Synthetic and natural polyanions induce cytochrome c release from mitochondria in vitro and in situ

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 5, 2011, Pages

  Krasnikov, Boris F ^a,b   Melik Nubarov, Nickolay S ^a   Zorova, Lubava D ^a   Kuzminova, Alevtina E ^a   Isaev, Nickolay K ^a   Cooper, Arthur J L ^b   Zorov, Dmitry B ^a,b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Permeability transition; Viral RNA

Indexed keywords

CALCIUM; CARDIOLIPIN; CYCLOSPORIN A; CYTOCHROME C; FLUORESCEIN; MALEIC ANHYDRIDE; METHACRYLIC ACID; PHOSPHATIDYLCHOLINE; POLYANION; STYRENE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CYTOSOL; LIVER MITOCHONDRION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ASTROCYTES; CALCIUM; CELL DEATH; CELL RESPIRATION; CEREBELLUM; CYCLOSPORINE; CYTOCHROMES C; LIPOSOMES; MITOCHONDRIA, LIVER; MITOCHONDRIAL SWELLING; POLYMERS; RATS; RATS, WISTAR;

RATTUS; TOBACCO MOSAIC VIRUS;

EID: 79955564357     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00519.2009     Document Type: Article

References (62)

1. Abdullaev ZKh Bodrova ME, Chernyak BV, Dolgikh DA, Kluck RM, Pereverzev MO, Arseniev AS, Efremov RG, Kirpichnikov MP, Mokhova EN, Newmeyer DD, Roder H, Skulachev VP. A cytochrome c mutant with high electron transfer and antioxidant activities but devoid of apoptogenic effect. Biochem J 362: 749-754, 2002.
2. Alakhova DY, Rapoport NY, Batrakova EV, Timoshin AA, Li S, Nicholls D, Alakhov VY, Kabanov AV. Differential metabolic responses to pluronic in MDR and non-MDR cells: a novel pathway for chemosensitization of drug resistant cancers. J Control Release 142: 89-100, 2010.
3. Andreyev AY, Fahy B, Fiskum G. Cytochrome c release from brain mitochondria is independent of the mitochondrial permeability transition. FEBS Lett 439: 373-376, 1998.
4. Antonsson B, Montessuit S, Sanchez B, Martinou JC. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276: 11615-11623, 2001.
5. Ballou D, Palmer C, Massey Y. Direct demonstration of superoxide anion production during the oxidation of reduced flavin and of its catalytic decomposition by erythrocuprein. Biochem Biophys Res Commun 36: 898-904, 1969.
6. Butler J, Jayson GG, Swallow AJ. The reaction between the superoxide anion radical and cytochrome c. Biochim Biophys Acta 408: 215-222, 1975.
7. Bruer U, Weih MK, Isaev NK, Meisel A, Ruscher K, Bergk A, Trendelenburg G, Wiegand F, Victorov IV, Dirnagl U. Induction of tolerance in rat cortical neurons: hypoxic preconditioning. FEBS Lett 414: 117-121, 1997.
8. Cantor CR, Schimmel PR. Biophysical Chemistry. San Francisco, CA: Freeman, 1980.
9. Chance B. Techniques for the assay of the respiratory enzymes. Methods Enzymol 4: 273-329, 1957.
10. Chang DD, Clayton DA. Mouse RNAase MRP RNA is encoded by a nuclear gene and contains a decamer sequence complementary to a conserved region of mitochondrial RNA substrate. Cell 56: 131-139, 1989.
11. Colombini M, Yeung CL, Tungm J, König T. The mitochondrial outer membrane channel, VDAC, is regulated by a synthetic polyanion. Biochim Biophys Acta 905: 279-286, 1987.
12. Doménech Ó, Redondo L, Montero MT, Hernández-Borrell J. Specific adsorption of cytochrome c on cardiolipin-glycerophospholipid monolayers and bilayers. Langmuir 23: 5651-5656, 2007.
13. Erecinska M, Vanderkooi JM, Wilson DF. Cytochrome c interactions with membranes. A photoaffinity-labeled cytochrome c. Arch Biochem Biophys 171: 108-116, 1975.
14. Estabrook RW. The low temperature spectra of hemoproteins. J Biol Chem 223: 781-794, 1956.
15. Gulik-Krzywicki T, Shechter E, Luzzati V, Faure M. Interactions of proteins and lipids: structure and polymorphism of protein-lipid-water phases. Nature 223: 1116-1121, 1969.
16. Hattori T, Nishimura Y, Sakai N, Yamada H, Kawai K, Nozawa Y. Effect of cytochrome c on formation of lipid peroxides in rat brain in vitro. Free Radic Res Commun 4: 41-49, 1987.
