The neuroprotective role of metformin in advanced glycation end product treated human neural stem cells is AMPK-dependent

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 5, 2015, Pages 720-731

  Chung, Ming Min ^a   Chen, Yen Lin ^a   Pei, Dee ^a   Cheng, Yi Chuan ^b   Sun, Binggui ^c   Nicol, Christopher J ^d,e   Yen, Chia Hui ^f   Chen, Han Min ^g   Liang, Yao Jen ^g   Chiang, Ming Chang ^g  

^a FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d QUEEN S UNIVERSITY   (Canada)

^e QUEEN S UNIVERSITY   (Canada)

^f MING CHUAN UNIVERSITY   (Taiwan)

^g FU JEN CATHOLIC UNIVERSITY   (Taiwan)

Author keywords

AGEs; AMPK; HNSCs; Metformin

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADVANCED GLYCATION END PRODUCT; CASPASE 3; CASPASE 9; CYTOCHROME C; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; METFORMIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROSTAGLANDIN SYNTHASE; ANTIDIABETIC AGENT; NRF1 PROTEIN, HUMAN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PPARGC1A PROTEIN, HUMAN; PROTEIN BCL 2; TRANSCRIPTION FACTOR;

ARTICLE; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; CYTOSOL; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NERVE DEGENERATION; NEURAL STEM CELL; NEUROPROTECTION; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SECRETION (PROCESS); SIGNAL TRANSDUCTION; WESTERN BLOTTING;

AMP-ACTIVATED PROTEIN KINASES; BLOTTING, WESTERN; CASPASE 3; CASPASE 9; CELL SURVIVAL; CELLS, CULTURED; CYTOCHROMES C; GENE EXPRESSION; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; HYPOGLYCEMIC AGENTS; METFORMIN; MITOCHONDRIA; NEURAL STEM CELLS; NUCLEAR RESPIRATORY FACTOR 1; PPAR GAMMA; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84922364445     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.01.006     Document Type: Article

References (76)

