Mitochondrial involvement in cell death of non-mammalian eukaryotes

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 4, 2011, Pages 597-607

  Abdelwahid, Eltyeb ^a   Rolland, Stephane ^b   Teng, Xinchen ^c   Conradt, Barbara ^b   Hardwick, J Marie ^c   White, Kristin ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; C. elegans; Drosophila; Mitochondria; Yeast

Indexed keywords

APOPTOSIS; CAENORHABDITIS ELEGANS; CELL DEATH; CELL STRUCTURE; DROSOPHILA; EUKARYOTE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE;

ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; HUMANS; MITOCHONDRIA; SACCHAROMYCES CEREVISIAE;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 79952740220     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.10.008     Document Type: Review

References (204)

1. Yuan J., Shaham S., Ledoux S., Ellis H.M., Horvitz H.R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 1993, 75:641-652.
2. Miura M., Zhu H., Rotello R., Hartwieg E.A., Yuan J. Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 1993, 75:653-660.
3. Hengartner M.O., Horvitz H.R. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 1994, 76:665-676.
4. Crook N.E., Clem R.J., Miller L.K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 1993, 67:2168-2174.
5. Hay B.A., Wassarman D.A., Rubin G.M. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 1995, 83:1253-1262.
6. Rothe M., Pan M.G., Henzel W.J., Ayres T.M., Goeddel D.V. The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 1995, 83:1243-1252.
7. Deveraux Q.L., Reed J.C. IAP family proteins-suppressors of apoptosis. Genes Dev. 1999, 13:239-252.
8. White K., Grether M.E., Abrams J.M., Young L., Farrell K., Steller H. Genetic control of programmed cell death in Drosophila. Science 1994, 264:677-683.
9. Vucic D., Kaiser W.J., Harvey A.J., Miller L.K. Inhibition of reaper-induced apoptosis by interaction with inhibitor of apoptosis proteins (IAPs). Proc. Natl. Acad. Sci. U. S. A. 1997, 94:10183-10188.
10. Wang S.L., Hawkins C.J., Yoo S.J., Muller H.A., Hay B.A. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 1999, 98:453-463.
11. Lisi S., Mazzon I., White K. Diverse domains of THREAD/DIAP1 are required to inhibit apoptosis induced by REAPER and HID in Drosophila. Genetics 2000, 154:669-678.
12. Goyal L., McCall K., Agapite J., Hartwieg E., Steller H. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 2000, 19:589-597.
13. Kanki T., Klionsky D.J. The molecular mechanism of mitochondria autophagy in yeast. Mol. Microbiol. 2010, 75:795-800.
14. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
15. Baehrecke E.H. Autophagy: dual roles in life and death?. Nat. Rev. Mol. Cell Biol. 2005, 6:505-510.
16. Kornbluth S., White K. Apoptosis in Drosophila: neither fish nor fowl (nor man, nor worm). J. Cell Sci. 2005, 118:1779-1787.
17. Hay B.A., Guo M. Caspase-dependent cell death in Drosophila. Annu. Rev. Cell Dev. Biol. 2006, 22:623-650.
18. Green D.R., Reed J.C. Mitochondria and apoptosis. Science 1998, 281:1309-1312.
19. H.R. Horvitz, Worms, Life, and Death (Nobel Lecture), Chembiochem 4 (2003) 697-711.
20. A.M. Chinnaiyan, K. O'Rourke, B.R. Lane, V.M., Dixit, interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death, Science 275 (1997) 1122-1126.
21. F. Chen, B.M. Hersh, B. Conradt, Z. Zhou, D. Riemer, Y. Gruenbaum, H.R. Horvitz, Translocation of C. elegans CED-4 to nuclear membranes during programmed cell death, Science 287 (2000) 1485-1489.
22. D. Wu, H.D. Wallen, G. Nunez, Interaction and regulation of subcellular localization of CED-4 by CED-9, Science 275 (1997) 1126-1129.
23. Spector M.S., Desnoyers S., Hoeppner D.J., Hengartner M.O. Interaction between the C. elegans cell-death regulators CED-9 and CED-4. Nature 1997, 385:653-656.
24. Conradt B., Horvitz H.R. The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 1998, 93:519-529.
25. L. del Peso, V.M. Gonzalez, G. Nunez, Caenorhabditis elegans EGL-1 disrupts the interaction of CED-9 with CED-4 and promotes CED-3 activation, J. Biol. Chem. 273 (1998) 33495-33500.
26. A.M. Chinnaiyan, D. Chaudhary, K. O'Rourke, E.V. Koonin, V.M. Dixit, Role of CED-4 in the activation of CED-3, Nature 388 (1997) 728-729.
27. S. Seshagiri, L.K. Miller, Caenorhabditis elegans CED-4 stimulates CED-3 processing and CED-3-induced apoptosis, Curr. Biol. 7 (1997) 455-460.
28. N. Yan, J. Chai, E.S. Lee, L. Gu, Q. Liu, J. He, J.W. Wu, D. Kokel, H. Li, Q. Hao, D. Xue, Y. Shi, Structure of the CED-4-CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans, Nature 437 (2005) 831-837.
