Ceramide and the mitochondrial respiratory chain

Biochimie

Volumn 100, Issue 1, 2014, Pages 88-94

  Kogot Levin, Aviram ^a   Saada, Ann ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

Apoptosis; Ceramide; Mitochondria; Mitophagy; OXPHOS; Respiratory chain

Indexed keywords

CERAMIDE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; CELL MEMBRANE PERMEABILITY; HUMAN; LIPID METABOLISM; MACROAUTOPHAGY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL OUTER MEMBRANE PERMEABILIZATION; MITOCHONDRIAL RESPIRATORY CHAIN; MITOCHONDRION; MITOPHAGY; NONHUMAN; OUTER MEMBRANE; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; RESPIRATORY CHAIN; SHORT SURVEY;

SPHINGOIDEA;

APOPTOSIS; CERAMIDE; MITOCHONDRIA; MITOPHAGY; OXPHOS; RESPIRATORY CHAIN;

ANIMALS; APOPTOSIS; CERAMIDES; ELECTRON TRANSPORT; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84897034027     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2013.07.027     Document Type: Short Survey

References (74)

1. Y.A. Hannun, Functions of ceramide in coordinating cellular responses to stress, Science 274 (1996) 1855-1859. (Pubitemid 26424756)
2. A.H. Futerman, Y.A. Hannun, The complex life of simple sphingolipids, EMBO Rep. 5 (2004) 777-782. (Pubitemid 39199166)
3. Y.A. Hannun, L.M. Obeid, Many ceramides, J. Biol. Chem. 286 (2011) 27855-27862.
4. S.A. Morad, M.C. Cabot, Ceramide-orchestrated signalling in cancer cells, Nat. Rev. Cancer 13 (2013) 51-65.
5. E.S. Elkhayat, G.A. Mohamed, S.R.M. Ibrahim, Activity and structure elucidation of ceramidese, Curr. Bioact. Compd. 8 (2012) 370-409.
6. J. Yu, S.A. Novgorodov, D. Chudakova, H. Zhu, A. Bielawska, J. Bielawski, L.M. Obeid, M.S. Kindy, T.I. Gudz, JNK3 signaling pathway activates ceramide synthase leading to mitochondrial dysfunction, J. Biol. Chem. 282 (2007) 25940-25949. (Pubitemid 47372813)
7. T.I. Gudz, K.Y. Tserng, C.L. Hoppel, Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide, J. Biol. Chem. 272 (1997) 24154-24158. (Pubitemid 27418612)
8. V. Ganesan, M.N. 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.
9. Y.A. Hannun, L.M. Obeid, Principles of bioactive lipid signalling: lessons from sphingolipids, Nat. Rev. Mol. Cell Biol. 9 (2008) 139-150. (Pubitemid 351158911)
10. R. Tidhar, A.H. Futerman, The complexity of sphingolipid biosynthesis in the endoplasmic reticulum, Biochim. Biophys. Acta (2013).
11. Y. Pewzner-Jung, S. Ben-Dor, A.H. Futerman, When do Lasses (longevity assurance genes) become CerS (ceramide synthases)?: insights into the regulation of ceramide synthesis, J. Biol. Chem. 281 (2006) 25001-25005. (Pubitemid 44401887)
12. E.L. Laviad, L. Albee, I. Pankova-Kholmyansky, S. Epstein, H. Park, A.H. Merrill, A.H. Futerman, Characterization of ceramide synthase 2: tissue distribution, substrate specificity, and inhibition by sphingosine 1-phosphate, J. Biol. Chem. 283 (2008) 5677-5684.
13. M. Levy, A.H. Futerman, Mammalian ceramide synthases, IUBMB Life 62 (2010) 347-356.
14. K. Kitatani, J. Idkowiak-Baldys, Y.A. Hannun, The sphingolipid salvage pathway in ceramide metabolism and signaling, Cell. Signal 20 (2008) 1010-1018.
