The calcium-signaling toolkit: Updates needed

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 6, 2016, Pages 1337-1343

  Dubois, Charlotte ^a,b   Prevarskaya, Natalia ^a,b   Vanden Abeele, Fabien ^a,b  

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

^b Laboratory of Excellence in Ion Channel Science and Therapeutics   (France)

Author keywords

Apoptosis; Autophagy; Calcium; Inhibitor; SERCA; Unfold Protein Response

Indexed keywords

CALCIUM; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CALCIUM CELL LEVEL; CALCIUM DEPLETION; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL FATE; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; MITOCHONDRION; MOLECULAR INTERACTION; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; UNFOLDED PROTEIN RESPONSE; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PHYSIOLOGY;

ANIMALS; APOPTOSIS; AUTOPHAGY; CALCIUM; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; HUMANS; MODELS, BIOLOGICAL; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; UNFOLDED PROTEIN RESPONSE;

EID: 84949883453     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.11.033     Document Type: Article

References (79)

1. Galluzzi L., Vitale I., Abrams J.M., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., Dawson T.M., Dawson V.L., El-Deiry W.S., Fulda S., Gottlieb E., Green D.R., Hengartner M.O., Kepp O., Knight R.A., Kumar S., Lipton S.A., Lu X., Madeo F., Malorni W., et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012, 19:107-120.
2. Galluzzi L., Bravo-San Pedro J.M., Vitale I., Aaronson S.A., Abrams J.M., Adam D., Alnemri E.S., Altucci L., Andrews D., Annicchiarico-Petruzzelli M., Baehrecke E.H., Bazan N.G., Bertrand M.J., Bianchi K., Blagosklonny M.V., Blomgren K., Borner C., Bredesen D.E., Brenner C., Campanella M., et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 2014.
3. Orrenius S., Zhivotovsky B., Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 2003, 4:552-565.
4. 2+ signaling, mitochondria and cell death. Curr. Mol. Med. 2008, 8:119-130.
5. Bonora M., Bononi A., De Marchi E., Giorgi C., Lebiedzinska M., Marchi S., Patergnani S., Rimessi A., Suski J.M., Wojtala A., Wieckowski M.R., 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.
6. Giorgio V., von Stockum S., Antoniel M., Fabbro A., Fogolari F., Forte M., Glick G.D., Petronilli V., Zoratti M., Szabó I., Lippe G., Bernardi P. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:5887-5892.
7. Forte M., Bernardi P. The permeability transition and BCL-2 family proteins in apoptosis: co-conspirators or independent agents?. Cell Death Differ. 2006, 13:1287-1290.
8. Dubois C., Vanden Abeele F., yacheslav Lehen'kyi V.'., Gkika D., Guarmit B., Lepage G., Slomianny C., Borowiec A.S., 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.
9. Faouzi M., Hague F., Potier M., Ahidouch A., Sevestre H., Ouadid-Ahidouch H. Down-regulation of Orai3 arrests cell-cycle progression and induces apoptosis in breast cancer cells but not in normal breast epithelial cells. J. Cell. Physiol. 2011, 226:542-551.
10. Motiani R.K., Abdullaev I.F., Trebak M. A novel native store-operated calcium channel encoded by Orai3: selective requirement of Orai3 versus Orai1 in estrogen receptor-positive versus estrogen receptor-negative breast cancer cells. J. Biol. Chem. 2010, 285:19173-19183.
11. Berna-Erro A., Galan C., Dionisio N., Gomez L.J., Salido G.M., Rosado J.A. Capacitative and non-capacitative signaling complexes in human platelets. Biochim. Biophys. Acta 2012, 1823:1242-1251.
12. X. Yang, H. Jin, X. Cai, S. Li, Y. Shen, Structural and Mechanistic Insights Into the Activation of Stromal Interaction Molecule 1 (STIM1), (n.d.).
13. Vanden Abeele F., Skryma R., Shuba Y., Van Coppenolle F., Slomianny C., Roudbaraki M., Mauroy B., Wuytack F., Prevarskaya N. Bcl-2-dependent modulation of Ca(2+) homeostasis and store-operated channels in prostate cancer cells. Cancer Cell 2002, 1:169-179.
