Emerging roles of lipids in BCL-2 family-regulated apoptosis

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1831, Issue 10, 2013, Pages 1542-1554

  Zhang, Tejia ^a   Saghatelian, Alan ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Apoptosis; BCL 2 protein; Lipid; Metabolism; Mitochondrion

Indexed keywords

BH3 PROTEIN; CARDIOLIPIN; CASPASE 8; CELL MEMBRANE PROTEIN; CERAMIDE; CYTOCHROME C; LIPID; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; SMALL INTERFERING RNA; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOSINE KINASE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2;

ALPHA HELIX; APOPTOSIS; CELL MEMBRANE; CELL STRAIN MCF 7; CHANNEL GATING; ENZYME ACTIVATION; HELA CELL; HUMAN; LIPID METABOLISM; MASS SPECTROMETRY; METABOLISM; MITOCHONDRIAL MEMBRANE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN HOMEOSTASIS; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84885179403     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.03.001     Document Type: Review

References (209)

1. F. Gonzalvez, Z.T. Schug, R.H. Houtkooper, E.D. MacKenzie, D.G. Brooks, R.J.A. Wanders, P.X. Petit, F.M. Vaz, E. Gottlieb, Cardiolipin provides an essential activating platform for caspase-8 on mitochondria, J. Cell Biol. 183 (2008) 681-696.
2. LD. Walensky, BCL-2 in the crosshairs: tipping the balance of life and death, Cell Death Differ. 13 (2006) 1339-1350. (Pubitemid 44057469)
3. J.I. Fletcher, D.C.S. Huang, BH3-only proteins: orchestrating cell death, Cell Death Differ. 13 (2006) 1268-1271. (Pubitemid 44057457)
4. E. Gavathiotis, M. Suzuki, M.L. Davis, K. Pitter, G.H. Bird, S.G. Katz, H.-C. Tu, H. Kim, E.H.Y. Cheng, N. Tjandra, LD. Walensky, BAX activation is initiated at a novel interaction site, Nature 455 (2008) 1076-1081.
5. G. van Loo, X. Saelens, M. van Gurp, M. MacFarlane, S.J. Martin, P. Vandenabeele, The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet, Cell Death Differ. 9 (2002) 1031-1042.
6. M. Crimi, M.D. Esposti, Apoptosis-induced changes in mitochondrial lipids, Biochim. Biophys. Acta Mol. Cell Res. 1813 (2011) 551-557.
7. Z.T. Schug, E. Gottlieb, Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis, Biochim. Biophys. Acta Biomembr. 1788 (2009) 2022-2031.
8. T.S. Tirodkar, C. Voelkel-Johnson, Sphingolipids in apoptosis, Exp. Oncol. 34 (2012) 231-242.
9. S.M. Claypool, C.M. Koehler, The complexity of cardiolipin in health and disease, Trends Biochem. Sci. 37 (2012) 32-41.
10. D. Canals, D.M. Perry, R.W. Jenkins, Y.A. Hannun, Drug targeting of sphingolipid metabolism: sphingomyelinases and ceramidases, Br. J. Pharmacol. 163 (2011) 694-712.
11. J.R. Van Brocklyn, J.B. Williams, The control of the balance between ceramide and sphingosine-1-phosphate by sphingosine kinase: oxidative stress and the seesaw of cell survival and death, Comp. Biochem. Physiol. B Biochem. Mol. Biol. 163 (2012) 26-36.
12. N. Robinson, Functional binding of cardiolipin to cytochromec oxidase, J. Bioenerg. Biomembr. 25 (1993) 153-163. (Pubitemid 23133523)
13. Jerry E. Chipuk, Gavin P. McStay, A. Bharti, T. Kuwana, Christopher J. Clarke, Leah J. Siskind, Lina M. Obeid, Douglas R. Green, Sphingolipid metabolism cooperates with BAK and BAX to promote the mitochondrial pathway of apoptosis, Cell 148 (2012) 988-1000.
14. T.D. Mullen, Y.A. Hannun, L.M. Obeid, Ceramide synthases at the centre of sphingolipid metabolism and biology, Biochem. J. 441 (2012) 789-802.
15. The AOCS Lipid Library, http://lipidlibrary.aocs.org2013.
16. B.J. Pettus, C.E. Chalfant, Y.A. Hannun, Ceramide in apoptosis: an overview and current perspectives, Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1585 (2002) 114-125. (Pubitemid 36092075)
17. T.D. Mullen, L. Obeid, Ceramide and apoptosis: exploring the enigmatic connections between sphingolipid metabolism and programmed cell death, Anticancer Agents Med. Chem. 12 (2012) 340-363.
18. A.H. Futerman, H. Riezman, The ins and outs of sphingolipid synthesis, Trends Cell Biol. 15 (2005) 312-318. (Pubitemid 40805327)
19. A.H. Futerman, Y.A. Hannun, The complex life of simple sphingolipids, EMBO Rep. 5 (2004) 777-782. (Pubitemid 39199166)
20. F.M. Goñi, A. Alonso, Sphingomyelinases: enzymology and membrane activity, FEBS Lett. 531 (2002) 38-46. (Pubitemid 35232782)
21. A.H. Merrill Jr., D.D. Jones, An update of the enzymology and regulation of sphingomyelin metabolism, Biochim. Biophys. Acta Lipids Lipid Metab. 1044 (1990) 1-12. (Pubitemid 20144101)
22. D.L. Siow, C.D. Anderson, E.V. Berdyshev, A. Skobeleva, V. Natarajan, S.M. Pitson, B.W. Wattenberg, Sphingosine kinase localization in the control of sphingolipid metabolism, Adv. Enzyme Regul. 51 (2011) 229-244.
23. M. Serra, J.D. Saba, Sphingosine 1-phosphate lyase, a key regulator of sphingosine 1-phosphate signaling and function, Adv. Enzyme Regul. 50 (2010) 349-362.
24. S. El Bawab, H. Birbes, P. Roddy, Z.M. Szulc, A. Bielawska, Y.A. Hannun, Biochemical characterization of the reverse activity of rat brain ceramidase: a CoA-independent and fumonisin B1-insensitive ceramide synthase, J. Biol. Chem. 276 (2001) 16758-16766.
25. M. Tani, N. Okino, S. Mitsutake, T. Tanigawa, H. Izu, M. Ito, Purification and characterization of a neutral ceramidase from mouse liver: a single protein catalyzes the reversible reaction in which ceramide is both hydrolyzed and synthesized, J. Biol. Chem. 275 (2000) 3462-3468. (Pubitemid 30083054)
26. S.A. Novgorodov, B.X. Wu, T.I. Gudz, J. Bielawski, T.V. Ovchinnikova, Y.A. Hannun, L.M. Obeid, Novel pathway of ceramide production in mitochondria: thioesterase and neutral ceramidase produce ceramide from sphingosine and acyl-CoA, J. Biol. Chem. 286 (2011) 25352-25362.
27. Y.A. Hannun, L.M. Obeid, Many ceramides, J. Biol. Chem. 286 (2011) 27855-27862.
28. M.M. Young, M. Kester, H.-G. Wang, Sphingolipids: regulators of crosstalk between apoptosis and autophagy, J. Lipid Res. 54 (2013) 5-19.
29. J. Mesicek, H. Lee, T. Feldman, X. Jiang, A. Skobeleva, E.V. Berdyshev, A. Haimovitz-Friedman, Z. Fuks, R. Kolesnick, Ceramide synthases 2, 5, and 6 confer distinct roles in radiation-induced apoptosis in HeLa cells, Cell. Signal. 22 (2010) 1300-1307.
