Neuroprotective effects of the andrographolide analogue AL-1 in the MPP+/MPTP-induced Parkinson's disease model in vitro and in mice

Pharmacology Biochemistry and Behavior

Volumn 122, Issue , 2014, Pages 191-202

  Zhang, Zaijun ^a   Lai, Daoxu ^a   Wang, Liang ^b   Yu, Pei ^a   Zhu, Longjun ^a   Guo, Baojian ^a   Xu, Lipeng ^a   Zhou, Libing ^a   Sun, Yewei ^a   Lee, Simon Ming Yuen ^b,c   Wang, Yuqiang ^a  

^a JINAN UNIVERSITY   (China)

^b China jack1987168 163com   (Macao)

^c University of Macau   (Macao)

Author keywords

Andrographolide lipoic acid conjugate; Neuroprotection; NF B p65; Parkinson's disease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 1,1 DIPHENYL 2 PICRYLHYDRAZYL; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 3,4 DIHYDROXYPHENYLACETIC ACID; ANDROGRAPHOLIDE; ANDROGRAPHOLIDE LIPOIC ACID CONJUGATE 1; DOPAMINE; I KAPPA B KINASE ALPHA; MALONALDEHYDE; NITRIC OXIDE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR RELA; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; AL 1 SPIROKETAL ENOL ETHER EPOXIDE; DITERPENE; NEUROPROTECTIVE AGENT; PYRAN DERIVATIVE; SPIRO COMPOUND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR CHANGE; BEHAVIOR DISORDER; CELL DAMAGE; CELL VIABILITY; CEREBELLAR GRANULE NEURON; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DOPAMINERGIC NERVE CELL; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MPTP-INDUCED PARKINSONISM; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SUBSTANTIA NIGRA; UPREGULATION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; DISEASE MODEL; DOSE RESPONSE; METABOLISM; MPTP POISONING; PARKINSON DISEASE, SECONDARY; RAT; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DITERPENES; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MALE; MICE; MICE, INBRED C57BL; MPTP POISONING; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE, SECONDARY; PYRANS; RATS; RATS, SPRAGUE-DAWLEY; SPIRO COMPOUNDS;

EID: 84899547718     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2014.03.028     Document Type: Article

References (65)

