Inositol 1,4,5-trisphosphate-induced Ca2+ signalling is involved in estradiol-induced breast cancer epithelial cell growth

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Szatkowski, Cécilia ^a   Parys, Jan B ^b   Ouadid Ahidouch, Halima ^a   Matifat, Fabrice ^a  

^a AMIENS UNIVERSITY HOSPITAL   (France)

^b Laboratory of Molecular and Cellular Signaling   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; 2 AMINOETHOXYDIPHENYLBORANE; CAFFEINE; CALCIUM ION; ESTRADIOL; FULVESTRANT; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; SMALL INTERFERING RNA; XESTOSPONGIN C;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL GROWTH; CELL PROLIFERATION; CELL STRAIN MCF 7; CONTROLLED STUDY; CULTURE MEDIUM; EPITHELIUM CELL; FETAL CALF SERUM; GENE SILENCING; GROWTH INHIBITION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; RNA INTERFERENCE; WESTERN BLOTTING; BREAST TUMOR; CELL DIFFERENTIATION; CELL DIVISION; DRUG EFFECT; FEMALE; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

BLOTTING, WESTERN; BREAST NEOPLASMS; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE, TUMOR; EPITHELIAL CELLS; ESTRADIOL; FEMALE; GENE SILENCING; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; RNA INTERFERENCE;

EID: 77953669483     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-156     Document Type: Article

References (55)

