Zinc-dependent multi-conductance channel activity in mitochondria isolated from ischemic brain

Journal of Neuroscience

Volumn 26, Issue 25, 2006, Pages 6851-6862

  Bonanni, Laura ^a   Chachar, Mushtaque ^b   Jover Mengual, Teresa ^c   Li, Hongmei ^b   Jones, Adrienne ^b   Yokota, Hidenori ^c   Ofengeim, Dimitry ^c   Flannery, Richard J ^b   Miyawaki, Takahiro ^c   Cho, Chang Hoon ^b   Polster, Brian M ^d   Pypaert, Marc ^b   Hardwick, J Marie ^d   Sensi, Stefano L ^a   Zukin, R Suzanne ^c   Jonas, Elizabeth A ^b  

^a UNIVERSITY OF CHIETI   (Italy)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

BCL xL; Global ischemia; Ion channels; Mitochondria; Programmed cell death; Zinc

Indexed keywords

ANION CHANNEL; EDETATE CALCIUM; ETHYLENEDIAMINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN BCL XL; RECOMBINANT PROTEIN; TETRAKIS (2 PYRIDYLMETHYL)ETHYLENEDIAMINE; UNCLASSIFIED DRUG; ZINC ION; CASPASE; CHELATING AGENT; DIAGNOSTIC AGENT; ETHYLENEDIAMINE DERIVATIVE; ION CHANNEL; N,N,N',N' TETRAKIS(2 PYRIDYLMETHYL)ETHYLENEDIAMINE; N,N,N',N'-TETRAKIS(2-PYRIDYLMETHYL)ETHYLENEDIAMINE; RHODZIN 3; RHODZIN-3; XANTHENE DERIVATIVE; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CHANNEL GATING; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; ION TRANSPORT; MALE; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; CELL MEMBRANE POTENTIAL; CLASSIFICATION; COMPARATIVE STUDY; DIAGNOSTIC IMAGING; DOSE RESPONSE; DRUG EFFECT; METABOLISM; METHODOLOGY; MITOCHONDRION; PATCH CLAMP; PATHOLOGY; PHYSIOLOGY; RADIATION EXPOSURE; SPRAGUE DAWLEY RAT; SYNAPTOSOME; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN ISCHEMIA; CASPASES; CHELATING AGENTS; DIAGNOSTIC IMAGING; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHYLENEDIAMINES; ION CHANNEL GATING; ION CHANNELS; MALE; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NAD; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTOSOMES; XANTHENES; ZINC;

EID: 33745790340     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5444-05.2006     Document Type: Article

References (97)

