The evolution of ERMIONE in mitochondrial biogenesis and lipid homeostasis: An evolutionary view from comparative cell biology

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1861, Issue 8, 2016, Pages 900-912

  Wideman, Jeremy G ^a   Muñoz Gómez, Sergio A ^b  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

ERMES; ERMIONE; Evolutionary cell biology; MCS; Membrane contact sites; MICOS

Indexed keywords

ALPHAPROTEOBACTERIA; CELL PLASTICITY; CELL VACUOLE; CYTOLOGY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MITOCHONDRIA ORGANIZING NETWORK; LIPID HOMEOSTASIS; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL MEMBRANE; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW; SACCHAROMYCES CEREVISIAE; ANIMAL; EVOLUTION; HOMEOSTASIS; HUMAN; LIPID METABOLISM; METABOLISM; MITOCHONDRION; ORGANELLE BIOGENESIS; PHYLOGENY; PHYSIOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; ENDOPLASMIC RETICULUM; HOMEOSTASIS; HUMANS; LIPID METABOLISM; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; ORGANELLE BIOGENESIS; PHYLOGENY;

EID: 84974577792     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2016.01.015     Document Type: Review

References (150)

1. S. Lahiri, A. Toulmay, and W.A. Prinz Membrane contact sites, gateways for lipid homeostasis Curr. Opin. Cell Biol. 33 2015 82 87 10.1016/j.ceb.2014.12.004
2. M.A. Block, and J. Jouhet Lipid trafficking at endoplasmic reticulum-chloroplast membrane contact sites Curr. Opin. Cell Biol. 35 2015 21 29 10.1016/j.ceb.2015.03.004
3. W.M. Henne, J. Liou, and S.D. Emr Molecular mechanisms of inter-organelle ER-PM contact sites Curr. Opin. Cell Biol. 35 2015 123 130 10.1016/j.ceb.2015.05.001
4. X. Du, A.J. Brown, and H. Yang Novel mechanisms of intracellular cholesterol transport: oxysterol-binding proteins and membrane contact sites Curr. Opin. Cell Biol. 35 2015 37 42 10.1016/j.ceb.2015.04.002
5. M.A. De Matteis, and L.R. Rega Endoplasmic reticulum-Golgi complex membrane contact sites Curr. Opin. Cell Biol. 35 2015 43 50 10.1016/j.ceb.2015.04.001
6. S. Hoppins, S.R. Collins, A. Cassidy-Stone, E. Hummel, R.M. Devay, L.L. Lackner, and et al. A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria J. Cell Biol. 195 2011 323 340 10.1083/jcb.201107053
7. K. Jin, G. Musso, J. Vlasblom, M. Jessulat, V. Deineko, J. Negroni, and et al. Yeast mitochondrial protein-protein interactions reveal diverse complexes and disease-relevant functional relationships J. Proteome Res. 14 2015 1220 1237 10.1021/pr501148q
8. M. van der Laan, M. Bohnert, N. Wiedemann, and N. Pfanner Role of MINOS in mitochondrial membrane architecture and biogenesis Trends Cell Biol. 22 2012 185 192 10.1016/j.tcb.2012.01.004
9. H.A. Krebs The August Krogh Principle: "For many problems there is an animal on which it can be most conveniently studied J. Exp. Zool. 194 1975 221 226 10.1002/jez.1401940115
10. C.B. Jørgensen August Krogh and Claude Bernard on basic principles in experimental physiology Bioscience 51 2001 59 10.1641/0006-3568(2001)051[0059:AKACBO]2.0.CO;2
11. M. Ridley The Explanation of Organic Diversity: the Comparative Method and Adaptations for Mating 1983 Clarendon Press (https://books.google.ca/books/about/The-explanation-of-organic-diversity.html?id=dPgUAQAAIAAJ&pgis=1 (accessed November 15, 2015))
12. D.J. Futuyma Evolutionary Biology 1986 Sinauer Associates (https://books.google.ca/books/about/Evolutionary-biology.html?id=g6XuAAAAMAAJ&pgis=1 (accessed November 15, 2015))
13. M.A. O'Malley, A.G.B. Simpson, and A.J. Roger The other eukaryotes in light of evolutionary protistology Biol. Philos. 28 2012 299 330 10.1007/s10539-012-9354-y
14. J.B. Dacks, and W.F. Doolittle Reconstructing/deconstructing the earliest eukaryotes: how comparative genomics can help Cell 107 2001 419 425 http://www.ncbi.nlm.nih.gov/pubmed/11719183 (accessed October 14, 2015)
15. S.M. Adl, A.G.B. Simpson, C.E. Lane, J. Lukeš, D. Bass, S.S. Bowser, and et al. The revised classification of eukaryotes J. Eukaryot. Microbiol. 59 2012 429 493 10.1111/j.1550-7408.2012.00644.x
