Cardiolipin is a key determinant for mtDNA stability and segregation during mitochondrial stress

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1847, Issue 6-7, 2015, Pages 587-598

  Luévano Martínez, Luis Alberto ^a   Forni, Maria Fernanda ^a   Dos Santos, Valquiria Tiago ^a   Souza Pinto, Nadja C ^a   Kowaltowski, Alicia J ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Membrane plasticity; Mitochondrial DNA; Mitochondrion; Phospholipid

Indexed keywords

CARDIOLIPIN; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; PHOSPHOLIPID;

ARTICLE; CELL STRESS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DAUGHTER CELL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA REPLICATION; GENE SEGREGATION; GENETIC STABILITY; LIPID COMPOSITION; MEMBRANE STRUCTURE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL STRESS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TEMPERATURE STRESS; CELL RESPIRATION; CHEMISTRY; COPY NUMBER VARIATION; ELECTRON TRANSPORT; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; METABOLISM; MITOCHONDRION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PATHOLOGY; PHYSIOLOGY; TEMPERATURE;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

CARDIOLIPINS; CELL RESPIRATION; DNA COPY NUMBER VARIATIONS; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT; FLUORESCENCE RESONANCE ENERGY TRANSFER; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE; TEMPERATURE;

EID: 84927145475     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.03.007     Document Type: Article

References (66)

