Advertisement

AMPK in Neurodegenerative Diseases

  • Manon Domise
  • Valérie VingtdeuxEmail author
Part of the Experientia Supplementum book series (EXS, volume 107)

Abstract

Alzheimer’s disease, Parkinson’s disease, Huntington’s disease, and amyotrophic lateral sclerosis are neurodegenerative disorders that are characterized by a progressive degeneration of nerve cells eventually leading to dementia. While these diseases affect different neuronal populations and present distinct clinical features, they share in common several features and signaling pathways. In particular, energy metabolism defects, oxidative stress, and excitotoxicity are commonly described and might be correlated with AMP-activated protein kinase (AMPK) deregulation. AMPK is a master energy sensor which was reported to be overactivated in the brain of patients affected by these neurodegenerative disorders. While the exact role played by AMPK in these diseases remains to be clearly established, several studies reported the implication of AMPK in various signaling pathways that are involved in these diseases’ progression. In this chapter, we review the current literature regarding the involvement of AMPK in the development of these diseases and discuss the common pathways involved.

Keywords

AMPK Neurodegeneration Alzheimer’s disease Parkinson’s disease Huntington’s disease Amyotrophic lateral sclerosis 

Notes

Acknowledgments

This work was supported by the French Fondation pour la cooperation Scientifique—Plan Alzheimer 2008–2012 (Senior Innovative Grant 2013) and in part through the Labex DISTALZ (Development of Innovative Strategies for a Transdisciplinary Approach to Alzheimer’s Disease). MD holds a doctoral fellowship from Lille 2 University.

