Mitochondrial homeostasis: The interplay between mitophagy and mitochondrial biogenesis

Experimental Gerontology

Volumn 56, Issue , 2014, Pages 182-188

  Palikaras, Konstantinos ^a   Tavernarakis, Nektarios ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

Ageing; Autophagy; Mitochondria; Mitophagy; Parkin; PGC 1 ; PINK1

Indexed keywords

ADENYLATE KINASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CARRIER PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; ESTROGEN RELATED RECEPTOR ALPHA; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; PARKIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE D; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; MITOCHONDRIAL PROTEIN;

AGING; BIOGENESIS; CELL DIFFERENTIATION; CELL METABOLISM; CITRIC ACID CYCLE; COORDINATION; ENVIRONMENTAL STRESS; ENZYME SYNTHESIS; ERYTHROCYTE; FATTY ACID OXIDATION; FERTILIZATION; HOMEOSTASIS; HUMAN; MITOCHONDRION; MITOPHAGY; MOLECULAR DYNAMICS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UBIQUITINATION; AGE; ANIMAL; ENERGY METABOLISM; METABOLISM; MITOCHONDRIAL DYNAMICS; PATHOLOGY;

AGE FACTORS; AGING; ANIMALS; ENERGY METABOLISM; HOMEOSTASIS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL TURNOVER; SIGNAL TRANSDUCTION;

EID: 84901826020     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.01.021     Document Type: Review

References (96)

