Mitochondrial NM23-H4/NDPK-D: A bifunctional nanoswitch for bioenergetics and lipid signaling

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 388, Issue 2, 2015, Pages 271-278

  Schlattner, Uwe ^a,b   Tokarska Schlattner, Malgorzata ^a,b   Epand, Richard M ^c   Boissan, Mathieu ^d,e,f   Lacombe, Marie Lise ^d,e   Klein Seetharaman, Judith ^g   Kagan, Valerian E ^h  

^a UNIV GRENOBLE ALPES   (France)

^b INSERM   (France)

^c MCMASTER UNIVERSITY   (Canada)

^d SORBONNE UNIVERSITÉ   (France)

^e CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^f HÔPITAL TENON   (France)

^g UNIVERSITY OF WARWICK   (United Kingdom)

^h UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Apoptosis; Cardiolipin; Lipid trafficking; Lipid transfer proteins; Membranes; Mitochondria; Mitophagy; Moonlighting proteins; NM23; Nucleoside diphosphate kinase

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARDIOLIPIN; GUANOSINE TRIPHOSPHATE; NUCLEOSIDE DIPHOSPHATE KINASE D; NUCLEOSIDE DIPHOSPHATE KINASE NM23;

APOPTOSIS; BIOENERGY; IN VITRO STUDY; MITOPHAGY; NANODEVICE; NANOSWITCH; PROTEIN CROSS LINKING; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; CHEMISTRY; ENERGY METABOLISM; HUMAN; LIPID METABOLISM; METABOLISM; MITOCHONDRION;

APOPTOSIS; CARDIOLIPINS; ENERGY METABOLISM; HUMANS; LIPID METABOLISM; MITOCHONDRIA; NUCLEOSIDE DIPHOSPHATE KINASE D;

EID: 84921939575     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-014-1047-4     Document Type: Review

References (66)

