Enlargement and contracture of C2-ceramide channels

Biophysical Journal

Volumn 85, Issue 3, 2003, Pages 1560-1575

  Siskind, Leah J ^a   Davoody, Amirparviz ^a   Lewin, Naomi ^a   Marshall, Stephanie ^a   Colombini, Marco ^a  

^a Bldg 142   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; CYTOCHROME C; LANTHANUM; DRUG DERIVATIVE; EDDA; EDETIC ACID; ION; ION CHANNEL; LIPID; N ACETYLSPHINGOSINE; N-ACETYLSPHINGOSINE; SPHINGOSINE;

APOPTOSIS; ARTICLE; MEMBRANE CHANNEL; MEMBRANE PERMEABILITY; MITOCHONDRION; NONHUMAN; PHOSPHOLIPID MEMBRANE; ARTIFICIAL MEMBRANE; BIOPHYSICS; CELL MEMBRANE POTENTIAL; CHEMICAL STRUCTURE; CHEMISTRY; ELECTROPHYSIOLOGY; KINETICS; METABOLISM; TIME;

INSERTION SEQUENCES;

BIOPHYSICS; CYTOCHROMES C; EDETIC ACID; ELECTROPHYSIOLOGY; ION CHANNELS; IONS; KINETICS; LANTHANUM; LIPIDS; MEMBRANE POTENTIALS; MEMBRANES, ARTIFICIAL; MODELS, MOLECULAR; SPHINGOSINE; TIME FACTORS;

EID: 0041320897     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74588-3     Document Type: Article

References (102)

