Bax and Bcl-xL exert their regulation on different sites of the ceramide channel

Biochemical Journal

Volumn 445, Issue 1, 2012, Pages 81-91

  Perera, Meenu N ^a   Lin, Shang H ^a   Peterson, Yuri K ^b   Bielawska, Alicja ^c   Szulc, Zdzislaw M ^c   Bittman, Robert ^d   Colombini, Marco ^a  

^a Bldg 142   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

2 methoxyantimicin A 3; ABT 263; ABT 737; Apoptosis; Bcl 2 family protein; Ceramide analogue; Ceramide channel; Mitochondrion

Indexed keywords

2 METHOXYANTIMYCIN A3; 4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; C18:1 CER (N OLEOYL DEXTRO ERYTHRO SPHINGOSINE); C2 CER (N ACETYL DEXTRO ERYTHRO SPHINGOSINE); C20 CER (N ARACHIDOYL DEXTRO ERYTHRO SPHINGOSINE); C4 CER (N BUTYRYL DEXTRO ERYTHRO SPHINGOSINE); C8 CER (N PALMITOYL DEXTRO ERYTHRO SPHINGOSINE); CERAMIDE DERIVATIVE; NAVITOCLAX; PROTEIN BAX; PROTEIN BCL XL; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; RAT; REGULATORY MECHANISM; STEREOCHEMISTRY;

ANILINE COMPOUNDS; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BIPHENYL COMPOUNDS; CASPASES; CERAMIDES; COMPUTER SIMULATION; CYTOCHROMES C; ION CHANNELS; MALE; MITOCHONDRIA, LIVER; MODELS, MOLECULAR; NITROPHENOLS; OXIDATION-REDUCTION; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; SULFONAMIDES;

EID: 84862499445     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20112103     Document Type: Article

References (58)

