The neuroprotective action of pyrroloquinoline quinone against glutamate-induced apoptosis in hippocampal neurons is mediated through the activation of PI3K/Akt pathway

Toxicology and Applied Pharmacology

Volumn 252, Issue 1, 2011, Pages 62-72

  Zhang, Qi ^a   Shen, Mi ^a   Ding, Mei ^a   Shen, Dingding ^a   Ding, Fei ^a  

^a NANTONG UNIVERSITY   (China)

Author keywords

Akt signaling; Apoptosis; Glutamate; Hippocampal neurons; Pyrroloquinoline quinone; Reactive oxygen species

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CALCIUM ION; CASPASE 3; GLUTAMIC ACID; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; PYRROLOQUINOLINEQUINONE; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE; WORTMANNIN;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; LIPID PEROXIDATION; NERVE CELL CULTURE; NERVE CELL LESION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; RAT; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; ENZYME ACTIVATION; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; NEURONS; NEUROPROTECTIVE AGENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PQQ COFACTOR; PREGNANCY; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 79952624790     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.02.006     Document Type: Article

References (81)

1. Aizenman E., Hartnett K.A., Zhong C., Gallop P.M., Rosenberg P.A. Interaction of the putative essential nutrient pyrroloquinoline quinone with the N-methyl-d-aspartate receptor redox modulatory site. J. Neurosci. 1992, 12:2362-2369.
2. Aizenman E., Jensen F.E., Gallop P.M., Rosenberg P.A., Tang L.H. Further evidence that pyrroloquinoline quinone interacts with the N-methyl-d-aspartate receptor redox site in rat cortical neurons in vitro. Neurosci. Lett. 1994, 168:189-192.
3. Antonsson B. Mitochondria and the Bcl-2 family proteins in apoptosis signaling pathways. Mol. Cell. Biochem. 2004, 256-257:141-155.
4. Bauerly K.A., Storms D.H., Harris C.B., Hajizadeh S., Sun M.Y., Cheung C.P., Satre M.A., Fascetti A.J., Tchaparian E., Rucker R.B. Pyrroloquinoline quinone nutritional status alters lysine metabolism and modulates mitochondrial DNA content in the mouse and rat. Biochim. Biophys. Acta 2006, 1760:1741-1748.
5. Bennett B.L., Sasaki D.T., Murray B.W., O'Leary E.C., Sakata S.T., Xu W., Leisten J.C., Motiwala A., Pierce S., Satoh Y., Bhagwat S.S., Manning A.M., Anderson D.W. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl Acad. Sci. USA 2001, 98:13681-13686.
6. Brazil D.P., Hemmings B.A. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci. 2001, 26:657-664.
7. Brecht S., Kirchhof R., Chromik A., Willesen M., Nicolaus T., Raivich G., Wessig J., Waetzig V., Goetz M., Claussen M., Pearse D., Kuan C.Y., Vaudano E., Behrens A., Wagner E., Flavell R.A., Davis R.J., Herdegen T. Specific pathophysiological functions of JNK isoforms in the brain. Eur. J. Neurosci. 2005, 21:363-377.
8. Brewer G.J., Torricelli J.R., Evege E.K., Price P.J. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 1993, 35:567-576.
9. Cao J., Semenova M.M., Solovyan V.T., Han J.H., Coffey E.T., Courtney M.J. Distinct requirements for p38 alpha and c-jun N-terminal kinase stress-activated protein kinases in different forms of apoptotic neuronal death. J. Biol. Chem. 2004, 279:35903-35913.
10. Chen R.W., Lu X.C., Yao C., Liao Z., Jiang Z.G., Wei H., Ghanbari H.A., Tortella F.C., Dave J.R. PAN-811 provides neuroprotection against glutamate toxicity by suppressing activation of JNK and p38 MAPK. Neurosci. Lett. 2007, 422:64-67.
11. Chen S.X., Song T., Zhou S.H., Liu Y.H., Wu S.J., Liu L.Y. Protective effects of ACE inhibitors on vascular endothelial dysfunction induced by exogenous advanced oxidation protein products in rats. Eur. J. Pharmacol. 2008, 584:368-375.