30. C.E. Senkal, S. Ponnusamy, J. Bielawski, Y.A. Hannun, B. Ogretmen, Antiapoptotic roles of ceramide-synthase-6-generated C16-ceramide via selective regulation of the ATF6/CHOP arm of ER-stress-response pathways, FASEB J. 24 (2010) 296-308.
31. T.A. Taha, T.D. Mullen, L.M. Obeid, A house divided: ceramide, sphingosine, and sphingosine-1-phosphate in programmed cell death, Biochim. Biophys. Acta Biomembr. 1758 (2006) 2027-2036. (Pubitemid 44879375)
32. S. Pyne, R. Bittman, N.J. Pyne, Sphingosine kinase inhibitors and cancer: seeking the golden sword of Hercules, Cancer Res. 71 (2011) 6576-6582.
33. H. Lee, J.A. Rotolo, J. Mesicek, T. Penate-Medina, A. Rimner, W.-C. Liao, X. Yin, G. Ragupathi, D. Ehleiter, E. Gulbins, D. Zhai, J.C. Reed, A. Haimovitz-Friedman, Z. Fuks, R. Kolesnick, Mitochondrial ceramide-rich macrodomains functionalize Bax upon irradiation, PLoS One 6 (2011) e19783.
34. R. Kolesnick, The therapeutic potential of modulating the ceramide/sphingomyelin pathway, J. Clin. Invest. 110 (2002) 3-8. (Pubitemid 34743457)
35. R.L. Shaner, J.C. Allegood, H. Park, E. Wang, S. Kelly, C.A. Haynes, M.C. Sullards, A.H. Merrill, Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers, J. Lipid Res. 50 (2009) 1692-1707.
36. E. Martínez-Abundis, F. Correa, N. Pavón, C. Zazueta, Bax distribution into mitochondrial detergent-resistant microdomains is related to ceramide and cholesterol content in postischemic hearts, FEBS J. 276 (2009) 5579-5588.
37. Y.A. Hannun, R.M. Bell, Functions of sphingolipids and sphingolipid breakdown products in cellular regulation, Science 243 (1989) 500-507. (Pubitemid 19048748)
38. T. Okazaki, R.M. Bell, Y.A. Hannun, Sphingomyelin turnover induced by vitamin D3 in HL-60 cells. Role in cell differentiation, J. Biol. Chem. 264 (1989) 19076-19080. (Pubitemid 19285812)
39. P. Irun, M. Mallén, C. Dominguez, V. Rodriguez-Sureda, L.A. Alvarez-Sala, N. Arslan, N. Bermejo, C. Guerrero, I. Perez de Soto, L. Villalón, P. Giraldo, M. Pocovi, Identification of seven novel SMPD1 mutations causing Niemann-Pick disease types A and B, Clin. Genet. (article first published online on Jan. 4, 2013).
40. H. Birbes, S. El Bawab, Y.A. Hannun, L.M. Obeid, Selective hydrolysis of a mitochondrial pool of sphingomyelin induces apoptosis, FASEB J. 15 (2001) 2669-2679. (Pubitemid 33131093)
41. P. Zhang, B. Liu, G.M. Jenkins, Y.A. Hannun, L.M. Obeid, Expression of neutral sphingomyelinase identifies a distinct pool of sphingomyelin involved in apoptosis, J. Biol. Chem. 272 (1997) 9609-9612. (Pubitemid 27171616)
42. M. Sawada, S. Nakashima, Y. Banno, H. Yamakawa, K. Hayashi, K. Takenaka, Y. Nishimura, N. Sakai, Y. Nozawa, Ordering of ceramide formation, caspase activation, and Bax/Bcl-2 expression during etoposide-induced apoptosis in C6 glioma cells, Cell Death Differ. 7 (2000) 761-772.
43. G. Ion, R. Fajka-Boja, F. Kovács, G. Szebeni, I. Gombos, Á. Czibula, J. Matkó, É. Monostori, Acid sphingomyelinase mediated release of ceramide is essential to trigger the mitochondrial pathway of apoptosis by galectin-1, Cell. Signal. 18 (2006) 1887-1896. (Pubitemid 44485979)
44. M.A. Mikati, M. Zeinieh, R.A. Habib, J. El Hokayem, A. Rahmeh, M. El Sabban, J. Usta, G. Dbaibo, Changes in sphingomyelinases, ceramide, Bax, Bcl2, and caspase-3 during and after experimental status epilepticus, Epilepsy Res. 81 (2008) 161-166.
45. C. Dumitru, I. Sandalcioglu, M. Wagner, M. Weller, E. Gulbins, Lysosomal ceramide mediates gemcitabine-induced death of glioma cells, J. Mol. Med. 87 (2009) 1123-1132.
46. C.-M. Tang, C.-S. Hwang, S.-D. Chen, D.-I. Yang, Neuroprotective mechanisms of minocycline against sphingomyelinase/ceramide toxicity: roles of Bcl-2 and thioredoxin, Free Radic. Biol. Med. 50 (2011) 710-721.
47. J. Jin, Q. Hou, T.D. Mullen, Y.H. Zeidan, J. Bielawski, J.M. Kraveka, A. Bielawska, L.M. Obeid, Y.A. Hannun, Y.-T. Hsu, Ceramide generated by sphingomyelin hydrolysis and the salvage pathway is involved in hypoxia/reoxygenation-induced bax redistribution to mitochondria in NT-2 cells, J. Biol. Chem. 283 (2008) 26509-26517.
48. M.-C. Morales, G. Pérez-Yarza, N.N. Rementería, M.-D. Boyano, A. Apraiz, A. Gómez-Muñoz, E. Pérez-Andrés, A. Asumendi, 4-HPR-mediated leukemia cell cytotoxicity is triggered by ceramide-induced mitochondrial oxidative stress and is regulated downstream by Bcl-2, Free Radic. Res. 41 (2007) 591-601. (Pubitemid 46511124)
49. H. Birbes, C. Luberto, Y.-T. Hsu, S. El Bawab, Y.A. Hannun, L.M. Obeid, A mitochondrial pool of sphingomyelin is involved in TNFalpha-induced Bax translocation to mitochondria, Biochem. J. 386 (2005) 445-451. (Pubitemid 40445868)
50. G.S. Dbaibo, W. El-Assaad, A. Krikorian, B. Liu, K. Diab, N.Z. Idriss, M. El-Sabban, T.A. Driscoll, D.K. Perry, Y.A. Hannun, Ceramide generation by two distinct pathways in tumor necrosis factor α-induced cell death, FEBS Lett. 503 (2001) 7-12. (Pubitemid 32769946)
51. H. Kashkar, K. Wiegmann, B. Yazdanpanah, D. Haubert, M. Krönke, Acid sphingomyelinase is indispensable for UV light-induced Bax conformational change at the mitochondrial membrane, J. Biol. Chem. 280 (2005) 20804-20813. (Pubitemid 40776785)
52. K. Horinouchi, S. Erlich, D.P. Perl, K. Ferlinz, C.L. Bisgaier, K. Sandhoff, R.J. Desnick, C.L. Stewart, E.H. Schuchman, Acid sphingomyelinase deficient mice: a model of types A and B Niemann-Pick disease, Nat. Genet. 10 (1995) 288-293.
53. P. Santana, L.A. Peña, A. Haimovitz-Friedman, S. Martin, D. Green, M. McLoughlin, C. Cordon-Cardo, E.H. Schuchman, Z. Fuks, R. Kolesnick, Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis, Cell 86 (1996) 189-199. (Pubitemid 26286102)
54. C. García-Ruiz, A. Colell, M. Montserrat, A. Morales, M. Calvo, C. Enrich, J.C. Fernández-Checa, Defective TNF-α-mediated hepatocellular apoptosis and liver damage in acidic sphingomyelinase knockout mice, J. Clin. Invest. 111 (2003) 197-208. (Pubitemid 36105918)
55. N.T. Xuan, E. Shumilina, E. Schmid, S.K. Bhavsar, R. Rexhepaj, F. Götz, E. Gulbins, F. Lang, Role of acidic sphingomyelinase in thymol-mediated dendritic cell death, Mol. Nutr. Food Res. 54 (2010) 1833-1841.