1. Siskind, L. J., Kolesnick, R. N. and Colombini, M. (2006) Ceramide forms channels in mitochondrial outer membranes at physiologically relevant concentrations. Mitochondrion 6, 118-125 (Pubitemid 43872021)
2. Dejean, L. M., Martinez-Caballero, S., Guo, L., Hughes, C., Teijido, O., Ducret, T., Ichas, F., Korsmeyer, S. J., Antonsson, B., Jonas, E. A. and Kinnally, K. W. (2005) Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel. Mol. Biol. Cell 16, 2424-2432 (Pubitemid 40632223)
3. Chiara, F., Castellaro, D., Marin, O., Petronilli, V., Brusilow, W. S., Juhaszova, M., Sollott, S. J., Forte, M., Bernardi, P. and Rasola, A. (2008) Hexokinase II detachment from mitochondria triggers apoptosis through the permeability transition pore independent of voltage-dependent anion channels. PLoS ONE 3, e1852
4. Montessuit, S., Somasekharan, S. P., Terrones, O., Lucken-Ardjomande, S., Herzig, S., Schwarzenbacher, R., Manstein, D. J., Bossy-Wetzel, E., Basañez, G., Meda, P. and Martinou, J. C. (2010) Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142, 889-901
5. Lovell, J. F., Billen, L. P., Bindner, S., Shamas-Din, A., Fradin, C., Leber, B. and Andrews, D. W. (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135, 1074-1084
6. Terrones, O., Antonsson, B., Yamaguchi, H., Wang, H. G., Liu, J., Lee, R. M., Herrmann, A. and Basañez, G. (2004) Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J. Biol. Chem. 279, 30081-30091 (Pubitemid 38937930)
7. Birbes, H., El Bawab, S., Hannun, Y. A. and Obeid, L. M. (2001) Selective hydrolysis of a mitochondrial pool of sphingomyelin induces apoptosis. FASEB J. 15, 2669-2679 (Pubitemid 33131093)
8. Birbes, H., Luberto, C., Hsu, Y. T., El Bawab, S., Hannun, Y. A. and Obeid, L. M. (2005) A mitochondrial pool of sphingomyelin is involved in TNFα-induced Bax translocation to mitochondria. Biochem. J. 386, 445-451 (Pubitemid 40445868)
9. Dai, Q., Liu, J., Chen, J., Durrant, D., McIntyre, T. M. and Lee, R. M. (2004) Mitochondrial ceramide increases in UV-irradiated HeLa cells and is mainly derived from hydrolysis of sphingomyelin. Oncogene 23, 3650-3658 (Pubitemid 38658432)
10. Matsko, C. M., Hunter, O. C., Rabinowich, H., Lotze, M. T. and Amoscato, A. A. (2001) Mitochondrial lipid alterations during Fas- and radiation-induced apoptosis. Biochem. Biophys. Res. Commun. 287, 1112-1120 (Pubitemid 32980567)
11. Siskind, L. J. (2005) Mitochondrial ceramide and the induction of apoptosis. J. Bioenerg. Biomembr. 37, 143-153
12. Mullen, T. D. and Obeid, L. (2012) Ceramide and apoptosis: exploring the enigmatic connections between sphingolipid metabolism and programmed cell death. Anticancer Agents Med. Chem. 12, 340-363
13. Stiban, J., Caputo, L. and Colombini, M. (2008) Ceramide synthesis in the endoplasmic reticulum can permeabilize mitochondria to proapoptotic proteins. J. Lipid Res. 49, 625-634
14. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B. and Korsmeyer, S. J. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730 (Pubitemid 32385543)
15. Zong, W. X., Lindsten, T., Ross, A. J., MacGregor, G. R. and Thompson, C. B. (2001) BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 15, 1481-1486 (Pubitemid 32552527)
16. Siskind, L. J., Mullen, T. D., Romero Rosales, K., Clarke, C. J., Hernandez-Corbacho, M. J., Edinger, A. L. and Obeid, L. M. (2010) The BCL-2 protein BAK is required for long-chain ceramide generation during apoptosis. J. Biol. Chem. 285, 11818-11826
17. Liu, Y. Y., Han, T. Y., Giuliano, A. E. and Cabot, M. C. (2001) Ceramide glycosylation potentiates cellular multidrug resistance. FASEB J. 15, 719-730 (Pubitemid 32245990)
18. Komori, H., Ichikawa, S., Hirabayashi, Y. and Ito, M. (1999) Regulation of intracellular ceramide content in B16 melanoma cells: biological implications of ceramide glycosylation. J. Biol. Chem. 274, 8981-8987 (Pubitemid 29164701)
19. Itoh, M., Kitano, T., Watanabe, M., Kondo, T., Yabu, T., Taguchi, Y., Iwai, K., Tashima, M., Uchiyama, T. and Okazaki, T. (2003) Possible role of ceramide as an indicator of chemoresistance: decrease of the ceramide content via activation of glucosylceramide synthase and sphingomyelin synthase in chemoresistant leukemia. Clin. Cancer Res. 9, 415-423 (Pubitemid 36109759)