29. S. Qi, Y. Pang, Q. Hu, Q. Liu, H. Li, Y. Zhou, T. He, Q. Liang, Y. Liu, X. Yuan, G. Luo, H. Li, J. Wang, N. Yan, Y. Shi, 2010. Crystal structure of the Caenorhabditis elegans apoptosome reveals an octameric assembly of CED-4, Cell 141 (2010) 446-457.
30. S. Rolland, B. Conradt, The role of mitochondria in apoptosis induction in Caenorhabditis elegans: more than just innocent bystanders? Cell Death Differ. 13 (2006) 1281-1286.
31. M.O. Hengartner, H.R. Horvitz, Activation of C. elegans cell death protein CED-9 by an ammo-acid substitution in a domain conserved in Bcl-2, Nature 369 (1994).
32. Chen P., Nordstrom W., Gish B., Abrams J.M. grim, A novel cell death gene in Drosophila. Genes Dev. 1996, 10:1773-1782.
33. Christich A., Kauppila S., Chen P., Sogame N., Ho S.I., Abrams J.M. The damage-responsive Drosophila gene sickle encodes a novel IAP binding protein similar to but distinct from reaper, grim, and hid. Curr. Biol. 2002, 12:137-140.
34. Grether M.E., Abrams J.M., Agapite J., White K., Steller H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 1995, 9:1694-1708.
35. O'Riordan M.X., Bauler L.D., Scott F.L., Duckett C.S. Inhibitor of apoptosis proteins in eukaryotic evolution and development: a model of thematic conservation. Dev. Cell. 2008, 15:497-508.
36. Xu D., Li Y., Arcaro M., Lackey M., Bergmann A. The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila. Development 2005, 132:2125-2134.
37. Kanuka H., Sawamoto K., Inohara N., Matsuno K., Okano H., Miura M. Control of the cell death pathway by Dapaf-1, a Drosophila Apaf-1/CED-4-related caspase activator. Mol. Cell 1999, 4:757-769.
38. Rodriguez A., Oliver H., Zou H., Chen P., Wang X., Abrams J.M. Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. Nat. Cell Biol. 1999, 1:272-279.
39. Zhou L., Song Z., Tittel J., Steller H. HAC-1, a Drosophila homolog of APAF-1 and CED-4 functions in developmental and radiation-induced apoptosis. Mol. Cell 1999, 4:745-755.
40. Ivanovska I., Hardwick J.M. Viruses activate a genetically conserved cell death pathway in a unicellular organism. J. Cell Biol. 2005, 170:391-399.
41. Breinig F., Sendzik T., Eisfeld K., Schmitt M.J. Dissecting toxin immunity in virus-infected killer yeast uncovers an intrinsic strategy of self-protection. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:3810-3815.
42. Cap M., Vachova L., Palkova Z. Yeast colony survival depends on metabolic adaptation and cell differentiation rather than on stress defense. J. Biol. Chem. 2009, 284:32572-32581.
43. Palkova Z., Vachova L. Life within a community: benefit to yeast long-term survival. FEMS Microbiol. Rev. 2006, 30:806-824.
44. Longo V.D., Mitteldorf J., Skulachev V.P. Programmed and altruistic ageing. Nat. Rev. Genet. 2005, 6:866-872.
45. Ameisen J.C. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ. 2002, 9:367-393.
46. Borello M.E. The rise, fall and resurrection of group selection. Endvour 2005, 29:43-47.
47. Madeo F., Herker E., Maldener C., Wissing S., Lachelt S., Herlan M., Fehr M., Lauber K., Sigrist S.J., Wesselborg S., Frohlich K.U. A caspase-related protease regulates apoptosis in yeast. Mol. Cell 2002, 9:911-917.
48. Sundstrom J.F., Vaculova A., Smertenko A.P., Savenkov E.I., Golovko A., Minina E., Tiwari B.S., Rodriguez-Nieto S., Zamyatnin A.A., Valineva T., Saarikettu J., Frilander M.J., Suarez M.F., Zavialov A., Stahl U., Hussey P.J., Silvennoinen O., Sundberg E., Zhivotovsky B., Bozhkov P.V. Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat. Cell Biol. 2009, 11:1347-1354.
49. Hardwick J.M., Youle R.J. SnapShot: BCL-2 proteins. Cell 2009, 138:404. (404.e1).
50. Walter D., Wissing S., Madeo F., Fahrenkrog B. The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2. J. Cell Sci. 2006, 119:1843-1851.
51. Abdelwahid E., Yokokura T., Krieser R.J., Balasundaram S., Fowle W.H., White K. Mitochondrial disruption in Drosophila apoptosis. Dev. Cell. 2007, 12:793-806.
52. Claveria C., Caminero E., Martinez-A C., Campuzano S., Torres M. GH3, a novel proapoptotic domain in Drosophila Grim, promotes a mitochondrial death pathway. EMBO J. 2002, 21:3327-3336.
53. Olson M.R., Holley C.L., Gan E.C., Colon-Ramos D.A., Kaplan B., Kornbluth S. A GH3-like domain in reaper is required for mitochondrial localization and induction of IAP degradation. J. Biol. Chem. 2003, 278:44758-44768.
54. Sandu C., Ryoo H.D., Steller H. Drosophila IAP antagonists form multimeric complexes to promote cell death. J. Cell Biol. 2010, 190:1039-1052.