56. C. Ginkel, D. Hartmann, K. vom Dorp, A. Zlomuzica, H. Farwanah, M. Eckhardt, R. Sandhoff, J. Degen, M. Rabionet, E. Dere, P. Dörmann, K. Sandhoff, K. Willecke, Ablation of neuronal ceramide synthase 1 in mice decreases ganglioside levels and expression of myelin-associated glycoprotein in oligodendrocytes, J. Biol. Chem. 287 (2012) 41888-41902.
57. Y. Pewzner-Jung, H. Park, E.L. Laviad, L.C. Silva, S. Lahiri, J. Stiban, R. Erez-Roman, B. Brügger, T. Sachsenheimer, F. Wieland, M. Prieto, A.H. Merrill, A.H. Futerman, A critical role for ceramide synthase 2 in liver homeostasis: I. Alterations in lipid metabolic pathways, J. Biol. Chem. 285 (2010) 10902-10910.
58. S. Imgrund, D. Hartmann, H. Farwanah, M. Eckhardt, R. Sandhoff, J. Degen, V. Gieselmann, K. Sandhoff, K. Willecke, Adult ceramide synthase 2 (CERS2)-deficient mice exhibit myelin sheath defects, cerebellar degeneration, and hepatocarcinomas, J. Biol. Chem. 284 (2009) 33549-33560.
59. R. Jennemann, M. Rabionet, K. Gorgas, S. Epstein, A. Dalpke, U. Rothermel, A. Bayerle, F. van der Hoeven, S. Imgrund, J. Kirsch, W. Nickel, K. Willecke, H. Riezman, H.-J. Gröne, R. Sandhoff, Loss of ceramide synthase 3 causes lethal skin barrier disruption, Hum. Mol. Genet. 21 (2012) 586-608.
60. T.D. Mullen, S. Spassieva, R.W. Jenkins, K. Kitatani, J. Bielawski, Y.A. Hannun, L.M. Obeid, Selective knockdown of ceramide synthases reveals complex interregulation of sphingolipid metabolism, J. Lipid Res. 52 (2011) 68-77.
61. C.E. Chalfant, K. Rathman, R.L. Pinkerman, R.E. Wood, L.M. Obeid, B. Ogretmen, Y.A. Hannun, De novo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells: dependence on protein phosphatase-1, J. Biol. Chem. 277 (2002) 12587-12595. (Pubitemid 34952617)
62. Z.-H. Lu, Y.-M. Mu, B.-A. Wang, X.-L. Li, J.-M. Lu, J.-Y. Li, C.-Y. Pan, T. Yanase, H. Nawata, Saturated free fatty acids, palmitic acid and stearic acid, induce apoptosis by stimulation of ceramide generation in rat testicular Leydig cell, Biochem. Biophys. Res. Commun. 303 (2003) 1002-1007. (Pubitemid 36390242)
63. S.-T. Huang, R.-C. Yang, M.-Y. Chen, J.-H.S. Pang, Phyllanthus urinaria induces the Fas receptor/ligand expression and ceramide-mediated apoptosis in HL-60 cells, Life Sci. 75 (2004) 339-351. (Pubitemid 38591645)
64. J. Jin, T.D. Mullen, Q. Hou, J. Bielawski, A. Bielawska, X. Zhang, L.M. Obeid, Y.A. Hannun, Y.-T. Hsu, AMPK inhibitor Compound C stimulates ceramide production and promotes Bax redistribution and apoptosis in MCF7 breast carcinoma cells, J. Lipid Res. 50 (2009) 2389-2397.
65. L.J. Siskind, T.D. Mullen, K. Romero Rosales, C.J. Clarke, M.J. Hernandez-Corbacho, A.L. Edinger, L.M. Obeid, The BCL-2 protein BAK is required for long-chain ceramide generation during apoptosis, J. Biol. Chem. 285 (2010) 11818-11826.
66. X. Deng, X. Yin, R. Allan, D.D. Lu, C.W. Maurer, A. Haimovitz-Friedman, Z. Fuks, S. Shaham, R. Kolesnick, Ceramide biogenesis is required for radiation-induced apoptosis in the germ line of C. elegans, Science 322 (2008) 110-115.
67. K. Kitatani, J. Idkowiak-Baldys, Y.A. Hannun, The sphingolipid salvage pathway in ceramide metabolism and signaling, Cell. Signal. 20 (2008) 1010-1018.
68. D. Hartmann, J. Lucks, S. Fuchs, S. Schiffmann, Y. Schreiber, N. Ferreirós, J. Merkens, R. Marschalek, G. Geisslinger, S. Grösch, Long chain ceramides and very long chain ceramides have opposite effects on human breast and colon cancer cell growth, Int. J. Biochem. Cell Biol. 44 (2012) 620-628.
69. T.D. Mullen, R.W. Jenkins, C.J. Clarke, J. Bielawski, Y.A. Hannun, L.M. Obeid, Ceramide synthase-dependent ceramide generation and programmed cell death: involvement of salvage pathway in regulating postmitochondrial events, J. Biol. Chem. 286 (2011) 15929-15942.
70. T. Kohama, A. Olivera, L. Edsall, M.M. Nagiec, R. Dickson, S. Spiegel, Molecular cloning and functional characterization of murine sphingosine kinase, J. Biol. Chem. 273 (1998) 23722-23728. (Pubitemid 28435703)
71. H. Liu, M. Sugiura, V.E. Nava, L.C. Edsall, K. Kono, S. Poulton, S. Milstien, T. Kohama, S. Spiegel, Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform, J. Biol. Chem. 275 (2000) 19513-19520. (Pubitemid 30441543)
72. M. Maceyka, K.B. Harikumar, S. Milstien, S. Spiegel, Sphingosine-1- phosphate signaling and its role in disease, Trends Cell Biol. 22 (2012) 50-60.
73. M. Maceyka, H. Sankala, N.C. Hait, H. Le Stunff, H. Liu, R. Toman, C. Collier, M. Zhang, L.S. Satin, A.H. Merrill, S. Milstien, S. Spiegel, SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism, J. Biol. Chem. 280 (2005) 37118-37129. (Pubitemid 41587796)
74. X. Liu, Q.-H. Zhang, G.-H. Yi, Regulation of metabolism and transport of sphingosine-1-phosphate in mammalian cells, Mol. Cell. Biochem. 363 (2012) 21-33.
75. H. Liu, R.E. Toman, S.K. Goparaju, M. Maceyka, V.E. Nava, H. Sankala, S.G. Payne, M. Bektas, I. Ishii, J. Chun, S. Milstien, S. Spiegel, Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis, J. Biol. Chem. 278 (2003) 40330-40336. (Pubitemid 37248601)
76. M.L. Allende, T. Sasaki, H. Kawai, A. Olivera, Y. Mi, G. van Echten-Deckert, R. Hajdu, M. Rosenbach, C.A. Keohane, S. Mandala, S. Spiegel, R.L. Proia, Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720, J. Biol. Chem. 279 (2004) 52487-52492. (Pubitemid 39656625)
77. Y. Kharel, S. Lee, A.H. Snyder, S.L. Sheasley-O'Neill, M.A. Morris, Y. Setiady, R. Zhu, M.A. Zigler, T.L. Burcin, K. Ley, K.S.K. Tung, V.H. Engelhard, T.L. Macdonald, S. Pearson-White, K.R. Lynch, Sphingosine kinase 2 is required for modulation of lymphocyte traffic by FTY720, J. Biol. Chem. 280 (2005) 36865-36872. (Pubitemid 41587768)
78. D.A. Vessey, L. Li, Z.-Q. Jin, M. Kelley, N. Honbo, J. Zhang, J.S. Karliner, A sphingosine kinase form 2 knockout sensitizes mouse myocardium to ischemia/reoxygenation injury and diminishes responsiveness to ischemic preconditioning, Oxid. Med. Cell. Longev. 2011 (2011) 8, http://dx.doi.org/10. 1155/2011/961059 (Article ID 961059).