1. Arias-Cartin R, Grimaldi S, Pommier J, Lanciano P, Schaefer C, Arnoux P, Giordano G, Guigliarelli B, Magalon A (2011) Cardiolipin-based respiratory complex activation in bacteria. Proc Natl Acad Sci U S A 108:7781-7786
2. Basova LV, Kurnikov IV, Wang L, Ritov VB, Belikova NA, Vlasova II, Pacheco AA, Winnica DE, Peterson J, Bayir H, Waldeck DH, Kagan VE (2007) Cardiolipin switch in mitochondria: shutting off the reduction of cytochrome c and turning on the peroxidase activity. Biochemistry 46:3423-3434
3. Belenguer P, Pellegrini L (2013) The dynamin GTPase OPA1: more than mitochondria? Biochim Biophys Acta 1833:176-183
4. Bione S, D'Adamo P, Maestrini E, Gedeon AK, Bolhuis PA, Toniolo D (1996) A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat Genet 12:385-389
5. Boissan M, Lacombe ML (2011) Learning about the functions of NME/NM23: lessons from knockout mice to silencing strategies. Naunyn Schmiedeberg's Arch Pharmacol 384:421-431
6. Boissan M, Dabernat S, Peuchant E, Schlattner U, Lascu I, Lacombe ML (2009) The mammalian Nm23/NDPK family: from metastasis control to cilia movement. Mol Cell Biochem 329:51-62
7. Boissan M, Montagnac G, Shen Q, Griparic L, Guitton J, Romao M, Sauvonnet N, Lagache T, Lascu I, Raposo G, Desbourdes C, Schlattner U, Lacombe ML, Polo S, van der Bliek AM, Roux A, Chavrier P (2014) Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling. Science 344:1510-1515
8. Brdiczka D, Wallimann T (1994) The importance of the outer mitochondrial compartment in regulation of energy metabolism. Mol Cell Biochem 133-134:69-83
9. Chu CT, Ji J, Dagda RK, Jiang JF, Tyurina YY, Kapralov AA, Tyurin VA, Yanamala N, Shrivastava IH, Mohammadyani D, Qiang Wang KZ, Zhu J, Klein-Seetharaman J, Balasubramanian K, Amoscato AA, Borisenko G, Huang Z, Gusdon AM, Cheikhi A, Steer EK,Wang R, Baty C,Watkins S, Bahar I, Bayir H, Kagan VE (2013) Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat Cell Biol 15:1197-1205
10. Claypool SM, Koehler CM (2011) The complexity of cardiolipin in health and disease. Trends Biochem Sci 37:32-41
11. Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, Corrado M, Cipolat S, Costa V, Casarin A, Gomes LC, Perales-Clemente E, Salviati L, Fernandez-Silva P, Enriquez JA, Scorrano L (2013) Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 155: 160-171
12. Copley SD (2012) Moonlighting is mainstream: paradigm adjustment required. Bioessays 34:578-588
13. Desvignes T, Pontarotti P, Fauvel C, Bobe J (2009) Nme protein family evolutionary history, a vertebrate perspective. BMC Evol Biol 9:256
14. Epand RF, Schlattner U, Wallimann T, Lacombe ML, Epand RM (2007a) Novel lipid transfer property of two mitochondrial proteins that bridge the inner and outer membranes. Biophys J 92:126-137
15. Epand RF, Tokarska-Schlattner M, Schlattner U, Wallimann T, Epand RM (2007b) Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. J Mol Biol 365:968-980
16. Gebert N, Joshi AS, Kutik S, Becker T, McKenzie M, Guan XL, Mooga VP, Stroud DA, Kulkarni G, Wenk MR, Rehling P, Meisinger C, Ryan MT, Wiedemann N, Greenberg ML, Pfanner N (2009) Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome. Curr Biol 19:2133-2139
17. Gonzalvez F, Pariselli F, Dupaigne P, Budihardjo I, Lutter M, Antonsson B, Diolez P, Manon S, Martinou JC, Goubern M,Wang X, Bernard S, Petit PX (2005) tBid interaction with cardiolipin primarily orchestrates mitochondrial dysfunctions and subsequently activates Bax and Bak. Cell Death Differ 12:614-626
18. Gonzalvez F, Schug ZT, Houtkooper RH, MacKenzie ED, Brooks DG, Wanders RJ, Petit PX, Vaz FM, Gottlieb E (2008) Cardiolipin provides an essential activating platform for caspase-8 onmitochondria. J Cell Biol 183:681-696
19. Green DR, Galluzzi L, Kroemer G (2011) Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 333:1109-1112
20. Horvath SE, Daum G (2013) Lipids of mitochondria. Prog Lipid Res 52:590-614
21. Huttemann M, Pecina P, Rainbolt M, Sanderson TH, Kagan VE, Samavati L, Doan JW, Lee I (2011) The multiple functions of cytochrome c and their regulation in life and death decisions of the mammalian cell: from respiration to apoptosis. Mitochondrion 11:369-381
