Transfer of IP 3 through gap junctions is critical, but not sufficient, for the spread of apoptosis

Cell Death and Differentiation

Volumn 19, Issue 6, 2012, Pages 947-957

  Decrock, E ^a,k   Krysko, D V ^b,c,k   Vinken, M ^d,k   Kaczmarek, A ^b,c,k   Crispino, G ^e   Bol, M ^a   Wang, N ^a   De Bock, M ^a   De Vuyst, E ^a   Naus, C C ^f   Rogiers, V ^d   Vandenabeele, P ^b,c   Erneux, C ^g   Mammano, F ^e,h,i   Bultynck, G ^j   Leybaert, L ^a  

^a GHENT UNIVERSITY   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d FACULTY OF MEDICINE AND PHARMACY   (Belgium)

^e Fondazione per la Ricerca Biomedica Avanzata   (Italy)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^g UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^h UNIVERSITY OF PADOVA   (Italy)

ⁱ CNR   (Italy)

^j UNIVERSITY OF LEUVEN   (Belgium)

^k RESEARCH FOUNDATION FLANDERS FWO   (Belgium)

more..

Author keywords

Apoptosis; Calcium; Connexin; Gap junction; Inositol 1,4,5 trisphosphate

Indexed keywords

CONNEXIN 26; CONNEXIN 43; CYTOCHROME C; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE PERMEABILITY; GAP JUNCTION; GLIOMA CELL; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL COMMUNICATION; CELL MEMBRANE PERMEABILITY; CONNEXIN 43; CONNEXINS; CYTOCHROMES C; GAP JUNCTIONS; INOSITOL 1,4,5-TRISPHOSPHATE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; RATS; SIGNAL TRANSDUCTION;

EID: 84860722401     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2011.176     Document Type: Article

References (40)

