IP3, a small molecule with a powerful message

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 7, 2013, Pages 1772-1786

  Decrock, Elke ^a   De Bock, Marijke ^a   Wang, Nan ^a   Gadicherla, Ashish K ^a   Bol, Mélissa ^a   Delvaeye, Tinneke ^a,b   Vandenabeele, Peter ^a,b   Vinken, Mathieu ^c   Bultynck, Geert ^d   Krysko, Dmitri V ^a,b   Leybaert, Luc ^a  

^a GHENT UNIVERSITY   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

Author keywords

Calcium; Cell death; Connexin; Gap junction; Inositol 1,4,5 trisphosphate; Intercellular communication

Indexed keywords

CALCIUM ION; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

APOPTOSIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL COMMUNICATION; CELL SURVIVAL; ENDOPLASMIC RETICULUM; HUMAN; INTRACELLULAR SIGNALING; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM SIGNALING; CELL COMMUNICATION; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; SIGNAL TRANSDUCTION;

MLCS; MLOWN;

EID: 84878220788     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.12.016     Document Type: Review

References (288)

1. Zhivotovsky B., Orrenius S. Calcium and cell death mechanisms: a perspective from the cell death community. Cell Calcium 2011, 50:211-221.
2. Sammels E., Parys J.B., Missiaen L., De Smedt H., Bultynck G. Intracellular Ca2+ storage in health and disease: a dynamic equilibrium. Cell Calcium 2010, 47:297-314.
3. Decuypere J.P., Monaco G., Bultynck G., Missiaen L., De Smedt H., Parys J.B. The IP(3) receptor-mitochondria connection in apoptosis and autophagy. Biochim. Biophys. Acta 2011, 1813:1003-1013.
4. Decrock E., Vinken M., De Vuyst E., Krysko D.V., D'Herde K., Vanhaecke T., Vandenabeele P., Rogiers V., Leybaert L. Connexin-related signaling in cell death: to live or let die?. Cell Death Differ. 2009, 16:524-536.
5. Saez J.C., Berthoud V.M., Branes M.C., Martinez A.D., Beyer E.C. Plasma membrane channels formed by connexins: their regulation and functions. Physiol. Rev. 2003, 83:1359-1400.
6. Alexander D.B., Goldberg G.S. Transfer of biologically important molecules between cells through gap junction channels. Curr. Med. Chem. 2003, 10:2045-2058.
7. Sohl G., Willecke K. An update on connexin genes and their nomenclature in mouse and man. Cell Commun. Adhes. 2003, 10:173-180.
8. Wang N., De Bock M., Decrock E., Bol M., Gadicherla A., Vinken M., Rogiers V., Bukauskas F.F., Bultynck G., Leybaert L. Paracrine signaling through plasma membrane hemichannels. Biochim. Biophys. Acta 2012, 1828:35-50.
9. D'Hondt C., Ponsaerts R., De Smedt H., Bultynck G., Himpens B. Pannexins, distant relatives of the connexin family with specific cellular functions?. Bioessays 2009, 31:953-974.
10. Sosinsky G.E., Boassa D., Dermietzel R., Duffy H.S., Laird D.W., MacVicar B., Naus C.C., Penuela S., Scemes E., Spray D.C., Thompson R.J., Zhao H.B., Dahl G. Pannexin channels are not gap junction hemichannels. Channels (Austin) 2011, 5:193-197.
11. Huang Y., Grinspan J.B., Abrams C.K., Scherer S.S. Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia 2007, 55:46-56.
12. Penuela S., Bhalla R., Gong X.Q., Cowan K.N., Celetti S.J., Cowan B.J., Bai D., Shao Q., Laird D.W. Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J. Cell Sci. 2007, 120:3772-3783.
13. Laird D.W. Life cycle of connexins in health and disease. Biochem. J. 2006, 394:527-543.
14. Dobrowolski R., Willecke K. Connexin-caused genetic diseases and corresponding mouse models. Antioxid. Redox Signal. 2009, 11:283-295.
15. Krysko D.V., Leybaert L., Vandenabeele P., D'Herde K. Gap junctions and the propagation of cell survival and cell death signals. Apoptosis 2005, 10:459-469.
16. Rodriguez-Sinovas A., Cabestrero A., Lopez D., Torre I., Morente M., Abellan A., Miro E., Ruiz-Meana M., Garcia-Dorado D. The modulatory effects of connexin 43 on cell death/survival beyond cell coupling. Prog. Biophys. Mol. Biol. 2007, 94:219-232.
17. Decrock E., Krysko D.V., Vinken M., Kaczmarek A., Crispino G., Bol M., Wang N., De Bock M., De Vuyst E., Naus C.C., Rogiers V., Vandenabeele P., Erneux C., Mammano F., Bultynck G., Leybaert L. Transfer of IP(3) through gap junctions is critical, but not sufficient, for the spread of apoptosis. Cell Death Differ. 2012, 19:947-957.
18. Berridge M.J. Inositol trisphosphate and calcium signalling mechanisms. Biochim. Biophys. Acta 2009, 1793:933-940.
19. Vines C.M. Phospholipase C. Adv. Exp. Med. Biol. 2012, 740:235-254.
20. Dupont G., Combettes L., Leybaert L. Calcium dynamics: spatio-temporal organization from the subcellular to the organ level. Int. Rev. Cytol. 2007, 261:193-245.
21. Leybaert L., Sanderson M.J. Intercellular Ca(2+) waves: mechanisms and function. Physiol. Rev. 2012, 92:1359-1392.
22. Case R.M., Eisner D., Gurney A., Jones O., Muallem S., Verkhratsky A. Evolution of calcium homeostasis: from birth of the first cell to an omnipresent signalling system. Cell Calcium 2007, 42:345-350.
23. Iino M. Spatiotemporal dynamics of Ca2+ signaling and its physiological roles. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2010, 86:244-256.
24. Prank K., Gabbiani F., Brabant G. Coding efficiency and information rates in transmembrane signaling. Biosystems 2000, 55:15-22.
25. Boitano S., Dirksen E.R., Sanderson M.J. Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science 1992, 258:292-295.
26. Churchill G.C., Louis C.F. Roles of Ca2+, inositol trisphosphate and cyclic ADP-ribose in mediating intercellular Ca2+ signaling in sheep lens cells. J. Cell Sci. 1998, 111(Pt 9):1217-1225.
27. Allbritton N.L., Meyer T., Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 1992, 258:1812-1815.
28. Hofer T., Venance L., Giaume C. Control and plasticity of intercellular calcium waves in astrocytes: a modeling approach. J. Neurosci. 2002, 22:4850-4859.
29. Arcuino G., Lin J.H., Takano T., Liu C., Jiang L., Gao Q., Kang J., Nedergaard M. Intercellular calcium signaling mediated by point-source burst release of ATP. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:9840-9845.
30. Stout C.E., Costantin J.L., Naus C.C., Charles A.C. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem. 2002, 277:10482-10488.
31. Hoogland T.M., Kuhn B., Gobel W., Huang W., Nakai J., Helmchen F., Flint J., Wang S.S. Radially expanding transglial calcium waves in the intact cerebellum. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3496-3501.
32. Scemes E., Suadicani S.O., Spray D.C. Intercellular communication in spinal cord astrocytes: fine tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation. J. Neurosci. 2000, 20:1435-1445.
33. Hassinger T.D., Guthrie P.B., Atkinson P.B., Bennett M.V., Kater S.B. An extracellular signaling component in propagation of astrocytic calcium waves. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:13268-13273.
34. Montana V., Malarkey E.B., Verderio C., Matteoli M., Parpura V. Vesicular transmitter release from astrocytes. Glia 2006, 54:700-715.
35. Gomes P., Srinivas S.P., Van Driessche W., Vereecke J., Himpens B. ATP release through connexin hemichannels in corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 2005, 46:1208-1218.
36. Braet K., Vandamme W., Martin P.E., Evans W.H., Leybaert L. Photoliberating inositol-1,4,5-trisphosphate triggers ATP release that is blocked by the connexin mimetic peptide gap 26. Cell Calcium 2003, 33:37-48.
37. Locovei S., Wang J., Dahl G. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 2006, 580:239-244.
38. Suadicani S.O., Iglesias R., Spray D.C., Scemes E. Point mutation in the mouse P2X7 receptor affects intercellular calcium waves in astrocytes. ASN Neuro 2009, 1.