14. Flourakis M., Lehen'kyi V., Beck B., Raphaël 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.
15. 2+ current in human prostate cancer LNCaP cells: involvement in apoptosis. J. Physiol. 2000, 527:71-83.
16. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999, 284:339-343.
17. Shou Y., Li L., Prabhakaran K., Borowitz J.L., Isom G.E. Calcineurin-mediated BAD translocation regulates cyanide-induced neuronal apoptosis. Biochem. J. 2004, 379:805-813.
18. Robertson J.D., Orrenius S., Zhivotovsky B. Review: nuclear events in apoptosis. J. Struct. Biol. 2000, 129:346-358.
19. Altznauer F., Conus S., Cavalli A., Folkers G., Simon H.-U. Calpain-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. J. Biol. Chem. 2004, 279:5947-5957.
20. Zong W.-X., Li C., Hatzivassiliou G., Lindsten T., Yu Q.-C., Yuan J., Thompson C.B. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 2003, 162:59-69.
21. Weber H., Müller L., Jonas L., Schult C., Sparmann G., Schuff-Werner P. Calpain mediates caspase-dependent apoptosis initiated by hydrogen peroxide in pancreatic acinar AR42J cells. Free Radic. Res. 2013, 47:432-446.
22. 2+-ATPase 2. Cell Death Dis. 2014, 5:e1581.
23. 2+ signaling and apoptosis by the BH4 domain of Bcl-2 versus Bcl-Xl. Cell Death Differ. 2012, 19:295-309.
24. Rong Y.-P., Bultynck G., Aromolaran A.S., Zhong F., Parys J.B., De Smedt H., Mignery G.A., Roderick H.L., Bootman M.D., Distelhorst C.W. The BH4 domain of Bcl-2 inhibits ER calcium release and apoptosis by binding the regulatory and coupling domain of the IP3 receptor. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14397-14402.
25. Wang M., Kaufman R.J. The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat. Rev. Cancer 2014, 14:581-597.
26. Schwarze S.R., Lin E.W., Christian P.A., Gayheart D.T., Kyprianou N. Intracellular death platform steps-in: targeting prostate tumors via endoplasmic reticulum (ER) apoptosis. Prostate 2008, 68:1615-1623.
27. Oyadomari S., Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004, 11:381-389.
28. Tabas I., Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 2011, 13:184-190.
29. Yoneda T., Imaizumi K., Oono K., Yui D., Gomi F., Katayama T., Tohyama M. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem. 2001, 276:13935-13940.
30. Nakagawa T., Yuan J. Cross-talk between two cysteine protease families activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 2000, 150:887-894.
31. Martinez J.A., Zhang Z., Svetlov S.I., Hayes R.L., Wang K.K., Larner S.F. Calpain and caspase processing of caspase-12 contribute to the ER stress-induced cell death pathway in differentiated PC12 cells. Apoptosis 2010, 15:1480-1493.
32. Clarke H.J., Chambers J.E., Liniker E., Marciniak S.J. Endoplasmic reticulum stress in malignancy. Cancer Cell 2014, 25:563-573.
33. Nagelkerke A., Bussink J., Sweep F.C.G.J., Span P.N. The unfolded protein response as a target for cancer therapy. Biochim Biophys Acta 2014, 1846:277-284.
34. Chen X., Iliopoulos D., Zhang Q., Tang Q., Greenblatt M.B., Hatziapostolou M., Lim E., Tam W.L., Ni M., Chen Y., Mai J., Shen H., Hu D.Z., Adoro S., Hu B., Song M., Tan C., Landis M.D., Ferrari M., Shin S.J., et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1α pathway. Nature 2014, 508:103-107.
35. Dubois C., Vanden Abeele F., Sehgal P., Olesen C., Junker S., Christensen S.B., Prevarskaya N., Møller J.V. Differential effects of thapsigargin analogues on apoptosis of prostate cancer cells: complex regulation by intracellular calcium. FEBS J. 2013, 280:5430-5440.
36. 2+ transfer to mitochondria. Cell 2010, 142:270-283.
37. Høyer-Hansen M., Jäättelä M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 2007, 14:1576-1582.
38. Mariño G., Niso-Santano M., Baehrecke E.H., Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2014, 15:81-94.
39. Gordon P.B., Holen I., Fosse M., Røtnes J.S., Seglen P.O. Dependence of hepatocytic autophagy on intracellularly sequestered calcium. J. Biol. Chem. 1993, 268:26107-26112.
40. 2+ in autophagy regulation. Cell Calcium 2011, 50:242-250.