12. Chen X., Liu J., Gu X., Ding F. Salidroside attenuates glutamate-induced apoptotic cell death in primary cultured hippocampal neurons of rats. Brain Res. 2008, 1238:189-198.
13. Choi D.W. Ionic dependence of glutamate neurotoxicity. J. Neurosci. 1987, 7:369-379.
14. 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.
15. Cline H.T., Tsien R.W. Glutamate-induced increases in intracellular Ca2+ in cultured frog tectal cells mediated by direct activation of NMDA receptor channels. Neuron 1991, 6:259-267.
16. Coyle J.T., Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science 1993, 262:689.
17. Dargusch R., Piasecki D., Tan S., Liu Y., Schubert D. The role of Bax in glutamate-induced nerve cell death. J. Neurochem. 2001, 76:295-301.
18. Datta S.R., Brunet A., Greenberg M.E. Cellular survival: a play in three Akts. Genes Dev. 1999, 13:2905-2927.
19. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103:239-252.
20. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl Acad. Sci. USA 1991, 88:6368-6371.
21. Dhanasekaran D.N., Reddy E.P. JNK signaling in apoptosis. Oncogene 2008, 27:6245-6251.
22. Du K., Montminy M. CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 1998, 273:32377-32379.
23. Duan Y., Gross R.A., Sheu S.S. Ca2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity. J. Physiol. 2007, 585:741-758.
24. Ekinci F.J., Linsley M.D., Shea T.B. Beta-amyloid-induced calcium influx induces apoptosis in culture by oxidative stress rather than tau phosphorylation. Brain Res. Mol. Brain Res. 2000, 76:389-395.
25. Eminel S., Roemer L., Waetzig V., Herdegen T. c-Jun N-terminal kinases trigger both degeneration and neurite outgrowth in primary hippocampal and cortical neurons. J. Neurochem. 2008, 104:957-969.
26. Felton L.M., Anthony C. Biochemistry: role of PQQ as a mammalian enzyme cofactor?. Nature 2005, 433:E10. discussion E11-2.
27. Glazner G.W., Chan S.L., Lu C., Mattson M.P. Caspase-mediated degradation of AMPA receptor subunits: a mechanism for preventing excitotoxic necrosis and ensuring apoptosis. J. Neurosci. 2000, 20:3641-3649.
28. Gross A., McDonnell J.M., Korsmeyer S.J. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 1999, 13:1899-1911.
29. Gunasekar P.G., Kanthasamy A.G., Borowitz J.L., Isom G.E. NMDA receptor activation produces concurrent generation of nitric oxide and reactive oxygen species: implication for cell death. J. Neurochem. 1995, 65:2016-2021.
30. Hara H., Hiramatsu H., Adachi T. Pyrroloquinoline quinone is a potent neuroprotective nutrient against 6-hydroxydopamine-induced neurotoxicity. Neurochem. Res. 2007, 32:489-495.
31. Hauge J.G. Glucose dehydrogenase of bacterium anitratum: an enzyme with a novel prosthetic group. J. Biol. Chem. 1964, 239:3630-3639.
32. Hilton G.D., Nunez J.L., Bambrick L., Thompson S.M., McCarthy M.M. Glutamate-mediated excitotoxicity in neonatal hippocampal neurons is mediated by mGluR-induced release of Ca++ from intracellular stores and is prevented by estradiol. Eur. J. Neurosci. 2006, 24:3008-3016.
33. Hirakawa A., Shimizu K., Fukumitsu H., Furukawa S. Pyrroloquinoline quinone attenuates iNOS gene expression in the injured spinal cord. Biochem. Biophys. Res. Commun. 2009, 378:308-312.
34. 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.
35. Kasahara T., Kato T. Nutritional biochemistry: a new redox-cofactor vitamin for mammals. Nature 2003, 422:832.
36. Keller J.N., Kindy M.S., Holtsberg F.W., St Clair D.K., Yen H.C., Germeyer A., Steiner S.M., Bruce-Keller A.J., Hutchins J.B., Mattson M.P. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J. Neurosci. 1998, 18:687-697.
37. Killgore J., Smidt C., Duich L., Romero-Chapman N., Tinker D., Reiser K., Melko M., Hyde D., Rucker R.B. Nutritional importance of pyrroloquinoline quinone. Science 1989, 245:850-852.
