Ginsenosides attenuate methylglyoxal-induced impairment of insulin signaling and subsequent apoptosis in primary astrocytes

Neuropharmacology

Volumn 85, Issue , 2014, Pages 215-223

  Chu, John M T ^a   Lee, Dicky K M ^a   Wong, Daniella P K ^a   Wong, Ricky N S ^a   Yung, Ken K L ^a   Cheng, Christopher H K ^b   Yue, Kevin K M ^a  

^a HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Astrocytes; Diabetes; Ginsenosides; Insulin signaling; Methylglyoxal

Indexed keywords

CASPASE; GINSENOSIDE; GINSENOSIDE RD; GINSENOSIDE RH 2; GLIAL FIBRILLARY ACIDIC PROTEIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; METHYLGLYOXAL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; INSULIN; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, RAT; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; ASTROCYTE; ASTROCYTE CULTURE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIABETES MELLITUS; HYPERGLYCEMIA; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; ASTROCYTES; CELL SURVIVAL; CELLS, CULTURED; GINSENOSIDES; GLIAL FIBRILLARY ACIDIC PROTEIN; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; NEUROPROTECTIVE AGENTS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PYRUVALDEHYDE; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84902511203     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.05.029     Document Type: Article

References (65)

1. I. Allaman, M. Belanger, and P.J. Magistretti Astrocyte-neuron metabolic relationships: for better and for worse Trends Neurosci. 34 2 2011 76 87
2. L.C. Ang, B. Bhaumick, D.G. Munoz, J. Sass, and B.H. Juurlink Effects of astrocytes, insulin and insulin-like growth factor I on the survival of motoneurons in vitro J. Neurol. Sci. 109 2 1992 168 172
3. S.G. de Arriba, G. Stuchbury, J. Yarin, J. Burnell, and C. Loske et al. Methylglyoxal impairs glucose metabolism and leads to energy depletion in neuronal cells-protection by carbonyl scavengers Neurobiol. Aging 28 7 2007 1044 1050
4. M. Belanger, J. Yang, J.M. Petit, T. Laroche, and P.J. Magistretti et al. Role of the glyoxalase system in astrocyte-mediated neuroprotection J. Neurosci. 31 50 2011 18338 18352
5. L. Berliocchi, M.T. Corasaniti, G. Bagetta, and S.A. Lipton Neuroinflammation in neuronal degeneration and repair Cell Death Differ. 14 4 2007 883 884
6. Y. Bordon Neuroinflammation: inflammatory brain drain Nat. Rev. Immunol. 13 2 2013 69
7. L.S. Chan, P.Y. Yue, T.W. Kok, M.H. Keung, and N.K. Mak et al. Ginsenoside-Rb1 promotes adipogenesis through regulation of PPARgamma and microRNA-27b Horm. Metab. Res. 44 11 2012 819 824
8. L.W. Chen, K.L. Yung, and Y.S. Chan Reactive astrocytes as potential manipulation targets in novel cell replacement therapy of Parkinson's disease Curr. Drug Targets 6 7 2005 821 833
9. L.M. Chen, Z.Y. Lin, Y.G. Zhu, N. Lin, and J. Zhang et al. Ginsenoside Rg1 attenuates beta-amyloid generation via suppressing PPARgamma-regulated BACE1 activity in N2a-APP695 cells Eur. J. Pharmacol. 675 1-3 2012 15 21
10. W.C. Cho, W.S. Chung, S.K. Lee, A.W. Leung, and C.H. Cheng et al. Ginsenoside Re of Panax ginseng possesses significant antioxidant and antihyperlipidemic efficacies in streptozotocin-induced diabetic rats Eur. J. Pharmacol. 550 1-3 2006 173 179
11. E. Coleman, R. Judd, L. Hoe, J. Dennis, and P. Posner Effects of diabetes mellitus on astrocyte GFAP and glutamate transporters in the CNS Glia 48 2 2004 166 178
12. C. Cunha, R. Brambilla, and K.L. Thomas A simple role for BDNF in learning and memory? Front. Mol. Neurosci. 3 2010 1
13. N.C. Danbolt Glutamate uptake Prog. Neurobiol. 65 1 2001 1 105
14. S. Desagher, J. Glowinski, and J. Premont Astrocytes protect neurons from hydrogen peroxide toxicity J. Neurosci. 16 8 1996 2553 2562
15. K.M. Desai, T. Chang, H. Wang, A. Banigesh, and A. Dhar et al. Oxidative stress and aging: is methylglyoxal the hidden enemy? Can J. Physiol. Pharmacol. 88 3 2010 273 284
16. M.S. Forman, D. Lal, B. Zhang, D.V. Dabir, and E. Swanson et al. Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration J. Neurosci. 25 14 2005 3539 3550