39. Pellegatti P., Falzoni S., Pinton P., Rizzuto R., Di Virgilio F. A novel recombinant plasma membrane-targeted luciferase reveals a new pathway for ATP secretion. Mol. Biol. Cell 2005, 16:3659-3665.
40. Woehrle T., Yip L., Elkhal A., Sumi Y., Chen Y., Yao Y., Insel P.A., Junger W.G. Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 2010, 116:3475-3484.
41. Burnstock G. Purinergic signalling: its unpopular beginning, its acceptance and its exciting future. Bioessays 2012, 34:218-225.
42. Paemeleire K., Martin P.E., Coleman S.L., Fogarty K.E., Carrington W.A., Leybaert L., Tuft R.A., Evans W.H., Sanderson M.J. Intercellular calcium waves in HeLa cells expressing GFP-labeled connexin 43, 32, or 26. Mol. Biol. Cell 2000, 11:1815-1827.
43. Braet K., Paemeleire K., D'Herde K., Sanderson M.J., Leybaert L. Astrocyte-endothelial cell calcium signals conveyed by two signalling pathways. Eur. J. Neurosci. 2001, 13:79-91.
44. De Vuyst E., Wang N., Decrock E., De Bock M., Vinken M., Van Moorhem M., Lai C., Culot M., Rogiers V., Cecchelli R., Naus C.C., Evans W.H., Leybaert L. Ca(2+) regulation of connexin 43 hemichannels in C6 glioma and glial cells. Cell Calcium 2009, 46:176-187.
45. Clair C., Chalumeau C., Tordjmann T., Poggioli J., Erneux C., Dupont G., Combettes L. Investigation of the roles of Ca(2+) and InsP(3) diffusion in the coordination of Ca(2+) signals between connected hepatocytes. J. Cell Sci. 2001, 114:1999-2007.
46. De Bock M., Culot M., Wang N., da Costa A., Decrock E., Bol M., Bultynck G., Cecchelli R., Leybaert L. Low extracellular Ca(2+) conditions induce an increase in brain endothelial permeability that involves intercellular Ca(2+) waves. Brain Res. 2012, 1487:78-87.
47. Robb-Gaspers L.D., Thomas A.P. Coordination of Ca2+ signaling by intercellular propagation of Ca2+ waves in the intact liver. J. Biol. Chem. 1995, 270:8102-8107.
48. Parthasarathi K., Ichimura H., Monma E., Lindert J., Quadri S., Issekutz A., Bhattacharya J. Connexin 43 mediates spread of Ca2+-dependent proinflammatory responses in lung capillaries. J. Clin. Invest. 2006, 116:2193-2200.
49. Schipke C.G., Boucsein C., Ohlemeyer C., Kirchhoff F., Kettenmann H. Astrocyte Ca2+ waves trigger responses in microglial cells in brain slices. FASEB J. 2002, 16:255-257.
50. Hirase H., Qian L., Bartho P., Buzsaki G. Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol. 2004, 2:E96.
51. Sauer H., Sharifpanah F., Hatry M., Steffen P., Bartsch C., Heller R., Padmasekar M., Howaldt H.P., Bein G., Wartenberg M. NOS inhibition synchronizes calcium oscillations in human adipose tissue-derived mesenchymal stem cells by increasing gap-junctional coupling. J. Cell. Physiol. 2011, 226:1642-1650.
52. Stauffer P.L., Zhao H., Luby-Phelps K., Moss R.L., Star R.A., Muallem S. Gap junction communication modulates [Ca2+]i oscillations and enzyme secretion in pancreatic acini. J. Biol. Chem. 1993, 268:19769-19775.
53. Fanchaouy M., Serir K., Meister J.J., Beny J.L., Bychkov R. Intercellular communication: role of gap junctions in establishing the pattern of ATP-elicited Ca2+ oscillations and Ca2+-dependent currents in freshly isolated aortic smooth muscle cells. Cell Calcium 2005, 37:25-34.
54. Verma V., Hallett M.B., Leybaert L., Martin P.E., Evans W.H. Perturbing plasma membrane hemichannels attenuates calcium signalling in cardiac cells and HeLa cells expressing connexins. Eur. J. Cell Biol. 2009, 88:79-90.
55. De Bock M., Culot M., Wang N., Bol M., Decrock E., De Vuyst E., da Costa A., Dauwe I., Vinken M., Simon A.M., Rogiers V., De Ley G., Evans W.H., Bultynck G., Dupont G., Cecchelli R., Leybaert L. Connexin channels provide a target to manipulate brain endothelial calcium dynamics and blood-brain barrier permeability. J. Cereb. Blood Flow Metab. 2011, 31:1942-1957.
56. Verderio C., Bruzzone S., Zocchi E., Fedele E., Schenk U., De Flora A., Matteoli M. Evidence of a role for cyclic ADP-ribose in calcium signalling and neurotransmitter release in cultured astrocytes. J. Neurochem. 2001, 78:646-657.
57. Foskett J.K., White C., Cheung K.H., Mak D.O. Inositol trisphosphate receptor Ca2+ release channels. Physiol. Rev. 2007, 87:593-658.
58. Parys J.B., De Smedt H. Inositol 1,4,5-trisphosphate and its receptors. Adv. Exp. Med. Biol. 2012, 740:255-279.
59. Iwai M., Michikawa T., Bosanac I., Ikura M., Mikoshiba K. Molecular basis of the isoform-specific ligand-binding affinity of inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 2007, 282:12755-12764.
60. Bezprozvanny I., Watras J., Ehrlich B.E. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 1991, 351:751-754.
61. Tu H., Wang Z., Bezprozvanny I. Modulation of mammalian inositol 1,4,5-trisphosphate receptor isoforms by calcium: a role of calcium sensor region. Biophys. J. 2005, 88:1056-1069.
62. Mak D.O., McBride S.M., Petrenko N.B., Foskett J.K. Novel regulation of calcium inhibition of the inositol 1,4,5-trisphosphate receptor calcium-release channel. J. Gen. Physiol. 2003, 122:569-581.
63. Marchenko S.M., Yarotskyy V.V., Kovalenko T.N., Kostyuk P.G., Thomas R.C. Spontaneously active and InsP3-activated ion channels in cell nuclei from rat cerebellar Purkinje and granule neurones. J. Physiol. 2005, 565:897-910.
64. Shinohara T., Michikawa T., Enomoto M., Goto J., Iwai M., Matsu-ura T., Yamazaki H., Miyamoto A., Suzuki A., Mikoshiba K. Mechanistic basis of bell-shaped dependence of inositol 1,4,5-trisphosphate receptor gating on cytosolic calcium. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:15486-15491.
65. Foskett J.K., Mak D.O. Novel model of calcium and inositol 1,4,5-trisphosphate regulation of InsP3 receptor channel gating in native endoplasmic reticulum. Biol. Res. 2004, 37:513-519.
66. Diambra L., Marchant J.S. Inositol (1,4,5)-trisphosphate receptor microarchitecture shapes Ca2+ puff kinetics. Biophys. J. 2011, 100:822-831.
67. Vermassen E., Parys J.B., Mauger J.P. Subcellular distribution of the inositol 1,4,5-trisphosphate receptors: functional relevance and molecular determinants. Biol. Cell 2004, 96:3-17.
68. Tinel H., Cancela J.M., Mogami H., Gerasimenko J.V., Gerasimenko O.V., Tepikin A.V., Petersen O.H. Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca(2+) signals. EMBO J. 1999, 18:4999-5008.
69. Pizzo P., Drago I., Filadi R., Pozzan T. Mitochondrial Ca(2)(+) homeostasis: mechanism, role, and tissue specificities. Pflugers Arch. 2012, 464:3-17.
70. Shoshan-Barmatz V., De Pinto V., Zweckstetter M., Raviv Z., Keinan N., Arbel N. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol. Aspects Med. 2010, 31:227-285.
71. De Stefani D., Raffaello A., Teardo E., Szabo I., Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011, 476:336-340.
72. Baughman J.M., Perocchi F., Girgis H.S., Plovanich M., Belcher-Timme C.A., Sancak Y., Bao X.R., Strittmatter L., Goldberger O., Bogorad R.L., Koteliansky V., Mootha V.K. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011, 476:341-345.
73. Rizzuto R., Brini M., Murgia M., Pozzan T. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 1993, 262:744-747.
74. 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.
