The non-glycosylated isoform of MIC26 is a constituent of the mammalian MICOS complex and promotes formation of crista junctions

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 7, 2015, Pages 1551-1563

  Koob, Sebastian ^a   Barrera, Miguel ^a   Anand, Ruchika ^b   Reichert, Andreas S ^a,b  

^a GOETHE UNIVERSITY   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Apolipoproteins; Arteriosclerosis; Cardiolipin metabolism; Crista junctions; MICOS complex; Mitochondria

Indexed keywords

APOLIPOPROTEIN; ENZYME; GLYCOSYLATED PROTEIN; ISOPROTEIN; MIC10 PROTEIN; MIC26 PROTEIN; MIC27 PROTEIN; MIC60 PROTEIN; MITOCHONDRIAL PROTEIN; TAFAZZIN; UNCLASSIFIED DRUG; APOLIPOPROTEIN O, HUMAN; CD46 PROTEIN, HUMAN; MEMBRANE COFACTOR PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN BINDING; PROTEIN SUBUNIT; REACTIVE OXYGEN METABOLITE; TAZ PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CELL JUNCTION; CONTROLLED STUDY; CRISTA JUNCTION; DOWN REGULATION; FEMALE; HEART; HUMAN; HUMAN CELL; HUMAN TISSUE; INNER MEMBRANE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL RESPIRATION; EXTRACELLULAR SPACE; GENE SILENCING; GLYCOSYLATION; MAMMAL; METABOLISM; MITOCHONDRION; MOLECULAR WEIGHT; PROTEIN SUBUNIT; SECRETION (PROCESS); TUMOR CELL LINE; ULTRASTRUCTURE;

MAMMALIA;

ANIMALS; ANTIGENS, CD46; APOLIPOPROTEINS; CELL LINE, TUMOR; CELL RESPIRATION; EXTRACELLULAR SPACE; GENE KNOCKDOWN TECHNIQUES; GLYCOSYLATION; HUMANS; MAMMALS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MOLECULAR WEIGHT; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN SUBUNITS; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS;

EID: 84926386874     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.03.004     Document Type: Article

References (63)

