Metformin increases APP expression and processing via oxidative stress, mitochondrial dysfunction and NF-κB activation: Use of insulin to attenuate metformin's effect

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 5, 2015, Pages 1046-1059

  Picone, Pasquale ^a   Nuzzo, Domenico ^a   Caruana, Luca ^a   Messina, Elisa ^a   Barera, Annalisa ^b   Vasto, Sonya ^a,b   Di Carlo, Marta ^a  

^a CNR Consiglio Nazionale delle Ricerche   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

Author keywords

Alzheimer's disease; Antidiabetic drug; Antioxidant; Insulin; NF B; Oxidative stress

Indexed keywords

3 (4 TERT BUTYLPHENYLSULFONYL) 2 PROPENENITRILE; AMYLOID PRECURSOR PROTEIN; CURCUMIN; CYTOCHROME C; FERULIC ACID; HEXOKINASE; INSULIN; METFORMIN; PRESENILIN; PRESENILIN 1; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TRANSCRIPTION FACTOR; ADENYLATE KINASE; AMYLOID BETA PROTEIN; ANTIOXIDANT; APP PROTEIN, HUMAN; ASPARTIC PROTEINASE; BACE1 PROTEIN, MOUSE; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SECRETASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL DEATH; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFECT; DRUG MECHANISM; ENZYME RELEASE; EX VIVO STUDY; IN VITRO STUDY; MALE; MOUSE; NEUROBLASTOMA CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; ADULT; ANIMAL; BIOLOGICAL MODEL; BRAIN; C57BL MOUSE; CELL PROTECTION; DRUG EFFECTS; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; MITOCHONDRION; MONONUCLEAR CELL; PATHOLOGY; PROTEIN TRANSPORT; TUMOR CELL LINE;

ADENYLATE KINASE; ADULT; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIOXIDANTS; ASPARTIC ACID ENDOPEPTIDASES; BRAIN; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPROTECTION; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; INSULIN; LEUKOCYTES, MONONUCLEAR; MALE; METFORMIN; MICE, INBRED C57BL; MITOCHONDRIA; MODELS, BIOLOGICAL; NF-KAPPA B; OXIDATIVE STRESS; PRESENILIN-1; PROTEIN TRANSPORT;

EID: 84923345656     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.01.017     Document Type: Article

References (50)

