Loss of Mfn2 results in progressive, retrograde degeneration of dopaminergic neurons in the nigrostriatal circuit

Human Molecular Genetics

Volumn 21, Issue 22, 2012, Pages 4817-4826

  Pham, Anh H ^a   Meng, Shuxia ^a   Chu, Quynh N ^a   Chan, David C ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPA; MITOFUSIN 2;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL TRANSPORT; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE SEVERITY; DOPAMINERGIC NERVE CELL; GENE DELETION; KNOCKOUT GENE; MESENCEPHALON; MITOCHONDRION; MOTOR DYSFUNCTION; MOUSE; NERVE CELL DEGENERATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OPEN FIELD TEST; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN DEPLETION; REARING; STRIATONIGRAL DEGENERATION;

ANIMALS; BIOLOGICAL TRANSPORT; CORPUS STRIATUM; DOPAMINERGIC NEURONS; FEMALE; GENE DELETION; GROWTH CHARTS; GTP PHOSPHOHYDROLASES; LEVODOPA; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MOTOR ACTIVITY; MOVEMENT DISORDERS; PHENOTYPE; RETROGRADE DEGENERATION;

MUS;

EID: 84868127674     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds311     Document Type: Article

References (47)

1. Schapira, A.H., Cooper, J.M., Dexter, D., Jenner, P., Clark, J.B. and Marsden, C.D. (1989) Mitochondrial complex I deficiency in Parkinson's disease. Lancet, 1, 1269.
2. Parker, W.D. Jr and Swerdlow, R.H. (1998) Mitochondrial dysfunction in idiopathic Parkinson disease. Am. J. Hum. Genet., 62, 758-762.
3. Langston, J.W., Ballard, P., Tetrud, J.W. and Irwin, I. (1983) Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science, 219, 979-980.
4. Cannon, J.R. and Greenamyre, J.T. (2010) Neurotoxic in vivo models of Parkinson's disease recent advances. Prog. Brain Res., 184, 17-33.
5. Irrcher, I., Aleyasin, H., Seifert, E.L., Hewitt, S.J., Chhabra, S., Phillips, M., Lutz, A.K., Rousseaux, M.W., Bevilacqua, L., Jahani-Asl, A. et al. (2010) Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics. Hum. Mol. Genet., 19, 3734-3746.
6. 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.
7. 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. USA, 100, 4078-4083.
8. Park, J., Lee, S.B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M., Kim, J.M. et al. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature, 441, 1157-1161.
9. Krebiehl, G., Ruckerbauer, S., Burbulla, L.F., Kieper, N., Maurer, B., Waak, J., Wolburg, H., Gizatullina, Z., Gellerich, F.N., Woitalla, D. et al. (2010) Reduced basal autophagy and impaired mitochondrial dynamics due to loss of Parkinson's disease-associated protein DJ-1. PLoS One, 5, e9367.
10. Wang, X., Yan, M.H., Fujioka, H., Liu, J., Wilson-Delfosse, A., Chen, S.G., Perry, G., Casadesus, G. and Zhu, X. (2012) LRRK2 regulates mitochondrial dynamics and function through direct interaction with DLP1. Hum. Mol. Genet., 21, 1931-1944.
11. Detmer, S.A. and Chan, D.C. (2007) Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol., 8, 870-879.
12. Chen, H. and Chan, D.C. (2009) Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet., 18, R169-R176.
13. Yang, Y., Gehrke, S., Imai, Y., Huang, Z., Ouyang, Y., Wang, J.W., Yang, L., Beal, M.F., Vogel, H. and Lu, B. (2006) Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl Acad. Sci. USA, 103, 10793-10798.
14. Poole, A.C., Thomas, R.E., Andrews, L.A., McBride, H.M., Whitworth, A.J. and Pallanck, L.J. (2008) The PINK1/Parkin pathway regulates mitochondrial morphology. Proc. Natl Acad. Sci. USA, 105, 1638-1643.
15. 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. USA, 105, 7070-7075.
16. Deng, H., Dodson, M.W., Huang, H. and Guo, M. (2008) The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl Acad. Sci. USA, 105, 14503-14508.
17. Tanaka, A., Cleland, M.M., Xu, S., Narendra, D.P., Suen, D.F., Karbowski, M. and Youle, R.J. (2010) Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol., 191, 1367-1380.
18. Twig, G., Elorza, A., Molina, A.J., Mohamed, H., Wikstrom, J.D., Walzer, G., Stiles, L., Haigh, S.E., Katz, S., Las, G. et al. (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J., 27, 433-446.
19. Wang, X., Petrie, T.G., Liu, Y., Liu, J., Fujioka, H. and Zhu, X. (2012) Parkinson's disease-associated DJ-1 mutations impair mitochondrial dynamics and cause mitochondrial dysfunction. J. Neurochem., 121, 830-839.
20. Thomas, K.J., McCoy, M.K., Blackinton, J., Beilina, A., van der Brug, M., Sandebring, A., Miller, D., Maric, D., Cedazo-Minguez, A. and Cookson, M.R. (2011) DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum. Mol. Genet., 20, 40-50.