1. A.A. Abdin, and N.I. Sarhan Intervention of mitochondrial dysfunction-oxidative stress-dependent apoptosis as a possible neuroprotective mechanism of alpha-lipoic acid against rotenone-induced parkinsonism and L-dopa toxicity Neurosci Res 71 2011 387 395
2. A.A. Abu-Ghefreh, H. Canatan, and C.I. Ezeamuzie In vitro and in vivo anti-inflammatory effects of andrographolide Int Immunopharmacol 9 2009 313 318
3. E. Amroyan, E. Gabrielian, A. Panossian, G. Wikman, and H. Wagner Inhibitory effect of andrographolide from Andrographis paniculata on PAF-induced platelet aggregation Phytomedicine 6 1999 27 31 (Pubitemid 129632490)
4. Z. Bao, S. Guan, C. Cheng, S. Wu, S.H. Wong, and D.M. Kemeny et al. A novel antiinflammatory role for andrographolide in asthma via inhibition of the nuclear factor-kappaB pathway Am J Respir Crit Care Med 179 2009 657 665
5. M.L. Block, L. Zecca, and J.S. Hong Microglia-mediated neurotoxicity: uncovering the molecular mechanisms Nat Rev Neurosci 8 2007 57 69 (Pubitemid 46011999)
6. D. Blum, S. Torch, N. Lambeng, M.F. Nissou, A.L. Benabid, and R. Sadoul et al. Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease Prog Neurobiol 65 2001 135 172 (Pubitemid 32524182)
7. J.P. Bolanos, S. Peuchen, S.J. Heales, J.M. Land, and J.B. Clark Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes J Neurochem 63 1994 910 916 (Pubitemid 24266603)
8. S.J. Chan, W.S. Wong, P.T. Wong, and J.S. Bian Neuroprotective effects of andrographolide in a rat model of permanent cerebral ischaemia Br J Pharmacol 161 2010 668 679
9. J.X. Chen, H.J. Xue, W.C. Ye, B.H. Fang, Y.H. Liu, and S.H. Yuan et al. Activity of andrographolide and its derivatives against influenza virus in vivo and in vitro Biol Pharm Bull 32 2009 1385 1391
10. C.S. Chuang, H.L. Su, F.C. Cheng, S.H. Hsu, C.F. Chuang, and C.S. Liu Quantitative evaluation of motor function before and after engraftment of dopaminergic neurons in a rat model of Parkinson's disease J Biomed Sci 17 2010 9
11. S. Gal, H. Zheng, M. Fridkin, and M.B. Youdim Novel multifunctional neuroprotective iron chelator-monoamine oxidase inhibitor drugs for neurodegenerative diseases. In vivo selective brain monoamine oxidase inhibition and prevention of MPTP-induced striatal dopamine depletion J Neurochem 95 2005 79 88 (Pubitemid 41384427)
12. H.M. Gao, B. Liu, W. Zhang, and J.S. Hong Novel anti-inflammatory therapy for Parkinson's disease Trends Pharmacol Sci 24 2003 395 401 (Pubitemid 36952555)
13. M.T. Ge, S.B. Rananavare, and J.H. Freed ESR studies of stearic acid binding to bovine serum albumin Biochim Biophys Acta 1036 1990 228 236
14. S. Hayley, S.J. Crocker, P.D. Smith, T. Shree, V. Jackson-Lewis, and S. Przedborski et al. Regulation of dopaminergic loss by Fas in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease J Neurosci 24 2004 2045 2053 (Pubitemid 38292818)
15. X.J. He, H. Yamauchi, K. Uetsuka, and H. Nakayama Neurotoxicity of MPTP to migrating neuroblasts: studies in acute and subacute mouse models of Parkinson's disease Neurotoxicology 29 2008 413 420
16. M.A. Hidalgo, A. Romero, J. Figueroa, P. Cortes, I.I. Concha, and J.L. Hancke et al. Andrographolide interferes with binding of nuclear factor-kappaB to DNA in HL-60-derived neutrophilic cells Br J Pharmacol 144 2005 680 686 (Pubitemid 40445616)
17. L.A. Holcomb, M. Dhanasekaran, A.R. Hitt, K.A. Young, M. Riggs, and B.V. Manyam Bacopa monniera extract reduces amyloid levels in PSAPP mice J Alzheimers Dis 9 2006 243 251 (Pubitemid 44253342)
18. O. Hornykiewicz, and S.J. Kish Biochemical pathophysiology of Parkinson's disease Adv Neurol 45 1987 19 34
19. C.Y. Hsieh, M.J. Hsu, G. Hsiao, Y.H. Wang, C.W. Huang, and S.W. Chen et al. Andrographolide enhances nuclear factor-kappaB subunit p65 Ser536 dephosphorylation through activation of protein phosphatase 2A in vascular smooth muscle cells J Biol Chem 286 2011 5942 5955
20. A.Y. Hung, and M.A. Schwarzschild Clinical trials for neuroprotection in Parkinson's disease: overcoming angst and futility? Curr Opin Neurol 20 2007 477 483 (Pubitemid 47051997)
21. S. Hunot, F. Boissiere, B. Faucheux, B. Brugg, A. Mouatt-Prigent, and Y. Agid et al. Nitric oxide synthase and neuronal vulnerability in Parkinson's disease Neuroscience 72 1996 355 363 (Pubitemid 26111202)
