The endoplasmic reticulum mitochondrial calcium cross talk is downregulated in malignant pleural mesothelioma cells and plays a critical role in apoptosis inhibition

Oncotarget

Volumn 6, Issue 27, 2015, Pages 23427-23444

  Patergnani, Simone ^a   Giorgi, Carlotta ^a   Maniero, Stefania ^a   Missiroli, Sonia ^a   Maniscalco, Pio ^a   Bononi, Ilaria ^a   Martini, Fernanda ^a   Cavallesco, Giorgio ^a   Tognon, Mauro ^a   Pinton, Paolo ^a  

^a UNIVERSITY OF FERRARA   (Italy)

Author keywords

Apoptosis; Calcium; Mesothelioma; Mitochondria; Therapy

Indexed keywords

AEQUORIN; CALCIUM; ANTINEOPLASTIC AGENT; REACTIVE OXYGEN METABOLITE;

ADULT; APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CANCER CELL CULTURE; CANCER GROWTH; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; MESOTHELIOMA CELL LINE; MITOCHONDRION; PLEURA MESOTHELIOMA; REGULATORY MECHANISM; BIOPSY; CHEMISTRY; CYTOPLASM; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; LUNG NEOPLASMS; MESOTHELIOMA; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; PLEURAL NEOPLASMS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADULT; AEQUORIN; ANTINEOPLASTIC AGENTS; APOPTOSIS; BIOPSY; CALCIUM; CALCIUM SIGNALING; CELL LINE, TUMOR; CYTOPLASM; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MESOTHELIOMA; MITOCHONDRIA; PLEURAL NEOPLASMS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84943419628     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4370     Document Type: Article

References (56)