16. M. Lynch, M.C. Field, H.V. Goodson, H.S. Malik, J.B. Pereira-Leal, D.S. Roos, and et al. Evolutionary cell biology: two origins, one objective Proc. Natl. Acad. Sci. U. S. A. 111 2014 16990 16994 10.1073/pnas.1415861111
17. J. Hirst, L.D. Barlow, G.C. Francisco, D.A. Sahlender, M.N.J. Seaman, J.B. Dacks, and et al. The fifth adaptor protein complex PLoS Biol. 9 2011 e1001170 10.1371/journal.pbio.1001170
18. J. Hirst, A. Schlacht, J.P. Norcott, D. Traynor, G. Bloomfield, R. Antrobus, and et al. Characterization of TSET, an ancient and widespread membrane trafficking complex Elife 3 2014 e02866 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4031984&tool=pmcentrez&rendertype=abstract (accessed October 14, 2015))
19. M.M. Leger, M. Petrů, V. Žárský, L. Eme, Č. Vlček, T. Harding, and et al. An ancestral bacterial division system is widespread in eukaryotic mitochondria Proc. Natl. Acad. Sci. U. S. A. 112 2015 10239 10246 10.1073/pnas.1421392112
20. J.G. Wideman, R.M.R. Gawryluk, M.W. Gray, and J.B. Dacks The ancient and widespread nature of the ER-mitochondria encounter structure Mol. Biol. Evol. 30 2013 2044 2049 10.1093/molbev/mst120
21. N. Flinner, L. Ellenrieder, S.B. Stiller, T. Becker, E. Schleiff, and O. Mirus Mdm10 is an ancient eukaryotic porin co-occurring with the ERMES complex Biochim. Biophys. Acta 1833 2013 3314 3325 10.1016/j.bbamcr.2013.10.006
22. S.A. Muñoz-Gómez, C.H. Slamovits, J.B. Dacks, K.A. Baier, K.D. Spencer, and J.G. Wideman Ancient homology of the mitochondrial contact site and cristae organizing system points to an endosymbiotic origin of mitochondrial cristae Curr. Biol. 25 2015 1489 1495 10.1016/j.cub.2015.04.006
23. D.C. Hess, C.L. Myers, C. Huttenhower, M.A. Hibbs, A.P. Hayes, J. Paw, and et al. Computationally driven, quantitative experiments discover genes required for mitochondrial biogenesis PLoS Genet. 5 2009 e1000407 10.1371/journal.pgen.1000407
24. E. Braschi, V. Goyon, R. Zunino, A. Mohanty, L. Xu, and H.M. McBride Vps35 mediates vesicle transport between the mitochondria and peroxisomes Curr. Biol. 20 2010 1310 1315 10.1016/j.cub.2010.05.066
25. M. Neuspiel, A.C. Schauss, E. Braschi, R. Zunino, P. Rippstein, R. a Rachubinski, and et al. Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers Curr. Biol. 18 2008 102 108 10.1016/j.cub.2007.12.038
26. G.-L. McLelland, V. Soubannier, C.X. Chen, H.M. McBride, and E.A. Fon Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control EMBO J. 33 2014 282 295 10.1002/embj.201385902
27. A. Sugiura, G.-L. McLelland, E.A. Fon, and H.M. McBride A new pathway for mitochondrial quality control: mitochondrial-derived vesicles EMBO J. 2014 10.15252/embj.201488104
28. S.E. Horvath, and G. Daum Lipids of mitochondria Prog. Lipid Res. 52 2013 590 614 10.1016/j.plipres.2013.07.002
29. C. Osman, D.R. Voelker, and T. Langer Making heads or tails of phospholipids in mitochondria J. Cell Biol. 192 2011 7 16 10.1083/jcb.201006159
30. 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 10.1074/jbc.M505478200
31. Y. Tamura, M. Iijima, and H. Sesaki Mdm35p imports Ups proteins into the mitochondrial intermembrane space by functional complex formation EMBO J. 29 2010 2875 2887 10.1038/emboj.2010.149
32. C. Potting, C. Wilmes, T. Engmann, C. Osman, and T. Langer Regulation of mitochondrial phospholipids by Ups1/PRELI-like proteins depends on proteolysis and Mdm35 EMBO J. 29 2010 2888 2898 10.1038/emboj.2010.169
33. Y. Tamura, O. Onguka, A.E.A. Hobbs, R.E. Jensen, M. Iijima, S.M. Claypool, and et al. Role for two conserved intermembrane space proteins, Ups1p and Ups2p, [corrected] in intra-mitochondrial phospholipid trafficking J. Biol. Chem. 287 2012 15205 15218 10.1074/jbc.M111.338665
34. M. Connerth, T. Tatsuta, M. Haag, T. Klecker, B. Westermann, and T. Langer Intramitochondrial transport of phosphatidic acid in yeast by a lipid transfer protein Science 338 2012 815 818 10.1126/science.1225625
35. Y. Tamura, H. Sesaki, and T. Endo Phospholipid transport via mitochondria Traffic 15 2014 933 945 10.1111/tra.12188
36. Y. Watanabe, Y. Tamura, S. Kawano, and T. Endo Structural and mechanistic insights into phospholipid transfer by Ups1-Mdm35 in mitochondria Nat. Commun. 6 2015 7922 10.1038/ncomms8922
