Monitoring mitochondrial dynamics and complex i dysfunction in neurons: Implications for Parkinson's disease

Biochemical Society Transactions

Volumn 41, Issue 6, 2013, Pages 1618-1624

  Simcox, Eve M ^a   Reeve, Amy ^a   Turnbull, Doug ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Dynamics; Electron transport chain; Mitochondrion; Morphology; Neuron; Parkinson's disease; Trafficking

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE;

BIOENERGY; CAENORHABDITIS ELEGANS; CELL FUSION; CELL MIGRATION; CELL MOTILITY; COMPLEX I DYSFUNCTION; CONFERENCE PAPER; DOPAMINERGIC NERVE CELL; DROSOPHILA; ENZYME DEFECT; HUMAN; MITOCHONDRIAL DYNAMICS; MITOPHAGY; MONITORING; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; RESPIRATORY CHAIN; SUBSTANTIA NIGRA;

ANIMALS; ELECTRON TRANSPORT COMPLEX I; HUMANS; MITOCHONDRIA; NEURONS; PARKINSON DISEASE;

EID: 84887934707     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20130189     Document Type: Conference Paper

References (48)

1. Papa, S. and De Rasmo, D. (2013) Complex I deficiencies in neurological disorders. Trends Mol. Med. 19, 61-69
2. Chan, D.C. (2012) Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46, 265-287
3. Chan, D.C. (2006) Mitochondrial fusion and fission in mammals, Annu. Rev. Cell Dev. Biol. 22, 79-99
4. Twig, G., Graf, S.A., Wikstrom, J.D., Mohamed, H., Haigh, S.E., Elorza, A., Deutsch, M., Zurgil, N., Reynolds, N. and Shirihai, O.S. (2006) Tagging and tracking individual networks within a complex mitochondrial web with photoactivatable GFP. Am. J. Physiol. Cell Physiol. 291, C176-C184
5. Chen, H., Vermulst, M., Wang, Y.E., Chomyn, A., Prolla, T.A., McCaffery, J.M. and Chan, D.C. (2010) Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141, 280-289
6. Westermann, B. (2010) Mitochondrial fusion and fission in cell life and death, Nat. Rev. Mol. Cell Biol. 11, 872-884
7. Cagalinec, M., Safiulina, D., Liiv, M., Liiv, J., Choubey, V., Wareski, P., Veksler, V. and Kaasik, A. (2013) Principles of the mitochondrial fusion and fission cycle in neurons. J. Cell Sci. 126, 2187-2197
8. Amati-Bonneau, P., Valentino, M.L., Reynier, P., Gallardo, M.E., Bornstein, B., Boissiere, A., Campos, Y., Rivera, H., de la Aleja, J.G., Carroccia, R. et al. (2008) OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain 131, 338-351
9. Schulz, K.L., Eckert, A., Rhein, V., Mai, S., Haase, W., Reichert, A.S., Jendrach, M., Muller, W.E. and Leuner, K. (2012) A new link to mitochondrial impairment in tauopathies. Mol. Neurobiol. 46, 205-216
10. Pham, A.H., Meng, S., Chu, Q.N. and Chan, D.C. (2012) Loss of Mfn2 results in progressive, retrograde degeneration of dopaminergic neurons in the nigrostriatal circuit. Hum. Mol. Genet. 21, 4817-4826
11. Jin, S.M., Lazarou, M., Wang, C., Kane, L.A., Narendra, D.P. and Youle, R.J. (2010) Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 191, 933-942
12. Okatsu, K., Oka, T., Iguchi, M., Imamura, K., Kosako, H., Tani, N., Kimura, M., Go, E., Koyano, F., Funayama, M. et al. (2012) PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat. Commun. 3, 1016
13. Gautier, C.A., Kitada, T. and Shen, J. (2008) Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 105, 11364-11369
14. Gispert, S., Ricciardi, F., Kurz, A., Azizov, M., Hoepken, H.-H., Becker, D., Voos, W., Leuner, K., Muller, W.E., Kudin, A.P. et al. (2009) Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS ONE 4, e5777
