The neuritogenic and neuroprotective potential of senegenin against Aβ-induced neurotoxicity in PC 12 cells

BMC Complementary and Alternative Medicine

Volumn 16, Issue 1, 2016, Pages

  Jesky, Robert ^a   Chen, Hailong ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

Cytotoxicity; Neuritogenesis; Neuroprotective; Nootropic; PC 12 cells; Senegenin

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[25-35]; APOPTOSIS SIGNAL REGULATING KINASE 1; MICROTUBULE ASSOCIATED PROTEIN 2; NEUROMODULIN; NEUROPROTECTIVE AGENT; PLANT MEDICINAL PRODUCT; SENEGENIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; AMYLOID BETA-PROTEIN (25-35); HERBACEOUS AGENT; NEUROTOXIN; PEPTIDE FRAGMENT; TENUIGENIN;

ARTICLE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG IDENTIFICATION; DRUG MECHANISM; DRUG STRUCTURE; ENZYME INHIBITION; IMMUNOFLUORESCENCE; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEUROPROTECTION; NEUROTOXICITY; PC12 CELL LINE; POLYGALA TENUIFOLIA; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; NEURITE; POLYGALA; RAT;

AMYLOID BETA-PEPTIDES; ANIMALS; CELL SURVIVAL; CYTOPROTECTION; DRUGS, CHINESE HERBAL; MOLECULAR STRUCTURE; NEURITES; NEUROPROTECTIVE AGENTS; NEUROTOXINS; PC12 CELLS; PEPTIDE FRAGMENTS; POLYGALA; RATS;

EID: 84956681780     PISSN: None     EISSN: 14726882     Source Type: Journal    
DOI: 10.1186/s12906-016-1006-3     Document Type: Article

References (71)