1. Aizenman E, Stout AK, Hartnett KA, Dineley KE, McLaughlin B, Reynolds IJ (2000) Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release. J Neurochem 75:1878-1888.
2. Alkayed NJ, Goto S, Sugo N, Joh HD, Klaus J, Crain BJ, Bernard O, Traystman RJ, Hurn PD (2001) Estrogen and Bcl-2: gene induction and effect of transgene in experimental stroke. J Neurosci 21:7543-7550.
3. 2+. J Biol Chem 260:2719-2727.
4. 2+ from brain tissue during activity. Nature 308:734-736.
5. Banasiak KJ, Xia Y, Haddad GG (2000) Mechanisms underlying hypoxia-induced neuronal apoptosis. Prog Neurobiol 62:215-249.
6. Basañez G, Sharpe JC, Galanis J, Brandt TA, Hardwick JM, Zimmerber J (2002) Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 277:49360-49365.
7. Boise LH, González-Garcia M, Postema CE, Ding L, Lindstein T, Turka LA, Mao X, Nûñez G, Thompson CB (1993) bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608.
8. Bolay H, Gursoy-Ozdemir Y, Sara Y, Onur R, Can A, Dalkara T (2002) Persistent defect in transmitter release and synapsin phosphorylation in cerebral cortex after transient moderate ischemic injury. Stroke 33:1369-1375.
9. + channels. Neuron 41:351-365.
10. Calderone A, Jover T, Noh KM, Tanaka H, Yokota H, Lin Y, Grooms SY, Regis R, Bennett MV, Zukin RS (2003) Ischemic insults derepress the gene silencer REST in neurons destined to die. J Neurosci 23:2112-2121.
11. Calderone A, Jover T, Mashiko T, Noh K-M, Tanaka H, Bennett MVL, Zukin RS (2004) Late calcium EDTA rescues hippocampal CA1 neurons from global ischemia-induced death. J Neurosci 24:9903-9913.
12. Cheng EH, Wei MC, Weiler S, Flavell RA, Mak TW, Lindsten T, Korsmeyer SJ (2001) BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell 8:705-711.
13. Cheng EHY, Kirsch DG, Clem RJ, Ravi R, Kastan MB, Bedi A, Ueno K, Hardwick JM (1997) Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278:1966-1968.
14. Choi DW (1994) Calcium and excitotoxic neuronal injury. Ann NY Acad Sci 747:162-171.
15. Choi DW, Koh JY (1998) Zinc and brain injury. Annu Rev Neurosci 21:347-375.
16. L through caspase interaction. Proc Natl Acad Sci USA 95:554-559.
17. Colbourne F, Sutherland GR, Auer RN (1999) Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J Neurosci 19:4200-4210.
18. Colombini M, Blachly-Dyson E, Forte M (1996) VDAC, a channel in the outer mitochondrial membrane. Ion Channels 4:169-202.
19. Condorelli F, Salomoni P, Cotteret S, Cesi V, Srinivasula SM, Elnemri ES, Calabretta B (2001) Caspase cleavage enhances the apoptosis-inducing effects of BAD. Mol Cell Biol 21:3025-3036.
20. Dallas M, Deuchars SA, Deuchars J (2005) Immunopharmacology: antibodies for specific modulation of proteins involved in neuronal function. J Neurosci Methods 146:133-148.
21. Danscher G, Jensen KB, Frederickson CJ, Kemp K, Andreasen A, Juhl S, Stoltenberg M, Ravid R (1997) Increased amount of zinc in the hippocampus and amygdala of Alzheimer's diseased brains: a proton-induced X-ray emission spectroscopic analysis of cryostat sections from autopsy material. J Neurosci Methods 76:53-59.
22. De Giorgi F, Lartigue L, Bauer MK, Schubert A, Grimm S, Hanson GT, Remington SJ, Youle RJ, Ichas F (2002) The permeability transition pore signals apoptosis by directing Bax translocation and multimerization. FASEB J 16:607-609.
23. Dejean LM, Martinez-Caballero S, Guo L, Hughes C, Teijido O, Ducret T, Ichas F, Korsmeyer SJ, Antonsson B, Jonas EA, Kinnally KW (2005) Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel. Molec Biol Cell 16:2424-2432.
24. Fiskum G, Rosenthal RE, Vereczki V, Martin E, Hoffman GE, Chinopoulos C, Kowaltowski A (2004) Protection against ischemic brain injury by inhibition of mitochondrial oxidative stress. J Bioenerg Biomem 36:347-352.
