Probing the outer mitochondrial membrane in cardiac mitochondria with nanoparticles

Biophysical Journal

Volumn 92, Issue 3, 2007, Pages 1058-1071

  Salnikov, V ^a,c   Lukyanenko Y O ^b   Frederick, C A ^a   Lederer, W J ^a   Lukyánenko, Valériy ^a  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c KAZAN INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; ANION CHANNEL; GREEN FLUORESCENT PROTEIN; NANOPARTICLE; POLYANION; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HEART MITOCHONDRION; MALE; MITOCHONDRIAL MEMBRANE; NONHUMAN; RAT;

RATTUS;

EID: 33846805632     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.094318     Document Type: Article

References (64)

1. Rostovtseva, T. K., W. Tan, and M. Colombini. 2005. On the role of VDAC in apoptosis: fact and fiction. J. Bioenerg. Biomembr. 37:129-142.
2. Tsujimoto, Y., T. Nakagawa, and S. Shimizu. 2006. Mitochondrial membrane permeability transition and cell death. Biochim. Biophys. Acta. 1757:1297-1300.
3. Parfenov, A. S., V. Salnikov, W. J. Lederer, and V. Lukyanenko. 2006. Aqueous diffusion pathways as a part of the ventricular cell ultrastructure. Biophys. J. 90:1107-1119.
4. Mannella, C. A. 1998. Conformational changes in the mitochondrial channel protein, VDAC, and their functional implications. J. Struct. Biol. 121:207-218.
5. Zoratti, M., and I. Szabo. 1995. The mitochondrial permeability transition. Biochim. Biophys. Acta. 1241:139-176.
6. Crompton, M. 1999. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341:233-249.
7. Vyssokikh, M., and D. Brdiczka. 2004. VDAC and peripheral channeling complexes in health and disease. Mol. Cell. Biochem. 256:117-126.
8. Pavlov, E. V., M. Priault, D. Pietkiewicz, E. H. Cheng, B. Antonsson, S. Manon, S. J. Korsmeyer, C. A. Mannella, and K. W. Kinnally. 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.
9. Guo, L., D. Pietkiewicz, E. V. Pavlov, S. M. Grigoriev, J. J. Kasianowicz, L. M. Dejean, S. J. Korsmeyer, B. Antonsson, and K. W. Kinnally. 2004. Effects of cytochrome c on the mitochondrial apoptosis-induced channel MAC. Am. J. Physiol. Cell Physiol. 286:C1109-C1117.
10. Siskind, L. J., A. Davoody, N. Lewin, S. Marshall, and M. Colombini. 2003. Enlargement and contracture of C2-ceramide channels. Biophys. J. 85:1560-1575.
11. Siskind, L. J., R. N. Kolesnick, and M. Colombini. 2006. Ceramide forms channels in mitochondrial outer membranes at physiologically relevant concentrations. Mitochondrion. 6:118-125.
12. Zamzami, N., and G. Kroemer. 2001. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell Biol. 2:67-71.
13. Brustovetsky, N., T. Brustovetsky, R. Jemmerson, and J. M. Dubinsky. 2002. Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J. Neurochem. 80:207-218.
14. Halestrap, A. 2005. A pore way to die. Nature. 434:578-579.
15. Mannella, C. A. 2006. The relevance of mitochondrial membrane topology to mitochondrial function. Biochim. Biophys. Acta. 1762:140-147.
16. Hill, K., K. Model, M. T. Ryan, K. Dietmeier, F. Martin, R. Wagner, and N. Pfanner. 1998. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature. 395:516-521.
17. Schwartz, M. P., and A. Matouschek. 1999. The dimensions of the protein import channels in the outer and inner mitochondrial membranes. Proc. Natl. Acad. Sci. USA. 96:13086-13090.
18. Schein, S. J., M. Colombini, and A. Finkelstein. 1976. Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from Paramecium mitochondria. J. Membr. Biol. 30:99-120.
19. Colombini, M., C. L. Yeung, J. Tung, and T. König. 1987. The mitochondrial outer membrane channel, VDAC, is regulated by a synthetic polyanion. Biochim. Biophys. Acta. 905:279-286.
