Acetylcorynoline attenuates dopaminergic neuron degeneration and α-synuclein aggregation in animal models of Parkinson's disease

Neuropharmacology

Volumn 82, Issue , 2014, Pages 108-120

  Fu, Ru Huei ^a,b   Wang, Yu Chi ^c   Chen, Chang Shi ^d   Tsai, Rong Tzong ^e   Liu, Shih Ping ^a,b   Chang, Wen Lin ^a   Lin, Hsin Lien ^a   Lu, Chia Hui ^a   Wei, Jing Rong ^a   Wang, Zih Wan ^a   Shyu, Woei Cherng ^a,b   Lin, Shinn Zong ^a,b,f  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c INDUSTRIAL TECHNOLOGY RESEARCH INSTITUTE   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^f CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

Author keywords

Acetylcorynoline; Caenorhabditis elegans; Dopaminergic neurons; Parkinson's disease; Proteasome; Synuclein

Indexed keywords

ACETYLCORYNOLIN; ALKALOID; ALPHA SYNUCLEIN; ANTIPARKINSON AGENT; CELL PROTEIN; DOPAMINE; OXIDOPAMINE; PROTEASOME; PROTEIN EGL 1; PROTEIN RPN5; UNCLASSIFIED DRUG; ACETYLCORYNOLINE; BERBERINE DERIVATIVE; CAENORHABDITIS ELEGANS PROTEIN; EGL-1 PROTEIN, C ELEGANS; GREEN FLUORESCENT PROTEIN; REPRESSOR PROTEIN; SNCA PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG MECHANISM; DRUG STRUCTURE; ENZYME ACTIVITY; FEEDING BEHAVIOR; LIFESPAN; LIPID COMPOSITION; NERVE CELL DEGENERATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; ANIMAL; APPETITE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MUSCLE CELL; NERVE DEGENERATION; PARKINSONIAN DISORDERS; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ALPHA-SYNUCLEIN; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIPARKINSON AGENTS; APPETITIVE BEHAVIOR; BERBERINE ALKALOIDS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DOPAMINE; DOPAMINERGIC NEURONS; GREEN FLUORESCENT PROTEINS; HUMANS; MOLECULAR STRUCTURE; MUSCLE CELLS; NERVE DEGENERATION; OXIDOPAMINE; PARKINSONIAN DISORDERS; REPRESSOR PROTEINS;

EID: 84901003579     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.08.007     Document Type: Article

References (76)

1. S. Asikainen, M. Rudgalvyte, L. Heikkinen, K. Louhiranta, M. Lakso, G. Wong, and R. Nass Global microRNA expression profiling of Caenorhabditis elegans Parkinson's disease models J. Mol. Neurosci. 41 2010 210 218
2. C.I. Bargmann Neurobiology of the Caenorhabditis elegans genome Science 282 1998 2028 2033 (Pubitemid 29001254)
3. A. Benedetto, C. Au, D.S. Avila, D. Milatovic, and M. Aschner Extracellular dopamine potentiates Mn-induced oxidative stress, lifespan reduction, and dopaminergic neurodegeneration in a BLI-3-dependent manner in Caenorhabditis elegans PLoS Genet. 6 2010 e1001084
4. F. Blandini, and M.T. Armentero Animal models of Parkinson's disease FEBS J. 279 2012 1156 1166
5. R. Bodhicharla, A. Nagarajan, J. Winter, A. Adenle, A. Nazir, D. Brady, K. Vere, J. Richens, P. O'Shea, D.R. Bell, and D. de Pomerai Effects of alpha-synuclein overexpression in transgenic Caenorhabditis elegans strains CNS Neurol. Disord. Drug Targets 11 2012 965 975
6. J. Bove, and C. Perier Neurotoxin-based models of Parkinson's disease Neuroscience 211 2012 51 76