1. Taylor JP, Hardy T, Fischbeck KH. Toxic Proteins in Neurodegenerative Disease. Science. 2002;296(5575):1991-5.
2. Selkoe DJ. Alzheimer's Disease: genes, proteins, and therapy. Physiol Rev. 2001;81(2):741-66.
3. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science. 2002;297:353-6.
4. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A. 1998;95(11):6448-53.
5. Selkoe DJ. Alzheimer's disease is a synaptic failure. Science. 2002;298(5594):789-91.
6. Glabe CG. Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol Aging. 2006;27(4):570-5.
7. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, et al. Synaptic Targeting by Alzheimer's-Related Amyloid-β Oligomers. J Neurosci. 2004;24(45):10191-200.
8. Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, et al. Alzheimer's Disease International: Global prevalence of dementia: a Delphi consensus study. Lancet. 2005;366(9503):2112-7.
9. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells with respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976;73(7):2424-8.
10. Pollock JD, Krempin M, Rudy B. Differential effects of NGF, FGF, EGF, cAMP, and dexamethasone on neurite outgrowth and sodium channel expression in PC12 cells. J Neurosci. 1990;10(8):2626-37.
11. Brugg B, Matus A. PC 12 cells express juvenile microtubule-associated proteins during nerve growth factor-induced neurite growth. J Cell Biol. 1988;107(2):643-50.
12. Karns LR, Ng SC, Freeman JA, Fishman MC. Cloning of complementary DNA for GAP-43, a neuronal growth-related protein. Science. 1987;236(4801):597-600.
13. Van Hooff CO, De Graan PN, Oestreicher AB, Gispen WH. B-50 phosphorylation and polyphosphoinositide metabolism in nerve growth cone membranes. J Neurosci. 1988;8(5):1789-95.
14. Meiri KF, Pfenninger KH, Willard MB. Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp 46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc Natl Acad Sci U S A. 1986;83(10):3537-41.
15. Costello B, Meymandi A, Freeman JA. Factors Influencing GAP-43 Gene Expression in PC1 2 Pheochromocytoma Cells. J Neurosci. 1990;10(4):1396-406.
16. Yamada KM, Spooner BS, Wessells NK. Axon growth: role of microfilaments and microtubules. Proc Natl Acad Sci U S A. 1970;66(4):1206-12.
17. Seeds NW, Gilman AG, Amano T, Nirenberg MW. Regulation of axon formation by clonal lines of neural tumor. Proc Natl Acad Sci U S A. 1970;66(1):160-7.
18. Sánchez C, Díaz-Nido J, Avila J. Variations in in viva phosphorylation at the proline-rich domain of the microtubule-associated protein 2 (MAP2) during rat brain development. J Biochem. 1995;306:481-7.
19. Sánchez C, Díaz-Nido J, Avila J. Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol. 2000;61(2):133-68.
20. Pang L, Sawada T, Decker SJ, Saltiel AR. Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J Biol Chem. 1995;270:13585-8.
21. Cáceres A, Banker GA, Binder L. Immunocytochemical Localization of Tubulin and Microtubule-Associated Protein 2 During the Development of Hippocampal Neurons in Culture. J Neurosci. 1986;6(3):714-22.
22. Jahn R, Schiebler W, Ouimet C, Greengard P. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci U S A. 1985;82(12):4137-41.
23. Nieto-Sampedro M, Nieto-Díaz M. Neural Plasticity: changes with age. J Neural Transm. 2005;112(1):3-27.
24. Burke SN, Barnes CA. Neural plasticity in the ageing brain. Nature Rev Neurosci. 2006;7:30-40.
25. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature. 1997;386(6624):493-5.
26. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4(11):1313-7.
27. Kromer LF. Nerve growth factor treatment after brain injury prevents neuronal death. Science. 1987;235(4785):214-6.
28. Prakash N, Cohen-Cory S, Penschuck S, Frostig RD. Basal forebrain cholinergic system is involved in rapid nerve growth factor (NGF)-induced plasticity in the barrel cortex of adult rats. J Neurophysiol. 2004;91(1):424-37.
29. Patapoutian A, Reichardt LF. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol. 2001;11(3):272-80.