25. Fleidervish IA, Gebhardt C, Astman N, Gutnick MJ, Heinemann U (2001) Enhanced spontaneous transmitter release is the earliest consequence of neocortical hypoxia that can explain the disruption of normal circuit function. J Neurosci 21:4600-4608.
26. Frederickson CJ, Danscher G (1990) Zinc-containing neurons in hippocampus and related CNS structures. Prog Brain Res 83:71-84.
27. Frederickson CJ, Manton WI, Frederickson MH, Howell GA, Mallory MA (1982) Stable-isotope dilution measurement of zinc and lead in rat hippocampus and spinal cord. Brain Res 246:338-341.
28. Frederickson CJ, Suh SW, Koh JY, Cha YK, Thompson RB, LaBuda CJ, Balaji RV, Cuajungco MP (2002) Depletion of intracellular zinc from neurons by use of an extracellular chelator in vivo and in vitro. J Histochem Cytochem 50:1659-1662.
29. Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25:319-324.
30. Fujita N, Nagahashi A, Nagashima K, Rokudai S, Tsuruo T (1998) Acceleration of apoptotic cell death after the cleavage of Bcl-xL protein by caspase-3-like proteases. Oncogene 17:1295-1304.
31. González-Garcia M, Garcia I, Ding L, O'Shea S, Boise LH, Thompson CB, Nunez G (1995) Bcl-x is expressed in embryonic and postnatal neural tissues and functions to prevent neuronal cell death. Proc Natl Acad Sci USA 92:4304-4309.
32. Gottlieb E, Armour SM, Thompson CB (2002) Mitochondrial respiratory control is lost during growth factor deprivation. Proc Natl Acad Sci USA 99:12801-12806.
33. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626-629.
34. Hackenbrock CR (1966) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J Cell Biol 30:269-297.
35. Halestrap A (2005) A pore way to die. Nature 434:578-579.
36. Hille B (2001) Ion channel of excitable membranes, Ed 2, pp 351-352. Sunderland, MA: Sinauer.
37. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770-776.
38. Honkaniemi J, Massa SM, Breckinridge M, Sharp FR (1996) Global ischemia induces apoptosis-associated genes in hippocampus. Brain Res Mol Brain Res 42:79-88.
39. Howard EM, Gao TM, Pulsinelli WA, Xu ZC (1998) Electrophysiological changes of CA3 neurons and dentate granule cells following transient forebrain ischemia. Brain Res 798:109-118.
40. Hunter DR, Haworth RA, Southard JH (1976) Relationship between configuration, function and permeability in calcium-treated mitochondria. J Biol Chem 251:5069-5077.
41. 2+ induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria. J Biol Chem 276:47524-47529.
42. Jonas EA, Buchanan J, Kaczmarek LK (1999) Prolonged activation of mitochondrial conductances during synaptic transmission. Science 286:1347-1350.
43. Jonas EA, Hoit D, Hickman JA, Brandt TA, Polster BM, Fannjiang Y, McCarthy E, Montanez MK, Hardwick JM, Kaczmarek LK (2003) Modulation of synaptic transmission by the BCL-2 family protein BCL-xL. J Neurosci 23:8423-8431.
44. Jonas EA, Hickman JA, Chachar M, Polster BM, Brandt TA, Fannjiang Y, Ivanovska I, Basañez G, Kinnally KW, Zimmerberg J, Hardwick JM, Kaczmarek LK (2004) Proapoptotic N-truncated BCL-xL protein activates endogenous mitochondrial channels in living synaptic terminals. Proc Natl Acad Sci USA 101:13590-13595.
45. Jonas EA, Hickman JA, Hardwick JM, Kaczmarek LK (2005) Exposure to hypoxia rapidly induces mitochondrial channel activity within a living synapse. J Biol Chem 280:4491-4497.
46. Kaufmann T, Schlipf S, Sanz J, Neubert K, Stein R, Borner C (2003) Characterization of the signal that directs Bcl-x(L), but not Bcl-2, to the mitochondrial outer membrane. J Cell Biol 160:53-64.
47. Kay AR (2003) Evidence for chelatable zinc in the extracellular space of the hippocampus, but little evidence for synaptic release of Zn. J Neurosci 23:6847-6855.