1. Boehning D, van Rossum DB, Patterson RL, Snyder SH. A peptide inhibitor of cytochrome c/inositol 1,4,5-trisphosphate receptor binding blocks intrinsic and extrinsic cell death pathways. Proc Natl Acad Sci USA 2005; 102: 1466-1471.
2. Verkhratsky A. Calcium and cell death. Subcell Biochem 2007; 45: 465-480.
3. Decuypere JP, Monaco G, Bultynck G, Missiaen L, De Smedt H, Parys JB. The IP(3) receptor-mitochondria connection in apoptosis and autophagy. Biochim Biophys Acta 2011; 1813: 1003-1013.
4. Sammels E, Parys JB, Missiaen L, De Smedt H, Bultynck G. Intracellular Ca2+ storage in health and disease: a dynamic equilibrium. Cell Calcium 2010; 47: 297-314.
5. Szalai G, Krishnamurthy R, Hajnoczky G. Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J 1999; 18: 6349-6361.
6. 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.
7. Rong YP, Distelhorst CW. Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 2008; 70: 73-91.
8. Boitano S, Dirksen ER, Sanderson MJ. Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science 1992; 258: 292-295.
9. Saez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC. Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 2003; 83: 1359-1400.
10. Decrock E, Vinken M, De Vuyst E, Krysko DV, D'Herde K, Vanhaecke T et al. Connexinrelated signaling in cell death: to live or let die? Cell Death Differ 2009; 16: 524-536.
11. Decrock E, De Vuyst E, Vinken M, Van Moorhem M, Vranckx K, Wang N et al. 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.
12. Cusato K, Bosco A, Rozental R, Guimaraes CA, Reese BE, Linden R et al. Gap junctions mediate bystander cell death in developing retina. J Neurosci 2003; 23: 6413-6422.
13. Cusato K, Ripps H, Zakevicius J, Spray DC. Gap junctions remain open during cytochrome c-induced cell death: relationship of conductance to 'bystander' cell killing. Cell Death Differ 2006; 13: 1707-1714.
14. Frank DK, Szymkowiak B, Josifovska-Chopra O, Nakashima T, Kinnally KW. 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.
15. Udawatte C, Ripps H. The spread of apoptosis through gap-junctional channels in BHK cells transfected with Cx32. Apoptosis 2005; 10: 1019-1029.
16. Peixoto PM, Ryu SY, Pruzansky DP, Kuriakose M, Gilmore A, Kinnally KW. Mitochondrial apoptosis is amplified through gap junctions. Biochem Biophys Res Commun 2009; 390: 38-43.
17. Decrock E, Vinken M, Bol M, D'Herde K, Rogiers V, Vandenabeele P et al. Calcium and connexin-based intercellular communication, a deadly catch? Cell Calcium 2011; 50: 310-321.
18. Allbritton NL, Meyer T, Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 1992; 258: 1812-1815.
19. Hofer T, Venance L, Giaume C. Control and plasticity of intercellular calcium waves in astrocytes: a modeling approach. J Neurosci 2002; 22: 4850-4859.
20. Assefa Z, Bultynck G, Szlufcik K, Nadif Kasri N, Vermassen E, Goris J et al. 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.
21. Verbert L, Lee B, Kocks SL, Assefa Z, Parys JB, Missiaen L et al. 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.
22. Huang DC, Adams JM, Cory S. The conserved N-terminal BH4 domain of Bcl-2 homologues is essential for inhibition of apoptosis and interaction with CED-4. EMBO J 1998; 17: 1029-1039.
23. Rong YP, Bultynck G, Aromolaran AS, Zhong F, Parys JB, De Smedt H et al. 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 USA 2009; 106: 14397-14402.
24. Monaco G, Decrock E, Akl H, Ponsaerts R, Vervliet T, Luyten T et al. 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 2011; e-pub ahead of print 5 August 2011.
25. Bruzzone R, Veronesi V, Gomes D, Bicego M, Duval N, Marlin S et al. Loss-of-function and residual channel activity of connexin26 mutations associated with non-syndromic deafness. FEBS Lett 2003; 533: 79-88.
26. Beltramello M, Piazza V, Bukauskas FF, 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.
27. Anselmi F, Hernandez VH, Crispino G, Seydel A, Ortolano S, Roper SD et al. ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc Natl Acad Sci USA 2008; 105: 18770-18775.
28. Nutt LK, Chandra J, Pataer A, Fang B, Roth JA, Swisher SG et al. Bax-mediated Ca2+ mobilization promotes cytochrome c release during apoptosis. J Biol Chem 2002; 277: 20301-20308.
29. Peng TI, Jou MJ. Oxidative stress caused by mitochondrial calcium overload. Ann N Y Acad Sci 2010; 1201: 183-188.
30. Tang EH, Vanhoutte PM. Gap junction inhibitors reduce endothelium-dependent contractions in the aorta of spontaneously hypertensive rats. J Pharmacol Exp Ther 2008; 327: 148-153.
31. 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.
32. De Smedt F, Verjans B, Mailleux P, Erneux C. Cloning and expression of human brain type I inositol 1,4,5-trisphosphate 5-phosphatase. High levels of mRNA in cerebellar Purkinje cells. FEBS Lett 1994; 347: 69-72.
33. Morales AP, Carvalho AC, Monteforte PT, Hirata H, Han SW, Hsu YT et al. Endoplasmic reticulum calcium release engages Bax translocation in cortical astrocytes. Neurochem Res 2011; 36: 829-838.
34. Peixoto PM, Lue JK, Ryu SY, Wroble BN, Sible JC, Kinnally KW. Mitochondrial apoptosisinduced channel (MAC) function triggers a Bax/Bak-dependent bystander effect. Am J Pathol 2011; 178: 48-54.
35. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T et al. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science (New York, NY) 2003; 300: 135-139.
36. Carvalho AC, Sharpe J, Rosenstock TR, Teles AF, Youle RJ, Smaili SS. Bax affects intracellular Ca2+ stores and induces Ca2+ wave propagation. Cell Death Differ 2004; 11: 1265-1276.
37. Oakes SA, Scorrano L, Opferman JT, Bassik MC, Nishino M, Pozzan T et al. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proce Natl Acad Sci USA 2005; 102: 105-110.
38. Niessen H, Harz H, Bedner P, Kramer K, Willecke K. Selective permeability of different connexin channels to the second messenger inositol 1,4,5-trisphosphate. J Cell Sci 2000; 113 (Part 8): 1365-1372.
39. Baumgartner HK, Gerasimenko JV, Thorne C, Ferdek P, Pozzan T, Tepikin AV et al. Calcium elevation in mitochondria is the main Ca2+ requirement for mitochondrial permeability transition pore (mPTP) opening. J Biol Chem 2009; 284: 20796-20803.
40. Sims CE, Allbritton NL. 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.