22. S. Hunot, B. Brugg, D. Ricard, P.P. Michel, M.P. Muriel, and M. Ruberg et al. Nuclear translocation of NF-kappaB is increased in dopaminergic neurons of patients with parkinson disease Proc Natl Acad Sci U S A 94 1997 7531 7536 (Pubitemid 27345350)
23. J.A. Hutter-Saunders, H.E. Gendelman, and R.L. Mosley Murine motor and behavior functional evaluations for acute 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine (MPTP) intoxication J Neuroimmune Pharmacol 7 2012 279 288
24. V. Jackson-Lewis, and S. Przedborski Protocol for the MPTP mouse model of Parkinson's disease Nat Protoc 2 2007 141 151 (Pubitemid 47044700)
25. M. Jalali-Nadoushan, and M. Roghani Alpha-lipoic acid protects against 6-hydroxydopamine-induced neurotoxicity in a rat model of hemi-parkinsonism Brain Res 1505 2013 68 74
26. X. Jiang, P. Yu, J. Jiang, Z. Zhang, Z. Wang, and Z. Yang et al. Synthesis and evaluation of antibacterial activities of andrographolide analogues Eur J Med Chem 44 2009 2936 2943
27. J.W. Langston, P. Ballard, J.W. Tetrud, and I. Irwin Chronic parkinsonism in humans due to a product of meperidine-analog synthesis Science 219 1983 979 980 (Pubitemid 13189531)
28. H.A. Lee, and D.A. Hughes Alpha-lipoic acid modulates NF-kappaB activity in human monocytic cells by direct interaction with DNA Exp Gerontol 37 2002 401 410 (Pubitemid 34073558)
29. Y. Levites, O. Weinreb, G. Maor, M.B. Youdim, and S. Mandel Green tea polyphenol (-)-epigallocatechin-3-gallate prevents N-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-induced dopaminergic neurodegeneration J Neurochem 78 2001 1073 1082 (Pubitemid 32823156)
30. W. Li, R. Pi, H.H.N. Chan, H. Fu, N.T.K. Lee, and H.W. Tsang et al. Novel dimeric acetylcholinesterase inhibitor bis (7)-tacrine, but not donepezil, prevents glutamate-induced neuronal apoptosis by blocking N-methyl-d-aspartate receptors J Biol Chem 280 2005 18179 18188 (Pubitemid 41389063)
31. M.T. Lin, and M.F. Beal Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases Nature 443 2006 787 795 (Pubitemid 44622683)
32. L. Ma, X. Liu, H. Liang, Y. Che, C. Chen, and H. Dai et al. Effects of 14-alpha-lipoyl andrographolide on quorum sensing in Pseudomonas aeruginosa Antimicrob Agents Chemother 56 2012 6088 6094
33. L.K. Mischley, J. Allen, and R. Bradley Coenzyme Q10 deficiency in patients with Parkinson's disease J Neurol Sci 318 2012 72 75
34. T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J Immunol Methods 65 1983 55 63 (Pubitemid 14203433)
35. T. Nagatsu, and M. Sawada Inflammatory process in Parkinson's disease: role for cytokines Curr Pharm Des 11 2005 999 1016 (Pubitemid 40331301)
36. A.B. Nathens, M.J. Neff, G.J. Jurkovich, P. Klotz, K. Farver, and J.T. Ruzinski et al. Randomized, prospective trial of antioxidant supplementation in critically ill surgical patients Ann Surg 236 2002 814
37. A. Puri, R. Saxena, R.P. Saxena, K.C. Saxena, V. Srivastava, and J.S. Tandon Immunostimulant agents from Andrographis paniculata J Nat Prod 56 1993 995 999 (Pubitemid 23222198)
38. M. Roxas, and J. Jurenka Colds and influenza: a review of diagnosis and conventional, botanical, and nutritional considerations Altern Med Rev 12 2007 25 48 (Pubitemid 46668726)
39. N. Schmidt, and B. Ferger Neurochemical findings in the MPTP model of Parkinson's disease J Neural Transm 108 2001 1263 1282 (Pubitemid 33141302)
40. C.K. Sen Cellular thiols and redox-regulated signal transduction Curr Top Cell Regul 36 2000 1 30
41. Y.C. Shen, C.F. Chen, and W.F. Chiou Andrographolide prevents oxygen radical production by human neutrophils: possible mechanism(s) involved in its anti-inflammatory effect Br J Pharmacol 135 2002 399 406
42. Y. Sun, P. Yu, G. Zhang, L. Wang, H. Zhong, and Z. Zhai et al. Therapeutic effects of tetramethylpyrazine nitrone in rat ischemic stroke models J Neurosci Res 90 2012 1662 1669
43. Y. Sun, G. Zhang, Z. Zhang, P. Yu, H. Zhong, and J. Du et al. Novel multi-functional nitrones for treatment of ischemic stroke Bioorg Med Chem 20 2012 3939 3945
44. P. Teismann, and J.B. Schulz Cellular pathology of Parkinson's disease: astrocytes, microglia and inflammation Cell Tissue Res 318 2004 149 161 (Pubitemid 39362635)
45. K.F. Tipton, and T.P. Singer The radiochemical assay for monoamine oxidase activity. Problems and pitfalls Biochem Pharmacol 46 1993 1311