1. Zick M., Rabl R., Reichert A.S. Cristae formation-linking ultrastructure and function of mitochondria. Biochim. Biophys. Acta 2009, 1793:5-19.
2. Shen X., Zheng S., Thongboonkerd V., Xu M., Pierce W.M., Klein J.B., Epstein P.N. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am. J. Physiol. Endocrinol. Metab. 2004, 287:E896-E905.
3. Duncan J.G. Mitochondrial dysfunction in diabetic cardiomyopathy. Biochim. Biophys. Acta 2011, 1813:1351-1359.
4. Frustaci A., Kajstura J., Chimenti C., Jakoniuk I., Leri A., Maseri A., Nadal-Ginard B., Anversa P. Myocardial cell death in human diabetes. Circ. Res. 2000, 87:1123-1132.
5. Sasaki S. Determination of altered mitochondria ultrastructure by electron microscopy. Methods Mol. Biol. 2010, 648:279-290.
6. Winklhofer K.F., Haass C. Mitochondrial dysfunction in Parkinson's disease. Biochim. Biophys. Acta 2010, 1802:29-44.
7. Chou S.M. "Megaconial" mitochondria observed in a case of chronic polymyositis. Acta Neuropathol. 1968, 12:68-89.
8. Zerbes R.M., van der Klei I.J., Veenhuis M., Pfanner N., van der Laan M., Bohnert M. Mitofilin complexes: conserved organizers of mitochondrial membrane architecture. Biol. Chem. 2012, 393:1247-1261.
9. Kleschevnikov A.M., Belichenko P.V., Salehi A., Wu C. Discoveries in Down syndrome: moving basic science to clinical care. Prog. Brain Res. 2012, 197:199-221.
10. Mannella C.A., Marko M., Buttle K. Reconsidering mitochondrial structure: new views of an old organelle. Trends Biochem. Sci. 1997, 22:37-38.
11. Frey T.G., Mannella C.A. The internal structure of mitochondria. Trends Biochem. Sci. 2000, 25:319-324.
12. Sukhorukov V.M., Bereiter-Hahn J. Anomalous diffusion induced by cristae geometry in the inner mitochondrial membrane. PLoS One 2009, 4:e4604.
13. Monian P., Jiang X. Clearing the final hurdles to mitochondrial apoptosis: regulation post cytochrome C release. Exp. Oncol. 2012, 34:185-191.
14. Dibrova D.V., Cherepanov D.A., Galperin M.Y., Skulachev V.P., Mulkidjanian A.Y. Evolution of cytochrome bc complexes: from membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates. Biochim. Biophys. Acta 2013, 1827:1407-1427.
15. Gilkerson R.W., Selker J.M., Capaldi R.A. The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett. 2003, 546:355-358.
16. Vogel F., Bornhovd C., Neupert W., Reichert A.S. Dynamic subcompartmentalization of the mitochondrial inner membrane. J. Cell Biol. 2006, 175:237-247.
17. Wurm C.A., Jakobs S. Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast. FEBS Lett. 2006, 580:5628-5634.
18. Hoppins S. The regulation of mitochondrial dynamics. Curr. Opin. Cell Biol. 2014, 29C:46-52.
19. Belenguer P., Pellegrini L. The dynamin GTPase OPA1: more than mitochondria?. Biochim. Biophys. Acta 1833, 2013:176-183.
20. Wagner K., Mick D.U., Rehling P. Protein transport machineries for precursor translocation across the inner mitochondrial membrane. Biochim. Biophys. Acta 2009, 1793:52-59.
21. Osman C., Voelker D.R., Langer T. Making heads or tails of phospholipids in mitochondria. J. Cell Biol. 2011, 192:7-16.
22. Schägger H. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 2002, 1555:154-159.
23. Schägger H., de Coo R., Bauer M.F., Hofmann S., Godinot C., Brandt U. Significance of respirasomes for the assembly/stability of human respiratory chain complex I. J. Biol. Chem. 2004, 279:36349-36353.
24. Walker J.E. The ATP synthase: the understood, the uncertain and the unknown. Biochem. Soc. Trans. 2013, 41:1-16.
25. Tatsuta T., Scharwey M., Langer T. Mitochondrial lipid trafficking. Trends Cell Biol. 2006, 24:44-52.
26. Gebert N., Joshi A.S., Kutik S., Becker T., McKenzie M., Guan X.L., Mooga V.P., Stroud D.A., Kulkarni G., Wenk M.R., Rehling P., Meisinger C., Ryan M.T., Wiedemann N., Greenberg M.L., Pfanner N. Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome. Curr. Biol. 2009, 19:2133-2139.