20. Lavie, Y., Cao, H., Volner, A., Lucci, A., Han, T. Y., Geffen, V., Giuliano, A. E. and Cabot, M. C. (1997) Agents that reverse multidrug resistance, tamoxifen, verapamil, and cyclosporin A, block glycosphingolipid metabolism by inhibiting ceramide glycosylation in human cancer cells. J. Biol. Chem. 272, 1682-1687 (Pubitemid 27043253)
21. Liu, Y. Y., Patwardhan, G. A., Bhinge, K., Gupta, V., Gu, X. and Jazwinski, S. M. (2011) Suppression of glucosylceramide synthase restores p53-dependent apoptosis in mutant p53 cancer cells. Cancer Res. 71, 2276-2285
22. Patwardhan, G. A., Zhang, Q. J., Yin, D. M., Gupta, V., Bao, J. X., Senkal, C. E., Ogretmen, B., Cabot, M. C., Shah, G. V., Sylvester, P. W. et al. (2009) A new mixed-backbone oligonucleotide against glucosylceramide synthase sensitizes multidrug-resistant tumors to apoptosis. PloS ONE 4, e6938
23. Chapman, J. V., Gouazé-Andersson, V., Messner, M. C., Flowers, M., Karimi, R., Kester, M., Barth, B. M., Liu, X., Liu, Y. Y., Giuliano, A. E. and Cabot, M. C. (2010) Metabolism of short-chain ceramide by human cancer cells: implications for therapeutic approaches. Biochem. Pharmacol. 80, 308-315
24. Siskind, L. J., Feinstein, L., Yu, T., Davis, J. S., Jones, D., Choi, J., Zuckerman, J. E., Tan, W., Hill, R. B., Hardwick, J. M. and Colombini, M. (2008) Anti-apoptotic Bcl-2 family proteins disassemble ceramide channels. J. Biol. Chem. 283, 6622-6630
25. Siskind, L. J., Kolesnick, R. N. and Colombini, M. (2002) Ceramide channels increase the permeability of the mitochondrial outer membrane to small proteins. J. Biol. Chem. 277, 26796-26803 (Pubitemid 34951684)
26. Samanta, S., Stiban, J., Maugel, T. K. and Colombini, M. (2011) Visualization of ceramide channels by transmission electron microscopy. Biochim. Biophys. Acta 1808, 1196-1201
27. Anishkin, A., Sukharev, S. and Colombini, M. (2006) Searching for the molecular arrangement of transmembrane ceramide channels. Biophys. J. 90, 2414-2426
28. Megha, Sawatzki, P., Kolter, T., Bittman, R. and London, E. (2007) Effect of ceramide N-acyl chain and polar headgroup structure on the properties of ordered lipid domains (lipid rafts). Biochim. Biophys. Acta 1768, 2205-2212
29. Pruett, S. T., Bushnev, A., Hagedorn, K., Adiga, M., Haynes, C. A., Sullards, M. C., Liotta, D. C. and Merrill, A. H. (2008) Biodiversity of sphingoid bases ("sphingosines") and related amino alcohols. J. Lipid Res. 49, 1621-1639
30. Siskind, L. J., Davoody, A., Lewin, N., Marshall, S. and Colombini, M. (2003) Enlargement and contracture of C2-ceramide channels. Biophys. J. 85, 1560-1575
31. Ganesan, V., Perera, M. N., Colombini, D., Datskovskiy, D., Chadha, K. and Colombini, M. (2010) Ceramide and activated Bax act synergistically to permeabilize the mitochondrial outer membrane. Apoptosis 15, 553-562
32. Usta, J., El Bawab, S., Roddy, P., Szulc, Z. M., Yusuf, Hannun, A. and Bielawska, A. (2001) Structural requirements of ceramide and sphingosine based inhibitors of mitochondrial ceramidase. Biochemistry 40, 9657-9668 (Pubitemid 32757905)
33. Brockman, H. L., Momsen, M. M., Brown, R. E., He, L., Chun, J., Byun, H. S. and Bittman, R. (2004) The 4,5-double bond of ceramide regulates its dipole potential, elastic properties, and packing behavior. Biophys. J. 87, 1722-1731 (Pubitemid 39167028)
34. He, L., Byun, H. S. and Bittman, R. (2000) A stereocontrolled, efficient synthetic route to bioactive sphingolipids: synthesis of phytosphingosine and phytoceramides from unsaturated ester precursors via cyclic sulfate intermediates. J. Org. Chem. 65, 7618-7626
35. He, L., Byun, H. S. and Bittman, R. (2000) Stereoselective preparation of ceramide and its skeleton backbone modified analogues via cyclic thionocarbonate intermediates derived by catalytic asymmetric dihydroxylation of α,β-unsaturated ester precursors. J. Org. Chem. 65, 7627-7633
36. Bieberich, E., Hu, B., Silva, J., MacKinnon, S., Yu, R. K., Fillmore, H., Broaddus, W. C. and Ottenbrite, R. M. (2002) Synthesis and characterization of novel ceramide analogs for induction of apoptosis in human cancer cells. Cancer Lett. 181, 55-64 (Pubitemid 34310662)
37. Parsons, D. F., Williams, G. R. and Chance, B. (1966) Characteristics of isolated and purified preparations of the outer and inner membranes of mitochondria. Ann. N.Y. Acad. Sci. 137, 643-666
38. Douce, R., Bourguignon, J., Brouquisse, R. and Neuburger, M. (1987) Isolation of plant mitochondria: general principles and criteria of integrity. Methods Enzymol. 148, 403-415
