Shared and cell type-specific mitochondrial defects and metabolic adaptations in primary cells from PINK1-deficient mice

Neurodegenerative Diseases

Volumn 12, Issue 3, 2013, Pages 136-149

  Akundi, Ravi S ^a   Zhi, Lianteng ^a   Sullivan, Patrick G ^a   Büeler, Hansruedi ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Cristae degeneration; Mitochondrial dynamics; Mitochondrial swelling; PTEN induced kinase 1; Spare respiratory capacity; Uncoupling protein 2; Warburg effect

Indexed keywords

PROTEIN SERINE THREONINE KINASE; PTEN INDUCED KINASE 1; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 2; OXYGEN; PHOSPHOTRANSFERASE;

ACIDIFICATION; ANIMAL CELL; ARTICLE; BIOGENESIS; BRAIN CELL; CELL DEGENERATION; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; CORPUS STRIATUM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EMBRYONIC STEM CELL; FIBROBLAST; GLYCOLYSIS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ADAPTATION; ANIMAL EXPERIMENT; DROSOPHILA; MAMMAL CELL; MEMBRANE POTENTIAL; METABOLIC CAPACITY; MOLECULAR DYNAMICS; MUTATION; PARKINSON DISEASE; PINK1 MUTANT (DROSOPHILA); PRIMARY CELL; QUALITY CONTROL;

EID: 84884286745     PISSN: 16602854     EISSN: 16602862     Source Type: Journal    
DOI: 10.1159/000345689     Document Type: Article

References (61)

