Post-translational modification of mitochondria as a novel mode of regulation

Experimental Gerontology

Volumn 56, Issue , 2014, Pages 202-220

  Hofer, Annette ^a   Wenz, Tina ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b German Network for Mitochondrial Disorders (mitoNET)   (Germany)

Author keywords

Acetylation; Apoptosis; Immune response; Mitochondrial metabolism; Mitochondrial posttranslational modifications; Phosphorylation; Succinylation; Ubiquitination

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOCHONDRIAL PROTEIN; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; SIRTUIN 3; SIRTUIN 4; SIRTUIN 5; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID DERIVATIVE;

ACETYLATION; ADENOSINE DIPHOSPHATE RIBOSYLATION; AMINO ACID METABOLISM; APOPTOSIS; AUTOPHAGY; CELLULAR DISTRIBUTION; CELLULAR STRESS RESPONSE; DEACETYLATION; ENZYME ACTIVITY; ENZYME SPECIFICITY; GLUCOSE METABOLISM; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TARGETING; REVIEW; UBIQUITINATION; ANIMAL; ENERGY METABOLISM; METABOLISM; PATHOLOGY; PHOSPHORYLATION;

MAMMALIA;

ACETYLATION; ANIMALS; APOPTOSIS; AUTOPHAGY; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SUCCINATES; UBIQUITINATION;

EID: 84901854646     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.03.006     Document Type: Review

References (182)

1. Abdel-Hafiz H.A., Horwitz K.B. Post-translational modifications of the progesterone receptors. J. Steroid Biochem. Mol. Biol. 2014, 140:80-89.
2. Acin-Perez R., Salazar E., Brosel S., Yang H., Schon E.A., Manfredi G. Modulation of mitochondrial protein phosphorylation by soluble adenylyl cyclase ameliorates cytochrome oxidase defects. EMBO Mol. Med. 2009, 1:392-406.
3. Acin-Perez R., Salazar E., Kamenetsky M., Buck J., Levin L.R., Manfredi G. Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab. 2009, 9:265-276.
4. Acin-Perez R., Gatti D.L., Bai Y., Manfredi G. Protein phosphorylation and prevention of cytochrome oxidase inhibition by ATP: coupled mechanisms of energy metabolism regulation. Cell Metab. 2011, 13:712-719.
5. Acin-Perez R., Russwurm M., Gunnewig K., Gertz M., Zoidl G., Ramos L., Buck J., Levin L.R., Rassow J., Manfredi G., Steegborn C. A phosphodiesterase 2A isoform localized to mitochondria regulates respiration. J. Biol. Chem. 2011, 286:30423-30432.
6. Affaitati A., Cardone L., de Cristofaro T., Carlucci A., Ginsberg M.D., Varrone S., Gottesman M.E., Avvedimento E.V., Feliciello A. Essential role of A-kinase anchor protein 121 for cAMP signaling to mitochondria. J. Biol. Chem. 2003, 278:4286-4294.
7. Ahn B.H., Kim H.S., Song S., Lee I.H., Liu J., Vassilopoulos A., Deng C.X., Finkel T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14447-14452.
8. Anderson K.A., Hirschey M.D. Mitochondrial protein acetylation regulates metabolism. Essays Biochem. 2012, 52:23-35.
9. Arachiche A., Augereau O., Decossas M., Pertuiset C., Gontier E., Letellier T., Dachary-Prigent J. Localization of PTP-1B, SHP-2, and Src exclusively in rat brain mitochondria and functional consequences. J. Biol. Chem. 2008, 283:24406-24411.
10. Arena G., Gelmetti V., Torosantucci L., Vignone D., Lamorte G., De Rosa P., Cilia E., Jonas E.A., Valente E.M. PINK1 protects against cell death induced by mitochondrial depolarization, by phosphorylating Bcl-xL and impairing its pro-apoptotic cleavage. Cell Death Differ. 2013, 20:920-930.
11. Augereau O., Claverol S., Boudes N., Basurko M.J., Bonneu M., Rossignol R., Mazat J.P., Letellier T., Dachary-Prigent J. Identification of tyrosine-phosphorylated proteins of the mitochondrial oxidative phosphorylation machinery. Cell. Mol. Life Sci. 2005, 62:1478-1488.
12. Azzu V., Brand M.D. Degradation of an intramitochondrial protein by the cytosolic proteasome. J. Cell Sci. 2010, 123:578-585.
13. Azzu V., Mookerjee S.A., Brand M.D. Rapid turnover of mitochondrial uncoupling protein 3. Biochem. J. 2010, 426:13-17.
14. Bae S., Kim S.Y., Jung J.H., Yoon Y., Cha H.J., Lee H., Kim K., Kim J., An I.S., Um H.D., Park I.C., Lee S.J., Nam S.Y., Jin Y.W., Lee J.H., An S. Akt is negatively regulated by the MULAN E3 ligase. Cell Res. 2012, 22:873-885.
15. Bao J., Scott I., Lu Z., Pang L., Dimond C.C., Gius D., Sack M.N. SIRT3 is regulated by nutrient excess and modulates hepatic susceptibility to lipotoxicity. Free Radic. Biol. Med. 2010, 49:1230-1237.
16. Bharathi S.S., Zhang Y., Mohsen A.W., Uppala R., Balasubramani M., Schreiber E., Uechi G., Beck M.E., Rardin M.J., Vockley J., Verdin E., Gibson B.W., Hirschey M.D., Goetzman E.S. SIRT3 regulates long-chain Acyl-CoA dehydrogenase by deacetylating conserved lysines near the active site. J. Biol. Chem. 2013, 288(47):33837-33847.