75. Bononi A., Missiroli S., Poletti F., Suski J.M., Agnoletto C., Bonora M., De Marchi E., Giorgi C., Marchi S., Patergnani S., Rimessi A., Wieckowski M.R., Pinton P. Mitochondria-associated membranes (MAMs) as hotspot Ca(2+) signaling units. Adv. Exp. Med. Biol. 2012, 740:411-437.
76. Csordas G., Varnai P., Golenar T., Roy S., Purkins G., Schneider T.G., Balla T., Hajnoczky G. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol. Cell 2010, 39:121-132.
77. Csordas G., Thomas A.P., Hajnoczky G. Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J. 1999, 18:96-108.
78. Hayashi T., Rizzuto R., Hajnoczky G., Su T.P. MAM: more than just a housekeeper. Trends Cell Biol. 2009, 19:81-88.
79. Patergnani S., Suski J.M., Agnoletto C., Bononi A., Bonora M., De Marchi E., Giorgi C., Marchi S., Missiroli S., Poletti F., Rimessi A., Duszynski J., Wieckowski M.R., Pinton P. Calcium signaling around Mitochondria Associated Membranes (MAMs). Cell Commun. Signal. 2011, 9:19.
80. Szabadkai G., Bianchi K., Varnai P., De Stefani D., Wieckowski M.R., Cavagna D., Nagy A.I., Balla T., Rizzuto R. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J. Cell Biol. 2006, 175:901-911.
81. Jouaville L.S., Pinton P., Bastianutto C., Rutter G.A., Rizzuto R. Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:13807-13812.
82. Cardenas C., Miller R.A., Smith I., Bui T., Molgo J., Muller M., Vais H., Cheung K.H., Yang J., Parker I., Thompson C.B., Birnbaum M.J., Hallows K.R., Foskett J.K. Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 2010, 142:270-283.
83. Bonora M., Patergnani S., Rimessi A., De Marchi E., Suski J.M., Bononi A., Giorgi C., Marchi S., Missiroli S., Poletti F., Wieckowski M.R., Pinton P. ATP synthesis and storage. Purinergic Signal 2012, 8:343-357.
84. Palty R., Silverman W.F., Hershfinkel M., Caporale T., Sensi S.L., Parnis J., Nolte C., Fishman D., Shoshan-Barmatz V., Herrmann S., Khananshvili D., Sekler I. NCLX is an essential component of mitochondrial Na+/Ca2+ exchange. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:436-441.
85. Palty R., Sekler I. The mitochondrial Na(+)/Ca(2+) exchanger. Cell Calcium 2012, 52:9-15.
86. Villa A., Garcia-Simon M.I., Blanco P., Sese B., Bogonez E., Satrustegui J. Affinity chromatography purification of mitochondrial inner membrane proteins with calcium transport activity. Biochim. Biophys. Acta 1998, 1373:347-359.
87. Decuypere J.P., Bultynck G., Parys J.B. A dual role for Ca(2+) in autophagy regulation. Cell Calcium 2011, 50:242-250.
88. Mussche S., Leybaert L., D'Herde K. First and second messenger role of calcium. Survival versus apoptosis in serum-free cultured granulosa explants. Ann. N. Y. Acad. Sci. 2000, 926:101-115.
89. Fleckenstein A., Janke J., Doring H.J., Leder O. Myocardial fiber necrosis due to intracellular Ca overload-a new principle in cardiac pathophysiology. Recent Adv. Stud. Cardiac Struct. Metab. 1974, 4:563-580.
90. Mekahli D., Bultynck G., Parys J.B., De Smedt H., Missiaen L. Endoplasmic-reticulum calcium depletion and disease. Cold Spring Harb. Perspect. Biol. 2011, 3.
91. Kim I., Xu W., Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 2008, 7:1013-1030.
92. Deegan S., Saveljeva S., Gorman A.M., Samali A. Stress-induced self-cannibalism: on the regulation of autophagy by endoplasmic reticulum stress. Cell. Mol. Life Sci. 2012, (epub ahead of print).
93. Higo T., Hamada K., Hisatsune C., Nukina N., Hashikawa T., Hattori M., Nakamura T., Mikoshiba K. Mechanism of ER stress-induced brain damage by IP(3) receptor. Neuron 2010, 68:865-878.
94. 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.
95. Baumgartner H.K., Gerasimenko J.V., Thorne C., Ferdek P., Pozzan T., Tepikin A.V., Petersen O.H., Sutton R., Watson A.J., Gerasimenko O.V. Calcium elevation in mitochondria is the main Ca2+ requirement for mitochondrial permeability transition pore (mPTP) opening. J. Biol. Chem. 2009, 284:20796-20803.
96. Wertz I.E., Dixit V.M. Characterization of calcium release-activated apoptosis of LNCaP prostate cancer cells. J. Biol. Chem. 2000, 275:11470-11477.
97. 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.
98. Csordas G., Renken C., Varnai P., Walter L., Weaver D., Buttle K.F., Balla T., Mannella C.A., Hajnoczky G. Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 2006, 174:915-921.
99. De Stefani D., Bononi A., Romagnoli A., Messina A., De Pinto V., Pinton P., Rizzuto R. VDAC1 selectively transfers apoptotic Ca2+ signals to mitochondria. Cell Death Differ. 2012, 19:267-273.
100. 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.
101. Jones R.G., Bui T., White C., Madesh M., Krawczyk C.M., Lindsten T., Hawkins B.J., Kubek S., Frauwirth K.A., Wang Y.L., Conway S.J., Roderick H.L., Bootman M.D., Shen H., Foskett J.K., Thompson C.B. The proapoptotic factors Bax and Bak regulate T Cell proliferation through control of endoplasmic reticulum Ca(2+) homeostasis. Immunity 2007, 27:268-280.
102. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
103. Rasola A., Bernardi P. Mitochondrial permeability transition in Ca(2+)-dependent apoptosis and necrosis. Cell Calcium 2011, 50:222-233.
104. Szalai G., Krishnamurthy R., Hajnoczky G. Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J. 1999, 18:6349-6361.
105. Leist M., Single B., Castoldi A.F., Kuhnle S., Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 1997, 185:1481-1486.
106. Petronilli V., Miotto G., Canton M., Brini M., Colonna R., Bernardi P., Di Lisa F. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 1999, 76:725-734.
107. Baines C.P. The molecular composition of the mitochondrial permeability transition pore. J. Mol. Cell. Cardiol. 2009, 46:850-857.
108. Baines C.P., Kaiser R.A., Sheiko T., Craigen W.J., Molkentin J.D. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 2007, 9:550-555.
109. Kokoszka J.E., Waymire K.G., Levy S.E., Sligh J.E., Cai J., Jones D.P., MacGregor G.R., Wallace D.C. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 2004, 427:461-465.
110. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn G.W., Robbins J., Molkentin J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434:658-662.
111. Roy S.S., Ehrlich A.M., Craigen W.J., Hajnoczky G. VDAC2 is required for truncated BID-induced mitochondrial apoptosis by recruiting BAK to the mitochondria. EMBO Rep. 2009, 10:1341-1347.
112. Chipuk J.E., Green D.R. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization?. Trends Cell Biol. 2008, 18:157-164.
113. Tait S.W., Green D.R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Cancer 2010, 11:621-632.
114. Yu J., Qian H., Li Y., Wang Y., Zhang X., Liang X., Fu M., Lin C. Therapeutic effect of arsenic trioxide (As2O3) on cervical cancer in vitro and in vivo through apoptosis induction. Cancer Biol. Ther. 2007, 6:580-586.
115. Rostovtseva T.K., Antonsson B., Suzuki M., Youle R.J., Colombini M., Bezrukov S.M. Bid, but not Bax, regulates VDAC channels. J. Biol. Chem. 2004, 279:13575-13583.
116. Sugiyama T., Shimizu S., Matsuoka Y., Yoneda Y., Tsujimoto Y. Activation of mitochondrial voltage-dependent anion channel by apro-apoptotic BH3-only protein Bim. Oncogene 2002, 21:4944-4956.
117. Shimizu S., Shinohara Y., Tsujimoto Y. Bax and Bcl-xL independently regulate apoptotic changes of yeast mitochondria that require VDAC but not adenine nucleotide translocator. Oncogene 2000, 19:4309-4318.