1. Bueler H: Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson's disease. Exp Neurol 2009; 218: 235-246.
2. Henchcliffe C, Beal MF: Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nat Clin Pract Neurol 2008; 4: 600-609.
3. Tansey MG, Goldberg MS: Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol Dis 2010; 37: 510-518.
4. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, González-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, Auburger G, Wood NW: Hereditary earlyonset Parkinson's disease caused by mutations in PINK1. Science 2004; 304: 1158-1160.
5. Jin SM, Lazarou M, Wang C, Kane LA, Narendra DP, Youle RJ: Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol 2010; 191: 933-942.
6. Greene AW, Grenier K, Aguileta MA, Muise S, Farazifard R, Haque ME, McBride HM, Park DS, Fon EA: Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep 2012; 13: 378-385.
7. Meissner C, Lorenz H, Weihofen A, Selkoe DJ, Lemberg MK: The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J Neurochem 2011; 117: 856-867.
8. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ: PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8:e1000298.
9. Geisler S, Holmström KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, Springer W: PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12: 119-131.
10. Cai Q, Zakaria HM, Simone A, Sheng ZH: Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr Biol 2012; 22: 545-552.
11. Gautier CA, Kitada T, Shen J: Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc Natl Acad Sci USA 2008; 105: 11364-11369.
12. Akundi RS, Huang Z, Eason J, Pandya JD, Zhi L, Cass WA, Sullivan PG, Büeler H: Increased mitochondrial calcium sensitivity and abnormal expression of innate immunity genes precede dopaminergic defects in Pink1-deficient mice. PLoS One 2011; 6:e16038.
13. Gandhi S, Wood-Kaczmar A, Yao Z, Plun- Favreau H, Deas E, Klupsch K, Downward J, Latchman DS, Tabrizi SJ, Wood NW, Duchen MR, Abramov AY: Pink1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol Cell 2009; 33: 627-638.
14. Haque ME, Thomas KJ, D'Souza C, Callaghan S, Kitada T, Slack RS, Fraser P, Cookson MR, Tandon A, Park DS: Cytoplasmic Pink1 activity protects neurons from dopaminergic neurotoxin MPTP. Proc Natl Acad Sci USA 2008; 105: 1716-1721.
15. Akundi RS, Zhi L, Büeler H: PINK1 enhances insulin-like growth factor-1-dependent Akt signaling and protection against apoptosis. Neurobiol Dis 2012; 45: 469-478.
16. Pang Z, Geddes JW: Mechanisms of cell death induced by the mitochondrial toxin 3-nitropropionic acid: acute excitotoxic necrosis and delayed apoptosis. J Neurosci 1997; 17: 3064-3073.
17. Roth JF, Shikama N, Henzen C, Desbaillets I, Lutz W, Marino S, Wittwer J, Schorle H, Gassmann M, Eckner R: Differential role of p300 and CBP acetyltransferase during myogenesis: p300 acts upstream of MyoD and Myf5. EMBO J 2003; 22: 5186-5196.
18. Wood-Kaczmar A, Gandhi S, Yao Z, Abramov AY, Miljan EA, Keen G, Stanyer L, Hargreaves I, Klupsch K, Deas E, Downward J, Mansfield L, Jat P, Taylor J, Heales S, Duchen MR, Latchman D, Tabrizi SJ, Wood NW: PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons. PLoS One 2008; 3:e2455.
19. Handschin C, Spiegelman BM: Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 2006; 27: 728-735.
20. 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.
21. Arboleda G, Huang TJ, Waters C, Verkhratsky A, Fernyhough P, Gibson RM: Insulin- like growth factor-1-dependent maintenance of neuronal metabolism through the phosphatidylinositol 3-kinase-Akt pathway is inhibited by C2-ceramide in CAD cells. Eur J Neurosci 2007; 25: 3030-3038.
22. Robinson BH, Petrova-Benedict R, Buncic JR, Wallace DC: Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts. Biochem Med Metab Biol 1992; 48: 122-126.
23. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, Seol JH, Yoo SJ, Hay BA, Guo M: Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 2006; 441: 1162-1166.
24. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, Bae E, Kim J, Shong M, Kim JM, Chung J: Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 2006; 441: 1157-1161.
25. Deng H, Dodson MW, 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 USA 2008; 105: 14503-14508.
26. Heeman B, Van den Haute C, Aelvoet SA, Valsecchi F, Rodenburg RJ, Reumers V, Debyser Z, Callewaert G, Koopman WJ, Willems PH, Baekelandt V: Depletion of PINK1 affects mitochondrial metabolism, calcium homeostasis and energy maintenance. J Cell Sci 2011; 124: 1115-1125.
27. Abramov AY, Gegg M, Grunewald A, Wood NW, Klein C, Schapira AH: Bioenergetic consequences of PINK1 mutations in Parkinson disease. PLoS One 2011; 6:e25622.
28. Morais VA, Verstreken P, Roethig A, Smet J, Snellinx A, Vanbrabant M, Haddad D, Frezza C, Mandemakers W, Vogt-Weisenhorn D, Van Coster R, Wurst W, Scorrano L, De Strooper B: Parkinson's disease mutations in PINK1 result in decreased Complex I activity and deficient synaptic function. EMBO Mol Med 2009; 1: 99-111.
29. Gegg ME, Cooper JM, Schapira AH, Taanman JW: Silencing of PINK1 expression affects mitochondrial DNA and oxidative phosphorylation in dopaminergic cells. PLoS One 2009; 4:e4756.
30. Exner N, Treske B, Paquet D, Holmström K, Schiesling C, Gispert S, Carballo-Carbajal I, Berg D, Hoepken HH, Gasser T, Krüger R, Winklhofer KF, Vogel F, Reichert AS, Auburger G, Kahle PJ, Schmid B, Haass C: Lossof- function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J Neurosci 2007; 27: 12413-12418.
31. Amo T, Sato S, Saiki S, Wolf AM, Toyomizu M, Gautier CA, Shen J, Ohta S, Hattori N: Mitochondrial membrane potential decrease caused by loss of PINK1 is not due to proton leak, but to respiratory chain defects. Neurobiol Dis 2011; 41: 111-118.