References

  1. Abbud W, Habinowski S, Zhang JZ, Kendrew J, Elkairi FS, Kemp BE, Witters LA, Ismail-Beigi F (2000) Stimulation of AMP-activated protein kinase (AMPK) is associated with enhancement of Glut1-mediated glucose transport. Arch Biochem Biophys 380(2):347–352PubMedCrossRefGoogle Scholar
  2. Abnous K, Storey KB (2008) Skeletal muscle hexokinase: regulation in mammalian hibernation. Mol Cell Biochem 319(1–2):41–50PubMedCrossRefGoogle Scholar
  3. Bae BI, Hara MR, Cascio MB, Wellington CL, Hayden MR, Ross CA, Ha HC, Li XJ, Snyder SH, Sawa A (2006) Mutant huntingtin: nuclear translocation and cytotoxicity mediated by GAPDH. Proc Natl Acad Sci USA 103(9):3405–3409PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barberger-Gateau P, Lambert JC, Feart C, Peres K, Ritchie K, Dartigues JF, Alperovitch A (2013) From genetics to dietetics: the contribution of epidemiology to understanding Alzheimer’s disease. J Alzheimers Dis 33(Suppl 1):S457–S463PubMedGoogle Scholar
  5. Beitz JM (2014) Parkinson’s disease: a review. Front Biosci (Schol Ed) 6:65–74CrossRefGoogle Scholar
  6. Bezprozvanny I, Mattson MP (2008) Neuronal calcium mishandling and the pathogenesis of Alzheimer’s disease. Trends Neurosci 31(9):454–463PubMedPubMedCentralCrossRefGoogle Scholar
  7. Blokhuis AM, Groen EJ, Koppers M, van den Berg LH, Pasterkamp RJ (2013) Protein aggregation in amyotrophic lateral sclerosis. Acta Neuropathol 125(6):777–794PubMedPubMedCentralCrossRefGoogle Scholar
  8. Browne SE, Bowling AC, MacGarvey U, Baik MJ, Berger SC, Muqit MM, Bird ED, Beal MF (1997) Oxidative damage and metabolic dysfunction in Huntington’s disease: selective vulnerability of the basal ganglia. Ann Neurol 41(5):646–653PubMedCrossRefGoogle Scholar
  9. Browne GJ, Finn SG, Proud CG (2004) Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J Biol Chem 279(13):12220–12231PubMedCrossRefGoogle Scholar
  10. Bubber P, Haroutunian V, Fisch G, Blass JP, Gibson GE (2005) Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann Neurol 57(5):695–703PubMedCrossRefGoogle Scholar
  11. Burke JR, Enghild JJ, Martin ME, Jou YS, Myers RM, Roses AD, Vance JM, Strittmatter WJ (1996) Huntingtin and DRPLA proteins selectively interact with the enzyme GAPDH. Nat Med 2(3):347–350PubMedCrossRefGoogle Scholar
  12. Cabezas-Opazo FA, Vergara-Pulgar K, Perez MJ, Jara C, Osorio-Fuentealba C, Quintanilla RA (2015) Mitochondrial dysfunction contributes to the pathogenesis of Alzheimer’s disease. Oxid Med Cell Longev 2015:509654PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chen Y, Zhou K, Wang R, Liu Y, Kwak YD, Ma T, Thompson RC, Zhao Y, Smith L, Gasparini L, Luo Z, Xu H, Liao FF (2009) Antidiabetic drug metformin (GlucophageR) increases biogenesis of Alzheimer’s amyloid peptides via up-regulating BACE1 transcription. Proc Natl Acad Sci USA 106(10):3907–3912PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chen Z, Shen X, Shen F, Zhong W, Wu H, Liu S, Lai J (2013) TAK1 activates AMPK-dependent cell death pathway in hydrogen peroxide-treated cardiomyocytes, inhibited by heat shock protein-70. Mol Cell Biochem 377(1–2):35–44PubMedCrossRefGoogle Scholar
  15. Choi JS, Park C, Jeong JW (2010) AMP-activated protein kinase is activated in Parkinson’s disease models mediated by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Biochem Biophys Res Commun 391(1):147–151PubMedCrossRefGoogle Scholar
  16. Chou SY, Lee YC, Chen HM, Chiang MC, Lai HL, Chang HH, Wu YC, Sun CN, Chien CL, Lin YS, Wang SC, Tung YY, Chang C, Chern Y (2005) CGS21680 attenuates symptoms of Huntington’s disease in a transgenic mouse model. J Neurochem 93(2):310–320PubMedCrossRefGoogle Scholar
  17. Ciarmiello A, Giovacchini G, Orobello S, Bruselli L, Elifani F, Squitieri F (2012) 18F-FDG PET uptake in the pre-Huntington disease caudate affects the time-to-onset independently of CAG expansion size. Eur J Nucl Med Mol Imaging 39(6):1030–1036PubMedCrossRefGoogle Scholar
  18. Connolly NM, Dussmann H, Anilkumar U, Huber HJ, Prehn JH (2014) Single-cell imaging of bioenergetic responses to neuronal excitotoxicity and oxygen and glucose deprivation. J Neurosci 34(31):10192–10205PubMedCrossRefGoogle Scholar
  19. Coughlan KS, Mitchem MR, Hogg MC, Prehn JH (2015) “Preconditioning” with latrepirdine, an adenosine 5′-monophosphate-activated protein kinase activator, delays amyotrophic lateral sclerosis progression in SOD1(G93A) mice. Neurobiol Aging 36(2):1140–1150PubMedCrossRefGoogle Scholar
  20. Dash PK, Orsi SA, Moore AN (2006) Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-Mammalian target of rapamycin pathway. J Neurosci 26(31):8048–8056PubMedCrossRefGoogle Scholar