118. Zheng Y., Shi Y., Tian C., Jiang C., Jin H., Chen J., Almasan A., Tang H., Chen Q. Essential role of the voltage-dependent anion channel (VDAC) in mitochondrial permeability transition pore opening and cytochrome c release induced by arsenic trioxide. Oncogene 2004, 23:1239-1247.
119. Banerjee J., Ghosh S. Bax increases the pore size of rat brain mitochondrial voltage-dependent anion channel in the presence of tBid. Biochem. Biophys. Res. Commun. 2004, 323:310-314.
120. Arbel N., Shoshan-Barmatz V. Voltage-dependent anion channel 1-based peptides interact with Bcl-2 to prevent antiapoptotic activity. J. Biol. Chem. 2010, 285:6053-6062.
121. Arbel N., Ben-Hail D., Shoshan-Barmatz V. Mediation of the antiapoptotic activity of Bcl-xL protein upon interaction with VDAC1 protein. J. Biol. Chem. 2012, 287:23152-23161.
122. Zalk R., Israelson A., Garty E.S., Azoulay-Zohar H., Shoshan-Barmatz V. Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria. Biochem. J. 2005, 386:73-83.
123. Keinan N., Tyomkin D., Shoshan-Barmatz V. Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis. Mol. Cell. Biol. 2010, 30:5698-5709.
124. Elinder F., Akanda N., Tofighi R., Shimizu S., Tsujimoto Y., Orrenius S., Ceccatelli S. Opening of plasma membrane voltage-dependent anion channels (VDAC) precedes caspase activation in neuronal apoptosis induced by toxic stimuli. Cell Death Differ. 2005, 12:1134-1140.
125. Shoshan-Barmatz V., Keinan N., Abu-Hamad S., Tyomkin D., Aram L. Apoptosis is regulated by the VDAC1 N-terminal region and by VDAC oligomerization: release of cytochrome c, AIF and Smac/Diablo. Biochim. Biophys. Acta 2010, 1797:1281-1291.
126. Sugawara H., Kurosaki M., Takata M., Kurosaki T. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 1997, 16:3078-3088.
127. Jayaraman T., Marks A.R. T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol. Cell. Biol. 1997, 17:3005-3012.
128. Assefa Z., Bultynck G., Szlufcik K., Nadif Kasri N., Vermassen E., Goris J., Missiaen L., Callewaert G., Parys J.B., De Smedt H. Caspase-3-induced truncation of type 1 inositol trisphosphate receptor accelerates apoptotic cell death and induces inositol trisphosphate-independent calcium release during apoptosis. J. Biol. Chem. 2004, 279:43227-43236.
129. Tantral L., Malathi K., Kohyama S., Silane M., Berenstein A., Jayaraman T. Intracellular calcium release is required for caspase-3 and -9 activation. Cell Biochem. Funct. 2004, 22:35-40.
130. Jayaraman T., Marks A.R. Calcineurin is downstream of the inositol 1,4,5-trisphosphate receptor in the apoptotic and cell growth pathways. J. Biol. Chem. 2000, 275:6417-6420.
131. Joseph S.K., Hajnoczky G. IP3 receptors in cell survival and apoptosis: Ca2+ release and beyond. Apoptosis 2007, 12:951-968.
132. Kiviluoto S., Akl H., Vervliet T., Bultynck G., Parys J.B., Missiaen L., De Smedt H. IP3 receptor-binding partners in cell-death mechanisms. Wiley Interdiscip. Rev. Membr. Transp. Signal. 2012, 1:201-210.
133. Mendes C.C., Gomes D.A., Thompson M., Souto N.C., Goes T.S., Goes A.M., Rodrigues M.A., Gomez M.V., Nathanson M.H., Leite M.F. The type III inositol 1,4,5-trisphosphate receptor preferentially transmits apoptotic Ca2+ signals into mitochondria. J. Biol. Chem. 2005, 280:40892-40900.
134. Wozniak A.L., Wang X., Stieren E.S., Scarbrough S.G., Elferink C.J., Boehning D. Requirement of biphasic calcium release from the endoplasmic reticulum for Fas-mediated apoptosis. J. Cell Biol. 2006, 175:709-714.
135. Park K.M., Yule D.I., Bowers W.J. Impaired TNF-alpha control of IP3R-mediated Ca2+ release in Alzheimer's disease mouse neurons. Cell. Signal. 2010, 22:519-526.
136. Kiviluoto S., Schneider L., Luyten T., Vervliet T., Missiaen L., De Smedt H., Parys J.B., Methner A., Bultynck G. Bax inhibitor-1 is a novel IP(3) receptor-interacting and -sensitizing protein. Cell Death Dis. 2012, 3:e367.
137. Boehning D., Patterson R.L., Sedaghat L., Glebova N.O., Kurosaki T., Snyder S.H. Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat. Cell Biol. 2003, 5:1051-1061.
138. Boehning D., van Rossum D.B., Patterson R.L., Snyder S.H. A peptide inhibitor of cytochrome c/inositol 1,4,5-trisphosphate receptor binding blocks intrinsic and extrinsic cell death pathways. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:1466-1471.
139. Beresewicz M., Kowalczyk J.E., Zablocka B. Cytochrome c binds to inositol (1,4,5) trisphosphate and ryanodine receptors in vivo after transient brain ischemia in gerbils. Neurochem. Int. 2006, 48:568-571.
140. Verbert L., Lee B., Kocks S.L., Assefa Z., Parys J.B., Missiaen L., Callewaert G., Fissore R.A., De Smedt H., Bultynck G. Caspase-3-truncated type 1 inositol 1,4,5-trisphosphate receptor enhances intracellular Ca2+ leak and disturbs Ca2+ signalling. Biol. Cell 2008, 100:39-49.
141. Elkoreh G., Blais V., Beliveau E., Guillemette G., Denault J.B. Type 1 inositol-1,4,5-trisphosphate receptor is a late substrate of caspases during apoptosis. J. Cell. Biochem. 2012, 113:2775-2784.
142. Akimzhanov A.M., Barral J.M., Boehning D. Caspase 3 cleavage of the inositol 1,4,5-trisphosphate receptor does not contribute to apoptotic calcium release. Cell Calcium 2012, (epub ahead of print).
143. Kopil C.M., Siebert A.P., Kevin Foskett J., Neumar R.W. Calpain-cleaved type 1 inositol 1,4,5-trisphosphate receptor impairs ER Ca(2+) buffering and causes neurodegeneration in primary cortical neurons. J. Neurochem. 2012, 123:147-158.
144. Rong Y.P., Distelhorst C.W. Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu. Rev. Physiol. 2008, 70:73-91.
145. Distelhorst C.W., Bootman M.D. Bcl-2 interaction with the inositol 1,4,5-trisphosphate receptor: role in Ca(2+) signaling and disease. Cell Calcium 2012, 50:234-241.
146. Li C., Wang X., Vais H., Thompson C.B., Foskett J.K., White C. Apoptosis regulation by Bcl-x(L) modulation of mammalian inositol 1,4,5-trisphosphate receptor channel isoform gating. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12565-12570.
147. White C., Li C., Yang J., Petrenko N.B., Madesh M., Thompson C.B., Foskett J.K. The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat. Cell Biol. 2005, 7:1021-1028.
148. Eckenrode E.F., Yang J., Velmurugan G.V., Foskett J.K., White C. Apoptosis protection by Mcl-1 and Bcl-2 modulation of inositol 1,4,5-trisphosphate receptor-dependent Ca2+ signaling. J. Biol. Chem. 2010, 285:13678-13684.
149. Monaco G., Beckers M., Ivanova H., Missiaen L., Parys J.B., De Smedt H., Bultynck G. Profiling of the Bcl-2/Bcl-X(L)-binding sites on type 1 IP(3) receptor. Biochem. Biophys. Res. Commun. 2012, 428:31-35.
150. Oakes S.A., Scorrano L., Opferman J.T., Bassik M.C., Nishino M., Pozzan T., Korsmeyer S.J. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:105-110.
151. Chen R., Valencia I., Zhong F., McColl K.S., Roderick H.L., Bootman M.D., Berridge M.J., Conway S.J., Holmes A.B., Mignery G.A., Velez P., Distelhorst C.W. Bcl-2 functionally interacts with inositol 1,4,5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1,4,5-trisphosphate. J. Cell Biol. 2004, 166:193-203.
152. Hanson C.J., Bootman M.D., Distelhorst C.W., Wojcikiewicz R.J., Roderick H.L. Bcl-2 suppresses Ca2+ release through inositol 1,4,5-trisphosphate receptors and inhibits Ca2+ uptake by mitochondria without affecting ER calcium store content. Cell Calcium 2008, 44:324-338.