1. Al Rawi S., Louvet-Vallee S., Djeddi A., Sachse M., Culetto E., Hajjar C., Boyd L., Legouis R., Galy V. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 2011, 334:1144-1147.
2. Artal-Sanz M., Tavernarakis N. Prohibitin couples diapause signalling to mitochondrial metabolism during ageing in C. elegans. Nature 2009, 461:793-797.
3. Baker B.M., Haynes C.M. Mitochondrial protein quality control during biogenesis and aging. Trends Biochem. Sci. 2011, 36:254-261.
4. Bakkar N., Ladner K., Canan B.D., Liyanarachchi S., Bal N.C., Pant M., Periasamy M., Li Q., Janssen P.M., Guttridge D.C. IKKalpha and alternative NF-kappaB regulate PGC-1beta to promote oxidative muscle metabolism. J. Cell Biol. 2012, 196:497-511.
5. Bellot G., Garcia-Medina R., Gounon P., Chiche J., Roux D., Pouyssegur J., Mazure N.M. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell Biol. 2009, 29:2570-2581.
6. Bereiter-Hahn J., Voth M., Mai S., Jendrach M. Structural implications of mitochondrial dynamics. Biotechnol. J. 2008, 3:765-780.
7. Birkenfeld A.L., Lee H.Y., Guebre-Egziabher F., Alves T.C., Jurczak M.J., Jornayvaz F.R., Zhang D., Hsiao J.J., Martin-Montalvo A., Fischer-Rosinsky A., Spranger J., Pfeiffer A.F., Jordan J., Fromm M.F., Konig J., Lieske S., Carmean C.M., Frederick D.W., Weismann D., Knauf F., Irusta P.M., De Cabo R., Helfand S.L., Samuel V.T., Shulman G.I. Deletion of the mammalian INDY homolog mimics aspects of dietary restriction and protects against adiposity and insulin resistance in mice. Cell Metab. 2011, 14:184-195.
8. Blattler S.M., Cunningham J.T., Verdeguer F., Chim H., Haas W., Liu H., Romanino K., Ruegg M.A., Gygi S.P., Shi Y., Puigserver P. Yin Yang 1 deficiency in skeletal muscle protects against rapamycin-induced diabetic-like symptoms through activation of insulin/IGF signaling. Cell Metab. 2012, 15:505-517.
9. Burchell V.S., Nelson D.E., Sanchez-Martinez A., Delgado-Camprubi M., Ivatt R.M., Pogson J.H., Randle S.J., Wray S., Lewis P.A., Houlden H., Abramov A.Y., Hardy J., Wood N.W., Whitworth A.J., Laman H., Plun-Favreau H. The Parkinson's disease-linked proteins Fbxo7 and Parkin interact to mediate mitophagy. Nat. Neurosci. 2013, 16:1257-1265.
10. Calvo S.E., Mootha V.K. The mitochondrial proteome and human disease. Annu. Rev. Genomics Hum. Genet. 2010, 11:25-44.
11. Canto C., Gerhart-Hines Z., Feige J.N., Lagouge M., Noriega L., Milne J.C., Elliott P.J., Puigserver P., Auwerx J. AMPK regulates energy expenditure by modulating NAD+metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.
12. Cardenas C., Foskett J.K. Mitochondrial Ca(2+) signals in autophagy. Cell Calcium 2011, 52:44-51.
13. Carreira R.S., Lee Y., Ghochani M., Gustafsson A.B., Gottlieb R.A. Cyclophilin D is required for mitochondrial removal by autophagy in cardiac cells. Autophagy 2010, 6:462-472.
14. 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.
15. Chen Y., Dorn G.W. PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 2013, 340:471-475.
16. Cherra S.J., Steer E., Gusdon A.M., Kiselyov K., Chu C.T. Mutant LRRK2 elicits calcium imbalance and depletion of dendritic mitochondria in neurons. Am. J. Pathol. 2012, 182:474-484.
17. Cho W., Stahelin R.V. Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta 2006, 1761:838-849.
18. Costello M.J., Brennan L.A., Basu S., Chauss D., Mohamed A., Gilliland K.O., Johnsen S., Menko S., Kantorow M. Autophagy and mitophagy participate in ocular lens organelle degradation. Exp. Eye Res. 2013, 116:141-150.
19. Cunningham J.T., Rodgers J.T., Arlow D.H., Vazquez F., Mootha V.K., Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 2007, 450:736-740.
20. Dagda R.K., Zhu J., Kulich S.M., Chu C.T. Mitochondrially localized ERK2 regulates mitophagy and autophagic cell stress: implications for Parkinson's disease. Autophagy 2008, 4:770-782.
21. Decuypere J.P., Bultynck G., Parys J.B. A dual role for Ca(2+) in autophagy regulation. Cell Calcium 2011, 50:242-250.