55. Haining W.N., Carboy-Newcomb C., Wei C.L., Steller H. The proapoptotic function of Drosophila Hid is conserved in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4936-4941.
56. Freel C.D., Richardson D.A., Thomenius M.J., Gan E.C., Horn S.R., Olson M.R., Kornbluth S. Mitochondrial localization of Reaper to promote inhibitors of apoptosis protein degradation conferred by GH3 domain-lipid interactions. J. Biol. Chem. 2008, 283:367-379.
57. Fannjiang Y., Cheng W.C., Lee S.J., Qi B., Pevsner J., McCaffery J.M., Hill R.B., Basanez G., Hardwick J.M. Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev. 2004, 18:2785-2797.
58. Wissing S., Ludovico P., Herker E., Buttner S., Engelhardt S.M., Decker T., Link A., Proksch A., Rodrigues F., Corte-Real M., Frohlich K.U., Manns J., Cande C., Sigrist S.J., Kroemer G., Madeo F. An AIF orthologue regulates apoptosis in yeast. J. Cell Biol. 2004, 166:969-974.
59. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nat. Med. 2000, 6:513-519.
60. Tait S.W., Parsons M.J., Llambi F., Bouchier-Hayes L., Connell S., Munoz-Pinedo C., Green D.R. Resistance to caspase-independent cell death requires persistence of intact mitochondria. Dev. Cell. 2010, 18:802-813.
61. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997, 275:1132-1136.
62. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., Peng T.I., Jones D.P., Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 1997, 275:1129-1132.
63. Brachmann C.B., Jassim O.W., Wachsmuth B.D., Cagan R.L. The Drosophila bcl-2 family member dBorg-1 functions in the apoptotic response to UV-irradiation. Curr. Biol. 2000, 10:547-550.
64. Colussi P.A., Quinn L.M., Huang D.C., Coombe M., Read S.H., Richardson H., Kumar S. Debcl, a proapoptotic Bcl-2 homologue, is a component of the Drosophila melanogaster cell death machinery. J. Cell Biol. 2000, 148:703-714.
65. Igaki T., Kanuka H., Inohara N., Sawamoto K., Nunez G., Okano H., Miura M. Drob-1, a Drosophila member of the Bcl-2/CED-9 family that promotes cell death. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:662-667.
66. Cory S., Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2002, 2:647-656.
67. Doumanis J., Dorstyn L., Kumar S. Molecular determinants of the subcellular localization of the Drosophila Bcl-2 homologues DEBCL and BUFFY. Cell Death Differ. 2007, 14:907-915.
68. Galindo K.A., Lu W.J., Park J.H., Abrams J.M. The Bax/Bak ortholog in Drosophila, Debcl, exerts limited control over programmed cell death. Development 2009, 136:275-283.
69. Zhang H., Huang Q., Ke N., Matsuyama S., Hammock B., Godzik A., Reed J.C. Drosophila pro-apoptotic Bcl-2/Bax homologue reveals evolutionary conservation of cell death mechanisms. J. Biol. Chem. 2000, 275:27303-27306.
70. Quinn L., Coombe M., Mills K., Daish T., Colussi P., Kumar S., Richardson H. Buffy, a Drosophila Bcl-2 protein, has anti-apoptotic and cell cycle inhibitory functions. EMBO J. 2003, 22:3568-3579.
71. Park J., Lee S.B., Lee S., Kim Y., Song S., Kim S., Bae E., Kim J., Shong M., Kim J.M., Chung J. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 2006, 441:1157-1161.
72. Wu J.N., Nguyen N., Aghazarian M., Sevrioukov E.A., Monserrate J.P., Tang W., Mabuchi M., Tan Y., White K., Brachmann C.B. grim promotes programmed cell death of Drosophila microchaete glial cells. Mech. Dev. 2010.
73. Senoo-Matsuda N., Igaki T., Miura M. Bax-like protein Drob-1 protects neurons from expanded polyglutamine-induced toxicity in Drosophila. EMBO J. 2005, 24(14):2700-2713.
74. Lewis J., Oyler G.A., Ueno K., Fannjiang Y.R., Chau B.N., Vornov J., Korsmeyer S.J., Zou S., Hardwick J.M. Inhibition of virus-induced neuronal apoptosis by Bax. Nat. Med. 1999, 5:832-835.
75. Fannjiang Y., Kim C.H., Huganir R.L., Zou S., Lindsten T., Thompson C.B., Mito T., Traystman R.J., Larsen T., Griffin D.E., Mandir A.S., Dawson T.M., Dike S., Sappington A.L., Kerr D.A., Jonas E.A., Kaczmarek L.K., Hardwick J.M. BAK alters neuronal excitability and can switch from anti- to pro-death function during postnatal development. Dev. Cell 2003, 4:575-585.
76. Sevrioukov E.A., Burr J., Huang E.W., Assi H.H., Monserrate J.P., Purves D.C., Wu J.N., Song E.J., Brachmann C.B. Drosophila Bcl-2 proteins participate in stress-induced apoptosis, but are not required for normal development. Genesis 2007, 45:184-193.
77. Chen P., Ho S.I., Shi Z., Abrams J.M. Bifunctional killing activity encoded by conserved reaper proteins. Cell Death Differ. 2004, 11:704-713.