1. Berridge MJ. Calcium signalling and cell proliferation. Bioessays 1995, 17:491-500. 10.1002/bies.950170605, 7575490.
2. Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nature Rev 2000, 1:11-21.
3. Berridge MJ. Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta 2009, 1793:933-940. 10.1016/j.bbamcr.2008.10.005, 19010359.
4. Roderick HL, Cook SJ. Ca2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival. Nature Rev 2008, 8:361-375.
5. Vucenik I, Ramakrishna G, Tantivejkul K, Anderson LM, Ramljak D. Inositol hexaphosphate (IP6) blocks proliferation of human breast cancer cells through a PKCδ-dependent increase in p27Kip1 and decrease in retinoblastoma protein (pRb) phosphorylation. Breast Cancer Res and Tr 2005, 91:35-45.
6. Powis G, Phil D. Inhibitors of phosphatidylinositol signalling as antiproliferative agents. Cancer Metast Rev 1994, 13:91-105.
7. Cole K, Kohn E. Calcium-mediated signal transduction: biology, chemistry and therapy. Cancer Metast Rev 1994, 13:31-44.
8. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ. Calcium and cancer: targeting Ca2+ transport. Nat Rev Cancer 2007, 7:519-530. 10.1038/nrc2171, 17585332.
9. Sergeev IN. Calcium as a mediator of 1,25-dihydroxyvitamin D3-induced apoptosis. J Steroid Biochem Mol Biol 2004, 90:419-425.
10. Sergeev IN. Calcium signaling in cancer and vitamin D. J Steroid Biochem Mol Biol 2005, 97:145-151. 10.1016/j.jsbmb.2005.06.007, 16081284.
11. Sergeev IN. Genistein induces Ca2+ -mediated, calpain/caspase-12-dependent apoptosis in breast cancer cells. Biochem Biophys Res Commun 2004, 321:462-467. 10.1016/j.bbrc.2004.06.173, 15358198.
12. Foskett JK, White C, Cheung KH, Mak DO. Inositol trisphosphate receptor Ca2+ release channel. Physiol Rev 2007, 87:593-658. 10.1152/physrev.00035.2006, 17429043.
13. Miyakawa T, Maeda A, Yamazawa T, Hirose K, Kurosaki T, Iino M. Encoding of Ca2+ signals by diffential expression of IP3 receptor subtypes. EMBO J 1999, 18:1303-1308. 10.1093/emboj/18.5.1303, 1171220, 10064596.
14. Hattori M, Suzuki A, Higo T, Miyauchi H, Michikawa T, Nakamura T, Inoue T, Mikoshiba K. Distinct roles of inositol 1,4,5-trisphosphate receptor types 1 and 3 in Ca2+ signalling. J Biol Chem 2004, 279:11967-11975. 10.1074/jbc.M311456200, 14707143.
15. Lipskaia L, Lompré AM. Alteration in temporal kinetics of Ca2+ signalling and control of growth and proliferation. Biol Cell 2004, 96:55-68. 10.1016/j.biolcel.2003.11.001, 15093128.
16. Li W, Llopis J, Whitney M, Zlokarnic G, Tsien RY. Cell-permeant caged-InsP3 ester shows that Ca2+ spike frequency can optimize gene expression. Nature 1998, 392:936-941. 10.1038/31965, 9582076.
17. Dolmetsch RE, Xu K, Lewis RS. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998, 392:933-936. 10.1038/31960, 9582075.
18. Henderson IC. Risk factors for breast cancer development. Cancer 1993, 71:2127-4210. 10.1002/1097-0142(19930315)71:6+<2127::AID-CNCR2820711602>3.0.CO;2-2, 8443762.
19. Platet N, Cathiard AM, Gleizes M, Garcia M. Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit Rev Oncol Hematol 2004, 51:55-67. 10.1016/j.critrevonc.2004.02.001, 15207254.
20. Huang J, Li X, Yi P, Hilf R, Bambara RA, Muyan M. Targeting estrogen responsive elements (EREs): design of potent transactivators for ERE-containing genes. Mol Cell Endocrinol 2004, 218:65-78. 10.1016/j.mce.2003.12.005, 15130512.
21. Foster JS, Henley DC, Ahamed S, Wimalasena J. Estrogens and cell-cycle regulation in breast cancer. Trends Endocrinol Metab 2001, 12:320-327. 10.1016/S1043-2760(01)00436-2, 11504672.
22. Dukik D, Shiu RP. Mechanisms of estrogen activation of c-myc oncogene expression. Oncogene 1992, 7:1587-1594.
23. Prall OW, Rogan EM, Musgrove EA, Watts CK, Sutherland RL. c-Myc or Cyclin D1 Mimics Estrogen Effects on Cyclin E-Cdk2 Activation and Cell Cycle Re-entry. Mol Cell Biol 1998, 18:4499-4508. 109035, 9671459.