37. F. Yu, F. He, H. Yao, C. Wang, J. Wang, J. Li, and et al. Structural basis of intramitochondrial phosphatidic acid transport mediated by Ups1-Mdm35 complex EMBO Rep. 16 2015 813 823 10.15252/embr.201540137
38. X. Miliara, J.A. Garnett, T. Tatsuta, F. Abid Ali, H. Baldie, I. Pérez-Dorado, and et al. Structural insight into the TRIAP1/PRELI-like domain family of mitochondrial phospholipid transfer complexes EMBO Rep. 16 2015 824 835 10.15252/embr.201540229
39. B. Kornmann, E. Currie, S.R. Collins, M. Schuldiner, J. Nunnari, J.S. Weissman, and et al. An ER-mitochondria tethering complex revealed by a synthetic biology screen Science 325 2009 477 481 10.1126/science.1175088
40. K.O. Kopec, V. Alva, and A.N. Lupas Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria Bioinformatics 26 2010 1927 1931 10.1093/bioinformatics/btq326
41. K.O. Kopec, V. Alva, and A.N. Lupas Bioinformatics of the TULIP domain superfamily Biochem. Soc. Trans. 39 2011 1033 1038 10.1042/BST0391033
42. R.L. Frederick, J.M. McCaffery, K.W. Cunningham, K. Okamoto, and J.M. Shaw Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway J. Cell Biol. 167 2004 87 98 10.1083/jcb.200405100
43. B. Kornmann, C. Osman, and P. Walter The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections Proc. Natl. Acad. Sci. U. S. A. 108 2011 14151 14156 10.1073/pnas.1111314108
44. D.A. Stroud, S. Oeljeklaus, S. Wiese, M. Bohnert, U. Lewandrowski, A. Sickmann, and et al. Composition and topology of the endoplasmic reticulum-mitochondria encounter structure J. Mol. Biol. 413 2011 743 750 10.1016/j.jmb.2011.09.012
45. G. Vlahou, M. Eliáš, J.-C. von Kleist-Retzow, R.J. Wiesner, and F. Rivero The Ras related GTPase Miro is not required for mitochondrial transport in Dictyostelium discoideum Eur. J. Cell Biol. 90 2011 342 355 10.1016/j.ejcb.2010.10.012
46. B. Kornmann, and P. Walter ERMES-mediated ER-mitochondria contacts: molecular hubs for the regulation of mitochondrial biology J. Cell Sci. 123 2010 1389 1393 10.1242/jcs.058636
47. A.H. Michel, and B. Kornmann The ERMES complex and ER-mitochondria connections Biochem. Soc. Trans. 40 2012 445 450 10.1042/BST20110758
48. A. Lang, A.T. John Peter, and B. Kornmann ER-mitochondria contact sites in yeast: beyond the myths of ERMES Curr. Opin. Cell Biol. 35 2015 7 12 10.1016/j.ceb.2015.03.002
49. A.P. AhYoung, J. Jiang, J. Zhang, X. Khoi Dang, J.A. Loo, Z.H. Zhou, and et al. Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly Proc. Natl. Acad. Sci. U. S. A. 112 2015 E3179 E3188 10.1073/pnas.1422363112
50. C. Meisinger, M. Rissler, A. Chacinska, L.K.S. Szklarz, D. Milenkovic, V. Kozjak, and et al. The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane Dev. Cell 7 2004 61 71 10.1016/j.devcel.2004.06.003
51. C. Meisinger, S. Pfannschmidt, M. Rissler, D. Milenkovic, T. Becker, D. Stojanovski, and et al. The morphology proteins Mdm12/Mmm1 function in the major beta-barrel assembly pathway of mitochondria EMBO J. 26 2007 2229 2239 10.1038/sj.emboj.7601673
52. J.G. Wideman, N.E. Go, A. Klein, E. Redmond, S.W.K. Lackey, T. Tao, and et al. Roles of the Mdm10, Tom7, Mdm12, and Mmm1 proteins in the assembly of mitochondrial outer membrane proteins in Neurospora crassa Mol. Biol. Cell 21 2010 1725 1736 10.1091/mbc.E09-10-0844
53. J.G. Wideman, S.W.K. Lackey, M. a Srayko, K. a Norton, and F.E. Nargang Analysis of mutations in Neurospora crassa ERMES components reveals specific functions related to β-barrel protein assembly and maintenance of mitochondrial morphology PLoS One 8 2013 e71837 10.1371/journal.pone.0071837
54. S. Böckler, and B. Westermann Mitochondrial ER contacts are crucial for mitophagy in yeast Dev. Cell 28 2014 450 458 10.1016/j.devcel.2014.01.012
55. S. Böckler, and B. Westermann ER-mitochondria contacts as sites of mitophagosome formation Autophagy 10 2014 1346 1347 10.4161/auto.28981
56. A. Murley, L.L. Lackner, C. Osman, M. West, G.K. Voeltz, P. Walter, and et al. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast Elife 2 2013 e00422 10.7554/eLife.00422