1. P. Fagone, and S. Jackowski Phosphatidylcholine and the CDP-choline cycle Biochim. Biophys. Acta 1831 2013 523 532
2. G. Li, S. Chen, M.N. Thompson, and M.L. Greenberg New insights into the regulation of cardiolipin biosynthesis in yeast: implications for Barth syndrome Biochim. Biophys. Acta 1771 2007 432 441
3. A.K. Menon, and V.L. Stevens Phosphatidylethanolamine is the donor of the ethanolamine residue linking a glycosylphosphatidylinositol anchor to protein J. Biol. Chem. 267 1992 15277 15280
4. P. Rockenfeller, M. Koska, F. Pietrocola, N. Minois, O. Knittelfelder, V. Sica, J. Franz, D. Carmona-Gutierrez, G. Kroemer, and F. Madeo Phosphatidylethanolamine positively regulates autophagy and longevity Cell Death Differ. 22 2015 499 508
5. M.G. Baile, Y.W. Lu, and S.M. Claypool The topology and regulation of cardiolipin biosynthesis and remodeling in yeast Chem. Phys. Lipids 3084 2013 136 139
6. M. Dezi, F. Francia, A. Mallardi, G. Colafemmina, G. Palazzo, and G. Venturoli Stabilization of charge separation and cardiolipin confinement in antenna-reaction center complexes purified from Rhodobacter sphaeroides Biochim. Biophys. Acta 1767 2007 1041 1056
7. V.M. Gohil, and M.L. Greenberg Mitochondrial membrane biogenesis: phospholipids and proteins go hand in hand J. Cell Biol. 184 2009 469 472
8. B. Hoffmann, A. Stöckl, M. Schlame, K. Beyer, and M. Klingenberg The reconstituted ADP/ATP carrier activity has an absolute requirement for cardiolipin as shown in cysteine mutants J. Biol. Chem. 269 1994 1940 1944
9. T. Hoang, M.D. Smith, and M. Jelokhani-Niaraki Expression, folding, and proton transport activity of human Uncoupling Protein-1 (UCP1) in lipid membranes: evidence for associated functional forms J. Biol. Chem. 288 2013 36244 36258
10. D. Acehan, A. Malhotra, Y. Xu, M. Ren, D.L. Stokes, and M. Schlame Cardiolipin affects the supramolecular organization of ATP synthase in mitochondria Biophys. J. 100 2011 2184 2192
11. M. Zhang, E. Mileykovskaya, and W. Dowhan Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria J. Biol. Chem. 280 2005 29403 29408
12. I. Arechaga Membrane invaginations in bacteria and mitochondria: common features and evolutionary scenarios J. Mol. Microbiol. Biotechnol. 23 2013 13 23
13. A. Ortiz, J.A. Killian, A.J. Verkleij, and J. Wilschut Membrane fusion and the lamellar-to-inverted-hexagonal phase transition in cardiolipin vesicle systems induced by divalent cations Biophys. J. 77 1999 2003 2014
14. N. Khalifat, N. Puff, S. Bonneau, J.B. Fournier, and M.I. Angelova Membrane deformation under local pH gradient: mimicking mitochondrial cristae dynamics Biophys. J. 95 2008 4924 4933
15. T. Romantsov, Z. Guan, and J.M. Wood Cardiolipin and the osmotic stress responses of bacteria Biochim. Biophys. Acta 1788 2009 2092 2100
16. R. Saxena, N. Fingland, D. Patil, A.K. Sharma, and E. Crooke Crosstalk between DnaA protein, the initiator of Escherichia coli chromosomal replication, and acidic phospholipids present in bacterial membranes Int. J. Mol. Sci. 14 2013 8517 8537
17. V. Koshkin, and M.L. Greenberg Oxidative phosphorylation in cardiolipin-lacking yeast mitochondria Biochem. J. 347 2000 687 691
18. F. Jiang, M.T. Ryan, M. Schlame, M. Zhao, Z. Gu, M. Klingenberg, N. Pfanner, and M.L. Greenberg Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function J. Biol. Chem. 275 2000 22387 22394
19. Q. Zhong, V.M. Gohil, L. Ma, and M.L. Greenberg Absence of cardiolipin results in temperature sensitivity, respiratory defects, and mitochondrial DNA instability independent of pet56 J. Biol. Chem. 279 2004 32294 32300
20. A.S. Joshi, M.N. Thompson, N. Fei, M. Hüttemann, and M.L. Greenberg Cardiolipin and mitochondrial phosphatidylethanolamine have overlapping functions in mitochondrial fusion in Saccharomyces cerevisiae J. Biol. Chem. 287 2012 17589 17597
21. V.M. Gohil, M.N. Thompson, and M.L. Greenberg Synthetic lethal interaction of the mitochondrial phosphatidylethanolamine and cardiolipin biosynthetic pathways in Saccharomyces cerevisiae J. Biol. Chem. 280 2005 35410 35416
