Limited mitochondrial permeabilization is an early manifestation of palmitate-induced lipotoxicity in pancreatic β-cells

Journal of Biological Chemistry

Volumn 283, Issue 12, 2008, Pages 7936-7948

  Koshkin, Vasilij ^a   Dai, Feihan F ^a   Robson Doucette, Christine A ^a   Chan, Catherine B ^b   Wheeler, Michael B ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDES; APPLICATIONS; BIOCHEMISTRY; CALCIUM; CELL CULTURE; CELL DEATH; CELL MEMBRANES; CELLS; CYTOLOGY; FATTY ACIDS; METABOLISM; MITOCHONDRIA; PHYSIOLOGY;

ANTI-OXIDANTS; APOPTOSIS; CELL LINES; CELL METABOLISMS; CELL SUSCEPTIBILITIES; CERAMIDE; CYTOTOXIC; EARLY STAGES; LONG TERMS; MEMBRANE FLUIDITIES; MEMBRANE POTENTIALS; MITOCHONDRIAL PERMEABILITY TRANSITIONS; MITOCHONDRIAL RESPIRATIONS; PERMEABILIZATION; PHOSPHATIDYLINOSITOL; PORE OPENINGS;

PLASMA JETS;

ANTIOXIDANT; CALCIUM ION; CERAMIDE; OLEIC ACID; PALMITIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; CALCIUM; ENZYME INHIBITOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONDUCTANCE; CYTOTOXICITY; LONG TERM EXPOSURE; MEMBRANE FLUIDITY; MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SOLUTE; ANIMAL; CELL LINE; CELL MEMBRANE PERMEABILITY; DRUG EFFECT; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; OXYGEN CONSUMPTION; PATHOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; CALCIUM; CELL LINE; CELL MEMBRANE PERMEABILITY; ENZYME INHIBITORS; INSULIN-SECRETING CELLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; OLEIC ACID; OXYGEN CONSUMPTION; PALMITIC ACID;

EID: 43149084152     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M705652200     Document Type: Article

References (106)