57. K.V. Koch, R. Suelmann, and R. Fischer Deletion of mdmB impairs mitochondrial distribution and morphology in Aspergillus nidulans Cell Motil. Cytoskeleton 55 2003 114 124 10.1002/cm.10117
58. K.H. Berger, L.F. Sogo, and M.P. Yaffe Mdm12p, a component required for mitochondrial inheritance that is conserved between budding and fission yeast J. Cell Biol. 136 1997 545 553 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2134291&tool=pmcentrez&rendertype=abstract (accessed September 29, 2015))
59. C. Jamet-Vierny, V. Contamine, J. Boulay, D. Zickler, and M. Picard Mutations in genes encoding the mitochondrial outer membrane proteins Tom70 and Mdm10 of Podospora anserina modify the spectrum of mitochondrial DNA rearrangements associated with cellular death Mol. Cell. Biol. 17 1997 6359 6366 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=232487&tool=pmcentrez&rendertype=abstract (accessed September 30, 2015))
60. L.F. Sogo, and M.P. Yaffe Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane J. Cell Biol. 126 1994 1361 1373 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2290945&tool=pmcentrez&rendertype=abstract (accessed September 29, 2015))
61. 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 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2199622&tool=pmcentrez&rendertype=abstract (accessed September 29, 2015))
62. M.J. Youngman, A.E.A. Hobbs, S.M. Burgess, M. Srinivasan, and R.E. Jensen Mmm2p, a mitochondrial outer membrane protein required for yeast mitochondrial shape and maintenance of mtDNA nucleoids J. Cell Biol. 164 2004 677 688 10.1083/jcb.200308012
63. T.T. Nguyen, A. Lewandowska, J.-Y. Choi, D.F. Markgraf, M. Junker, M. Bilgin, and et al. Gem1 and ERMES do not directly affect phosphatidylserine transport from ER to mitochondria or mitochondrial inheritance Traffic 13 2012 880 890 10.1111/j.1600-0854.2012.01352.x
64. N. Gebert, A.S. Joshi, S. Kutik, T. Becker, M. McKenzie, X.L. Guan, and et al. Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome Curr. Biol. 19 2009 2133 2139 10.1016/j.cub.2009.10.074
65. T. Becker, S.E. Horvath, L. Böttinger, N. Gebert, G. Daum, and N. Pfanner Role of phosphatidylethanolamine in the biogenesis of mitochondrial outer membrane proteins J. Biol. Chem. 288 2013 16451 16459 10.1074/jbc.M112.442392
66. M.-H. Schuler, F. Di Bartolomeo, L. Boettinger, S.E. Horvath, L.-S. Wenz, G. Daum, and et al. Phosphatidylcholine affects the role of the sorting and assembly machinery in the biogenesis of mitochondrial β-barrel proteins J. Biol. Chem. 2015 10.1074/jbc.M115.687921
67. F.-N. Vögtle, M. Keller, A.A. Taskin, S.E. Horvath, X.L. Guan, C. Prinz, and et al. The fusogenic lipid phosphatidic acid promotes the biogenesis of mitochondrial outer membrane protein Ugo1 J. Cell Biol. 210 2015 951 960 10.1083/jcb.201506085
68. I.R. Boldogh, D.W. Nowakowski, H.-C. Yang, H. Chung, S. Karmon, P. Royes, and et al. A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery Mol. Biol. Cell 14 2003 4618 4627 10.1091/mbc.E03-04-0225
69. T. Hanekamp, M.K. Thorsness, I. Rebbapragada, E.M. Fisher, C. Seebart, M.R. Darland, and et al. Maintenance of mitochondrial morphology is linked to maintenance of the mitochondrial genome in Saccharomyces cerevisiae Genetics 162 2002 1147 1156 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1462334&tool=pmcentrez&rendertype=abstract (accessed September 29, 2015))
70. S.M. Burgess, M. Delannoy, and R.E. Jensen MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria J. Cell Biol. 126 1994 1375 1391 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2290956&tool=pmcentrez&rendertype=abstract (accessed September 29, 2015))
71. C. Osman, M. Haag, C. Potting, J. Rodenfels, P.V. Dip, F.T. Wieland, and et al. The genetic interactome of prohibitins: coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria J. Cell Biol. 184 2009 583 596 10.1083/jcb.200810189
72. C.M. Schauder, X. Wu, Y. Saheki, P. Narayanaswamy, F. Torta, M.R. Wenk, and et al. Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer Nature 510 2014 552 555 10.1038/nature13269