1. Akutsu, H., and J. Seelig. 1981. Interaction of metal ions with phosphatidylcholine bilayer membranes. Biochemistry. 20:7366-7373.
2. Amarante-Mendes, G. P., C. Naekyung Kim, L. Liu, Y. Huang, C. L. Perkins, D. R. Green, and K. Bhalla. 1998. Bcr-Abl exerts its antiapoptotic effect against diverse apoptotic stimuli through blockage of mitochondrial release of cytochrome c and activation of caspase-3. Blood. 91:1700-1705.
3. Antonsson, B., S. Montessuit, S. Lauper, R. Eskes, and J. C. Martinou. 2000. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem. J. 345:271-278.
4. Antonsson, B., S. Montessuit, B. Sanchez, and J. C. Martinou. 2001. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J. Biol. Chem. 276:11615-11623.
5. Ariga, T., W. D. Jarvis, and R. K. Yu. 1998. Role of sphingolipid-mediated cell death in neurodegenerative diseases. J. Lipid Res. 39:1-16.
6. Armstrong, C. M., and G. Cota. 1990. Modification of sodium channel gating by lanthanum. Some effects cannot be explained by surface charge theory. J. Gen. Physiol. 96:1129-1140.
7. Arora, A. S., B. J. Jones, T. C. Patel, S. F. Bronk, and G. J. Gores. 1997. Ceramide induces hepatocyte cell death through disruption of mitochondrial function in the rat. Hepatology. 25:958-963.
8. L, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc. Natl. Acad. Sci. USA. 96:5492-5497.
9. Belaud-Rotureau, M. A., N. Leducq, F. Macouillard Poulletier de Gannes, P. Diolez, L. Lacoste, F. Lacombe, P. Bernard, and F. Belloc. 2000. Early transitory rise in intracellular pH leads to Bax conformational change during ceramide-induced apoptosis. Apoptosis. 5:551-560.
10. 3+-induced fusion of phosphatidylserine liposomes. Close approach, intermembrane intermediates, and the electrostatic surface potential. Biophys. J. 53:593-607.
11. Bernardi, P., L. Scorrano, R. Colonna, V. Petronilli, and F. Di Lisa. 1999. Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur. J. Biochem. 264:687-701.
12. Bezrukov, S. M., and I. Vodyanoy. 1993. Probing alamethicin channels with water-soluble polymers. Effect on conductance of channel states. Biophys. J. 64:16-25.
13. Bose, R., M. Verheij, A. Haimovitz-Friedman, K. Scotto, Z. Fuks, and R. Kolesnick. 1995. Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals. Cell. 82:405-414.
14. Cafiso, D. S. 1994. Alamethicin: a peptide model for voltage-gating and protein-membrane interactions. Annu. Rev. Biophys. Biomol. Struct. 23:141-165.
15. Caldwell, R. A., H. F. Clemo, and C. M. Baumgarten. 1998. Using gadolinium to identify stretch-activated channels: technical considerations. Am. J. Physiol. 275:C619-C621.
16. Castedo, M., T. Hirsch, S. A. Susin, N. Zamzami, P. Marchetti, A. Macho, and G. Kroemer. 1996. Sequential acquisition of mitochondrial and plasma membrane alterations during early lymphocyte apoptosis. J. Immunol. 157:512-521.
17. Charles, A. G., T. Y. Han, Y. Y. Liu, N. Hansen, A. E. Giuliano, and M. C. Cabot. 2001. Taxol-induced ceramide generation and apoptosis in human breast cancer cells. Cancer Chemother. Pharmacol. 47:444-450.
18. Cheng, Y., M. Liu, R. Li, C. Wang, C. Bai, and K. Wang. 1999. Gadolinium induces domain and pore formation of human erythrocyte membrane: an atomic force microscopic study. Biochim. Biophys. Acta. 1421:249-260.
19. Chugh, J. K., and B. A. Wallace. 2001. Peptaibols: models for ion channels. Biochem. Soc. Trans. 29:565-570.
20. Colombini, M. 1987. Characterization of channels isolated from plant mitochondria. Method. Enzymol. 148:465-475.
21. Colvin, R. A. 1998. Characterization of a membrane zinc transporter in rat brain. Neurosci. Lett. 247:147-150.
22. Colvin, R. A., N. Davis, R. W. Nipper, and P. A. Carter. 2000. Evidence for a zinc/proton antiporter in rat brain. Neurochem. Int. 36:539-547.
23. Crompton, M. 1999. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341:233-249.
24. De-Maria, R., L. Lenti, F. Malisan, F. d'Agostino, B. Tomassini, A. Zeuner, M. R. Rippo, and R. Testi. 1997. Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis. Science. 277:1652-1655.
25. Di Paola, M., T. Cocco, and M. Lorusso. 2000. Ceramide interaction with the respiratory chain of heart mitochondria. Biochemistry. 39:6660-6668.
26. Ehrenstein, G., and H. Lecar. 1977. Electrically gated ionic channels in lipid bilayers. Q. Rev. Biophys. 10:1-34.