17. T.F. Franke, C.P. Hornik, L. Segev, G.A. Shostak, and C. Sugimoto PI3K/Akt and apoptosis: size matters Oncogene 22 56 2003 8983 8998
18. G.K. Gandhi, K.K. Ball, N.F. Cruz, and G.A. Dienel Hyperglycaemia and diabetes impair gap junctional communication among astrocytes ASN Neuro 2 2 2010 e00030
19. Q. Guo, T. Mori, Y. Jiang, C. Hu, and Y. Osaki et al. Methylglyoxal contributes to the development of insulin resistance and salt sensitivity in Sprague-Dawley rats J. Hypertens. 27 8 2009 1664 1671
20. M.N. Haan Therapy Insight: type 2 diabetes mellitus and the risk of late-onset Alzheimer's disease Nat. Clin. Pract. Neurol. 2 3 2006 159 166
21. L. Heimfarth, S.O. Loureiro, P. Pierozan, B.O. de Lima, and K.P. Reis et al. Methylglyoxal-induced cytotoxicity in neonatal rat brain: a role for oxidative stress and MAP kinases Metab. Brain Dis. 28 3 2013 429 438
22. M.O. Hengartner The biochemistry of apoptosis Nature 407 6805 2000 770 776
23. M.H. Jang, H.K. Chang, M.C. Shin, T.H. Lee, and Y.P. Kim et al. Effect of ginseng radix on c-Fos expression in the hippocampus of streptozotocin-induced diabetic rats J. Pharmacol. Sci. 91 2 2003 149 152
24. G.R. John, S.C. Lee, and C.F. Brosnan Cytokines: powerful regulators of glial cell activation Neuroscientist 9 1 2003 10 22
25. B.B. Kahn, and J.S. Flier Obesity and insulin resistance J. Clin. Investig. 106 4 2000 473 481
26. M.P. Kalapos Methylglyoxal in living organisms: chemistry, biochemistry, toxicology and biological implications Toxicol. Lett. 110 3 1999 145 175
27. M.P. Kalapos Methylglyoxal and glucose metabolism: a historical perspective and future avenues for research Drug Metabol. Drug Interact. 23 1-2 2008 69 91
28. A. Khwaja Akt is more than just a Bad kinase Nature 401 6748 1999 33 34
29. H.J. Kim, P. Kim, and C.Y. Shin A comprehensive review of the therapeutic and pharmacological effects of ginseng and ginsenosides in central nervous system J. Ginseng Res. 37 1 2013 8 29
30. B. Kuhla, H.J. Luth, D. Haferburg, K. Boeck, and T. Arendt et al. Methylglyoxal, glyoxal, and their detoxification in Alzheimer's disease Ann. N. Y. Acad. Sci. 1043 2005 211 216
31. A. Lapolla, R. Flamini, A. Dalla Vedova, A. Senesi, and R. Reitano et al. Glyoxal and methylglyoxal levels in diabetic patients: quantitative determination by a new GC/MS method Clin. Chem. Lab. Med. 41 9 2003 1166 1173
32. E. Lee, M. Sidoryk-Wegrzynowicz, N. Wang, A. Webb, and D.S. Son et al. GPR30 regulates glutamate transporter GLT-1 expression in rat primary astrocytes J. Biol. Chem. 287 32 2012 26817 26828
33. K.W. Leung, K.K. Yung, N.K. Mak, Y.S. Chan, and T.P. Fan et al. Neuroprotective effects of ginsenoside-Rg1 in primary nigral neurons against rotenone toxicity Neuropharmacology 52 3 2007 827 835
34. X.F. Li, C.N. Lui, Z.H. Jiang, and Y.K. Ken Neuroprotective effects of ginsenosides Rh1 and Rg2 on neuronal cells Chin. Med. 6 1 2011 19
35. R.M. Lindsay Adult rat brain astrocytes support survival of both NGF-dependent and NGF-insensitive neurones Nature 282 5734 1979 80 82
36. H. Liu, J. Yang, F. Du, X. Gao, and X. Ma et al. Absorption and disposition of ginsenosides after oral administration of Panax notoginseng extract to rats Drug Metab. Dispos. 37 12 2009 2290 2298
37. Y.W. Liu, X. Zhu, W. Li, Q. Lu, and J.Y. Wang et al. Ginsenoside Re attenuates diabetes-associated cognitive deficits in rats Pharmacol. Biochem. Behav. 101 1 2012 93 98
38. M.V. Lopez, M.P. Cuadrado, O.M. Ruiz-Poveda, A.M. Del Fresno, and M.E. Accame Neuroprotective effect of individual ginsenosides on astrocytes primary culture Biochim. Biophys. Acta 1770 9 2007 1308 1316
39. N.J. Maragakis, and J.D. Rothstein Glutamate transporters: animal models to neurologic disease Neurobiol. Dis. 15 3 2004 461 473
40. N.J. Maragakis, and J.D. Rothstein Mechanisms of disease: astrocytes in neurodegenerative disease Nat. Clin. Pract. Neurol. 2 12 2006 679 689
41. E. De Marinis, E. Acaz-Fonseca, M.A. Arevalo, P. Ascenzi, and M. Fiocchetti et al. 17beta-Oestradiol anti-inflammatory effects in primary astrocytes require oestrogen receptor beta-mediated neuroglobin up-regulation J. Neuroendocrinol. 25 3 2013 260 270