48. Kim JS, He L, Lemasters JJ (2003) Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 304:463-470.
49. Kinnally KW, Campo ML, Tedeschi H (1989) Mitochondrial channel activity studied by patch-clamping mitoplasts. J Bioenerg Biomembr 21:497-506.
50. Kirino T (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239:57-69.
51. Koh J-Y, Suh SW, Gwag BJ, He YY, Hsu CY, Choi DW (1996) The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272:1013-1016.
52. Krajewska M, Rosenthal RE, Mikolajczyk J, Stennicke HR, Wiesenthal T, Mai J, Naito M, Salvesen GS, Reed JC, Fiskum G, Krajewski S (2004) Early processing of Bid and caspase-6, -8, -10, -14 in the canine brain during cardiac arrest and resuscitation. Exp Neurol 189:261-279.
53. Krajewski S, Krajewska M, Shabaik A, Wang HG, Irie S, Fong L, Reed JC (1994) Immunohistochemical analysis of in vivo patterns of bcl-x expression. Cancer Res 54:5501-5507.
54. Kroemer G, Reed JC (2000) Mitochondrial control of cell death. Nat Med 6:513-519.
55. Lee AC, Zizi M, Colombini M (1994) Beta-NADH decreases the permeability of the mitochondrial outer membrane to ADP by a factor of 6. J Biol Chem 269:30974-30980.
56. Lee JM, Zipfel GJ, Choi DW (1999) The changing landscape of ischaemic brain injury mechanisms. Nature [Suppl] 399:A7-A14.
57. Lee JY, Cole TB, Palmiter RD, Koh JY (2000) Accumulation of zinc in degenerating hippocampal neurons of ZnT3-null mice after seizures: evidence against synaptic vesicle origin. J Neurosci 20:RC79(1-5).
58. Lehninger AL (1982) Principles of biochemistry. New York: Worth.
59. Li H, Zhu H, Xu C, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491-501.
60. 2+ from presynaptic terminals into postsynaptic hippocampal neurons after physiological stimulation. J Neurophysiol 86:2597-2604.
61. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568.
62. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X (1998) Bid, a Bcl-2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481-490.
63. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC, Kroemer G (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281:2027-2031.
64. Nakagawa T, Yuan J (2000) Cross-talk between two cysteine protease families: activation of caspase-12 by calpain in apoptosis. J Cell Biol 150:887-894.
65. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80:315-360.
66. Nishizawa Y (2001) Glutamate release and neuronal damage in ischemia. Life Sci 69:369-381.
67. Northington FJ, Ferriero DM, Flock DL, Martin LJ (2001) Delayed neurodegeneration in neonatal rat thalamus after hypoxia-ischemia is apoptosis. J Neurosci 21:1931-1938.
68. Ouyang YB, Tan Y, Comb M, Liu CL, Martone ME, Siesjo BK, Hu BR (1999) Survival- and death-promoting events after transient cerebral ischemia: phosphorylation of Akt, release of cytochrome. c and activation of caspase-like proteases. J Cereb Blood Flow Metab 19:1126-1135.
69. Pavlov EV, Priault M, Pietkiewicz D, Cheng EHY, Antonsson B, Manon S, Korsmeyer SJ, Mannella CA, Kinnally KW (2001) A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. J Cell Biol 155:725-731.
70. Petronilli V, Szabo I, Zoratti M (1989) The inner mitochondrial membrane contains ion-conducting channels similar to those found in bacteria. FEBS Lett 259:137-143.
71. Pozarowski P, Huang X, Halicka DH, Lee B, Johnson G, Darzynkiewicz Z (2003) Interactions of fluorochrome-labeled caspase inhibitors with apoptotic cells: a caution in data interpretation. Cytometry A 55:50-60.
72. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491-498.
73. Sattler R, Tymianski M (2000) Molecular mechanisms of calcium-dependent excitotoxicity. J Mol Med 78:3-13.