39. Suzuki, M., Youle, R. J. and Tjandra, N. (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103, 645-654
40. Basañez, G., Zhang, J., Chau, B. N., Maksaev, G. I., Frolov, V. A., Brandt, T. A., Burch, J., Hardwick, J. M. and Zimmerberg, J. (2001) Pro-apoptotic cleavage products of Bcl-xL form cytochrome c -conducting pores in pure lipid membranes. J. Biol. Chem. 276, 31083-31091
41. Wojtczak, L., Zaluska, H., Wroniszewska, A. and Wojtczak, A. B. (1972) Assay for the intactness of the outer membrane in isolated mitochondria. Acta Biochim. Pol. 19, 227-234
42. Kluck, R. M., Esposti, M. D., Perkins, G., Renken, C., Kuwana, T., Bossy-Wetzel, E., Goldberg, M., Allen, T., Barber, M. J., Green, D. R. and Newmeyer, D. D. (1999) The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J. Cell Biol. 147, 809-822
43. von Ahsen, O., Renken, C., Perkins, G., Kluck, R. M., Bossy-Wetzel, E. and Newmeyer, D. D. (2000) Preservation of mitochondrial structure and function after Bid- or Bax-mediated cytochrome c release. J. Cell Biol. 150, 1027-1036
44. Li, F., Srinivasan, A., Wang, Y., Armstrong, R. C., Tomaselli, K. J. and Fritz, L. C. (1997) Cell-specific induction of apoptosis by microinjection of cytochrome c : Bcl-xL has activity independent of cytochrome c release. J. Biol. Chem. 272, 30299-30305 (Pubitemid 27512235)
45. Zhivotovsky, B., Orrenius, S., Brustugun, O. T. and Doskeland, S. O. (1998) Injected cytochrome c induces apoptosis. Nature 391, 449-450
46. Grösch, S., Schiffmann, S. and Geisslinger, G. (2012) Chain length-specific properties of ceramides. Prog. Lipid Res. 51, 50-62
47. Menuz, V., Howell, K. S., Gentina, S., Epstein, S., Riezman, I., Fornallaz-Mulhauser, M., Hengartner, M. O., Gomez, M., Riezman, H. and Martinou, J. C. (2009) Protection of C. elegans from anoxia by HYL-2 ceramide synthase. Science 324, 381-384
48. 18-(dihydro)ceramide) synthesis in a fumonisin B1-independent manner in mammalian cells. J. Biol. Chem. 277, 35642-35649
49. Mizutani, Y., Kihara, A. and Igarashi, Y. (2005) Mammalian Lass6 and its related family members regulate synthesis of specific ceramides. Biochem. J. 390, 263-271 (Pubitemid 41192252)
50. Laviad, E. L., Albee, L., Pankova-Kholmyansky, I., Epstein, S., Park, H., Merrill, A. H. and Futerman, A. H. (2008) Characterization of ceramide synthase 2: tissue distribution, substrate specificity, and inhibition by sphingosine 1-phosphate. J. Biol. Chem. 283, 5677-5684
51. Riebeling, C., Allegood, J. C., Wang, E., Merrill, A. H. and Futerman, A. H. (2003) Two mammalian longevity assurance gene (LAG1) family members, trh1 and trh4, regulate dihydroceramide synthesis using different fatty acyl-CoA donors. J. Biol. Chem. 278, 43452-43459 (Pubitemid 37345968)
52. 24-ceramide formation and sphingolipid-dependent activation of the proteasome. J. Biol. Chem. 278, 14723-14731
53. Wijesinghe, D. S., Massiello, A., Subramanian, P., Szulc, Z., Bielawska, A. and Chalfant, C. E. (2005) Substrate specificity of human ceramide kinase. J. Lipid Res. 46, 2706-2716 (Pubitemid 43107483)
54. Phillips, S. C., Triola, G., Fabrias, G., Goñi, F. M., DuPré, D. B. and Yappert, M. C. (2009) cis- versus trans-ceramides: effects of the double bond on conformation and H-bonding interactions. J. Phys. Chem. B. 113, 15249-15255
55. Perera, M. N., Ganesan, V., Siskind, L. J., Szulc, Z. M., Bielawski, J., Bielawska, A., Bittman, R. and Colombini, M. (2012) Ceramide channels: influence of molecular structure on channel formation in membranes. Biochim. Biophys. Acta 1818, 1291-1301
56. Manion, M. K., O'Neill, J. W., Giedt, C. D., Kim, K. M., Zhang, K. Y. and Hockenbery, D. M. (2004) Bcl-XL mutations suppress cellular sensitivity to antimycin A. J. Biol. Chem. 279, 2159-2165 (Pubitemid 38084489)
57. Tse, C., Shoemaker, A. R., Adickes, J., Anderson, M. G., Chen, J., Jin, S., Johnson, E. F., Marsh, K. C., Mitten, M. J., Nimmer, P. et al. (2008) ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res. 68, 3421-3428
58. Wendt, M. D., Shen, W., Kunzer, A., McClellan, W. J., Bruncko, M., Oost, T. K., Ding, H., Joseph, M. K., Zhang, H., Nimmer, P. M. et al. (2006) Discovery and structure-activity relationship of antagonists of B-cell lymphoma 2 family proteins with chemopotentiation activity in vitro and in vivo. J. Med. Chem. 49, 1165-1181 (Pubitemid 43221663)