17. Hildebrandt P. Polyanion binding to cytochrome c probed by resonance Raman spectroscopy. Biochim Biophys Acta 1040: 175-186, 1990.
18. Hüser J, Rechenmacher CE, Blatter LA. Imaging the permeability pore transition in single mitochondria. Biophys J 74: 2129-2137, 1998.
19. Ilan Y, Shafferman A, Feinberg BA, Lau YK. Partitioning of electrostatic and conformational contributions in the redox reactions of modified cytochromes c. Biochim Biophys Acta 548: 565-578, 1979.
20. Jackson KL, Pace N. Some permeability properties of isolated rat liver cell mitochondria. J Gen Physiol 40: 47-71, 1956.
21. Kadenbach B. Der Einfluss von Thyreoidhormonen in vivo auf die oxidative phosphorylierung und Enzymaktivitaten in Mitochondrien. Biochem Z 344: 49-75, 1966.
22. Kalanxhi E, Wallace CJ. Cytochrome c impaled: investigation of the extended lipid anchorage of a soluble protein to mitochondrial membrane models. Biochem J 407: 179-187, 2007.
23. Kolesnikova OA, Entelis NS, Mireau H, Fox TD, Martin Tarassov IA RP. Suppression of mutations in mitochondrial DNA by tRNAs imported from the cytoplasm. Science 289: 1931-1933, 2000.
24. König T, Kocsis B, Mészáros L, Nahm K, Zoltán S, Horváth I. Interaction of a synthetic polyanion with rat liver mitochondria. Biochim Biophys Acta 462: 380-389, 1977.
25. Krasnikov BF, Zorov DB, Antonenko YN, Zaspa AA, Kulikov IV, Kristal BS, Cooper AJL, Brown AM. Comparative kinetic analysis reveals that inducer-specific ion release precedes the mitochondrial permeability transition. Biochim Biophys Acta 1708: 375-392, 2005.
26. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157, 1996.
27. Mahler HR, Perlman PS. Mitochondriogenesis analyzed by blocks on mitochondrial translation and transcription. Biochemistry 10: 2979-2990, 1971.
28. Mao M, Kim C, Wi S, Turner SR. Chain structure of substituted stilbene-maleic anhydride alternating copolymer probed by solid-state NMR. Macromolecules 41: 387-389, 2008.
29. Martin MM, Jensen NP. Alternation copolymerization. J Org Chem 27: 1201-1205, 1962.
30. Martinou JC, Desagher S, Antonsson B. Cytochrome c release from mitochondria: all or nothing. Nat Cell Biol 2: E41-E43, 2000.
31. Mateu L, Caron F, Luzzati V, Billecocq A. The influence of proteinlipid interactions on the order-disorder conformational transitions of the hydrocarbon chain. Biochim Biophys Acta 508: 109-121, 1978.
32. Minakami S, Mokhova EN. Spectrum of cytochromes and verdoperoxisase in intact leucocytds. J Biochem 64: 561-562, 1968.
33. McMillin JB, Dowhan W. Cardiolipin and apoptosis. Biochem Biophys Acta 1585: 97-107, 2002.
34. Nicholls P. Cytochrome c binding to enzymes and membranes. Biochim Biophys Acta 346: 261-310, 1974.
35. Ott M, Robertson J, Gogvadze V, Zhivotovsky B, Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci USA 99: 1259-1263, 2002.
36. Ow YP, Green DR, Hao Z, Mak TW. Cytochrome c: functions beyond respiration. Nat Rev Mol Cell Biol 9: 532-542, 2008.
37. Petersen LC, Cox RP. The effect of complex-formation with polyanions on the redox properties of cytochrome c. Biochem J 192: 687-693, 1980.
38. Petit PX, Goubern M, Diolez P, Susin SA, Zamzami N, Kroemer G. Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: the impact of irreversible permeability transition. FEBS Lett 426: 111-116, 1998.
39. Pious DA. Induction of cytochromes in human cells by oxygen. Proc Natl Acad Sci USA 65: 1001-1008, 1970.
40. Polster BM, Kinnally KW, Fiskum G. BH3 death domain peptide induces cell type-selective mitochondrial outer membrane permeability. J Biol Chem 276: 37887-37894, 2001.
41. Pronevich LA, Mirzabekov TA, Rozhdestvenskaya ZE. Mitochondrial porin regulates the sensitivity of anion carriers to inhibitors. FEBS Lett 247: 330-332, 1989.