24. Coiret G, Matifat F, Hague F, Ouadid-Ahidouch H. 17-beta-estradiol activates maxi-K channels through a non-genomic pathway in human breast cancer cells. FEBS Lett 2005, 579:2995-3000. 10.1016/j.febslet.2005.02.085, 15893312.
25. Walsh DE, Dockery P, Doolan CM. Estrogen receptor independent rapid non-genomic effects of environmental estrogens on [Ca2+]i in human breast cancer cells. Mol Cell Endocrinol 2005, 230:23-30. 10.1016/j.mce.2004.11.006, 15664448.
26. DeWald DB, Torabinejad J, Samant RS, Johnston D, Erin N, Shope JC, Xie Y, Welch DR. Metastasis suppression by breast cancer metastasis suppressor 1 involves reduction of phosphoinositide signaling in MDA-MB-435 breast carcinoma cells. Cancer Res 2005, 65:713-717.
27. Taylor JA, Grady LH, Engler KS, Welshons WV. Relationship of growth stimulated by lithium, estradiol, and EGF to phospholipase C activity in MCF-7 human breast cancer cells. Breast Cancer Res Tr 1995, 34:265-277.
28. Thomas W, Coen N, Faherty S, Flatharta CO, Harvey BJ. Estrogen induces phospholipase A2 activation through ERK1/2 to mobilize intracellular calcium in MCF-7 cells. Steroids 2006, 71:256-265. 10.1016/j.steroids.2005.10.010, 16375935.
29. Bollig A, Xu L, Thakur A, Wu J, Kuo TH, Liao JD. Regulation of intracellular calcium release and PP1alpha in a mechanism for 4-hydroxytamoxifen-induced cytotoxicity. Mol Cell Biochem 2007, 305:45-54. 10.1007/s11010-007-9526-2, 17646931.
30. Xu L, Kong D, Zhu L, Zhu W, Andrews DW, Kuo TH. Suppression of IP3-mediated calcium release and apoptosis by Bcl-2 involves the participation of protein phosphatase-1. Mol Cell Biochem 2007, 295:153-165. 10.1007/s11010-006-9285-5, 16874461.
31. Patel KV, Schrey MP. Activation of Inositol Phospholipid Signaling and Ca2+ Efflux in Human Breast Cancer Cells by Bombesin. Cancer Res 1990, 50:235-239.
32. Maruyama T, Kanaji T, Nakade S, Kanno T, Mikoshiba K. 2APB, 2-aminoethoxydiphenyl borate, a membrane-penetrable modulator of Ins(1,4,5)P3-induced Ca2+ release. J Biochem 1997, 122:498-505.
33. Wakeling AE, Dukes M, Bowler J. A potent specific pure antiestrogen with clinical potential. Cancer Research 1991, 51:3867-73.
34. Dixon CJ, Bowler WB, Fleetwood P, Ginty AF, Gallagher JA, Carron JA. Extracellular nucleotides stimulate proliferation in MCF-7 breast cancer cells via P2-purinoceptors. Br J Cancer 1997, 75:34-39. 2222689, 9000595.
35. Improta-Brears T, Whorton AR, Codazzi F, York JD, Meyer T, McDonnell DP. Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium. Proc Natl Acad Sci USA 1999, 96:4686-4691. 10.1073/pnas.96.8.4686, 16393, 10200323.
36. Wilkerson MK, Heppner TJ, Boney AD, Nelson MT. Inositol trisphosphate receptor calcium release is required for cerebral artery smooth muscle cell proliferation. Am J Physiol Heart Circ Physiol 2006, 290:240-247.
37. Francis H, Glaser S, DeMorrow S, Gaudio E, Ueno Y, Venter J, Dostal D, Onori P, Franchitto A, Marzioni M, Vaculin S, Vaculin B, Katki K, Stutes M, Savage J, Alpini G. Small mouse cholangiocytes proliferate in response to H1 histamine receptor stimulation by activation of the IP3/CaMKI/CREB pathway. Am J Physiol Cell Physiol 2008, 295:499-513.
38. Sakakura C, Hagiwara A, Fukuda K, Shimomura K, Takagi T, Kin S, Nakase Y, Fujiyama J, Mikoshiba K, Okazaki Y, Yamagishi H. Possible involvement of inositol 1,4,5-trisphosphate receptor type 3 (IP3R3) in the peritoneal dissemination of gastric cancers. Anticancer Res 2003, 23:3691-3697.
39. Soghoian D, Jayaraman V, Silane M, Berenstein A, Jayaraman T. Inositol 1,4,5-trisphosphate receptor phosphorylation in breast cancer. Tumour Biol 2005, 26:207-212. 10.1159/000086954, 16006774.
40. Taylor CW, Genazzani AA, Morris SA. Expression of Inositol trisphosphate receptors. Cell Calcium 1999, 26:237-251. 10.1054/ceca.1999.0090, 10668562.
41. Mesonero JE, Tanfin Z, Hilly M, Colosetti P, Mauger JP, Harbon S. Differential expression of Inositol 1,4,5-trisphosphate receptor types 1, 2 and 3 in rat myometrium and endometrium during gestation. Biol Reprod 2000, 63:532-537. 10.1095/biolreprod63.2.532, 10906061.
