2dys Citations

Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase.

Abstract

All 13 lipids, including two cardiolipins, one phosphatidylcholine, three phosphatidylethanolamines, four phosphatidylglycerols and three triglycerides, were identified in a crystalline bovine heart cytochrome c oxidase (CcO) preparation. The chain lengths and unsaturated bond positions of the fatty acid moieties determined by mass spectrometry suggest that each lipid head group identifies its specific binding site within CcOs. The X-ray structure demonstrates that the flexibility of the fatty acid tails facilitates their effective space-filling functions and that the four phospholipids stabilize the CcO dimer. Binding of dicyclohexylcarbodiimide to the O(2) transfer pathway of CcO causes two palmitate tails of phosphatidylglycerols to block the pathway, suggesting that the palmitates control the O(2) transfer process.The phosphatidylglycerol with vaccenate (cis-Delta(11)-octadecenoate) was found in CcOs of bovine and Paracoccus denitrificans, the ancestor of mitochondrion, indicating that the vaccenate is conserved in bovine CcO in spite of the abundance of oleate (cis-Delta(9)-octadecenoate). The X-ray structure indicates that the protein moiety selects cis-vaccenate near the O(2) transfer pathway against trans-vaccenate. These results suggest that vaccenate plays a critical role in the O(2) transfer mechanism.

Reviews - 2dys mentioned but not cited (1)

  1. Copper active sites in biology. Solomon EI, Heppner DE, Johnston EM, Ginsbach JW, Cirera J, Qayyum M, Kieber-Emmons MT, Kjaergaard CH, Hadt RG, Tian L. Chem Rev 114 3659-3853 (2014)

Articles - 2dys mentioned but not cited (2)



Reviews citing this publication (69)