17. Braschi E., Zunino R., McBride H.M. MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep. 2009, 10:748-754.
18. Cardone L., de Cristofaro T., Affaitati A., Garbi C., Ginsberg M.D., Saviano M., Varrone S., Rubin C.S., Gottesman M.E., Avvedimento E.V., Feliciello A. A-kinase anchor protein 84/121 are targeted to mitochondria and mitotic spindles by overlapping amino-terminal motifs. J. Mol. Biol. 2002, 320:663-675.
19. Cardone L., Carlucci A., Affaitati A., Livigni A., DeCristofaro T., Garbi C., Varrone S., Ullrich A., Gottesman M.E., Avvedimento E.V., Feliciello A. Mitochondrial AKAP121 binds and targets protein tyrosine phosphatase D1, a novel positive regulator of src signaling. Mol. Cell. Biol. 2004, 24:4613-4626.
20. Cesaro L., Salvi M. Mitochondrial tyrosine phosphoproteome: new insights from an up-to-date analysis. Biofactors 2010, 36:437-450.
21. Chan N.C., Salazar A.M., Pham A.H., Sweredoski M.J., Kolawa N.J., Graham R.L., Hess S., Chan D.C. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum. Mol. Genet. 2011, 20:1726-1737.
22. Chang C.R., Blackstone C. Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 2007, 282:21583-21587.
23. Chen D., Kon N., Li M., Zhang W., Qin J., Gu W. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 2005, 121:1071-1083.
24. Chen Y., Zhang J., Lin Y., Lei Q., Guan K.L., Zhao S., Xiong Y. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep. 2011, 12:534-541.
25. Cheng Y., Ren X., Gowda A.S., Shan Y., Zhang L., Yuan Y.S., Patel R., Wu H., Huber-Keener K., Yang J.W., Liu D., Spratt T.E., Yang J.M. Interaction of Sirt3 with OGG1 contributes to repair of mitochondrial DNA and protects from apoptotic cell death under oxidative stress. Cell Death Dis. 2013, 4:e731.
26. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
27. Cimen H., Han M.J., Yang Y., Tong Q., Koc H., Koc E.C. Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry 2010, 49:304-311.
28. Clarke K.J., Adams A.E., Manzke L.H., Pearson T.W., Borchers C.H., Porter R.K. A role for ubiquitinylation and the cytosolic proteasome in turnover of mitochondrial uncoupling protein 1 (UCP1). Biochim. Biophys. Acta 2012, 1817:1759-1767.
29. Consortium T.U. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2014, 42:D191-D198.
30. Cribbs J.T., Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 2007, 8:939-944.
31. De Rasmo D., Signorile A., Roca E., Papa S. cAMP response element-binding protein (CREB) is imported into mitochondria and promotes protein synthesis. FEBS J. 2009, 276:4325-4333.
32. Demory M.L., Boerner J.L., Davidson R., Faust W., Miyake T., Lee I., Huttemann M., Douglas R., Haddad G., Parsons S.J. Epidermal growth factor receptor translocation to the mitochondria: regulation and effect. J. Biol. Chem. 2009, 284:36592-36604.
33. 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.
34. Dewan S.K., Zheng S.B., Xia S.J., Bill K. Senescent remodeling of the immune system and its contribution to the predisposition of the elderly to infections. Chin. Med. J. (Engl.) 2012, 125:3325-3331.
35. Ding Y., Liu Z., Desai S., Zhao Y., Liu H., Pannell L.K., Yi H., Wright E.R., Owen L.B., Dean-Colomb W., Fodstad O., Lu J., LeDoux S.P., Wilson G.L., Tan M. Receptor tyrosine kinase ErbB2 translocates into mitochondria and regulates cellular metabolism. Nat. Commun. 2012, 3:1271.
36. Du J., Zhou Y., Su X., Yu J.J., Khan S., Jiang H., Kim J., Woo J., Kim J.H., Choi B.H., He B., Chen W., Zhang S., Cerione R.A., Auwerx J., Hao Q., Lin H. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science 2011, 334:806-809.
37. El Khouri E., Le Pavec G., Toledano M.B., Delaunay-Moisan A. RNF185 is a novel E3 ligase of Endoplasmic Reticulum Associated Degradation (ERAD) that targets Cystic Fibrosis Transmembrane conductance Regulator (CFTR). J. Biol. Chem. 2013, 288(43):31177-31191.
38. Finley L.W., Carracedo A., Lee J., Souza A., Egia A., Zhang J., Teruya-Feldstein J., Moreira P.I., Cardoso S.M., Clish C.B., Pandolfi P.P., Haigis M.C. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell 2011, 19:416-428.
39. Finley L.W., Haas W., Desquiret-Dumas V., Wallace D.C., Procaccio V., Gygi S.P., Haigis M.C. Succinate dehydrogenase is a direct target of sirtuin 3 deacetylase activity. PLoS One 2011, 6:e23295.
40. Frye R.A. Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem. Biophys. Res. Commun. 2000, 273:793-798.
41. Galluzzi L., Kepp O., Trojel-Hansen C., Kroemer G. Mitochondrial control of cellular life, stress, and death. Circ. Res. 2012, 111:1198-1207.
42. Gegg M.E., Cooper J.M., Chau K.Y., Rojo M., Schapira A.H., Taanman J.W. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum. Mol. Genet. 2010, 19:4861-4870.
43. Geisler S., Holmstrom K.M., Skujat D., Fiesel F.C., Rothfuss O.C., Kahle P.J., Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 2010, 12:119-131.
44. Glauser L., Sonnay S., Stafa K., Moore D.J. Parkin promotes the ubiquitination and degradation of the mitochondrial fusion factor mitofusin 1. J. Neurochem. 2011, 118:636-645.