15. H. Shimeno, S. Soeda, M. Sakamoto, T. Kouchi, T. Kowakame, T. Kihara, Partial purification and characterization of sphingosine N-acyltransferase (ceramide synthase) from bovine liver mitochondrion-rich fraction, Lipids 33 (1998) 601-605. (Pubitemid 28283711)
16. C. Bionda, J. Portoukalian, D. Schmitt, C. Rodriguez-Lafrasse, D. Ardail, Subcellular compartmentalization of ceramide metabolism: MAM (mitochondria-associated membrane) and/or mitochondria? Biochem. J. 382 (2004) 527-533. (Pubitemid 39243919)
17. K. Kitatani, S. Akiba, T. Sato, Ceramide-induced enhancement of secretory phospholipase A2 expression via generation of reactive oxygen species in tumor necrosis factor-alpha-stimulated mesangial cells, Cell Signal. 16 (2004) 967-974. (Pubitemid 38638786)
18. C. Osman, D.R. Voelker, T. Langer, Making heads or tails of phospholipids in mitochondria, J. Cell Biol. 192 (2011) 7-16.
19. D. Ardail, I. Popa, K. Alcantara, A. Pons, J.P. Zanetta, P. Louisot, L. Thomas, J. Portoukalian, Occurrence of ceramides and neutral glycolipids with unusual long-chain base composition in purified rat liver mitochondria, FEBS Lett. 488 (2001) 160-164. (Pubitemid 32103589)
20. E.B. Babiychuk, A.P. Atanassoff, K. Monastyrskaya, C. Brandenberger, D. Studer, C. Allemann, A. Draeger, The targeting of plasmalemmal ceramide to mitochondria during apoptosis, PloS One 6 (2011) e23706.
21. K. Kitatani, J. Idkowiak-Baldys, J. Bielawski, T.A. Taha, R.W. Jenkins, C.E. Senkal, B. Ogretmen, L.M. Obeid, Y.A. Hannun, Protein kinase C-induced activation of a ceramide/protein phosphatase 1 pathway leading to dephosphorylation of p38 MAPK, J. Biol. Chem. 281 (2006) 36793-36802. (Pubitemid 46042147)
22. H. Zigdon, A. Kogot-Levin, J.W. Park, R. Goldschmidt, S. Kelly, A.H. Merrill Jr., A. Scherz, Y. Pewzner-Jung, A. Saada, A.H. Futerman, Ablation of ceramide synthase 2 causes chronic oxidative stress due to disruption of the mitochondrial respiratory chain, J. Biol. Chem. 288 (2013) 4947-4956.
23. J. Stiban, L. Caputo, M. Colombini, Ceramide synthesis in the endoplasmic reticulum can permeabilize mitochondria to proapoptotic proteins, J. Lipid Res. 49 (2008) 625-634.
24. B.X. Wu, V. Rajagopalan, P.L. Roddy, C.J. Clarke, Y.A. Hannun, Identification and characterization of murine mitochondria-associated neutral sphingomyelinase (MA-nSMase), the mammalian sphingomyelin phosphodiesterase 5, J. Biol. Chem. 285 (2010) 17993-18002.
25. S. El Bawab, P. Roddy, T. Qian, A. Bielawska, J.J. Lemasters, Y.A. Hannun, Molecular cloning and characterization of a human mitochondrial ceramidase, J. Biol. Chem. 275 (2000) 21508-21513. (Pubitemid 30481855)
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. K.S. Eble, W.B. Coleman, R.R. Hantgan, C.C. Cunningham, Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy, J. Biol. Chem. 265 (1990) 19434-19440. (Pubitemid 120013882)
28. Y. Hatefi, The mitochondrial electron transport and oxidative phosphorylation system, Annu. Rev. Biochem. 54 (1985) 1015-1069. (Pubitemid 15073670)
29. K. Shinzawa-Itoh, H. Aoyama, K. Muramoto, H. Terada, T. Kurauchi, Y. Tadehara, A. Yamasaki, T. Sugimura, S. Kurono, K. Tsujimoto, T. Mizushima, E. Yamashita, T.T. sukihara, S. Yoshikawa, Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase, EMBO J. 26 (2007) 1713-1725. (Pubitemid 46480942)