79. K. Mizugishi, T. Yamashita, A. Olivera, G.F. Miller, S. Spiegel, R.L. Proia, Essential role for sphingosine kinases in neural and vascular development, Mol. Cell. Biol. 25 (2005) 11113-11121. (Pubitemid 41747151)
80. H.J. Kim, J.Y. Mun, Y.J. Chun, K.H. Choi, M.Y. Kim, Bax-dependent apoptosis induced by ceramide in HL-60 cells, FEBS Lett. 505 (2001) 264-268. (Pubitemid 32896678)
81. M. Manggau, D.-S. Kim, L. Ruwisch, R. Vogler, H.C. Korting, M. Schafer-Korting, B. Kleuser, 1α,25-Dihydroxyvitamin D3 protects human keratinocytes from apoptosis by the formation of sphingosine-1-phosphate, 117 (2001) 1241-1249.
82. B. Sauer, H. Gonska, M. Manggau, D.S. Kim, C. Schraut, M. Schafer-Korting, B. Kleuser, Sphingosine 1-phosphate is involved in cytoprotective actions of calcitriol in human fibroblasts and enhances the intracellular Bcl-2/Bax rheostat, Pharmazie 60 (2005) 298-304. (Pubitemid 40571196)
83. O. Cuvillier, T. Levade, Sphingosine 1-phosphate antagonizes apoptosis of human leukemia cells by inhibiting release of cytochrome c and Smac/DIABLO from mitochondria, Blood 98 (2001) 2828-2836.
84. V. Limaye, X. Li, C. Hahn, P. Xia, M.C. Berndt, M.A. Vadas, J.R. Gamble, Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1-dependent activation of PI-3K/Akt and regulation of Bcl-2 family members, Blood 105 (2005) 3169-3177.
85. J.R. Gamble, W.Y. Sun, X. Li, C.N. Hahn, S.M. Pitson, M.A. Vadas, C.S. Bonder, Sphingosine kinase-1 associates with integrin αVβ3 to mediate endothelial cell survival, Am. J. Pathol. 175 (2009) 2217-2225.
86. H. Guan, L. Song, J. Cai, Y. Huang, J. Wu, J. Yuan, J. Li, M. Li, Sphingosine kinase 1 regulates the Akt/FOXO3a/Bim pathway and contributes to apoptosis resistance in glioma cells, PLoS One 6 (2011) e19946.
87. M. Bektas, P.S. Jolly, C. Muller, J. Eberle, S. Spiegel, C.C. Geilen, Sphingosine kinase activity counteracts ceramide-mediated cell death in human melanoma cells: role of Bcl-2 expression, Oncogene 24 (2005) 178-187. (Pubitemid 40143877)
88. Q.F. Li, W.R. Huang, H.F. Duan, H. Wang, C.T. Wu, L.S. Wang, Sphingosine kinase-1 mediates BCR//ABL-induced upregulation of Mcl-1 in chronic myeloid leukemia cells, Oncogene 26 (2007) 7904-7908. (Pubitemid 350261782)
89. E. Bonhoure, A. Lauret, D.J. Barnes, C. Martin, B. Malavaud, T. Kohama, J.V. Melo, O. Cuvillier, Sphingosine kinase-1 is a downstream regulator of imatinib-induced apoptosis in chronic myeloid leukemia cells, Leukemia 22 (2008) 971-979. (Pubitemid 351689879)
90. Q.-F. Li, J. Yan, K. Zhang, Y.-F. Yang, F.-J. Xiao, C.-T. Wu, H. Wang, L.-S. Wang, Bortezomib and sphingosine kinase inhibitor interact synergistically to induces apoptosis in BCR/ABl+ cells sensitive and resistant to STI571 through down-regulation Mcl-1, Biochem. Biophys. Res. Commun. 405 (2011) 31-36.
91. T.A. Taha, K. Kitatani, M. El-Alwani, J. Bielawski, Y.A. Hannun, L.M. Obeid, Loss of sphingosine kinase-1 activates the intrinsic pathway of programmed cell death: modulation of sphingolipid levels and the induction of apoptosis, FASEB J. 20 (2005) 482-484. (Pubitemid 46671223)
92. M. Sawada, S. Nakashima, Y. Banno, H. Yamakawa, K. Takenaka, J. Shinoda, Y. Nishimura, N. Sakai, Y. Nozawa, Influence of Bax of Bcl-2 overexpression on the ceramide-dependent apoptotic pathway in glioma cells, Oncogene 19 (2000) 3508-3520. (Pubitemid 30487448)
93. S.-i. Yoshimura, Y. Banno, S. Nakashima, K. Takenaka, H. Sakai, Y. Nishimura, N. Sakai, S. Shimizu, Y. Eguchi, Y. Tsujimoto, Y. Nozawa, Ceramide formation leads to caspase-3 activation during hypoxic PC12 cell death: inhibitory effects of Bcl-2 on ceramide formation and caspase-3 activation, J. Biol. Chem. 273 (1998) 6921-6927. (Pubitemid 28160357)
94. Y. Okamoto, L.M. Obeid, Y.A. Hannun, Bcl-xL interrupts oxidative activation of neutral sphingomyelinase, FEBS Lett. 530 (2002) 104-108. (Pubitemid 35248194)
95. T.A. Taha, W. Osta, L. Kozhaya, J. Bielawski, K.R. Johnson, W.E. Gillanders, G.S. Dbaibo, Y.A. Hannun, L.M. Obeid, Down-regulation of sphingosine kinase-1 by DNA damage: dependence on proteases and p53, J. Biol. Chem. 279 (2004) 20546-20554. (Pubitemid 38623502)
96. D.A. Wiesner, J.P. Kilkus, A.R. Gottschalk, J. Quintáns, G. Dawson, Anti-immunoglobulin-induced apoptosis in WEHI 231 cells involves the slow formation of ceramide from sphingomyelin and is blocked by bcl-xL, J. Biol. Chem. 272 (1997) 9868-9876. (Pubitemid 27171654)
97. C. von Haefen, T. Wieder, B. Gillissen, L. Stärck, V. Graupner, B. Dörken, P.T. Daniel, Ceramide induces mitochondrial activation and apoptosis via a Bax-dependent pathway in human carcinoma cells, Oncogene 21 (2002) 4009-4019. (Pubitemid 34679242)
98. J.A. Rotolo, J.G. Maj, R. Feldman, D. Ren, A. Haimovitz-Friedman, C. Cordon-Cardo, E.H.Y. Cheng, R. Kolesnick, Z. Fuks, Bax and Bak do not exhibit functional redundancy in mediating radiation-induced endothelial apoptosis in the intestinal mucosa, Int. J. Radiat. Oncol. Biol. Phys. 70 (2008) 804-815.
99. M. Colombini, Ceramide channels and their role in mitochondria-mediated apoptosis, Biochim. Biophys. Acta Bioenerg. 1797 (2010) 1239-1244.