30. McAllister AK, Katz LC, Lo DC. Neurotrophins and synaptic plasticity. Annu Rev Neurosci. 1999;22:295-318.
31. Friden PM, Walus LR, Watson P, Doctrow SR, Kozarich JW, Backman C, et al. Blood-brain barrier penetration and in vivo activity of an NGF conjugate. Science. 1993;259(5093):373-7.
32. Bäckman C, Rose GM, Hoffer BJ, Henry MA, Bartus RT, Friden P, et al. Systemic administration of a Nerve Growth Factor Conjugate Reverses Age-Related Cognitive Dysfunction and Prevents Cholinergic Neuron Atrophy. J Neurosci. 1996;16(17):5437-42.
33. Yamada K, Nitta A, Hasegawa T, Fuji K, Hiramatsu M, Kameyama T, et al. Orally active NGF synthesis stimulators: potential therapeutic agents in Alzheimer's disease. Behav Brain Res. 1997;83(1-2):117-22.
34. Pardridge WM. The Blood-brain Barrier: Bottleneck in Brain Drug Development. NeuroRx. 2005;2(1):3-14.
35. Liu WB, Liu WZ. Disciplinarian investigation of Chinese complex prescription with promoting intelligence in past dynasties. Jiangxi J Traditional Chin Med. 2005;36:62-3.
36. Park CH, Choi SH, Koo JW, Seo JH, Kim HS, Jeong SJ, et al. Novel cognitive improving and neuroprotective activities of Polygala tenuifolia Willdenow extract, BT-11. J Neurosci Res. 2002;70(3):484-92.
37. Karakida F, Ikeya Y, Tsunakawa M, Yamaguchi T, Ikarashi Y, Takeda S, et al. Cerebral Protective and Cognition-Improving Effects of Sinapic Acid in Rodents. Biol Pharm Bull. 2007;30(3):514-9.
38. Jia H, Jiang Y, Ruan Y, Zhang Y, Ma X, Zhang J, et al. Tenuigenin treatment decreases secretion of the Alzheimer's disease amyloid-β protein in cultured cells. Neurosci Lett. 2004;367(1):123-8.
39. Lv J, Jia H, Jiang Y, Ruan Y, Liu Z, Yue W, et al. Tenuifolin, an extract derived from tenuigenin, inhibits amyloid-β secretion in vitro. Acta Physiol (Oxf). 2009;196(4):419-25.
40. Zhang H, Han T, Zhang L, Yu CH, Wan DG, Rahman K, et al. Effects of tenuifolin extracted from radix polygalae on learning and memory: A behavioral and biochemical study on aged and amnesic mice. Phytomedicine. 2008;15(8):587-94.
41. Yabe T, Tuchida H, Kiyohara H, Takeda T, Yamada H. Induction of NGF synthesis in astrocytes by onjisaponins of Polygala tenuifolia, constituents of kampo (Japanese herbal) medicine Ninjin-yoei-to. Phytomedicine. 2003;10(2-3):106-14.
42. Park HJ, Lee K, Heo H, Lee M, Kim JW, Whang WW, et al. Effects of Polygala tenuifolia Root Extract on Proliferation of Neural Stem Cells in the Hippocampal CA1 Region. Phytother Res. 2008;22(10):1324-9.
43. Ban JY, Cho SO, Koh SB, Song KS, Bae K, Seong YH. Protection of amyloid beta protein (25-35)-induced neurotoxicity by methanol extract of Smilacis chinae rhizome in cultured rat cortical neurons. J Ethnopharmacol. 2006;106(2):230-7.
44. Qian YH, Han H, Hu XD, Shi LL. Protective effect of ginsenoside Rb1 on β-amyloid protein (1-42)-induced neurotoxicity in cortical neurons. Neurol Res. 2008;31:663-7.
45. Sano M, Grossman H, Van Dyk K. Preventing Alzheimer's disease separating fact from fiction. CNS Drugs. 2008;22:887-902.
46. Tohda C, Matsumoto N, Zou K, Meselhy MR, Komatsu K. Abeta(25-35)-induced memory impairment, axonal atrophy, and synaptic loss are ameliorated by M1, A metabolite of protopanaxadiol-type saponins. Neuropsychopharmacology. 2004;29(5):860-8.
47. Kim JH, Ha HC, Lee MS, Kang JI, Kim HS, Lee SY, et al. Effect of Tremella fuciformis on the Neurite Outgrowth of PC12h Cells and the Improvement of Memory in Rats. Biol Pharm Bull. 2007;30(4):708-14.
48. Cui L, Locatelli L, Xie MY, Sommadossi JP. Effect of Nucleoside Analogs on Neurite Regeneration and Mitochondrial DNA Synthesis in PC-12 Cells. J Pharmacol Exp Ther. 1997;280(3):1228-34.
49. Kuboyama T, Tohda C, Komatsu K. Neuritic regeneration and synaptic reconstruction induced by withanolide A. Br J Pharmacol. 2005;144(7):961-71.
50. Tohda C, Tamura T, Matsuyama S, Komatsu K. Promotion of axonal maturation and prevention of memory loss in mice by extracts of Astragalus mongholicus. Br J Pharmacol. 2006;149(5):532-41.