73. S. Lahiri, J.T. Chao, S. Tavassoli, A.K.O. Wong, V. Choudhary, B.P. Young, and et al. A conserved endoplasmic reticulum membrane protein complex (EMC) facilitates phospholipid transfer from the ER to mitochondria PLoS Biol. 12 2014 e1001969 10.1371/journal.pbio.1001969
74. Y. Elbaz-Alon, E. Rosenfeld-Gur, V. Shinder, A.H. Futerman, T. Geiger, and M. Schuldiner A dynamic interface between vacuoles and mitochondria in yeast Dev. Cell 30 2014 95 102 10.1016/j.devcel.2014.06.007
75. C. Hönscher, M. Mari, K. Auffarth, M. Bohnert, J. Griffith, W. Geerts, and et al. Cellular metabolism regulates contact sites between vacuoles and mitochondria Dev. Cell 30 2014 86 94 10.1016/j.devcel.2014.06.006
76. A.B. Lang, A.T.J. Peter, P. Walter, and B. Kornmann ER-mitochondrial junctions can be bypassed by dominant mutations in the endosomal protein Vps13 J. Cell Biol. 210 2015 883 890 10.1083/jcb.201502105
77. Y. Elbaz-Alon, M. Eisenberg-Bord, V. Shinder, S.B. Stiller, E. Shimoni, N. Wiedemann, and et al. Lam6 regulates the extent of contacts between organelles Cell Rep. 12 2015 7 14 10.1016/j.celrep.2015.06.022
78. A. Murley, R.D. Sarsam, A. Toulmay, J. Yamada, W.A. Prinz, and J. Nunnari Ltc1 is an ER-localized sterol transporter and a component of ER-mitochondria and ER-vacuole contacts J. Cell Biol. 209 2015 539 548 10.1083/jcb.201502033
79. J.G. Wideman The Ubiquitous And Ancient Er Membrane Protein Complex (EMC): Tether Or Not? F1000Research 4 2015 10.12688/f1000research.6944.1
80. J.C. Christianson, J. a Olzmann, T. a Shaler, M.E. Sowa, E.J. Bennett, C.M. Richter, and et al. Defining human ERAD networks through an integrative mapping strategy Nat. Cell Biol. 14 2012 93 105 10.1038/ncb2383
81. M. Jonikas, S. Collins, V. Denic, and E. Oh Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum Science 80-. 2009 1693 1697 10.1126/science.1167983
82. M. Richard, T. Boulin, V.J.P. Robert, J.E. Richmond, and J.-L. Bessereau Biosynthesis of ionotropic acetylcholine receptors requires the evolutionarily conserved ER membrane complex Proc. Natl. Acad. Sci. U. S. A. 110 2013 E1055 E1063 10.1073/pnas.1216154110
83. Y. Li, Y. Zhao, J. Hu, J. Xiao, L. Qu, Z. Wang, and et al. A novel ER-localized transmembrane protein, EMC6, interacts with RAB5A and regulates cell autophagy Autophagy 9 2013 150 163 10.4161/auto.22742
84. T. Satoh, A. Ohba, Z. Liu, T. Inagaki, and A.K. Satoh dPob/EMC is essential for biosynthesis of rhodopsin and other multi-pass membrane proteins in Drosophila photoreceptors Elife 4 2015 10.7554/eLife.06306
85. K. Dietmeier, A. Hönlinger, U. Bömer, P.J. Dekker, C. Eckerskorn, F. Lottspeich, and et al. Tom5 functionally links mitochondrial preprotein receptors to the general import pore Nature 388 1997 195 200 10.1038/40663
86. S. Schmitt, U. Ahting, L. Eichacker, B. Granvogl, N.E. Go, F.E. Nargang, and et al. Role of Tom5 in maintaining the structural stability of the TOM complex of mitochondria J. Biol. Chem. 280 2005 14499 14506 10.1074/jbc.M413667200
87. E.L. Sherman, N.E. Go, and F.E. Nargang Functions of the small proteins in the TOM complex of Neurospora crasssa Mol. Biol. Cell 16 2005 4172 4182 10.1091/mbc.E05-03-0187
88. H. Kato, and K. Mihara Identification of Tom5 and Tom6 in the preprotein translocase complex of human mitochondrial outer membrane Biochem. Biophys. Res. Commun. 369 2008 958 963 10.1016/j.bbrc.2008.02.150
89. D. Maćasev, J. Whelan, E. Newbigin, M.C. Silva-Filho, T.D. Mulhern, and T. Lithgow Tom22', an 8-kDa trans-site receptor in plants and protozoans, is a conserved feature of the TOM complex that appeared early in the evolution of eukaryotes Mol. Biol. Evol. 21 2004 1557 1564 10.1093/molbev/msh166
90. J. Mani, C. Meisinger, and A. Schneider Peeping at TOMs - diverse entry gates to mitochondria provide insights into the evolution of eukaryotes Mol. Biol. Evol. 2015 msv219 10.1093/molbev/msv219
91. J.M.T. Hyttinen, M. Niittykoski, A. Salminen, and K. Kaarniranta Maturation of autophagosomes and endosomes: a key role for Rab7 Biochim. Biophys. Acta 1833 2013 503 510 10.1016/j.bbamcr.2012.11.018
92. J. Numrich, and C. Ungermann Endocytic Rabs in membrane trafficking and signaling Biol. Chem. 395 2014 327 333 10.1515/hsz-2013-0258