42. M.G. Myers Jr., X.J. Sun, B. Cheatham, B.R. Jachna, and E.M. Glasheen et al. IRS-1 is a common element in insulin and insulin-like growth factor-I signaling to the phosphatidylinositol 3'-kinase Endocrinology 132 4 1993 1421 1430
43. D.W. Nicholson, A. Ali, N.A. Thornberry, J.P. Vaillancourt, and C.K. Ding et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis Nature 376 6535 1995 37 43
44. K. Paz, R. Hemi, D. LeRoith, A. Karasik, and E. Elhanany et al. A molecular basis for insulin resistance. Elevated serine/threonine phosphorylation of IRS-1 and IRS-2 inhibits their binding to the juxtamembrane region of the insulin receptor and impairs their ability to undergo insulin-induced tyrosine phosphorylation J. Biol. Chem. 272 47 1997 29911 29918
45. T. Ramesh, S.W. Kim, J.H. Sung, S.Y. Hwang, and S.H. Sohn et al. Effect of fermented Panax ginseng extract (GINST) on oxidative stress and antioxidant activities in major organs of aged rats Exp. Gerontol. 47 1 2012 77 84
46. A.R. Saltiel, and C.R. Kahn Insulin signalling and the regulation of glucose and lipid metabolism Nature 414 6865 2001 799 806
47. M.W. Schwartz, and D. Porte Jr. Diabetes, obesity, and the brain Science 307 5708 2005 375 379
48. S. Sengupta, S.A. Toh, L.A. Sellers, J.N. Skepper, and P. Koolwijk et al. Modulating angiogenesis: the yin and the yang in ginseng Circulation 110 10 2004 1219 1225
49. K. Shapiro, and W.C. Gong Natural products used for diabetes J. Am. Pharm. Assoc. (Wash) 42 2 2002 217 226
50. E.J. Shin, J.H. Jeong, A.Y. Kim, Y.H. Koh, and S.Y. Nah et al. Protection against kainate neurotoxicity by ginsenosides: attenuation of convulsive behavior, mitochondrial dysfunction, and oxidative stress J. Neurosci. Res. 87 3 2009 710 722
51. M.V. Sofroniew, and H.V. Vinters Astrocytes: biology and pathology Acta Neuropathol. 119 1 2010 7 35
52. V. Srikanth, B. Westcott, J. Forbes, T.G. Phan, and R. Beare et al. Methylglyoxal, cognitive function and cerebral atrophy in older people J. Gerontol. A Biol. Sci. Med. Sci. 68 1 2013 68 73
53. M.L. Steele, and S.R. Robinson Reactive astrocytes give neurons less support: implications for Alzheimer's disease Neurobiol. Aging 33 2 2012 423 e1-13
54. E. Steen, B.M. Terry, E.J. Rivera, J.L. Cannon, and T.R. Neely et al. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes? J. Alzheimers Dis. 7 1 2005 63 80
55. M.W. Strachan, R.M. Reynolds, R.E. Marioni, and J.F. Price Cognitive function, dementia and type 2 diabetes mellitus in the elderly Nat. Rev. Endocrinol. 7 2 2011 108 114
56. Z. Turk Glycotoxines, carbonyl stress and relevance to diabetes and its complications Physiol. Res. 59 2 2010 147 156
57. H. Umegaki Neurodegeneration in diabetes mellitus Adv. Exp. Med. Biol. 724 2012 258 265
58. H. Vlassara, and M.R. Palace Diabetes and advanced glycation end products J. Intern. Med. 251 2 2002 87 101
59. W. Wang, Y. Zhao, E.R. Rayburn, D.L. Hill, and H. Wang et al. In vitro anti-cancer activity and structure-activity relationships of natural products isolated from fruits of Panax ginseng Cancer Chemother. Pharmacol. 59 5 2007 589 601
60. Y. Xie, M.R. Hayden, and B. Xu BDNF overexpression in the forebrain rescues Huntington's disease phenotypes in YAC128 mice J. Neurosci. 30 44 2010 14708 14718
61. Q. Xu, Y. Park, X. Huang, A. Hollenbeck, and A. Blair et al. Diabetes and risk of Parkinson's disease Diabetes Care 34 4 2011 910 915
62. Z. Yang, S. Gao, J. Wang, T. Yin, and Y. Teng et al. Enhancement of oral bioavailability of 20(S)-ginsenoside Rh2 through improved understanding of its absorption and efflux mechanisms Drug Metab. Dispos. 39 10 2011 1866 1872
63. Z. Zhang, X. Li, W. Lv, Y. Yang, and H. Gao et al. Ginsenoside Re reduces insulin resistance through inhibition of c-Jun NH2-terminal kinase and nuclear factor-kappaB Mol. Endocrinol. 22 1 2008 186 195
64. Y. Zick Ser/Thr phosphorylation of IRS proteins: a molecular basis for insulin resistance Sci. STKE 2005 268 2005 pe4
65. C. Zuccato, and E. Cattaneo Brain-derived neurotrophic factor in neurodegenerative diseases Nat. Rev. Neurol. 5 6 2009 311 322