The MICOS complex of human mitochondria

Cell and Tissue Research

Volumn 367, Issue 1, 2017, Pages 83-93

  Kozjak Pavlovic, Vera ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Cristae; MIB; MICOS; Mitochondria; SAM

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOLIPOPROTEIN; APOPTOSIS INDUCING FACTOR; CARDIOLIPIN; HEAT SHOCK PROTEIN 70; METAXIN 1; METAXIN 2; METAXIN 3; MITOCHONDRIAL DNA; MITOCHONDRIAL GENOME MAINTENANCE EXONUCLEASE 1; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL PROTEIN DNAJC11; MITOCHONDRIAL PROTEIN MIC10; MITOCHONDRIAL PROTEIN MIC13; MITOCHONDRIAL PROTEIN MIC14; MITOCHONDRIAL PROTEIN MIC19; MITOCHONDRIAL PROTEIN MIC23; MITOCHONDRIAL PROTEIN MIC25; MITOCHONDRIAL PROTEIN MIC26; MITOCHONDRIAL PROTEIN MIC27; MITOCHONDRIAL PROTEIN MIC60; MITOCHONDRIAL PROTEIN SAM50; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN OPA1; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRANSLOCASE OF THE INNER MEMBRANE 22; TRANSLOCASE OF THE INNER MEMBRANE 23; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE MUL1; UNCLASSIFIED DRUG; UNINDEXED DRUG; MULTIPROTEIN COMPLEX;

CELL STRUCTURE; HUMAN; MITOCHONDRIAL CONTACT SITE AND CRISTAE ORGANIZING SYSTEM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; BIOLOGICAL MODEL; CELL RESPIRATION; METABOLISM;

CELL RESPIRATION; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES;

EID: 84973163298     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-016-2433-7     Document Type: Review

References (65)