78. X. Wang, C. Yang, J. Chai, Y. Shi, D. Xue, Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans, Science 298 (2002) 1587-1592.
79. Q. Shen, F. Qin, Z. Gao, J. Cui, H. Xiao, Z. Xu, C. Yang, Adenine nucleotide translocator cooperates with core cell death machinery to promote apoptosis in Caenorhabditis elegans, Mol. Cell. Biol. 29 (2009) 3881-3893.
80. Wang C., Youle R.J. The role of mitochondria in apoptosis. Annu. Rev. Genet. 2009, 43:95-118.
81. Ludovico P., Rodrigues F., Almeida A., Silva M.T., Barrientos A., Corte-Real M. Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Mol. Biol. Cell 2002, 13:2598-2606.
82. Manon S., Chaudhuri B., Guerin M. Release of cytochrome c and decrease of cytochrome c oxidase in Bax-expressing yeast cells, and prevention of these effects by coexpression of Bcl-xL. FEBS Lett. 1997, 415:29-32.
83. Pereira C., Silva R.D., Saraiva L., Johansson B., Sousa M.J., Corte-Real M. Mitochondria-dependent apoptosis in yeast. Biochim. Biophys. Acta 2008, 1783:1286-1302.
84. Pereira C., Chaves S., Alves S., Salin B., Camougrand N., Manon S., Sousa M.J., Corte-Real M. Mitochondrial degradation in acetic acid-induced yeast apoptosis: the role of Pep4 and the ADP/ATP carrier. Mol. Microbiol. 2010, 76:1398-1410.
85. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91:479-489.
86. Heiskanen K.M., Bhat M.B., Wang H.W., Ma J., Nieminen A.L. Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J. Biol. Chem. 1999, 274:5654-5658.
87. Desagher S., Martinou J.C. Mitochondria as the central control point of apoptosis. Trends Cell Biol. 2000, 10:369-377.
88. Danial N.N., Korsmeyer S.J. Cell death: critical control points. Cell 2004, 116:205-219.
89. Korsmeyer S.J., Wei M.C., Saito M., Weiler S., Oh K.J., Schlesinger P.H. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ. 2000, 7:1166-1173.
90. Varkey J., Chen P., Jemmerson R., Abrams J.M. Altered cytochrome c display precedes apoptotic cell death in Drosophila. J. Cell Biol. 1999, 144:701-710.
91. Means J.C., Muro I., Clem R.J. Lack of involvement of mitochondrial factors in caspase activation in a Drosophila cell-free system. Cell Death Differ. 2006, 13:1222-1234.
92. Dorstyn L., Read S., Cakouros D., Huh J.R., Hay B.A., Kumar S. The role of cytochrome c in caspase activation in Drosophila melanogaster cells. J. Cell Biol. 2002, 156:1089-1098.
93. Zimmermann K.C., Ricci J.E., Droin N.M., Green D.R. The role of ARK in stress-induced apoptosis in Drosophila cells. J. Cell Biol. 2002, 156:1077-1087.
94. Challa M., Malladi S., Pellock B.J., Dresnek D., Varadarajan S., Yin Y.W., White K., Bratton S.B. Drosophila Omi, a mitochondrial-localized IAP antagonist and proapoptotic serine protease. EMBO J. 2007, 26:3144-3156.
95. Hao Z., Duncan G.S., Chang C.C., Elia A., Fang M., Wakeham A., Okada H., Calzascia T., Jang Y., You-Ten A., Yeh W.C., Ohashi P., Wang X., Mak T.W. Specific ablation of the apoptotic functions of cytochrome c reveals a differential requirement for cytochrome c and Apaf-1 in apoptosis. Cell 2005, 121:579-591.
96. Dorstyn L., Mills K., Lazebnik Y., Kumar S. The two cytochrome c species, DC3 and DC4, are not required for caspase activation and apoptosis in Drosophila cells. J. Cell Biol. 2004, 167:405-410.
97. Arama E., Agapite J., Steller H. Caspase activity and a specific cytochrome c are required for sperm differentiation in Drosophila. Dev. Cell 2003, 4:687-697.
98. Huh J.R., Vernooy S.Y., Yu H., Yan N., Shi Y., Guo M., Hay B.A. Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization. PLoS Biol. 2004, 2:E15.
99. Arama E., Bader M., Srivastava M., Bergmann A., Steller H. The two Drosophila cytochrome c proteins can function in both respiration and caspase activation. EMBO J. 2006, 25:232-243.
100. Mendes C.S., Arama E., Brown S., Scherr H., Srivastava M., Bergmann A., Steller H., Mollereau B. Cytochrome c-d regulates developmental apoptosis in the Drosophila retina. EMBO Rep. 2006, 7:933-939.
101. Yu X., Wang L., Acehan D., Wang X., Akey C.W. Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J. Mol. Biol. 2006, 355:577-589.
102. Kumarswamy R., Seth R.K., Dwarakanath B.S., Chandna S. Mitochondrial regulation of insect cell apoptosis: evidence for permeability transition pore-independent cytochrome-c release in the Lepidopteran Sf9 cells. Int. J. Biochem. Cell Biol. 2009, 41:1430-1440.