7. S. Brenner The genetics of Caenorhabditis elegans Genetics 77 1974 71 94
8. F. Calahorro, and M. Ruiz-Rubio Caenorhabditis elegans as an experimental tool for the study of complex neurological diseases: Parkinson's disease, Alzheimer's disease and autism spectrum disorder Invert. Neurosci. 11 2011 73 83
9. K.A. Caldwell, M.L. Tucci, J. Armagost, T.W. Hodges, J. Chen, S.B. Memon, J.E. Blalock, S.M. DeLeon, R.H. Findlay, Q. Ruan, P.J. Webber, D.G. Standaert, J.B. Olson, and G.A. Caldwell Investigating bacterial sources of toxicity as an environmental contributor to dopaminergic neurodegeneration PLoS One 4 2009 e7227
10. P. Cao, Y. Yuan, E.A. Pehek, A.R. Moise, Y. Huang, K. Palczewski, and Z. Feng Alpha-synuclein disrupted dopamine homeostasis leads to dopaminergic neuron degeneration in Caenorhabditis elegans PLoS One 5 2010 e9312
11. C. Charriaut-Marlangue Apoptosis: a target for neuroprotection Therapie 59 2004 185 190 (Pubitemid 39024702)
12. A. Ciobica, M. Padurariu, and L. Hritcu The effects of short-term nicotine administration on behavioral and oxidative stress deficiencies induced in a rat model of Parkinson's disease Psychiatr. Danub. 24 2012 194 205
13. M. Coelho, and J.J. Ferreira Late-stage Parkinson disease Nat. Rev. Neurol. 8 2012 435 442
14. L.M. Collins, A. Toulouse, T.J. Connor, and Y.M. Nolan Contributions of central and systemic inflammation to the pathophysiology of Parkinson's disease Neuropharmacology 62 2012 2154 2168
15. E.M. Cornejo Castro, J. Waak, S.S. Weber, F.C. Fiesel, P. Oberhettinger, M. Schutz, I.B. Autenrieth, W. Springer, and P.J. Kahle Parkinson's disease-associated DJ-1 modulates innate immunity signaling in Caenorhabditis elegans J. Neural Transm. 117 2010 599 604
16. H. De Jesus-Cortes, P. Xu, J. Drawbridge, S.J. Estill, P. Huntington, S. Tran, J. Britt, R. Tesla, L. Morlock, J. Naidoo, L.M. Melito, G. Wang, N.S. Williams, J.M. Ready, S.L. McKnight, and A.A. Pieper Neuroprotective efficacy of aminopropyl carbazoles in a mouse model of Parkinson disease Proc. Natl. Acad. Sci. U. S. A. 109 2012 17010 17015
17. R.H. Fu, Y.C. Wang, S.P. Liu, C.L. Chu, R.T. Tsai, Y.C. Ho, W.L. Chang, S.C. Chiu, H.J. Harn, W.C. Shyu, and S.Z. Lin Acetylcorynoline impairs the maturation of mouse bone marrow-derived dendritic cells via suppression of IkappaB kinase and mitogen-activated protein kinase activities PLoS One 8 2013 e58398
18. S. Hamamichi, R.N. Rivas, A.L. Knight, S. Cao, K.A. Caldwell, and G.A. Caldwell Hypothesis-based RNAi screening identifies neuroprotective genes in a Parkinson's disease model Proc. Natl. Acad. Sci. U. S. A. 105 2008 728 733 (Pubitemid 351171776)
19. C. Hansen, and J.Y. Li Beyond alpha-synuclein transfer: pathology propagation in Parkinson's disease Trends Mol. Med. 18 2012 248 255
20. A.J. Harrington, S. Hamamichi, G.A. Caldwell, and K.A. Caldwell C. elegans as a model organism to investigate molecular pathways involved with Parkinson's disease Dev. Dyn. 239 2010 1282 1295