100. V. Ganesan, M. Colombini, Regulation of ceramide channels by Bcl-2 family proteins, FEBS Lett. 584 (2010) 2128-2134.
101. L.J. Siskind, M. Colombini, The lipids C2- and C16-ceramide form large stable channels: implications for apoptosis, J. Biol. Chem. 275 (2000) 38640-38644. (Pubitemid 32009194)
102. L.J. Siskind, A. Davoody, N. Lewin, S. Marshall, M. Colombini, Enlargement and contracture of C2-ceramide channels, Biophys. J. 85 (2003) 1560-1575.
103. L.J. Siskind, R.N. Kolesnick, M. Colombini, Ceramide channels increase the permeability of the mitochondrial outer membrane to small proteins, J. Biol. Chem. 277 (2002) 26796-26803. (Pubitemid 34951684)
104. L.J. Siskind, R.N. Kolesnick, M. Colombini, Ceramide forms channelsin mitochondrial outer membranes at physiologically relevant concentrations, Mitochondrion 6 (2006) 118-125. (Pubitemid 43872021)
105. J. Stiban, D. Fistere, M. Colombini, Dihydroceramide hinders ceramide channel formation: implications on apoptosis, Apoptosis 11 (2006) 773-780. (Pubitemid 43876846)
106. M.J. Elrick, S. Fluss, M. Colombini, Sphingosine, a product of ceramide hydrolysis, influences the formation of ceramide channels, Biophys. J. 91 (2006) 1749-1756. (Pubitemid 44352439)
107. L. Siskind, S. Fluss, M. Bui, M. Colombini, Sphingosine forms channels in membranes that differ greatly from those formed by ceramide, J. Bioenerg. Biomembr. 37 (2005) 227-236. (Pubitemid 41420459)
108. M.N. Perera, V. Ganesan, L.J. Siskind, Z.M. Szulc, J. Bielawski, A. Bielawska, R. Bittman, M. Colombini, Ceramide channels: influence of molecular structure on channel formation in membranes, Biochim. Biophys. Acta Biomembr. 1818 (2012) 1291-1301.
109. S. Samanta, J. Stiban, T.K. Maugel, M. Colombini, Visualization of ceramide channels by transmission electron microscopy, Biochim. Biophys. Acta Biomembr. 1808 (2011) 1196-1201.
110. V. Ganesan, M. Perera, D. Colombini, D. Datskovskiy, K. Chadha, M. Colombini, Ceramide and activated Bax act synergistically to permeabilize the mitochondrial outer membrane, Apoptosis 15 (2010) 553-562.
111. L.J. Siskind, L. Feinstein, T. Yu, J.S. Davis, D. Jones, J. Choi, J.E. Zuckerman, W. Tan, R.B. Hill, J.M. Hardwick, M. Colombini, Anti-apoptotic Bcl-2 family proteins disassemble ceramide channels, J. Biol. Chem. 283 (2008) 6622-6630.
112. M.N. Perera, S.H. Lin, Y.K. Peterson, A. Bielawska, Z.M. Szulc, R. Bittman, M. Colombini, Bax and Bcl-xL exert their regulation on different sites of the ceramide channel, Biochem. J. 445 (2012) 81-91.
113. S.L. Iverson, S. Orrenius, The cardiolipin-cytochrome c interaction and the mitochondrial regulation of apoptosis, Arch. Biochem. Biophys. 423 (2004) 37-46. (Pubitemid 38198211)
114. J.B. McMillin, W. Dowhan, Cardiolipin and apoptosis, Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1585 (2002) 97-107. (Pubitemid 36092073)
115. J. Zhang, Z. Guan, Anne N. Murphy, Sandra E. Wiley, Guy A. Perkins, Carolyn A. Worby, James L. Engel, P. Heacock, Oanh K. Nguyen, Jonathan H. Wang, Christian R.H. Raetz, W. Dowhan, Jack E. Dixon, Mitochondrial phosphatase PTPMT1 is essential for cardiolipin biosynthesis, Cell Metab. 13 (2011) 690-700.
116. M. Schlame, Thematic Review Series: Glycerolipids. Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes, J. Lipid Res. 49 (2008) 1607-1620.
117. M. Schlame, D. Acehan, B. Berno, Y. Xu, S. Valvo, M. Ren, D.L. Stokes, R.M. Epand, The physical state of lipid substrates provides transacylation specificity for tafazzin, Nat. Chem. Biol. 8 (2012) 862-869.
118. M. Schlame, Cardiolipin remodeling and the function of tafazzin, Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1831 (2013) 582-588.
119. D.J. Mancuso, H.F. Sims, K. Yang, M.A. Kiebish, X. Su, C.M. Jenkins, S. Guan, S.H. Moon, T. Pietka, F. Nassir, T. Schappe, K. Moore, X. Han, N.A. Abumrad, R.W. Gross, Genetic ablation of calcium-independent phospholipase A2γ prevents obesity and insulin resistance during high fat feeding by mitochondrial uncoupling and increased adipocyte fatty acid oxidation, J. Biol. Chem. 285 (2010) 36495-36510.
120. A. Malhotra, I. Edelman-Novemsky, Y. Xu, H. Plesken, J. Ma, M. Schlame, M. Ren, Role of calcium-independent phospholipase A2 in the pathogenesis of Barth syndrome, Proc. Natl. Acad. Sci. 106 (2009) 2337-2341.
121. M. Schlame, S. Blais, I. Edelman-Novemsky, Y. Xu, F. Montecillo, C.K.L. Phoon, M. Ren, T.A. Neubert, Comparison of cardiolipins from Drosophila strains with mutations in putative remodeling enzymes, Chem. Phys. Lipids 165 (2012) 512-519.
122. Y. Xu, M. Condell, H. Plesken, I. Edelman-Novemsky, J. Ma, M. Ren, M. Schlame, A Drosophila model of Barth syndrome, Proc. Natl. Acad. Sci. 103 (2006) 11584-11588. (Pubitemid 44182495)
123. Z. Gu, F. Valianpour, S. Chen, F.M. Vaz, G.A. Hakkaart, R.J.A. Wanders, M.L. Greenberg, Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome, Mol. Microbiol. 51 (2004) 149-158. (Pubitemid 38031078)
124. D. Acehan, F. Vaz, R.H. Houtkooper, J. James, V. Moore, C. Tokunaga, W. Kulik, J. Wansapura, M.J. Toth, A. Strauss, Z. Khuchua, Cardiac and skeletal muscle defects in a mouse model of human Barth syndrome, J. Biol. Chem. 286 (2011) 899-908.
125. S.L. Iverson, M. Enoksson, V. Gogvadze, M. Ott, S. Orrenius, Cardiolipin is not required for Bax-mediated cytochrome c release from yeast mitochondria, J. Biol. Chem. 279 (2004) 1100-1107. (Pubitemid 38082631)
126. K. Wang, X.M. Yin, D.T. Chao, C.L. Milliman, S.J. Korsmeyer, BID: a novel BH3 domain-only death agonist, Genes Dev. 10 (1996) 2859-2869. (Pubitemid 26394246)
127. X. Luo, I. Budihardjo, H. Zou, C. Slaughter, X. Wang, Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors, Cell 94 (1998) 481-490. (Pubitemid 28391864)
128. H. Li, H. Zhu, C.-j. Xu, J. Yuan, Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis, Cell 94 (1998) 491-501. (Pubitemid 28391865)
129. C. Scaffidi, S. Fulda, A. Srinivasan, C. Friesen, F. Li, K.J. Tomaselli, K.-M. Debatin, P.H. Krammer, M.E. Peter, Two CD95 (APO-1/Fas) signaling pathways, EMBO J. 17 (1998) 1675-1687. (Pubitemid 28119121)
130. J.B. Alimonti, L. Shi, P.K. Baijal, A.H. Greenberg, Granzyme B induces BID-mediated cytochrome c release and mitochondrial permeability transition, J. Biol. Chem. 276 (2001) 6974-6982.