22. Dominy J.E., Puigserver P. Mitochondrial biogenesis through activation of nuclear signaling proteins. Cold Spring Harb. Perspect. Biol. 2013, 5.
23. Egan D.F., Shackelford D.B., Mihaylova M.M., Gelino S., Kohnz R.A., Mair W., Vasquez D.S., Joshi A., Gwinn D.M., Taylor R., Asara J.M., Fitzpatrick J., Dillin A., Viollet B., Kundu M., Hansen M., Shaw R.J. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011, 331:456-461.
24. Eisenberg-Lerner A., Kimchi A. PKD is a kinase of Vps34 that mediates ROS-induced autophagy downstream of DAPk. Cell Death Differ. 2012, 19:788-797.
25. Exner N., Lutz A.K., Haass C., Winklhofer K.F. Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J. 2012, 31:3038-3062.
26. Fan W., Waymire K.G., Narula N., Li P., Rocher C., Coskun P.E., Vannan M.A., Narula J., Macgregor G.R., Wallace D.C. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 2008, 319:958-962.
27. Fimia G.M., Stoykova A., Romagnoli A., Giunta L., Di Bartolomeo S., Nardacci R., Corazzari M., Fuoco C., Ucar A., Schwartz P., Gruss P., Piacentini M., Chowdhury K., Cecconi F. Ambra1 regulates autophagy and development of the nervous system. Nature 2007, 447:1121-1125.
28. 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.
29. Gerbeth C., Schmidt O., Rao S., Harbauer A.B., Mikropoulou D., Opalinska M., Guiard B., Pfanner N., Meisinger C. Glucose-induced regulation of protein import receptor Tom22 by cytosolic and mitochondria-bound kinases. Cell Metab. 2013, 18:578-587.
30. Gleyzer N., Vercauteren K., Scarpulla R.C. Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol. Cell Biol. 2005, 25:1354-1366.
31. Hanna R.A., Quinsay M.N., Orogo A.M., Giang K., Rikka S., Gustafsson A.B. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J. Biol. Chem. 2012, 287:19094-19104.
32. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 2007, 8:774-785.
33. Hickson-Bick D.L., Jones C., Buja L.M. Stimulation of mitochondrial biogenesis and autophagy by lipopolysaccharide in the neonatal rat cardiomyocyte protects against programmed cell death. J. Mol. Cell. Cardiol. 2008, 44:411-418.
34. Itakura E., Kishi C., Inoue K., Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 2008, 19:5360-5372.
35. Jager S., Handschin C., St-Pierre J., Spiegelman B.M. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12017-12022.
36. Jaggi M., Du C., Zhang W., Balaji K.C. Protein kinase D1: a protein of emerging translational interest. Front. Biosci. 2007, 12:3757-3767.
37. Kaeberlein M. Lessons on longevity from budding yeast. Nature 2010, 464:513-519.
38. Karbowski M., Youle R.J. Regulating mitochondrial outer membrane proteins by ubiquitination and proteasomal degradation. Curr. Opin. Cell Biol. 2011, 23:476-482.
39. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
40. 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.
41. Kubli D.A., Gustafsson A.B. Mitochondria and mitophagy: the yin and yang of cell death control. Circ. Res. 2012, 111:1208-1221.
42. Kuroda Y., Mitsui T., Kunishige M., Shono M., Akaike M., Azuma H., Matsumoto T. Parkin enhances mitochondrial biogenesis in proliferating cells. Hum. Mol. Genet. 2006, 15:883-895.
43. Lazarou M., Jin S.M., Kane L.A., Youle R.J. Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev. Cell 2012, 22:320-333.
44. Lee H.C., Yin P.H., Chi C.W., Wei Y.H. Increase in mitochondrial mass in human fibroblasts under oxidative stress and during replicative cell senescence. J. Biomed. Sci. 2002, 9:517-526.
45. Lee T.M., Su S.F., Chou T.F., Lee Y.T., Tsai C.H. Loss of preconditioning by attenuated activation of myocardial ATP-sensitive potassium channels in elderly patients undergoing coronary angioplasty. Circulation 2002, 105:334-340.
46. Lee Y., Lee H.Y., Hanna R.A., Gustafsson A.B. Mitochondrial autophagy by Bnip3 involves Drp1-mediated mitochondrial fission and recruitment of Parkin in cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 2011, 301:H1924-H1931.
