Mic60/Mitofilin determines MICOS assembly essential for mitochondrial dynamics and mtDNA nucleoid organization

Cell Death and Differentiation

Volumn 23, Issue 3, 2016, Pages 380-392

  Li, H ^a   Ruan, Y ^a   Zhang, K ^a   Jian, F ^a   Hu, C ^a   Miao, L ^b   Gong, L ^a   Sun, L ^c   Zhang, X ^a   Chen, S ^a   Chen, H ^a   Liu, D ^a   Song, Z ^a  

^a WUHAN UNIVERSITY   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

METALLOPROTEINASE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOFILIN PROTEIN, MOUSE; MUSCLE PROTEIN; PROTEIN BINDING; YME1L PROTEIN, MOUSE;

ANIMAL; CELL CULTURE; CHEMISTRY; FIBROBLAST; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN; METABOLISM; MITOCHONDRIAL DYNAMICS; MOUSE; PHYSIOLOGY; PROTEIN DOMAIN;

ANIMALS; CELLS, CULTURED; DNA, MITOCHONDRIAL; FIBROBLASTS; HEK293 CELLS; HELA CELLS; HUMANS; METALLOENDOPEPTIDASES; MICE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MUSCLE PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; TRANSCRIPTION, GENETIC;

EID: 84957428131     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2015.102     Document Type: Article

References (58)

1. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. Importing mitochondrial proteins: machineries and mechanisms. Cell 2009; 138: 628-644.
2. Neupert W, Herrmann JM. Translocation of proteins into mitochondria. Annu Rev Biochem 2007; 76: 723-749.
3. Frey TG, Mannella CA. The internal structure of mitochondria. Trends Biochem Sci 2000; 25: 319-324.
4. Zick M, Rabl R, Reichert AS. Cristae formation-linking ultrastructure and function of mitochondria. Biochim Biophys Acta 2009; 1793: 5-19.
5. Vogel F, Bornhövd C, Neupert W, Reichert AS. Dynamic subcompartmentalization of the mitochondrial inner membrane. J Cell Biol 2006; 175: 237-247.
6. Tamura Y, HaradaY, Shiota T, Yamano K, Watanabe K, Yokota M et al. Tim23-Tim50 pair coordinates functions of translocators and motor proteins in mitochondrial protein import. J Cell Biol 2009; 184: 129-141.
7. Chacinska A, Lind M, Frazier AE, Dudek J, Meisinger C, Geissler A et al. Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 2005; 120: 817-829.
8. Gilkerson RW, Selker JM, Capaldi RA. The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett 2003; 546: 355-358.
9. Renken C, Siragusa G, Perkins G, Washington L, Nulton J, Salamon P et al. A thermodynamic model describing the nature of the crista junction: a structural motif in the mitochondrion. J Struct Biol 2002; 138: 137-144.
10. Harner M, Körner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U et al. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 2011; 30: 4356-4370.
11. Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, Devay RM, Lackner LL et al. 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.
12. Von der Malsburg K, Müller JM, Bohnert M, Oeljeklaus S, Kwiatkowska P, Becker T et al. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev Cell 2011; 21: 694-70.
13. Alkhaja AK, Jans DC, Nikolov M, Jans DC, Nikolov M, Vukotic M et al. MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol Biol Cell 2012; 23: 247-257.
14. Pfanner N, van der Laan M, Amati P, Capaldi RA, Caudy AA, Chacinska A et al. Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J Cell Biol 2014; 204: 1083-1086.
15. Xie J, Marusich MF, Souda P, Whitelegge J, Capaldi RA. The mitochondrial inner membrane protein mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiledcoil-helix domain-containing protein 3 and 6 and DnaJC11. FEBS Lett 2007; 581: 3545-3549.
16. Darshi M, Mendiola VL, Mackey MR, Murphy AN, Koller A, Perkins GA et al. ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochondrial function. J Biol Chem 2011; 286: 2918-2932.
17. An J, Shi J, He Q, Lui K, Liu Y, Huang Y et al. CHCM1/CHCHD6, novel mitochondrial protein linked to regulation of mitofilin and mitochondrial cristae morphology. J Biol Chem 2012; 287: 7411-7426.
18. Weber TA, Koob S, Heide H, Wittig I, Head B, van der Bliek A et al. APOOL is a cardiolipinbinding constituent of the Mitofilin/MINOS protein complex determining cristae morphology in mammalian mitochondria. PLoS One 2013; 8: e63683.
19. Baker MJ, Tatsuta T, Langer T. Quality control of mitochondrialproteostasis. Cold Spring Harb Perspect Biol 2011; 3: a007559.
20. Song Z, Chen H, Fiket M, Alexander C, Chan DC. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol 2007; 178: 749-755.
21. Ruan Y, Li H, Zhang K, Jian F, Tang J, Song Z. Loss of Yme1L perturbates mitochondrial dynamics. Cell Death Dis 2013; 4: e896.
22. Stiburek L, Cesnekova J, Kostkova O, Fornuskova D, Vinsova K, Wenchich L et al. YME1L controls the accumulation of respiratory chain subunits and is required for apoptotic resistance, cristae morphogenesis, and cell proliferation. Mol Biol Cell 2012; 23: 1010-1023.
23. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science 2012; 337: 1062-1065.
24. Song Z, Ghochani M, McCaffery JM, Frey TG, Chan DC. Mitofusins and OPA1 mediate sequential steps in mitochondrial membrane fusion. Mol Biol Cell 2009; 20: 3525-3532.
25. Losón OC, Song Z, Chen H, Chan DC. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol Biol Cell 2013; 24: 659-667.
26. Chan DC. Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet 2012; 46: 265-287.
27. Zuchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J et al. Mutations in themitochondrial GTPasemitofusin 2 cause Charcot-Marie-Toothneuropathy type 2 A. Nat Genet 2004; 36: 449-451.
28. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S et al. OPA1, encoding a dynaminrelated GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 2000; 26: 211-215.
29. Yen WL, Klionsky DJ. How to livelong and prosper: autophagy, mitochondria, and aging. Physiology (Bethesda) 2008; 23: 248-262.
30. Kanzaki Y, Terasaki F, Okabe M, Otsuka K, Katashima T, Fujita S et al. Giant mitochondria in the myocardium of a patient with mitochondrial cardiomyopathy: transmission and 3-dimensional scanning electron microscopy. Circulation 2010; 121: 831-832.