93. H.J. kleine Balderhaar, and C. Ungermann CORVET and HOPS tethering complexes - coordinators of endosome and lysosome fusion J. Cell Sci. 126 2013 1307 1316 10.1242/jcs.107805
94. H.G. Suresh, A.X. da Silveira Dos Santos, W. Kukulski, J. Tyedmers, H. Riezman, B. Bukau, and et al. Prolonged starvation drives reversible sequestration of lipid biosynthetic enzymes and organelle reorganization in Saccharomyces cerevisiae Mol. Biol. Cell 26 2015 1601 1615 10.1091/mbc.E14-11-1559
95. C.M. Klinger, M.J. Klute, and J.B. Dacks Comparative genomic analysis of multi-subunit tethering complexes demonstrates an ancient pan-eukaryotic complement and sculpting in Apicomplexa PLoS ONE 8 2013 e76278 10.1371/journal.pone.0076278
96. V.L. Koumandou, J.B. Dacks, R.M.R. Coulson, and M.C. Field Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins BMC Evol. Biol. 7 2007 29 10.1186/1471-2148-7-29
97. S. Muñoz-Braceras, R. Calvo, and R. Escalante TipC and the chorea-acanthocytosis protein VPS13A regulate autophagy in Dictyostelium and human HeLa cells Autophagy 11 2015 918 927 10.1080/15548627.2015.1034413
98. J.-S. Park, S. Halegoua, S. Kishida, and A.M. Neiman A conserved function in phosphatidylinositol metabolism for mammalian Vps13 family proteins PLoS ONE 10 2015 e0124836 10.1371/journal.pone.0124836
99. H.S. Samaranayake, A.E. Cowan, and L.A. Klobutcher Vacuolar protein sorting protein 13 A, TtVPS13A, localizes to the tetrahymena thermophila phagosome membrane and is required for efficient phagocytosis Eukaryot. Cell 10 2011 1207 1218 10.1128/EC.05089-11
100. J.H. Brickner, and R.S. Fuller SOI1 encodes a novel, conserved protein that promotes TGN-endosomal cycling of Kex2p and other membrane proteins by modulating the function of two TGN localization signals J. Cell Biol. 139 1997 23 36 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2139830&tool=pmcentrez&rendertype=abstract (accessed September 30, 2015))
101. J.-S. Park, Y. Okumura, H. Tachikawa, and A.M. Neiman SPO71 encodes a developmental stage-specific partner for Vps13 in Saccharomyces cerevisiae Eukaryot. Cell 12 2013 1530 1537 10.1128/EC.00239-13
102. J.-S. Park, and A.M. Neiman VPS13 regulates membrane morphogenesis during sporulation in Saccharomyces cerevisiae J. Cell Sci. 125 2012 3004 3011 10.1242/jcs.105114
103. A.T. Gatta, L.H. Wong, Y.Y. Sere, D.M. Calderón-Noreña, S. Cockcroft, A.K. Menon, and et al. A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport Elife 4 2015 10.7554/eLife.07253
104. T. Tan, C. Ozbalci, B. Brügger, D. Rapaport, and K.S. Dimmer Mcp1 and Mcp2, two novel proteins involved in mitochondrial lipid homeostasis J. Cell Sci. 126 2013 3563 3574 10.1242/jcs.121244
105. K. von der Malsburg, J.M. Müller, M. Bohnert, S. Oeljeklaus, P. Kwiatkowska, T. Becker, and et al. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis Dev. Cell 21 2011 694 707 10.1016/j.devcel.2011.08.026
106. M. Harner, C. Körner, D. Walther, D. Mokranjac, J. Kaesmacher, U. Welsch, and et al. The mitochondrial contact site complex, a determinant of mitochondrial architecture EMBO J. 30 2011 4356 4370 10.1038/emboj.2011.379
107. R. Rabl, V. Soubannier, R. Scholz, F. Vogel, N. Mendl, A. Vasiljev-Neumeyer, and et al. Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g J. Cell Biol. 185 2009 1047 1063 10.1083/jcb.200811099
108. D.C. Jans, C.A. Wurm, D. Riedel, D. Wenzel, F. Stagge, M. Deckers, and et al. STED super-resolution microscopy reveals an array of MINOS clusters along human mitochondria Proc. Natl. Acad. Sci. U. S. A. 110 2013 8936 8941 10.1073/pnas.1301820110
109. F. Vogel, C. Bornhövd, W. Neupert, and A.S. Reichert Dynamic subcompartmentalization of the mitochondrial inner membrane J. Cell Biol. 175 2006 237 247 10.1083/jcb.200605138
110. C.A. Wurm, and S. Jakobs Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast FEBS Lett. 580 2006 5628 5634 10.1016/j.febslet.2006.09.012
111. J.R. Friedman, A. Mourier, J. Yamada, J.M. McCaffery, and J. Nunnari MICOS coordinates with respiratory complexes and lipids to establish mitochondrial inner membrane architecture Elife 4 2015 10.7554/eLife.07739