46. C. Vandeputte, J.M. Taymans, C. Casteels, F. Coun, Y. Ni, and K. Van Laere et al. Automated quantitative gait analysis in animal models of movement disorders BMC Neurosci 11 2010 92
47. R. Vlamings, V. Visser-Vandewalle, G. Koopmans, E.A. Joosten, R. Kozan, and S. Kaplan et al. High frequency stimulation of the subthalamic nucleus improves speed of locomotion but impairs forelimb movement in parkinsonian rats Neuroscience 148 2007 815 823 (Pubitemid 47418373)
48. T. Wang, B. Liu, W. Zhang, B. Wilson, and J.S. Hong Andrographolide reduces inflammation-mediated dopaminergic neurodegeneration in mesencephalic neuron-glia cultures by inhibiting microglial activation J Pharmacol Exp Ther 308 2004 975 983 (Pubitemid 38263973)
49. Y.J. Wang, J.T. Wang, Q.X. Fan, and J.G. Geng Andrographolide inhibits NF-kappaBeta activation and attenuates neointimal hyperplasia in arterial restenosis Cell Res 17 2007 933 941
50. Y. Wei, J.R. Sowers, S.E. Clark, W. Li, C.M. Ferrario, and C.S. Stump Angiotensin II-induced skeletal muscle insulin resistance mediated by NF-kappaB activation via NADPH oxidase Am J Physiol Endocrinol Metab 294 2008 E345 E351
51. J.E. Westin, M.L. Janssen, T.N. Sager, and Y. Temel Automated gait analysis in bilateral parkinsonian rats and the role of L-DOPA therapy Behav Brain Res 226 2012 519 528
52. Y.F. Xia, B.Q. Ye, Y.D. Li, J.G. Wang, X.J. He, and X. Lin et al. Andrographolide attenuates inflammation by inhibition of NF-kappa B activation through covalent modification of reduced cysteine 62 of p50 J Immunol 173 2004 4207 4217 (Pubitemid 39280787)
53. +-induced apoptotic cell death in neuroblastoma cells SH-EP1 through JNK and c-Jun/AP-1 Neurochem Int 56 2010 128 134
54. H. Yao, S. Li, P. Yu, X. Tang, J. Jiang, and Y. Wang Reaction characteristics of andrographolide and its analogue AL-1 with GSH, as a simple chemical simulation of NF-kappaB inhibition Molecules 17 2012 728 739
55. L. Yao, W. Li, H. She, J. Dou, L. Jia, and Y. He et al. Activation of transcription factor MEF2D by bis(3)-cognitin protects dopaminergic neurons and ameliorates parkinsonian motor defects J Biol Chem 287 2012 34246 34255
56. H. Yokoyama, S. Takagi, Y. Watanabe, H. Kato, and T. Araki Role of reactive nitrogen and reactive oxygen species against MPTP neurotoxicity in mice J Neural Transm 115 2008 831 842
57. S.A. Zaitone, D.M. Abo-Elmatty, and A.A. Shaalan Acetyl-l-carnitine and alpha-lipoic acid affect rotenone-induced damage in nigral dopaminergic neurons of rat brain, implication for Parkinson's disease therapy Pharmacol Biochem Behav 100 2012 347 360
58. X. Zeng, X. Liu, J. Bian, G. Pei, H. Dai, and S.W. Polyak et al. Synergistic effect of 14-alpha-lipoyl andrographolide and various antibiotics on the formation of biofilms and production of exopolysaccharide and pyocyanin by Pseudomonas aeruginosa Antimicrob Agents Chemother 55 2011 3015 3017
59. C.Y. Zhang, and B.K. Tan Hypotensive activity of aqueous extract of Andrographis paniculata in rats Clin Exp Pharmacol Physiol 23 1996 675 678 (Pubitemid 26373911)
60. X.F. Zhang, and B.K. Tan Antihyperglycaemic and anti-oxidant properties of Andrographis paniculata in normal and diabetic rats Clin Exp Pharmacol Physiol 27 2000 358 363 (Pubitemid 30313434)
61. Z. Zhang, W. Cui, G. Li, S. Yuan, D. Xu, and M.P. Hoi et al. Baicalein protects against 6-OHDA-induced neurotoxicity through activation of Keap1/Nrf2/HO-1 and involving PKCalpha and PI3K/AKT signaling pathways J Agric Food Chem 60 2012 8171 8182
62. Z. Zhang, J. Jiang, P. Yu, X. Zeng, J.W. Larrick, and Y. Wang Hypoglycemic and beta cell protective effects of andrographolide analogue for diabetes treatment J Transl Med 7 2009 62
63. Q. Zhao, J. Gao, W. Li, and D. Cai Neurotrophic and neurorescue effects of echinacoside in the subacute MPTP mouse model of Parkinson's disease Brain Res 1346 2010 224 236
64. T. Zhu, D.X. Wang, W. Zhang, X.Q. Liao, X. Guan, and H. Bo et al. Andrographolide protects against LPS-induced acute lung injury by inactivation of NF-kappaB PLoS One 8 2013 e56407
65. Y.Y. Zhu, G. Yu, Y. Zhang, Z. Xu, Y.Q. Wang, and G.R. Yan et al. A novel andrographolide derivative AL-1 exerts its cytotoxicity on K562 cells through a ROS-dependent mechanism Proteomics 13 2013 169 178