45. Hafner A.V., Dai J., Gomes A.P., Xiao C.Y., Palmeira C.M., Rosenzweig A., Sinclair D.A. Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging (Albany NY) 2010, 2:914-923.
46. Haigis M.C., Mostoslavsky R., Haigis K.M., Fahie K., Christodoulou D.C., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Karow M., Blander G., Wolberger C., Prolla T.A., Weindruch R., Alt F.W., Guarente L. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell 2006, 126:941-954.
47. Hallows W.C., Lee S., Denu J.M. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10230-10235.
48. Hallows W.C., Yu W., Smith B.C., Devries M.K., Ellinger J.J., Someya S., Shortreed M.R., Prolla T., Markley J.L., Smith L.M., Zhao S., Guan K.L., Denu J.M. Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction. Mol. Cell 2011, 41:139-149.
49. Harada H., Becknell B., Wilm M., Mann M., Huang L.J., Taylor S.S., Scott J.D., Korsmeyer S.J. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell 1999, 3:413-422.
50. He W., Newman J.C., Wang M.Z., Ho L., Verdin E. Mitochondrial sirtuins: regulators of protein acylation and metabolism. Trends Endocrinol. Metab. 2012, 23:467-476.
51. Hebert Chatelain E., Dupuy J.W., Letellier T., Dachary-Prigent J. Functional impact of PTP1B-mediated Src regulation on oxidative phosphorylation in rat brain mitochondria. Cell. Mol. Life Sci. 2011, 68:2603-2613.
52. Hebert-Chatelain E. Src kinases are important regulators of mitochondrial functions. Int. J. Biochem. Cell Biol. 2013, 45:90-98.
53. Hebert-Chatelain E., Jose C., Gutierrez Cortes N., Dupuy J.W., Rocher C., Dachary-Prigent J., Letellier T. Preservation of NADH ubiquinone-oxidoreductase activity by Src kinase-mediated phosphorylation of NDUFB10. Biochim. Biophys. Acta 2012, 1817:718-725.
54. Herrero-Yraola A., Bakhit S.M., Franke P., Weise C., Schweiger M., Jorcke D., Ziegler M. Regulation of glutamate dehydrogenase by reversible ADP-ribosylation in mitochondria. EMBO J. 2001, 20:2404-2412.
55. Hirschey M.D., Shimazu T., Goetzman E., Jing E., Schwer B., Lombard D.B., Grueter C.A., Harris C., Biddinger S., Ilkayeva O.R., Stevens R.D., Li Y., Saha A.K., Ruderman N.B., Bain J.R., Newgard C.B., Farese R.V., Alt F.W., Kahn C.R., Verdin E. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 2010, 464:121-125.
56. Hirschey M.D., Shimazu T., Jing E., Grueter C.A., Collins A.M., Aouizerat B., Stancakova A., Goetzman E., Lam M.M., Schwer B., Stevens R.D., Muehlbauer M.J., Kakar S., Bass N.M., Kuusisto J., Laakso M., Alt F.W., Newgard C.B., Farese R.V., Kahn C.R., Verdin E. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol. Cell 2011, 44:177-190.
57. Horbinski C., Chu C.T. Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic. Biol. Med. 2005, 38:2-11.
58. Ikeda H., Kerppola T.K. Lysosomal localization of ubiquitinated Jun requires multiple determinants in a lysine-27-linked polyubiquitin conjugate. Mol. Biol. Cell 2008, 19:4588-4601.
59. Ito Y., Pandey P., Mishra N., Kumar S., Narula N., Kharbanda S., Saxena S., Kufe D. Targeting of the c-Abl tyrosine kinase to mitochondria in endoplasmic reticulum stress-induced apoptosis. Mol. Cell. Biol. 2001, 21:6233-6242.
60. Itoh S., Lemay S., Osawa M., Che W., Duan Y., Tompkins A., Brookes P.S., Sheu S.S., Abe J. Mitochondrial Dok-4 recruits Src kinase and regulates NF-κB activation in endothelial cells. J. Biol. Chem. 2005, 280:26383-26396.
61. Itoh K., Nakamura K., Iijima M., Sesaki H. Mitochondrial dynamics in neurodegeneration. Trends Cell Biol. 2013, 23:64-71.
62. Jenkins K., Khoo J.J., Sadler A., Piganis R., Wang D., Borg N.A., Hjerrild K., Gould J., Thomas B.J., Nagley P., Hertzog P.J., Mansell A. Mitochondrially localised MUL1 is a novel modulator of antiviral signaling. Immunol. Cell Biol. 2013, 91:321-330.
63. Jin S.M., Lazarou M., Wang C., Kane L.A., Narendra D.P., Youle R.J. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 2010, 191:933-942.
64. Jing E., Emanuelli B., Hirschey M.D., Boucher J., Lee K.Y., Lombard D., Verdin E.M., Kahn C.R. Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14608-14613.
65. Jing E., O'Neill B.T., Rardin M.J., Kleinridders A., Ilkeyeva O.R., Ussar S., Bain J.R., Lee K.Y., Verdin E.M., Newgard C.B., Gibson B.W., Kahn C.R. Sirt3 regulates metabolic flexibility of skeletal muscle through reversible enzymatic deacetylation. Diabetes 2013, 62(10):3404-3417.
66. Jorcke D., Ziegler M., Herrero-Yraola A., Schweiger M. Enzymic, cysteine-specific ADP-ribosylation in bovine liver mitochondria. Biochem. J. 1998, 332(Pt 1):189-193.
67. Karbowski M., Youle R.J. Regulating mitochondrial outer membrane proteins by ubiquitination and proteasomal degradation. Curr. Opin. Cell Biol. 2011, 23:476-482.