131. J.K. Sax, P. Fei, M.E. Murphy, E. Bernhard, S.J. Korsmeyer, W.S. El-Deiry, BID regulation by p53 contributes to chemosensitivity, Nat. Cell Biol. 4 (2002) 842-849. (Pubitemid 35331358)
132. I. Kamer, R. Sarig, Y. Zaltsman, H. Niv, G. Oberkovitz, L. Regev, G. Haimovich, Y. Lerenthal, R.C. Marcellus, A. Gross, Proapoptotic BID is an ATM effector in the DNA-damage response, Cell 122 (2005) 593-603. (Pubitemid 41191157)
133. S.S. Zinkel, K.E. Hurov, C. Ong, F.M. Abtahi, A. Gross, S.J. Korsmeyer, A role for proapoptotic BID in the DNA-damage response, Cell 122 (2005) 579-591. (Pubitemid 41191156)
134. T. Kaufmann, L. Tai, P.G. Ekert, D.C.S. Huang, F. Norris, R.K. Lindemann, R.W. Johnstone, V.M. Dixit, A. Strasser, The BH3-only protein bid is dispensable for DNA damage- and replicative stress-induced apoptosis or cell-cycle arrest, Cell 129 (2007) 423-433. (Pubitemid 46574974)
135. A.J. Valentijn, A.P. Gilmore, Translocation of full-length bid to mitochondria during anoikis, J. Biol. Chem. 279 (2004) 32848-32857. (Pubitemid 39014745)
136. F. Gonzalvez, E. Gottlieb, Cardiolipin: setting the beat of apoptosis, Apoptosis 12 (2007) 877-885. (Pubitemid 46653287)
137. M.G. Fernandez, L. Troiano, L. Moretti, M. Nasi, M. Pinti, S. Salvioli, J. Dobrucki, A. Cossarizza, Early changes in intramitochondrial cardiolipin distribution during apoptosis, Cell Growth Differ. 13 (2002) 449-455.
138. L. Scorrano, M. Ashiya, K. Buttle, S. Weiler, S.A. Oakes, C.A. Mannella, S.J. Korsmeyer, A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis, Dev. Cell 2 (2002) 55-67. (Pubitemid 34065906)
139. M. Lutter, M. Fang, X. Luo, M. Nishijima, X.-s. Xie, X. Wang, Cardiolipin provides specificity for targeting of tBid to mitochondria, Nat. Cell Biol. 2 (2000) 754-761.
140. M. Lutter, G. Perkins, X. Wang, The pro-apoptotic Bcl-2 family member tBid localizes to mitochondrial contact sites, BMC Cell Biol. 2 (2001) 22.
141. T. Kuwana, M.R. Mackey, G. Perkins, M.H. Ellisman, M. Latterich, R. Schneiter, D.R. Green, D.D. Newmeyer, Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane, Cell 111 (2002) 331-342. (Pubitemid 35341388)
142. S. Lucken-Ardjomande, S. Montessuit, J.C. Martinou, Contributions to Bax insertion and oligomerization of lipids of the mitochondrial outer membrane, Cell Death Differ. 15 (2008) 929-937. (Pubitemid 351524434)
143. B. Schafer, J. Quispe, V. Choudhary, J.E. Chipuk, T.G. Ajero, H. Du, R. Schneiter, T. Kuwana, Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation, Mol. Biol. Cell 20 (2009) 2276-2285.
144. O. Landeta, A. Landajuela, D. Gil, S. Taneva, C. DiPrimo, B. Sot, M. Valle, V.A. Frolov, G. Basañez, Reconstitution of proapoptotic BAK function in liposomes reveals a dual role for mitochondrial lipids in the BAK-driven membrane perme-abilization process, J. Biol. Chem. 286 (2011) 8213-8230.
145. G. Dewson, T. Kratina, H.W. Sim, H. Puthalakath, J.M. Adams, P.M. Colman, R.M. Kluck, To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3: groove interactions, Mol. Cell 30 (2008) 369-380. (Pubitemid 351626944)
146. M. Sorice, A. Circella, I.M. Cristea, T. Garofalo, L.D. Renzo, C. Alessandri, G. Valesini, M.D. Esposti, Cardiolipin and its metabolites move from mitochondria to other cellular membranes during death receptor-mediated apoptosis, Cell Death Differ. 11 (2004) 1133-1145. (Pubitemid 39341639)
147. J. Liu, D. Durrant, H.-S. Yang, Y. He, F.G. Whitby, D.G. Myszka, R.M. Lee, The interaction between tBid and cardiolipin or monolysocardiolipin, Biochem. Biophys. Res. Commun. 330 (2005) 865-870. (Pubitemid 40462166)
148. J. Liu, A. Weiss, D. Durrant, N.-w. Chi, R.M. Lee, The cardiolipin-binding domain of Bid affects mitochondrial respiration and enhances cytochrome c release, Apoptosis 9 (2004) 533-541. (Pubitemid 39158629)
149. M.D. Esposti, I.M. Cristea, S.J. Gaskell, Y. Nakao, C. Dive, Proapoptotic Bid binds to monolysocardiolipin, a new molecular connection between mitochondrial membranes and cell death, Cell Death Differ. 10 (2003) 1300-1309. (Pubitemid 37536735)
150. N. Mau, A.V. Kajava, C. Bonfils, J.C. Martinou, M.C. Harricane, Interactions of Bax and tBid with lipid monolayers, J. Membr. Biol. 207 (2005) 1-9. (Pubitemid 43208508)
151. O. Jalmar, A.J. Garcia-Saez, L. Berland, F. Gonzalvez, P.X. Petit, Giant unilamellar vesicles (GUVs) as a new tool for analysis of caspase-8/Bid-FL complex binding to cardiolipin and its functional activity, Cell Death Dis. 1 (2010) e103.
152. A. Goonesinghe, E.S. Mundy, M. Smith, R. Khosravi-Far, J.-C. Martinou, M.D. Esposti, Pro-apoptotic Bid induces membrane perturbation by inserting selected lysolipids into the bilayer, Biochem. J. 387 (2005) 109-118. (Pubitemid 40524080)
153. L. Scorrano, Caspase-8 goes cardiolipin: a new platform to provide mitochondria with microdomains of apoptotic signals? J. Cell Biol. 183 (2008) 579-581.
154. F. Gonzalvez, J.J. Bessoule, F. Rocchiccioli, S. Manon, P.X. Petit, Role of cardiolipin on tBid and tBid//Bax synergistic effects on yeast mitochondria, Cell Death Differ. 12 (2005) 659-667. (Pubitemid 40767168)
155. F. Gonzalvez, F. Pariselli, P. Dupaigne, I. Budihardjo, M. Lutter, B. Antonsson, P. Diolez, S. Manon, J.C. Martinou, M. Goubern, X. Wang, S. Bernard, P.X. Petit, tBid interaction with cardiolipin primarily orchestrates mitochondrial dysfunctions and subsequently activates Bax and Bak, Cell Death Differ. 12 (2005) 614-626. (Pubitemid 40767164)
156. V.E. Kagan, H.A. Bayir, N.A. Belikova, O. Kapralov, Y.Y. Tyurina, V.A. Tyurin, J. Jiang, D.A. Stoyanovsky, P. Wipf, P.M. Kochanek, J.S. Greenberger, B. Pitt, A.A. Shvedova, G. Borisenko, Cytochrome c/cardiolipin relations in mitochondria: a kiss of death, Free Radic. Biol. Med. 46 (2009) 1439-1453.