  21. Davis JD, Lin SY (2011) DNA damage and breast cancer. World J Clin Oncol 2(9):329–338PubMedPubMedCentralCrossRefGoogle Scholar
  22. Djouder N, Tuerk RD, Suter M, Salvioni P, Thali RF, Scholz R, Vaahtomeri K, Auchli Y, Rechsteiner H, Brunisholz RA, Viollet B, Makela TP, Wallimann T, Neumann D, Krek W (2010) PKA phosphorylates and inactivates AMPKalpha to promote efficient lipolysis. EMBO J 29(2):469–481PubMedCrossRefGoogle Scholar
  23. Domise M, Didier S, Marinangeli C, Zhao H, Chandakkar P, Buée L, Viollet B, Davies P, Marambaud P, Vingtdeux V (2016) AMP-activated protein kinase modulates tau phosphorylation and tau pathology in vivo. Sci Rep 6:26758PubMedPubMedCentralCrossRefGoogle Scholar
  24. DuBoff B, Feany M, Gotz J (2013) Why size matters—balancing mitochondrial dynamics in Alzheimer’s disease. Trends Neurosci 36(6):325–335PubMedCrossRefGoogle Scholar
  25. Dulovic M, Jovanovic M, Xilouri M, Stefanis L, Harhaji-Trajkovic L, Kravic-Stevovic T, Paunovic V, Ardah MT, El-Agnaf OM, Kostic V, Markovic I, Trajkovic V (2014) The protective role of AMP-activated protein kinase in alpha-synuclein neurotoxicity in vitro. Neurobiol Dis 63:1–11PubMedCrossRefGoogle Scholar
  26. Dupuis L, Pradat PF, Ludolph AC, Loeffler JP (2011) Energy metabolism in amyotrophic lateral sclerosis. Lancet Neurol 10(1):75–82PubMedCrossRefGoogle Scholar
  27. Eckert T, Barnes A, Dhawan V, Frucht S, Gordon MF, Feigin AS, Eidelberg D (2005) FDG PET in the differential diagnosis of parkinsonian disorders. Neuroimage 26(3):912–21PubMedCrossRefGoogle Scholar
  28. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ (2011) Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331(6016):456–461PubMedCrossRefGoogle Scholar
  29. Ferreira IL, Resende R, Ferreiro E, Rego AC, Pereira CF (2010) Multiple defects in energy metabolism in Alzheimer’s disease. Curr Drug Targets 11(10):1193–1206PubMedCrossRefGoogle Scholar
  30. 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 (2014) Effect of resveratrol on mitochondrial function: implications in parkin-associated familiar Parkinson’s disease. Biochim Biophys Acta 1842(7):902–915PubMedCrossRefGoogle Scholar
  31. Fischer D, Mukrasch MD, Biernat J, Bibow S, Blackledge M, Griesinger C, Mandelkow E, Zweckstetter M (2009) Conformational changes specific for pseudophosphorylation at serine 262 selectively impair binding of tau to microtubules. Biochemistry 48(42):10047–10055PubMedCrossRefGoogle Scholar
  32. Fu J, Jin J, Cichewicz RH, Hageman SA, Ellis TK, Xiang L, Peng Q, Jiang M, Arbez N, Hotaling K, Ross CA, Duan W (2012) trans-(-)-epsilon-Viniferin increases mitochondrial sirtuin 3 (SIRT3), activates AMP-activated protein kinase (AMPK), and protects cells in models of Huntington Disease. J Biol Chem 287(29):24460–24472PubMedPubMedCentralCrossRefGoogle Scholar
  33. Garcia-Escudero V, Martin-Maestro P, Perry G, Avila J (2013) Deconstructing mitochondrial dysfunction in Alzheimer disease. Oxid Med Cell Longev 2013:162152PubMedPubMedCentralCrossRefGoogle Scholar
  34. Gouarne C, Tardif G, Tracz J, Latyszenok V, Michaud M, Clemens LE, Yu-Taeger L, Nguyen HP, Bordet T, Pruss RM (2013) Early deficits in glycolysis are specific to striatal neurons from a rat model of huntington disease. PLoS One 8(11):e81528PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gowans GJ, Hawley SA, Ross FA, Hardie DG (2013) AMP is a true physiological regulator of AMP-activated protein kinase by both allosteric activation and enhancing net phosphorylation. Cell Metab 18(4):556–566PubMedPubMedCentralCrossRefGoogle Scholar
  36. Greco SJ, Sarkar S, Johnston JM, Tezapsidis N (2009) Leptin regulates tau phosphorylation and amyloid through AMPK in neuronal cells. Biochem Biophys Res Commun 380(1):98–104PubMedPubMedCentralCrossRefGoogle Scholar
  37. Greco SJ, Hamzelou A, Johnston JM, Smith MA, Ashford JW, Tezapsidis N (2011) Leptin boosts cellular metabolism by activating AMPK and the sirtuins to reduce tau phosphorylation and beta-amyloid in neurons. Biochem Biophys Res Commun 414(1):170–174PubMedPubMedCentralCrossRefGoogle Scholar
  38. Green KN, LaFerla FM (2008) Linking calcium to Abeta and Alzheimer’s disease. Neuron 59(2):190–194PubMedCrossRefGoogle Scholar
  39. Grimm A, Schmitt K, Eckert A (2016) Advanced mitochondrial respiration assay for evaluation of mitochondrial dysfunction in Alzheimer’s disease. Methods Mol Biol 1303:171–183PubMedCrossRefGoogle Scholar
  40. Gu M, Gash MT, Mann VM, Javoy-Agid F, Cooper JM, Schapira AH (1996) Mitochondrial defect in Huntington’s disease caudate nucleus. Ann Neurol 39(3):385–389PubMedCrossRefGoogle Scholar
