Orai1 and STIM1 mediate SOCE and contribute to apoptotic resistance of pancreatic adenocarcinoma

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 10, 2014, Pages 2263-2269

  Kondratska, Kateryna ^a   Kondratskyi, Artem ^a   Yassine, Maya ^a   Lemonnier, Loic ^a   Lepage, Gilbert ^a   Morabito, Angela ^a   Skryma, Roman ^a   Prevarskaya, Natalia ^a  

^a Université des Sciences et Technologies de Lille   (France)

Author keywords

Apoptosis; Calcium; Chemotherapy; Pancreatic adenocarcinoma; Resistance; SOCE

Indexed keywords

CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; FLUOROURACIL; GEMCITABINE; SMALL INTERFERING RNA; STROMAL INTERACTION MOLECULE 1; THAPSIGARGIN;

ADENOCARCINOMA CELL LINE; ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CANCER CHEMOTHERAPY; DOWN REGULATION; EPITHELIUM CELL; GENETIC TRANSFECTION; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STORE OPERATED CALCIUM ENTRY; UPREGULATION; WESTERN BLOTTING;

APOPTOSIS; CALCIUM; CHEMOTHERAPY; PANCREATIC ADENOCARCINOMA; RESISTANCE; SOCE;

ADENOCARCINOMA; ANTINEOPLASTIC AGENTS; APOPTOSIS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL LINE, TUMOR; CELL PROLIFERATION; DEOXYCYTIDINE; DRUG RESISTANCE, NEOPLASM; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; PANCREATIC NEOPLASMS; RNA, SMALL INTERFERING;

EID: 84904975204     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.02.012     Document Type: Article

References (41)