68. Karbowski M., Neutzner A., Youle R.J. The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 2007, 178:71-84.
69. Karch K.R., Denizio J.E., Black B.E., Garcia B.A. Identification and interrogation of combinatorial histone modifications. Front. Genet. 2013, 4:264.
70. Kim S.C., Sprung R., Chen Y., Xu Y., Ball H., Pei J., Cheng T., Kho Y., Xiao H., Xiao L., Grishin N.V., White M., Yang X.J., Zhao Y. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 2006, 23:607-618.
71. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998, 392:605-608.
72. Koc E.C., Koc H. Regulation of mammalian mitochondrial translation by post-translational modifications. Biochim. Biophys. Acta 2012, 1819:1055-1066.
73. Kon N., Zhong J., Qiang L., Accili D., Gu W. Inactivation of arf-bp1 induces p53 activation and diabetic phenotypes in mice. J. Biol. Chem. 2012, 287:5102-5111.
74. Koopman W.J., Distelmaier F., Smeitink J.A., Willems P.H. OXPHOS mutations and neurodegeneration. EMBO J. 2013, 32:9-29.
75. Koshiba T. Mitochondrial-mediated antiviral immunity. Biochim. Biophys. Acta 2013, 1833:225-232.
76. Kumar S., Bharti A., Mishra N.C., Raina D., Kharbanda S., Saxena S., Kufe D. Targeting of the c-Abl tyrosine kinase to mitochondria in the necrotic cell death response to oxidative stress. J. Biol. Chem. 2001, 276:17281-17285.
77. Lagouge M., Larsson N.G. The role of mitochondrial DNA mutations and free radicals in disease and ageing. J. Intern. Med. 2013, 273:529-543.
78. Lasfer M., Davenne L., Vadrot N., Alexia C., Sadji-Ouatas Z., Bringuier A.F., Feldmann G., Pessayre D., Reyl-Desmars F. Protein kinase PKC delta and c-Abl are required for mitochondrial apoptosis induction by genotoxic stress in the absence of p53, p73 and Fas receptor. FEBS Lett. 2006, 580:2547-2552.
79. Laurent G., German N.J., Saha A.K., de Boer V.C., Davies M., Koves T.R., Dephoure N., Fischer F., Boanca G., Vaitheesvaran B., Lovitch S.B., Sharpe A.H., Kurland I.J., Steegborn C., Gygi S.P., Muoio D.M., Ruderman N.B., Haigis M.C. SIRT4 coordinates the balance between lipid synthesis and catabolism by repressing malonyl CoA decarboxylase. Mol. Cell 2013, 50:686-698.
80. Leboucher G.P., Tsai Y.C., Yang M., Shaw K.C., Zhou M., Veenstra T.D., Glickman M.H., Weissman A.M. Stress-induced phosphorylation and proteasomal degradation of mitofusin 2 facilitates mitochondrial fragmentation and apoptosis. Mol. Cell 2012, 47:547-557.
81. Lee I., Salomon A.R., Ficarro S., Mathes I., Lottspeich F., Grossman L.I., Huttemann M. cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J. Biol. Chem. 2005, 280:6094-6100.
82. Lee J., Kim C.H., Simon D.K., Aminova L.R., Andreyev A.Y., Kushnareva Y.E., Murphy A.N., Lonze B.E., Kim K.S., Ginty D.D., Ferrante R.J., Ryu H., Ratan R.R. Mitochondrial cyclic AMP response element-binding protein (CREB) mediates mitochondrial gene expression and neuronal survival. J. Biol. Chem. 2005, 280:40398-40401.
83. Lee J., Xu Y., Chen Y., Sprung R., Kim S.C., Xie S., Zhao Y. Mitochondrial phosphoproteome revealed by an improved IMAC method and MS/MS/MS. Mol. Cell. Proteomics 2007, 6:669-676.
84. Lewandrowski U., Sickmann A., Cesaro L., Brunati A.M., Toninello A., Salvi M. Identification of new tyrosine phosphorylated proteins in rat brain mitochondria. FEBS Lett. 2008, 582:1104-1110.
85. Li W., Bengtson M.H., Ulbrich A., Matsuda A., Reddy V.A., Orth A., Chanda S.K., Batalov S., Joazeiro C.A. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PLoS One 2008, 3:e1487.
86. Liang Q., Benavides G.A., Vassilopoulos A., Gius D., Darley-Usmar V., Zhang J. Bioenergetic and autophagic control by Sirt3 in response to nutrient deprivation in mouse embryonic fibroblasts. Biochem. J. 2013, 454:249-257.
87. Liesa M., Shirihai O.S. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 2013, 17:491-506.
88. Lin Z.F., Xu H.B., Wang J.Y., Lin Q., Ruan Z., Liu F.B., Jin W., Huang H.H., Chen X. SIRT5 desuccinylates and activates SOD1 to eliminate ROS. Biochem. Biophys. Res. Commun. 2013, 441:191-195.
89. Ling Q., Jarvis P. Dynamic regulation of endosymbiotic organelles by ubiquitination. Trends Cell Biol. 2013, 23:399-408.
90. Liu S., Chen J., Cai X., Wu J., Chen X., Wu Y.T., Sun L., Chen Z.J. MAVS recruits multiple ubiquitin E3 ligases to activate antiviral signaling cascades. Elife 2013, 2:e00785.
91. Livigni A., Scorziello A., Agnese S., Adornetto A., Carlucci A., Garbi C., Castaldo I., Annunziato L., Avvedimento E.V., Feliciello A. Mitochondrial AKAP121 links cAMP and src signaling to oxidative metabolism. Mol. Biol. Cell 2006, 17:263-271.