103. Gottfried Y., Rotem A., Lotan R., Steller H., Larisch S. The mitochondrial ARTS protein promotes apoptosis through targeting XIAP. EMBO J. 2004, 23:1627-1635.
104. Oberst A., Bender C., Green D.R. Living with death: the evolution of the mitochondrial pathway of apoptosis in animals. Cell Death Differ. 2008, 15:1139-1146.
105. Hegde R., Srinivasula S.M., Zhang Z., Wassell R., Mukattash R., Cilenti L., DuBois G., Lazebnik Y., Zervos A.S., Fernandes-Alnemri T., Alnemri E.S. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem. 2002, 277:432-438.
106. Suzuki Y., Imai Y., Nakayama H., Takahashi K., Takio K., Takahashi R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell 2001, 8:613-621.
107. Igaki T., Suzuki Y., Tokushige N., Aonuma H., Takahashi R., Miura M. Evolution of mitochondrial cell death pathway: proapoptotic role of HtrA2/Omi in Drosophila. Biochem. Biophys. Res. Commun. 2007, 356:993-997.
108. Khan F.S., Fujioka M., Datta P., Fernandes-Alnemri T., Jaynes J.B., Alnemri E.S. The interaction of DIAP1 with dOmi/HtrA2 regulates cell death in Drosophila. Cell Death Differ. 2008, 15:1073-1083.
109. Alnemri E.S. HtrA2 and Parkinson's disease: think PINK?. Nat. Cell Biol. 2007, 9:1227-1229.
110. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
111. Lipton S.A., Bossy-Wetzel E. Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 2002, 111:147-150.
112. Joza N., Galindo K., Pospisilik J.A., Benit P., Rangachari M., Kanitz E.E., Nakashima Y., Neely G.G., Rustin P., Abrams J.M., Kroemer G., Penninger J.M. The molecular archaeology of a mitochondrial death effector: AIF in Drosophila. Cell Death Differ. 2008, 15:1009-1018.
113. J. Parrish, L. Li, K. Klotz, D. Ledwich, X. Wang, D. Xue, Mitochondrial endonuclease G is important for apoptosis in C. elegans, Nature 412 (2001) 90-94.
114. Fraser A.G., James C., Evan G.I., Hengartner M.O. Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis. Curr. Biol. 1999, 9:292-301.
115. Li W., Sun L., Liang Q., Wang J., Mo W., Zhou B. Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol. Biol. Cell 2006, 17:1802-1811.
116. Sanz A., Soikkeli M., Portero-Otin M., Wilson A., Kemppainen E., McIlroy G., Ellila S., Kemppainen K.K., Tuomela T., Lakanmaa M., Kiviranta E., Stefanatos R., Dufour E., Hutz B., Naudi A., Jove M., Zeb A., Vartiainen S., Matsuno-Yagi A., Yagi T., Rustin P., Pamplona R., Jacobs H.T. Expression of the yeast NADH dehydrogenase Ndi1 in Drosophila confers increased lifespan independently of dietary restriction. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9105-9110.
117. Bahadorani S., Cho J., Lo T., Contreras H., Lawal H.O., Krantz D.E., Bradley T.J., Walker D.W. Neuronal expression of a single-subunit yeast NADH-ubiquinone oxidoreductase (Ndi1) extends Drosophila lifespan. Aging Cell 2010, 9:191-202.
118. Marella M., Seo B.B., Yagi T., Matsuno-Yagi A. Parkinson's disease and mitochondrial complex I: a perspective on the Ndi1 therapy. J. Bioenerg. Biomembr. 2009, 41:493-497.
119. Fahrenkrog B., Sauder U., Aebi U. The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis. J. Cell Sci. 2004, 117:115-126.
120. Buttner S., Eisenberg T., Carmona-Gutierrez D., Ruli D., Knauer H., Ruckenstuhl C., Sigrist C., Wissing S., Kollroser M., Frohlich K.U., Sigrist S., Madeo F. Endonuclease G regulates budding yeast life and death. Mol. Cell 2007, 25:233-246.
121. Collins T.J., Berridge M.J., Lipp P., Bootman M.D. Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 2002, 21:1616-1627.
122. Martinou J.C., Youle R.J. Which came first, the cytochrome c release or the mitochondrial fission?. Cell Death Differ. 2006, 13:1291-1295.
123. Smirnova E., Griparic L., Shurland D.L., van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 2001, 12:2245-2256.
124. Yoon Y., Pitts K.R., McNiven M.A. Mammalian dynamin-like protein DLP1 tubulates membranes. Mol. Biol. Cell 2001, 12:2894-2905.
125. James D.I., Parone P.A., Mattenberger Y., Martinou J.C. hFis1, a novel component of the mammalian mitochondrial fission machinery. J. Biol. Chem. 2003, 278:36373-36379.
126. Yoon Y., Krueger E.W., Oswald B.J., McNiven M.A. The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell. Biol. 2003, 23:5409-5420.
127. Stojanovski D., Koutsopoulos O.S., Okamoto K., Ryan M.T. Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology. J. Cell Sci. 2004, 117:1201-1210.
128. Karbowski M., Jeong S.Y., Youle R.J. Endophilin B1 is required for the maintenance of mitochondrial morphology. J. Cell Biol. 2004, 166:1027-1039.