153. Petros A.M., Medek A., Nettesheim D.G., Kim D.H., Yoon H.S., Swift K., Matayoshi E.D., Oltersdorf T., Fesik S.W. Solution structure of the antiapoptotic protein bcl-2. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:3012-3017.
154. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997, 275:1132-1136.
155. Monaco G., Decrock E., Akl H., Ponsaerts R., Vervliet T., Luyten T., De Maeyer M., Missiaen L., Distelhorst C.W., De Smedt H., Parys J.B., Leybaert L., Bultynck G. Selective regulation of IP(3)-receptor-mediated Ca(2+) signaling and apoptosis by the BH4 domain of Bcl-2 versus Bcl-Xl. Cell Death Differ. 2012, 19:295-309.
156. 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.
157. Zhong F., Harr M.W., Bultynck G., Monaco G., Parys J.B., De Smedt H., Rong Y.P., Molitoris J.K., Lam M., Ryder C., Matsuyama S., Distelhorst C.W. Induction of Ca(2)+-driven apoptosis in chronic lymphocytic leukemia cells by peptide-mediated disruption of Bcl-2-IP3 receptor interaction. Blood 2011, 117:2924-2934.
158. Rong Y.P., Aromolaran A.S., Bultynck G., Zhong F., Li X., McColl K., Matsuyama S., Herlitze S., Roderick H.L., Bootman M.D., Mignery G.A., Parys J.B., De Smedt H., Distelhorst C.W. Targeting Bcl-2-IP3 receptor interaction to reverse Bcl-2's inhibition of apoptotic calcium signals. Mol. Cell 2008, 31:255-265.
159. Decrock E., De Vuyst E., Vinken M., Van Moorhem M., Vranckx K., Wang N., Van Laeken L., De Bock M., D'Herde K., Lai C.P., Rogiers V., Evans W.H., Naus C.C., Leybaert L. Connexin 43 hemichannels contribute to the propagation of apoptotic cell death in a rat C6 glioma cell model. Cell Death Differ. 2009, 16:151-163.
160. De Vuyst E., De Bock M., Decrock E., Van Moorhem M., Naus C., Mabilde C., Leybaert L. In situ bipolar electroporation for localized cell loading with reporter dyes and investigating gap junctional coupling. Biophys. J. 2008, 94:469-479.
161. Cusato K., Ripps H., Zakevicius J., Spray D.C. Gap junctions remain open during cytochrome c-induced cell death: relationship of conductance to 'bystander' cell killing. Cell Death Differ. 2006, 13:1707-1714.
162. Peixoto P.M., Ryu S.Y., Pruzansky D.P., Kuriakose M., Gilmore A., Kinnally K.W. Mitochondrial apoptosis is amplified through gap junctions. Biochem. Biophys. Res. Commun. 2009, 390:38-43.
163. Budd S.L., Lipton S.A. Calcium tsunamis: do astrocytes transmit cell death messages via gap junctions during ischemia?. Nat. Neurosci. 1998, 1:431-432.
164. Wolszon L.R., Rehder V., Kater S.B., Macagno E.R. Calcium wave fronts that cross gap junctions may signal neuronal death during development. J. Neurosci. 1994, 14:3437-3448.
165. Decrock E., Vinken M., Bol M., D'Herde K., Rogiers V., Vandenabeele P., Krysko D.V., Bultynck G., Leybaert L. Calcium and connexin-based intercellular communication, a deadly catch?. Cell Calcium 2011, 50:310-321.
166. Morales A.P., Carvalho A.C., Monteforte P.T., Hirata H., Han S.W., Hsu Y.T., Smaili S.S. Endoplasmic reticulum calcium release engages Bax translocation in cortical astrocytes. Neurochem. Res. 2011, 36:829-838.
167. Carvalho A.C., Sharpe J., Rosenstock T.R., Teles A.F., Youle R.J., Smaili S.S. Bax affects intracellular Ca2+ stores and induces Ca2+ wave propagation. Cell Death Differ. 2004, 11:1265-1276.
168. Frank D.K., Szymkowiak B., Josifovska-Chopra O., Nakashima T., Kinnally K.W. Single-cell microinjection of cytochrome c can result in gap junction-mediated apoptotic cell death of bystander cells in head and neck cancer. Head Neck 2005, 27:794-800.
169. Udawatte C., Ripps H. The spread of apoptosis through gap-junctional channels in BHK cells transfected with Cx32. Apoptosis 2005, 10:1019-1029.
170. Cusato K., Bosco A., Rozental R., Guimaraes C.A., Reese B.E., Linden R., Spray D.C. Gap junctions mediate bystander cell death in developing retina. J. Neurosci. 2003, 23:6413-6422.
171. Beltramello M., Piazza V., Bukauskas F.F., Pozzan T., Mammano F. Impaired permeability to Ins(1,4,5)P3 in a mutant connexin underlies recessive hereditary deafness. Nat. Cell Biol. 2005, 7:63-69.
172. Scorrano L., Oakes S.A., Opferman J.T., Cheng E.H., Sorcinelli M.D., Pozzan T., Korsmeyer S.J. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 2003, 300:135-139.
173. Ferrari D., Pinton P., Campanella M., Callegari M.G., Pizzirani C., Rimessi A., Di Virgilio F., Pozzan T., Rizzuto R. Functional and structural alterations in the endoplasmic reticulum and mitochondria during apoptosis triggered by C2-ceramide and CD95/APO-1/FAS receptor stimulation. Biochem. Biophys. Res. Commun. 2010, 391:575-581.
174. Dix M.M., Simon G.M., Cravatt B.F. Global mapping of the topography and magnitude of proteolytic events in apoptosis. Cell 2008, 134:679-691.
175. Pang B., Neijssen J., Qiao X., Janssen L., Janssen H., Lippuner C., Neefjes J. Direct antigen presentation and gap junction mediated cross-presentation during apoptosis. J. Immunol. 2009, 183:1083-1090.
176. Neijssen J., Herberts C., Drijfhout J.W., Reits E., Janssen L., Neefjes J. Cross-presentation by intercellular peptide transfer through gap junctions. Nature 2005, 434:83-88.
177. Johnson D.E. Noncaspase proteases in apoptosis. Leukemia 2000, 14:1695-1703.
178. Szlufcik K., Missiaen L., Parys J.B., Callewaert G., De Smedt H. Uncoupled IP3 receptor can function as a Ca2+-leak channel: cell biological and pathological consequences. Biol. Cell 2006, 98:1-14.
179. Bootman M.D., Lipp P. Ringing changes to the 'bell-shaped curve'. Curr. Biol. 1999, 9:R876-R878.
180. Ramos-Franco J., Fill M., Mignery G.A. Isoform-specific function of single inositol 1,4,5-trisphosphate receptor channels. Biophys. J. 1998, 75:834-839.
181. Ramos-Franco J., Bare D., Caenepeel S., Nani A., Fill M., Mignery G. Single-channel function of recombinant type 2 inositol 1,4, 5-trisphosphate receptor. Biophys. J. 2000, 79:1388-1399.
182. Mak D.O., McBride S., Foskett J.K. Regulation by Ca2+ and inositol 1,4,5-trisphosphate (InsP3) of single recombinant type 3 InsP3 receptor channels. Ca2+ activation uniquely distinguishes types 1 and 3 insp3 receptors. J. Gen. Physiol. 2001, 117:435-446.
183. Hagar R.E., Burgstahler A.D., Nathanson M.H., Ehrlich B.E. Type III InsP3 receptor channel stays open in the presence of increased calcium. Nature 1998, 396:81-84.
184. Missiaen L., Parys J.B., Sienaert I., Maes K., Kunzelmann K., Takahashi M., Tanzawa K., De Smedt H. Functional properties of the type-3 InsP3 receptor in 16HBE14o- bronchial mucosal cells. J. Biol. Chem. 1998, 273:8983-8986.
185. Adkins C.E., Taylor C.W. Lateral inhibition of inositol 1,4,5-trisphosphate receptors by cytosolic Ca(2+). Curr. Biol. 1999, 9:1115-1118.
186. Dupont G., Koukoui O., Clair C., Erneux C., Swillens S., Combettes L. Ca2+ oscillations in hepatocytes do not require the modulation of InsP3 3-kinase activity by Ca2+. FEBS Lett. 2003, 534:101-105.