32. Anichtchik O, Diekmann H, Fleming A, Roach A, Goldsmith P, Rubinsztein DC: Loss of pink1 function affects development and results in neurodegeneration in zebrafish. J Neurosci 2008; 28: 8199-8207.
33. Javadov S, Karmazyn M, Escobales N: Mitochondrial permeability transition pore opening as a promising therapeutic target in cardiac diseases. J Pharmacol Exp Ther 2009; 330: 670-678.
34. Rasola A, Sciacovelli M, Pantic B, Bernardi P: Signal transduction to the permeability transition pore. FEBS Lett 2010; 584: 1989-1996.
35. Grünewald A, Gegg ME, Taanman JW, King RH, Kock N, Klein C, Schapira AH: Differential effects of PINK1 nonsense and missense mutations on mitochondrial function and morphology. Exp Neurol 2009; 219: 266-273.
36. Azzu V, Jastroch M, Divakaruni AS, Brand MD: The regulation and turnover of mitochondrial uncoupling proteins. Biochim Biophys Acta 2010; 1797: 785-791.
37. Pi J, Bai Y, Daniel KW, Liu D, Lyght O, Edelstein D, Brownlee M, Corkey BE, Collins S: Persistent oxidative stress due to absence of uncoupling protein 2 associated with impaired pancreatic beta-cell function. Endocrinology 2009; 150: 3040-3048.
38. Azzu V, Brand MD: The on-off switches of the mitochondrial uncoupling proteins. Trends Biochem Sci 2010; 35: 298-307.
39. Sullivan PG, Dube C, Dorenbos K, Steward O, Baram TZ: Mitochondrial uncoupling protein-2 protects the immature brain from excitotoxic neuronal death. Ann Neurol 2003; 53: 711-717.
40. Islam R, Yang L, Sah M, Kannan K, Anamani D, Vijayan C, Kwok J, Cantino ME, Beal MF, Fridell YW: A neuroprotective role of the human uncoupling protein 2 (hUCP2) in a Drosophila Parkinson's disease model. Neurobiol Dis 2012; 46: 137-146.
41. Andrews ZB, Horvath B, Barnstable CJ, Elsworth J, Yang L, Beal MF, Roth RH, Matthews RT, Horvath TL: Uncoupling protein- 2 is critical for nigral dopamine cell survival in a mouse model of Parkinson's disease. J Neurosci 2005; 25: 184-191.
42. Haque ME, Mount MP, Safarpour F, Abdel- Messih E, Callaghan S, Mazerolle C, Kitada T, Slack RS, Wallace V, Shen J, Anisman H, Park DS: Inactivation of Pink1 in vivo sensitizes dopamine producing neurons to 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine (MPTP) and can be rescued by autosomal recessive Parkinson disease genes, Parkin or DJ-1. J Biol Chem 2012; 287: 23162-23170.
43. Cairns RA, Harris IS, Mak TW: Regulation of cancer cell metabolism. Nat Rev Cancer 2011; 11: 85-95.
44. Warburg O: On the origin of cancer cells. Science 1956; 123: 309-314.
45. Zhang C, Lin M, Wu R, Wang X, Yang B, Levine AJ, Hu W, Feng Z: Parkin, a p53 target gene, mediates the role of p53 in glucose metabolism and the Warburg effect. Proc Natl Acad Sci USA 2011; 108: 16259-16264.
46. Sha D, Chin LS, Li L: Phosphorylation of parkin by Parkinson disease-linked kinase PINK1 activates parkin E3 ligase function and NF-kappaB signaling. Hum Mol Genet 2010; 19: 352-363.
47. Bolanos JP, Almeida A, Moncada S: Glycolysis: a bioenergetic or a survival pathway? Trends Biochem Sci 2010; 35: 145-149.
48. Deng H, Dodson MW, 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 USA 2008; 105: 14503-14508.
49. Poole AC, Thomas RE, Andrews LA, Mc- Bride HM, Whitworth AJ, Pallanck LJ: The PINK1/Parkin pathway regulates mitochondrial morphology. Proc Natl Acad Sci USA 2008; 105: 1638-1643.
50. Park J, Lee G, Chung J: The PINK1-Parkin pathway is involved in the regulation of mitochondrial remodeling process. Biochem Biophys Res Commun 2008; 378: 518-523.
51. Dagda RK, Cherra SJ 3rd, Kulich SM, Tandon A, Park D, Chu CT: Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 2009; 284: 13843-13855.
52. Lutz AK, Exner N, Fett ME, Schlehe JS, Kloos K, Lämmermann K, Brunner B, Kurz-Drexler A, Vogel F, Reichert AS, Bouman L, Vogt- Weisenhorn D, Wurst W, Tatzelt J, Haass C, Winklhofer KF: Loss of parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation. J Biol Chem 2009; 284: 22938-22951.
53. Butler EK, Voigt A, Lutz AK, Toegel JP, Gerhardt E, Karsten P, Falkenburger B, Reinartz A, Winklhofer KF, Schulz JB: The mitochondrial chaperone protein TRAP1 mitigates - Synuclein toxicity. PLoS Genet 2012; 8:e1002488.
54. Joselin AP, Hewitt SJ, Callaghan SM, Kim RH, Chung YH, Mak TW, Shen J, Slack RS, Park DS: ROS-dependent regulation of Parkin and DJ-1 localization during oxidative stress in neurons. Hum Mol Genet 2012; 21: 4888-4903.
55. Yu W, Sun Y, Guo S, Lu B: The PINK1/Parkin pathway regulates mitochondrial dynamics and function in mammalian hippocampal and dopaminergic neurons. Hum Mol Genet 2011; 20: 3227-3240.
56. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, Mosharov EV, Hodara R, Fredenburg R, Wu DC, Follenzi A, Dauer W, Przedborski S, Ischiropoulos H, Lansbury PT, Sulzer D, Cuervo AM: Dopamine- modified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest 2008; 118: 777-788.
57. LaVoie MJ, Ostaszewski BL, Weihofen A, Schlossmacher MG, Selkoe DJ: Dopamine covalently modifies and functionally inactivates parkin. Nat Med 2005; 11: 1214-1221.
58. Gandhi S, Vaarmann A, Yao Z, Duchen MR, Wood NW, Abramov AY: Dopamine induced neurodegeneration in a PINK1 model of Parkinson's disease. PLoS One 2012; 7:e37564.
59. Mosharov EV, Larsen KE, Kanter E, Phillips KA, Wilson K, Schmitz Y, Krantz DE, Kobayashi K, Edwards RH, Sulzer D: Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons. Neuron 2009; 62: 218-229.
60. Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW: Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/ parkin-dependent manner upon induction of mitophagy. Hum Mol Genet 2010; 19: 4861-4870.
61. Rakovic A, Grünewald A, Kottwitz J, Brüggemann N, Pramstaller PP, Lohmann K, Klein C: Mutations in PINK1 and Parkin impair ubiquitination of Mitofusins in human fibroblasts. PLoS One 2011; 6:e16746.