92. Lluis J.M., Buricchi F., Chiarugi P., Morales A., Fernandez-Checa J.C. Dual role of mitochondrial reactive oxygen species in hypoxia signaling: activation of nuclear factor-κB via c-SRC and oxidant-dependent cell death. Cancer Res. 2007, 67:7368-7377.
93. Lokireddy S., Wijesoma I.W., Teng S., Bonala S., Gluckman P.D., McFarlane C., Sharma M., Kambadur R. The ubiquitin ligase Mul1 induces mitophagy in skeletal muscle in response to muscle-wasting stimuli. Cell Metab. 2012, 16:613-624.
94. Lombard D.B., Alt F.W., Cheng H.L., Bunkenborg J., Streeper R.S., Mostoslavsky R., Kim J., Yancopoulos G., Valenzuela D., Murphy A., Yang Y., Chen Y., Hirschey M.D., Bronson R.T., Haigis M., Guarente L.P., Farese R.V., Weissman S., Verdin E., Schwer B. Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol. Cell. Biol. 2007, 27:8807-8814.
95. Lu B., Lee J., Nie X., Li M., Morozov Y.I., Venkatesh S., Bogenhagen D.F., Temiakov D., Suzuki C.K. Phosphorylation of human TFAM in mitochondria impairs DNA binding and promotes degradation by the AAA+Lon protease. Mol. Cell 2013, 49:121-132.
96. Machida K., Ohta Y., Osada H. Suppression of apoptosis by cyclophilin D via stabilization of hexokinase II mitochondrial binding in cancer cells. J. Biol. Chem. 2006, 281:14314-14320.
97. Margineantu D.H., Emerson C.B., Diaz D., Hockenbery D.M. Hsp90 inhibition decreases mitochondrial protein turnover. PLoS One 2007, 2:e1066.
98. Mazat J.P., Ransac S., Heiske M., Devin A., Rigoulet M. Mitochondrial energetic metabolism-some general principles. IUBMB Life 2013, 65:171-179.
99. Meissner C., Lorenz H., Weihofen A., Selkoe D.J., Lemberg M.K. The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J. Neurochem. 2011, 117:856-867.
100. Miyazaki T., Neff L., Tanaka S., Horne W.C., Baron R. Regulation of cytochrome c oxidase activity by c-Src in osteoclasts. J. Cell Biol. 2003, 160:709-718.
101. Moldoveanu T., Follis A.V., Kriwacki R.W., Green D.R. Many players in BCL-2 family affairs. Trends Biochem. Sci. 2014, 39(3):101-111.
102. Myers C.E., Mirza N.N., Lustgarten J. Immunity, cancer and aging: lessons from mouse models. Aging Dis. 2011, 2:512-523.
103. Nakagawa T., Lomb D.J., Haigis M.C., Guarente L. SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell 2009, 137:560-570.
104. Nakamura N., Hirose S. Regulation of mitochondrial morphology by USP30, a deubiquitinating enzyme present in the mitochondrial outer membrane. Mol. Biol. Cell 2008, 19:1903-1911.
105. Nakamura N., Kimura Y., Tokuda M., Honda S., Hirose S. MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 2006, 7:1019-1022.
106. Nakamura Y., Ogura M., Ogura K., Tanaka D., Inagaki N. SIRT5 deacetylates and activates urate oxidase in liver mitochondria of mice. FEBS Lett. 2012, 586:4076-4081.
107. Narendra D.P., Youle R.J. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid. Redox Signal. 2011, 14:1929-1938.
108. 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.
109. Neuspiel M., Schauss A.C., Braschi E., Zunino R., Rippstein P., Rachubinski R.A., Andrade-Navarro M.A., McBride H.M. Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 2008, 18:102-108.
110. Nunnari J., Suomalainen A. Mitochondria: in sickness and in health. Cell 2012, 148:1145-1159.
111. Ogura M., Nakamura Y., Tanaka D., Zhuang X., Fujita Y., Obara A., Hamasaki A., Hosokawa M., Inagaki N. Overexpression of SIRT5 confirms its involvement in deacetylation and activation of carbamoyl phosphate synthetase 1. Biochem. Biophys. Res. Commun. 2010, 393:73-78.
112. Ogura M., Yamaki J., Homma M.K., Homma Y. Mitochondrial c-Src regulates cell survival through phosphorylation of respiratory chain components. Biochem. J. 2012, 447:281-289.
113. Pagliarini D.J., Dixon J.E. Mitochondrial modulation: reversible phosphorylation takes center stage?. Trends Biochem. Sci. 2006, 31:26-34.
114. Pagliarini D.J., Wiley S.E., Kimple M.E., Dixon J.R., Kelly P., Worby C.A., Casey P.J., Dixon J.E. Involvement of a mitochondrial phosphatase in the regulation of ATP production and insulin secretion in pancreatic beta cells. Mol. Cell 2005, 19:197-207.
115. Papa S., Sardanelli A.M., Cocco T., Speranza F., Scacco S.C., Technikova-Dobrova Z. The nuclear-encoded 18kDa (IP) AQDQ subunit of bovine heart complex I is phosphorylated by the mitochondrial cAMP-dependent protein kinase. FEBS Lett. 1996, 379:299-301.
116. Papa S., Scacco S., Sardanelli A.M., Vergari R., Papa F., Budde S., van den Heuvel L., Smeitink J. Mutation in the NDUFS4 gene of complex I abolishes cAMP-dependent activation of the complex in a child with fatal neurological syndrome. FEBS Lett. 2001, 489:259-262.
117. Park Y.Y., Lee S., Karbowski M., Neutzner A., Youle R.J., Cho H. Loss of MARCH5 mitochondrial E3 ubiquitin ligase induces cellular senescence through dynamin-related protein 1 and mitofusin 1. J. Cell Sci. 2010, 123:619-626.