21. A.J. Harrington, A.L. Knight, G.A. Caldwell, and K.A. Caldwell Caenorhabditis elegans as a model system for identifying effectors of alpha-synuclein misfolding and dopaminergic cell death associated with Parkinson's disease Methods 53 2011 220 225
22. A.J. Harrington, T.A. Yacoubian, S.R. Slone, K.A. Caldwell, and G.A. Caldwell Functional analysis of VPS41-mediated neuroprotection in Caenorhabditis elegans and mammalian models of Parkinson's disease J. Neurosci. 32 2012 2142 2153
23. D. Hoogewijs, K. Houthoofd, F. Matthijssens, J. Vandesompele, and J.R. Vanfleteren Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans BMC Mol. Biol. 9 2008 9
24. B.T. Hyman, and J. Yuan Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology Nat. Rev. Neurosci. 13 2012 395 406
25. P. Jadiya, M. Chatterjee, S.R. Sammi, S. Kaur, G. Palit, and A. Nazir Sir-2.1 modulates 'calorie-restriction-mediated' prevention of neurodegeneration in Caenorhabditis elegans: implications for Parkinson's disease Biochem. Biophys. Res. Commun. 413 2011 306 310
26. P. Jadiya, A. Khan, S.R. Sammi, S. Kaur, S.S. Mir, and A. Nazir Anti-Parkinsonian effects of Bacopa monnieri: insights from transgenic and pharmacological Caenorhabditis elegans models of Parkinson's disease Biochem. Biophys. Res. Commun. 413 2011 605 610
27. P. Jadiya, and A. Nazir Environmental toxicants as extrinsic epigenetic factors for Parkinsonism: studies employing transgenic C. elegans model CNS Neurol. Disord. Drug Targets 11 2012 976 983
28. J. Jankovic, and W. Poewe Therapies in Parkinson's disease Curr. Opin. Neurol. 25 2012 433 447
29. F. Kamp, N. Exner, A.K. Lutz, N. Wender, J. Hegermann, B. Brunner, B. Nuscher, T. Bartels, A. Giese, K. Beyer, S. Eimer, K.F. Winklhofer, and C. Haass Inhibition of mitochondrial fusion by alpha-synuclein is rescued by PINK1, Parkin and DJ-1 EMBO J. 29 2010 3571 3589
30. D.P. Karpinar, M.B. Balija, S. Kugler, F. Opazo, N. Rezaei-Ghaleh, N. Wender, H.Y. Kim, G. Taschenberger, B.H. Falkenburger, H. Heise, A. Kumar, D. Riedel, L. Fichtner, A. Voigt, G.H. Braus, K. Giller, S. Becker, A. Herzig, M. Baldus, H. Jackle, S. Eimer, J.B. Schulz, C. Griesinger, and M. Zweckstetter Pre-fibrillar alpha-synuclein variants with impaired beta-structure increase neurotoxicity in Parkinson's disease models EMBO J. 28 2009 3256 3268
31. S. Kaur, S.R. Sammi, P. Jadiya, and A. Nazir RNAi of cat-2, a putative tyrosine hydroxylase, increases alpha synuclein aggregation and associated effects in transgenic C. elegans CNS Neurol. Disord. Drug Targets 11 2012 387 394
32. T. Kuwahara, A. Koyama, K. Gengyo-Ando, M. Masuda, H. Kowa, M. Tsunoda, S. Mitani, and T. Iwatsubo Familial Parkinson mutant alpha-synuclein causes dopamine neuron dysfunction in transgenic Caenorhabditis elegans J. Biol. Chem. 281 2006 334 340 (Pubitemid 43671193)
33. T. Kuwahara, A. Koyama, S. Koyama, S. Yoshina, C.H. Ren, T. Kato, S. Mitani, and T. Iwatsubo A systematic RNAi screen reveals involvement of endocytic pathway in neuronal dysfunction in alpha-synuclein transgenic C. elegans Hum. Mol. Genet. 17 2008 2997 3009
