Parkin-induced defects in neurophysiology and locomotion are generated by metabolic dysfunction and not oxidative stress

Human Molecular Genetics

Volumn 21, Issue 8, 2012, Pages 1760-1769

  Vincent, Amanda ^a   Briggs, Laura ^a   Chatwin, Griff F J ^a   Emery, Elizabeth ^a   Tomlins, Rose ^a   Oswald, Matt ^a,b   Middleton, C Adam ^a   Evans, Gareth J O ^a   Sweeney, Sean T ^a   Elliott, Christopher J H ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; LACTIC ACID; PARKIN; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; BRADYKINESIA; CONTROLLED STUDY; DEPOLARIZATION; DROSOPHILA; ENERGY YIELD; EXCITATORY JUNCTION POTENTIAL; GENE OVEREXPRESSION; GLYCOLYSIS; LARVA; LOCOMOTION; MEMBRANE STEADY POTENTIAL; METABOLIC DISORDER; MITOCHONDRIAL RESPIRATION; MOTONEURON; MOTOR DYSFUNCTION; MUSCLE CONTRACTION; NEUROLOGIC DISEASE; NEUROMUSCULAR SYNAPSE; NEUROPHYSIOLOGY; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PARKINSON DISEASE; PERISTALSIS; PHENOTYPE; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANIMALS; CATALASE; DROSOPHILA; DROSOPHILA PROTEINS; ENERGY METABOLISM; GLYCOLYSIS; LARVA; LOCOMOTION; MEMBRANE POTENTIALS; MITOCHONDRIA; MUSCLE CONTRACTION; NEURONS; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRESYNAPTIC TERMINALS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; SYNAPTIC POTENTIALS; UBIQUITIN-PROTEIN LIGASES;

PARKINSONIA;

EID: 84859233375     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr609     Document Type: Article

References (44)