187. De Smedt F., Missiaen L., Parys J.B., Vanweyenberg V., De Smedt H., Erneux C. Isoprenylated human brain type I inositol 1,4,5-trisphosphate 5-phosphatase controls Ca2+ oscillations induced by ATP in Chinese hamster ovary cells. J. Biol. Chem. 1997, 272:17367-17375.
188. Guo Y., Golebiewska U., D'Amico S., Scarlata S. The small G protein Rac1 activates phospholipase Cdelta1 through phospholipase Cbeta2. J. Biol. Chem. 2010, 285:24999-25008.
189. Allen V., Swigart P., Cheung R., Cockcroft S., Katan M. Regulation of inositol lipid-specific phospholipase cdelta by changes in Ca2+ ion concentrations. Biochem. J. 1997, 327(Pt 2):545-552.
190. Sims C.E., Allbritton N.L. Metabolism of inositol 1,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate by the oocytes of Xenopus laevis. J. Biol. Chem. 1998, 273:4052-4058.
191. Lin M.J., Yang X.R., Cao Y.N., Sham J.S. Hydrogen peroxide-induced Ca2+ mobilization in pulmonary arterial smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 292:L1598-L1608.
192. Kaja S., Duncan R.S., Longoria S., Hilgenberg J.D., Payne A.J., Desai N.M., Parikh R.A., Burroughs S.L., Gregg E.V., Goad D.L., Koulen P. Novel mechanism of increased Ca2+ release following oxidative stress in neuronal cells involves type 2 inositol-1,4,5-trisphosphate receptors. Neuroscience 2011, 175:281-291.
193. Bultynck G., Szlufcik K., Kasri N.N., Assefa Z., Callewaert G., Missiaen L., Parys J.B., De Smedt H. Thimerosal stimulates Ca2+ flux through inositol 1,4,5-trisphosphate receptor type 1, but not type 3, via modulation of an isoform-specific Ca2+-dependent intramolecular interaction. Biochem. J. 2004, 381:87-96.
194. Miyazaki S., Shirakawa H., Nakada K., Honda Y., Yuzaki M., Nakade S., Mikoshiba K. Antibody to the inositol trisphosphate receptor blocks thimerosal-enhanced Ca(2+)-induced Ca2+ release and Ca2+ oscillations in hamster eggs. FEBS Lett. 1992, 309:180-184.
195. Bootman M.D., Taylor C.W., Berridge M.J. The thiol reagent, thimerosal, evokes Ca2+ spikes in HeLa cells by sensitizing the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 1992, 267:25113-25119.
196. Kaplin A.I., Ferris C.D., Voglmaier S.M., Snyder S.H. Purified reconstituted inositol 1,4,5-trisphosphate receptors. Thiol reagents act directly on receptor protein. J. Biol. Chem. 1994, 269:28972-28978.
197. Redondo P.C., Salido G.M., Rosado J.A., Pariente J.A. Effect of hydrogen peroxide on Ca2+ mobilisation in human platelets through sulphydryl oxidation dependent and independent mechanisms. Biochem. Pharmacol. 2004, 67:491-502.
198. Zheng Y., Shen X. H2O2 directly activates inositol 1,4,5-trisphosphate receptors in endothelial cells. Redox Rep. 2005, 10:29-36.
199. Higo T., Hattori M., Nakamura T., Natsume T., Michikawa T., Mikoshiba K. Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell 2005, 120:85-98.
200. Peng T.I., Jou M.J. Oxidative stress caused by mitochondrial calcium overload. Ann. N. Y. Acad. Sci. 2010, 1201:183-188.
201. Tang E.H., Vanhoutte P.M. Gap junction inhibitors reduce endothelium-dependent contractions in the aorta of spontaneously hypertensive rats. J. Pharmacol. Exp. Ther. 2008, 327:148-153.
202. VanSlyke J.K., Musil L.S. Cytosolic stress reduces degradation of connexin 43 internalized from the cell surface and enhances gap junction formation and function. Mol. Biol. Cell 2005, 16:5247-5257.
203. Retamal M.A., Cortes C.J., Reuss L., Bennett M.V., Saez J.C. S-nitrosylation and permeation through connexin 43 hemichannels in astrocytes: induction by oxidant stress and reversal by reducing agents. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:4475-4480.
204. Hamada N., Maeda M., Otsuka K., Tomita M. Signaling pathways underpinning the manifestations of ionizing radiation-induced bystander effects. Curr. Mol. Pharmacol. 2011, 4:79-95.
205. Trosko J.E., Inoue T. Oxidative stress, signal transduction, and intercellular communication in radiation carcinogenesis. Stem Cells 1997, 15(Suppl. 2):59-67.
206. Shao C., Prise K.M., Folkard M. Signaling factors for irradiated glioma cells induced bystander responses in fibroblasts. Mutat. Res. 2008, 638:139-145.
207. Lyng F.M., Howe O.L., McClean B. Reactive oxygen species-induced release of signalling factors in irradiated cells triggers membrane signalling and calcium influx in bystander cells. Int. J. Radiat. Biol. 2011, 87:683-695.
208. Azzam E.I., de Toledo S.M., Little J.B. Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect. Oncogene 2003, 22:7050-7057.
209. Harada T., Kashino G., Suzuki K., Matsuda N., Kodama S., Watanabe M. Different involvement of radical species in irradiated and bystander cells. Int. J. Radiat. Biol. 2008, 84:809-814.
210. Tu H., Wang Z., Nosyreva E., De Smedt H., Bezprozvanny I. Functional characterization of mammalian inositol 1,4,5-trisphosphate receptor isoforms. Biophys. J. 2005, 88:1046-1055.
211. Bezprozvanny I., Ehrlich B.E. ATP modulates the function of inositol 1,4,5-trisphosphate-gated channels at two sites. Neuron 1993, 10:1175-1184.
212. Zamaraeva M.V., Sabirov R.Z., Maeno E., Ando-Akatsuka Y., Bessonova S.V., Okada Y. Cells die with increased cytosolic ATP during apoptosis: a bioluminescence study with intracellular luciferase. Cell Death Differ. 2005, 12:1390-1397.
213. Xu K.Y., Zweier J.L., Becker L.C. Hydroxyl radical inhibits sarcoplasmic reticulum Ca(2+)-ATPase function by direct attack on the ATP binding site. Circ. Res. 1997, 80:76-81.
214. Li J.H., Yue W., Huang Z., Chen Z.Q., Zhan Q., Ren F.B., Liu J.Y., Fu S.B. Calcium overload induces C6 rat glioma cell apoptosis in sonodynamic therapy. Int. J. Radiat. Biol. 2011, 87:1061-1066.
215. Bultynck G., Vermassen E., Szlufcik K., De Smet P., Fissore R.A., Callewaert G., Missiaen L., De Smedt H., Parys J.B. Calcineurin and intracellular Ca2+-release channels: regulation or association?. Biochem. Biophys. Res. Commun. 2003, 311:1181-1193.
216. Vanderheyden V., Devogelaere B., Missiaen L., De Smedt H., Bultynck G., Parys J.B. Regulation of inositol 1,4,5-trisphosphate-induced Ca2+ release by reversible phosphorylation and dephosphorylation. Biochim. Biophys. Acta 2009, 1793:959-970.
217. Szado T., Vanderheyden V., Parys J.B., De Smedt H., Rietdorf K., Kotelevets L., Chastre E., Khan F., Landegren U., Soderberg O., Bootman M.D., Roderick H.L. Phosphorylation of inositol 1,4,5-trisphosphate receptors by protein kinase B/Akt inhibits Ca2+ release and apoptosis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2427-2432.
218. Follin-Arbelet V., Hofgaard P.O., Hauglin H., Naderi S., Sundan A., Blomhoff R., Bogen B., Blomhoff H.K. Cyclic AMP induces apoptosis in multiple myeloma cells and inhibits tumor development in a mouse myeloma model. BMC Cancer 2011, 11:301.
219. Fallahian F., Karami-Tehrani F., Salami S., Aghaei M. Cyclic GMP induced apoptosis via protein kinase G in oestrogen receptor-positive and -negative breast cancer cell lines. FEBS J. 2011, 278:3360-3369.
220. Bevans C.G., Kordel M., Rhee S.K., Harris A.L. Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J. Biol. Chem. 1998, 273:2808-2816.