34. T. Kuwahara, R. Tonegawa, G. Ito, S. Mitani, and T. Iwatsubo Phosphorylation of alpha-synuclein protein at Ser-129 reduces neuronal dysfunction by lowering its membrane binding property in Caenorhabditis elegans J. Biol. Chem. 287 2012 7098 7109
35. J.Y. Lee, J. Song, K. Kwon, S. Jang, C. Kim, K. Baek, J. Kim, and C. Park Human DJ-1 and its homologs are novel glyoxalases Hum. Mol. Genet. 21 2012 3215 3225
36. Z. Liu, S. Hamamichi, B.D. Lee, D. Yang, A. Ray, G.A. Caldwell, K.A. Caldwell, T.M. Dawson, W.W. Smith, and V.L. Dawson Inhibitors of LRRK2 kinase attenuate neurodegeneration and Parkinson-like phenotypes in Caenorhabditis elegans and Drosophila Parkinson's disease models Hum. Mol. Genet. 20 2011 3933 3942
37. C.J. Locke, S.A. Fox, G.A. Caldwell, and K.A. Caldwell Acetaminophen attenuates dopamine neuron degeneration in animal models of Parkinson's disease Neurosci. Lett. 439 2008 129 133
38. J.H. Lu, J.Q. Tan, S.S. Durairajan, L.F. Liu, Z.H. Zhang, L. Ma, H.M. Shen, H.Y. Chan, and M. Li Isorhynchophylline, a natural alkaloid, promotes the degradation of alpha-synuclein in neuronal cells via inducing autophagy Autophagy 8 2012 98 108
39. E.J. Martinez-Finley, D.S. Avila, S. Chakraborty, and M. Aschner Insights from Caenorhabditis elegans on the role of metals in neurodegenerative diseases Metallomics 3 2011 271 279
40. R. Nass, D.H. Hall, D.M. Miller 3rd, and R.D. Blakely Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans Proc. Natl. Acad. Sci. U. S. A. 99 2002 3264 3269 (Pubitemid 34240620)
41. R. Nass, K.M. Merchant, and T. Ryan Caenohabditis elegans in Parkinson's disease drug discovery: addressing an unmet medical need Mol. Interv. 8 2008 284 293
42. N.B. Nedelsky, P.K. Todd, and J.P. Taylor Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection Biochim. Biophys. Acta 1782 2008 691 699
43. L. Niu, Z. Xie, T. Cai, P. Wu, P. Xue, X. Chen, Z. Wu, Y. Ito, F. Li, and F. Yang Preparative isolation of alkaloids from Corydalis bungeana Turcz. by high-speed counter-current chromatography using stepwise elution J. Sep. Sci. 34 2011 987 994
44. H. Onishi, and Y. Machida Macromolecular and nanotechnological modification of camptothecin and its analogs to improve the efficacy Curr. Drug Discov. Technol. 2 2005 169 183 (Pubitemid 41242962)
45. I.S. Pienaar, J. Gotz, and M.B. Feany Parkinson's disease: insights from non-traditional model organisms Prog. Neurobiol. 92 2010 558 571
46. E. Pourkarimi, S. Greiss, and A. Gartner Evidence that CED-9/Bcl2 and CED-4/Apaf-1 localization is not consistent with the current model for C. elegans apoptosis induction Cell Death Differ. 19 2012 406 415
47. L. Qian, Z. Xu, W. Zhang, B. Wilson, J.S. Hong, and P.M. Flood Sinomenine, a natural dextrorotatory morphinan analog, is anti-inflammatory and neuroprotective through inhibition of microglial NADPH oxidase J. Neuroinflammation 4 2007 23
48. C. Roodveldt, C.W. Bertoncini, A. Andersson, A.T. van der Goot, S.T. Hsu, R. Fernandez-Montesinos, J. de Jong, T.J. van Ham, E.A. Nollen, D. Pozo, J. Christodoulou, and C.M. Dobson Chaperone proteostasis in Parkinson's disease: stabilization of the Hsp70/alpha-synuclein complex by Hip EMBO J. 28 2009 3758 3770