1. Hardy, J. (2010) Genetic analysis of pathways to Parkinson disease. Neuron, 68, 201-206.
2. Dawson, T.M., Ko, H.S. and Dawson, V.L. (2010) Genetic animal models of Parkinson's disease. Neuron, 66, 646-661.
3. Whitworth, A.J. (2011) Drosophila models of Parkinson's disease. Adv. Genet., 73, 1-50.
4. Lu, B. (2009) Recent advances in using Drosophila to model neurodegenerative diseases. Apoptosis, 14, 1008-1020.
5. Botella, J.A., Bayersdorfer, F., Gmeiner, F. and Schneuwly, S. (2009) Modelling Parkinson's disease in Drosophila. NeuroMol. Med., 11, 268-280.
6. Venken, K., Simpson, J. and Bellen, H. (2011) Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron, 72, 202-230.
7. Tain, L.S., Mortiboys, H., Tao, R.N., Ziviani, E., Bandmann, O. and Whitworth, A.J. (2009) Rapamycin activation of 4E-BP prevents Parkinsonian dopaminergic neuron loss. Nat. Neurosci., 12, 1129-1135.
8. Budnik, V. and Ruiz-Canada, C. (2006) The fly neuromuscular junction: structure and function, 2nd edn. Academic Press, San Diego, CA, USA.
9. Pesah, Y., Pham, T., Burgess, H., Middlebrooks, B., Verstreken, P., Zhou, Y., Harding, M., Bellen, H. and Mardon, G. (2004) Drosophila parkin mutants have decreased mass and cell size and increased sensitivity to oxygen radical stress. Development, 131, 2183-2194.
10. Meulener, M., Whitworth, A.J., Armstrong-Gold, C.E., Rizzu, P., Heutink, P., Wes, P.D., Pallanck, L.J. and Bonini, N.M. (2005) Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease. Curr. Biol., 15, 1572-1577.
11. Whitworth, A.J., Theodore, D.A., Greene, J.C., Benes, H., Wes, P.D. and Pallanck, L.J. (2005) Increased glutathione S-transferase activity rescues dopaminergic neuron loss in a Drosophila model of Parkinson's disease. Proc. Natl Acad. Sci. USA, 102, 8024-8029.
12. Im, J.Y., Lee, K.W., Junn, E. and Mouradian, M.M. (2010) DJ-1 protects against oxidative damage by regulating the thioredoxin/ASK1 complex. Neurosci. Res., 67, 203-208.
13. Umeda-Kameyama, Y., Tsuda, M., Ohkura, C., Matsuo, T., Namba, Y., Ohuchi, Y. and Aigaki, T. (2007) Thioredoxin suppresses Parkin-associated endothelin receptor-like receptor-induced neurotoxicity and extends longevity in Drosophila. J. Biol. Chem., 282, 11180-11187.
14. Botella, J.A., Bayersdorfer, F. and Schneuwly, S. (2008) Superoxide dismutase overexpression protects dopaminergic neurons in a Drosophila model of Parkinson's disease. Neurobiol. Dis., 30, 65-73.
15. Shen, W. and Ganetzky, B. (2009) Autophagy promotes synapse development in Drosophila. J. Cell. Biol., 187, 71-79.
16. Milton, V.J., Jarrett, H.E., Gowers, K., Chalak, S., Briggs, L., Robinson, I.M. and Sweeney, S.T. (2011) Oxidative stress induces overgrowth of the Drosophila neuromuscular junction. Proc. Natl Acad. Sci. USA, 108, 17521-17526.
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. USA, 100, 4078-4083.
18. Bellen, H.J., Tong, C. and Tsuda, H. (2010) 100 years of Drosophila research and its impact on vertebrate neuroscience: a history lesson for the future. Nat. Rev. Neurosci., 11, 514-522.
19. Kurdyak, P., Atwood, H.L., Stewart, B.A. and Wu, C.F. (1994) Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J. Comp. Neurol., 350, z463-472.
20. 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.
21. Sang, T.K., Chang, H.Y., Lawless, G.M., Ratnaparkhi, A., Mee, L., Ackerson, L.C., Maidment, N.T., Krantz, D.E. and Jackson, G.R. (2007) A Drosophila model of mutant human Parkin-induced toxicity demonstrates selective loss of dopaminergic neurons and dependence on cellular dopamine. J. Neurosci., 27, 981-992.
22. Cha, G.H., Kim, S., Park, J., Lee, E., Kim, M., Lee, S.B., Kim, J.M., Chung, J. and Cho, K.S. (2005) Parkin negatively regulates JNK pathway in the dopaminergic neurons of Drosophila. Proc. Natl Acad. Sci. USA, 102, 10345-10350.
23. Saini, N. and Schaffner, W. (2010) Zinc supplement greatly improves the condition of parkin mutant Drosophila. Biol. Chem., 391, 513-518.
24. Saini, N., Oelhafen, S., Hua, H., Georgiev, O., Schaffner, W. and Bueler, H. (2010) Extended lifespan of Drosophila parkin mutants through sequestration of redox-active metals enhancement of anti-oxidative pathways. Neurobiol. Dis., 40, 82-92.