118. Park J., Chen Y., Tishkoff D.X., Peng C., Tan M., Dai L., Xie Z., Zhang Y., Zwaans B.M., Skinner M.E., Lombard D.B., Zhao Y. SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways. Mol. Cell 2013, 50:919-930.
119. Pedersen P.L., Mathupala S., Rempel A., Geschwind J.F., Ko Y.H. Mitochondrial bound type II hexokinase: a key player in the growth and survival of many cancers and an ideal prospect for therapeutic intervention. Biochim. Biophys. Acta 2002, 1555:14-20.
120. Peng C., Lu Z., Xie Z., Cheng Z., Chen Y., Tan M., Luo H., Zhang Y., He W., Yang K., Zwaans B.M., Tishkoff D., Ho L., Lombard D., He T.C., Dai J., Verdin E., Ye Y., Zhao Y. The first identification of lysine malonylation substrates and its regulatory enzyme. Mol. Cell. Proteomics 2011, 10. (M111 012658).
121. Penuela S., Simek J., Thompson R.J. Regulation of pannexin channels by post-translational modifications. FEBS Lett 2014, (pii: S0014-5793(14)00057-X). 10.1016/j.febslet.2014.01.028.
122. Poole A.C., Thomas R.E., Yu S., Vincow E.S., Pallanck L. The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINK1/parkin pathway. PLoS One 2010, 5:e10054.
123. Qi X., Mochly-Rosen D. The PKCdelta-Abl complex communicates ER stress to the mitochondria - an essential step in subsequent apoptosis. J. Cell Sci. 2008, 121:804-813.
124. Qi C.F., Kim Y.S., Xiang S., Abdullaev Z., Torrey T.A., Janz S., Kovalchuk A.L., Sun J., Chen D., Cho W.C., Gu W., Morse H.C. Characterization of ARF-BP1/HUWE1 interactions with CTCF, MYC, ARF and p53 in MYC-driven B cell neoplasms. Int. J. Mol. Sci. 2012, 13:6204-6219.
125. Qiu X., Brown K., Hirschey M.D., Verdin E., Chen D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 2010, 12:662-667.
126. Rardin M.J., He W., Nishida Y., Newman J.C., Carrico C., Danielson S.R., Guo A., Gut P., Sahu A.K., Li B., Uppala R., Fitch M., Riiff T., Zhu L., Zhou J., Mulhern D., Stevens R.D., Ilkayeva O.R., Newgard C.B., Jacobson M.P., Hellerstein M., Goetzman E.S., Gibson B.W., Verdin E. SIRT5 regulates the mitochondrial lysine succinylome and metabolic networks. Cell Metab. 2013, 18:920-933.
127. Rardin M.J., Newman J.C., Held J.M., Cusack M.P., Sorensen D.J., Li B., Schilling B., Mooney S.D., Kahn C.R., Verdin E., Gibson B.W. Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of SIRT3 in metabolic pathways. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6601-6606.
128. Ryu H., Lee J., Impey S., Ratan R.R., Ferrante R.J. Antioxidants modulate mitochondrial PKA and increase CREB binding to D-loop DNA of the mitochondrial genome in neurons. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13915-13920.
129. Salminen A., Ojala J., Kaarniranta K., Kauppinen A. Mitochondrial dysfunction and oxidative stress activate inflammasomes: impact on the aging process and age-related diseases. Cell. Mol. Life Sci. 2012, 69:2999-3013.
130. Salvi M., Brunati A.M., Bordin L., La Rocca N., Clari G., Toninello A. Characterization and location of Src-dependent tyrosine phosphorylation in rat brain mitochondria. Biochim. Biophys. Acta 2002, 1589:181-195.
131. Salvi M., Brunati A.M., Toninello A. Tyrosine phosphorylation in mitochondria: a new frontier in mitochondrial signaling. Free Radic. Biol. Med. 2005, 38:1267-1277.
132. Salvi M., Morrice N.A., Brunati A.M., Toninello A. Identification of the flavoprotein of succinate dehydrogenase and aconitase as in vitro mitochondrial substrates of Fgr tyrosine kinase. FEBS Lett. 2007, 581:5579-5585.
133. Samraj A.K., Stroh C., Fischer U., Schulze-Osthoff K. The tyrosine kinase Lck is a positive regulator of the mitochondrial apoptosis pathway by controlling Bak expression. Oncogene 2006, 25:186-197.
134. Sardanelli A.M., Technikova-Dobrova Z., et al. Characterization of proteins phosphorylated by the cAMP-dependent protein kinase of bovine heart mitochondria. FEBS Lett 1995, 377(3):470-474.
135. Sardanelli A.M., Technikova-Dobrova Z., et al. Topology of the mitochondrial cAMP-dependent protein kinase and its substrates. FEBS Lett 1996, 396(2-3):276-278.
136. Sarraf S.A., Raman M., Guarani-Pereira V., Sowa M.E., Huttlin E.L., Gygi S.P., Harper J.W. Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 2013, 496:372-376.
137. Sato H., Sato M., Kanai H., Uchiyama T., Iso T., Ohyama Y., Sakamoto H., Tamura J., Nagai R., Kurabayashi M. Mitochondrial reactive oxygen species and c-Src play a critical role in hypoxic response in vascular smooth muscle cells. Cardiovasc. Res. 2005, 67:714-722.
138. Scacco S., Vergari R., Scarpulla R.C., Technikova-Dobrova Z., Sardanelli A., Lambo R., Lorusso V., Papa S. cAMP-dependent phosphorylation of the nuclear encoded 18-kDa (IP) subunit of respiratory complex I and activation of the complex in serum-starved mouse fibroblast cultures. J. Biol. Chem. 2000, 275:17578-17582.