47. Liu L., Feng D., Chen G., Chen M., Zheng Q., Song P., Ma Q., Zhu C., Wang R., Qi W., Huang L., Xue P., Li B., Wang X., Jin H., Wang J., Yang F., Liu P., Zhu Y., Sui S., Chen Q. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 2012, 14:177-185.
48. Lopez-Otin C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
49. Lu K., Li P., Zhang M., Xing G., Li X., Zhou W., Bartlam M., Zhang L., Rao Z., He F. Pivotal role of the C2 domain of the Smurf1 ubiquitin ligase in substrate selection. J. Biol. Chem. 2011, 286:16861-16870.
50. Malpass K. Neurodegenerative disease: defective mitochondrial dynamics in the hot seat-a therapeutic target common to many neurological disorders?. Nat. Rev. Neurol. 2013, 9:417.
51. Manji H., Kato T., Di Prospero N.A., Ness S., Beal M.F., Krams M., Chen G. Impaired mitochondrial function in psychiatric disorders. Nat. Rev. Neurosci. 2012, 13:293-307.
52. Martinez-Vicente M., Talloczy Z., Wong E., Tang G., Koga H., Kaushik S., de Vries R., Arias E., Harris S., Sulzer D., Cuervo A.M. Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat. Neurosci. 2010, 13:567-576.
53. Matsushima Y., Kaguni L.S. Matrix proteases in mitochondrial DNA function. Biochim. Biophys. Acta 2012, 1819:1080-1087.
54. 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.
55. 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.
56. 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.
57. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., Rogov V., Lohr F., Popovic D., Occhipinti A., Reichert A.S., Terzic J., Dotsch V., Ney P.A., Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11:45-51.
58. Orvedahl A., Sumpter R., Xiao G., Ng A., Zou Z., Tang Y., Narimatsu M., Gilpin C., Sun Q., Roth M., Forst C.V., Wrana J.L., Zhang Y.E., Luby-Phelps K., Xavier R.J., Xie Y., Levine B. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 2011, 480:113-117.
59. Palikaras K., Tavernarakis N. Mitophagy in neurodegeneration and aging. Front. Genet. 2012, 3:297.
60. Pallanck L. Mitophagy: mitofusin recruits a mitochondrial killer. Curr. Biol. 2013, 23:R570-R572.
61. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
62. Preston C.C., Oberlin A.S., Holmuhamedov E.L., Gupta A., Sagar S., Syed R.H., Siddiqui S.A., Raghavakaimal S., Terzic A., Jahangir A. Aging-induced alterations in gene transcripts and functional activity of mitochondrial oxidative phosphorylation complexes in the heart. Mech. Ageing Dev. 2008, 129:304-312.
63. Radke S., Chander H., Schafer P., Meiss G., Kruger R., Schulz J.B., Germain D. Mitochondrial protein quality control by the proteasome involves ubiquitination and the protease Omi. J. Biol. Chem. 2008, 283:12681-12685.
64. Rasbach K.A., Schnellmann R.G. PGC-1alpha over-expression promotes recovery from mitochondrial dysfunction and cell injury. Biochem. Biophys. Res. Commun. 2007, 355:734-739.
65. Rothfuss O., Fischer H., Hasegawa T., Maisel M., Leitner P., Miesel F., Sharma M., Bornemann A., Berg D., Gasser T., Patenge N. Parkin protects mitochondrial genome integrity and supports mitochondrial DNA repair. Hum. Mol. Genet. 2009, 18:3832-3850.
66. Sandoval H., Thiagarajan P., Dasgupta S.K., Schumacher A., Prchal J.T., Chen M., Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008, 454:232-235.
67. Sato M., Sato K. Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 2011, 334:1141-1144.
68. Scarpulla R.C. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 2008, 88:611-638.
69. Schieke S.M., Phillips D., McCoy J.P., Aponte A.M., Shen R.F., Balaban R.S., Finkel T. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 2006, 281:27643-27652.
70. Schmidt O., Harbauer A.B., Rao S., Eyrich B., Zahedi R.P., Stojanovski D., Schonfisch B., Guiard B., Sickmann A., Pfanner N., Meisinger C. Regulation of mitochondrial protein import by cytosolic kinases. Cell 2011, 144:227-239.