112. G.B. John, Y. Shang, L. Li, C. Renken, C.A. Mannella, J.M.L. Selker, and et al. The mitochondrial inner membrane protein mitofilin controls cristae morphology Mol. Biol. Cell 16 2005 1543 1554 10.1091/mbc.E04-08-0697
113. C. Körner, M. Barrera, J. Dukanovic, K. Eydt, M. Harner, R. Rabl, and et al. 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 2012 2143 2155 10.1091/mbc.E11-10-0831
114. C.A. Mannella, W.J. Lederer, and M.S. Jafri The connection between inner membrane topology and mitochondrial function J. Mol. Cell. Cardiol. 62 2013 51 57 10.1016/j.yjmcc.2013.05.001
115. M. Zick, R. Rabl, and A.S. Reichert Cristae formation-linking ultrastructure and function of mitochondria Biochim. Biophys. Acta 1793 2009 5 19 10.1016/j.bbamcr.2008.06.013
116. R.M. Zerbes, I.J. van der Klei, M. Veenhuis, N. Pfanner, M. van der Laan, and M. Bohnert Mitofilin complexes: conserved organizers of mitochondrial membrane architecture Biol. Chem. 393 2012 1247 1261 10.1515/hsz-2012-0239
117. S. Meeusen, R. DeVay, J. Block, A. Cassidy-Stone, S. Wayson, J.M. McCaffery, and et al. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1 Cell 127 2006 383 395 10.1016/j.cell.2006.09.021
118. S. Cogliati, C. Frezza, M.E. Soriano, T. Varanita, R. Quintana-Cabrera, M. Corrado, and et al. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency Cell 155 2013 160 171 10.1016/j.cell.2013.08.032
119. M. Strauss, G. Hofhaus, R.R. Schröder, and W. Kühlbrandt Dimer ribbons of ATP synthase shape the inner mitochondrial membrane EMBO J. 27 2008 1154 1160 10.1038/emboj.2008.35
120. K.M. Davies, C. Anselmi, I. Wittig, J.D. Faraldo-Gomez, and W. Kuhlbrandt Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae Proc. Natl. Acad. Sci. 109 2012 13602 13607 10.1073/pnas.1204593109
121. N. Pfanner, M. van der Laan, P. Amati, R.A. Capaldi, A.A. Caudy, A. Chacinska, and et al. Uniform nomenclature for the mitochondrial contact site and cristae organizing system J. Cell Biol. 204 2014 1083 1086 10.1083/jcb.201401006
122. R.M. Zerbes, M. Bohnert, D.A. Stroud, K. von der Malsburg, A. Kram, S. Oeljeklaus, and et al. Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially depend on mitofilin domains J. Mol. Biol. 422 2012 183 191 10.1016/j.jmb.2012.05.004
123. C. Ott, K. Ross, S. Straub, B. Thiede, M. Götz, C. Goosmann, and et al. Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes Mol. Cell. Biol. 32 2012 1173 1188 10.1128/MCB.06388-11
124. M. Barbot, D.C. Jans, C. Schulz, N. Denkert, B. Kroppen, M. Hoppert, and et al. Mic10 oligomerizes to bend mitochondrial inner membranes at cristae junctions Cell Metab. 21 2015 756 763 10.1016/j.cmet.2015.04.006
125. M. Bohnert, R.M. Zerbes, K.M. Davies, A.W. Mühleip, H. Rampelt, S.E. Horvath, and et al. Central role of Mic10 in the mitochondrial contact site and cristae organizing system Cell Metab. 21 2015 747 755 10.1016/j.cmet.2015.04.007
126. S. Koob, and A.S. Reichert Novel intracellular functions of apolipoproteins: the ApoO protein family as constituents of the Mitofilin/MINOS complex determines cristae morphology in mitochondria Biol. Chem. 395 2014 285 296 10.1515/hsz-2013-0274
127. M.A. Huynen, M. Mühlmeister, K. Gotthardt, S. Guerrero-Castillo, and U. Brandt Evolution and structural organization of the mitochondrial contact site (MICOS) complex and the mitochondrial intermembrane space bridging (MIB) complex Biochim. Biophys. Acta 1863 2015 91 101 10.1016/j.bbamcr.2015.10.009
128. S.A. Muñoz-Gómez, C.H. Slamovits, J.B. Dacks, and J.G. Wideman The evolution of MICOS: ancestral and derived functions and interactions Commun. Integr. Biol. 8 2015 10.1080/19420889.2015.1094593
129. V. Jayashankar, and S.M. Rafelski Integrating mitochondrial organization and dynamics with cellular architecture Curr. Opin. Cell Biol. 26 2014 34 40 10.1016/j.ceb.2013.09.002
130. S.E. Horvath, H. Rampelt, S. Oeljeklaus, B. Warscheid, M. van der Laan, and N. Pfanner Role of membrane contact sites in protein import into mitochondria Protein Sci. 24 2015 277 297 10.1002/pro.2625