22. Janin J, Dumas C, Morera S, Xu Y, Meyer P, Chiadmi M, Cherfils J (2000) Three-dimensional structure of nucleoside diphosphate kinase. J Bioenerg Biomembr 32:215-225
23. Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, Amoscato AA, Osipov AN, Belikova NA, Kapralov AA, Kini V, Vlasova II, Zhao Q, Zou M, Di P, Svistunenko DA, Kurnikov IV, Borisenko GG (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 1:223-232
24. Kagan VE, Tyurina YY, Bayir H, Chu CT, Kapralov AA, Vlasova II, Belikova NA, Tyurin VA, Amoscato A, Epperly M, Greenberger J, Dekosky S, Shvedova AA, Jiang J (2006) The "pro-apoptotic genies" get out of mitochondria: oxidative lipidomics and redox activity of cytochrome c/cardiolipin complexes. Chem Biol Interact 163:15-28
25. Kagan VE, Bayir HA, Belikova NA, Kapralov O, Tyurina YY, Tyurin VA, Jiang J, Stoyanovsky DA, Wipf P, Kochanek PM, Greenberger JS, Pitt B, Shvedova AA, Borisenko G (2009) Cytochrome c/cardiolipin relations in mitochondria: a kiss of death. Free Radic Biol Med 46:1439-1453
26. Kagan VE, Chu CT, Tyurina YY, Cheikhi A, Bayir H (2014) Cardiolipin asymmetry, oxidation and signaling. Chem Phys Lipids 179:64-69
27. Kapralov AA, Yanamala N, Tyurina YY, Castro L, Samhan-Arias A, Vladimirov YA, Maeda A, Weitz AA, Peterson J, Mylnikov D, Demicheli V, Tortora V, Klein-Seetharaman J, Radi R, Kagan VE (2011) Topography of tyrosine residues and their involvement in peroxidation of polyunsaturated cardiolipin in cytochrome c/cardiolipin peroxidase complexes. Biochim Biophys Acta 1808:2147-2155
28. Kaufman RJ, Malhotra JD (2014) Calcium trafficking integrates endoplasmic reticulum function with mitochondrial bioenergetics. Biochim Biophys Acta
29. Korytowski W, Basova LV, Pilat A, Kernstock RM, Girotti AW (2011) 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 286:26334-26343
30. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, Newmeyer DD (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111:331-342
31. Lacombe ML, Milon L, Munier A, Mehus JG, Lambeth DO (2000) The human Nm23/nucleoside diphosphate kinases. J Bioenerg Biomembr 32:247-258
32. Lacombe ML, Tokarska-Schlattner M, Epand RF, Boissan M, Epand RM, Schlattner U (2009) Interaction of NDPK-D with cardiolipin-containing membranes: structural basis and implications for mitochondrial physiology. Biochimie 91:779-783
33. Landeta O, Landajuela A, Gil D, Taneva S, Di Primo C, Sot B, Valle M, Frolov VA, Basanez G (2011) Reconstitution of proapoptotic BAK function in liposomes reveals a dual role for mitochondrial lipids in the BAK-driven membrane permeabilization process. J Biol Chem 286:8213-8230
34. Lee J, Giordano S, Zhang J (2011) Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 441:523-540
35. Lenaers G, Hamel C, Delettre C, Amati-Bonneau P, Procaccio V, Bonneau D, Reynier P, Milea D (2012) Dominant optic atrophy. Orphanet J Rare Dis 7:46
36. Mejia EM, Nguyen H, Hatch GM (2014) Mammalian cardiolipin biosynthesis. Chem Phys Lipids 179:11-16
37. Mileykovskaya E, Dowhan W (2009) Cardiolipin membrane domains in prokaryotes and eukaryotes. Biochim Biophys Acta 1788:2084-2091
38. Mileykovskaya E, Dowhan W (2014) Cardiolipin-dependent formation of mitochondrial respiratory supercomplexes. Chem Phys Lipids 179:42-48
39. Milon L, Rousseau-Merck MF, Munier A, Erent M, Lascu I, Capeau J, Lacombe ML (1997) nm23-H4, a new member of the family of human nm23/nucleoside diphosphate kinase genes localised on chromosome 16p13. Hum Genet 99:550-557
40. Milon L, Meyer P, Chiadmi M, Munier A, Johansson M, Karlsson A, Lascu I, Capeau J, Janin J, Lacombe ML (2000) The human nm23-H4 gene product is amitochondrial nucleoside diphosphate kinase. J Biol Chem 275:14264-14272
41. Osman C, Voelker DR, Langer T (2011) Making heads or tails of phospholipids in mitochondria. J Cell Biol 192:7-16
42. Pagliarini DJ, Rutter J (2013) Hallmarks of a new era in mitochondrial biochemistry. Genes Dev 27:2615-2627
43. Petronilli V, Cola C, Massari S, Colonna R, Bernardi P (1993) Physiological effectors modify voltage sensing by the cyclosporin A-sensitive permeability transition pore of mitochondria. J Biol Chem 268:21939-21945