30. H. Palsdottir, C. Hunte, Lipids in membrane protein structures, Biochim. Biophys. Acta 1666 (2004) 2-18. (Pubitemid 39425195)
31. M.S. Sharpley, R.J. Shannon, F. Draghi, J. Hirst, Interactions between phospholipids and NADH: ubiquinone oxidoreductase (complex I) from bovine mitochondria, Biochemistry 45 (2006) 241-248. (Pubitemid 43054102)
32. D.M. Laird, J.W. Parce, R.I. Montgomery, C.C. Cunningham, Effect of phospholipids on the catalytic subunits of the mitochondrial F0.F1-ATPase, J. Biol. Chem. 261 (1986) 14851-14856. (Pubitemid 17220287)
33. E. Sedlák, N.C. Robinson, Phospholipase A(2) digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure, Biochemistry 38 (1999) 14966-14972.
34. R.H. Houtkooper, M. Turkenburg, B.T. Poll-The, D. Karall, C. Pérez-Cerdá, A. Morrone, S. Malvagia, R.J. Wanders, W. Kulik, F.M. Vaz, The enigmatic role of tafazzin in cardiolipin metabolism, Biochim. Biophys. Acta 1788 (2009) 2003-2014.
35. S.B. Wortmann, F.M. Vaz, T. Gardeitchik, L.E. Vissers, G.H. Renkema, J.H. Schuurs-Hoeijmakers, W. Kulik, M. Lammens, C. Christin, L.A. Kluijtmans, R.J. Rodenburg, L.G. Nijtmans, A. Grünewald, C. Klein, J.M. Gerhold, T. Kozicz, P.M. van Hasselt, M. Harakalova, W. Kloosterman, I. Bariæ, E. Pronicka, S.K. Ucar, K. Naess, K.K. Singhal, Z. Krumina, C. Gilissen, H. van Bokhoven, J.A. Veltman, J.A. Smeitink, D.J. Lefeber, J.N. Spelbrink, R.A. Wevers, E. Morava, A.P. de Brouwer, Mutations in the phospholipid remodeling gene SERAC1 impair mitochondrial function and intracellular cholesterol traf ficking and cause dystonia and deafness, Nat. Genet. 44 (2012) 797-802.
36. M.C. Patterson, M.T. Vanier, K. Suzuki, J.A. Morris, E. Carstea, E.B. Neufeld, J.E. Blanchette-Mackie, P.G. Pentchev, Niemann-Pick disease type C. A lipid trafficking disorder, in: C.R. Scriver, W.S. Sly, D. Valle (Eds.), The Metabolic and Molecular Basis of Inherited Disease, vol. 2, 2001, pp. 3611-3633. New York.
37. W. Yu, J.S. Gong, M. Ko, W.S. Garver, K. Yanagisawa, M. Michikawa, Altered cholesterol metabolism in Niemann-Pick type C1 mouse brains affects mitochondrial function, J. Biol. Chem. 280 (2005) 11731-11739. (Pubitemid 40418487)
38. M. Charman, B.E. Kennedy, N. Osborne, B. Karten, MLN64 mediates egress of cholesterol from endosomes to mitochondria in the absence of functional Niemann-Pick Type C1 protein, J. Lipid Res. 51 (2010) 1023-1034.
39. A. Fernández, L. Llacuna, J.C. Fernández-Checa, A. Colell, Mitochondrial cholesterol loading exacerbates amyloid beta peptide-induced inflammation and neurotoxicity, J. Neurosci. 29 (2009) 6394-6405.
40. T. Lücke, W. Höppner, E. Schmidt, S. Illsinger, A.M. Das, Fabry disease: reduced activities of respiratory chain enzymes with decreased levels of energy-rich phosphates in fibroblasts, Mol. Genet. Metab. 82 (2004) 93-97. (Pubitemid 38523330)
41. A.M. Das, R.D. Jolly, A. Kohlschütter, Anomalies of mitochondrial ATP synthase regulation in four different types of neuronal ceroid lipofuscinosis, Mol. Genet. Metab. 66 (1999) 349-355. (Pubitemid 29390200)
42. A. Schulz, T. Mousallem, M. Venkataramani, D.A. Persaud-Sawin, A. Zucker, C. Luberto, A. Bielawska, J. Bielawski, J.C. Holthuis, S.M. Jazwinski, L. Kozhaya, G.S. Dbaibo, R.M. Boustany, The CLN9 protein, a regulator of dihydroceramide synthase, J. Biol. Chem. 281 (2006) 2784-2794. (Pubitemid 43845742)