1. Selkoe D.J. The cell biology of β-amyloid precursor protein and presenilin in Alzheimer's disease. Trends Cell Biol. 1998, 8:447-453.
2. Cole S.L., Vassar R. The Alzheimer's disease beta-secretase enzyme, BACE1. Mol. Neurodegener. 2007, 2:1-25.
3. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., Klein W.L. Diffusible, nonfibrillar ligands derived from A-beta 1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6448-6453.
4. Gong Y., Chang L., Viola K.L., Lacor P.N., Lambert M.P., Finch C.E., Krafft G.A., Klein W.L. Alzheimer's disease-affected brain: presence of oligomeric Abeta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl. Acad. Sci. U. S. A. 1998, 100:10417-10422.
5. Beeri S.M., Goldbourt U., Silverman J.M., Noy S., Schmeidler J., Ravona-Springer R., Sverdlick A., Davidson M. Diabetes mellitus in midlife and the risk of dementia three decades later. Neurology 2004, 63:1902-1907.
6. De Felice F.G. Alzheimer's disease and insulin resistance: translating basic science into clinical applications. J. Clin. Invest. 2013, 123:531-539.
7. Gasparini L., Xu H. Potential roles of insulin and IGF-1 in Alzheimer's disease. Trends Neurosci. 2003, 26:404-406.
8. Reger M.A., Watson G.S., Green P.S., Baker L.D., Cholerton B., Fishel M.A., Plymate S.R., Cherrier M.M., Schellenberg G.D., Frey W., Craft S. Intranasal insulin improves cognition and modulates beta-amyloid in early AD. J. Alzheimers Dis. 2008, 13:323-331.
9. Craft S., Baker L.D., Montine T.J., Minoshima S., Watson G.S., Claxton A., Arbuckle M., Callaghan M., Tsai E., Plymate S.R., Green P.S., Leverenz J., Cross D., Gerton B. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch. Neurol. 2012, 69:29-38.
10. Wang J., Gallagher D., DeVito L.M., Cancino G.I., Tsui D., He L., Keller G.M., Frankland P.W., Kaplan D.R., Miller F.D. Metformin activates an atypical PKC-CBP pathway to promote neurogenesis and enhance spatial memory formation. Cell Stem Cell 2011, 11:23-35.
11. Chen Y., Zhou K., Wang R., Liu Y., Kwak Y.D., Ma T., Thompson R.C., Zhao Y., Smith L., Gasparini L., Luo Z., Xu H., Liao F.F. Antidiabetic drug metformin (GlucophageR) increases biogenesis of Alzheimer's amyloid peptides via up-regulating BACE1 transcription. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3907-3912.
12. Beeri M.S., Schmeidler J., Silverman J.M., et al. Insulin in combination with other diabetes medication is associated with less Alzheimer neuropathology. Neurology 2008, 71:750-757.
13. Imfeld P., Bodmer M., Jick S.S., Meier C.R. Metformin, other antidiabetic drugs, and risk of Alzheimer's disease: a population-based case-control study. J. Am. Geriatr. Soc. 2012, 60:916-921.
14. Zhou G., Myers R., Li Y., Chen Y., Shen X., Fenyk-Melody J., Wu M., Ventre J., Doebber T., Fujii N., Musi N., Hirshman M.F., Goodyear L.J., Moller D.E. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 2001, 108:1167-1174.
15. Di Carlo M., Picone P., Carrotta R., Giacomazza D., San Biagio P.L. Insulin promotes survival of amyloid-beta oligomers neuroblastoma damaged cells via caspase 9 inhibition and Hsp70 upregulation. J. Biomed. Biotechnol. 2010, (Published online). 10.1155/2010/147835.
16. Picone P., Giacomazza D., Vetri V., Carrotta R., Militello V., San Biagio P.L., Di Carlo M. Insulin-activated Akt rescues Aβ oxidative stress-induced cell death by orchestrating molecular trafficking. Aging Cell 2011, 10:832-843.
17. Kang S., Song J., Kang H., Kim S., Lee Y., Park D. Insulin can block apoptosis by decreasing oxidative stress via phosphatidylinositol 3-kinase- and extracellular signal-regulated protein kinase-dependent signaling pathways in HepG2 cells. Eur. J. Endocrinol. 2003, 148:147-155.
18. Di Carlo M. Beta amyloid peptide: from different aggregation forms to the activation of different biochemical pathways. Eur. Biophys. J. 2010, 39:877-888.
19. Velez-Pardo C., Ospina G.G., Jimenez del Rio M. Abeta peptide and iron promote apoptosis in lymphocytes by an oxidative stress mechanism: involvement of H2O2, caspase-3, NF-kappaB, p53 and c-Jun. Neurotoxicology 2002, 23:351-365.
20. Pellicanò M., Bulati M., Buffa S., Barbagallo M., Di Prima A., Misiano G., Picone P., Di Carlo M., Nuzzo D., Candore G., Vasto S., Lio D., Caruso C., Colonna-Romano G. Systemic immune responses in Alzheimer's disease: in vitro mononuclear cell activation and cytokine production. J. Alzheimers Dis. 2010, 21:181-192.
21. Graf E. Antioxidant potential of ferulic acid. Free Radic. Biol. Med. 1992, 13:435-448.
22. Menon V.P., Sudheer A.R. Antioxidant and anti-inflammatory properties of curcumin. Adv. Exp. Med. Biol. 2007, 595:105-125.
23. Chami L., Buggia-Prévot V., Duplan E., Delprete D., Chami M., Peyron J.F., Checler F. Nuclear factor-κB regulates βAPP and β- and γ-secretases differently at physiological and supraphysiological Aβ concentrations. J. Biol. Chem. 2012, 287:24573-24584.
24. Behl C., Davis J.B., Lesley R., Schubert D. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 1997, 77:817-827.