27. Bazan S., Mileykovskaya E., Mallampalli V.K., Heacock P., Sparagna G.C., Dowhan W. Cardiolipin-dependent reconstitution of respiratory supercomplexes from purified Saccharomyces cerevisiae complexes III and IV. J. Biol. Chem. 2013, 288:401-411.
28. Bottinger L., Horvath S.E., Kleinschroth T., Hunte C., Daum G., Pfanner N., Becker T. Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes. J. Mol. Biol. 2012, 423:677-686.
29. Acehan D., Malhotra A., Xu Y., Ren M., Stokes D.L., Schlame M. Cardiolipin affects the supramolecular organization of ATP synthase in mitochondria. Biophys. J. 2011, 100:2184-2192.
30. Schlame M. Cardiolipin remodeling and the function of tafazzin. Biochim. Biophys. Acta 2013, 1831:582-588.
31. Bione S., D'Adamo P., Maestrini E., Gedeon A.K., Bolhuis P.A., Toniolo D. A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat. Genet. 1996, 12:385-389.
32. Acehan D., Xu Y., Stokes D.L., Schlame M. Comparison of lymphoblast mitochondria from normal subjects and patients with Barth syndrome using electron microscopic tomography. Lab. Invest. 2007, 87:40-48.
33. Dudek J., Cheng I.F., Balleininger M., Vaz F.M., Streckfuss-Bomeke K., Hubscher D., Vukotic M., Wanders R.J., Rehling P., Guan K. Cardiolipin deficiency affects respiratory chain function and organization in an induced pluripotent stem cell model of Barth syndrome. Stem Cell Res. 2013, 11:806-819.
34. Weber T.A., Koob S., Heide H., Wittig I., Head B., van der Bliek A., Brandt U., Mittelbronn M., Reichert A.S. APOOL is a cardiolipin-binding constituent of the Mitofilin/MINOS protein complex determining cristae morphology in mammalian mitochondria. PLoS One 2013, 8:e63683.
35. Rabl R., Soubannier V., Scholz R., Vogel F., Mendl N., Vasiljev-Neumeyer A., Korner C., Jagasia R., Keil T., Baumeister W., Cyrklaff M., Neupert W., Reichert A.S. Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J. Cell Biol. 2009, 185:1047-1063.
36. von der Malsburg K., Muller J.M., Bohnert M., Oeljeklaus S., Kwiatkowska P., Becker T., Loniewska-Lwowska A., Wiese S., Rao S., Milenkovic D., Hutu D.P., Zerbes R.M., Schulze-Specking A., Meyer H.E., Martinou J.C., Rospert S., Rehling P., Meisinger C., Veenhuis M., Warscheid B., van der Klei I.J., Pfanner N., Chacinska A., van der Laan M. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev. Cell 2011, 21:694-707.
37. Harner M., Korner C., Walther D., Mokranjac D., Kaesmacher J., Welsch U., Griffith J., Mann M., Reggiori F., Neupert W. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J. 2011, 30:4356-4370.
38. Hoppins S., Collins S.R., Cassidy-Stone A., Hummel E., Devay R.M., Lackner L.L., Westermann B., Schuldiner M., Weissman J.S., Nunnari J. A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J. Cell Biol. 2011, 195:323-340.
39. Pfanner N., van der Laan M., Amati P., Capaldi R.A., Caudy A.A., Chacinska A., Darshi M., Deckers M., Hoppins S., Icho T., Jakobs S., Ji J., Kozjak-Pavlovic V., Meisinger C., Odgren P.R., Park S.K., Rehling P., Reichert A.S., Sheikh M.S., Taylor S.S., Tsuchida N., van der Bliek A.M., van der Klei I.J., Weissman J.S., Westermann B., Zha J., Neupert W., Nunnari J. Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J. Cell Biol. 2014, 204:1083-1086.
40. John G.B., Shang Y., Li L., Renken C., Mannella C.A., Selker J.M., Rangell L., Bennett M.J., Zha J. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol. Biol. Cell 2005, 16:1543-1554.
41. Darshi M., Mendiola V.L., Mackey M.R., Murphy A.N., Koller A., Perkins G.A., Ellisman M.H., Taylor S.S. ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochondrial function. J. Biol. Chem. 2011, 286:2918-2932.
42. Alkhaja A.K., Jans D.C., Nikolov M., Vukotic M., Lytovchenko O., Ludewig F., Schliebs W., Riedel D., Urlaub H., Jakobs S., Deckers M. MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol. Biol. Cell 2012, 23:247-257.
