Pyrroloquinoline quinone-conferred neuroprotection in rotenone models of Parkinson's disease

Toxicology Letters

Volumn 238, Issue 3, 2015, Pages 70-82

  Qin, Jiaojiao ^a   Wu, Meilong ^a   Yu, Shu ^a   Gao, Xiaorong ^a   Zhang, Jingjing ^a   Dong, Xingyue ^a   Ji, Jinyan ^a   Zhang, Yuxi ^a   Zhou, Lin ^a   Zhang, Qi ^a   Ding, Fei ^a  

^a NANTONG UNIVERSITY   (China)

Author keywords

Dopamine; Neuroprotection; Parkinson's disease (PD); Pyrroloquinoline quinone (PQQ); Reactive oxygen species (ROS); Rotenone

Indexed keywords

APOMORPHINE; DOPAMINE; NDUFS1 PROTEIN; NDUFS2 PROTEIN; NDUFS3 PROTEIN; NDUFS4 PROTEIN; OXIDOREDUCTASE; PROTEIN BAX; PROTEIN BCL 2; PYRROLOQUINOLINEQUINONE; REACTIVE OXYGEN METABOLITE; ROTENONE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TYROSINE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; VESICULAR MONOAMINE TRANSPORTER 2; ANTIOXIDANT; GLUTATHIONE; MALONALDEHYDE; NEUROPROTECTIVE AGENT; SLC18A2 PROTEIN, RAT; SUPEROXIDE DISMUTASE; VESICULAR MONOAMINE TRANSPORTER;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL LOSS; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; EVOKED MUSCLE RESPONSE; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LOW DRUG DOSE; MALE; MEDIAL FOREBRAIN BUNDLE; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL CULTURE; NERVE CELL DEGENERATION; NEUROBLASTOMA CELL; NEUROPROTECTION; NITRATION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; ROTATION; SCAVENGING SYSTEM; ANIMAL; CELL LINE; CELL SURVIVAL; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PARKINSON DISEASE, SECONDARY;

ANIMALS; ANTIOXIDANTS; CELL LINE; CELL SURVIVAL; GENE EXPRESSION REGULATION; GLUTATHIONE; HUMANS; MALONDIALDEHYDE; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE, SECONDARY; PQQ COFACTOR; RATS; ROTENONE; SUPEROXIDE DISMUTASE; TYROSINE 3-MONOOXYGENASE; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 84940854514     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.08.011     Document Type: Article

References (52)

