yang SH, et al. Anti-proliferative and gene expression actions of resveratrol in breast cancer cells in vitro. Oncotarget. 2014; 5:12891–12907.
26. Wu Z, Liu B, E C, et al. Resveratrol inhibits the proliferation of human melanoma cells by inducing G1/S cell cycle arrest and apoptosis. Mol Med Rep. 2015; 11:400–404.
27. Alkhalaf M. Resveratrol-induced apoptosis is associated with activation of p53 and inhibition of protein translation in T47D human breast cancer cells. Pharmacology. 2007; 80:134–143.
28. Alkhalaf M, El-Mowafy A, Renno W, Rachid O, Ali A, Al-Attyiah R. Resveratrol-induced apoptosis in human breast cancer cells is mediated primarily through the caspase-3-dependent pathway. Arch Med Res. 2008; 39:162–168.
29. Benitez DA, Pozo-Guisado E, Alvarez-Barrientos A, Fernandez-Salguero PM, Castellon EA. Mechanisms involved in resveratrol-induced apoptosis and cell cycle arrest in prostate cancer-derived cell lines. J Androl. 2007; 28:282–293.
30. Demoulin B, Hermant M, Castrogiovanni C, Staudt C, Dumont P. Resveratrol induces DNA damage in colon cancer cells by poisoning topoisomerase II and activates the ATM kinase to trigger p53-dependent apoptosis. Toxicol In Vitro. 2015; 29:1156–1165.
31. Lang F, Qin Z, Li F, Zhang H, Fang Z, Hao E. Apoptotic cell death induced by resveratrol is partially mediated by the autophagy pathway in human ovarian cancer cells. PLoS ONE. 2015; 10:e0129196.
32. Lucas IK, Kolodziej H. Trans-resveratrol induces apoptosis through ROS-triggered mitochondria-dependent pathways in A549 human lung adenocarcinoma epithelial cells. Planta Med. 2015; 81:1038–1044.
33. Wong RS. Apoptosis in cancer: From pathogenesis to treatment. J Exp Clin Cancer Res. 2011; 30:87.
34. Sulaiman M, Matta MJ, Sunderesan NR, Gupta MP, Periasamy M, Gupta M. Resveratrol, an activator of SIRT1, upregulates sarcoplasmic calcium ATPase and improves cardiac function in diabetic cardiomyopathy. Am J Physiol Heart Circulat Physiol. 2010; 298:H833–H843.
35. Contreras-Leal E, Hernandez-Oliveras A, Flores-Peredo L, Zarain-Herzberg A, Santiago-Garcia J. Histone deacetylase inhibitors promote the expression of ATP2A3 gene in breast cancer cell lines. Mol Carcinog. 2016; 55:1477–1485.
36. Sergeev IN, Rhoten WB. Regulation of intracellular calcium in human breast cancer cells. Endocrine. 1998; 9:321–327.
37. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R. Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene. 2008; 27:6407–6418.
38. Chen FP, Chien MH. Phytoestrogens induce differential effects on both normal and malignant human breast cells in vitro. Climacteric. 2014; 17:682–691.
39. Sareen D, Darjatmoko SR, Albert DM, Polans AS. Mitochondria, calcium, and calpain are key mediators of resveratrol-induced apoptosis in breast cancer. Mol Pharmacol. 2007; 72:1466–1475.
40. Alayev A, Berger SM, Kramer MY, Schwartz NS, Holz MK. The combination of rapamycin and resveratrol blocks autophagy and induces apoptosis in breast cancer cells. J Cell Biochem. 2015; 116:450–457.
41. Chatterjee A, Ronghe A, Singh B, Bhat NK, Chen J, Bhat HK. Natural antioxidants exhibit chemopreventive characteristics through the regulation of CNC b-Zip transcription factors in estrogen-induced breast carcinogenesis. J Biochem Mol Toxicol. 2014; 28:529–538.
42. Khan A, Aljarbou AN, Aldebasi YH, Faisal SM, Khan MA. Resveratrol suppresses the proliferation of breast cancer cells by inhibiting fatty acid synthase signaling pathway. Cancer Epidemiol. 2014; 38:765–772.
43. Khan MA, Chen HC, Wan XX, et al. Regulatory effects of resveratrol on antioxidant enzymes: A mechanism of growth inhibition and apoptosis induction in cancer cells. Mol Cells. 2013; 35:219–225.
44. Lee-Chang C, Bodogai M, Martin-Montalvo A, et al. Inhibition of breast cancer metastasis by resveratrol-mediated inactivation of tumor-evoked regulatory B cells. J Immunol. 2013; 191:4141–4151.
45. Qin Y, Ma Z, Dang X, Li W, Ma Q. Effect of resveratrol on proliferation and apoptosis of human pancreatic cancer MIA PaCa-2 cells may involve inhibition of the Hedgehog signaling pathway. Mol Med Rep. 2014; 10:2563–2567.
46. Subik K, Lee JF, Baxter L, et al. The expression patterns of ER, PR, HER2, CK5/6, EGFR, ki-67 and AR by immunohistochemical analysis in Breast cancer cell lines. Breast Cancer. 2010; 4:35–41.
47. Mooney LM, Al-Sakkaf KA, Brown BL, Dobson PR. Apoptotic mechanisms in T47D and MCF-7 human breast cancer cells. Br J Cancer. 2002; 87:909–917.
48. Lin HY, Lansing L, Merillon JM, et al. Integrin alphaVbeta3 contains a receptor site for resveratrol. FASEB J. 2006; 20:1742–1744.
49. Bhat KP, Pezzuto JM. Cancer chemopreventive activity of resveratrol. Ann NY Acad Sci. 2002; 957:210–229.
50. Teixeira C, Reed JC, Pratt MA. Estrogen promotes chemotherapeutic drug resistance by a mechanism involving Bcl-2 proto-oncogene expression in human breast cancer cells. Cancer Res. 1995; 55:3902–3907.
51. Chandrasekera PC, Kargacin ME, Deans JP, Lytton J. Determination of apparent calcium affinity for endogenously expressed human sarco(endo)plasmic reticulum calcium-ATPase isoform SERCA3. Am J Physiol Cell Physiol. 2009; 296:C1105–C1114.
52. Dode L, Vilsen B, Van Baelen K, Wuytack F, Clausen JD, Andersen JP. Dissection of the functional differences between sarco(endo)plasmic reticulum Ca2 + −ATPase (SERCA) 1 and 3 isoforms by steady-state and transient kinetic analyses. J Biol Chem. 2002; 277:45579–45591.
53. Azimi I, Roberts-Thomson SJ, Monteith GR. Calcium influx pathways in breast cancer: Opportunities for pharmacological intervention. Br J Pharmacol. 2014; 171:945–960.
54. Brini M, Bano D, Manni S, Rizzuto R, Carafoli E. Effects of PMCA and SERCA pump overexpression on the kinetics of cell Ca(2 +) signalling. EMBO J. 2000; 19:4926–4935.
55. Oancea E, Meyer T. Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell. 1998; 95:307–318.
56. De Koninck P, Schulman H. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science. 1998; 279:227–230.
57. Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature. 1997; 386:855–858.
58. Dolmetsch RE, Xu K, Lewis RS. Calcium oscillations increase the efficiency and specificity of gene expression. Nature. 1998; 392:933–936.
59. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: The calcium-apoptosis link. Nat Rev Mol Cell Biol 2003; 4:552–565.
60. Bonneau B, Prudent J, Popgeorgiev N, Gillet G. Non-apoptotic roles of Bcl-2 family: The calcium connection. Biochim Biophys Acta. 2013; 1833:1755–1765.