1. Bernardi, P. (1999) Physiol. Rev. 79, 1127-1155
2. Bernardi, P., Scorrano, L., Colonna, R., Petronilli, V., and Di Lisa, F. (1999) Eur. J. Biochem. 264, 687-701
3. Zoratti, M., and Szabo, I. (1995) Biochim. Biophys. Acta 1241, 139-176
4. Gunter, T. E., and Pfeiffer, D. R. (1990) Am. J. Physiol. 258, C755-C786
5. Crompton, M. (1999) Biochem. J. 341, 233-249
6. Ichas, F., and Mazat, J. P. (1998) Biochim. Biophys. Acta 1366, 33-50
7. Novgorodov, S. A., and Gudz, T. I. (1996) J. Bioenerg. Biomembr. 28, 139-146
8. Reid, A. B., Kurten, R. C., McCullough, S. S., Brock, R. W., and Hinson, J. A. (2005) J. Pharmacol. Exp. Ther. 312, 509-516
9. Weiss, J. N., Korge, P., Honda, H. M., and Ping, P. (2003) Circ. Res. 93, 292-301
10. Halestrap, A. P. (2006) Biochem. Soc. Trans. 34, 232-237
11. Stavrovskaya, I. G., and Kristal, B. S. (2005) Free Radic. Biol. Med. 38, 687-697
12. Hausenloy, D., Wynne, A., Duchen, M., and Yellon, D. (2004) Circulation 109, 1714-1717
13. Brustovetsky, N., and Dubinsky, J. M. (2000) J. Neurosci. 20, 103-113
14. Kowaltowski, A. J., Smaili, S. S., Russell, J. T., and Fiskum, G. (2000) Am. J. Physiol. 279, C852-C859
15. Barbu, A., Welsh, N., and Saldeen, J. (2002) Mol. Cell. Endocrinol. 190, 75-82
16. Donath, M. Y., Ehses, J. A., Maedler, K., Schumann, D. M., Ellingsgaard, H., Eppler, E., and Reinecke, M. (2005) Diabetes 54, Suppl. 2, 108-113
17. Maestre, I., Jordan, J., Calvo, S., Reig, J. A., Cena, V., Soria, B., Prentki, M., and Roche, E. (2003) Endocrinology 144, 335-345
18. Silva, J. P., Kohler, M., Graff, C., Oldfors, A., Magnuson, M. A., Berggren, P. O., and Larsson, N. G. (2000) Nat. Genet. 26, 336-340
19. LeRoith, D. (2002) Am. J. Med. 113, Suppl. 6A, 3-11
20. Asghar, Z., Yau, D., Chan, F., LeRoith, D., Chan, C. B., and Wheeler, M. B. (2006) Diabetologia 49, 90-99
21. Jimenez-Chillaron, J. C., Hernandez-Valencia, M., Reamer, C., Fisher, S., Joszi, A., Hirshman, M., Oge, A., Walrond, S., Przybyla, R., Boozer, C., Goodyear, L. J., and Patti, M. E. (2005) Diabetes 54, 702-711
22. Busch, A. K., Cordery, D., Denyer, G. S., and Biden, T. J. (2002) Diabetes 51, 977-987
23. Biden, T. J., Robinson, D., Cordery, D., Hughes, W. E., and Busch, A. K. (2004) Diabetes 53, Suppl. 1, 159-165
24. Busch, A. K., Gurisik, E., Cordery, D. V., Sudlow, M., Denyer, G. S., Laybutt, D. R., Hughes, W. E., and Biden, T. J. (2005) Diabetes 54, 2917-2924
25. Maedler, K., Oberholzer, J., Bucher, P., Spinas, G. A., and Donath, M. Y. (2003) Diabetes 52, 726-733
26. Fry, J. R., Jones, C. A., Wiebkin, P., Bellemann, P., and Bridges, J. W. (1976) Anal. Biochem. 71, 341-350
27. Civelek, V. N., Deeney, J. T., Shalosky, N. J., Tornheim, K., Hansford, R. G., Prentki, M., and Corkey, B. E. (1996) Biochem. J. 318, 615-621
28. Estabrook, R. (1967) Methods Enzymol. 10, 41-47
29. Reynafarje, B., Costa, L. E., and Lehninger, A. L. (1985) Anal. Biochem. 145, 406-418
30. Akerman, K. E., and Wikstrom, M. K. (1976) FEBS Lett. 68, 191-197
31. Vercesi, A. E., Bernardes, C. F., Hoffmann, M. E., Gadelha, F. R., and Docampo, R. (1991) J. Biol. Chem. 266, 14431-14434
32. MacDonald, M. J. (1981) J. Biol. Chem. 256, 8287-8290
33. Korge, P., and Weiss, J. N. (1999) Eur. J. Biochem. 265, 273-280
34. Lecoeur, H., Prevost, M. C., and Gougeon, M. L. (2001) Cytometry 44, 65-72
35. Rello, S., Stockert, J. C., Moreno, V., Gamez, A., Pacheco, M., Juarranz, A., Canete, M., and Villanueva, A. (2005) Apoptosis 10, 201-208
36. Chernyak, B. V. (1997) FEBS Lett. 418, 131-134
37. Smaili, S. S., and Russell, J. T. (1999) Cell Calcium 26, 121-130
38. Rosenstock, T. R., Carvalho, A. C., Jurkiewicz, A., Frussa-Filho, R., and Smaili, S. S. (2004) J. Neurochem. 88, 1220-1228
39. Thomas, A. P., and Delaville, F. (1991) in Cellular Calcium: A Practical Approach (McCormack, J. G., and Cobbold, P. H., eds) pp. 1-54, IRL Press at Oxford University Press, Oxford