15. Mortiboys, H., Thomas, K.J., Koopman, W.J. H., Klaffke, S., Abou-Sleiman, P., Olpin, S., Wood, N.W., Willems, P.H.G.M., Smeitink, J.A.M., Cookson, M.R. and Bandmann, O. (2008) Mitochondrial function and morphology are impaired in parkin-mutant fibroblasts. Ann. Neurol. 64, 555-565
16. Kitada, T., Pisani, A., Porter, D.R., Yamaguchi, H., Tscherter, A., Martella, G., Bonsi, P., Zhang, C., Pothos, E.N. and Shen, J. (2007) Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 104, 11441-11446
17. Greene, J.C., Whitworth, A.J., Kuo, I., Andrews, L.A., Feany, M.B. and Pallanck, L.J. (2003) Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl. Acad. Sci. U.S.A. 100, 4078-4083
18. Clark, I.E., Dodson, M.W., Jiang, C., Cao, J.H., Huh, J.R., Seol, J.H., Yoo, S.J., Hay, B.A. and Guo, M. (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441, 1162-1166
19. Wood-Kaczmar, A., Gandhi, S., Yao, Z., Abramov, A.Y., Miljan, E.A., Keen, G., Stanyer, L., Hargreaves, I., Klupsch, K., Deas, E. et al. (2008) PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons. PLoS ONE. 3, e2455
20. Chen, S., Owens, G.C., Crossin, K.L. and Edelman, D.B. (2007) Serotonin stimulates mitochondrial transport in hippocampal neurons. Mol. Cell. Neurosci. 36, 472-483
21. Overly, C.C., Rieff, H.I. and Hollenbeck, P.J. (1996) Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons. J. Cell Sci. 109, 971-980
22. Waters, J. and Smith, S.J. (2003) Mitochondria and release at hippocampal synapses. Pflügers Arch. 447, 363-370
23. Saxton, W.M. and Hollenbeck, P.J. (2012) The axonal transport of mitochondria. J. Cell Sci. 125, 2095-2104
24. Baas, P.W., Black, M.M. and Banker, G.A. (1989) Changes in microtubule polarity orientation during the development of hippocampal neurons in culture. J. Cell Biol. 109, 3085-3094
25. Liu, S., Sawada, T., Lee, S., Yu, W., Silverio, G., Alapatt, P., Millan, I., Shen, A., Saxton, W., Kanao, T. et al. (2012) Parkinson's disease-associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet. 8, e1002537
26. Wang, X., Winter, D., Ashrafi, G., Schlehe, J., Wong, Y.L., Selkoe, D., Rice, S., Steen, J., LaVoie, M.J. and Schwarz, T.L. (2011) PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147, 893-906
27. Kaasik, A., Safiulina, D., Choubey, V., Kuum, M., Zharkovsky, A. and Veksler, V. (2007) Mitochondrial swelling impairs the transport of organelles in cerebellar granule neurons. J. Biol. Chem. 282, 32821-32826
28. Karbowski, M., Arnoult, D., Chen, H., Chan, D.C., Smith, C.L. and Youle, R.J. (2004) Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis. J. Cell Biol. 164, 493-499
29. Frezza, C., Cipolat, S., Martins de Brito, O., Mii, M., Beznoussenko, G.V., Rudka, T., Bartoli, D., Polishuck, R.S., Danial, N.N., De Strooper, B. and Scorrano, L. (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126, 177-189
30. Morais, V.A., Verstreken, P., Roethig, A., Smet, J., Snellinx, A., Vanbrabant, M., Haddad, D., Frezza, C., Mandemakers, W., Vogt-Weisenhorn, D. et al. (2009) Parkinson's disease mutations in PINK1 result in decreased Complex I activity and deficient synaptic function. EMBO Mol. Med. 1, 99-111
31. Scorrano, L., Ashiya, M., Buttle, K., Weiler, S., Oakes, S.A., Mannella, C.A. and Korsmeyer, S.J. (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2, 55-67