1. Ajroud-Driss S, Fecto F, Ajroud K, Lalani I, Calvo SE, Mootha VK, Deng HX, Siddique N, Tahmoush AJ, Heiman-Patterson TD, Siddique T (2015) Mutation in the novel nuclear-encoded mitochondrial protein CHCHD10 in a family with autosomal dominant mitochondrial myopathy. Neurogenetics 16:1–9
2. Alkhaja AK, Jans DC, Nikolov M, Vukotic M, Lytovchenko O, Ludewig F, Schliebs W, Riedel D, Urlaub H, Jakobs S, Deckers M (2012) MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol Biol Cell 23:247–257
3. An J, Shi J, He Q, Lui K, Liu Y, Huang Y, Sheikh MS (2012) CHCM1/CHCHD6, novel mitochondrial protein linked to regulation of mitofilin and mitochondrial cristae morphology. J Biol Chem 287:7411–7426
4. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465
5. Armstrong LC, Komiya T, Bergman BE, Mihara K, Bornstein P (1997) Metaxin is a component of a preprotein import complex in the outer membrane of the mammalian mitochondrion. J Biol Chem 272:6510–6518
6. Armstrong LC, Saenz AJ, Bornstein P (1999) Metaxin 1 interacts with metaxin 2, a novel related protein associated with the mammalian mitochondrial outer membrane. J Cell Biochem 74:11–22
7. Bannwarth S, Ait-El-Mkadem S, Chaussenot A, Genin EC, Lacas-Gervais S, Fragaki K, Berg-Alonso L, Kageyama Y, Serre V, Moore DG, Verschueren A, Rouzier C, Le Ber I, Auge G, Cochaud C, Lespinasse F, N’Guyen K, de Septenville A, Brice A, Yu-Wai-Man P et al (2014) A mitochondrial origin for frontotemporal dementia and amyotrophic lateral sclerosis through CHCHD10 involvement. Brain 137:2329–2345
8. Barbot M, Jans DC, Schulz C, Denkert N, Kroppen B, Hoppert M, Jakobs S, Meinecke M (2015) Mic10 oligomerizes to bend mitochondrial inner membranes at cristae junctions. Cell Metab 21:756–763
9. Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180
10. Bohnert M, Wenz LS, Zerbes RM, Horvath SE, Stroud DA, von der Malsburg K, Muller JM, Oeljeklaus S, Perschil I, Warscheid B, Chacinska A, Veenhuis M, van der Klei IJ, Daum G, Wiedemann N, Becker T, Pfanner N, van der Laan M (2012) Role of mitochondrial inner membrane organizing system in protein biogenesis of the mitochondrial outer membrane. Mol Biol Cell 23:3948–3956
11. Bohnert M, Zerbes RM, Davies KM, Muhleip AW, Rampelt H, Horvath SE, Boenke T, Kram A, Perschil I, Veenhuis M, Kuhlbrandt W, van der Klei IJ, Pfanner N, van der Laan M (2015) Central role of Mic10 in the mitochondrial contact site and cristae organizing system. Cell Metab 21:747–755
12. Bornstein P, Mckinney CE, Lamarca ME, Winfield S, Shingu T, Devarayalu S, Vos HL, Ginns EI (1995) Metaxin, a gene contiguous to both thrombospondin 3 and glucocerebrosidase, is required for embryonic development in the mouse: implications for Gaucher disease. Proc Natl Acad Sci U S A 92:4547–4551
13. Darshi M, Mendiola VL, Mackey MR, Murphy AN, Koller A, Perkins GA, Ellisman MH, Taylor SS (2011) ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochondrial function. J Biol Chem 286:2918–2932
14. Darshi M, Trinh KN, Murphy AN, Taylor SS (2012) Targeting and import mechanism of coiled-coil helix coiled-coil helix domain-containing protein 3 (ChChd3) into the mitochondrial intermembrane space. J Biol Chem 287:39480–39491
15. Ding C, Wu Z, Huang L, Wang Y, Xue J, Chen S, Deng Z, Wang L, Song Z, Chen S (2015) Mitofilin and CHCHD6 physically interact with Sam50 to sustain cristae structure. Sci Rep 5:16064
16. Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25:319–324
17. Frezza C, Cipolat S, Martins De Brito O, Micaroni M, Beznoussenko GV, Rudka T, Bartoli D, Polishuck RS, Danial NN, De Strooper B, Scorrano L (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126:177–189
18. Genin EC, Plutino M, Bannwarth S, Villa E, Cisneros‐Barroso E, Roy M, Ortega‐Vila B, Fragaki K, Lespinasse F, Pinero‐Martos E, Augé G, Moore D, Burté F, Lacas‐Gervais S, Kageyama Y, Itoh K, Yu‐Wai‐Man P, Sesaki H, Ricci JE, Vives‐Bauza C et al (2016) CHCHD10 mutations promote loss of mitochondrial cristae junctions with impaired mitochondrial genome maintenance and inhibition of apoptosis. EMBO Mol Med 8:58–72
19. Gentle I, Gabriel K, Beech P, Waller R, Lithgow T (2004) The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164:19–24
20. Ghezzi D, Arzuffi P, Zordan M, Da Re C, Lamperti C, Benna C, D’Adamo P, Diodato D, Costa R, Mariotti C, Uziel G, Smiderle C, Zeviani M (2011) Mutations in TTC19 cause mitochondrial complex III deficiency and neurological impairment in humans and flies. Nat Genet 43:259–263
21. Ghochani M, Nulton JD, Salamon P, Frey TG, Rabinovitch A, Baljon ARC (2010) Tensile forces and shape entropy explain observed crista structure in mitochondria. Biophys J 99:3244–3254