  1. Making heads or tails of phospholipids in mitochondria. Osman C, Voelker DR, Langer T. J Cell Biol 192 7-16 (2011)
  2. Molecular mechanisms of ischemia-reperfusion injury in brain: pivotal role of the mitochondrial membrane potential in reactive oxygen species generation. Sanderson TH, Reynolds CA, Kumar R, Przyklenk K, Hüttemann M. Mol Neurobiol 47 9-23 (2013)
  3. Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells. Vance JE, Tasseva G. Biochim Biophys Acta 1831 543-554 (2013)
  4. Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes. Schlame M. J Lipid Res 49 1607-1620 (2008)
  5. Cardiolipin membrane domains in prokaryotes and eukaryotes. Mileykovskaya E, Dowhan W. Biochim Biophys Acta 1788 2084-2091 (2009)
  6. Role of Cardiolipin in Mitochondrial Signaling Pathways. Dudek J. Front Cell Dev Biol 5 90 (2017)
  7. The sarcoplasmic Ca2+-ATPase: design of a perfect chemi-osmotic pump. Møller JV, Olesen C, Winther AM, Nissen P. Q Rev Biophys 43 501-566 (2010)
  8. Cytochrome c oxidase: exciting progress and remaining mysteries. Brzezinski P, Gennis RB. J Bioenerg Biomembr 40 521-531 (2008)
  9. Metabolism and function of mitochondrial cardiolipin. Ren M, Phoon CK, Schlame M. Prog Lipid Res 55 1-16 (2014)
  10. The styrene-maleic acid copolymer: a versatile tool in membrane research. Dörr JM, Scheidelaar S, Koorengevel MC, Dominguez JJ, Schäfer M, van Walree CA, Killian JA. Eur Biophys J 45 3-21 (2016)
  11. Structures of mitochondrial oxidative phosphorylation supercomplexes and mechanisms for their stabilisation. Chaban Y, Boekema EJ, Dudkina NV. Biochim Biophys Acta 1837 418-426 (2014)
  12. The role of cardiolipin in the structural organization of mitochondrial membranes. Schlame M, Ren M. Biochim Biophys Acta 1788 2080-2083 (2009)
  13. Cardiolipin-dependent formation of mitochondrial respiratory supercomplexes. Mileykovskaya E, Dowhan W. Chem Phys Lipids 179 42-48 (2014)
  14. Phosphatidylethanolamine Metabolism in Health and Disease. Calzada E, Onguka O, Claypool SM. Int Rev Cell Mol Biol 321 29-88 (2016)
  15. Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Claypool SM. Biochim Biophys Acta 1788 2059-2068 (2009)
  16. Ethanolamine and Phosphatidylethanolamine: Partners in Health and Disease. Patel D, Witt SN. Oxid Med Cell Longev 2017 4829180 (2017)
  17. Oxygen Activation and Energy Conservation by Cytochrome c Oxidase. Wikström M, Krab K, Sharma V. Chem Rev 118 2469-2490 (2018)
  18. Stress-responsive regulation of mitochondria through the ER unfolded protein response. Rainbolt TK, Saunders JM, Wiseman RL. Trends Endocrinol Metab 25 528-537 (2014)
  19. Disorders of phospholipid metabolism: an emerging class of mitochondrial disease due to defects in nuclear genes. Lu YW, Claypool SM. Front Genet 6 3 (2015)
  20. Mitochondrial phospholipids: role in mitochondrial function. Mejia EM, Hatch GM. J Bioenerg Biomembr 48 99-112 (2016)
  21. Lipid interaction sites on channels, transporters and receptors: Recent insights from molecular dynamics simulations. Hedger G, Sansom MSP. Biochim Biophys Acta 1858 2390-2400 (2016)
  22. The assembly, regulation and function of the mitochondrial respiratory chain. Vercellino I, Sazanov LA. Nat Rev Mol Cell Biol 23 141-161 (2022)
  23. Ceramide and the mitochondrial respiratory chain. Kogot-Levin A, Saada A. Biochimie 100 88-94 (2014)
  24. Lipids in the assembly of membrane proteins and organization of protein supercomplexes: implications for lipid-linked disorders. Bogdanov M, Mileykovskaya E, Dowhan W. Subcell Biochem 49 197-239 (2008)
  25. The role of nonbilayer phospholipids in mitochondrial structure and function. Basu Ball W, Neff JK, Gohil VM. FEBS Lett 592 1273-1290 (2018)
  26. Non-covalent binding of membrane lipids to membrane proteins. Yeagle PL. Biochim Biophys Acta 1838 1548-1559 (2014)
  27. Specificity of intramembrane protein-lipid interactions. Contreras FX, Ernst AM, Wieland F, Brügger B. Cold Spring Harb Perspect Biol 3 a004705 (2011)
  28. Recent progress on lipid lateral heterogeneity in plasma membranes: From rafts to submicrometric domains. Carquin M, D'Auria L, Pollet H, Bongarzone ER, Tyteca D. Prog Lipid Res 62 1-24 (2016)
  29. Structure-function of the cytochrome b6f complex. Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA. Photochem Photobiol 84 1349-1358 (2008)
  30. Biogenesis of cbb(3)-type cytochrome c oxidase in Rhodobacter capsulatus. Ekici S, Pawlik G, Lohmeyer E, Koch HG, Daldal F. Biochim Biophys Acta 1817 898-910 (2012)
  31. A retrospective: use of Escherichia coli as a vehicle to study phospholipid synthesis and function. Dowhan W. Biochim Biophys Acta 1831 471-494 (2013)
  32. Membrane rafting: from apical sorting to phase segregation. Coskun U, Simons K. FEBS Lett 584 1685-1693 (2010)
  33. Cardiolipin remodeling: a regulatory hub for modulating cardiolipin metabolism and function. Ye C, Shen Z, Greenberg ML. J Bioenerg Biomembr 48 113-123 (2016)
  34. Cardiolipin, Mitochondria, and Neurological Disease. Falabella M, Vernon HJ, Hanna MG, Claypool SM, Pitceathly RDS. Trends Endocrinol Metab 32 224-237 (2021)
  35. Mitochondrial membrane lipid remodeling in pathophysiology: a new target for diet and therapeutic interventions. Monteiro JP, Oliveira PJ, Jurado AS. Prog Lipid Res 52 513-528 (2013)
  36. Mitochondrial biology, targets, and drug delivery. Milane L, Trivedi M, Singh A, Talekar M, Amiji M. J Control Release 207 40-58 (2015)