1. Hezel A.F., Kimmelman A.C., Stanger B.Z., Bardeesy N., Depinho R.A. Genetics and biology of pancreatic ductal adenocarcinoma. Genes Dev. 2006, 20:1218-1249.
2. Cancer Society American Cancer Facts & Figs. 2013 2013, American Cancer Society, Atlanta.
3. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J. Clin. 2013, 63:11-30.
4. Erkan M., Reiser-Erkan C., Michalski C.W., Kong B., Esposito I., Friess H., Kleeff J. The impact of the activated stroma on pancreatic ductal adenocarcinoma biology and therapy resistance. Curr. Mol. Med. 2012, 12:288-303.
5. Kindler H.L., Niedzwiecki D., Hollis D., Sutherland S., Schrag D., Hurwitz H., Innocenti F., Mulcahy M.F., O'Reilly E., Wozniak T.F., Picus J., Bhargava P., Mayer R.J., Schilsky R.L., Goldberg R.M. Gemcitabine plus bevacizumab compared with gemcitabine plus placebo in patients with advanced pancreatic cancer: phase III trial of the Cancer and Leukemia Group B (CALGB 80303). J. Clin. Oncol. 2010, 28:3617-3622.
6. Kindler H.L., Wroblewski K., Wallace J.A., Hall M.J., Locker G., Nattam S., Agamah E., Stadler W.M., Vokes E.E. Gemcitabine plus sorafenib in patients with advanced pancreatic cancer: a phase II trial of the University of Chicago Phase II Consortium. Invest. New Drugs 2012, 30:382-386.
7. Jones S., Zhang X., Parsons D.W., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Kamiyama H., Jimeno A., Hong S.M., Fu B., Lin M.T., Calhoun E.S., Kamiyama M., Walter K., Nikolskaya T., Nikolsky Y., Hartigan J., Smith D.R., Hidalgo M., Leach S.D., Klein A.P., Jaffee E.M., Goggins M., Maitra A., Iacobuzio-Donahue C., Eshleman J.R., Kern S.E., Hruban R.H., Karchin R., Papadopoulos N., Parmigiani G., Vogelstein B., Velculescu V.E., Kinzler K.W. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321:1801-1806.
8. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
9. 2+ transfer in the control of apoptosis. Oncogene 2008, 27:6407-6418.
10. Rizzuto R., Pinton P., Ferrari D., Chami M., Szabadkai G., Magalhaes P.J., Di Virgilio F., Pozzan T. Calcium and apoptosis: facts and hypotheses. Oncogene 2003, 22:8619-8627.
11. Prevarskaya N., Skryma R., Shuba Y. Ion channels and the hallmarks of cancer. Trends Mol. Med. 2010, 16:107-121.
12. Prevarskaya N., Skryma R., Shuba Y. Targeting Ca(2)(+) transport in cancer: close reality or long perspective?. Expert Opin. Ther. Targets 2013, 17:225-241.
13. Park C.Y., Hoover P.J., Mullins F.M., Bachhawat P., Covington E.D., Raunser S., Walz T., Garcia K.C., Dolmetsch R.E., Lewis R.S. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 2009, 136:876-890.
14. 2+ homeostasis in skeletal-muscle development and function. Skelet. Muscle 2011, 1:16.
15. Abdullaev I.F., Bisaillon J.M., Potier M., Gonzalez J.C., Motiani R.K., Trebak M. Stim1 and Orai1 mediate CRAC currents and store-operated calcium entry important for endothelial cell proliferation. Circ. Res. 2008, 103:1289-1299.
16. Bisaillon J.M., Motiani R.K., Gonzalez-Cobos J.C., Potier M., Halligan K.E., Alzawahra W.F., Barroso M., Singer H.A., Jourd'heuil D., Trebak M. Essential role for STIM1/Orai1-mediated calcium influx in PDGF-induced smooth muscle migration. Am. J. Physiol. Cell Physiol. 2010, 298:C993-1005.
17. Potier M., Gonzalez J.C., Motiani R.K., Abdullaev I.F., Bisaillon J.M., Singer H.A., Trebak M. Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J. 2009, 23:2425-2437.
18. Stiber J., Hawkins A., Zhang Z.S., Wang S., Burch J., Graham V., Ward C.C., Seth M., Finch E., Malouf N., Williams R.S., Eu J.P., Rosenberg P. STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat. Cell Biol. 2008, 10:688-697.
19. Vandenberghe M., Raphael M., Lehen'kyi V., Gordienko D., Hastie R., Oddos T., Rao A., Hogan P.G., Skryma R., Prevarskaya N. ORAI1 calcium channel orchestrates skin homeostasis. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E4839-4848.
20. McAndrew D., Grice D.M., Peters A.A., Davis F.M., Stewart T., Rice M., Smart C.E., Brown M.A., Kenny P.A., Roberts-Thomson S.J., Monteith G.R. ORAI1-mediated calcium influx in lactation and in breast cancer. Mol. Cancer Ther. 2011, 10:448-460.
21. Chen Y.F., Chiu W.T., Chen Y.T., Lin P.Y., Huang H.J., Chou C.Y., Chang H.C., Tang M.J., Shen M.R. Calcium store sensor stromal-interaction molecule 1-dependent signaling plays an important role in cervical cancer growth, migration, and angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:15225-15230.
22. Flourakis M., Lehen'kyi V., Beck B., Raphael M., Vandenberghe M., Abeele F.V., Roudbaraki M., Lepage G., Mauroy B., Romanin C., Shuba Y., Skryma R., Prevarskaya N. Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells. Cell Death Dis. 2010, 1:e75.
23. 2+ entry, regulates recruitment of protein kinase C (PKC) beta2, and prevents death-inducing signaling complex formation. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:19072-19077.
24. Liu H., Hughes J.D., Rollins S., Chen B., Perkins E. Calcium entry via ORAI1 regulates glioblastoma cell proliferation and apoptosis. Exp. Mol. Pathol. 2011, 91:753-760.
25. Malleter M., Tauzin S., Bessede A., Castellano R., Goubard A., Godey F., Leveque J., Jezequel P., Campion L., Campone M., Ducret T., MacGrogan G., Debure L., Collette Y., Vacher P., Legembre P. CD95L cell surface cleavage triggers a prometastatic signaling pathway in triple-negative breast cancer. Cancer Res. 2013, 73:6711-6721.
26. Motiani R.K., Hyzinski-Garcia M.C., Zhang X., Henkel M.M., Abdullaev I.F., Kuo Y.H., Matrougui K., Mongin A.A., Trebak M. STIM1 and Orai1 mediate CRAC channel activity and are essential for human glioblastoma invasion. Pflugers Arch. 2013, 465:1249-1260.
27. Prevarskaya N., Skryma R., Shuba Y. Calcium in tumour metastasis: new roles for known actors. Nat. Rev. Cancer 2011, 11:609-618.
28. Putney J.W. The physiological function of store-operated calcium entry. Neurochem. Res. 2011, 36:1157-1165.
29. Yang S., Zhang J.J., Huang X.Y. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 2009, 15:124-134.
30. Henke N., Albrecht P., Bouchachia I., Ryazantseva M., Knoll K., Lewerenz J., Kaznacheyeva E., Maher P., Methner A. The plasma membrane channel ORAI1 mediates detrimental calcium influx caused by endogenous oxidative stress. Cell Death Dis. 2013, 4:e470.
31. Li W., Zhang M., Xu L., Lin D., Cai S., Zou F. The apoptosis of non-small cell lung cancer induced by cisplatin through modulation of STIM1. Exp. Toxicol. Pathol. 2013, 65:1073-1081.
32. Rao W., Zhang L., Su N., Wang K., Hui H., Wang L., Chen T., Luo P., Yang Y.F., Liu Z.B., Fei Z. Blockade of SOCE protects HT22 cells from hydrogen peroxide-induced apoptosis. Biochem. Biophys. Res. Commun. 2013, 441:351-356.
33. Limnander A., Depeille P., Freedman T.S., Liou J., Leitges M., Kurosaki T., Roose J.P., Weiss A. STIM1, PKC-delta and RasGRP set a threshold for proapoptotic Erk signaling during B cell development. Nat. Immunol. 2011, 12:425-433.
34. Soltoff S.P., Lannon W.A. Activation of ERK1/2 by store-operated calcium entry in rat parotid acinar cells. PLoS One 2013, 8:e72881.
35. Lang F., Eylenstein A., Shumilina E. Regulation of Orai1/STIM1 by the kinases SGK1 and AMPK. Cell Calcium 2012, 52:347-354.
36. 2+ entry and affect cellular functions. J. Biol. Chem. 2012, 287:2719-2730.
37. Vanoverberghe K., Lehen'kyi V., Thebault S., Raphael M., Vanden Abeele F., Slomianny C., Mariot P., Prevarskaya N. Cytoskeleton reorganization as an alternative mechanism of store-operated calcium entry control in neuroendocrine-differentiated cells. PLoS One 2012, 7:e45615.
38. Feng M., Grice D.M., Faddy H.M., Nguyen N., Leitch S., Wang Y., Muend S., Kenny P.A., Sukumar S., Roberts-Thomson S.J., Monteith G.R., Rao R. Store-independent activation of Orai1 by SPCA2 in mammary tumors. Cell 2010, 143:84-98.
39. Soboloff J., Madesh M., Gill D.L. Sensing cellular stress through STIM proteins. Nat. Chem. Biol. 2011, 7:488-492.
40. Yuan J.P., Zeng W., Huang G.N., Worley P.F., Muallem S. STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat. Cell Biol. 2007, 9:636-645.
41. Park C.Y., Shcheglovitov A., Dolmetsch R. The CRAC channel activator STIM1 binds and inhibits l-type voltage-gated calcium channels. Science 2010, 330:101-105.