20. Colombini, M. 2004. VDAC: the channel at the interface between mitochondria and the cytosol. Mol. Cell. Biochem. 256/257:107-115.
21. Mannella, C. A. 1992. The 'ins' and 'outs' of mitochondrial membrane channels. Trends Biochem. Sci. 17:315-320.
22. Lemasters, J. J., and E. Holmuhamedov. 2006. Voltage-dependent anion channel (VDAC) as mitochondrial governator. Thinking outside the box. Biochim. Biophys. Acta. 1762:181-190.
23. Guo, X. W., P. R. Smith, B. Cognon, D. D'Arcangelis, E. Dolginova, and C. A. Mannella. 1995. Molecular design of the voltage-dependent, anion-selective channel in the mitochondrial outer membrane. J. Struct. Biol. 114:41-59.
24. Yehezkel, G., N. Hadad, H. Zaid, S. Sivan, and V. Shoshan-Barmatz. 2006. Nucleotide-binding sites in the voltage-dependent anion channel: characterization and localization. J. Biol. Chem. 281:5938-5946.
25. Anflous, K., O. Blondel, A. Bernard, M. Khrestchatisky, and R. Ventura-Clapier. 1998. Characterization of rat porin isoforms: cloning of a cardiac type-3 variant encoding an additional methionine at its putative N-terminal region. Biochim. Biophys. Acta. 1399:47-50.
26. Komarov, A. G., D. Deng, W. J. Craigen, and M. Colombini. 2005. New insights into the mechanism of permeation through large channels. Biophys. J. 89:3950-3959.
27. Carneiro, C. M., P. G. Merzlyak, L. N. Yuldasheva, L. G. Silva, F. P. Thinnes, and O. V. Krasilnikov. 2003. Probing the volume changes during voltage gating of Porin 31BM channel with nonelectrolyte polymers. Biochim. Biophys. Acta. 1612:144-153.
28. Shoshan-Barmatz, V., and A. Israelson. 2005. The voltage-dependent anion channel in endoplasmic/sarcoplasmic reticulum: characterization, modulation and possible function. J. Membr. Biol. 204:57-66.
29. Madesh, M., and G. Hajnoczky. 2001. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J. Cell Biol. 155:1003-1015.
30. Borutaite, V., A. Jekabsone, R. Morkuniene, and G. C. Brown. 2003. Inhibition of mitochondrial permeability transition prevents mitochondrial dysfunction, cytochrome c release and apoptosis induced by heart ischemia. J. Mol. Cell. Cardiol. 35:357-366.
31. Krauskopf, A., O. Eriksson, W. J. Craigen, M. A. Forte, and P. Bernardi. 2006. Properties of the permeability transition in VDAC1-/-mitochondria. Biochim. Biophys. Acta. 1757:590-605.
32. Zalk, R., A. Israelson, E. S. Garty, H. Azoulay-Zohar, and V. Shoshan-Barmatz. 2005. Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria. Biochem. J. 386:73-83.
33. Brenner, C., and G. Kroemer. 2000. Apoptosis. Mitochondria - the death signal integrators. Science. 289:1150-1151.
34. Elrick, M. J., S. Fluss, and M. Colombini. 2006. Sphingosine, a product of ceramide hydrolysis, influences the formation of ceramide channels. Biophys. J. 91:1749-1756.
35. Gross, A., J. Jockel, M. C. Wei, and S. J. Korsmeyer. 1998. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17:3878-3885.
36. Vergun, O., T. V. Votyakova, and I. J. Reynolds. 2003. Spontaneous changes in mitochondrial membrane potential in single isolated brain mitochondria. Biophys. J. 85:3358-3366.
37. 2+ waves in saponin-permeabilized cardiac myocytes. J. Physiol. 521:575-585.
38. + currents responsible for repolarization in mouse ventricle and their modulation by FK-506 and rapamycin. Am. J. Physiol. Heart Circ. Physiol. 278:H886-H897.
39. Peachey, L. D. 1964. Electron Microscopic observations on the accumulation of divalent cations in intramitochondrial granules. J. Cell Biol. 20:95-111.
40. Fawcett, D. W., and N. S. McNutt. 1969. The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J. Cell Biol. 42:1-45.
41. De Roe, C., P. J. Courtoy, and P. Baudhuin. 1987. A model of protein-colloidal gold interactions. J. Histochem. Cytochem. 35:1191-1198.