43. O. Ben-David, A.H. Futerman, The role of the ceramide acyl chain length in neurodegeneration: involvement of ceramide synthases, Neuromol. Med. 12 (2010) 341-350.
44. M. Di Paola, T. Cocco, M. Lorusso, Ceramide interaction with the respiratory chain of heart mitochondria, Biochemistry 39 (2000) 6660-6668. (Pubitemid 30353998)
45. H. Igisu, N. Hamasaki, A. Ito, W. Ou, Inhibition of cytochrome c oxidase and hemolysis caused by lysosphingolipids, Lipids 23 (1988) 345-348.
46. X. Wang, R.P. Rao, T. Kosakowska-Cholody, M.A. Masood, E. Southon, H. Zhang, C. Berthet, K. Nagashim, T.K. Veenstra, L. Tessarollo, U. Acharya, J.K. Acharya, Mitochondrial degeneration and not apoptosis is the primary cause of embryonic lethality in ceramide transfer protein mutant mice, J. Cell Biol. 184 (2009) 143-158.
47. Y. Pewzner-Jung, O. Brenner, S. Braun, E.L. Laviad, S. Ben-Dor, E. Feldmesser, S. Horn-Saban, D. Amann-Zalcenstein, C. Raanan, T. Berkutzki, R. Erez-Roman, O. Ben-David, M. Levy, D. Holzman, H. Park, A. Nyska, A.H. Merrill Jr., A.H. Futerman, A critical role for ceramide synthase 2 in liver homeostasis: II. Insights into molecular changes leading to hepatopathy, J. Biol. Chem. 285 (2010) 10911-10923.
48. Y. Pewzner-Jung, H. Park, E.L. Laviad, L.C. Silva, S. Lahiri, J. Stiban, R. Erez-Roman, B. Brugger, T. Sachsenheimer, F. Wieland, M. Prieto, A.H. Merrill Jr., 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.
49. C. García-Ruiz, A. Colell, M. Marí, A. Morales, J.C. Fernández-Checa, Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione, J. Biol. Chem. 272 (1997) 11369-11377.
50. M. Zhang, E. Mileykovskaya, W. Dowhan, Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane, J. Biol. Chem. 277 (2002) 43553-43556. (Pubitemid 36157767)
51. M.M. Siddique, Y. Li, L. Wang, J. Ching, M. Mal, O. Ilkayeva, Y.J. Wu, B.H. Bay, S.A. Summers, Ablation of dihydroceramide desaturase 1, a therapeutic target for the treatment of metabolic diseases, simultaneously stimulates anabolic and catabolic signaling, Mol. Cell. Biol. 33 (2013) 2353-2369.
52. V. Kota, Z.M. Szulc, H. Hama, Identification of C(6) -ceramide- interacting proteins in D6P2T Schwannoma cells, Proteomics 12 (2012) 2179-2184.
53. N. Zamzami, P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S.A. Susin, P.X. Petit, B. Mignotte, G. Kroemer, Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death, J. Exp. Med. 182 (1995) 367-377.
54. A.S. Arora, B.J. Jones, T.C. Patel, S.F. Bronk, G.J. Gores, Ceramide induces hepatocyte cell death through disruption of mitochondrial function in the rat, Hepatology 25 (1997) 958-963. (Pubitemid 27157141)
55. T.H. Beckham, P. Lu, E.E. Jones, T. Marrison, C.S. Lewis, J.C. Cheng, V.K. Ramshesh, G. Beeson, C.C. Beeson, R.R. Drake, A. Bielawska, J. Bielawski, Z.M. Szulc, B. Ogretmen, J.S. Norris, X. Liu, LCL124, a cationic analog of ceramide, selectively induces pancreatic cancer cell death by accumulating in mitochondria, J. Pharmacol. Exp. Ther. 344 (2013) 167-178.
56. K. Hofmann, V.M. Dixit, Ceramide in apoptosis e does it really matter? Trends Biochem. Sci. 23 (1998) 374-377. (Pubitemid 28511373)