51. Murphy AN, Fiskum G, Beal MF. Mitochondria in neurodegeneration: bioenergetic function in cell life and death. J Cereb Blood Flow Metab. 1999;19(3):231-45.
52. Hensley K, Carney JM, Mattson MP, Aksenova M, Harris M, Wu JF, et al. A model for 3-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: Relevance to Alzheimer disease. Proc Natl Acad Sci U S A. 1994;91(8):3270-4.
53. Shearman MS, Ragan CI, Iversen LL. Inhibition of PC12 cell redox activity is a specific, early indicator of the mechanism of 1-amyloid-mediated cell death. Proc Natl Acad Sci U S A. 1994;91(4):1470-4.
54. Hughes E, Burke RM, Doig AJ. Inhibition of Toxicity in the β-Amyloid Peptide Fragment β-(25-35) Using N-Methylated Derivatives: a general strategy to prevent amyloid formation. J Biol Chem. 2000;275(33):25109-15.
55. Nishida H, Kushida M, Nakajima Y, Ogawa Y, Tatewaki N, Sato S, et al. Amyloid-β-Induced Cytotoxicity of PC-12 Cell Was Attenuated by Shengmai-san Through Redox Regulation and Outgrowth Induction. J Pharmacol Sci. 2007;104(1):73-81.
56. Troy CM, Rabacchi SA, Friedman WJ, Frappier TF, Brown K, Shelanski ML. Caspase-2 mediates neuronal cell death induced by β-Amyloid. J Neurosci. 2000;20(4):1386-92.
57. Kadowaki H, Nishitoh H, Urano F, Sadamitsu C, Matsuzawa A, Takeda K, et al. Amyloid-β induces neuronal cell death through ROS-mediated ASK1 activation. Cell Death Differ. 2005;12(1):19-24.
58. Hsu MJ, Hsu CY, Chen BC, Chen MC, Ou G, Lin CH. Apoptosis signal regulating kinase 1 in amyloid beta peptide-induced cerebral endothelial cell apoptosis. J Neurosci. 2007;27:5719-29.
59. Morishima Y, Gotoh Y, Zieg J, Barrett T, Takano H, Flavell R, et al. Beta-amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of Fas ligand. J Neurosci. 2001;21(19):7551-60.
60. Shea TB, Perrone-Bizzozero NI, Beermann ML, Benowitz LI. Phospholipid-mediated delivery of anti-GAP-43 antibodies into neuroblastoma cells prevents neuritogenesis. J Neurosci. 1991;11(6):1685-90.
61. Meiri KF, Willard M, Johnson MI. Distribution and Phosphorylation of the Growth-Associated Protein GAP-43 in Regenerating Sympathetic Neurons in Culture. J Neurosci. 1988;8(7):2571-81.
62. Aloyo VJ, Zwiers H, Gispen WH. Phosphorylation of B-50 protein by calcium-activated, phospholipid-dependent protein kinase and B-50 protein kinase. J Neurochem. 1983;41(3):649-53.
63. Shen Y, Mani S, Donovan SL, Schwob JE, Meiri KF. Growth-Associated Protein-43 is required for commissural axon guidance in the developing vertebrate nervous system. J Neurosci. 2002;22(1):239-47.
64. Hsu L, Jeng AY, Chen KY. Induction of neurite outgrowth from chick embryonic ganglia explants by activators of protein kinase C. Neurosci Lett. 1989;99(3):257-62.
65. Yankner BA, Benowitz LI, Villa-Komaroff L, Neve RL. Transfection of PC12 cells with the human GAP-43 gene: effects on neurite outgrowth and regeneration. Brain Res Mol Brain Res. 1990;7(1):39-44.
66. Quinlan EM, Halpain S. Emergence of activity-dependent, bidirectional control of microtubule-associated protein MAP2 phosphorylation during postnatal development. J Neurosci. 1996;16(23):7627-37.
67. Diez-Guerra FJ, Avila J. An increase in phosphorylation of microtubule-associated protein 2 accompanies dendrite extension during the differentiation of cultured hippocampal neurons. Eur J Biochem. 1995;227(1-2):68-77.
68. Caceres A, Binder LI, Payne MR, Bender P, Rebhun L, Steward O. Different sub cellular localization of tubulin and the microtubule associated protein MAP2 in brain tissue as revealed by immunocytochemistry with monoclonal hybridoma antibodies. J Neurosci. 1984;4:394-410.
69. Brugg B, Matus A. Phosphorylation Determines the Binding of Microtubule-associated Protein 2 (MAP2) to Microtubules in Living Cells. J Cell Biol. 1991;114(4):735-43.
70. Ainsztein AM, Purich DL. Stimulation of Tubulin Polymerization by MAP-2. J Biol Chem. 1994;269(45):28465-71.
71. Miyasaka T, Chao MV, Sherline P, Saltiel AR. Nerve growth factor stimulates a protein kinase in PC-12 cells that phosphorylates microtubule-associated protein-2. J Biol Chem. 1990;265(8):4730-5.