41. Cárdenas C., Foskett J.K. Mitochondrial Ca(2+) signals in autophagy. Cell Calcium 2012, 52:44-51.
42. 2+-release channel in autophagy. Cell Commun. Signal. 2012, 10:17.
43. Gao W., Ding W.-X., Stolz D.B., Yin X.-M. Induction of macroautophagy by exogenously introduced calcium. Autophagy 2008, 4:754-761.
44. Chen X., Li M., Chen D., Gao W., Guan J.-L., Komatsu M., Yin X.-M. Autophagy induced by calcium phosphate precipitates involves endoplasmic reticulum membranes in autophagosome biogenesis. PLoS One 2012, 7.
45. Zalckvar E., Berissi H., Eisenstein M., Kimchi A. Phosphorylation of Beclin 1 by DAP-kinase promotes autophagy by weakening its interactions with Bcl-2 and Bcl-XL. Autophagy 2009, 5:720-722.
46. Zalckvar E., Berissi H., Mizrachy L., Idelchuk Y., Koren I., Eisenstein M., Sabanay H., Pinkas-Kramarski R., Kimchi A. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep. 2009, 10:285-292.
47. Khan M.T., Joseph S.K. Role of inositol trisphosphate receptors in autophagy in DT40 cells. J. Biol. Chem. 2010, 285:16912-16920.
48. Medina D.L., Di Paola S., Peluso I., Armani A., De Stefani D., Venditti R., Montefusco S., Scotto-Rosato A., Prezioso C., Forrester A., Settembre C., Wang W., Gao Q., Xu H., Sandri M., Rizzuto R., De Matteis M.A., Ballabio A. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat. Cell Biol. 2015, 17:288-299.
49. Sardiello M., Palmieri M., di Ronza A., Medina D.L., Valenza M., Gennarino V.A., Malta C.D., Donaudy F., Embrione V., Polishchuk R.S., Banfi S., Parenti G., Cattaneo E., Ballabio A. A gene network regulating lysosomal biogenesis and function. Science 2009, 325:473-477.
50. Settembre C., Di Malta C., Polito V.A., Garcia Arencibia M., Vetrini F., Erdin S., Erdin S.U., Huynh T., Medina D., Colella P., Sardiello M., Rubinsztein D.C., Ballabio A. TFEB links autophagy to lysosomal biogenesis. Science 2011, 332:1429-1433.
51. Kondratskyi A., Yassine M., Kondratska K., Skryma R., Slomianny C., Prevarskaya N. Calcium-permeable ion channels in control of autophagy and cancer. Front. Physiol. 2013, 4:272.
52. Ganley I.G., Wong P.-M., Jiang X. Thapsigargin distinguishes membrane fusion in the late stages of endocytosis and autophagy. Autophagy 2011, 7:1397-1399.
53. Engedal N., Torgersen M.L., Guldvik I.J., Barfeld S.J., Bakula D., Sætre F., Hagen L.K., Patterson J.B., Proikas-Cezanne T., Seglen P.O., Simonsen A., Mills I.G. Modulation of intracellular calcium homeostasis blocks autophagosome formation. Autophagy 2013, 9:1475-1490.
54. Ganley I.G., Wong P.-M., Gammoh N., Jiang X. Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol. Cell 2011, 42:731-743.
55. Saetre F., Hagen L.K., Engedal N., Seglen P.O. Novel steps in the autophagic-lysosomal pathway. FEBS J. 2015, 282:2202-2214.
56. 2+ pump inhibitors. Biochem. Soc. Trans. 2011, 39:789-797.
57. Ali H., Christensen S.B., Foreman J.C., Pearce F.L., Piotrowski W., Thastrup O. The ability of thapsigargin and thapsigargicin to activate cells involved in the inflammatory response. Br. J. Pharmacol. 1985, 85:705-712.
58. 2(+)-ATPase. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:2466-2470.
59. 2+ pump isoforms 1, 2, and 3 to thapsigargin and other inhibitors. J. Biol. Chem. 2006, 281:6970-6976.
60. 2+,Mg(2+)-ATPase. FEBS Lett. 1992, 304:109-113.
61. Denmeade S.R., Mhaka A.M., Rosen D.M., Brennen W.N., Dalrymple S., Dach I., Olesen C., Gurel B., Demarzo A.M., Wilding G., Carducci M.A., Dionne C.A., Møller J.V., Nissen P., Christensen S.B., Isaacs J.T. Engineering a prostate-specific membrane antigen-activated tumor endothelial cell prodrug for cancer therapy. Sci. Transl. Med. 2012, 4:140ra86.
62. Hammadi M., Oulidi A., Gackière F., Katsogiannou M., Slomianny C., Roudbaraki M., Dewailly E., Delcourt P., Lepage G., Lotteau S., Ducreux S., Prevarskaya N., Van Coppenolle F. Modulation of ER stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: involvement of GRP78. FASEB J. 2013, 27:1600-1609.
63. Ilagan M.X.G., Kopan R. Selective blockade of transport via SERCA inhibition: the answer for oncogenic forms of notch?. Cancer Cell 2013, 23:267-269.