42. Franzini-Armstrong, C. 1971. Studies of the triad. II. Penetration of tracers into the junctional gap. J. Cell Biol. 49:196-203.
43. Hayat, M. A. 1986. Glutaraldehyde: role in electron microscopy. Micron and Microscopica Acta. 17:115-135.
44. Konstantinova, S. A., C. A. Mannella, V. P. Skulachev, and D. B. Zorov. 1995. Immunoelectron microscopic study of the distribution of porin on outer membranes of rat heart mitochondria. J. Bioenerg. Biomembr. 27:93-99.
45. Maunsbach, A. B., and B. A. Afzelius. 1999. Biomedical Electron Microscopy. Academic Press, New York.
46. 2+. Biophys. J. 88:2174. (Abstr.)
47. Gincel, D., H. Zaid, and V. Shoshan-Barmatz. 2001. Calcium binding and translocation by the voltage-dependent anion channel: a possible regulatory mechanism in mitochondrial function. Biochem. J. 358:147-155.
48. Gizatullina, Z. Z., Y. Chen, S. Zierz, and F. N. Gellerich. 2005. Effects of extramitochondrial ADP on permeability transition of mouse liver mitochondria. Biochim. Biophys. Acta. 1706:98-104.
49. Gostimskaya, I. S., V. G. Grivennikova, T. V. Zharova, L. E. Bakeeva, and A. D. Vinogradov. 2003. In situ assay of the intramitochondrial enzymes: use of alamethicin for permeabilization of mitochondria. Anal. Biochem. 313:46-52.
50. Bechinger, B. 1999. The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta. 1462:157-183.
51. Blondin, G. A., and D. E. Green. 1967. The mechanism of mitochondrial swelling. Proc. Natl. Acad. Sci. USA. 58:612-619.
52. Yang, F., L. G. Moss, and G. N. Phillips, Jr. 1996. The molecular structure of green fluorescent protein. Nat. Biotechnol. 14:1246-1251.
53. König, T., B. Kocsis, L. Meszaros, K. Nahm, S. Zoltan, and I. Horvath. 1977. Interaction of a synthetic polyanion with rat liver mitochondria. Biochim. Biophys. Acta. 462:380-389.
54. Bathori, G., I. Szabo, I. Schmehl, F. Tombola, A. Messina, V. De Pinto, and M. Zoratti. 1998. Novel aspects of the electrophysiology of mitochondrial porin. Biochem. Biophys. Res. Commun. 243:258-263.
55. Szabo, I., P. Bernardi, and M. Zoratti. 1992. Modulation of the mitochondrial megachannel by divalent cations and protons. J. Biol. Chem. 267:2940-2946.
56. 2+ cycling in isolated rat cardiac mitochondria. Biophys. J. 86:108a. (Abstr.)
57. Sau, T. K., A. Pal, N. R. Jana, Z. L. Wang, and T. Pal. 2001. Size controlled synthesis of gold nanoparticles using photochemically prepared seed particles. J. Nanoparticle Res. 3:257-261.
58. Margoliash, E. 1963. Primary structure and evolution of cytochrome C. Proc. Natl. Acad. Sci. USA. 50:672-679.
59. Feldherr, C. M., and J. M. Marshall. 1962. The use of colloidal gold for studies of intracellular exchanges in the ameba Chaos chaos. J. Cell Biol. 12:640-645.
60. Feldherr, C. M. 1962. The intracellular distribution of ferritin following microinjection. J. Cell Biol. 12:159-167.
61. Richter, G. W. 1959. The cellular transformation of injected colloidal iron complexes into ferritin and hemosiderin in experimental animals; a study with the aid of electron microscopy. J. Exp. Med. 109:197-216.
62. Kongas, O., M. J. Wagner, F. ter Veld, K. Nicolay, J. H. van Beek, and K. Krab. 2004. The mitochondrial outer membrane is not a major diffusion barrier for ADP in mouse heart skinned fibre bundles. Pflugers Arch. 447:840-844.
63. Pastorino, J. G., and J. B. Hoek. 2003. Hexokinase II: the integration of energy metabolism and control of apoptosis. Curr. Med. Chem. 10:1535-1551.
64. Bustamante, J. O., E. R. Michelette, J. P. Geibel, J. A. Hanover, T. J. McDonnell, and D. A. Dean. 2000. Dendrimer-assisted patch-clamp sizing of nuclear pores. Pflugers Arch. 439:829-837.