1. Robinson BW, Musk AW, Lake RA. Malignant mesothelioma. Lancet. 2005;366:397-408.
2. Yang H, Testa JR, Carbone M. Mesothelioma epidemiology, carcinogenesis, and pathogenesis. Curr Treat Options Oncol. 2008;9:147-157.
3. Carbone M, Yang H. Molecular pathways:targeting mechanisms of asbestos and erionite carcinogenesis in mesothelioma. Clin Cancer Res. 2012;18:598-604.
4. Fennell DA, Rudd RM. Defective core-apoptosis signalling in diffuse malignant pleural mesothelioma:opportunities for effective drug development. Lancet Oncol. 2004; 5:354-362.
5. de Assis LV, Locatelli J, Isoldi MC. The role of key genes and pathways involved in the tumorigenesis of Malignant Mesothelioma. Biochim Biophys Acta. 2014; 1845:232-247.
6. Bonora M, Bononi A, De Marchi E, Giorgi C, Lebiedzinska M, Marchi S, Patergnani S, Rimessi A, Suski JM, Wojtala A, Wieckowski MR, Kroemer G, Galluzzi L, Pinton P. Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition. Cell Cycle. 2013;12:674-683.
7. Akl H, Bultynck G. Altered Ca(2+) signaling in cancer cells:proto-oncogenes and tumor suppressors targeting IP3 receptors. Biochim Biophys Acta. 2013; 1835:180-193.
8. Monteith GR, Davis FM, Roberts-Thomson SJ. Calcium channels and pumps in cancer:changes and consequences. J Biol Chem. 2012;287:31666-31673.
9. Marchi S, Rimessi A, Giorgi C, Baldini C, Ferroni L, Rizzuto R, Pinton P. Akt kinase reducing endoplasmic reticulum Ca2+ release protects cells from Ca2+-dependent apoptotic stimuli. Biochemical and biophysical research communications. 2008;375:501-505.
10. Ivanova H, Vervliet T, Missiaen L, Parys JB, De Smedt H, Bultynck G. Inositol 1,4,5-trisphosphate receptor-isoform diversity in cell death and survival. Biochim Biophys Acta. 2014;1843:2164-2183.
11. Yoon MJ, Lee AR, Jeong SA, Kim YS, Kim JY, Kwon YJ, Choi KS. Release of Ca2+ from the endoplasmic reticulum and its subsequent influx into mitochondria trigger celastrol-induced paraptosis in cancer cells. Oncotarget. 2014; 5:6816-6831.
12. Schmidt S, Liu G, Yang W, Honisch S, Pantelakos S, Stournaras C, Honig A, Lang F. Enhanced Orai1 and STIM1 expression as well as store operated Ca2+ entry in therapy resistant ovary carcinoma cells. Oncotarget. 2014; 5:4799-4810.
13. Patergnani S, Suski JM, Agnoletto C, Bononi A, Bonora M, De Marchi E, Giorgi C, Marchi S, Missiroli S, Poletti F, Rimessi A, Duszynski J, Wieckowski MR, Pinton P. Calcium signaling around Mitochondria Associated Membranes (MAMs). Cell Commun Signal. 2011;9:19.
14. Shin DM, Muallem S. What the mitochondria see. Mol Cell. 2010;39:6-7.
15. 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. Ca(2+) transfer from the ER to mitochondria:when, how and why. Biochim Biophys Acta. 2009;1787:1342-1351.
16. Giorgi C, Baldassari F, Bononi A, Bonora M, De Marchi E, Marchi S, Missiroli S, Patergnani S, Rimessi A, Suski JM, Wieckowski MR, Pinton P. Mitochondrial Ca(2+) and apoptosis. Cell Calcium. 2012;52:36-43.
17. Akl H, Vervloessem T, Kiviluoto S, Bittremieux M, Parys JB, De Smedt H, Bultynck G. A dual role for the anti-apoptotic Bcl-2 protein in cancer:mitochondria versus endoplasmic reticulum. Biochim Biophys Acta. 2014; 1843:2240-2252.
18. Giorgi C, Bonora M, Missiroli S, Poletti F, Ramirez FG, Morciano G, Morganti C, Pandolfi PP, Mammano F, Pinton P. Intravital imaging reveals p53-dependent cancer cell death induced by phototherapy via calcium signaling. Oncotarget. 2015;6:1435-1445.
19. Azimi I, Roberts-Thomson SJ, Monteith GR. Calcium influx pathways in breast cancer:opportunities for pharmacological intervention. Br J Pharmacol. 2014;171:945-960.