38. Kirkland R.A., Saavedra G.M., Cummings B.S., Franklin J.L. Bax regulates production of superoxide in both apoptotic and nonapoptotic neurons: role of caspases. J. Neurosci. 2010, 30:16114-16127.
39. Kumazawa T., Hiwasa T., Takiguchi M., Suzuki O., Sato K. Activation of Ras signaling pathways by pyrroloquinoline quinone in NIH3T3 mouse fibroblasts. Int. J. Mol. Med. 2007, 19:765-770.
40. Lafon-Cazal M., Pietri S., Culcasi M., Bockaert J. NMDA-dependent superoxide production and neurotoxicity. Nature 1993, 364:535-537.
41. Li N., Liu B., Dluzen D.E., Jin Y. Protective effects of ginsenoside Rg2 against glutamate-induced neurotoxicity in PC12 cells. J. Ethnopharmacol. 2007, 111:458-463.
42. Liu C.L., Siesjo B.K., Hu B.R. Pathogenesis of hippocampal neuronal death after hypoxia-ischemia changes during brain development. Neuroscience 2004, 127:113-123.
43. Liu J., Lin A. Role of JNK activation in apoptosis: a double-edged sword. Cell Res. 2005, 15:36-42.
44. Liu S., Li H., Ou Yang J., Peng H., Wu K., Liu Y., Yang J. Enhanced rat sciatic nerve regeneration through silicon tubes filled with pyrroloquinoline quinone. Microsurgery 2005, 25:329-337.
45. Luetjens C.M., Bui N.T., Sengpiel B., Munstermann G., Poppe M., Krohn A.J., Bauerbach E., Krieglstein J., Prehn J.H. Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J. Neurosci. 2000, 20:5715-5723.
46. Mark L.P., Prost R.W., Ulmer J.L., Smith M.M., Daniels D.L., Strottmann J.M., Brown W.D., Hacein-Bey L. Pictorial review of glutamate excitotoxicity: fundamental concepts for neuroimaging. AJNR Am. J. Neuroradiol. 2001, 22:1813-1824.
47. Mebratu Y., Tesfaigzi Y. How ERK1/2 activation controls cell proliferation and cell death: is subcellular localization the answer?. Cell Cycle 2009, 8:1168-1175.
48. 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.
49. Murase K., Hattori A., Kohno M., Hayashi K. Stimulation of nerve growth factor synthesist/secretion in mouse astroglial cells by coenzymes. Biochem. Mol. Biol. Int. 1993, 30:615-621.
50. Nicotera P., Leist M., Manzo L. Neuronal cell death: a demise with different shapes. Trends Pharmacol. Sci. 1999, 20:46-51.
51. Nunome K., Miyazaki S., Nakano M., Iguchi-Ariga S., Ariga H. Pyrroloquinoline quinone prevents oxidative stress-induced neuronal death probably through changes in oxidative status of DJ-1. Biol. Pharm. Bull. 2008, 31:1321-1326.
52. 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.
53. Perkinton M.S., Sihra T.S., Williams R.J. Ca(2+)-permeable AMPA receptors induce phosphorylation of cAMP response element-binding protein through a phosphatidylinositol 3-kinase-dependent stimulation of the mitogen-activated protein kinase signaling cascade in neurons. J. Neurosci. 1999, 19:5861-5874.
54. Perkinton M.S., Ip J.K., Wood G.L., Crossthwaite A.J., Williams R.J. Phosphatidylinositol 3-kinase is a central mediator of NMDA receptor signalling to MAP kinase (Erk1/2). Akt/PKB and CREB in striatal neurones. J. Neurochem. 2002, 80:239-254.
55. Petit P.X., Susin S.A., Zamzami N., Mignotte B., Kroemer G. Mitochondria and programmed cell death: back to the future. FEBS Lett. 1996, 396:7-13.
56. Portera-Cailliau C., Price D.L., Martin L.J. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J. Comp. Neurol. 1997, 378:70-87.
57. Reynolds I.J., Hastings T.G. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 1995, 15:3318-3327.
58. Rucker R., Storms D., Sheets A., Tchaparian E., Fascetti A. Biochemistry: is pyrroloquinoline quinone a vitamin?. Nature 2005, 433:E10-1. discussion E11-2.
59. Rucker R., Chowanadisai W., Nakano M. Potential physiological importance of pyrroloquinoline quinone. Altern. Med. Rev. 2009, 14:268-277.
60. Salisbury S.A., Forrest H.S., Cruse W.B., Kennard O. A novel coenzyme from bacterial primary alcohol dehydrogenases. Nature 1979, 280:843-844.