64. Lu C.-N., Yuan Z.-G., Zhang X.-L., Yan R., Zhao Y.-Q., Liao M., Chen J.-X. Saikosaponin a and its epimer saikosaponin d exhibit anti-inflammatory activity by suppressing activation of NF-κB signaling pathway. Int. Immunopharmacol. 2012, 14:121-126.
65. Wong V.K.W., Li T., Law B.Y.K., Ma E.D.L., Yip N.C., Michelangeli F., Law C.K.M., Zhang M.M., Lam K.Y.C., Chan P.L., Liu L. Saikosaponin-d, a novel SERCA inhibitor, induces autophagic cell death in apoptosis-defective cells. Cell Death Dis. 2013, 4:e720.
66. Hermanson D., Addo S.N., Bajer A.A., Marchant J.S., Das S.G.K., Srinivasan B., Al-Mousa F., Michelangeli F., Thomas D.D., LeBien T.W., Xing C. Dual mechanisms of sHA 14-1 in inducing cell death through endoplasmic reticulum and mitochondria. Mol. Pharmacol. 2009, 76:667-678.
67. Das S.G., Hermanson D.L., Bleeker N., Lowman X., Li Y., Kelekar A., Xing C. Ethyl 2-amino-6-(3,5-dimethoxyphenyl)-4-(2-ethoxy-2-oxoethyl)-4H-chromene-3-carboxylate (CXL017) - a novel scaffold that re-sensitizes multidrug resistant leukemia cells to chemotherapy. ACS Chem. Biol. 2013, 8:327-335.
68. Das S.G., Srinivasan B., Hermanson D.L., Bleeker N.P., Doshi J.M., Tang R., Beck W.T., Xing C. Structure-activity relationship and molecular mechanisms of ethyl 2-amino-6-(3,5-dimethoxyphenyl)-4-(2-ethoxy-2-oxoethyl)-4H-chromene-3-carboxylate (CXL017) and its analogues. J. Med. Chem. 2011, 54:5937-5948.
69. Bleeker N.P., Cornea R.L., Thomas D.D., Xing C. A novel SERCA inhibitor demonstrates synergy with classic SERCA inhibitors and targets multidrug-resistant AML. Mol. Pharm. 2013, 10:4358-4366.
70. Chang W.-H., Chen C.-H., Lu F.-J. Different effects of baicalein, baicalin and wogonin on mitochondrial function, glutathione content and cell cycle progression in human hepatoma cell lines. Planta Med. 2002, 68:128-132.
71. Wang Z., Jiang C., Chen W., Zhang G., Luo D., Cao Y., Wu J., Ding Y., Liu B. Baicalein induces apoptosis and autophagy via endoplasmic reticulum stress in hepatocellular carcinoma cells. Biomed Res Int. 2014, 2014:732516.
72. Liu A.-J., Wang S.-H., Chen K.-C., Kuei H.-P., Shih Y.-L., Hou S.-Y., Chiu W.-T., Hsiao S.-H., Shih C.-M. Evodiamine, a plant alkaloid, induces calcium/JNK-mediated autophagy and calcium/mitochondria-mediated apoptosis in human glioblastoma cells. Chem. Biol. Interact. 2013, 205:20-28.
73. Law B.Y.K., Wang M., Ma D.-L., Al-Mousa F., Michelangeli F., Cheng S.-H., Ng M.H.L., To K.-F., Mok A.Y.F., Ko R.Y.Y., Lam S.K., Chen F., Che C.-M., Chiu P., Ko B.C.B. Alisol B, a novel inhibitor of the sarcoplasmic/endoplasmic reticulum Ca(2+) ATPase pump, induces autophagy, endoplasmic reticulum stress, and apoptosis. Mol. Cancer Ther. 2010, 9:718-730.
74. Denmeade S.R., Isaacs J.T. The SERCA pump as a therapeutic target: making a "smart bomb" for prostate cancer. Cancer Biol. Ther. 2005, 4:14-22.
75. Denmeade S.R., Jakobsen C.M., Janssen S., Khan S.R., Garrett E.S., Lilja H., Christensen S.B., Isaacs J.T. Prostate-specific antigen-activated thapsigargin prodrug as targeted therapy for prostate cancer. J. Natl. Cancer Inst. 2003, 95:990-1000.
76. Jakobsen C.M., Denmeade S.R., Isaacs J.T., Gady A., Olsen C.E., Christensen S.B. Design, synthesis, and pharmacological evaluation of thapsigargin analogues for targeting apoptosis to prostatic cancer cells. J. Med. Chem. 2001, 44:4696-4703.
77. 2+-ATPase with thapsigargin and thapsigargin analogs. J. Biol. Chem. 2010, 285:28883-28892.
78. N.T.Q. Doan, E.S. Paulsen, P. Sehgal, J.V. Møller, P. Nissen, S.R. Denmeade, J.T. Isaacs, C.A. Dionne, S.B. Christensen, Targeting thapsigargin towards tumors, Steroids, (n.d.).
79. Mahalingam D., Cetnar J., Wilding G., Denmeade S., Sarantopoulos J., Kurman M., Carducci M. Abstract B244: a first-in-human phase 1 clinical study of G-202, a thapsigargin-based prostate-specific membrane antigen (PSMA) activated prodrug, in patients with advanced solid tumors. Mol. Cancer Ther. 2013, 12:B244-B244.