20. Dubois C, Vanden Abeele F, Lehen'kyi V, Gkika D, Guarmit B, Lepage G, Slomianny C, Borowiec AS, Bidaux G, Benahmed M, Shuba Y, Prevarskaya N. Remodeling of channel-forming ORAI proteins determines an oncogenic switch in prostate cancer. Cancer Cell. 2014; 26:19-32.
21. Raphael M, Lehen'kyi V, Vandenberghe M, Beck B, Khalimonchyk S, Vanden Abeele F, Farsetti L, Germain E, Bokhobza A, Mihalache A, Gosset P, Romanin C, Clezardin P, Skryma R, Prevarskaya N. TRPV6 calcium channel translocates to the plasma membrane via Orai1-mediated mechanism and controls cancer cell survival. Proc Natl Acad Sci U S A. 2014;111:E3870-3879.
22. Weidinger C, Shaw PJ, Feske S. STIM1 and STIM2-mediated Ca(2+) influx regulates antitumour immunity by CD8(+) T cells. EMBO Mol Med. 2013;5:1311-1321.
23. Al-Taweel N, Varghese E, Florea AM, Busselberg D. Cisplatin (CDDP) triggers cell death of MCF-7 cells following disruption of intracellular calcium ([Ca(2+)]i) homeostasis. J Toxicol Sci. 2014;39:765-774.
24. Kamp DW, Liu G, Cheresh P, Kim SJ, Mueller A, Lam AP, Trejo H, Williams D, Tulasiram S, Baker M, Ridge K, Chandel NS, Beri R. Asbestos-induced alveolar epithelial cell apoptosis. The role of endoplasmic reticulum stress response. Am J Respir Cell Mol Biol. 2013;49:892-901.
25. Papp T, Schipper H, Pemsel H, Unverricht M, Muller KM, Wiethege T, Schiffmann D, Rahman Q. Mutational analysis of the PTEN/MMAC1 tumour suppressor gene in primary human malignant mesotheliomas. Oncol Rep. 2001; 8:1375-1379.
26. Ni Z, Liu Y, Keshava N, Zhou G, Whong W, Ong T. Analysis of K-ras and p53 mutations in mesotheliomas from humans and rats exposed to asbestos. Mutat Res. 2000; 468:87-92.
27. Mossman BT, Shukla A, Heintz NH, Verschraegen CF, Thomas A, Hassan R. New insights into understanding the mechanisms, pathogenesis, and management of malignant mesotheliomas. Am J Pathol. 2013;182:1065-1077.
28. Sekido Y. Molecular pathogenesis of malignant mesothelioma. Carcinogenesis. 2013;34:1413-1419.
29. Rimessi A, Marchi S, Patergnani S, Pinton P. H-Ras-driven tumoral maintenance is sustained through caveolin-1-dependent alterations in calcium signaling. Oncogene. 2014; 33:2329-2340.
30. Marchi S, Patergnani S, Pinton P. The endoplasmic reticulum-mitochondria connection:one touch, multiple functions. Biochim Biophys Acta. 2014;1837:461-469.
31. Aung CS, Ye W, Plowman G, Peters AA, Monteith GR, Roberts-Thomson SJ. Plasma membrane calcium ATPase 4 and the remodeling of calcium homeostasis in human colon cancer cells. Carcinogenesis. 2009;30:1962-1969.
32. Bononi A, Bonora M, Marchi S, Missiroli S, Poletti F, Giorgi C, Pandolfi PP, Pinton P. Identification of PTEN at the ER and MAMs and its regulation of Ca(2+) signaling and apoptosis in a protein phosphatase-dependent manner. Cell Death Differ. 2013;20:1631-1643.
33. Giorgi C, Ito K, Lin HK, Santangelo C, Wieckowski MR, Lebiedzinska M, Bononi A, Bonora M, Duszynski J, Bernardi R, Rizzuto R, Tacchetti C, Pinton P, Pandolfi PP. PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science. 2010;330:1247-1251.
34. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev. 2007; 87:99-163.
35. Giorgi C, Romagnoli A, Pinton P, Rizzuto R. Ca2+ signaling, mitochondria and cell death. Curr Mol Med. 2008;8:119-130.
36. Khan MT, Wagner L, 2nd, Yule DI, Bhanumathy C, Joseph SK. Akt kinase phosphorylation of inositol 1,4,5-trisphosphate receptors. J Biol Chem. 2006;281:3731-3737.
37. Marchi S, Marinello M, Bononi A, Bonora M, Giorgi C, Rimessi A, Pinton P. Selective modulation of subtype III IP(3)R by Akt regulates ER Ca(2)(+) release and apoptosis. Cell Death Dis. 2012;3:e304.
38. Amarjargal N, Mazurek B, Haupt H, Andreeva N, Fuchs J, Gross J. Effects of SERCA and PMCA inhibitors on the survival of rat cochlear hair cells during ischemia in vitro. Physiol Res. 2008;57:631-638.