131. L.-S. Wenz, Ł. Opaliński, N. Wiedemann, and T. Becker Cooperation of protein machineries in mitochondrial protein sorting Biochim. Biophys. Acta 1853 2015 1119 1129 10.1016/j.bbamcr.2015.01.012
132. J.R. Friedman, and J. Nunnari Mitochondrial form and function Nature 505 2014 335 343 10.1038/nature12985
133. K. Itoh, Y. Tamura, M. Iijima, and H. Sesaki Effects of Fcj1-Mos1 and mitochondrial division on aggregation of mitochondrial DNA nucleoids and organelle morphology Mol. Biol. Cell 24 2013 1842 1851 10.1091/mbc.E13-03-0125
134. K.S. Dimmer, S. Jakobs, F. Vogel, K. Altmann, and B. Westermann Mdm31 and Mdm32 are inner membrane proteins required for maintenance of mitochondrial shape and stability of mitochondrial DNA nucleoids in yeast J. Cell Biol. 168 2005 103 115 10.1083/jcb.200410030
135. S. Meeusen, and J. Nunnari Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome J. Cell Biol. 163 2003 503 510 10.1083/jcb.200304040
136. T.A. Brown, A.N. Tkachuk, G. Shtengel, B.G. Kopek, D.F. Bogenhagen, H.F. Hess, and et al. Superresolution fluorescence imaging of mitochondrial nucleoids reveals their spatial range, limits, and membrane interaction Mol. Cell. Biol. 31 2011 4994 5010 10.1128/MCB.05694-11
137. B.G. Kopek, G. Shtengel, C.S. Xu, D.A. Clayton, and H.F. Hess Correlative 3D superresolution fluorescence and electron microscopy reveal the relationship of mitochondrial nucleoids to membranes Proc. Natl. Acad. Sci. U. S. A. 109 2012 6136 6141 10.1073/pnas.1121558109
138. R.-F. Yang, L.-H. Sun, R. Zhang, Y. Zhang, Y.-X. Luo, W. Zheng, and et al. Suppression of Mic60 compromises mitochondrial transcription and oxidative phosphorylation Sci. Rep. 5 2015 7990 10.1038/srep07990
139. L.L. Lackner, and J.M. Nunnari The molecular mechanism and cellular functions of mitochondrial division Biochim. Biophys. Acta 1792 2009 1138 1144 10.1016/j.bbadis.2008.11.011
140. J.R. Friedman, L.L. Lackner, M. West, J.R. DiBenedetto, J. Nunnari, and G.K. Voeltz ER tubules mark sites of mitochondrial division Science 334 2011 358 362 10.1126/science.1207385
141. C. Osman, C. Merkwirth, and T. Langer Prohibitins and the functional compartmentalization of mitochondrial membranes J. Cell Sci. 122 2009 3823 3830 10.1242/jcs.037655
142. T. Tatsuta, K. Model, and T. Langer Formation of membrane-bound ring complexes by prohibitins in mitochondria Mol. Biol. Cell 16 2005 248 259 10.1091/mbc.E04-09-0807
143. C. Merkwirth, S. Dargazanli, T. Tatsuta, S. Geimer, B. Löwer, F.T. Wunderlich, and et al. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria Genes Dev. 22 2008 476 488 10.1101/gad.460708
144. D.F. Bogenhagen, Y. Wang, E.L. Shen, and R. Kobayashi Protein components of mitochondrial DNA nucleoids in higher eukaryotes Mol. Cell. Proteomics 2 2003 1205 1216 10.1074/mcp.M300035-MCP200
145. K.H. Berger, and M.P. Yaffe Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae Mol. Cell. Biol. 18 1998 4043 4052 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=108989&tool=pmcentrez&rendertype=abstract (accessed September 29, 2015))
146. K.S. Dimmer, S. Fritz, F. Fuchs, M. Messerschmitt, N. Weinbach, W. Neupert, and et al. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae Mol. Biol. Cell 13 2002 847 853 10.1091/mbc.01-12-0588
147. B. Kucejova A screen for nigericin-resistant yeast mutants revealed genes controlling mitochondrial volume and mitochondrial cation homeostasis Genetics 171 2005 517 526 10.1534/genetics.105.046540
148. B. Ivan, D. Lajdova, L. Abelovska, M. Balazova, J. Nosek, and L. Tomaska Mdm31 protein mediates sensitivity to potassium ionophores but does not regulate mitochondrial morphology or phospholipid trafficking in Schizosaccharomyces pombe Yeast 32 2015 345 354 10.1002/yea.3062
149. S.F. Altschul, T.L. Madden, A.A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 25 1997 3389 3402 http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=146917&tool=pmcentrez&rendertype=abstract (accessed July 9, 2014))
150. R.D. Finn, J. Clements, and S.R. Eddy HMMER web server: interactive sequence similarity searching Nucleic Acids Res. 39 2011 W29 W37 10.1093/nar/gkr367