157. D. Ardail, J.P. Privat, M. Egret-Charlier, C. Levrat, F. Lerme, P. Louisot, Mitochondrial contact sites. Lipid composition and dynamics, J. Biol. Chem. 265 (1990) 18797-18802.
158. V.E. Kagan, V.A. Tyurin, J. Jiang, Y.Y. Tyurina, V.B. Ritov, A.A. Amoscato, A.N. Osipov, N.A. Belikova, A.A. Kapralov, V. Kini, I.I. Vlasova, Q. Zhao, M. Zou, P. Di, D.A. Svistunenko, I.V. Kurnikov, G.G. Borisenko, Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors, Nat. Chem. Biol. 1 (2005) 223-232.
159. E.K.J. Tuominen, C.J.A. Wallace, P.K.J. Kinnunen, Phospholipid-cytochrome c interaction: evidence for the extended lipid anchorage, J. Biol. Chem. 277 (2002) 8822-8826. (Pubitemid 34952948)
160. Y.-L.P. Ow, D.R. Green, Z. Hao, T.W. Mak, Cytochrome c: functions beyond respiration, Nat. Rev. Mol. Cell Biol. 9 (2008) 532-542. (Pubitemid 351881842)
161. E. Goormaghtigh, P. Huart, R. Brasseur, J.M. Ruysschaert, Mechanism of inhibition of mitochondrial enzymatic complex I-III by adriamycin derivatives, Biochim. Biophys. Acta Biomembr. 861 (1986) 83-94. (Pubitemid 16031568)
162. M. Fry, D.E. Green, Cardiolipin requirement for electron transferin complex I and III of the mitochondrial respiratory chain, J. Biol. Chem. 256 (1981) 1874-1880.
163. K. Nicolay, B. de Kruijff, Effects of adriamycin on respiratory chain activities in mitochondria from rat liver, rat heart and bovine heart. Evidence for apreferential inhibition of complex III and IV, Biochim. Biophys. Acta Bioenerg. 892 (1987) 320-330. (Pubitemid 17114235)
164. Z. Beleznai, V. Jancsik, Role of cardiolipin in the functioning of mitochonbrial L-glycerol-3-phosphate dehydrogenase, Biochem. Biophys. Res. Commun. 159 (1989) 132-139. (Pubitemid 19087623)
165. H. Noël, S.V. Pande, An essential requirement of cardiolipin for mitochondrial carnitine acylcarnitine translocase activity, Eur. J. Biochem. 155 (1986) 99-102.
166. K. Beyer, M. Klingenberg, ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by phosphorus-31 nuclear magnetic resonance, Biochemistry 24 (1985) 3821-3826.
167. G. Brandolin, J. Doussiere, A. Gulik, T. Gulik-Krzywicki, G.J.M. Lauquin, P.V. Vignais, Kinetic, binding and ultrastructural properties of the beef heart adenine nucleotide carrier protein after incorporation into phospholipid vesicles, Biochim. Biophys. Acta Bioenerg. 592 (1980) 592-614.
168. R. Krämer, M. Klingenberg, Enhancement of reconstituted ADP, ATP exchange activity by phosphatidylethanolamine and by anionic phospholipids, FEBS Lett. 119 (1980) 257-260.
169. P. Mende, F.J. Hüther, B. Kadenbach, Specific and reversible activation and inactivation of the mitochondrial phosphate carrier by cardiolipin and nonionic detergents, respectively, FEBS Lett. 158 (1983) 331-334.
170. P. Mende, H.V.J. Kolbe, B. Kadenbach, I. Stipani, F. Palmieri, Reconstitution of the isolated phosphate-transport system of pig-heart mitochondria, Eur. J. Biochem. 128 (1982) 91-95.
171. R.S. Kaplan, R.D. Pratt, P.L. Pedersen, Purification and characterization of the reconstitutively active phosphate transporter from rat liver mitochondria, J. Biol. Chem. 261 (1986) 12767-12773. (Pubitemid 17204239)
172. B. Kadenbach, P. Mende, H.V.J. Kolbe, I. Stipani, F. Palmieri, The mitochondrial phosphate carrier has an essential requirement for cardiolipin, FEBS Lett. 139 (1982) 109-112.
173. K.A. Nałecz, R. Bolli, L. Wojtczak, A. Azzi, The monocarboxylate carrier from bovine heart mitochondria: partial purification and its substrate-transporting properties in a reconstituted system, Biochim. Biophys. Acta Bioenerg. 851 (1986) 29-37. (Pubitemid 16049732)
174. L.J. Sparvero, A.A. Amoscato, P.M. Kochanek, B.R. Pitt, V.E. Kagan, H. Bayir, Mass-spectrometry based oxidative lipidomics and lipid imaging: applications in traumatic brain injury, J. Neurochem. 115 (2010) 1322-1336.
175. W. Korytowski, L.V. Basova, A. Pilat, R.M. Kernstock, A.W. Girotti, Permeabilization of the mitochondrial outer membrane by Bax/truncated Bid (tBid) proteins as sensitized by cardiolipin hydroperoxide translocation: mechanistic implications for the intrinsic pathway of oxidative apoptosis, J. Biol. Chem. 286 (2011) 26334-26343.
176. J. Jiang, Z. Huang, Q. Zhao, W. Feng, N.A. Belikova, V.E. Kagan, Interplay between bax, reactive oxygen species production, and cardiolipin oxidation during apoptosis, Biochem. Biophys. Res. Commun. 368 (2008) 145-150.
177. Z. Huang, J. Jiang, V.A. Tyurin, Q. Zhao, A. Mnuskin, J. Ren, N.A. Belikova, W. Feng, I.V. Kurnikov, V.E. Kagan, Cardiolipin deficiency leads to decreased cardiolipin peroxidation and increased resistance of cells to apoptosis, Free Radic. Biol. Med. 44 (2008) 1935-1944.
178. S. Raha, B.H. Robinson, Mitochondria, oxygen free radicals, and apoptosis, Am. J. Med. Genet. 106 (2001) 62-70.
179. M. Ott, J.D. Robertson, V. Gogvadze, B. Zhivotovsky, S. Orrenius, Cytochrome c release from mitochondria proceeds by a two-step process, Proc. Natl. Acad. Sci. 99 (2002) 1259-1263. (Pubitemid 34136480)
180. M. Ott, B. Zhivotovsky, S. Orrenius, Role of cardiolipin in cytochrome c release from mitochondria, Cell Death Differ. 14 (2007) 1243-1247. (Pubitemid 46965253)
181. S.Y. Choi, F. Gonzalvez, G.M. Jenkins, C. Slomianny, D. Chretien, D. Arnoult, P.X. Petit, M.A. Frohman, Cardiolipin deficiency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis, Cell Death Differ. 14 (2006) 597-606.
182. R.F. Epand, J.-C. Martinou, M. Fornallaz-Mulhauser, D.W. Hughes, R.M. Epand, The apoptotic protein tBid promotes leakage by altering membrane curvature, J. Biol. Chem. 277 (2002) 32632-32639. (Pubitemid 34984768)
183. D. Zhai, Q. Miao, X. Xin, F. Yang, Leakage and aggregation of phospholipid vesicles induced by the BH3-only Bcl-2 family member, BID, Eur. J. Biochem. 268 (2001) 48-55. (Pubitemid 32052246)
184. G. Kudla, S. Montessuit, R. Eskes, C. Berrier, J.-C. Martinou, A. Ghazi, B. Antonsson, The destabilization of lipid membranes induced by the C-terminal fragment of caspase 8-cleaved Bid is inhibited by the N-terminal fragment, J. Biol. Chem. 275 (2000) 22713-22718. (Pubitemid 30646152)
185. S.L. Schendel, R. Azimov, K. Pawłowski, A. Godzik, B.L. Kagan, J.C. Reed, Ion channel activity of the BH3 only Bcl-2 family member, BID, J. Biol. Chem. 274 (1999) 21932-21936.