40. Merritt, J. E., McCarthy, S. A., Davies, M. P., and Moores, K. E. (1990) Biochem. J. 269, 513-519
41. Gee, K. R., Brown, K. A., Chen, W. N., Bishop-Stewart, J., Gray, D., and Johnson, I. (2000) Cell Calcium 27, 97-106
42. Arkhammar, P., Nilsson, T., and Berggren, P. O. (1989) Biochem. Biophys. Res. Commun. 159, 223-228
43. Arkhammar, P., Nilsson, T., and Berggren, P. O. (1990) FEBS Lett. 273, 182-184
44. Barrand, M. A., Bagrij, T., and Neo, S. Y. (1997) Gen. Pharmacol. 28, 639-645
45. Dai, F. F., Zhang, Y., Kang, Y., Wang, Q., Gaisano, H. Y., Braunewell, K. H., Chan, C. B., and Wheeler, M. B. (2006) J. Biol. Chem. 281, 21942-21953
46. Xia, S., Forman, L. W., and Faller, D. V. (2007) J. Biol. Chem. 282, 13199-13210
47. Wang, X., Li, H., De Leo, D., Guo, W., Koshkin, V., Fantus, I. G., Giacca, A., Chan, C. B., Der, S., and Wheeler, M. B. (2004) Diabetes 53, 129-140
48. Bernardi, P., Penzo, D., and Wojtczak, L. (2002) Vitam. Horm. 65, 97-126
49. Wojtczak, L., and Schonfeld, P. (1993) Biochim. Biophys. Acta 1183, 41-57
50. Schonfeld, P. (1990) FEBS Lett. 264, 246-248
51. Di Paola, M., and Lorusso, M. (2006) Biochim. Biophys. Acta 1757, 1330-1337
52. Wieckowski, M. R., and Wojtczak, L. (1998) FEBS Lett. 423, 339-342
53. Richieri, G. V., Anel, A., and Kleinfeld, A. M. (1993) Biochemistry 32, 7574-7580
54. Joseph, J. W., Koshkin, V., Zhang, C. Y., Wang, J., Lowell, B. B., Chan, C. B., and Wheeler, M. B. (2002) Diabetes 51, 3211-3219
55. Joseph, J. W., Koshkin, V., Saleh, M. C., Sivitz, W. I., Zhang, C. Y., Lowell, B. B., Chan, C. B., and Wheeler, M. B. (2004) J. Biol. Chem. 279, 51049-51056
56. Dufer, M., Krippeit-Drews, P., Lembert, N., Idahl, L. A., and Drews, G. (2001) Mol. Pharmacol. 60, 873-879
57. Koshkin, V., Bikopoulos, G., Chan, C. B., and Wheeler, M. B. (2004) J. Biol. Chem. 279, 41368-41376
58. Park, S. Y., Cho, N., Chang, I., Chung, J. H., Min, Y. K., Lee, M. K., Kim, K. W., Kim, S. J., and Lee, M. S. (2005) Apoptosis 10, 537-544
59. Migita, K., Tanaka, F., Abiru, S., Ida, H., Izumi, Y., Kawakami, A., and Eguchi, K. (2003) Immunol. Lett. 90, 87-91
60. Joshi, M. S., Julian, M. W., Huff, J. E., Bauer, J. A., Xia, Y., and Crouser, E. D. (2006) Am. J. Respir. Crit. Care Med. 173, 999-1007
61. Shimabukuro, M., Zhou, Y. T., Levi, M., and Unger, R. H. (1998) Proc. Natl. Acad. Sci. U. S. A. 95, 2498-2502
62. Shimabukuro, M., Higa, M., Zhou, Y. T., Wang, M. Y., Newgard, C. B., and Unger, R. H. (1998) J. Biol. Chem. 273, 32487-32490
63. Inoguchi, T., Li, P., Umeda, F., Yu, H. Y., Kakimoto, M., Imamura, M., Aoki, T., Etoh, T., Hashimoto, T., Naruse, M., Sano, H., Utsumi, H., and Nawata, H. (2000) Diabetes 49, 1939-1945
64. Panaretakis, T., Shabalina, I. G., Grander, D., Shoshan, M. C., and De-Pierre, J. W. (2001) Toxicol. Appl. Pharmacol. 173, 56-64
65. Takuma, K., Phuagphong, P., Lee, E., Mori, K., Baba, A., and Matsuda, T. (2001) J. Biol. Chem. 276, 48093-48099
66. Tsuboi, T., da Silva Xavier, G., Holz, G. G., Jouaville, L. S., Thomas, A. P., and Rutter, G. A. (2003) Biochem. J. 369, 287-299
67. Carlsson, C., Borg, L. A., and Welsh, N. (1999) Endocrinology 140, 3422-3428
68. Koshkin, V., Wang, X., Scherer, P. E., Chan, C. B., and Wheeler, M. B. (2003) J. Biol. Chem. 278, 19709-19715
69. Kowaltowski, A. J., Castilho, R. F., and Vercesi, A. E. (2001) FEBS Lett. 495, 12-15
70. Penzo, D., Tagliapietra, C., Colonna, R., Petronilli, V., and Bernardi, P. (2002) Biochim. Biophys. Acta 1555, 160-165
71. Dymkowska, D., Szczepanowska, J., Wieckowski, M. R., and Wojtczak, L. (2006) Biochim. Biophys. Acta 1763, 152-163
72. Maedler, K., Spinas, G. A., Dyntar, D., Moritz, W., Kaiser, N., and Donath, M. Y. (2001) Diabetes 50, 69-76
73. Beeharry, N., Chambers, J. A., and Green, I. C. (2004) Apoptosis 9, 599-607