43. Koob S., Reichert A.S. Novel intracellular functions of apolipoproteins: the ApoO protein family as constituents of the Mitofilin/MINOS complex determines cristae morphology in mitochondria. Biol. Chem. 2014, 395:285-296.
44. Lamant M., Smih F., Harmancey R., Philip-Couderc P., Pathak A., Roncalli J., Galinier M., Collet X., Massabuau P., Senard J.M., Rouet P. ApoO, a novel apolipoprotein, is an original glycoprotein up-regulated by diabetes in human heart. J. Biol. Chem. 2006, 281:36289-36302.
45. Yu B.L., Wu C.L., Zhao S.P. Plasma apolipoprotein O level increased in the patients with acute coronary syndrome. J. Lipid Res. 2012, 53:1952-1957.
46. Nijstad N., de Boer J.F., Lagor W.R., Toelle M., Usher D., Annema W., der Giet M., Rader D.J., Tietge U.J. Overexpression of apolipoprotein O does not impact on plasma HDL levels or functionality in human apolipoprotein A-I transgenic mice. Biochim. Biophys. Acta 2011, 1811:294-299.
47. Philip-Couderc P., Smih F., Pelat M., Vidal C., Verwaerde P., Pathak A., Buys S., Galinier M., Senard J.M., Rouet P. Cardiac transcriptome analysis in obesity-related hypertension. Hypertension 2003, 41:414-421.
48. Wu C.L., Zhao S.P., Yu B.L. Microarray analysis provides new insights into the function of apolipoprotein O in HepG2 cell line. Lipids Health Dis. 2013, 12:186.
49. Turkieh A., Caubere C., Barutaut M., Desmoulin F., Harmancey R., Galinier M., Berry M., Dambrin C., Polidori C., Casteilla L., Koukoui F., Rouet P., Smih F. Apolipoprotein O is mitochondrial and promotes lipotoxicity in heart. J. Clin. Invest. 2014, 124:2277-2286.
50. Koob S., Barrera M., Anand R., Reichert A.S. Data supporting the role of the non-glycosylated isoform of MIC26 in determining cristae morphology 2015, (Data in brief, in press).
51. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
52. Schagger H. Tricine-SDS-PAGE. Nat. Protoc. 2006, 1:16-22.
53. Schagger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100kDa. Anal. Biochem. 1987, 166:368-379.
54. Yu B.L., Wu C.L., Zhao S.P. Plasma apolipoprotein O level increased in the patients with acute coronary syndrome. J. Lipid Res. 2013, 53:1952-1957.
55. Morris R.L., Hollenbeck P.J. Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol. 1995, 131:1315-1326.
56. Scherz-Shouval R., Elazar Z. Monitoring starvation-induced reactive oxygen species formation. Methods Enzymol. 2009, 452:119-130.
57. Borggreve S.E., De Vries R., Dullaart R.P. Alterations in high-density lipoprotein metabolism and reverse cholesterol transport in insulin resistance and type 2 diabetes mellitus: role of lipolytic enzymes, lecithin:cholesterol acyltransferase and lipid transfer proteins. Eur. J. Clin. Invest. 2003, 33:1051-1069.
58. Raz I., Eldor R., Cernea S., Shafrir E. Diabetes: insulin resistance and derangements in lipid metabolism. Cure through intervention in fat transport and storage. Diabetes Metab. Res. Rev. 2005, 21:3-14.
59. Despres J.P., Moorjani S., Lupien P.J., Tremblay A., Nadeau A., Bouchard C. Regional distribution of body fat, plasma lipoproteins, and cardiovascular disease. Arteriosclerosis 1990, 10:497-511.
60. Mathieu P., Poirier P., Pibarot P., Lemieux I., Despres J.P. Visceral obesity: the link among inflammation, hypertension, and cardiovascular disease. Hypertension 2009, 53:577-584.
61. Harner M.E., Unger A.K., Izawa T., Walther D.M., Ozbalci C., Geimer S., Reggiori F., Brugger B., Mann M., Westermann B., Neupert W. Aim24 and MICOS modulate respiratory function, tafazzin-related cardiolipin modification and mitochondrial architecture. Elife 2014, 3:e01684.
62. Lowell B.B., Shulman G.I. Mitochondrial dysfunction and type 2 diabetes. Science 2005, 307:384-387.
63. Mantena S.K., King A.L., Andringa K.K., Eccleston H.B., Bailey S.M. Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol- and obesity-induced fatty liver diseases. Free Radic. Biol. Med. 2008, 44:1259-1272.