42. Kirkwood KL, Dziak R, Bradford PG. Inositol trisphosphate receptor gene expression and hormonal regulation in osteoblast-like cell lines and primary osteoblastic cell cultures. J Bone Miner Res 1996, 11:1889-1895. 10.1002/jbmr.5650111209, 8970890.
43. Kirkwood KL, Homick K, Dragon MB, Bradford PG. Cloning and characterization of the type I inositol 1,4,5-trisphosphate receptor gene promoter. Regulation by 17beta-estradiol in osteoblasts. J Biol Chem 1997, 272:22425-22431. 10.1074/jbc.272.36.22425, 2754576, 9278393.
44. Davis MC, McColl KS, Zhong F, Wang Z, Malone MH, Distelhorst CW. Dexamethasone-induced inositol 1,4,5-trisphosphate receptor elevation in murine lymphoma cells is not required for dexamethasone-mediated calcium elevation and apoptosis. J Biol Chem 2008, 283:10357-10365. 10.1074/jbc.M800269200, 2447640, 18272518.
45. Berra-Romani R, Mazzocco-Spezzia A, Pulina MV, Golovina VA. Ca2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture. Am J Physiol Cell Physiol 2008, 295:779-790.
46. Mendes CC, Gomes DA, Thompson M, Souto NC, Goes TS, Goes AM, Rodrigues MA, Gomez MV, Nathanson MH, Leite MF. The type III inositol 1,4,5-trisphosphate receptor preferentially transmits apoptotic Ca2+ signals into mitochondria. J Bio Chem 2005, 280:40892-40900.
47. Rizzuto R, Marchi S, Bonora M, Aguiari P, Bononi A, De Stefani D, Giorgi C, Leo S, Rimessi A, Siviero R, Zecchini E, Pinton P. Ca2+ transfer from the ER to mitochondria: when, how and why?. Biochimica et Biophysica Acta 2009, 1787:1342-1351. 10.1016/j.bbabio.2009.03.015, 19341702.
48. Wu Z, Bowen WD. Role of sigma-1 receptor C-terminal segment in inositol 1,4,5-trisphosphate receptor activation: constitutive enhancement of calcium signaling in MCF-7 tumor cells. J Biol Chem 2008, 283:28198-28215. 10.1074/jbc.M802099200, 2661391, 18539593.
49. Szado T, Vanderheyden V, Parys JB, De Smedt H, Rietdorf K, Kotelevets L, Chastre E, Khan F, Landegren U, Söderberg O, Bootman M, Roderick HL. Phosphorylation of Inositol 1,4,5-trisphosphate receptors by protein kinase B/Akt inhibits Ca2+ release and apoptosis. Proc Natl Acad Sci 2008, 105:2427-2432. USA, 10.1073/pnas.0711324105, 2268153, 18250332.
50. Rong YP, Aromolaran AS, Bultynck G, Zhong F, Li X, McColl K, Matsuyama S, Herlitze S, Roderick HL, Bootman MD, Mignery GA, Parys JB, De Smedt H, Distelhorst CW. Targeting Bcl-2-IP3 receptor interaction to reverse Bcl-2's inhibition of apoptotic calcium signals. Mol Cell 2008, 31:255-265. 10.1016/j.molcel.2008.06.014, 18657507.
51. Perillo B, Sasso A, Abbondanza C, Palumbo G. 17beta-estradiol inhibits apoptosis in MCF-7 cells, inducing bcl-2 expression via two estrogen-responsive elements present in the coding sequence. Mol Cell Biol 2000, 20:2890-901. 10.1128/MCB.20.8.2890-2901.2000, 85519, 10733592.
52. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63. 10.1016/0022-1759(83)90303-4, 6606682.
53. Vanlingen S, Parys JB, Missiaen L, De Smedt H, Wuytack F, Casteels R. Distribution of inositol 1,4,5-trisphosphate receptor isoforms, SERCA isoforms and Ca2+ binding proteins in RBL-2H3 rat basophilic leukemia cells. Cell Calcium 1997, 22:475-486. 10.1016/S0143-4160(97)90075-0, 9502197.
54. Parys JB, De Smedt H, Missiaen L, Bootman MD, Sienaert I, Casteels R. Rat basophilic leukemia cells as model system for inositol 1,4,5-trisphosphate receptor IV, a receptor of the type II family: functional comparison and immunological detection. Cell Calcium 1995, 17:239-249. 10.1016/0143-4160(95)90070-5, 7664312.
55. Wojcikiewicz RJ. Type I, II, and III inositol 1,4,5-trisphosphate receptors are unequally susceptible to down-regulation and are expressed in markedly different proportions in different cell types. J Biol Chem 1995, 270:11678-11683. 10.1074/jbc.270.19.11678, 7744807.