221. Wagner L.E., Joseph S.K., Yule D.I. Regulation of single inositol 1,4,5-trisphosphate receptor channel activity by protein kinase A phosphorylation. J. Physiol. 2008, 586:3577-3596.
222. Wagner L.E., Li W.H., Yule D.I. Phosphorylation of type-1 inositol 1,4,5-trisphosphate receptors by cyclic nucleotide-dependent protein kinases: a mutational analysis of the functionally important sites in the S2+ and S2- splice variants. J. Biol. Chem. 2003, 278:45811-45817.
223. Tertyshnikova S., Yan X., Fein A. cGMP inhibits IP3-induced Ca2+ release in intact rat megakaryocytes via cGMP- and cAMP-dependent protein kinases. J. Physiol. 1998, 512(Pt 1):89-96.
224. Giovannucci D.R., Groblewski G.E., Sneyd J., Yule D.I. Targeted phosphorylation of inositol 1,4,5-trisphosphate receptors selectively inhibits localized Ca2+ release and shapes oscillatory Ca2+ signals. J. Biol. Chem. 2000, 275:33704-33711.
225. Peixoto P.M., Lue J.K., Ryu S.Y., Wroble B.N., Sible J.C., Kinnally K.W. Mitochondrial apoptosis-induced channel (MAC) function triggers a Bax/Bak-dependent bystander effect. Am. J. Pathol. 2011, 178:48-54.
226. Nutt L.K., Chandra J., Pataer A., Fang B., Roth J.A., Swisher S.G., O'Neil R.G., McConkey D.J. Bax-mediated Ca2+ mobilization promotes cytochrome c release during apoptosis. J. Biol. Chem. 2002, 277:20301-20308.
227. Khan M.T., Bhanumathy C.D., Schug Z.T., Joseph S.K. Role of inositol 1,4,5-trisphosphate receptors in apoptosis in DT40 lymphocytes. J. Biol. Chem. 2007, 282:32983-32990.
228. Giorgi C., Baldassari F., Bononi A., Bonora M., De Marchi E., Marchi S., Missiroli S., Patergnani S., Rimessi A., Suski J.M., Wieckowski M.R., Pinton P. Mitochondrial Ca(2+) and apoptosis. Cell Calcium 2012, 52:36-43.
229. Davidson S.M., Yellon D.M., Murphy M.P., Duchen M.R. Slow calcium waves and redox changes precede mitochondrial permeability transition pore opening in the intact heart during hypoxia and reoxygenation. Cardiovasc. Res. 2012, 93:445-453.
230. Joiner M.L., Koval O.M., Li J., He B.J., Allamargot C., Gao Z., Luczak E.D., Hall D.D., Fink B.D., Chen B., Yang J., Moore S.A., Scholz T.D., Strack S., Mohler P.J., Sivitz W.I., Song L.S., Anderson M.E. CaMKII determines mitochondrial stress responses in heart. Nature 2012, 491:269-273.
231. Rizzuto R., De Stefani D., Raffaello A., Mammucari C. Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell Biol. 2012, 13:566-578.
232. Li H., Brodsky S., Kumari S., Valiunas V., Brink P., Kaide J., Nasjletti A., Goligorsky M.S. Paradoxical overexpression and translocation of connexin43 in homocysteine-treated endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H2124-H2133.
233. Azarashvili T., Baburina Y., Grachev D., Krestinina O., Evtodienko Y., Stricker R., Reiser G. Calcium-induced permeability transition in rat brain mitochondria is promoted by carbenoxolone through targeting connexin43. Am. J. Physiol. Cell Physiol. 2011, 300:C707-C720.
234. Goubaeva F., Mikami M., Giardina S., Ding B., Abe J., Yang J. Cardiac mitochondrial connexin 43 regulates apoptosis. Biochem. Biophys. Res. Commun. 2007, 352:97-103.
235. Boengler K., Dodoni G., Rodriguez-Sinovas A., Cabestrero A., Ruiz-Meana M., Gres P., Konietzka I., Lopez-Iglesias C., Garcia-Dorado D., Di Lisa F., Heusch G., Schulz R. Connexin 43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning. Cardiovasc. Res. 2005, 67:234-244.
236. Rottlaender D., Boengler K., Wolny M., Schwaiger A., Motloch L.J., Ovize M., Schulz R., Heusch G., Hoppe U.C. Glycogen synthase kinase 3beta transfers cytoprotective signaling through connexin 43 onto mitochondrial ATP-sensitive K+ channels. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E242-E251.
237. Lu G., Haider H., Porollo A., Ashraf M. Mitochondria-specific transgenic overexpression of connexin-43 simulates preconditioning-induced cytoprotection of stem cells. Cardiovasc. Res. 2010, 88:277-286.
238. Orellana J.A., Froger N., Ezan P., Jiang J.X., Bennett M.V., Naus C.C., Giaume C., Saez J.C. ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J. Neurochem. 2011, 118:826-840.
239. Takeuchi H., Jin S., Wang J., Zhang G., Kawanokuchi J., Kuno R., Sonobe Y., Mizuno T., Suzumura A. Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J. Biol. Chem. 2006, 281:21362-21368.
240. Orellana J.A., Shoji K.F., Abudara V., Ezan P., Amigou E., Saez P.J., Jiang J.X., Naus C.C., Saez J.C., Giaume C. Amyloid beta-induced death in neurons involves glial and neuronal hemichannels. J. Neurosci. 2011, 31:4962-4977.
241. Takeuchi H., Jin S., Suzuki H., Doi Y., Liang J., Kawanokuchi J., Mizuno T., Sawada M., Suzumura A. Blockade of microglial glutamate release protects against ischemic brain injury. Exp. Neurol. 2008, 214:144-146.
242. Takeuchi H., Mizoguchi H., Doi Y., Jin S., Noda M., Liang J., Li H., Zhou Y., Mori R., Yasuoka S., Li E., Parajuli B., Kawanokuchi J., Sonobe Y., Sato J., Yamanaka K., Sobue G., Mizuno T., Suzumura A. Blockade of gap junction hemichannel suppresses disease progression in mouse models of amyotrophic lateral sclerosis and Alzheimer's disease. PLoS One 2011, 6:e21108.
243. Sanchez H.A., Orellana J.A., Verselis V.K., Saez J.C. Metabolic inhibition increases activity of connexin-32 hemichannels permeable to Ca2+ in transfected HeLa cells. Am. J. Physiol. Cell Physiol. 2009, 297:C665-C678.
244. Ramachandran S., Xie L.H., John S.A., Subramaniam S., Lal R. A novel role for connexin hemichannel in oxidative stress and smoking-induced cell injury. PLoS One 2007, 2:e712.
245. Gossman D.G., Zhao H.B. Hemichannel-mediated inositol 1,4,5-trisphosphate (IP3) release in the cochlea: a novel mechanism of IP3 intercellular signaling. Cell Commun. Adhes. 2008, 15:305-315.
246. Przyklenk K., Maynard M., Darling C.E., Whittaker P. Pretreatment with D-myo-inositol trisphosphate reduces infarct size in rabbit hearts: role of inositol trisphosphate receptors and gap junctions in triggering protection. J. Pharmacol. Exp. Ther. 2005, 314:1386-1392.
247. Taylor C.W., Dellis O. Plasma membrane IP3 receptors. Biochem. Soc. Trans. 2006, 34:910-912.
248. Berridge M.J. Calcium signalling remodelling and disease. Biochem. Soc. Trans. 2012, 40:297-309.
249. Dhein S., Hagen A., Jozwiak J., Dietze A., Garbade J., Barten M., Kostelka M., Mohr F.W. Improving cardiac gap junction communication as a new antiarrhythmic mechanism: the action of antiarrhythmic peptides. Naunyn Schmiedebergs Arch. Pharmacol. 2010, 381:221-234.
250. Connors B.W., Long M.A. Electrical synapses in the mammalian brain. Annu. Rev. Neurosci. 2004, 27:393-418.
251. Dere E., Zlomuzica A. The role of gap junctions in the brain in health and disease. Neurosci. Biobehav. Rev. 2012, 36:206-217.
252. Ezan P., Andre P., Cisternino S., Saubamea B., Boulay A.C., Doutremer S., Thomas M.A., Quenech'du N., Giaume C., Cohen-Salmon M. Deletion of astroglial connexins weakens the blood-brain barrier. J. Cereb. Blood Flow Metab. 2012, 32:1457-1467.