129. Takahashi Y., Karbowski M., Yamaguchi H., Kazi A., Wu J., Sebti S.M., Youle R.J., Wang H.G. Loss of Bif-1 suppresses Bax/Bak conformational change and mitochondrial apoptosis. Mol. Cell. Biol. 2005, 25:9369-9382.
130. Tondera D., Czauderna F., Paulick K., Schwarzer R., Kaufmann J., Santel A. The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J. Cell Sci. 2005, 118:3049-3059.
131. Niemann A., Ruegg M., La Padula V., Schenone A., Suter U. Ganglioside-induced differentiation associated protein 1 is a regulator of the mitochondrial network: new implications for Charcot-Marie-Tooth disease. J. Cell Biol. 2005, 170:1067-1078.
132. Mukamel Z., Kimchi A. Death-associated protein 3 localizes to the mitochondria and is involved in the process of mitochondrial fragmentation during cell death. J. Biol. Chem. 2004, 279:36732-36738.
133. Chen H., Detmer S.A., Ewald A.J., Griffin E.E., Fraser S.E., Chan D.C. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 2003, 160:189-200.
134. Cipolat S., Martins de Brito O., Dal Zilio B., Scorrano L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:15927-15932.
135. Chen H., Chomyn A., Chan D.C. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 2005, 280:26185-26192.
136. Chan D.C. Dissecting mitochondrial fusion. Dev. Cell 2006, 11:592-594.
137. Goyal G., Fell B., Sarin A., Youle R.J., Sriram V. Role of mitochondrial remodeling in programmed cell death in Drosophila melanogaster. Dev. Cell 2007, 12:807-816.
138. S. Frank, B. Gaume, E. Bergmann-Leitner, W.W. Leitner, E.G. Robert, F. Catez, C.L. Smith, R.J. Youle, The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis, Dev. Cell 1 (2001) 515-525.
139. Jagasia R., Grote P., Westermann B., Conradt B. DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death in C. elegans. Nature 2005, 433:754-760.
140. Cheng W.C., Leach K.M., Hardwick J.M. Mitochondrial death pathways in yeast and mammalian cells. Biochim. Biophys. Acta 2008, 1783:1272-1279.
141. Arnoult D., Grodet A., Lee Y.J., Estaquier J., Blackstone C. Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J. Biol. Chem. 2005, 280:35742-35750.
142. Gao W., Pu Y., Luo K.Q., Chang D.C. Temporal relationship between cytochrome c release and mitochondrial swelling during UV-induced apoptosis in living HeLa cells. J. Cell Sci. 2001, 114:2855-2862.
143. Youle R.J., Karbowski M. Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 2005, 6:657-663.
144. Means J.C., Hays R. Mitochondrial membrane depolarization in Drosophila apoptosis. Cell Death Differ. 2007, 14:383-385.
145. Chipuk J.E., Bouchier-Hayes L., Green D.R. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 2006, 13:1396-1402.
146. Albeck J.G., Burke J.M., Aldridge B.B., Zhang M., Lauffenburger D.A., Sorger P.K. Quantitative analysis of pathways controlling extrinsic apoptosis in single cells. Mol. Cell 2008, 30:11-25.
147. Sun M.G., Williams J., Munoz-Pinedo C., Perkins G.A., Brown J.M., Ellisman M.H., Green D.R., Frey T.G. Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis. Nat. Cell Biol. 2007, 9:1057-1065.
148. A. Tanaka, R.J. Youle, A chemical inhibitor of DRP1 uncouples mitochondrial fission and apoptosis, Mol. Cell 29 (2008) 409-410.
149. Karbowski M., Lee Y.J., Gaume B., Jeong S.Y., Frank S., Nechushtan A., Santel A., Fuller M., Smith C.L., Youle R.J. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 2002, 159:931-938.
150. T. Kanazawa, M.D. Zappaterra, A. Hasegawa, A.P. Wright, E. Newman-Smith, K.F. Buttle, K. McDonald, C.A. Mannella, d.B. van, The C. elegans Opa1 homologue EAT-3 is essential for resistance to free radicals, PLoS Genet. 4 (2008) e1000022.
151. R. Ichishita, K. Tanaka, Y. Sugiura, T. Sayano, K. Mihara, T. Oka, An RNAi screen for mitochondrial proteins required to maintain the morphology of the organelle in Caenorhabditis elegans, J. Biochem. 143 (2008) 449-454.
152. Breckenridge D.G., Kang B.H., Kokel D., Mitani S., Staehelin L.A., Xue D. Caenorhabditis elegans drp-1 and fis-2 regulate distinct cell-death execution pathways downstream of ced-3 and independent of ced-9. Mol. Cell 2008, 31:586-597.
153. A.M. Labrousse, M.D. Zappaterra, D.A. Rube, d.B. van, C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane, Mol. Cell. 4 (1999) 815-826.
154. R. Sugioka, S. Shimizu, Y. Tsujimoto, Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis, J. Biol. Chem. 279 (2004) 52726-52734.
155. Karbowski M., Norris K.L., Cleland M.M., Jeong S.Y., Youle R.J. Role of Bax and Bak in mitochondrial morphogenesis. Nature 2006, 443:658-662.