22. Gieffers C, Korioth F, Heimann P, Ungermann C, Frey J (1997) Mitofilin Is a transmembrane protein of the inner mitochondrial membrane expressed as two isoforms. Exp Cell Res 232:395–399
23. Gilkerson RW, Selker JM, Capaldi RA (2003) The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett 546:355–358
24. Guarani V, Mcneill EM, Paulo JA, Huttlin EL, Frohlich F, Gygi SP, Van Vactor D, Harper JW (2015) QIL1 is a novel mitochondrial protein required for MICOS complex stability and cristae morphology. eLife 4:eLife.06265
25. Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U, Griffith J, Mann M, Reggiori F, Neupert W (2011) The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 30:4356–4370
26. Head BP, Zulaika M, Ryazantsev S, van der Bliek AM (2011) A novel mitochondrial outer membrane protein, MOMA-1, that affects cristae morphology in Caenorhabditis elegans. Mol Biol Cell 22:831–841
27. Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, Devay RM, Lackner LL, Westermann B, Schuldiner M, Weissman JS, Nunnari J (2011) A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J Cell Biol 195:323–340
28. Horvath SE, Rampelt H, Oeljeklaus S, Warscheid B, van der Laan M, Pfanner N (2015) Role of membrane contact sites in protein import into mitochondria. Prot Sci 24:277–297
29. Humphries AD, Streimann IC, Stojanovski D, Johnston AJ, Yano M, Hoogenraad NJ, Ryan MT (2005) Dissection of the mitochondrial import and assembly pathway for human Tom40. J Biol Chem 280:11535–11543
30. Huynen MA, Mühlmeister M, Gotthardt K, Guerrero-Castillo S, Brandt U (2015) Evolution and structural organization of the mitochondrial contact site (MICOS) complex and the mitochondrial intermembrane space bridging (MIB) complex. Biochim Biophys Acta 1863:91–101
31. Icho T, Ikeda T, Matsumoto Y, Hanaoka F, Kaji K, Tsuchida N (1994) A novel human gene that is preferentially transcribed in heart muscle. Gene 144:301–306
32. Ioakeimidis F, Ott C, Kozjak-Pavlovic V, Violitzi F, Rinotas V, Makrinou E, Eliopoulos E, Fasseas C, Kollias G, Douni E (2014) A splicing mutation in the novel mitochondrial protein DNAJC11 causes motor neuron pathology associated with cristae disorganization, and lymphoid abnormalities in mice. PLoS ONE 9, e104237
33. Jans DC, Wurm CA, Riedel D, Wenzel D, Stagge F, Deckers M, Rehling P, Jakobs S (2013) STED super-resolution microscopy reveals an array of MINOS clusters along human mitochondria. Proc Natl Acad Sci U S A 110:8936–8941
34. John GB, Shang Y, Li L, Renken C, Mannella CA, Selker JML, Rangell L, Bennett MJ, Zha J (2005) The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol Biol Cell 16:1543–1554
35. Khalifat N, Puff N, Bonneau S, Fournier JB, Angelova MI (2008) Membrane deformation under local pH gradient: mimicking mitochondrial cristae dynamics. Biophys J 95:4924–4933
36. Koob S, Barrera M, Anand R, Reichert AS (2015) The non-glycosylated isoform of MIC26 is a constituent of the mammalian MICOS complex and promotes formation of crista junctions. Biochim Biophys Acta 1853:1551–1563
37. Kornblum C, Nicholls TJ, Haack TB, Schöler S, Peeva V, Danhauser K, Hallmann K, Zsurka G, Rorbach J, Iuso A, Wieland T, Sciacco M, Ronchi D, Comi GP, Moggio M, Quinzii CM, Dimauro S, Calvo SE, Mootha VK, Klopstock T et al (2013) Loss-of-function mutations in MGME1 impair mtDNA replication and cause multi-systemic mitochondrial disease. Nat Genet 45:214–219
38. Korner C, Barrera M, Dukanovic J, Eydt K, Harner M, Rabl R, Vogel F, Rapaport D, Neupert W, Reichert AS (2012) The C-terminal domain of Fcj1 is required for formation of crista junctions and interacts with the TOB/SAM complex in mitochondria. Mol Biol Cell 23:2143–2155
39. Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N (2003) An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278:48520–48523
40. Kozjak-Pavlovic V, Ross K, Benlasfer N, Kimmig S, Karlas A, Rudel T (2007) Conserved roles of Sam50 and metaxins in VDAC biogenesis. EMBO Rep 8:576–582
41. Kozjak-Pavlovic V, Prell F, Thiede B, Götz M, Wosiek D, Ott C, Rudel T (2014) C1orf163/RESA1 is a novel mitochondrial intermembrane space protein connected to respiratory chain assembly. J Mol Biol 426:908–920
42. Li H, Ruan Y, Zhang K, Jian F, Hu C, Miao L, Gong L, Sun L, Zhang X, Chen S, Chen H, Liu D, Song Z (2015) Mic60/Mitofilin determines MICOS assembly essential for mitochondrial dynamics and mtDNA nucleoid organization. Cell Death Differ 23:380–392
43. McBride HM, Neuspiel M, Wasiak S (2006) Mitochondria: more than just a powerhouse. Curr Biol 16:R551–R560
44. Muñoz-Gómez SA, Slamovits CH, Dacks JB, Baier KA, Spencer KD, Wideman JG (2015) Ancient homology of the mitochondrial contact site and cristae organizing system points to an endosymbiotic origin of mitochondrial cristae. Curr Biol 25:1489–1495