253. Haydon P.G., Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol. Rev. 2006, 86:1009-1031.
254. Braet K., Cabooter L., Paemeleire K., Leybaert L. Calcium signal communication in the central nervous system. Biol. Cell 2004, 96:79-91.
255. Woodruff T.M., Thundyil J., Tang S.C., Sobey C.G., Taylor S.M., Arumugam T.V. Pathophysiology, treatment, and animal and cellular models of human ischemic stroke. Mol. Neurodegener. 2011, 6:11.
256. Moskowitz M.A., Lo E.H., Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010, 67:181-198.
257. Contreras J.E., Sanchez H.A., Veliz L.P., Bukauskas F.F., Bennett M.V., Saez J.C. Role of connexin-based gap junction channels and hemichannels in ischemia-induced cell death in nervous tissue. Brain Res. Brain Res. Rev. 2004, 47:290-303.
258. Wang Y., Denisova J.V., Kang K.S., Fontes J.D., Zhu B.T., Belousov A.B. Neuronal gap junctions are required for NMDA receptor-mediated excitotoxicity: implications in ischemic stroke. J. Neurophysiol. 2010, 104:3551-3556.
259. Wang Y., Song J.H., Denisova J.V., Park W.M., Fontes J.D., Belousov A.B. Neuronal gap junction coupling is regulated by glutamate and plays critical role in cell death during neuronal injury. J. Neurosci. 2012, 32:713-725.
260. Ding S., Wang T., Cui W., Haydon P.G. Photothrombosis ischemia stimulates a sustained astrocytic Ca2+ signaling in vivo. Glia 2009, 57:767-776.
261. Verkhratsky A., Toescu E.C. Endoplasmic reticulum Ca(2+) homeostasis and neuronal death. J. Cell. Mol. Med. 2003, 7:351-361.
262. Nagata E., Tanaka K., Suzuki S., Dembo T., Fukuuchi Y., Futatsugi A., Mikoshiba K. Selective inhibition of inositol 1,4,5-triphosphate-induced Ca2+ release in the CA1 region of the hippocampus in the ischemic gerbil. Neuroscience 1999, 93:995-1001.
263. Nagata E., Tanaka K., Gomi S., Mihara B., Shirai T., Nogawa S., Nozaki H., Mikoshiba K., Fukuuchi Y. Alteration of inositol 1,4,5-trisphosphate receptor after six-hour hemispheric ischemia in the gerbil brain. Neuroscience 1994, 61:983-990.
264. Hernandez-Fonseca K., Massieu L. Disruption of endoplasmic reticulum calcium stores is involved in neuronal death induced by glycolysis inhibition in cultured hippocampal neurons. J. Neurosci. Res. 2005, 82:196-205.
265. Haughey N.J., Mattson M.P. Alzheimer's amyloid beta-peptide enhances ATP/gap junction-mediated calcium-wave propagation in astrocytes. Neuromolecular Med. 2003, 3:173-180.
266. Kuchibhotla K.V., Lattarulo C.R., Hyman B.T., Bacskai B.J. Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 2009, 323:1211-1215.
267. Muller M., Cheung K.H., Foskett J.K. Enhanced ROS generation mediated by Alzheimer's disease presenilin regulation of InsP3R Ca2+ signaling. Antioxid. Redox Signal. 2011, 14:1225-1235.
268. Cheung K.H., Mei L., Mak D.O., Hayashi I., Iwatsubo T., Kang D.E., Foskett J.K. Gain-of-function enhancement of IP3 receptor modal gating by familial Alzheimer's disease-linked presenilin mutants in human cells and mouse neurons. Sci. Signal. 2010, 3:ra22.
269. Lezi E., Swerdlow R.H. Mitochondria in neurodegeneration. Adv. Exp. Med. Biol. 2012, 942:269-286.
270. Luo X.G., Ding J.Q., Chen S.D. Microglia in the aging brain: relevance to neurodegeneration. Mol. Neurodegener. 2010, 5:12.
271. Sieger D., Moritz C., Ziegenhals T., Prykhozhij S., Peri F. Long-range Ca2+ waves transmit brain-damage signals to microglia. Dev. Cell 2012, 22:1138-1148.
272. Roderick H.L., Bootman M.D. Pacemaking, arrhythmias, inotropy and hypertrophy: the many possible facets of IP3 signalling in cardiac myocytes. J. Physiol. 2007, 581:883-884.
273. Ju Y.K., Woodcock E.A., Allen D.G., Cannell M.B. Inositol 1,4,5-trisphosphate receptors and pacemaker rhythms. J. Mol. Cell. Cardiol. 2012, 53:375-381.
274. Bers D.M. Calcium fluxes involved in control of cardiac myocyte contraction. Circ. Res. 2000, 87:275-281.
275. Blum A. Heart failure-new insights. Isr. Med. Assoc. J. 2009, 11:105-111.
276. Proven A., Roderick H.L., Conway S.J., Berridge M.J., Horton J.K., Capper S.J., Bootman M.D. Inositol 1,4,5-trisphosphate supports the arrhythmogenic action of endothelin-1 on ventricular cardiac myocytes. J. Cell Sci. 2006, 119:3363-3375.
277. Mackenzie L., Roderick H.L., Proven A., Conway S.J., Bootman M.D. Inositol 1,4,5-trisphosphate receptors in the heart. Biol. Res. 2004, 37:553-557.
278. Domeier T.L., Zima A.V., Maxwell J.T., Huke S., Mignery G.A., Blatter L.A. IP3 receptor-dependent Ca2+ release modulates excitation-contraction coupling in rabbit ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H596-H604.
279. Escobar A.L., Perez C.G., Reyes M.E., Lucero S.G., Kornyeyev D., Mejia-Alvarez R., Ramos-Franco J. Role of inositol 1,4,5-trisphosphate in the regulation of ventricular Ca(2+) signaling in intact mouse heart. J. Mol. Cell. Cardiol. 2012, 53:768-779.
280. Gutstein D.E., Marks A.R. Role of inositol 1,4,5-trisphosphate receptors in regulating apoptotic signaling and heart failure. Heart Vessels Suppl. 1997, 12:53-57.
281. Binah O., Shilkrut M., Yaniv G., Larisch S. The Fas receptor-1,4,5-IP3 cascade: a potential target for treating heart failure and arrhythmias. Ann. N. Y. Acad. Sci. 2004, 1015:338-350.
282. Wong A., Grubb D.R., Cooley N., Luo J., Woodcock E.A. Regulation of autophagy in cardiomyocytes by Ins(1,4,5)P(3) and IP(3)-receptors. J. Mol. Cell. Cardiol. 2012, (epub ahead of print).
283. Nemchenko A., Chiong M., Turer A., Lavandero S., Hill J.A. Autophagy as a therapeutic target in cardiovascular disease. J. Mol. Cell. Cardiol. 2011, 51:584-593.
284. Arantes L.A., Aguiar C.J., Amaya M.J., Figueiro N.C., Andrade L.M., Rocha-Resende C., Resende R.R., Franchini K.G., Guatimosim S., Leite M.F. Nuclear inositol 1,4,5-trisphosphate is a necessary and conserved signal for the induction of both pathological and physiological cardiomyocyte hypertrophy. J. Mol. Cell. Cardiol. 2012, 53:475-486.
285. Higazi D.R., Fearnley C.J., Drawnel F.M., Talasila A., Corps E.M., Ritter O., McDonald F., Mikoshiba K., Bootman M.D., Roderick H.L. Endothelin-1-stimulated InsP3-induced Ca2+ release is a nexus for hypertrophic signaling in cardiac myocytes. Mol. Cell 2009, 33:472-482.
286. Zima A.V., Bare D.J., Mignery G.A., Blatter L.A. IP3-dependent nuclear Ca2+ signalling in the mammalian heart. J. Physiol. 2007, 584:601-611.
287. Wu X., Zhang T., Bossuyt J., Li X., McKinsey T.A., Dedman J.R., Olson E.N., Chen J., Brown J.H., Bers D.M. Local InsP3-dependent perinuclear Ca2+ signaling in cardiac myocyte excitation-transcription coupling. J. Clin. Invest. 2006, 116:675-682.
288. Giorgi C., Wieckowski M.R., Pandolfi P.P., Pinton P. Mitochondria associated membranes (MAMs) as critical hubs for apoptosis. Commun. Integr. Biol. 2011, 4:334-335.