61. Savolainen K.M., Loikkanen J., Eerikainen S., Naarala J. Glutamate-stimulated ROS production in neuronal cultures: interactions with lead and the cholinergic system. Neurotoxicology 1998, 19:669-674.
62. Scanlon J.M., Aizenman E., Reynolds I.J. Effects of pyrroloquinoline quinone on glutamate-induced production of reactive oxygen species in neurons. Eur. J. Pharmacol. 1997, 326:67-74.
63. Schulz J.B., Bremen D., Reed J.C., Lommatzsch J., Takayama S., Wullner U., Loschmann P.A., Klockgether T., Weller M. Cooperative interception of neuronal apoptosis by BCL-2 and BAG-1 expression: prevention of caspase activation and reduced production of reactive oxygen species. J. Neurochem. 1997, 69:2075-2086.
64. Schwarzschild M.A., Cole R.L., Hyman S.E. Glutamate, but not dopamine, stimulates stress-activated protein kinase and AP-1-mediated transcription in striatal neurons. J. Neurosci. 1997, 17:3455-3466.
65. Segura Torres J.E., Chaparro-Huerta V., Rivera Cervantres M.C., Montes-Gonzalez R., Flores Soto M.E., Beas-Zarate C. Neuronal cell death due to glutamate excitotocity is mediated by p38 activation in the rat cerebral cortex. Neurosci. Lett. 2006, 403:233-238.
66. Stites T., Storms D., Bauerly K., Mah J., Harris C., Fascetti A., Rogers Q., Tchaparian E., Satre M., Rucker R.B. Pyrroloquinoline quinone modulates mitochondrial quantity and function in mice. J. Nutr. 2006, 136:390-396.
67. 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.
68. Szydlowska K., Tymianski M. Calcium, ischemia and excitotoxicity. Cell Calcium 2010, 47:122-129.
69. 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.
70. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 2008, 9:231-241.
71. Valdivia A., Perez-Alvarez S., Aroca-Aguilar J.D., Ikuta I., Jordan J. Superoxide dismutases: a physiopharmacological update. J. Physiol. Biochem. 2009, 65:195-208.
72. Vila M., Jackson-Lewis V., Vukosavic S., Djaldetti R., Liberatore G., Offen D., Korsmeyer S.J., Przedborski S. Bax ablation prevents dopaminergic neurodegeneration in the 1-methyl- 4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson's disease. Proc. Natl Acad. Sci. USA 2001, 98:2837-2842.
73. Weisiger R.A., Fridovich I. Superoxide dismutase. Organelle specificity. J. Biol. Chem. 1973, 248:3582-3592.
74. Yeste-Velasco M., Folch J., Casadesus G., Smith M.A., Pallas M., Camins A. Neuroprotection by c-Jun NH2-terminal kinase inhibitor SP600125 against potassium deprivation-induced apoptosis involves the Akt pathway and inhibition of cell cycle reentry. Neuroscience 2009, 159:1135-1147.
75. Youle R.J., Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 2008, 9:47-59.
76. Zha H., Reed J.C. Heterodimerization-independent functions of cell death regulatory proteins Bax and Bcl-2 in yeast and mammalian cells. J. Biol. Chem. 1997, 272:31482-31488.
77. Zhang Y., Rosenberg P.A. The essential nutrient pyrroloquinoline quinone may act as a neuroprotectant by suppressing peroxynitrite formation. Eur. J. Neurosci. 2002, 16:1015-1024.
78. Zhang Y., Feustel P.J., Kimelberg H.K. Neuroprotection by pyrroloquinoline quinone (PQQ) in reversible middle cerebral artery occlusion in the adult rat. Brain Res. 2006, 1094:200-206.
79. Zheng W.H., Quirion R. Glutamate acting on N-methyl-d-aspartate receptors attenuates insulin-like growth factor-1 receptor tyrosine phosphorylation and its survival signaling properties in rat hippocampal neurons. J. Biol. Chem. 2009, 284:855-861.
80. 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.
81. Zhu B.Q., Simonis U., Cecchini G., Zhou H.Z., Li L., Teerlink J.R., Karliner J.S. Comparison of pyrroloquinoline quinone and/or metoprolol on myocardial infarct size and mitochondrial damage in a rat model of ischemia/reperfusion injury. J. Cardiovasc. Pharmacol. Ther. 2006, 11:119-128.