1. Abou-Sleiman P.M., Muqit M.M., Wood N.W. Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat. Rev. Neurosci. 2006, 7:207-219.
2. Alvarez-Fischer D., Fuchs J., Castagner F., Stettler O., Massiani-Beaudoin O., Moya K.L., Bouillot C., Oertel W.H., Lombes A., Faigle W., Joshi R.L., Hartmann A., Prochiantz A. Engrailed protects mouse midbrain dopaminergic neurons against mitochondrial complex I insults. Nat. Neurosci. 2011, 14:1260-1266.
3. Borlongan C.V., Sanberg P.R. Elevated body swing test: a new behavioral parameter for rats with 6-hydroxydopamine-induced hemiparkinsonism. J. Neurosci. 1995, 15:5372-5378.
4. Cannon J.R., Greenamyre J.T. Gene-environment interactions in Parkinson's disease: specific evidence in humans and mammalian models. Neurobiol. Dis. 2013, 57:38-46.
5. Cannon J.R., Tapias V., Na H.M., Honick A.S., Drolet R.E., Greenamyre J.T. A highly reproducible rotenone model of Parkinson's disease. Neurobiol. Dis. 2009, 34:279-290.
6. Chen C.X., Huang S.Y., Zhang L., Liu Y.J. Synaptophysin enhances the neuroprotection of VMAT2 in MPP+-induced toxicity in MN9D cells. Neurobiol. Dis. 2005, 19:419-426.
7. Cheng E., Wei M., Weiler S., Flavell R., Mak T., Lindsten T., Korsmeyer S. BCL-2, BCL-XL sequester BH3 domain-only molecules preventing BAX-and BAK-mediated mitochondrial apoptosis. Mol. Cell. 2001, 8:705-711.
8. Choi W.S., Kruse S.E., Palmiter R.D., Xia Z. Mitochondrial complex I inhibition is not required for dopaminergic neuron death induced by rotenone, MPP+, or paraquat. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15136-15141.
9. Choi W.S., Palmiter R.D., Xia Z. Loss of mitochondrial complex I activity potentiates dopamine neuron death induced by microtubule dysfunction in a Parkinson's disease model. J. Cell Biol. 2011, 192:873-882.
10. Chowanadisai W., Bauerly K.A., Tchaparian E., Wong A., Cortopassi G.A., Rucker R.B. Pyrroloquinoline quinone stimulates mitochondrial biogenesis through cAMP response element-binding protein phosphorylation and increased PGC-1alpha expression. J. Biol. Chem. 2009, 285:142-152.
11. Chung S.J., Armasu S.M., Anderson K.J., Biernacka J.M., Lesnick T.G., Rider D.N., Cunningham J.M., Ahlskog J.E., Frigerio R., Maraganore D.M. Genetic susceptibility loci, environmental exposures, and Parkinson's disease: a case-control study of gene-environment interactions. Parkinsonism Relat. Disord. 2013, 19:595-599.
12. 2+ in cultured frog tectal cells mediated by direct activation of NMDA receptor channels. Neuron 1991, 6:259-267.
13. Felton L.M., Anthony C. Biochemistry: role of PQQ as a mammalian enzyme cofactor?. Nature 2005, 433:E10. discussion E11-12.
14. Giasson B.I., Lee V.M.Y. A new link between pesticides and Parkinson's. Nat. Neurosci. 2000, 3:1227.
15. Giordano S., Lee J., Darley-Usmar V.M., Zhang J. Distinct effects of rotenone, 1-methyl-4-phenylpyridinium and 6-hydroxydopamine on cellular bioenergetics and cell death. PLoS One 2012, 7:e44610.
16. Gross A., Jockel J., Wei M., Korsmeyer S. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 1998, 17:3878-3885.
17. Hara H., Hiramatsu H., Adachi T. Pyrroloquinoline quinone is a potent neuroprotective nutrient against 6-hydroxydopamine-induced neurotoxicity. Neurochem. Res. 2007, 32:489-495.
18. Harrington K.A., Augood S.J., Kingsbury A.E., Foster O.J., Emson P.C. Dopamine transporter (Dat) and synaptic vesicle amine transporter (VMAT2) gene expression in the substantia nigra of control and Parkinson's disease. Brain Res. Mol. Brain Res. 1996, 36:157-162.
19. Hauge J.G. Glucose dehydrogenase of Bacterium Anitratum: an enzyme with a Novel Prosthetic Group. J. Biol. Chem. 1964, 239:3630-3639.
20. Hobara N., Watanabe A., Kobayashi M., Tsuji T., Gomita Y., Araki Y. Quinone derivatives lower blood and liver acetaldehyde but not ethanol concentrations following ethanol loading to rats. Pharmacology 1988, 37:264-267.
21. Jankovic J., Poewe W. Therapies in Parkinson's disease. Curr. Opin. Neurobiol. 2012, 25:433-447.
22. Jurgensmeier J.M., Xie Z., Deveraux Q., Ellerby L., Bredesen D., Reed J.C. Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:4997-5002.
23. Kasahara T., Kato T. Nutritional biochemistry: A new redox-cofactor vitamin for mammals. Nature 2003, 422:832.
24. Liu Y., Schubert D.R. The specificity of neuroprotection by antioxidants. J. Biomed. Sci. 2009, 16:98.
25. Ly J.D., Grubb D.R., Lawen A. The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis 2003, 8:115-128.
26. Mariani E., Polidori M.C., Cherubini A., Mecocci P. Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview. J. Chromatogr. B 2005, 827:65-75.
27. Miller G.W., Erickson J.D., Perez J.T., Penland S.N., Mash D.C., Rye D.B., Levey A.I. Immunochemical analysis of vesicular monoamine transporter (VMAT2) protein in Parkinson's disease. Exp. Neurol. 1999, 156:138-148.
28. Misra H.S., Khairnar N.P., Barik A., Indira Priyadarsini K., Mohan H., Apte S.K. Pyrroloquinoline-quinone: a reactive oxygen species scavenger in bacteria. FEBS Lett. 2004, 578:26-30.