27. El Bawab, S., P. Roddy, T. Qian, A. Bielawska, J. J. Lemasters, and Y. A. Hannun. 2000. Molecular cloning and characterization of a human mitochondrial ceramidase. J. Biol. Chem. 275:21508-21513.
28. Ermakov, Y. A., A. Z. Averbakh, A. I. Yusipovich, and S. Sukharev. 2001. Dipole potentials indicate that restructuring of the membrane interface induced by gadolinium and beryllium ions. Biophys. J. 80:1851-1862.
29. Fox, R. O., and F. M. Richards. 1982. A voltage-gated ion channel model interred from the crystal structure of alamethicin at 1.5 Å resolution. Nature. 300:325-330.
30. Ghafourifar, P., S. D. Klein, O. Schucht, U. Schenk, M. Pruschy, S. Rocha, and C. Richter. 1999. Ceramide induces cytochrome c release from isolated mitochondria. Importance of mitochondrial redox state. J. Biol. Chem. 274:6080-6084.
31. 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.
32. Green, D. R., and J. C. Reed. 1998. Mitochondria and apoptosis. Science. 281:1309-1312.
33. Grosman, C., and I. L. Reisin. 2000. Single-channel characterization of a nonselective cation channel from human placental microvillous membranes. Large conductance, multiplicity of conductance states, and inhibition by lanthanides. J. Membr. Biol. 174:59-70.
34. Gustin, M., X.-L. Zhou, B. Martinac, and C. Kung. 1988. A mechanosensitive ion channel in the yeast plasma membrane. Science. 242:762-765.
35. Hamill, O. P., and D. W. McBride, Jr. 1996. The pharmacology of mechanogated membrane ion channels. Pharmacol. Rev. 48:231-252.
36. 3+ with phosphatidylserine vesicles: binding, phase transition, leakage, and fusion. Biochim. Biophys. Acta. 558:338-343.
37. Hanke, W., and G. Boheim. 1980. The lowest conductance state of the alamethicin pore. Biochim. Biophys. Acta. 596:456-462.
38. Hanke, W., C. Methfessel, H. U. Wilmsen, E. Katz, G. Jung, and G. Boheim. 1983. Melittin and a chemically modified trichotoxin form alamethicin-type multi-state pores. Biochim. Biophys. Acta. 727:108-114.
39. Hannun, Y. A. 1996. Functions of ceramide in coordinating cellular responses to stress. Science. 274:1855-1859.
40. Helluin, O., J.-Y. Dugast, G. Molle, A. R. Machie, S. Ladha, and H. Doclohier. 1997. Lateral diffusion and conductance properties of a fluorescein-labelled alamethicin in planar lipid bilayers. Biochim. Biophys. Acta. 1330:284-292.
41. nd ed. Sinauer Assoc., Sunderland, MA. 59.
42. Hofmann, K., and V. M. Dixit. 1999. Reply to Kolesnick and Hannun, and Perry and Hannun. Trends Biochem. Sci. 24:227.
43. Keller, F., W. Hanke, D. Trissl, and T. Bakker-Grunwald. 1989. Poreforming protein from Entamoeba histolytica forms voltage- and pH-controlled multi-state channels with properties similar to those of the barrel-stave aggregates. Biochim. Biophys. Acta. 982:89-93.
44. Keller, S. L., S. M. Bezrukov, S. M. Gruner, M. W. Tate, I. Vodyanoy, and V. A. Parsegian. 1993. Probability of alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids. Biophys. J. 65:23-27.
45. Kolesnick, R. N., F. M. Goñi, and A. Alonoso. 2000. Compartmentalization of ceramide signaling: physical foundations and biological effects. J. Cell. Physiol. 184:285-300.
46. Kolesnick, R., and Y. A. Hannun. 1999. Ceramide and apoptosis. Trends Biochem. Sci. 24:224-227.
47. Kolesnick, R. N., and M. Krönke. 1998. Regulation of ceramide production and apoptosis. Annu. Rev. Physiol. 60:643-665.
48. Kroemer, G., B. Dallaporta, and M. Resche-Rigon. 1998. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60:619-642.
49. Kroesen, B. J., B. Pettus, C. Luberto, M. Busman, H. Sietsma, L. de Leij, and Y. A. Hannun. 2001. Induction of apoptosis through B-cell receptor cross-linking occurs via de novo generated C16-ceramide and involves mitochondria. J. Biol. Chem. 276:13606-13614.
50. Kuwana, T., M. R. Mackey, G. Perkins, M. H. Ellisman, M. Latterich, R. Schneiter, D. R. Green, and D. D. Newmeyer. 2002. Bid, bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell. 111:331-342.
51. Lee, H., Z. Fuks, A. Rimner, D. Ehleiter, J. Reed, W.-C. Liao, and R. Kolesnick. 2002. Ionizing radiation remodels mitochondrial membranes to facilitate Bax insertion. In preparation.
52. Lee, J., A. Ishihama, G. Oxford, B. Johnson, and K. Jacobson. 1999. Regulation of cell movement is mediated by stretch-activated calcium channels. Nature. 400:382-386.
53. 2+ transport. Arch. Biochem. Biophys. 143:506-515.