1. Butterfield D.A., Di Domenico F., Barone E. Elevated risk of type 2 diabetes for development of Alzheimer disease: a key role for oxidative stress in brain. Biochim. Biophys. Acta 2014, 1842:1693-1706.
2. McCall A.L. The impact of diabetes on the CNS. Diabetes 1992, 41:557-570.
3. Thomas V.S., Darvesh S., MacKnight C., Rockwood K. Estimating the prevalence of dementia in elderly people: a comparison of the Canadian study of health and aging and national population health survey approaches. Int. Psychogeriatr. 2001, 13(Suppl. 1):169-175.
4. Arnold S.E., Lucki I., Brookshire B.R., Carlson G.C., Browne C.A., Kazi H., Bang S., Choi B.R., Chen Y., McMullen M.F., Kim S.F. High fat diet produces brain insulin resistance, synaptodendritic abnormalities and altered behavior in mice. Neurobiol. Dis. 2014, 67:79-87.
5. Ott A., Stolk R.P., van Harskamp F., Pols H.A., Hofman A., Breteler M.M. Diabetes mellitus and the risk of dementia: the Rotterdam study. Neurology 1999, 53:1937-1942.
6. Peila R., Rodriguez B.L., Launer L.J. Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: the Honolulu-Asia aging study. Diabetes 2002, 51:1256-1262.
7. Arvanitakis Z., Wilson R.S., Bienias J.L., Evans D.A., Bennett D.A. Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Arch. Neurol. 2004, 61:661-666.
8. den Heijer T., Vermeer S.E., van Dijk E.J., Prins N.D., Koudstaal P.J., Hofman A., Breteler M.M. Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI. Diabetologia 2003, 46:1604-1610.
9. Stewart R., Liolitsa D. Type 2 diabetes mellitus, cognitive impairment and dementia. Diabet. Med. 1999, 16:93-112.
10. Magistretti P.J., Pellerin L. Cellular mechanisms of brain energy metabolism. Relevance to functional brain imaging and to neurodegenerative disorders. Ann. N. Y. Acad. Sci. 1996, 777:380-387.
11. Duarte A.I., Candeias E., Correia S.C., Santos R.X., Carvalho C., Cardoso S., Placido A., Santos M.S., Oliveira C.R., Moreira P.I. Crosstalk between diabetes and brain: glucagon-like peptide-1 mimetics as a promising therapy against neurodegeneration. Biochim. Biophys. Acta 2013, 1832:527-541.
12. Nelson P.T., Smith C.D., Abner E.A., Schmitt F.A., Scheff S.W., Davis G.J., Keller J.N., Jicha G.A., Davis D., Wang-Xia W., Hartman A., Katz D.G., Markesbery W.R. Human cerebral neuropathology of type 2 diabetes mellitus. Biochim. Biophys. Acta 2009, 1792:454-469.
13. Yamagishi S., Takeuchi M., Inagaki Y., Nakamura K., Imaizumi T. Role of advanced glycation end products (AGEs) and their receptor (RAGE) in the pathogenesis of diabetic microangiopathy. Int. J. Clin. Pharmacol. Res. 2003, 23:129-134.
14. Yamagishi S., Imaizumi T. Diabetic vascular complications: pathophysiology, biochemical basis and potential therapeutic strategy. Curr. Pharm. Des. 2005, 11:2279-2299.
15. Wang S.H., Sun Z.L., Guo Y.J., Yuan Y., Li L. PPARgamma-mediated advanced glycation end products regulation of neural stem cells. Mol. Cell. Endocrinol. 2009, 307:176-184.
16. Yamagishi S., Nakamura K., Matsui T., Ueda S., Fukami K., Okuda S. Agents that block advanced glycation end product (AGE)-RAGE (receptor for AGEs)-oxidative stress system: a novel therapeutic strategy for diabetic vascular complications. Expert Opin. Investig. Drugs 2008, 17:983-996.
17. Ruggiero-Lopez D., Lecomte M., Moinet G., Patereau G., Lagarde M., Wiernsperger N. Reaction of metformin with dicarbonyl compounds. Possible implication in the inhibition of advanced glycation end product formation. Biochem. Pharmacol. 1999, 58:1765-1773.
18. Steinberg G.R., Kemp B.E. AMPK in health and disease. Physiol. Rev. 2009, 89:1025-1078.
19. Fogarty S., Hardie D.G. Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer. Biochim. Biophys. Acta 2010, 1804:581-591.
20. Sun W., Lee T.S., Zhu M., Gu C., Wang Y., Zhu Y., Shyy J.Y. Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation 2006, 114:2655-2662.