44. Potting C, Tatsuta T, Konig T, Haag M, Wai T, Aaltonen MJ, Langer T (2013) TRIAP1/PRELI complexes prevent apoptosis by mediating intramitochondrial transport of phosphatidic acid. Cell Metab 18:287-295
45. Raemy E, Martinou JC (2014) Involvement of cardiolipin in tBID-induced activation of BAX during apoptosis. Chem Phys Lipids 179:70-74
46. Saini-Chohan HK, Mitchell RW, Vaz FM, Zelinski T, Hatch GM (2012) Delineating the role of alterations in lipid metabolism to the pathogenesis of inherited skeletal and cardiac muscle disorders: thematic review series: genetics of human lipid diseases. J Lipid Res 53:4-27
47. Schlame M, Ren M (2009) The role of cardiolipin in the structural organization of mitochondrial membranes. Biochim Biophys Acta 1788:2080-2083
48. Schlame M, Acechan B, Berno O, Xu Y, Valvo S, Ren D, Stokes L, Epand RM (2012) The physical state of lipid substrates provides transacylation specificity for tafazzin. Nat Chem Biol 8:862-869
49. Schlattner U, Tokarska-Schlattner M, Ramirez S, Bruckner A, Kay L, Polge C, Epand RF, Lee RM, Lacombe ML, Epand RM (2009) Mitochondrial kinases and their molecular interaction with cardiolipin. Biochim Biophys Acta 1788:2032-2047
50. Schlattner U, Tokarska-Schlattner M, Ramirez S, Tyurina YY, Amoscato AA,Mohammadyani D, Huang Z, Jiang J, Yanamala N, Seffouh A, Boissan M, Epand RF, Epand RM, Klein-Seetharaman J, Lacombe ML, Kagan VE (2013) Dual function of mitochondrial Nm23-H4 protein in phosphotransfer and intermembrane lipid transfer: a cardiolipin-dependent switch. J Biol Chem 288:111-121
51. Schlattner U, Tokarska-Schlattner M, Rousseau D, Boissan M, Mannella C, Epand R, Lacombe ML (2014) Mitochondrial cardiolipin/phospholipid trafficking: the role of membrane contact site complexes and lipid transfer proteins. Chem Phys Lipids 179:32-41
52. Schug ZT, Gottlieb E (2009) Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis. Biochim Biophys Acta 1788:2022-2031
53. Sesaki H, Jensen RE (2001) UGO1 encodes an outer membrane protein required for mitochondrial fusion. J Cell Biol 152:1123-1134, Erratum in: J Cell Biol 153: 635
54. Sevrioukova IF (2011) Apoptosis-inducing factor: structure, function, and redox regulation. Antioxid Redox Signal 14:2545-2579
55. Sorice M, Manganelli V, Matarrese P, Tinari A, Misasi R, Malorni W, Garofalo T (2009) Cardiolipin-enriched raft-like microdomains are essential activating platforms for apoptotic signals on mitochondria. FEBS Lett 583:2447-2450
56. Tait SW, Green DR (2013) Mitochondrial regulation of cell death. Cold Spring Harb Perspect Biol 5
57. Tatsuta T, Scharwey M, Langer T (2013) Mitochondrial lipid trafficking. Trends Cell Biol
58. Tokarska-Schlattner M, Boissan M, Munier A, Borot C, Mailleau C, Speer O, Schlattner U, Lacombe ML (2008) The nucleoside diphosphate kinase D (NM23-H4) binds the inner mitochondrial membrane with high affinity to cardiolipin and couples nucleotide transfer with respiration. J Biol Chem 283:26198-26207
59. Twig G, Shirihai OS (2010) The interplay between mitochondrial dynamics and mitophagy. Antioxid Redox Signal 14:1939-1951
60. Tyurina YY, Poloyac SM, Tyurin VA, Kapralov AA, Jiang J, Anthonymuthu TS, Kapralova VI, Vikulina AS, Jung MY, Epperly MW, Mohammadyani D, Klein-Seetharaman J, Jackson TC, Kochanek PM, Pitt BR, Greenberger JS, Vladimirov YA, Bayir H, Kagan VE (2014) A mitochondrial pathway for biosynthesis of lipid mediators. Nat Chem 6:542-552
61. van der Laan M, Bohnert M, Wiedemann N, Pfanner N (2012) Role of MINOS in mitochondrial membrane architecture and biogenesis. Trends Cell Biol 22:185-192
62. vanMeer G, de Kroon AI (2011) Lipid map of the mammalian cell. J Cell Sci 124:5-8
63. Wallimann T, Tokarska-Schlattner M, Schlattner U (2011) The creatine kinase system and pleiotropic effects of creatine. Amino Acids 40:1271-1296
64. Westermann B (2010) Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 11:872-884
65. Xu Y, Schlame M (2014) The turnover of glycerol and acyl moieties of cardiolipin. Chem Phys Lipids 179:17-24
66. Zerbes RM, Bohnert M, Stroud DA, von der Malsburg K, Kram A, Oeljeklaus S, Warscheid B, Becker T, Wiedemann N, Veenhuis M, van der Klei IJ, Pfanner N, van der Laan M (2012) Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially depend on mitofilin domains. J Mol Biol 422:183-191