42. Rong Y, Distelhorst CW. Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 70: 73-91, 2008.
43. Rytömaa M, Kinnunen PK. Evidence for two distinct acidic phospholipid-binding sites in cytochrome c. J Biol Chem 269: 1770-1774, 1994.
44. Rytömaa M, Kinnunen PK. Reversibility of the binding of cytochrome c to liposomes. Implications for lipid-protein interactions. J Biol Chem 270: 3197-3202, 1995.
45. Sahay G, Batrakova EV, Kabanov AV. Different internalization pathways of polymeric micelles and unimers and their effects on vesicular transport. Bioconjug Chem 19: 2023-2029, 2008.
46. Sato N, Hagihara B. Spectrophotometric analyses of cytochromes in ascites hepatomas of rats and mice. Cancer Res 30: 2061-2068, 1970.
47. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA, Korsmeyer SJ. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2: 55-67, 2002.
48. Sedlak E, Antalik M. Coulombic and noncoulombic effect of polyanions on cytochrome c structure. Biopolymers 46: 145-154, 1998.
49. Selishcheva AA, Obraztsov VV, Kozlov IuP. Different types of interaction of oxidized and reduced cytochrome c with phospholipid vesicles. Biochemistry (Moscow) 43: 2047-2054, 1978.
50. Shay JW, Werbin H. New evidence for the insertion of mitochondrial DNA into the human genome: significance for cancer and aging. Mutat Res 275: 227-235, 1992.
51. Skulachev VP. Why are mitochondria involved in apoptosis? Permeability transition pores and apoptosis as selective mechanisms to eliminate superoxide-producing mitochondria and cell. FEBS Lett 397: 7-10, 1996.
52. Somasundaran M, Zapp ML, Beattie LK, Pang L, Byron KS, Bassell GJ, Sullivan JL, Singer RH. Localization of HIV RNA in mitochondria of infected cells: potential role in cytopathogenicity. J Cell Biol 126: 1353-1360, 1994.
53. Szabo I, Bathori G, Tombola F, Coppola A, Schmehl I, Brini M, Ghazi A, De Pinto V, Zoratti M. Double-stranded DNA can be translocated across a planar membrane containing purified mitochondrial porin. FASEB J 12: 495-502, 1998.
54. Tarassov I, Entelis N, Martin RP. An intact protein translocating machinery is required for mitochondrial import of a yeast cytoplasmic tRNA. J Mol Biol 245: 315-323, 1995.
55. Tedeschi H, Harris DL. The osmotic behavior and permeability to non-electrolytes of mitochondria. Arch Biochem Biophys 58: 52-67, 1955.
56. Turkaly P, Kerner J, Hoppel C. A 22 kDa polyanion inhibits carnitinedependent fatty acid oxidation in rat liver mitochondria. FEBS Lett 460: 241-245, 1999.
57. Vyssokikh MY, Zorova L, Zorov D, Heimlich G, Jürgensmeier JM, Brdiczka D. Bax targets a cytochrome c fraction in rat brain mitochondria organised in a complex of porin and adenine nucleotide translocator. Hexokinase activity suppresses this effect. Mol Biol Reports 29: 93-96, 2002.
58. Yadaiah M, Rao PN, Harish P, Bhuyan AK. High affinity binding of Bcl-xL to cytochrome c: possible relevance for interception of translocated cytochrome c in apoptosis. Biochim Biophys Acta 1774: 1370-1379, 2007.
59. Yoshikawa S, Shinzawa-Itoh K, Nakashima R, Yaono R, Yamashita E, Inoue N, Yao M, Fei MJ, Libeu CP, Mizushima T, Yamaguchi H, Tomizaki T, Tsukihara T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280: 1723-1729, 1998.
60. Yu C, Yu L, King TE. Studies on cytochrome oxidase. Interactions of the cytochrome oxidase protein with phospholipids and cytochrome c. J Biol Chem 250: 1383-1392, 1975.
61. Zeng WP, Shirota Y. Studies on alternating radical copolymerization: analysis of microstructures of styrene-maleic anhydride, styrene-acrylonitrile, and styrene-methyl methacrylate copolymers by fluorescence spectroscopy. Macromolecules 22: 4204-4208, 1989.
62. Zorova LD, Krasnikov BF, Kuzminova AE, Polyakova IA, Dobrov EN, Zorov DB. Virus-induced permeability transition in mitochondria. FEBS Lett 466: 305-309, 2000.