25. Feany, M.B. and Bender, W.W. (2000) A Drosophila model of Parkinson's disease. Nature, 404, 394-398.
26. Pulver, S.R. and Griffith, L.C. (2010) Spike integration and cellular memory in a rhythmic network from Na+/K+ pump current dynamics. Nat. Neurosci., 13, 53-59.
27. Simon, A.F., Daniels, R., Romero-Calderon, R., Grygoruk, A., Chang, H.Y., Najibi, R., Shamouelian, D., Salazar, E.D., Solomon, M., Ackerson, L.C. et al. (2009) Drosophila vesicular monoamine transporter mutants can adapt to reduced or eliminated vesicular stores of dopamine and serotonin. Genetics, 181, 525-541.
28. Trempe, J.F., Chen, C.X.Q., Grenier, K., Camacho, E.M., Kozlov, G., McPherson, P.S., Gehring, K. and Fon, E.A. (2009) SH3 domains from a subset of BAR proteins define a Ubl-binding domain and implicate Parkin in synaptic ubiquitination. Mol. Cell., 36, 1034-1047.
29. Perez, F.A. and Palmiter, R.D. (2005) Parkin-deficient mice are not a robust model of parkinsonism. Proc. Natl Acad. Sci. USA, 102, 2174.
30. Kitada, T., Pisani, A., Karouani, M., Haburcak, M., Martella, G., Tscherter, A., Platania, P., Wu, B., Pothos, E.N. and Shen, J. (2009) Impaired dopamine release and synaptic plasticity in the striatum of Parkin-/- mice. J. Neurochem., 110, 613-621.
31. Lee, S., Liu, H.P., Lin, W.Y., Guo, H. and Lu, B. (2010) LRRK2 kinase regulates synaptic morphology through distinct substrates at the presynaptic and postsynaptic compartments of the Drosophila neuromuscular junction. J. Neurosci., 30, 16959-16969.
32. Mortiboys, H., Thomas, K.J., Koopman, W.J.H., Klaffke, S., bou-Sleiman, P., Olpin, S., Wood, N.W., Willems, P.H.G.M., Smeitink, J.A.M. and Cookson, M.R. (2008) Mitochondrial function and morphology are impaired in parkin-mutant fibroblasts. Ann. Neurol., 64, 555-565.
33. Liss, B., Haeckel, O., Wildmann, J., Miki, T., Seino, S. and Roeper, J. (2005) K-ATP channels promote the differential degeneration of dopaminergic midbrain neurons. Nat. Neurosci., 8, 1742-1751.
34. Wang, P., Saraswati, S., Guan, Z., Watkins, C.J., Wurtman, R.J. and Littleton, J.T. (2004) A Drosophila temperature-sensitive seizure mutant in phosphoglycerate kinase disrupts ATP generation and alters synaptic function. J. Neurosci., 24, 4518.
35. Ziviani, E., Tao, R.N. and Whitworth, A.J. (2010) Drosophila Parkin requires PINK1 for mitochondrial translocation and ubiquitinates Mitofusin. Proc. Natl Acad. Sci. USA, 107, 5018.
36. Bowen, B.C., Block, R.E., Sanchez-Ramos, J., Pattany, P.M., Lampman, D.A., Murdoch, J.B. and Quencer, R.M. (1995) Proton MR spectroscopy of the brain in 14 patients with Parkinson disease. Am. J. Neuroradiol., 16, 61-68.
37. Yamamoto, M., Ujike, H., Wada, K. and Tsuji, T. (1997) Cerebrospinal fluid lactate and pyruvate concentrations in patients with Parkinson's disease and mitochondrial encephalomyopathy, lactic acidosis, and stroke-like episodes (MELAS). J. Neurol. Neurosurg. Psych., 62, 290.
38. Ross, J.M., Oberg, J., Brene, S., Coppotelli, G., Terzioglu, M., Pernold, K., Goiny, M., Sitnikov, R., Kehr, J., Trifunovic, A. et al. (2010) High brain lactate is a hallmark of aging and caused by a shift in the lactate dehydrogenase A/B ratio. Proc. Natl Acad. Sci. USA, 107, 20087-20092.
39. Parkinson Study Group. (1993) Effects of tocopherol and deprenyl on the progression of disability in early Parkinson's disease. N. Engl. J. Med., 328, 176-183.
40. Löhle, M. and Reichmann, H. (2010) Clinical neuroprotection in Parkinson's disease: still waiting for the breakthrough. J. Neurol. Sci., 289, 104-114.
41. Hill, J.A. (2008) The roles of tyramine and octopamine in Drosophila melanogaster. PhD Thesis, University of York.
42. Klopfenstein, D.R. and Vale, R.D. (2004) The lipid binding pleckstrin homology domain in UNC-104 kinesin is necessary for synaptic vesicle transport in Caenorhabditis elegans. Mol. Biol. Cell., 15, 3729-3739.
43. Stewart, B.A., Atwood, H.L., Renger, J.J., Wang, J. and Wu, C.F. (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. physiol. A, 175, 179-191.
44. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.