22. M. Janitor, and J. Subík Molecular cloning of the PEL1 gene of Saccharomyces cerevisiae that is essential for the viability of petite mutants Curr. Genet. 24 1993 307 312
23. B. Pineau, M. Bourge, J. Marion, C. Mauve, F. Gilard, L. Maneta-Peyret, P. Moreau, B. Satiat-Jeunemaître, S.C. Brown, R. De Paepe, and A. Danon The importance of cardiolipin synthase for mitochondrial ultrastructure, respiratory function, plant development, and stress responses in Arabidopsis Plant Cell 25 2013 4195 4208
24. M. Tsai, R.L. Ohniwa, Y. Kato, S.L. Takeshita, T. Ohta, S. Saito, H. Hayashi, and K. Morikawa Staphylococcus aureus requires cardiolipin for survival under conditions of high salinity BMC Microbiol. 11 2011 13 25
25. L. Böttinger, S.E. Horvath, T. Kleinschroth, C. Hunte, G. Daum, N. Pfanner, and T. Becker Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes J. Mol. Biol. 423 2012 677 686
26. M. Ogur, R.St. John, and S. Nagai Tetrazolium overlay technique for population studies of respiration deficiency in yeast Science 125 1957 928 929
27. F. Sherman, and I.B. Ephrussi The relationship between respiratory deficiency and suppressiveness in yeast as determined with segregational mutants Genetics 47 1962 695 700
28. S.D. Taylor, H. Zhang, J.S. Eaton, M.S. Rodeheffer, M.A. Lebedeva, T.W. O'Rourke, W. Siede, and G.S. Shadel The conserved Mec1/Rad53 nuclear checkpoint pathway regulates mitochondrial DNA copy number in Saccharomyces cerevisiae Mol. Biol. Cell 16 2005 3010 3018
29. M. Kozłowski, and W. Zagórski Stable preparation of yeast mitochondria and mitoplasts synthesizing specific polypeptides Anal. Biochem. 172 1988 382 391
30. E. Zinser, and G. Daum Isolation and biochemical characterization of organelles from the yeast, Saccharomyces cerevisiae Yeast 11 1995 493 536
31. L.A. Luévano-Martínez, P. Appolinario, S. Miyamoto, S. Uribe-Carvajal, and A.J. Kowaltowski Deletion of the transcriptional regulator opi1p decreases cardiolipin content and disrupts mitochondrial metabolism in Saccharomyces cerevisiae Fungal Genet. Biol. 60 2013 150 158
32. E.B. Gutierrez-Cirlos, and B.L. Trumpower Inhibitory analogs of ubiquinol act anti-cooperatively on the yeast cytochrome bc1 complex. Evidence for an alternating, half-of-the-sites mechanism of ubiquinol oxidation J. Biol. Chem. 277 2002 1195 1202
33. B.L. Trumpower, and C.A. Edwards Purification of a reconstitutively active iron-sulfur protein (oxidation factor) from succinate-cytochrome c reductase complex of bovine heart mitochondria J. Biol. Chem. 254 1979 8697 8706
34. M. Spinazzi, A. Casarin, V. Pertegato, L. Salviati, and C. Angelini Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells Nat. Protoc. 7 2012 1235 1246
35. D. Lloyd, and B. Chance The cytochromes of mitochondria from Tetrahymena pyriformis strain ST Biochem. J. 128 1972 1171 1182
36. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
37. C.H. Fiske, and Y. Subbarow The colorimetric determination of phosphorous J. Biol. Chem. 66 1925 375 400
38. B.K. Tan, M. Bogdanov, J. Zhao, W. Dowhan, C.R. Raetz, and Z. Guan Discovery of a cardiolipin synthase utilizing phosphatidylethanolamine and phosphatidylglycerol as substrates Proc. Natl. Acad. Sci. U. S. A. 109 2012 16504 16509
39. D.E. Robertson, and H. Rottenberg Membrane potential and surface potential in mitochondria. Fluorescence and binding of 1-anilinonaphthalene-8-sulfonate J. Biol. Chem. 258 1983 11039 11048
40. T. Parasassi, G. De Stasio, G. Ravagnan, R.M. Rusch, and E. Gratton Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence Biophys. J. 60 1991 179 189
41. B.A. Kaufman, S.M. Newman, R.L. Hallberg, C.A. Slaughter, P.S. Perlman, and R.A. Butow In organello formaldehyde crosslinking of proteins to mtDNA: identification of bifunctional proteins Proc. Natl. Acad. Sci. U. S. A. 97 2000 7772 7777
42. B.A. Kaufman, J.E. Kolesar, P.S. Perlman, and R.A. Butow A function for the mitochondrial chaperonin Hsp60 in the structure and transmission of mitochondrial DNA nucleoids in Saccharomyces cerevisiae J. Cell Biol. 163 2003 457 461