21. Rahbar S., Natarajan R., Yerneni K., Scott S., Gonzales N., Nadler J.L. Evidence that pioglitazone, metformin and pentoxifylline are inhibitors of glycation. Clin. Chim. Acta 2000, 301:65-77.
22. Ronnett G.V., Ramamurthy S., Kleman A.M., Landree L.E., Aja S. AMPK in the brain: its roles in energy balance and neuroprotection. J. Neurochem. 2009, 109(Suppl. 1):17-23.
23. Carling D. The AMP-activated protein kinase cascade-a unifying system for energy control. Trends Biochem. Sci. 2004, 29:18-24.
24. Hardie D.G. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 2003, 144:5179-5183.
25. Shin S.M., Cho I.J., Kim S.G. Resveratrol protects mitochondria against oxidative stress through AMP-activated protein kinase-mediated glycogen synthase kinase-3beta inhibition downstream of poly(ADP-ribose)polymerase-LKB1 pathway. Mol. Pharmacol. 2009, 76:884-895.
26. Choi S.L., Kim S.J., Lee K.T., Kim J., Mu J., Birnbaum M.J., Soo Kim S., Ha J. The regulation of AMP-activated protein kinase by H(2)O(2). Biochem. Biophys. Res. Commun. 2001, 287:92-97.
27. Salt I.P., Johnson G., Ashcroft S.J., Hardie D.G. AMP-activated protein kinase is activated by low glucose in cell lines derived from pancreatic beta cells, and may regulate insulin release. Biochem. J. 1998, 335(Pt 3):533-539.
28. Arsikin K., Kravic-Stevovic T., Jovanovic M., Ristic B., Tovilovic G., Zogovic N., Bumbasirevic V., Trajkovic V., Harhaji-Trajkovic L. Autophagy-dependent and -independent involvement of AMP-activated protein kinase in 6-hydroxydopamine toxicity to SH-SY5Y neuroblastoma cells. Biochim. Biophys. Acta 2012, 1822:1826-1836.
29. Melemedjian O.K., Asiedu M.N., Tillu D.V., Sanoja R., Yan J., Lark A., Khoutorsky A., Johnson J., Peebles K.A., Lepow T., Sonenberg N., Dussor G., Price T.J. Targeting adenosine monophosphate-activated protein kinase (AMPK) in preclinical models reveals a potential mechanism for the treatment of neuropathic pain. Mol. Pain 2011, 7:70.
30. Zhang B.B., Zhou G., Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 2009, 9:407-416.
31. Salminen A., Kaarniranta K. AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res. Rev. 2012, 11:230-241.
32. Salminen A., Kaarniranta K., Haapasalo A., Soininen H., Hiltunen M. AMP-activated protein kinase: a potential player in Alzheimer's disease. J. Neurochem. 2011, 118:460-474.
33. Dulovic M., Jovanovic M., Xilouri M., Stefanis L., Harhaji-Trajkovic L., Kravic-Stevovic T., Paunovic V., Ardah M.T., El-Agnaf O.M., Kostic V., Markovic I., Trajkovic V. The protective role of AMP-activated protein kinase in alpha-synuclein neurotoxicity in vitro. Neurobiol. Dis. 2014, 63:1-11.
34. Ferretta A., Gaballo A., Tanzarella P., Piccoli C., Capitanio N., Nico B., Annese T., Di Paola M., Dell'aquila C., De Mari M., Ferranini E., Bonifati V., Pacelli C., Cocco T. Effect of resveratrol on mitochondrial function: implications in parkin-associated familiar Parkinson's disease. Biochim. Biophys. Acta 2014, 1842:902-915.
35. Chakraborty A., Chowdhury S., Bhattacharyya M. Effect of metformin on oxidative stress, nitrosative stress and inflammatory biomarkers in type 2 diabetes patients. Diabetes Res. Clin. Pract. 2011, 93:56-62.
36. Salminen A., Hyttinen J.M., Kaarniranta K. AMP-activated protein kinase inhibits NF-kappaB signaling and inflammation: impact on healthspan and lifespan. J. Mol. Med. (Berl.) 2011, 89:667-676.
37. Chiang M.C., Lin H., Cheng Y.C., Yen C.H., Huang R.N., Lin K.H. Beta-adrenoceptor pathway enhances mitochondrial function in human neural stem cells via rotary cell culture system. J. Neurosci. Methods 2012, 207:130-136.
38. Chiang M.C., Cheng Y.C., Chen H.M., Liang Y.J., Yen C.H. Rosiglitazone promotes neurite outgrowth and mitochondrial function in N2A cells via PPARgamma pathway. Mitochondrion 2014, 14:7-17.