74. Hardy, S., Langelier, Y., and Prentki, M. (2000) Cancer Res. 60, 6353-6358
75. El Kholy, W., MacDonald, P. E., Lin, J. H., Wang, J., Fox, J. M., Light, P. E., Wang, Q., Tsushima, R. G., and Wheeler, M. B. (2003) FASEB J. 17, 720-722
76. Aikin, R., Hanley, S., Maysinger, D., Lipsett, M., Castellarin, M., Paraskevas, S., and Rosenberg, L. (2006) Diabetologia 49, 2900-2909
77. Buteau, J., El Assaad, W., Rhodes, C. J., Rosenberg, L., Joly, E., and Prentki, M. (2004) Diabetologia 47, 806-815
78. Sabin, M. A., Stewart, C. E., Crowne, E. C., Turner, S. J., Hunt, L. P., Welsh, G. I., Grohmann, M. J., Holly, J. M., and Shield, J. P. (2007) J. Cell. Physiol. 211, 244-252
79. Quinlan, P. T., Thomas, A. P., Armston, A. E., and Halestrap, A. P. (1983) Biochem. J. 214, 395-404
80. Hoek, J. B., Farber, J. L., Thomas, A. P., and Wang, X. (1995) Biochim. Biophys. Acta 1271, 93-102
81. Al Nasser, I., and Crompton, M. (1986) Biochem. J. 239, 19-29
82. Krasnikov, B. F., Zorov, D. B., Antonenko, Y. N., Zaspa, A. A., Kulikov, I. V., Kristal, B. S., Cooper, A. J., and Brown, A. M. (2005) Biochim. Biophys. Acta 1708, 375-392
83. Riley, W. W., Jr., and Pfeiffer, D. R. (1985) J. Biol. Chem. 260, 12416-12425
84. Lotscher, H. R., Winterhalter, K. H., Carafoli, E., and Richter, C. (1979) Proc. Natl. Acad. Sci. U. S. A. 76, 4340-4344
85. Kristal, B. S., Park, B. K., and Yu, B. P. (1996) J. Biol. Chem. 271, 6033-6038
86. Vieira, H. L., Belzacq, A. S., Haouzi, D., Bernassola, F., Cohen, I., Jacotot, E., Ferri, K. F., El Hamel, C., Bartle, L. M., Melino, G., Brenner, C., Goldmacher, V., and Kroemer, G. (2001) Oncogene 20, 4305-4316
87. Smaili, S. S., Stellato, K. A., Burnett, P., Thomas, A. P., and Gaspers, L. D. (2001) J. Biol. Chem. 276, 23329-23340
88. Pacher, P., and Hajnoczky, G. (2001) EMBO J. 20, 4107-4121
89. Lukowiak, B., Vandewalle, B., Riachy, R., Kerr-Conte, J., Gmyr, V., Belaich, S., Lefebvre, J., and Pattou, F. (2001) J. Histochem. Cytochem. 49, 519-528
90. Elliott, J. I., and Brewer, J. M. (1980) J. Inorg. Biochem. 12, 323-334
91. Penzo, D., Petronilli, V., Angelin, A., Cusan, C., Colonna, R., Scorrano, L., Pagano, F., Prato, M., Di Lisa, F., and Bernardi, P. (2004) J. Biol. Chem. 279, 25219-25225
92. Ward, M. W., Rego, A. C., Frenguelli, B. G., and Nicholls, D. G. (2000) J. Neurosci. 20, 7208-7219
93. Kushnareva, Y. E., and Sokolove, P. M. (2000) Arch. Biochem. Biophys. 376, 377-388
94. Zago, E. B., Castilho, R. F., and Vercesi, A. E. (2000) FEBS Lett. 478, 29-33
95. Bodrova, M. E., Dedukhova, V. I., Samartsev, V. N., and Mokhova, E. N. (2000) IUBMB Life 50, 189-194
96. Bodrova, M. E., Brailovskaya, I. V., Efron, G. I., Starkov, A. A., and Mokhova, E. N. (2003) Biochemistry (Mosc.) 68, 391-398
97. Broekemeier, K. M., Klocek, C. K., and Pfeiffer, D. R. (1998) Biochemistry 37, 13059-13065
98. Bernardi, P., Krauskopf, A., Basso, E., Petronilli, V., Blalchy-Dyson, E., Di Lisa, F., and Forte, M. A. (2006) FEBS J. 273, 2077-2099
99. Moore, P. C., Ugas, M. A., Hagman, D. K., Parazzoli, S. D., and Poitout, V. (2004) Diabetes 53, 2610-2616
100. Sparagna, G. C., Hickson-Bick, D. L., Buja, L. M., and McMillin, J. B. (2000) Am. J. Physiol. 279, H2124-H2132
101. Kong, J. Y., and Rabkin, S. W. (2000) Biochim. Biophys. Acta 1485, 45-55
102. Di Paola, M., Cocco, T., and Lorusso, M. (2000) Biochemistry 39, 6660-6668
103. Belosludtsev, K. N., Belosludtseva, N. V., and Mironova, G. D. (2005) Biochemistry (Mosc.) 70, 815-821
104. Davies, S. P., Reddy, H., Caivano, M., and Cohen, P. (2000) Biochem. J. 351, 95-105
105. Aikawa, R., Nawano, M., Gu, Y., Katagiri, H., Asano, T., Zhu, W., Nagai, R., and Komuro, I. (2000) Circulation 102, 2873-2879
106. Smart, N., Mojet, M. H., Latchman, D. S., Marber, M. S., Duchen, M. R., and Heads, R. J. (2006) Cardiovasc. Res. 69, 164-177