43. S.V. Consonni, M. Gloerich, E. Spanjaard, and J.L. Bos cAMP regulates DEP domain-mediated binding of the guanine nucleotide exchange factor Epac1 to phosphatidic acid at the plasma membrane Proc. Natl. Acad. Sci. U. S. A. 109 2012 3814 3819
44. D.F. Bogenhagen, D. Rousseau, and S. Burke The layered structure of human mitochondrial DNA nucleoids J. Biol. Chem. 283 2008 3665 3675
45. F. Jiang, Z. Gu, J.M. Granger, and M.L. Greenberg Cardiolipin synthase expression is essential for growth at elevated temperature and is regulated by factors affecting mitochondrial development Mol. Microbiol. 31 1999 373 379
46. F. Jiang, H.S. Rizavi, and M.L. Greenberg Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non-fermentable carbon sources Mol. Microbiol. 26 1997 481 491
47. J. Slavík Anilinonaphthalene sulfonate as a probe of membrane composition and function Biochim. Biophys. Acta 694 1982 1 25
48. F.M. Harris, K.B. Best, and J.D. Bell Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order Biochim. Biophys. Acta 1565 2002 123 128
49. J.H. Crowe, L.M. Crowe, and F.A. Hoekstra Phase transitions and permeability changes in dry membranes during rehydration J. Bioenerg. Biomembr. 21 1989 77 91
50. J.J. Lawrence, and M. Daune Ethidium bromide as a probe of conformational heterogeneity of DNA in chromatin. The role of histone H1 Biochemistry 15 1976 3301 3307
51. X.J. Chen, X. Wang, B.A. Kaufman, and R.A. Butow Aconitase couples metabolic regulation to mitochondrial DNA maintenance Science 307 2005 714 717
52. A.E. Hobbs, M. Srinivasan, J.M. McCaffery, and R.E. Jensen Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability J. Cell Biol. 152 2001 401 410
53. S.A. Minskoff, and M.L. Greenberg Phosphatidylglycerophosphate synthase from yeast Biochim. Biophys. Acta 1348 1997 187 191
54. F. Sor, and H. Fukuhara Erythromycin and piramycin resistance mutations of yeast mitochondria: nature of the rib2 locus in the large ribosomal RNA gene Nucleic Acids Res. 12 1984 8313 8318
55. L. Solieri Mitochondrial inheritance in budding yeasts: towards an integrated understanding Trends Microbiol. 18 2010 521 530
56. M. Kucej, B. Kucejova, R. Subramanian, X.J. Chen, and R.A. Butow Mitochondrial nucleoids undergo remodeling in response to metabolic cues J. Cell Sci. 121 2008 1861 1868
57. A.M. Grant, P.K. Hanson, L. Malone, and J.W. Nichols NBD-labeled phosphatidylcholine and phosphatidylethanolamine are internalized by transbilayer transport across the yeast plasma membrane Traffic 2 2001 37 50
58. K. Muchová, J. Jamroškovič, and I. Barák Lipid domains in Bacillus subtilis anucleate cells Res. Microbiol. 161 2010 783 790
59. M. Albring, J. Griffith, and G. Attardi Association of a protein structure of probable membrane derivation with HeLa cell mitochondrial DNA near its origin of replication Proc. Natl. Acad. Sci. U. S. A. 74 1977 1348 1352
60. G. Tuller, T. Nemec, C. Hrastnik, and G. Daum Lipid composition of subcellular membranes of an FY1679-derived haploid yeast wild-type strain grown on different carbon sources Yeast 15 1999 1555 1564
61. J.Z. Meyer, and P.A. Whittaker Respiratory repression and the stability of the mitochondrial genome Mol. Gen. Genet. 151 1977 333 342
62. J.R. Hazel, E.E. Williams, R. Livermore, and N. Mozingo Thermal adaptation in biological membranes: functional significance of changes in phospholipid molecular species composition Lipids 26 1991 277 282
63. D. Steverding, C. Thiel, B. Kadenbach, N. Capitanio, and S. Papa Influence of surface charge on the incorporation and orientation of cytochrome c oxidase in liposomes FEBS Lett. 257 1989 131 133
64. S.C. Chang, P.N. Heacock, E. Mileykovskaya, D.R. Voelker, and W. Dowhan Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae J. Biol. Chem. 273 1998 14933 14941
65. I. Fishov, and V. Norris Membrane heterogeneity created by transertion is a global regulator in bacteria Curr. Opin. Microbiol. 15 2012 724 730
66. J. Nunnari, W.F. Marshall, A. Straight, A. Murray, J.W. Sedat, and P. Walter Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA Mol. Biol. Cell 8 1997 1233 1242