45. Odgren P, Toukatly G, Bangs P, Gilmore R, Fey E (1996) Molecular characterization of mitofilin (HMP), a mitochondria-associated protein with predicted coiled coil and intermembrane space targeting domains. J Cell Sci 109:2253–2264
46. Ott C, Ross K, Straub S, Thiede B, Gotz M, Goosmann C, Krischke M, Mueller MJ, Krohne G, Rudel T, Kozjak-Pavlovic V (2012) Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes. Mol Cell Biol 32:1173–1188
47. Ott C, Dorsch E, Fraunholz M, Straub S, Kozjak-Pavlovic V (2015) Detailed analysis of the human mitochondrial contact site complex indicate a hierarchy of subunits. PLoS ONE 10, e0120213
48. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong S-E, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thorburn DR, Carr SA, Mootha VK (2008) A mitochondrial protein compendium elucidates complex i disease biology. Cell 134:112–123
49. Palmer CS, Osellame LD, Stojanovski D, Ryan MT (2011) The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery. Cell Signal 23:1534–1545
50. Park Y-U, Jeong J, Lee H, Mun JY, Kim J-H, Lee JS, Nguyen MD, Han SS, Suh P-G, Park SK (2010) Disrupted-in-schizophrenia 1 (DISC1) plays essential roles in mitochondria in collaboration with Mitofilin. Proc Natl Acad Sci U S A 107:17785–17790
51. Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M, Hell K, Rapaport D, Neupert W (2003) Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 426:862–866
52. Paumard P, Vaillier J, Coulary B, Schaeffer J, Soubannier V, Mueller DM, Brethes D, di Rago JP, Velours J (2002) The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J 21:221–230
53. Pfanner N, van der Laan M, Amati P, Capaldi RA, Caudy AA, Chacinska A, Darshi M, Deckers M, Hoppins S, Icho T, Jakobs S, Ji J, Kozjak-Pavlovic V, Meisinger C, Odgren PR, Park SK, Rehling P, Reichert AS, Sheikh MS, Taylor SS et al (2014) Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J Cell Biol 204:1083–1086
54. Renken C, Siragusa G, Perkins G, Washington L, Nulton J, Salamon P, Frey TG (2002) A thermodynamic model describing the nature of the crista junction: a structural motif in the mitochondrion. J Struct Biol 138:137–144
55. Rossi MN, Carbone M, Mostocotto C, Mancone C, Tripodi M, Maione R, Amati P (2009) Mitochondrial localization of PARP-1 requires interaction with mitofilin and is involved in the maintenance of mitochondrial DNA integrity. J Biol Chem 284:31616–31624
56. Schauble S, King CC, Darshi M, Koller A, Shah K, Taylor SS (2007) Identification of ChChd3 as a novel substrate of the cAMP-dependent protein kinase (PKA) using an analog-sensitive catalytic subunit. J Biol Chem 282:14952–14959
57. Turkieh A, Caubère C, Barutaut M, Desmoulin F, Harmancey R, Galinier M, Berry M, Dambrin C, Polidori C, Casteilla L, Koukoui F, Rouet P, Smih F (2014) Apolipoprotein O is mitochondrial and promotes lipotoxicity in heart. J Clin Invest 124:2277–2286
58. Vogel F, Bornhovd C, Neupert W, Reichert AS (2006) Dynamic subcompartmentalization of the mitochondrial inner membrane. J Cell Biol 175:237–247
59. von der Malsburg K, Müller Judith M, Bohnert M, Oeljeklaus S, Kwiatkowska P, Becker T, Loniewska-Lwowska A, Wiese S, Rao S, Milenkovic D, Hutu Dana P, Zerbes Ralf M, Schulze-Specking A, Meyer Helmut E, Martinou J-C, Rospert S, Rehling P, Meisinger C, Veenhuis M, Warscheid B et al (2011) Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev Cell 21:694–707
60. Weber TA, Koob S, Heide H, Wittig I, Head B, van der Bliek A, Brandt U, Mittelbronn M, Reichert AS (2013) APOOL is a cardiolipin-binding constituent of the Mitofilin/MINOS protein complex determining cristae morphology in mammalian mitochondria. PLoS ONE 8, e63683
61. Wiedemann N, Kozjak V, Chacinska A, Schonfisch B, Rospert S, Ryan MT, Pfanner N, Meisinger C (2003) Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424:565–571
62. Wurm CA, Jakobs S (2006) Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast. FEBS Lett 580:5628–5634
63. Xie J, Marusich MF, Souda P, Whitelegge J, Capaldi RA (2007) The mitochondrial inner membrane protein Mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiled-coil-helix domain-containing protein 3 and 6 and DnaJC11. FEBS Lett 581:3545–3549
64. Yang R-F, Sun L-H, Zhang R, Zhang Y, Luo Y-X, Zheng W, Zhang Z-Q, Chen H-Z, Liu D-P (2015) Suppression of Mic60 compromises mitochondrial transcription and oxidative phosphorylation. Sci Rep 5:7990
65. Zerbes RM, Höß P, Pfanner N, van der Laan M, Bohnert M (2016) Distinct roles of Mic12 and Mic27 in the mitochondrial contact site and cristae organizing system. J Mol Biol. doi:10.1016/j.jmb.2016.02.031