139. Schlicker C., Gertz M., Papatheodorou P., Kachholz B., Becker C.F., Steegborn C. Substrates and regulation mechanisms for the human mitochondrial sirtuins Sirt3 and Sirt5. J. Mol. Biol. 2008, 382:790-801.
140. Schwer B., Bunkenborg J., Verdin R.O., Andersen J.S., Verdin E. Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10224-10229.
141. Schwickart M., Huang X., Lill J.R., Liu J., Ferrando R., French D.M., Maecker H., O'Rourke K., Bazan F., Eastham-Anderson J., Yue P., Dornan D., Huang D.C., Dixit V.M. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 2010, 463:103-107.
142. Scott I., Webster B.R., Li J.H., Sack M.N. Identification of a molecular component of the mitochondrial acetyltransferase programme: a novel role for GCN5L1. Biochem. J. 2012, 443:655-661.
143. Shi H.X., Liu X., Wang Q., Tang P.P., Liu X.Y., Shan Y.F., Wang C. Mitochondrial ubiquitin ligase MARCH5 promotes TLR7 signaling by attenuating TANK action. PLoS Pathog. 2011, 7:e1002057.
144. Shimazu T., Hirschey M.D., Hua L., Dittenhafer-Reed K.E., Schwer B., Lombard D.B., Li Y., Bunkenborg J., Alt F.W., Denu J.M., Jacobson M.P., Verdin E. SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab. 2010, 12:654-661.
145. Shulga N., Wilson-Smith R., Pastorino J.G. Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria. J. Cell Sci. 2010, 123:894-902.
146. Someya S., Yu W., Hallows W.C., Xu J., Vann J.M., Leeuwenburgh C., Tanokura M., Denu J.M., Prolla T.A. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 2010, 143:802-812.
147. Sugiura A., Yonashiro R., Fukuda T., Matsushita N., Nagashima S., Inatome R., Yanagi S. A mitochondrial ubiquitin ligase MITOL controls cell toxicity of polyglutamine-expanded protein. Mitochondrion 2011, 11:139-146.
148. Sugiura A., Nagashima S., Tokuyama T., Amo T., Matsuki Y., Ishido S., Kudo Y., McBride H.M., Fukuda T., Matsushita N., Inatome R., Yanagi S. MITOL regulates endoplasmic reticulum-mitochondria contacts via Mitofusin2. Mol. Cell 2013, 51:20-34.
149. Sun Y., Vashisht A.A., Tchieu J., Wohlschlegel J.A., Dreier L. Voltage-dependent anion channels (VDACs) recruit Parkin to defective mitochondria to promote mitochondrial autophagy. J. Biol. Chem. 2012, 287:40652-40660.
150. Tan J.M., Wong E.S., Kirkpatrick D.S., Pletnikova O., Ko H.S., Tay S.P., Ho M.W., Troncoso J., Gygi S.P., Lee M.K., Dawson V.L., Dawson T.M., Lim K.L. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum. Mol. Genet. 2008, 17:431-439.
151. Tanaka A., Cleland M.M., Xu S., Narendra D.P., Suen D.F., Karbowski M., Youle R.J. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 2010, 191:1367-1380.
152. Tang F., Wang B., Li N., Wu Y., Jia J., Suo T., Chen Q., Liu Y.J., Tang J. RNF185, a novel mitochondrial ubiquitin E3 ligase, regulates autophagy through interaction with BNIP1. PLoS One 2011, 6:e24367.
153. Tao R., Coleman M.C., Pennington J.D., Ozden O., Park S.H., Jiang H., Kim H.S., Flynn C.R., Hill S., Hayes McDonald W., Olivier A.K., Spitz D.R., Gius D. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol. Cell 2010, 40:893-904.
154. Teague W.M., Pettit F.H., Yeaman S.J., Reed L.J. Function of phosphorylation sites on pyruvate dehydrogenase. Biochem. Biophys. Res. Commun. 1979, 87:244-252.
155. Technikova-Dobrova Z., Sardanelli A.M., et al. cAMP-dependent protein phosphorylation in mitochondria of bovine heart. FEBS Lett 1994, 350(2-3):187-191.
156. Tibaldi E., Brunati A.M., Massimino M.L., Stringaro A., Colone M., Agostinelli E., Arancia G., Toninello A. Src-Tyrosine kinases are major agents in mitochondrial tyrosine phosphorylation. J. Cell. Biochem. 2008, 104:840-849.
157. Tibaldi E., Venerando A., Zonta F., Bidoia C., Magrin E., Marin O., Toninello A., Bordin L., Martini V., Pagano M.A., Brunati A.M. Interaction between the SH3 domain of Src family kinases and the proline-rich motif of HTLV-1 p13: a novel mechanism underlying delivery of Src family kinases to mitochondria. Biochem. J. 2011, 439:505-516.
158. Valente E.M., Abou-Sleiman P.M., Caputo V., Muqit M.M., Harvey K., Gispert S., Ali Z., Del Turco D., Bentivoglio A.R., Healy D.G., Albanese A., Nussbaum R., Gonzalez-Maldonado R., Deller T., Salvi S., Cortelli P., Gilks W.P., Latchman D.S., Harvey R.J., Dallapiccola B., Auburger G., Wood N.W. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004, 304:1158-1160.
159. van den Heuvel L., Ruitenbeek W., Smeets R., Gelman-Kohan Z., Elpeleg O., Loeffen J., Trijbels F., Mariman E., de Bruijn D., Smeitink J. Demonstration of a new pathogenic mutation in human complex I deficiency: a 5-bp duplication in the nuclear gene encoding the 18-kD (AQDQ) subunit. Am. J. Hum. Genet. 1998, 62:262-268.