  37. Gating and regulation of the cytochrome c oxidase proton pump. Ferguson-Miller S, Hiser C, Liu J. Biochim Biophys Acta 1817 489-494 (2012)
  38. Conserved lipid-binding sites in membrane proteins: a focus on cytochrome c oxidase. Qin L, Sharpe MA, Garavito RM, Ferguson-Miller S. Curr Opin Struct Biol 17 444-450 (2007)
  39. Common cases of improper lipid annotation using high-resolution tandem mass spectrometry data and corresponding limitations in biological interpretation. Koelmel JP, Ulmer CZ, Jones CM, Yost RA, Bowden JA. Biochim Biophys Acta Mol Cell Biol Lipids 1862 766-770 (2017)
  40. Phospholipid ebb and flow makes mitochondria go. Acoba MG, Senoo N, Claypool SM. J Cell Biol 219 e202003131 (2020)
  41. Determinants of specificity at the protein-lipid interface in membranes. Ernst AM, Contreras FX, Brügger B, Wieland F. FEBS Lett 584 1713-1720 (2010)
  42. Phosphoregulation on mitochondria: Integration of cell and organelle responses. Lucero M, Suarez AE, Chambers JW. CNS Neurosci Ther 25 837-858 (2019)
  43. The power of yeast to model diseases of the powerhouse of the cell. Baile MG, Claypool SM. Front Biosci (Landmark Ed) 18 241-278 (2013)
  44. Reign in the membrane: How common lipids govern mitochondrial function. Funai K, Summers SA, Rutter J. Curr Opin Cell Biol 63 162-173 (2020)
  45. Lipidomic profiling of model organisms and the world's major pathogens. Layre E, Layre E, Moody DB. Biochimie 95 109-115 (2013)
  46. Subunit III-depleted cytochrome c oxidase provides insight into the process of proton uptake by proteins. Varanasi L, Hosler JP. Biochim Biophys Acta 1817 545-551 (2012)
  47. Highlighting membrane protein structure and function: A celebration of the Protein Data Bank. Li F, Egea PF, Vecchio AJ, Asial I, Gupta M, Paulino J, Bajaj R, Dickinson MS, Ferguson-Miller S, Monk BC, Stroud RM. J Biol Chem 296 100557 (2021)
  48. Proteome-wide detection of phospholipid-protein interactions in mitochondria by photocrosslinking and click chemistry. Gubbens J, de Kroon AI. Mol Biosyst 6 1751-1759 (2010)
  49. HIGD-Driven Regulation of Cytochrome c Oxidase Biogenesis and Function. Timón-Gómez A, Bartley-Dier EL, Fontanesi F, Barrientos A. Cells 9 E2620 (2020)
  50. How lipids modulate mitochondrial protein import. Böttinger L, Ellenrieder L, Becker T. J Bioenerg Biomembr 48 125-135 (2016)
  51. Mitochondria and the thermal limits of ectotherms. Chung DJ, Schulte PM. J Exp Biol 223 jeb227801 (2020)
  52. The Protein Toxins Ricin and Shiga Toxin as Tools to Explore Cellular Mechanisms of Internalization and Intracellular Transport. Sandvig K, Kavaliauskiene S, Skotland T. Toxins (Basel) 13 377 (2021)
  53. Current advances in research of cytochrome c oxidase. Popović DM. Amino Acids 45 1073-1087 (2013)
  54. How bilayer properties influence membrane protein folding. Corin K, Bowie JU. Protein Sci 29 2348-2362 (2020)
  55. Life at the border: adaptation of proteins to anisotropic membrane environment. Pogozheva ID, Mosberg HI, Lomize AL. Protein Sci 23 1165-1196 (2014)
  56. The Role of Phosphatidylethanolamine Adducts in Modification of the Activity of Membrane Proteins under Oxidative Stress. Pohl EE, Jovanovic O. Molecules 24 E4545 (2019)
  57. The road to the structure of the mitochondrial respiratory chain supercomplex. Caruana NJ, Stroud DA. Biochem Soc Trans 48 621-629 (2020)
  58. Barth syndrome cardiomyopathy: targeting the mitochondria with elamipretide. Sabbah HN. Heart Fail Rev 26 237-253 (2021)
  59. Specific roles of phosphatidylglycerols in hosts and microbes. Dugail I, Kayser BD, Lhomme M. Biochimie 141 47-53 (2017)
  60. Mitochondrion as a Target of Astaxanthin Therapy in Heart Failure. Krestinina O, Baburina Y, Krestinin R. Int J Mol Sci 22 7964 (2021)
  61. How physical forces drive the process of helical membrane protein folding. Corin K, Bowie JU. EMBO Rep 23 e53025 (2022)
  62. Mitochondrial cholesterol: Metabolism and impact on redox biology and disease. Goicoechea L, Conde de la Rosa L, Torres S, García-Ruiz C, Fernández-Checa JC. Redox Biol 61 102643 (2023)
  63. The Interplay among Subunit Composition, Cardiolipin Content, and Aggregation State of Bovine Heart Cytochrome c Oxidase. Sedlák E, Kožár T, Musatov A. Cells 9 E2588 (2020)
  64. Chicken or Egg? Mitochondrial Phospholipids and Oxidative Stress in Disuse-Induced Skeletal Muscle Atrophy. Miranda ER, Shahtout JL, Funai K. Antioxid Redox Signal 38 338-351 (2023)
  65. Crosstalk between Mitochondrial Protein Import and Lipids. Hoffmann JJ, Becker T. Int J Mol Sci 23 5274 (2022)
  66. A Comprehensive Insight and Mechanistic Understanding of the Lipidomic Alterations Associated With DCM. Saha S, Singh P, Dutta A, Vaidya H, Negi PC, Sengupta S, Seth S, Basak T. JACC Asia 3 539-555 (2023)
  67. Interaction of Terminal Oxidases with Amphipathic Molecules. Azarkina NV, Borisov VB, Oleynikov IP, Sudakov RV, Vygodina TV. Int J Mol Sci 24 6428 (2023)
  68. Molecular Biophysics of Class A G Protein Coupled Receptors-Lipids Interactome at a Glance-Highlights from the A2A Adenosine Receptor. Tzortzini E, Kolocouris A. Biomolecules 13 957 (2023)
  69. Pathology-supported genetic testing as a method for disability prevention in multiple sclerosis (MS). Part I. Targeting a metabolic model rather than autoimmunity. van Rensburg SJ, van Toorn R, Erasmus RT, Hattingh C, Johannes C, Moremi KE, Kemp MC, Engel-Hills P, Kotze MJ. Metab Brain Dis 36 1151-1167 (2021)

Articles citing this publication (136)