39. Marchi S, Pinton P. The mitochondrial calcium uniporter complex:molecular components, structure and physiopathological implications. J Physiol. 2014;592:829-839.
40. Marchi S, Lupini L, Patergnani S, Rimessi A, Missiroli S, Bonora M, Bononi A, Corra F, Giorgi C, De Marchi E, Poletti F, Gafa R, Lanza G, Negrini M, Rizzuto R, Pinton P. Downregulation of the mitochondrial calcium uniporter by cancer-related miR-25. Curr Biol. 2013;23:58-63.
41. Cioce M, Canino C, Goparaju C, Yang H, Carbone M, Pass HI. Autocrine CSF-1R signaling drives mesothelioma chemoresistance via AKT activation. Cell Death Dis. 2014; 5:e1167.
42. Varani K, Maniero S, Vincenzi F, Targa M, Stefanelli A, Maniscalco P, Martini F, Tognon M, Borea PA. A(3) receptors are overexpressed in pleura from patients with mesothelioma and reduce cell growth via Akt/nuclear factor-kappaB pathway. Am J Respir Crit Care Med. 2011;183:522-530.
43. Braun F, de Carne Trecesson S, Bertin-Ciftci J, Juin P. Protect and serve:Bcl-2 proteins as guardians and rulers of cancer cell survival. Cell Cycle. 2013;12:2937-2947.
44. Pinton P, Ferrari D, Rapizzi E, Di Virgilio F, Pozzan T, Rizzuto R. The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis:significance for the molecular mechanism of Bcl-2 action. EMBO J. 2001;20:2690-2701.
45. Wu Y, Ma Y, Xu Z, Wang D, Zhao B, Pan H, Wang J, Xu D, Zhao X, Pan S, Liu L, Dai W, Jiang H. Sodium orthovanadate inhibits growth of human hepatocellular carcinoma cells in vitro and in an orthotopic model in vivo. Cancer Lett. 2014;351:108-116.
46. Evangelou AM. Vanadium in cancer treatment. Crit Rev Oncol Hematol. 2002;42:249-265.
47. Khan KH, Blanco-Codesido M, Molife LR. Cancer therapeutics:Targeting the apoptotic pathway. Crit Rev Oncol Hematol. 2014;90:200-219.
48. Brevet M, Shimizu S, Bott MJ, Shukla N, Zhou Q, Olshen AB, Rusch V, Ladanyi M. Coactivation of receptor tyrosine kinases in malignant mesothelioma as a rationale for combination targeted therapy. J Thorac Oncol. 2011; 6:864-874.
49. Ou WB, Hubert C, Corson JM, Bueno R, Flynn DL, Sugarbaker DJ, Fletcher JA. Targeted inhibition of multiple receptor tyrosine kinases in mesothelioma. Neoplasia. 2011; 13:12-22.
50. Kruman II, Mattson MP. Pivotal role of mitochondrial calcium uptake in neural cell apoptosis and necrosis. J Neurochem. 1999;72:529-540.
51. Zaid H, Abu-Hamad S, Israelson A, Nathan I, ShoshanBarmatz V. The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death Differ. 2005; 12:751-760.
52. Tsai LM, Yu D. MicroRNAs in common diseases and potential therapeutic applications. Clin Exp Pharmacol Physiol. 2010;37:102-107.
53. Kirschner MB, Cheng YY, Badrian B, Kao SC, Creaney J, Edelman JJ, Armstrong NJ, Vallely MP, Musk AW, Robinson BW, McCaughan BC, Klebe S, Mutsaers SE, van Zandwijk N, Reid G. Increased circulating miR-625-3p: a potential biomarker for patients with malignant pleural mesothelioma. J Thorac Oncol. 2012;7:1184-1191.
54. Balatti V, Maniero S, Ferracin M, Veronese A, Negrini M, Ferrocci G, Martini F, Tognon MG. MicroRNAs dysregulation in human malignant pleural mesothelioma. J Thorac Oncol. 2011;6:844-851.
55. Cristaudo A, Foddis R, Vivaldi A, Buselli R, Gattini V, Guglielmi G, Cosentino F, Ottenga F, Ciancia E, Libener R, Filiberti R, Neri M, Betta P, Tognon M, Mutti L, Puntoni R. SV40 enhances the risk of malignant mesothelioma among people exposed to asbestos:a molecular epidemiologic case-control study. Cancer Res. 2005; 65:3049-3052.
56. Bonora M, Giorgi C, Bononi A, Marchi S, Patergnani S, Rimessi A, Rizzuto R, Pinton P. Subcellular calcium measurements in mammalian cells using jellyfish photoprotein aequorin-based probes. Nat Protoc. 2013; 8:2105-2118.