71. Schwarten M., Mohrluder J., Ma P., Stoldt M., Thielmann Y., Stangler T., Hersch N., Hoffmann B., Merkel R., Willbold D. Nix directly binds to GABARAP: a possible crosstalk between apoptosis and autophagy. Autophagy 2009, 5:690-698.
72. Schweers R.L., Zhang J., Randall M.S., Loyd M.R., Li W., Dorsey F.C., Kundu M., Opferman J.T., Cleveland J.L., Miller J.L., Ney P.A. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19500-19505.
73. Shin J.H., Ko H.S., Kang H., Lee Y., Lee Y.I., Pletinkova O., Troconso J.C., Dawson V.L., Dawson T.M. PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell 2011, 144:689-702.
74. Soubannier V., McLelland G.L., Zunino R., Braschi E., Rippstein P., Fon E.A., McBride H.M. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr. Biol. 2012, 22:135-141.
75. Srivastava S., Diaz F., Iommarini L., Aure K., Lombes A., Moraes C.T. PGC-1alpha/beta induced expression partially compensates for respiratory chain defects in cells from patients with mitochondrial disorders. Hum. Mol. Genet. 2009, 18:1805-1812.
76. Storz P., Doppler H., Toker A. Protein kinase Cdelta selectively regulates protein kinase D-dependent activation of NF-kappaB in oxidative stress signaling. Mol. Cell Biol. 2004, 24:2614-2626.
77. Storz P., Doppler H., Toker A. Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol. Cell Biol. 2005, 25:8520-8530.
78. 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. 2011, 287:40652-40660.
79. Thomas R.L., Gustafsson A.B. Mitochondrial autophagy. Circ. J. 2013, 77:2449-2454.
80. Tracy K., Dibling B.C., Spike B.T., Knabb J.R., Schumacker P., Macleod K.F. BNIP3 is an RB/E2F target gene required for hypoxia-induced autophagy. Mol. Cell Biol. 2007, 27:6229-6242.
81. Vafai S.B., Mootha V.K. Mitochondrial disorders as windows into an ancient organelle. Nature 2012, 491:374-383.
82. 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.
83. van der Bliek A.M., Shen Q., Kawajiri S. Mechanisms of mitochondrial fission and fusion. Cold Spring Harb. Perspect. Biol. 2013, 5.
84. Van Humbeeck C., Cornelissen T., Hofkens H., Mandemakers W., Gevaert K., De Strooper B., Vandenberghe W. Parkin interacts with Ambra1 to induce mitophagy. J. Neurosci. 2011, 31:10249-10261.
85. Viscomi C., Bottani E., Civiletto G., Cerutti R., Moggio M., Fagiolari G., Schon E.A., Lamperti C., Zeviani M. In vivo correction of COX deficiency by activation of the AMPK/PGC-1alpha axis. Cell Metab. 2011, 14:80-90.
86. Waldron R.T., Rozengurt E. Oxidative stress induces protein kinase D activation in intact cells. Involvement of Src and dependence on protein kinase C. J. Biol. Chem. 2000, 275:17114-17121.
87. 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.
88. Wright D.C., Geiger P.C., Han D.H., Jones T.E., Holloszy J.O. Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J. Biol. Chem. 2007, 282:18793-18799.
89. Wu H., Kanatous S.B., Thurmond F.A., Gallardo T., Isotani E., Bassel-Duby R., Williams R.S. Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 2002, 296:349-352.
90. Xing L., Zhang M., Chen D. Smurf control in bone cells. J. Cell. Biochem. 2010, 110:554-563.
91. Yan J., Feng Z., Liu J., Shen W., Wang Y., Wertz K., Weber P., Long J. Enhanced autophagy plays a cardinal role in mitochondrial dysfunction in type 2 diabetic Goto-Kakizaki (GK) rats: ameliorating effects of (-)-epigallocatechin-3-gallate. J. Nutr. Biochem. 2012, 23:716-724.
92. Yang J.Y., Yang W.Y. Bit-by-bit autophagic removal of parkin-labelled mitochondria. Nat. Commun. 2013, 4:2428.
93. Yoshii S.R., Kishi C., Ishihara N., Mizushima N. Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J. Biol. Chem. 2011, 286:19630-19640.
94. Zhang J., Ney P.A. Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ. 2009, 16:939-946.
95. Zhu J.H., Horbinski C., Guo F., Watkins S., Uchiyama Y., Chu C.T. Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death. Am. J. Pathol. 2007, 170:75-86.
96. Zhu J., Wang K.Z., Chu C.T. After the banquet: mitochondrial biogenesis, mitophagy and cell survival. Autophagy 2013, 9.