160. Vianello A., Casolo V., Petrussa E., Peresson C., Patui S., Bertolini A., Passamonti S., Braidot E., Zancani M. The mitochondrial permeability transition pore (PTP) - an example of multiple molecular exaptation?. Biochim. Biophys. Acta 2012, 1817:2072-2086.
161. Wagner G.R., Payne R.M. Widespread and enzyme-independent Nε-acetylation and Nε-succinylation in the chemical conditions of the mitochondrial matrix. J. Biol. Chem. 2013, 288(40):29036-29045.
162. Walters A.M., Porter G.A., Brookes P.S. Mitochondria as a drug target in ischemic heart disease and cardiomyopathy. Circ. Res. 2012, 111:1222-1236.
163. Wang H., Song P., Du L., Tian W., Yue W., Liu M., Li D., Wang B., Zhu Y., Cao C., Zhou J., Chen Q. Parkin ubiquitinates Drp1 for proteasome-dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson disease. J. Biol. Chem. 2011, 286:11649-11658.
164. Wang X., Winter D., Ashrafi G., Schlehe J., Wong Y.L., Selkoe D., Rice S., Steen J., LaVoie M.J., Schwarz T.L. PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 2011, 147:893-906.
165. Webster B.R., Scott I., Han K., Li J.H., Lu Z., Stevens M.V., Malide D., Chen Y., Samsel L., Connelly P.S., Daniels M.P., McCoy J.P., Combs C.A., Gucek M., Sack M.N. Restricted mitochondrial protein acetylation initiates mitochondrial autophagy. J. Cell Sci. 2013, 126(Pt 21):4843-4849.
166. West A.P., Shadel G.S., Ghosh S. Mitochondria in innate immune responses. Nat. Rev. Immunol. 2011, 11:389-402.
167. Wu Y.T., Lee H.C., Liao C.C., Wei Y.H. Regulation of mitochondrial F(o)F(1)ATPase activity by Sirt3-catalyzed deacetylation and its deficiency in human cells harboring 4977bp deletion of mitochondrial DNA. Biochim. Biophys. Acta 2013, 1832:216-227.
168. Xiao K., Jiang J., Wang W., Cao S., Zhu L., Zeng H., Ouyang R., Zhou R., Chen P. Sirt3 is a tumor suppressor in lung adenocarcinoma cells. Oncol. Rep. 2013, 30(3):1323-1328.
169. +-dependent deacetylase SIRT3 regulates mitochondrial protein synthesis by deacetylation of the ribosomal protein MRPL10. J. Biol. Chem. 2010, 285:7417-7429.
170. Yonashiro R., Ishido S., Kyo S., Fukuda T., Goto E., Matsuki Y., Ohmura-Hoshino M., Sada K., Hotta H., Yamamura H., Inatome R., Yanagi S. A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J. 2006, 25:3618-3626.
171. Yonashiro R., Sugiura A., Miyachi M., Fukuda T., Matsushita N., Inatome R., Ogata Y., Suzuki T., Dohmae N., Yanagi S. Mitochondrial ubiquitin ligase MITOL ubiquitinates mutant SOD1 and attenuates mutant SOD1-induced reactive oxygen species generation. Mol. Biol. Cell 2009, 20:4524-4530.
172. Yonashiro R., Kimijima Y., Shimura T., Kawaguchi K., Fukuda T., Inatome R., Yanagi S. Mitochondrial ubiquitin ligase MITOL blocks S-nitrosylated MAP1B-light chain 1-mediated mitochondrial dysfunction and neuronal cell death. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:2382-2387.
173. Youle R.J., van der Bliek A.M. Mitochondrial fission, fusion, and stress. Science 2012, 337(6098):1062-1065. 10.1126/science.1219855.
174. Yu W., Dittenhafer-Reed K.E., Denu J.M. SIRT3 protein deacetylates isocitrate dehydrogenase 2 (IDH2) and regulates mitochondrial redox status. J. Biol. Chem. 2012, 287:14078-14086.
175. Yue W., Chen Z., Liu H., Yan C., Chen M., Feng D., Wu H., Du L., Wang Y., Liu J., Huang X., Xia L., Liu L., Wang X., Jin H., Wang J., Song Z., Hao X., Chen Q. A small natural molecule promotes mitochondrial fusion through inhibition of the deubiquitinase USP30. Cell Res 2014, (Epub ahead of print). 10.1038/cr.2014.20.
176. Zeng W., Sun L., Jiang X., Chen X., Hou F., Adhikari A., Xu M., Chen Z.J. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010, 141:315-330.
177. Zhang C.Z., Liu L., Cai M., Pan Y., Fu J., Cao Y., Yun J. Low SIRT3 expression correlates with poor differentiation and unfavorable prognosis in primary hepatocellular carcinoma. PLoS One 2012, 7:e51703.
178. Zhang Q., Wu J., Wu R., Ma J., Du G., Jiao R., Tian Y., Zheng Z., Yuan Z. DJ-1 promotes the proteasomal degradation of Fis1: implications of DJ-1 in neuronal protection. Biochem. J. 2012, 447:261-269.
179. Zhong Q., Gao W., Du F., Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 2005, 121:1085-1095.
180. Zhong B., Zhang L., Lei C., Li Y., Mao A.P., Yang Y., Wang Y.Y., Zhang X.L., Shu H.B. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 2009, 30:397-407.
181. Zhong B., Zhang Y., Tan B., Liu T.T., Wang Y.Y., Shu H.B. The E3 ubiquitin ligase RNF5 targets virus-induced signaling adaptor for ubiquitination and degradation. J. Immunol. 2010, 184:6249-6255.
182. Zsurka G., Kunz W.S. Mitochondrial involvement in neurodegenerative diseases. IUBMB Life 2013, 65:263-272.