54. Li, X., Y. Zhang, J. Ni, J. Chen, and F. Hwang. 1994. Effect of lanthanide ions on the phase behavior of dipalmitoylphosphatidylcholine multilamellar liposomes. J. Inorg. Biochem. 53:139-149.
55. Molle, G., H. Duclohier, and G. Spach. 1987. Voltage-dependent and multistate ionic channels induced by trichorzianines, anti-fungal peptides related to alamethicin. FEBS Lett. 224:208-212.
56. Montal, M., and P. Mueller. 1972. Formation of bimolecular membranes from lipid monolayers, and a study of their electrical properties. Proc. Natl. Acad. Sci. USA. 69:3561-3566.
57. Montes, L. R., M. B. Ruiz-Argüello, F. M. Goñi, and A. Alonoso. 2002. Membrane restructuring via ceramide results in enhanced solute efflux. J. Biol. Chem. 277:11788-11794.
58. Moore, D. J., M. E. Rerek, and R. Mendelsohn. 1997. FTIR spectroscopy studies of the conformational order and phase behavior of ceramides. J. Phys. Chem. B. 101:8933-8940.
59. Narula, J., P. Pandey, E. Arbustini, N. Haider, N. Narula, F. D. Kolodgie, B. Dal Bello, M. J. Semigran, A. Bielsa-Masdeu, G. W. Dec, S. Israels, M. Ballester, R. Virmani, S. Saxna, and S. Kharbanda. 1999. Apoptosis in heart failure: release of cytochrome c from mitochondria and activation of caspase-3 in human cardiomyopathy. Proc. Natl. Acad. Sci. USA. 96:8144-8149.
60. Negrete, H., R. Rivers, A. H. Gough, M. Colombini, and M. L. Zeidel. 1996. Individual leaflets of a membrane bilayer can independently regulate permeability. J. Biol. Chem. 271:11627-11630.
61. Nicholls, D., and K. Akerman. 1982. Mitochondrial calcium transport. Biochim. Biophys. Acta. 683:57-88.
62. Pascher, I. 1976. Molecular arrangements in sphingolipids. Conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability. Biochim. Biophys. Acta. 455:433-451.
63. Pastorino, J. G., M. Tafani, R. J. Rothman, A. Marcineviciute, J. B. Hoek, and J. L. Farber. 1999. Functional consequences of the sustained or transient activation by Bax of the mitochondrial permeability transition pore. J. Biol. Chem. 274:31734-31739.
64. Pavlov, E. V., M. Priault, D. Pietkiewicz, E. H.-Y. 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.
65. 3+ by phosphatidylserine. Biophys. J. 55:631-636.
66. Perry, D. K., J. Carton, A. K. Shah, F. Meredith, D. J. Uhlinger, and Y. A. Hannun. 2000. Serine palmitoyltransferase regulates de novo ceramide generation during etoposide-induced apoptosis. J. Biol. Chem. 275: 9078-9084.
67. Radin, N. S. 2001. Killing cancer cells by poly-drug elevation of ceramide levels: a hypothesis whose time has come? Eur. J. Biochem. 268:193-204.
68. Raisova, M., M. Bektas, T. Wieder, P. Daniel, P. Eberle, C. E. Orfanos, and C. C. Geilen. 2000. Resistance to CD95/Fas-induced and ceramide-mediated apoptosis of human melanoma cells is caused by a detective mitochondrial cytochrome c release. FEBS Lett. 473:27-32.
69. Rapaport, D., and Y. Shai. 1992. Aggregation and organization of pardaxin in phospholipid membranes. A fluorescence energy transfer study. J. Biol. Chem. 267:6502-6509.
70. Reed, K. C., and F. L. Bygrave. 1974. The inhibition of mitochondrial calcium transport by lanthanides and ruthenium red. Biochem. J. 140: 143-155.
71. Robinson, R. A., and R. H. Stokes. 1965. Electrolyte Solutions. Butterworths, London, England. 466.
72. Rodriguez-Lafrasse, C., G. Alphonse, P. Broquet, M.-T. Aloy, P. Louisot, and R. Rousson. 2001. Temporal relationships between ceramide production, caspase activation, and mitochondrial dysfunction in cell lines with varying sensitivity to anti-Fas-induced apoptosis. Biochem. J. 357:407-416.
73. Ruiz-Argüello, M. B., G. Basañez, F. M. Goñi, and A. Alonoso. 1996. Different effects of enzyme-generated ceramides and diacylglycerols in phospholipid membrane fusion and leakage. J. Biol. Chem. 271:26616-26621.
74. Saito, M., S. J. Korsmeyer, and P. H. Schlesinger. 2000. BAX-dependent transport of cytochrome c reconstituted in pure liposomes. Nat. Cell Biol. 2:553-555.
75. Sansom, M. S. P. 1991. The biophysics of peptide models of ion channels. Prog. Biophys. Mol. Biol. 55:139-236.
76. Sansom, M. S. P. 1993. Alamethicin and related peptaibols-model ion channels. Eur. Biophys. J. 22:105-124.
77. Schuller, F., R. Benz, and H. G. Sahl. 1989. The peptide antibiotic subtilin acts by formation of voltage-dependent multi-state pores in bacterial and artificial membranes. Eur. J. Biochem. 182:181-186.