186. K.J. Oh, S. Barbuto, N. Meyer, R.-S. Kim, R.J. Collier, S.J. Korsmeyer, Conformational changes in BID, a pro-apoptotic BCL-2 family member, upon membrane binding: a site-directed spin labeling study, J. Biol. Chem. 280 (2005) 753-767. (Pubitemid 40165044)
187. L. Yan, Q. Miao, Y. Sun, F. Yang, tBid forms a pore in the liposome membrane, FEBS Lett. 555 (2003) 545-550. (Pubitemid 37532608)
188. F. Gonzalvez, F. Pariselli, O. Jalmar, P. Dupaigne, F. Sureau, M. Dellinger, E.A. Hendrickson, S. Bernard, P.X. Petit, Mechanistic issues of the interaction of the hairpin-forming domain of tBid with mitochondrial cardiolipin, PLoS One 5 (2010) e9342.
189. P.X. Petit, P. Dupaigne, F. Pariselli, F. Gonzalvez, F. Etienne, C. Rameau, S. Bernard, Interaction of the alpha-helical H6 peptide from the pro-apoptotic protein tBid with cardiolipin, FEBS J. 276 (2009) 6338-6354.
190. I.M. Cristea, M. Degli Esposti, Membrane lipids and cell death: an overview, Chem. Phys. Lipids 129 (2004) 133-160. (Pubitemid 38476987)
191. U. Schlattner, M. Tokarska-Schlattner, S. Ramirez, A. Brückner, L. Kay, C. Polge, R.F. Epand, R.M. Lee, M.-L. Lacombe, R.M. Epand, Mitochondrial kinases and their molecular interaction with cardiolipin, Biochim. Biophys. Acta Biomembr. 1788 (2009) 2032-2047.
192. J. Liu, R.F. Epand, D. Durrant, D. Grossman, N.-w. Chi, R.M. Epand, R.M. Lee, Role of phospholipid scramblase 3 in the regulation of tumor necrosis factor-α-induced apoptosis, Biochemistry 47 (2008) 4518-4529. (Pubitemid 351522102)
193. M. Sorice, A. Circella, R Misasi, V. Pittoni, T. Garofalo, A. Cirelli, A. Pavan, G.M. Pontieri, G. Valesini, Cardiolipin on the surface of apoptotic cells as a possible trigger for antiphospholipid antibodies, Clin. Exp. Immunol. 122 (2000) 277-284.
194. R.F. Epand, J.-C. Martinou, S. Montessuit, R.M. Epand, Transbilayer lipid diffusion promoted by Bax: implications for apoptosis, Biochemistry 42 (2003) 14576-14582. (Pubitemid 37532004)
195. M. Sorice, V. Manganelli, P. Matarrese, A. Tinari, R. Misasi, W. Malorni, T. Garofalo, Cardiolipin-enriched raft-like microdomains are essential activating platforms for apoptotic signals on mitochondria, FEBS Lett. 583 (2009) 2447-2450.
196. Y.-G. Kim, A. Saghatelian, Functional analysis of protein targets by metabolomic approaches, in: S.A. Sieber (Ed.), Activity-based Protein Profiling, vol. 324, Springer, Berlin Heidelberg, 2012, pp. 137-162.
197. N. Vinayavekhin, E.A. Homan, A. Saghatelian, Exploring disease through metabolomics, ACS Chem. Biol. 5 (2009) 91-103.
198. P.J. Meikle, M.J. Christopher, Lipidomics is providing new insight into the metabolic syndrome and its sequelae, Curr. Opin. Lipidol. 22 (2011) 210-215.
199. V.E. Kagan, Y.Y. Tyurina, H. Bayir, C.T. Chu, A.A. Kapralov, I.I. Vlasova, N.A Belikova, V.A. Tyurin, A. Amoscato, M. Epperly, J. Greenberger, S. DeKosky, A.A. Shvedova, J. Jiang, The "pro-apoptotic genies" get out of mitochondria: oxidative lipidomics and redox activity of cytochrome c/cardiolipin complexes, Chem. Biol. Interact. 163 (2006) 15-28. (Pubitemid 44574491)
200. V.E. Kagan, G.G. Borisenko, Y.Y. Tyurina, VA Tyurin, J. Jiang, A.I. Potapovich, V Kini, A.A. Amoscato, Y. Fujii, Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine, Free Radic. Biol. Med. 37 (2004) 1963-1985. (Pubitemid 39491317)
201. V. Tyurin, Y. Tyurina, V. Ritov, A. Lysytsya, A. Amoscato, P. Kochanek, R Hamilton, S. DeKosky, J. Greenberger, H. Bayir, V. Kagan, Oxidative lipidomics of apoptosis: quantitative assessment of phospholipid hydroperoxides in cells and tissues, in: R.M. Uppu, S.N. Murthy, W.A. Pryor, N.L. Parinandi (Eds.), Free Radicals and Antioxidant Protocols, vol. 610, Humana Press, 2010, pp. 353-374.
202. VA Tyurin, Y.Y. Tyurina, P.M. Kochanek, R. Hamilton, S.T. DeKosky, J.S. Greenberger, H. Bayir, V.E. Kagan, Chapter nineteen oxidative lipidomics of programmed cell death, in: Z.Z.R.A.L. Roya Khosravi-Far, P. Mauro (Eds.), Methods in Enzymology, vol. 442, Academic Press, 2008, pp. 375-393.
203. J. Bielawski, Z.M. Szulc, YA Hannun, A. Bielawska, Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry, Methods 39 (2006) 82-91. (Pubitemid 44107706)
204. M. Valsecchi, L. Mauri, R. Casellato, S. Prioni, N. Loberto, A. Prinetti, V. Chigorno, S. Sonnino, Ceramide and sphingomyelin species of fibroblasts and neurons in culture, J. Lipid Res. 48 (2007) 417-424. (Pubitemid 46220608)
205. CA Haynes, J.C. Allegood, H. Park, M.C. Sullards, Sphingolipidomics: methods for the comprehensive analysis of sphingolipids, J. Chromatogr. B 877 (2009) 2696-2708.
206. K.R. Johnson, K.Y. Johnson, K.P. Becker, J. Bielawski, C. Mao, L.M. Obeid, Role of human sphingosine-1-phosphate phosphatase 1 in the regulation of intra- and extracellular sphingosine-1-phosphate levels and cell viability, J. Biol. Chem. 278 (2003) 34541-34547. (Pubitemid 37553303)
207. G. Fabrias, J. Muñoz-Olaya, F. Cingolani, P. Signorelli, J. Casas, V. Gagliostro, R Ghidoni, Dihydroceramide desaturase and dihydrosphingolipids: debutant players in the sphingolipid arena, Prog. Lipid Res. 51 (2012) 82-94.
208. J.M. McDonnell, D. Fushman, C.L. Milliman, S.J. Korsmeyer, D. Cowburn, Solution structure of the proapoptotic molecule BID: a structural basis for apoptotic agonists and antagonists, Cell 96 (1999) 625-634. (Pubitemid 29122805)
209. J.J. Chou, H. Li, G.S. Salvesen, J. Yuan, G. Wagner, Solution structure of BID, an intracellular amplifier of apoptotic signaling, Cell 96 (1999) 615-624. (Pubitemid 29122804)