21. Bäckman, C.M., Malik, N., Zhang, Y., Shan, L., Grinberg, A., Hoffer, B.J., Westphal, H. and Tomac, A.C. (2006) Characterization of a mouse strain expressing Cre recombinase from the 3' untranslated region of the dopamine transporter locus. Genesis, 44, 383-390.
22. Zhou, Q.Y. and Palmiter, R.D. (1995) Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell, 83, 1197-1209.
23. Palmiter, R.D. (2008) Dopamine signaling in the dorsal striatum is essential for motivated behaviors: lessons from dopamine-deficient mice. Ann. N.Y. Acad. Sci., 1129, 35-46.
24. Kish, S.J., Shannak, K. and Hornykiewicz, O. (1988) Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. New Eng. J. Med., 318, 876-880.
25. Stoessl, A.J. (2011) Neuroimaging in Parkinson's disease. Neurotherapeutics, 8, 72-81.
26. Hirsch, E., Graybiel, A.M. and Agid, Y.A. (1988) Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature, 334, 345-348.
27. Damier, P., Hirsch, E.C., Agid, Y. and Graybiel, A.M. (1999) The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain, 122(Pt 8), 1437-1448.
28. Pham, A.H., McCaffery, J.M. and Chan, D.C. (2012) Mouse lines with photo-activatable mitochondria (PhAM) to study mitochondrial dynamics. Genesis, doi:10.1002/dvg.22050. [Epub ahead of print].
29. Gahwiler, B.H., Capogna, M., Debanne, D., McKinney, R.A. and Thompson, S.M. (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci., 20, 471-477.
30. Cho, S., Wood, A. and Bowlby, M.R. (2007) Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Curr. Neuropharmacol., 5, 19-33.
31. Ammari, R., Lopez, C., Fiorentino, H., Gonon, F. and Hammond, C. (2009) A mouse juvenile or adult slice with preserved functional nigro-striatal dopaminergic neurons. Neuroscience, 159, 3-6.
32. Beurrier, C., Ben-Ari, Y. and Hammond, C. (2006) Preservation of the direct and indirect pathways in an in vitro preparation of the mouse basal ganglia. Neuroscience, 140, 77-86.
33. Misgeld, T., Kerschensteiner, M., Bareyre, F.M., Burgess, R.W. and Lichtman, J.W. (2007) Imaging axonal transport of mitochondria in vivo. Nat. Meth., 4, 559-561.
34. Kang, J.S., Tian, J.H., Pan, P.Y., Zald, P., Li, C., Deng, C. and Sheng, Z.H. (2008) Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell, 132, 137-148.
35. Sheng, Z.H. and Cai, Q. (2012) Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat. Rev. Neurosci., 13, 77-93.
36. Hornykiewicz, O. (1998) Biochemical aspects of Parkinson's disease. Neurology, 51, S2-S9.
37. Cheng, H.C., Ulane, C.M. and Burke, R.E. (2010) Clinical progression in Parkinson disease and the neurobiology of axons. Ann. Neurol., 67, 715-725.
38. Pickrell, A.M., Pinto, M., Hida, A. and Moraes, C.T. (2011) Striatal dysfunctions associated with mitochondrial DNA damage in dopaminergic neurons in a mouse model of Parkinson's disease. J Neurosci., 31, 17649-17658.
39. Pifl, C., Schingnitz, G. and Hornykiewicz, O. (1991) Effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on the regional distribution of brain monoamines in the rhesus monkey. Neuroscience, 44, 591-605.
40. Chen, H., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E. and Chan, D.C. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol., 160, 189-200.
41. Misko, A., Jiang, S., Wegorzewska, I., Milbrandt, J. and Baloh, R.H. (2010) Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J Neurosci., 30, 4232-4240.
42. de Brito, O.M. and Scorrano, L. (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature, 456, 605-610.
43. Dawson, T.M., Ko, H.S. and Dawson, V.L. (2010) Genetic animal models of Parkinson's disease. Neuron, 66, 646-661.
44. Chesselet, M.F. and Richter, F. (2011) Modelling of Parkinson's disease in mice. Lancet Neurol., 10, 1108-1118.
45. Ekstrand, M.I., Terzioglu, M., Galter, D., Zhu, S., Hofstetter, C., Lindqvist, E., Thams, S., Bergstrand, A., Hansson, F.S., Trifunovic, A. et al. (2007) Progressive parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc. Natl Acad. Sci. USA, 104, 1325-1330.
46. Sterky, F.H., Lee, S., Wibom, R., Olson, L. and Larsson, N.G. (2011) Impaired mitochondrial transport and Parkin-independent degeneration of respiratory chain-deficient dopamine neurons in vivo. Proc. Natl Acad. Sci. USA, 108, 12937-12942.
47. Chen, H., McCaffery, J.M. and Chan, D.C. (2007) Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell, 130, 548-562.