57. 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)
58. M. Colombini, Ceramide channels and their role in mitochondria-mediated apoptosis, Biochim. Biophys. Acta 1797 (2010) 1239-1244.
59. S.W. Tait, D.R. Green, Mitochondria and cell death: outer membrane permeabilization and beyond, Nat. Rev. Mol. Cell Biol. 11 (2010) 621-632.
60. 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)
61. 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)
62. J. Zhang, N. Alter, J.C. Reed, C. Borner, L.M. Obeid, Y.A. Hannun, Bcl-2 interrupts the ceramide-mediated pathway of cell death, Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 5325-5328. (Pubitemid 26159448)
63. S. Geley, B.L. Hartmann, R. Kofler, Ceramides induce a form of apoptosis in human acute lymphoblastic leukemia cells that is inhibited by Bcl-2, but not by CrmA, FEBS Lett. 400 (1997) 15-18. (Pubitemid 27046813)
64. 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.
65. Q. Dai, J. Liu, J. Chen, D. Durrant, T.M. McIntyre, R.M. Lee, Mitochondrial ceramide increases in UV-irradiated HeLa cells and is mainly derived from hydrolysis of sphingomyelin, Oncogene 23 (2004) 3650-3658. (Pubitemid 38658432)
66. C.M. Matsko, O.C. Hunter, H. Rabinowich, M.T. Lotze, A.A. Amoscato, Mitochondrial lipid alterations during Fas- and radiation-induced apoptosis, Biochem. Biophys. Res. Commun. 287 (2001) 1112-1120. (Pubitemid 32980567)
67. Y.A. Hannun, L.M. Obeid, The Ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind, J. Biol. Chem. 277 (2002) 25847-25850. (Pubitemid 34967060)
68. D.K. Perry, J. Carton, A.K. Shah, F. Meredith, D.J. Uhlinger, Y.A. Hannun, Serine palmitoyltransferase regulates de novo ceramide generation during etoposide-induced apoptosis, J. Biol. Chem. 275 (2000) 9078-9084. (Pubitemid 30180269)
69. B.J. Kroesen, B. Pettus, C. Luberto, M. Busman, H. Sietsma, L. de Leij, Y.A. Hannun, Induction of apoptosis through B-cell receptor cross-linking occurs via de novo generated C16-ceramide and involves mitochondria, J. Biol. Chem. 276 (2001) 13606-13614.
70. A. Adan-Gokbulut, M. Kartal-Yandim, G. Iskender, Y. Baran, Novel agents targeting bioactive sphingolipids for the treatment of cancer, Curr. Med. Chem. 20 (2013) 108-122.
71. D. Glick, S. Barth, K.F. Macleod, Autophagy: cellular and molecular mechanisms, J. Pathol. 221 (2010) 3-12.
72. K. Sims, C.A. Haynes, S. Kelly, J.C. Allegood, E. Wang, A. Momin, M. Leipelt, D. Reichart, C.K. Glass, M.C. Sullard, A.H. Merrill Jr., Kdo2-lipid A, a TLR4-specific agonist, induces de novo sphingolipid biosynthesis in RAW264.7 macrophages, which is essential for induction of autophagy, J. Biol. Chem. 285 (2010) 38568-38579.
73. F. Scarlatti, C. Bauvy, A. Ventruti, G. Sala, F. Cluzeaud, A. Vandewalle, R. Ghidoni, P. Codogno, Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of beclin 1, J. Biol. Chem. 279 (2004) 18384-18391. (Pubitemid 38623254)
74. R.D. Sentelle, C.E. Senkal, W. Jiang, S. Ponnusamy, S. Gencer, S.P. Selvam, V.K. Ramshesh, Y.K. Peterson, J.J. Lemasters, Z.M. Szulc, J. Bielawski, B. Ogretmen, Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy, Nat. Chem. Biol. 8 (2012) 831-838.