31. Coleman R, Silbermann M, Gershon D. Reznick AZ.Giant mitochondria in the myocardium of aging and endurance-trained mice. Gerontology 1987; 33: 34-39.
32. Tandler B, Dunlap M, Hoppel CL, Hassan M. Giant mitochondria in a cardiomyopathic heart. Ultrastruct Pathol 2002; 26: 177-183.
33. Terman A, Dalen H, Eaton JW, Neuzil J, Brunk UT. Aging of cardiac myocytes in culture: oxidative stress, lipofuscin accumulation, and mitochondrial turnover. Ann N Y Acad Sci 2004; 1019: 70-77.
34. Burgess SM, Delannoy M, Jensen RE. MMM1encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J Cell Biol 1994; 126: 1375-1391.
35. Berger KH, Sogo LF, Yaffe MP. Mdm12p a component required for mitochondrial inheritance that is conserved between budding and fission yeast. J Cell Biol 1997; 136: 545-553.
36. Sogo LF, Yaffe MP. Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. J Cell Biol 1994; 126: 1361-1373.
37. Dimmer KS, Jakobs S, Vogel F, Altmann K, Westermann B. Mdm3 1 and Mdm32 are inner membrane proteins required for maintenance of mitochondrial shape and stability of mitochondrial DNA nucleoids in yeast. J Cell Biol 2005; 168: 103-115.
38. Hensen F, Cansiz S, Gerhold JM, Spelbrink JN. To be or not to be a nucleoid protein: a comparison of mass-spectrometry based approaches in the identification of potential mtDNA-nucleoid associated proteins. Biochimie 2014; 100: 219-226.
39. Gilkerson R, Bravo L, Garcia I, Gaytan N, Herrera A, Maldonado A et al. The mitochondrialnucleoid: integratingmitochondrialDNA into cellular homeostasis. Cold Spring Harb Perspect Biol 2013; 5: a011080.
40. Gilkerson RW. Mitochondrial DNA nucleoids determine mitochondrial genetics and dysfunction. Int J Biochem Cell Biol 2009; 41: 1899-1906.
41. Ban-Ishihara R, Ishihara T, Sasaki N, Mihara K, Ishihara N. Dynamics of nucleoid structure regulated by mitochondrial fission contributes to cristae reformation and release of cytochrome c. Proc Natl Acad Sci USA 2013;.110: 11863-11868.
42. Bernert G, FountoulakisM, Lubec G. Manifolddecreased protein levels of matrin 3, reduced motor proteinHMP and hlark in fetal Down's syndrome brain. Proteomics 2002; 2: 1752-1757.
43. Baseler WA, Dabkowski ER, Williamson CL, Croston TL, Thapa D, Powell MJ et al. Proteomicalterations of distinctmitochondrial subpopulations in the type 1 diabetic heart: contribution of protein import dysfunction. Am J Physiol Regul Integr Comp Physiol 2011; 300: R186-R200.
44. Kim N, Lee Y, Kim H, Joo H, Youm JB, ParkWS et al. Potential biomarkers for ischemic heart damage identified in mitochondrial proteins by comparative proteomics. Proteomics 2006; 6: 1237-1249.
45. O'Connell K, Ohlendieck K. Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle. Proteomics 2009; 9: 5509-5524.
46. Guo Y, Darshi M, Ma Y, Perkins GA, Shen Z, Haushalter KJ et al. Quantitative proteomic and functional analysis of liver mitochondria from high fat diet (HFD) diabetic mice. Mol Cell Proteomics 2013; 12: 3744-3758.
47. John GB, Shang Y, Li L, Renken C, Mannella CA, Selker JM et al. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol Biol Cell 2005; 16: 1543-1554.
48. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, Rudka T. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 2006; 126: 177-189.
49. Wang Y, Bogenhagen DF. Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. J Biol Chem 2006; 281: 25791-25802.
50. Odgren PR, Toukatly G, Bangs PL, Gilmore R, Fey EG. Molecular characterization of mitofilin (HMP), a mitochondria-associated protein with predicted coiled coil and intermembrane space targeting domains. J Cell Sci 1996; 109: 2253-2264.
51. Hoppins S. The regulation of mitochondrial dynamics. Curr Opin Cell Biol 2014; 29: 46-52.
52. Elachouri G, Vidoni S, Zanna C, Pattyn A, Boukhaddaoui H, Gaget K et al. OPA1 links human mitochondrial genome maintenance to mtDNA replication and distribution. Genome Res 2011; 21: 12-20.
53. Itoh K, Tamura Y, Iijima M, Sesaki H. Effects of Fcj1-Mos1 and mitochondrial division on aggregation of mitochondrial DNA nucleoids and organelle morphology. Mol Biol Cell 2013; 24: 1842-1851.
54. Liesa M, Palacín M, Zorzano A. Mitochondrial dynamics in mammalian health and disease. Physiol Rev 2009; 89: 799-845.
55. Zerbes RM, van der Klei IJ, Veenhuis M, Pfanner N, van der Laan M, Bohnert M. Mitofilin complexes: conserved organizers of mitochondrial membrane architecture. Biol Chem 2012; 393: 1247-1261.
56. Zhang Y, Xu J, Luo YX, An XZ, Zhang R, Liu G et al. Overexpression of mitofilin in the mouse heart promotes cardiac hypertrophy in response to hypertrophic stimuli. Antioxid Redox Signal 2014; 21: 1693-1707.
57. Zhang K, Li H, Song Z. Membrane depolarization activates the mitochondrial protease OMA1 by stimulating self-cleavage. EMBO Rep 2014; 15: 576-585.
58. Zhang X, Zuo X, Yang B, Li Z, Xue Y, Zhou Y et al. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 2014; 158: 607-619.