25. Di Carlo M., Giacomazza D., Picone P., Nuzzo D., San Biagio P.L. Are oxidative stress and mitochondrial dysfunction the key player in the neurodegenerative diseases?. Free Radic. Res. 2012, 46:1327-1338.
26. Gasparini L., Gouras G.K., Wang R., Gross R.S., Beal M.F., Greengard P., Xu H. Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. J. Neurosci. 2001, 21:2561-2570.
27. Dandona P., Islam M., Ghanim H., Sia C.L., Dhindsa S., Dandona S., Makdissi A., Chaudhuri A. Insulin suppresses the expression of amyloid precursor protein, presenilins, and glycogen synthase kinase-3β in peripheral blood mononuclear cells. J. Clin. Endocrinol. Metab. 2011, 96:1783-1788.
28. Kanski J., Aksenova M., Stoyanova A., Butterfield D.A. Ferulic acid antioxidant protection against hydroxyl and peroxyl radical oxidation in synaptosomal and neuronal cell culture systems in vitro: structure-activity studies. J. Nutr. Biochem. 2002, 13:273-281.
29. Picone P., Bondì M.L., Montana G., Bruno A., Pitarresi G., Giammona G., Di Carlo M. Ferulic acid inhibits oxidative stress and cell death induced by Ab oligomers: improved delivery by solid lipid nanoparticles. Free Radic. Res. 2009, 43:1133-1145.
30. Pocernich C.B., Lange M.L.B., Sultana R., Butterfield D.A. Nutritional approaches to modulate oxidative stress in Alzheimer's disease. Curr. Alzheimer Res. 2011, 8:452-469.
31. Di Carlo M., Giacomazza D., San Biagio P.L. Alzheimer's disease: biological aspects, therapeutic perspectives and diagnostic tools. J. Biophys. Condens. Matter 2012, 24:244102-244119.
32. El-Mir M.Y., Nogueira V., Fontaine E., et al. Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 2000, 275:223-228.
33. Detaille D., Guigas B., Leverve X., et al. Obligatory role of membrane events in the regulatory effect of metformin on the respiratory chain function. Biochem. Pharmacol. 2002, 63:1259-1272.
34. Guigas B., Detaille D., Chauvin C., et al. Metformin inhibits mitochondrial permeability transition and cell death: a pharmacological in vitro study. Biochem. J. 2004, 382:877-884.
35. Detaille D., Guigas B., Chauvin C., et al. Metformin prevents high-glucose-induced endothelial cell death trough a mitochondrial permeability transition dependent process. Diabetes 2005, 54:2179-2187.
36. Isakovic A., Harhaji L., Stevanovic D., et al. Dual antiglioma action of metformin: cell cycle arrest and mitochondria-dependent apoptosis. Cell. Mol. Life Sci. 2007, 64:1290-1302.
37. Carvalho C., Correia S., Santos M.S., Seic R., Oliveira C.R., Moreira P.I. Metformin promotes isolated rat liver mitochondria impairment. Mol. Cell. Biochem. 2008, 308:75-83.
38. Wang X., Tao L., Hai X.C. Redox-regulating role of insulin: the essence of insulin effect. Mol. Cell. Endocrinol. 2012, 349:111-127.
39. Moreira P.I., Santos M.S., Sena C., Seica R., Oliveira C.R. Insulin protects against amyloid beta-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol. Dis. 2005, 18:628-637.
40. Moreira P.I., Zhu X., Wang X., Lee H., Nunomura A., Petersen R.B., Perry G., Smith M.A. Mitochondria: a therapeutic target in neurodegeneration. Biochim. Biophys. Acta 2010, 1802:212-220.
41. Bedard K., Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 2007, 87:245-313.
42. Shimohama S., Tanino H., Kawakami N., Okamura N., Kodama H., Yamaguchi T., Hayakawa T., Nunomura A., Chiba S., Perry G., Smith M.A., Fujimoto S. Activation of NADPH oxidase in Alzheimer's disease brains. Biochem. Biophys. Res. Commun. 2000, 273:5-9.
43. Ho L., Pieroni C., Winger D., Purohit D.P., Aisen P.S., Pasinetti G.M. Regional distribution of cyclooxygenase-2 in the hippocampal formation in Alzheimer's disease. J. Neurosci. Res. 1999, 57:295-303.
44. Perrin R., Briançon S., Jeandel C., Artur Y., Minn A., Penin F., Siest G. Blood activity of Cu/Zn superoxide dismutase, glutathione peroxidase and catalase in Alzheimer's disease: a case-control study. Gerontology 1990, 36:306-313.
45. Britschgi M., Wyss-Coray T. Systemic and acquired immune responses in Alzheimer's disease. Int. Rev. Neurobiol. 2007, 82:205-233.
46. Stieler J., Grimes R., Weber D., Gartner W., Sabbagh M., Arendt T. Multivariate analysis of differential lymphocyte cell cycle activity in Alzheimer's disease. Neurobiol. Aging 2012, 33:234-241.
47. Esteras N., Bartolomé F., Alquézar C., Antequera D., Muñoz Ú., Carro E., Martín-Requero Á. Altered cell cycle-related gene expression in brain and lymphocytes from a transgenic mouse model of Alzheimer's disease [amyloid precursor protein/presenilin 1 (PS1)]. Eur. J. Neurosci. 2012, 36:2609-2618.
48. Baeuerle P.A., Baltimore D. NF-kappa B: ten years after. Cell 1996, 87:13-20.
49. Choi D.Y., Lee J.W., Lin G., Lee Y.K., Lee Y.H., Choi I.S., Han S.B., Jung J.K., Kim Y.H., Kim K.H., Oh K.W., Hong J.T., Lee M.S. Obovatol attenuates LPS-induced memory impairments in mice via inhibition of NF-κB signaling pathway. Neurochem. Int. 2012, 60:68-77.
50. Valerio A., Boroni F., Benarese M., Sarnico I., Ghisi V., Bresciani L.G., Ferrario M., Borsani G., Spano P., Pizzi M. NF-kB pathway: a target for preventing β-amyloid (Aβ)-induced neuronal damage and Aβ42 production. Eur. J. Neurosci. 2006, 23:1711-1720.