29. Misra H.S., Rajpurohit Y.S., Khairnar N.P. Pyrroloquinoline-quinone and its versatile roles in biological processes. J. Biosci. 2012, 37:313-325.
30. Ohwada K., Takeda H., Yamazaki M., Isogai H., Nakano M., Shimomura M., Fukui K., Urano S. Pyrroloquinoline quinone (PQQ) prevents cognitive deficit caused by oxidative stress in rats. J. Clin. Biochem. Nutr. 2008, 42:29-34.
31. Panov A., Dikalov S., Shalbuyeva N., Taylor G., Sherer T., Greenamyre J.T. Rotenone model of Parkinson disease: multiple brain mitochondria dysfunctions after short term systemic rotenone intoxication. J. Biol. Chem. 2005, 280:42026-42035.
32. Park S.E., Sapkota K., Choi J.H., Kim M.K., Kim Y.H., Kim K.M., Kim K.J., Oh H.N., Kim S.J., Kim S. Rutin from Dendropanax morbifera Leveille protects human dopaminergic cells against rotenone induced cell injury through inhibiting JNK and p38 MAPK signaling. Neurochem. Res. 2014, 39:707-718.
33. Parsons R.B., Aravindan S., Kadampeswaran A., Evans E.A., Sandhu K.K., Levy E.R., Thomas M.G., Austen B.M., Ramsden D.B. The expression of nicotinamide N-methyltransferase increases ATP synthesis and protects SH-SY5Y neuroblastoma cells against the toxicity of Complex I inhibitors. Biochem. J. 2011, 436:145-155.
34. Rucker R., Chowanadisai W., Nakano M. Potential physiological importance of pyrroloquinoline quinone. Altern. Med. Rev. 2009, 14:268-277.
35. Rucker R., Storms D., Sheets A., Tchaparian E., Fascetti A. Biochemistry: is pyrroloquinoline quinone a vitamin?. Nature 2005, 433:E10-E11. discussion E11-12.
36. Salisbury S.A., Forrest H.S., Cruse W.B., Kennard O. A novel coenzyme from bacterial primary alcohol dehydrogenases. Nature 1979, 280:843-844.
37. Sanders L.H., Timothy Greenamyre J. Oxidative damage to macromolecules in human Parkinson disease and the rotenone model. Free Radic. Biol. Med. 2013, 62:111-120.
38. Scacco S., Petruzzella V., Budde S., Vergari R., Tamborra R., Panelli D., van den Heuvel L.P., Smeitink J.A., Papa S. Pathological mutations of the human NDUFS4 gene of the 18-kDa (AQDQ) subunit of complex I affect the expression of the protein and the assembly and function of the complex. J. Biol. Chem. 2003, 278:44161-44167.
39. Sherer T.B., Betarbet R., Testa C.M., Seo B.B., Richardson J.R., Kim J.H., Miller G.W., Yagi T., Matsuno-Yagi A., Greenamyre J.T. Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 2003, 23:10756-10764.
40. 2+-induced oxidative stress in brain mitochondria treated with the respiratory chain inhibitor rotenone. FEBS Lett. 2003, 543:179-183.
41. Stites T.E., Mitchell A.E., Rucker R.B. Physiological importance of quinoenzymes and the O-quinone family of cofactors. J. Nutr. 2000, 130:719-727.
42. Tao R., Karliner J.S., Simonis U., Zheng J., Zhang J., Honbo N., Alano C.C. Pyrroloquinoline quinone preserves mitochondrial function and prevents oxidative injury in adult rat cardiac myocytes. Biochem. Biophys. Res. Commun. 2007, 363:257-262.
43. Wang X.J., Xu J.X. Possible involvement of Ca2+ signaling in rotenone-induced apoptosis in human neuroblastoma SH-SY5Y cells. Neurosci. Lett. 2005, 376:127-132.
44. Watabe M., Nakaki T. Mitochondrial complex I inhibitor rotenone-elicited dopamine redistribution from vesicles to cytosol in human dopaminergic SH-SY5Y cells. J. Pharmacol. Exp. Ther. 2007, 323:499-507.
45. Watabe M., Nakaki T. Mitochondrial complex I inhibitor rotenone inhibits and redistributes vesicular monoamine transporter 2 via nitration in human dopaminergic SH-SY5Y cells. Mol. Pharmacol. 2008, 74:933-940.
46. Xu Q., Dou J., Wei P., Tan C., Yun X., Wu Y., Bai X., Ma X., Du Y. Chitooligosaccharides induce apoptosis of human hepatocellular carcinoma cells via up-regulation of Bax. Carbohydr. Polym. 2008, 71:509-514.
47. Xu S., Zhong W., Watson N., Dickerson E., Wake J., Lindow S., Newton C., Atkin S. Fluvastatin reduces oxidative damage in human vascular endothelial cells by upregulating Bcl-2. J. Thromb. Haemost. 2008, 6:692-700.
48. Zhang Q., Ding M., Cao Z., Zhang J., Ding F., Ke K. Pyrroloquinoline quinine protects rat brain cortex against acute glutamate-induced neurotoxicity. Neurochem. Res. 2013, 38:1661-1671.
49. Zhang Q., Ding M., Gao X.R., Ding F. Pyrroloquinoline quinone rescues hippocampal neurons from glutamate-induced cell death through activation of Nrf2 and up-regulation of antioxidant genes. Genet. Mol. Res. 2012, 11:2652-2664.
50. Zhang Q., Shen M., Ding M., Shen D., Ding F. The neuroprotective action of pyrroloquinoline quinone against glutamate-induced apoptosis in hippocampal neurons is mediated through the activation of PI3K/Akt pathway. Toxicol. Appl. Pharmacol. 2011, 252:62-72.
51. Zhang Q., Zhang J., Jiang C., Qin J., Ke K., Ding F. Involvement of ERK1/2 pathway in neuroprotective effects of pyrroloquinoline quinine against rotenone-induced SH-SY5Y cell injury. Neuroscience 2014, 270:183-191.
52. Zhu B.Q., Zhou H.Z., Teerlink J.R., Karliner J.S. Pyrroloquinoline quinone (PQQ) decreases myocardial infarct size and improves cardiac function in rat models of ischemia and ischemia/reperfusion. Cardiovasc. Drugs Ther. 2004, 18:421-431.