39. Chiang M.C., Cheng Y.C., Lin K.H., Yen C.H. PPARgamma regulates the mitochondrial dysfunction in human neural stem cells with tumor necrosis factor alpha. Neuroscience 2013, 229:118-129.
40. Chiang M.C., Chern Y., Huang R.N. PPARgamma rescue of the mitochondrial dysfunction in Huntington's disease. Neurobiol. Dis. 2012, 45:322-328.
41. Chiang M.C., Chern Y., Juo C.G. The dysfunction of hepatic transcriptional factors in mice with Huntington's disease. Biochim. Biophys. Acta 2011, 1812:1111-1120.
42. Ramasamy R., Vannucci S.J., Yan S.S., Herold K., Yan S.F., Schmidt A.M. Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. Glycobiology 2005, 15:16R-28R.
43. Srikanth V., Maczurek A., Phan T., Steele M., Westcott B., Juskiw D., Munch G. Advanced glycation endproducts and their receptor RAGE in Alzheimer's disease. Neurobiol. Aging 2011, 32:763-777.
44. Yan S.F., Yan S.D., Ramasamy R., Schmidt A.M. Tempering the wrath of RAGE: an emerging therapeutic strategy against diabetic complications, neurodegeneration, and inflammation. Ann. Med. 2009, 41:408-422.
45. Ishibashi Y., Yamagishi S., Matsui T., Ohta K., Tanoue R., Takeuchi M., Ueda S., Nakamura K., Okuda S. Pravastatin inhibits advanced glycation end products (AGEs)-induced proximal tubular cell apoptosis and injury by reducing receptor for AGEs (RAGE) level. Metab. Clin. Exp. 2012, 61:1067-1072.
46. Gasic-Milenkovic J., Loske C., Munch G. Advanced glycation endproducts cause lipid peroxidation in the human neuronal cell line SH-SY5Y. J. Alzheimers Dis. 2003, 5:25-30.
47. Chang P.C., Chong L.Y., Tsai S.C., Lim L.P. Aminoguanidine inhibits the AGE-RAGE axis to modulate the induction of periodontitis but has limited effects on the progression and recovery of experimental periodontitis: a preliminary study. J. Periodontol. 2014, 85:729-739.
48. Thornalley P.J. Use of aminoguanidine (pimagedine) to prevent the formation of advanced glycation endproducts. Arch. Biochem. Biophys. 2003, 419:31-40.
49. Green D.R., Reed J.C. Mitochondria and apoptosis. Science 1998, 281:1309-1312.
50. Naseer M.I., Ullah I., Narasimhan M.L., Lee H.Y., Bressan R.A., Yoon G.H., Yun D.J., Kim M.O. Neuroprotective effect of osmotin against ethanol-induced apoptotic neurodegeneration in the developing rat brain. Cell Death Dis. 2014, 5:e1150.
51. Saito M., Chakraborty G., Mao R.F., Wang R., Cooper T.B., Vadasz C. Ethanol alters lipid profiles and phosphorylation status of AMP-activated protein kinase in the neonatal mouse brain. J. Neurochem. 2007, 103:1208-1218.
52. Shirwany N.A., Zou M.H. AMPK: a cellular metabolic and redox sensor. A minireview. Front Biosci. 2014, 19:447-474. Landmark ed.
53. Scarpulla R.C. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim. Biophys. Acta 2011, 1813:1269-1278.
54. Jager S., Handschin C., St-Pierre J., Spiegelman B.M. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12017-12022.
55. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 2003, 24:78-90.
56. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
57. Pagel-Langenickel I., Bao J., Joseph J.J., Schwartz D.R., Mantell B.S., Xu X., Raghavachari N., Sack M.N. PGC-1alpha integrates insulin signaling, mitochondrial regulation, and bioenergetic function in skeletal muscle. J. Biol. Chem. 2008, 283:22464-22472.
58. Jimenez-Flores L.M., Lopez-Briones S., Macias-Cervantes M.H., Ramirez-Emiliano J., Perez-Vazquez V. A PPARgamma, NF-kappaB and AMPK-dependent mechanism may be involved in the beneficial effects of curcumin in the diabetic db/db mice liver. Molecules 2014, 19:8289-8302.
59. Alrashed F., Calay D., Thornton C., Bauer A., Kiprianos A., Haskard D., Boyle J., Mason J. P179Celecoxib-mediated activation of an AMPK-CREB-Nrf2 dependent pathway: a novel mechanism for endothelial cytoprotection in chronic systemic inflammation. Cardiovasc. Res. 2014, 103(Suppl. 1):S31-S32.