32. Exner, N., Treske, B., Paquet, D., Holmstrom, K., Schiesling, C., Gispert, S., Carballo-Carbajal, I., Berg, D., Hoepken, H.-H., Gasser, T. et al. (2007) Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J. Neurosci. 27, 12413-12418
33. Dagda, R.K., Cherra, III, S.J., Kulich, S.M., Tandon, A., Park, D. and Chu, C.T. (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem. 284, 13843-13855
34. Yang, Y., Ouyang, Y., Yang, L., Beal, M.F., McQuibban, A., Vogel, H. and Lu, B. (2008) Pink1 regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc. Natl. Acad. Sci. U.S.A. 105, 7070-7075
35. Swerdlow, R.H., Parks, J.K., Miller, S.W., Tuttle, J.B., Trimmer, P.A., Sheehan, J.P., Bennett, Jr, J.P., Davis, R.E. and Parker, Jr, W.D. (1996) Origin and functional consequences of the complex I defect in Parkinson's disease. Ann. Neurol. 40, 663-671
36. Rossignol, R., Gilkerson, R., Aggeler, R., Yamagata, K., Remington, S.J. and Capaldi, R.A. (2004) Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res. 64, 985-993
37. Benard, G., Bellance, N., James, D., Parrone, P., Fernandez, H., Letellier, T. and Rossignol, R. (2007) Mitochondrial bioenergetics and structural network organization. J. Cell Sci. 120, 838-848
38. Meeusen, S., McCaffery, J.M. and Nunnari, J. (2004) Mitochondrial fusion intermediates revealed in vitro. Science 305, 1747-1752
39. Koopman, W.J.H., Visch, H.-J., Verkaart, S., van den Heuvel, L.W.P.J., Smeitink, J.A.M. and Willems, P.H.G.M. (2005) Mitochondrial network complexity and pathological decrease in complex I activity are tightly correlated in isolated human complex I deficiency. Am. J. Physiol. Cell Physiol. 289, C881-C890
40. Koopman, W.J.H., Verkaart, S., Visch, H.-J., van der Westhuizen, F.H., Murphy, M.P., van den Heuvel, L.W.P.J., Smeitink, J.A. and Willems, P.H.G.M. (2005) Inhibition of complex I of the electron transport chain causes O2-mediated mitochondrial outgrowth. Am. J. Physiol. Cell. Physiol. 288, C1440-C1450
41. Frank, S., Gaume, B., Bergmann-Leitner, E.S., Leitner, W.W., Robert, E.G., Catez, F., Smith, C.L. and Youle, R.J. (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525
42. Rambold, A.S., Kostelecky, B. and Lippincott-Schwartz, J. (2011) Together we are stronger: fusion protects mitochondria from autophagosomal degradation. Autophagy 7, 1568-1569
43. Nakada, K., Inoue, K. and Hayashi, J. (2001) Interaction theory of mammalian mitochondria. Biochem. Biophys. Res. Commun. 288, 743-746
44. Morel, F., Mazet, F., Touraille, S. and Alziari, S. (1995) Changes in the respiratory chain complexes activities and in the mitochondrial DNA content during ageing in D. subobscura. Mech. Ageing Dev. 84, 171-181
45. Oda, Y., Yui, R., Sakamoto, K., Kita, K. and Matsuura, E.T. (2012) Age-related changes in the activities of respiratory chain complexes and mitochondrial morphology in Drosophila. Mitochondrion 12, 345-351
46. Yasuda, K., Ishii, T., Suda, H., Akatsuka, A., Hartman, P.S., Goto, S., Miyazawa, M. and Ishii, N. (2006) Age-related changes of mitochondrial structure and function in Caenorhabditis elegans. Mech. Ageing Dev. 127, 763-770
47. Miller, K.E. and Sheetz, M.P. (2004) Axonal mitochondrial transport and potential are correlated. J. Cell Sci. 117, 2791-2804
48. Cassidy-Stone, A., Chipuk, J.E., Ingerman, E., Song, C., Yoo, C., Kuwana, T., Kurth, M.J., Shaw, J.T., Hinshaw, J.E., Green, D.R. and Nunnari, J. (2008) Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 14, 193-204