49. Q. Ruan, A.J. Harrington, K.A. Caldwell, G.A. Caldwell, and D.G. Standaert VPS41, a protein involved in lysosomal trafficking, is protective in Caenorhabditis elegans and mammalian cellular models of Parkinson's disease Neurobiol. Dis. 37 2010 330 338
50. V. Ruiperez, F. Darios, and B. Davletov Alpha-synuclein, lipids and Parkinson's disease Prog. Lipid Res. 49 2010 420 428
51. E.R. Sawin, R. Ranganathan, and H.R. Horvitz C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway Neuron 26 2000 619 631
52. M.A. Schreiber, and S.L. McIntire A Caenorhabditis elegans p38 MAP kinase pathway mutant protects from dopamine, methamphetamine, and MDMA toxicity Neurosci. Lett. 498 2011 99 103
53. V. Shukla, S.C. Phulara, D. Yadav, S. Tiwari, S. Kaur, M.M. Gupta, A. Nazir, and R. Pandey Iridoid compound 10-O-trans-p-Coumaroylcatalpol extends longevity and reduces alpha synuclein aggregation in Caenorhabditis elegans CNS Neurol. Disord. Drug Targets 11 2012 984 992
54. V.V. Shvadchak, D.A. Yushchenko, R. Pievo, and T.M. Jovin The mode of alpha-synuclein binding to membranes depends on lipid composition and lipid to protein ratio FEBS Lett. 585 2011 3513 3519
55. P.K. Sonsalla, L.Y. Wong, S.L. Harris, J.R. Richardson, I. Khobahy, W. Li, B.S. Gadad, and D.C. German Delayed caffeine treatment prevents nigral dopamine neuron loss in a progressive rat model of Parkinson's disease Exp. Neurol. 234 2012 482 487
56. W. Tan, Y. Li, M. Chen, and Y. Wang Berberine hydrochloride: anticancer activity and nanoparticulate delivery system Int. J. Nanomedicine 6 2011 1773 1777
57. Y. Tsuboi Environmental-genetic interactions in the pathogenesis of Parkinson's disease Exp. Neurobiol. 21 2012 123 128
58. M. Tsunoda, K. Takezawa, T. Santa, and K. Imai Simultaneous automatic determination of catecholamines and their 3-O-methyl metabolites in rat plasma by high-performance liquid chromatography using peroxyoxalate chemiluminescence reaction Anal. Biochem. 269 1999 386 392 (Pubitemid 29201040)
59. M.L. Tucci, A.J. Harrington, G.A. Caldwell, and K.A. Caldwell Modeling dopamine neuron degeneration in Caenorhabditis elegans Methods Mol. Biol. 793 2011 129 148
60. M. Usenovic, A.L. Knight, A. Ray, V. Wong, K.R. Brown, G.A. Caldwell, K.A. Caldwell, I. Stagljar, and D. Krainc Identification of novel ATP13A2 interactors and their role in alpha-synuclein misfolding and toxicity Hum. Mol. Genet. 21 2012 3785 3794
61. A.T. van der Goot, W. Zhu, R.P. Vazquez-Manrique, R.I. Seinstra, K. Dettmer, H. Michels, F. Farina, J. Krijnen, R. Melki, R.C. Buijsman, M. Ruiz Silva, K.L. Thijssen, I.P. Kema, C. Neri, P.J. Oefner, and E.A. Nollen Delaying aging and the aging-associated decline in protein homeostasis by inhibition of tryptophan degradation Proc. Natl. Acad. Sci. U. S. A. 109 2012 14912 14917
62. T.J. van Ham, M.A. Holmberg, A.T. van der Goot, E. Teuling, M. Garcia-Arencibia, H.E. Kim, D. Du, K.L. Thijssen, M. Wiersma, R. Burggraaff, P. van Bergeijk, J. van Rheenen, G. Jerre van Veluw, R.M. Hofstra, D.C. Rubinsztein, and E.A. Nollen Identification of MOAG-4/SERF as a regulator of age-related proteotoxicity Cell 142 2010 601 612