60. Xu J.N., Zeng C., Zhou Y., Peng C., Zhou Y.F., Xue Q. Metformin inhibits StAR expression in human endometrial stromal cells via AMPK-mediated disruption of CREB-CRTC2 complex formation. J. Clin. Endocrinol. Metab. 2014, 99:2795-2803.
61. Hamdulay S.S., Wang B., Calay D., Kiprianos A.P., Cole J., Dumont O., Dryden N., Randi A.M., Thornton C.C., Al-Rashed F., Hoong C., Shamsi A., Liu Z., Holla V.R., Boyle J.J., Haskard D.O., Mason J.C. Synergistic therapeutic vascular cytoprotection against complement-mediated injury induced via a PKCalpha-AMPK-, and CREB-dependent pathway. J. Immunol. 2014, 192:4316-4327.
62. Moran C., Sanz-Rodriguez A., Jimenez-Pacheco A., Martinez-Villareal J., McKiernan R.C., Jimenez-Mateos E.M., Mooney C., Woods I., Prehn J.H., Henshall D.C., Engel T. Bmf upregulation through the AMP-activated protein kinase pathway may protect the brain from seizure-induced cell death. Cell Death Dis. 2013, 4:e606.
63. Kuhla B., Loske C., Garcia De Arriba S., Schinzel R., Huber J., Munch G. Differential effects of "advanced glycation endproducts" and beta-amyloid peptide on glucose utilization and ATP levels in the neuronal cell line SH-SY5Y. J. Neural Transm. 2004, 111:427-439.
64. de Arriba S.G., Stuchbury G., Yarin J., Burnell J., Loske C., Munch G. Methylglyoxal impairs glucose metabolism and leads to energy depletion in neuronal cells-protection by carbonyl scavengers. Neurobiol. Aging 2007, 28:1044-1050.
65. Wareski P., Vaarmann A., Choubey V., Safiulina D., Liiv J., Kuum M., Kaasik A. PGC-1{alpha} and PGC-1{beta} regulate mitochondrial density in neurons. J. Biol. Chem. 2009, 284:21379-21385.
66. Kamal A., Biessels G.J., Duis S.E., Gispen W.H. Learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing. Diabetologia 2000, 43:500-506.
67. Ullah I., Ullah N., Naseer M.I., Lee H.Y., Kim M.O. Neuroprotection with metformin and thymoquinone against ethanol-induced apoptotic neurodegeneration in prenatal rat cortical neurons. BMC Neurosci. 2012, 13:11.
68. El-Mir M.Y., Detaille D., R.V.G., Delgado-Esteban M., Guigas B., Attia S., Fontaine E., Almeida A., Leverve X., Journal of molecular neuroscience Neuroprotective role of antidiabetic drug metformin against apoptotic cell death in primary cortical neurons. J. Mol. Neurosci. 2008, 34:77-87. MN.
69. Reznick R.M., Zong H., Li J., Morino K., Moore I.K., Yu H.J., Liu Z.X., Dong J., Mustard K.J., Hawley S.A., Befroy D., Pypaert M., Hardie D.G., Young L.H., Shulman G.I. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab. 2007, 5:151-156.
70. Price N.L., Gomes A.P., Ling A.J., Duarte F.V., Martin-Montalvo A., North B.J., Agarwal B., Ye L., Ramadori G., Teodoro J.S., Hubbard B.P., Varela A.T., Davis J.G., Varamini B., Hafner A., Moaddel R., Rolo A.P., Coppari R., Palmeira C.M., de Cabo R., Baur J.A., Sinclair D.A. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012, 15:675-690.
71. Chowdhury S.K., Smith D.R., Fernyhough P. The role of aberrant mitochondrial bioenergetics in diabetic neuropathy. Neurobiol. Dis. 2013, 51:56-65.
72. Choi J., Chandrasekaran K., Inoue T., Muragundla A., Russell J.W. PGC-1alpha regulation of mitochondrial degeneration in experimental diabetic neuropathy. Neurobiol. Dis. 2014, 64:118-130.
73. Horvath T.L., Erion D.M., Elsworth J.D., Roth R.H., Shulman G.I., Andrews Z.B. GPA protects the nigrostriatal dopamine system by enhancing mitochondrial function. Neurobiol. Dis. 2011, 43:152-162.
74. Suwa M., Egashira T., Nakano H., Sasaki H., Kumagai S. Metformin increases the PGC-1alpha protein and oxidative enzyme activities possibly via AMPK phosphorylation in skeletal muscle in vivo. J. Appl. Physiol. 2006, 101:1685-1692.
75. Hardie D.G. AMPK: positive and negative regulation, and its role in whole-body energy homeostasis. Curr. Opin. Cell Biol. 2014, 33C:1-7.
76. Godoy J.A., Rios J.A., Zolezzi J.M., Braidy N., Inestrosa N.C. Signaling pathway cross talk in Alzheimer's disease. Cell Commun. Signal. 2014, 12:23.