156. H. Li, Y. Chen, A.F. Jones, R.H. Sanger, L.P. Collis, R. Flannery, E.C. McNay, T. Yu, R. Schwarzenbacher, B. Bossy, E. Bossy-Wetzel, M.V. Bennett, M. Pypaert, J.A. Hickman, P.J. Smith, J.M. Hardwick, E.A. Jonas, Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons, Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 2169-2174.
157. S.G. Rolland, Y. Lu, C.N. David, B. Conradt, The BCL-2-like protein CED-9 of C. elegans promotes FZO-1/Mfn1, 2- and EAT-3/Opa1-dependent mitochondrial fusion, J. Cell Biol. 186 (2009) 525-540.
158. P. Delivani, C. Adrain, R.C. Taylor, P.J. Duriez, S.J. Martin, Role for CED-9 and Egl-1 as regulators of mitochondrial fission and fusion dynamics, Mol. Cell. 21 (2006) 761-773.
159. F.J. Tan, M. Husain, C.M. Manlandro, M. Koppenol, A.Z. Fire, R.B. Hill, CED-9 and mitochondrial homeostasis in C. elegans muscle, J. Cell. Sci. 121 (2006) 3373-3382.
160. Carmona-Gutierrez D., Eisenberg T., Buttner S., Meisinger C., Kroemer G., Madeo F. Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ. 2010, 17:763-773.
161. Hardwick J.M., Cheng W.C. Mitochondrial programmed cell death pathways in yeast. Dev. Cell 2004, 7:630-632.
162. Okamoto K., Shaw J.M. Mitochondrial Morphology and Dynamics in Yeast and Multicellular Eukaryotes 2005.
163. S. Hoppins, J. Nunnari, The molecular mechanism of mitochondrial fusion, Biochim. Biophys. Acta 1793 (2009) 20-26.
164. Uren A.G., O'Rourke K., Aravind L.A., Pisabarro M.T., Seshagiri S., Koonin E.V., Dixit V.M. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 2000, 6:961-967.
165. Reiter J., Herker E., Madeo F., Schmitt M.J. Viral killer toxins induce caspase-mediated apoptosis in yeast. J. Cell Biol. 2005, 168:353-358.
166. Vachova L., Palkova Z. Physiological regulation of yeast cell death in multicellular colonies is triggered by ammonia. J. Cell Biol. 2005, 169:711-717.
167. Enoksson M., Salvesen G.S. Metacaspases are not caspases-always doubt. Cell Death Differ. 2010, 17:1221.
168. Cheng W.C., Teng X., Park H.K., Tucker C.M., Dunham M.J., Hardwick J.M. Fis1 deficiency selects for compensatory mutations responsible for cell death and growth control defects. Cell Death Differ. 2008, 15:1838-1846.
169. Clark I.E., Dodson M.W., Jiang C., Cao J.H., Huh J.R., Seol J.H., Yoo S.J., Hay B.A., Guo M. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 2006, 441:1162-1166.
170. Yang Y., Gehrke S., Imai Y., Huang Z., Ouyang Y., Wang J.W., Yang L., Beal M.F., Vogel H., Lu B. Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10793-10798.
171. Narendra D.P., Jin S.M., Tanaka A., Suen D.F., Gautier C.A., Shen J., Cookson M.R., Youle R.J. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010, 8:e1000298.
172. Narendra D., Tanaka A., Suen D.F., Youle R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 2008, 183:795-803.
173. Greene J.C., Whitworth A.J., Kuo I., Andrews L.A., Feany M.B., Pallanck L.J. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:4078-4083.
174. Deng H., Dodson M.W., Huang H., Guo M. The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14503-14508.
175. Ziviani E., Tao R.N., Whitworth A.J. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5018-5023.
176. Verstreken P., Ly C.V., Venken K.J., Koh T.W., Zhou Y., Bellen H.J. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 2005, 47:365-378.
177. Kieper N., Holmstrom K.M., Ciceri D., Fiesel F.C., Wolburg H., Ziviani E., Whitworth A.J., Martins L.M., Kahle P.J., Kruger R. Modulation of mitochondrial function and morphology by interaction of Omi/HtrA2 with the mitochondrial fusion factor OPA1. Exp. Cell Res. 2010, 316:1213-1224.
178. Ng C.H., Mok S.Z., Koh C., Ouyang X., Fivaz M.L., Tan E.K., Dawson V.L., Dawson T.M., Yu F., Lim K.L. Parkin protects against LRRK2 G2019S mutant-induced dopaminergic neurodegeneration in Drosophila. J. Neurosci. 2009, 29:11257-11262.
179. Dimmer K.S., Navoni F., Casarin A., Trevisson E., Endele S., Winterpacht A., Salviati L., Scorrano L. LETM1, deleted in Wolf-Hirschhorn syndrome is required for normal mitochondrial morphology and cellular viability. Hum. Mol. Genet. 2008, 17:201-214.
180. McQuibban A.G., Joza N., Megighian A., Scorzeto M., Zanini D., Reipert S., Richter C., Schweyen R.J., Nowikovsky K. A Drosophila mutant of LETM1, a candidate gene for seizures in Wolf-Hirschhorn syndrome. Hum. Mol. Genet. 2010, 19:987-1000.