74. 2+ in ischemic neuronal injury. Curr Mol Med 4:87-111.
75. 2+-permeable AMPA/kainate channels triggers prolonged mitochondrial superoxide production. Proc Natl Acad Sci USA 96:2414-2419.
76. 2+ uptake and persistent mitochondrial dysfunction. Eur J Neurosci 12:3813-3818.
77. 2+ pools. Proc Natl Acad Sci USA 100:6157-6162.
78. Sensi SL, Ton-That D, Weiss JH, Rothe A, Gee KR (2003b) A new mitochondrial fluorescent zinc sensor. Cell Calcium 34:281-284.
79. Sugawara T, Fujimura M, Morita-Fujimura Y, Kawase M, Chan PH (1999) Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient global cerebral ischemia. J Neurosci 19:RC39(1-6).
80. Sullivan PG, Rabchevsky AG, Keller JN, Lovell M, Sodhi A, Hart RP, Scheff SW (2004) Intrinsic differences in brain and spinal cord mitochondria: Implication for therapeutic interventions. J Comp Neurol 474:524-534.
81. Szabo I, Zoratti M (1991) The giant channel of the inner mitochondrial membrane is inhibited by cyclosporine A. J Biol Chem 266:3376-3379.
82. Tanaka H, Calderone A, Jover T, Grooms SY, Yokota H, Zukin RS, Bennett MVL (2002) Ischemic preconditioning acts upstream of GluR2 downregulation to afford neuroprotection in the hippocampal CA1. Proc Natl Acad Sci USA 99:2362-2367.
83. Tanaka H, Yokota H, Jover T, Cappuccio I, Calderone A, Simionescu M, Bennett MVL, Zukin RS (2004) Ischemic preconditioning: neuronal survival in the face of caspase-3 activation. J Neurosci 24:2750-2759.
84. Tedeschi H, Kinnally KW (1987) Channels in the mitochondrial outer membrane: evidence from patch clamp studies. J Bioenerg Biomembr 19:321-327.
85. Tedeschi H, Kinnally KW, Mannella CA (1989) Properties of channels in the mitochondrial outer membrane. J Bioenerg Biomembr 21:451-459.
86. Tian GF, Baker AJ (2000) Glycolysis prevents anoxia-induced synaptic transmission damage in rat hippocampal slices. J Neurophysiol 83:1830-1839.
87. Tonder N, Johansen FF, Frederickson CJ, Zimmer J, Diemer NH (1990) Possible role of zinc in the selective degeneration of dentate hilar neurons after cerebral ischemia in the adult rat. Neurosci Lett 109:247-252.
88. Vander Heiden MG, Chandel NS, Li XX, Schumacker PT, Colombini M, Thompson CB (2000) Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc Natl Acad Sci USA 97:4666-4667.
89. Vyssokikh MY, Zorova L, Zorov D, Heimlich G, Jurgensmeier JJ, Brdiczka D (2002) Bax releases cytochrome c preferentially from a complex between porin and adenine nucleotide translocator. Hexokinase activity suppresses this effect. Mol Biol Rep 29:93-96.
90. +-ATPase activity as a mechanism of neuronal death mediated by concurrent ATP deficiency and oxidant stress. J Cell Sci 116:2099-2110.
91. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727-730.
92. 2+ permeable AMPA or kainate receptors: Possible key factors in selective neurodegeneration. Trends Neurosci 23:365-371.
93. Wolter KG, Hsu Y-T, Smith CL, Nechushtan A, Xi X-G, Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139:1281-1292.
94. Wood DE, Newcomb EW (2000) Cleavage of Bax enhances its cell death function. Exp Cell Res 256:375-382.
95. 2+ accumulation and neuronal loss in hippocampal pyramidal neurons. J Neurosci 22:1273-1279.
96. Zhu Y, Prehn JH, Culmsee C, Krieglstein J (1999) The beta2-adrenoceptor agonist clenbuterol modulates Bcl-2, Bcl-xl and Bax protein expression following transient forebrain ischemia. Neuroscience 90:1255-1263.
97. Zukin RS, Jover T, Yokota H, Calderone A, Simionescu M, Lau C-Y (2004) Molecular and cellular mechanisms of ischemia-induced neuronal death. In: Stroke: pathophysiology, diagnosis, and management (Mohr JP, Choi DW, Grotta JC, Weir B, Wolf PA, eds), pp 829-854. Philadelphia: Churchill Livingstone.