63. T.J. van Ham, K.L. Thijssen, R. Breitling, R.M. Hofstra, R.H. Plasterk, and E.A. Nollen C. elegans model identifies genetic modifiers of alpha-synuclein inclusion formation during aging PLoS Genet. 4 2008 e1000027
64. A.G. Vidal-Gadea, and J.T. Pierce-Shimomura Conserved role of dopamine in the modulation of behavior Commun. Integr. Biol. 5 2012 440 447
65. D. Vilchez, I. Morantte, Z. Liu, P.M. Douglas, C. Merkwirth, A.P. Rodrigues, G. Manning, and A. Dillin RPN-6 determines C. elegans longevity under proteotoxic stress conditions Nature 489 2012 263 268
66. C. Voisine, H. Varma, N. Walker, E.A. Bates, B.R. Stockwell, and A.C. Hart Identification of potential therapeutic drugs for huntington's disease using Caenorhabditis elegans PLoS One 2 2007 e504
67. G. Walkinshaw, and C.M. Waters Neurotoxin-induced cell death in neuronal PC12 cells is mediated by induction of apoptosis Neuroscience 63 1994 975 987 (Pubitemid 24366149)
68. H.L. Wei, and G.T. Liu Protective action of corynoline, acetylcorynoline and protopine against experimental liver injury in mice Yao Xue Xue Bao 32 1997 331 336 (Pubitemid 127464113)
69. C. Wu, K. Yang, Q. Liu, M. Wakui, G.Z. Jin, X. Zhen, and J. Wu Tetrahydroberberine blocks ATP-sensitive potassium channels in dopamine neurons acutely-dissociated from rat substantia nigra pars compacta Neuropharmacology 59 2010 567 572
70. C. Xie, N.C. Veitch, P.J. Houghton, and M.S. Simmonds Flavonoid glycosides and isoquinolinone alkaloids from Corydalis bungeana Phytochemistry 65 2004 3041 3047 (Pubitemid 39422301)
71. T.A. Yacoubian, S.R. Slone, A.J. Harrington, S. Hamamichi, J.M. Schieltz, K.A. Caldwell, G.A. Caldwell, and D.G. Standaert Differential neuroprotective effects of 14-3-3 proteins in models of Parkinson's disease Cell Death Dis. 1 2010 e2
72. X. Yang, P. Zhang, J. Wu, S. Xiong, N. Jin, and Z. Huang The neuroprotective and lifespan-extension activities of Damnacanthus officinarum extracts in Caenorhabditis elegans J. Ethnopharmacol. 141 2012 41 47
73. C. Yao, R. El Khoury, W. Wang, T.A. Byrd, E.A. Pehek, C. Thacker, X. Zhu, M.A. Smith, A.L. Wilson-Delfosse, and S.G. Chen LRRK2-mediated neurodegeneration and dysfunction of dopaminergic neurons in a Caenorhabditis elegans model of Parkinson's disease Neurobiol. Dis. 40 2010 73 81
74. H.C. Yen, C. Espiritu, and E.C. Chang Rpn5 is a conserved proteasome subunit and required for proper proteasome localization and assembly J. Biol. Chem. 278 2003 30669 30676 (Pubitemid 36994572)
75. Z. Yu, O. Kleifeld, A. Lande-Atir, M. Bsoul, M. Kleiman, D. Krutauz, A. Book, R.D. Vierstra, K. Hofmann, N. Reis, M.H. Glickman, and E. Pick Dual function of Rpn5 in two PCI complexes, the 26S proteasome and COP9 signalosome Mol. Biol. Cell 22 2011 911 920
76. M. Zheng, O. Gorelenkova, J. Yang, and Z. Feng A liquid phase based C. elegans behavioral analysis system identifies motor activity loss in a nematode Parkinson's disease model J. Neurosci. Methods 204 2012 234 237