181. J. Samann, J. Hegermann, E. von Gromoff, S. Eimer, R. Baumeister, E. Schmidt, Caenorhabditits elegans LRK-1 and PINK-1 act antagonistically in stress response and neurite outgrowth, J. Biol. Chem. 284 (2009) 16482-16491.
182. Yao C., El Khoury R., Wang W., Byrd T.A., Pehek E.A., Thacker C., Zhu X., Smith M.A., Wilson-Delfosse A., Chen S.G. LRRK2-mediated neurodegeneration and dysfunction of dopaminergic neurons in a Caenorhabditis elegans model of Parkinson's disease 2010.
183. Perocchi F., Mancera E., Steinmetz L.M. Systematic screens for human disease genes, from yeast to human and back. Mol. Biosyst. 2008, 4:18-29.
184. Schwimmer C., Rak M., Lefebvre-Legendre L., Duvezin-Caubet S., Plane G., di Rago J.P. Yeast models of human mitochondrial diseases: from molecular mechanisms to drug screening. Biotechnol. J. 2006, 1:270-281.
185. Lai K., Klapa M.I. Alternative pathways of galactose assimilation: could inverse metabolic engineering provide an alternative to galactosemic patients?. Metab. Eng. 2004, 6:239-244.
186. Polge C., Thomas M. SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control?. Trends Plant Sci. 2007, 12:20-28.
187. Garbarino J., Sturley S.L. Saturated with fat: new perspectives on lipotoxicity. Curr. Opin. Clin. Nutr. Metab. Care 2009, 12:110-116.
188. Steinkraus K.A., Kaeberlein M., Kennedy B.K. Replicative aging in yeast: the means to the end. Annu. Rev. Cell Dev. Biol. 2008, 24:29-54.
189. Roux A.E., Chartrand P., Ferbeyre G., Rokeach L.A. Fission yeast and other yeasts as emergent models to unravel cellular aging in eukaryotes. J. Gerontol. A Biol. Sci. Med. Sci. 2010, 65:1-8.
190. Walberg M.W. Applicability of yeast genetics to neurologic disease. Arch. Neurol. 2000, 57:1129-1134.
191. Winderickx J., Delay C., De Vos A., Klinger H., Pellens K., Vanhelmont T., Van Leuven F., Zabrocki P. Protein folding diseases and neurodegeneration: lessons learned from yeast. Biochim. Biophys. Acta 2008, 1783:1381-1395.
192. Nitiss J.L., Heitman J. Yeast as a Tool in Cancer Research 2007, SpringerLink (Online service), Springer, Dordrecht.
193. Lindquist S., Krobitsch S., Li L., Sondheimer N. Investigating protein conformation-based inheritance and disease in yeast. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2001, 356:169-176.
194. Tenreiro S., Outeiro T.F. Simple is good: yeast models of neurodegeneration. FEMS Yeast Res. 2010, 10:970-979.
195. Auluck P.K., Caraveo G., Lindquist S. alpha-Synuclein: membrane interactions and toxicity in Parkinson's disease. Annu. Rev. Cell Dev. Biol. 2010, 26:194-208.
196. Su L.J., Auluck P.K., Outeiro T.F., Yeger-Lotem E., Kritzer J.A., Tardiff D.F., Strathearn K.E., Liu F., Cao S., Hamamichi S., Hill K.J., Caldwell K.A., Bell G.W., Fraenkel E., Cooper A.A., Caldwell G.A., McCaffery J.M., Rochet J.C., Lindquist S. Compounds from an unbiased chemical screen reverse both ER-to-Golgi trafficking defects and mitochondrial dysfunction in Parkinson's disease models. Dis. Model. Mech. 2010, 3:194-208.
197. Knight S.A., Kim R., Pain D., Dancis A. The yeast connection to Friedreich ataxia. Am. J. Hum. Genet. 1999, 64:365-371.
198. Pearce D.A., Ferea T., Nosel S.A., Das B., Sherman F. Action of BTN1, the yeast orthologue of the gene mutated in Batten disease. Nat. Genet. 1999, 22:55-58.
199. Phillips S.N., Muzaffar N., Codlin S., Korey C.A., Taschner P.E., de Voer G., Mole S.E., Pearce D.A. Characterizing pathogenic processes in Batten disease: use of small eukaryotic model systems. Biochim. Biophys. Acta 2006, 1762:906-919.
200. Zhang S., Ren J., Li H., Zhang Q., Armstrong J.S., Munn A.L., Yang H. Ncr1p, the yeast ortholog of mammalian Niemann Pick C1 protein, is dispensable for endocytic transport. Traffic 2004, 5:1017-1030.
201. Berger A.C., Hanson P.K., Wylie Nichols J., Corbett A.H. A yeast model system for functional analysis of the Niemann-Pick type C protein 1 homolog, Ncr1p. Traffic 2005, 6:907-917.
202. Moore J.K., Sept D., Cooper J.A. Neurodegeneration mutations in dynactin impair dynein-dependent nuclear migration. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:5147-5152.
203. Pearce D.A. Hereditary spastic paraplegia: mitochondrial metalloproteases of yeast. Hum. Genet. 1999, 104:443-448.
204. Shani N., Valle D. A Saccharomyces cerevisiae homolog of the human adrenoleukodystrophy transporter is a heterodimer of two half ATP-binding cassette transporters. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11901-11906.