78. Seelig, J., P. M. Macdonald, and P. G. Scherer. 1987. Phospholipid head groups as sensors of electric charge in membranes. Biochemistry. 26:7535-7541.
79. Shai, Y. 1994. Pardaxin: channel formation by a shark repellant peptide from fish. Toxicology. 87:109-129.
80. Shai, Y. 1999. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell nonselective membrane-lytic peptides. Biochim. Biophys. Acta. 1462:55-70.
81. Shimeno, H., S. Soeda, M. Sakamoto, T. Kouchi, T. Kowakame, and T. Kihara. 1998. Partial purification and characterization of sphingosine N-acyltransferase (ceramide synthase) from bovine liver mitochondrion-rich fraction. Lipids. 33:601-605.
82. Simon, C. G., and A. R. Gear. 1998. Membrane-destabilizing properties of C2-ceramide may be responsible for its ability to inhibit platelet aggregation. Biochemistry. 37:2059-2069.
83. Siskind, L. J., and M. Colombini. 2000. The lipids C2- and C16-ceramide form large stable channels. Implications for apoptosis. J. Biol. Chem. 275:38640-38644.
84. Siskind, L. J., R. N. Kolesnick, and M. Colombini. 2002. Ceramide channels increase the permeability of the mitochondrial outer membrane to small proteins. J. Biol. Chem. 277:26796-26803.
85. Spach, G., H. Duclohier, G. Molle, and J.-M. Valleton. 1989. Structure and supramolecular architecture of membrane channel-forming peptides. Biochimie. 71:11-21.
86. Sparagna, G. C., K. K. Gunter, S. S. Sheu, and T. E. Gunter. 1995. Mitochondrial calcium uptake from physiological-type pulses of calcium. A description of the rapid uptake mode. J. Biol. Chem. 270:27510-27515.
87. Susin, S. A., N. Zamzami, and G. Kroemer. 1998. Mitochondria as regulators of apoptosis: doubt no more. Biochim. Biophys. Acta. 1366:151-165.
88. Susin, S. A., N. Zamzami, M. Castedo, E. Daugas, E. G. Wang, S. Geley, F. Fassy, J. C. Reed, and G. Kroemer. 1997a. The central executioner in apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95 and ceramide induced cell death. J. Exp. Med. 186:25-37.
89. Susin, S. A., N. Zamzami, N. Larochette, B. Dallaporta, I. Marzo, C. Brenner, T. Hirsch, P. X. Petit, M. Geuskens, and G. Kroemer. 1997b. A cytofluorometric assay of nuclear apoptosis is induced in a cell-free system: application to ceramide induced apoptosis. Exp. Cell Res. 236:397-403.
90. Takata, M., W. F. Pickard, J. Y. Lettvin, and J. W. Moore. 1966. Ionic conductance changes in lobster axon membrane when lanthanum is substituted for calcium. J. Gen. Physiol. 50:461-471.
91. II) phase in phosphatidylethanolamine membranes. Biochim. Biophys. Acta. 1515:189-201.
92. Tapia, R., C. Arias, and E. Morales. 1985. Binding of lanthanum ions and ruthenium red to synaptosomes and its effects on neurotransmitter release. J. Neurochem. 45:1464-1470.
93. Thomas, R. L., Jr., C. M. Matsko, M. T. Lotze, and A. A. Amoscato. 1999. Mass spectrometric identification of increased C16-ceramide levels during apoptosis. J. Biol. Chem. 274:30580-30588.
94. Veiga, M. P., J. L. Arrondo, F. M. Goñi, and A. Alonoso. 1999. Ceramides in phospholipid membranes: effects on bilayer stability and transition to nonlamellar phases. Biophys. J. 76:342-350.
95. Verstraeten, S. V., L. V. Nogueira, S. Schreier, and P. I. Oteiza. 1997. Effect of trivalent metal ions on phase separation and membrane lipid packing: role in lipid peroxidation. Arch. Biochem. Biophys. 338:121-127.
96. Vodyanoy, I., S. M. Bezrukov, and V. A. Parsegian. 1993. Probing alamethicin channels with water-soluble polymers. Size-modulated osmotic action. Biophys. J. 65:2097-2105.
97. Witty, J. P., J. T. Bridgham, and A. L. Johnson. 1996. Induction of apoptotic cell death in hen granulosa cells by ceramide. Endocrinology. 137:5269-5277.
98. Woolley, G. A., and B. A. Wallace. 1992. Model ion channels: gramicidin and alamethicin. J. Membr. Biol. 129:109-136.
99. Yang, X. C., and F. Sachs. 1989. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science. 243:1068-1071.
100. Zamzami, N., P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsh, S. A. Susin, P. X. Petit, B. Mignotte, and G. Kroemer. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:367-377.
101. Zhang, P., B. Liu, S. W. Kang, M. S. Seo, S. G. Rhee, and L. M. Obeid. 1997. Thioredoxin peroxidase is a novel inhibitor of apoptosis with a mechanism distinct from that of Bcl-2. J. Biol. Chem. 272:30615-30618.
102. Zhou, X.-L., and C. Kung. 1992. A mechanosensitive ion channel in Schizosaccharomyces pombe. EMBO J. 11:2869-2875.