  41. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30(2):214–226PubMedPubMedCentralCrossRefGoogle Scholar
  42. Harold D, Abraham R, Hollingworth P, Sims R, Gerrish A, Hamshere ML, Pahwa JS, Moskvina V, Dowzell K, Williams A, Jones N, Thomas C, Stretton A, Morgan AR, Lovestone S, Powell J, Proitsi P, Lupton MK, Brayne C, Rubinsztein DC, Gill M, Lawlor B, Lynch A, Morgan K, Brown KS, Passmore PA, Craig D, McGuinness B, Todd S, Holmes C, Mann D, Smith AD, Love S, Kehoe PG, Hardy J, Mead S, Fox N, Rossor M, Collinge J, Maier W, Jessen F, Schurmann B, Heun R, van den Bussche H, Heuser I, Kornhuber J, Wiltfang J, Dichgans M, Frolich L, Hampel H, Hull M, Rujescu D, Goate AM, Kauwe JS, Cruchaga C, Nowotny P, Morris JC, Mayo K, Sleegers K, Bettens K, Engelborghs S, De Deyn PP, Van Broeckhoven C, Livingston G, Bass NJ, Gurling H, McQuillin A, Gwilliam R, Deloukas P, Al-Chalabi A, Shaw CE, Tsolaki M, Singleton AB, Guerreiro R, Muhleisen TW, Nothen MM, Moebus S, Jockel KH, Klopp N, Wichmann HE, Carrasquillo MM, Pankratz VS, Younkin SG, Holmans PA, O’Donovan M, Owen MJ, Williams J (2009) Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer’s disease. Nat Genet 41(10):1088–1093PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR, Hardie DG (2003) Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2(4):28PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG (2005) Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2(1):9–19PubMedCrossRefGoogle Scholar
  45. Hirai K, Aliev G, Nunomura A, Fujioka H, Russell RL, Atwood CS, Johnson AB, Kress Y, Vinters HV, Tabaton M, Shimohama S, Cash AD, Siedlak SL, Harris PL, Jones PK, Petersen RB, Perry G, Smith MA (2001) Mitochondrial abnormalities in Alzheimer’s disease. J Neurosci 21(9):3017–3023PubMedGoogle Scholar
  46. Horman S, Browne G, Krause U, Patel J, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud C, Rider M (2002) Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12(16):1419–1423PubMedCrossRefGoogle Scholar
  47. Horman S, Vertommen D, Heath R, Neumann D, Mouton V, Woods A, Schlattner U, Wallimann T, Carling D, Hue L, Rider MH (2006) Insulin antagonizes ischemia-induced Thr172 phosphorylation of AMP-activated protein kinase alpha-subunits in heart via hierarchical phosphorylation of Ser485/491. J Biol Chem 281(9):5335–5340PubMedCrossRefGoogle Scholar
  48. Hou YS, Guan JJ, Xu HD, Wu F, Sheng R, Qin ZH (2015) Sestrin2 protects dopaminergic cells against rotenone toxicity through AMPK-dependent autophagy activation. Mol Cell Biol 35(16):2740–2751PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hsu LJ, Sagara Y, Arroyo A, Rockenstein E, Sisk A, Mallory M, Wong J, Takenouchi T, Hashimoto M, Masliah E (2000) alpha-synuclein promotes mitochondrial deficit and oxidative stress. Am J Pathol 157(2):401–410PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, Witters LA (2005) The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem 280(32):29060–29066PubMedCrossRefGoogle Scholar
  51. Hwang S, Disatnik MH, Mochly-Rosen D (2015) Impaired GAPDH-induced mitophagy contributes to the pathology of Huntington’s disease. EMBO Mol Med 7(10):1307–1326PubMedPubMedCentralCrossRefGoogle Scholar
  52. Ingre C, Roos PM, Piehl F, Kamel F, Fang F (2015) Risk factors for amyotrophic lateral sclerosis. Clin Epidemiol 7:181–193PubMedPubMedCentralGoogle Scholar
  53. Inoki K, Zhu T, Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115(5):577–590PubMedCrossRefGoogle Scholar
  54. Jager S, Handschin C, St-Pierre J, Spiegelman BM (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci USA 104(29):12017–12022PubMedPubMedCentralCrossRefGoogle Scholar
  55. Jiang P, Gan M, Ebrahim AS, Castanedes-Casey M, Dickson DW, Yen SH (2013) Adenosine monophosphate-activated protein kinase overactivation leads to accumulation of alpha-synuclein oligomers and decrease of neurites. Neurobiol Aging 34(5):1504–1515PubMedCrossRefGoogle Scholar
  56. Ju TC, Chen HM, Lin JT, Chang CP, Chang WC, Kang JJ, Sun CP, Tao MH, Tu PH, Chang C, Dickson DW, Chern Y (2011) Nuclear translocation of AMPK-alpha1 potentiates striatal neurodegeneration in Huntington’s disease. J Cell Biol 194(2):209–227PubMedPubMedCentralCrossRefGoogle Scholar
  57. Ju TC, Chen HM, Chen YC, Chang CP, Chang C, Chern Y (2014) AMPK-alpha1 functions downstream of oxidative stress to mediate neuronal atrophy in Huntington’s disease. Biochim Biophys Acta 1842(9):1668–1680PubMedCrossRefGoogle Scholar
  58. Keeney PM, Xie J, Capaldi RA, Bennett JP Jr (2006) Parkinson’s disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J Neurosci 26(19):5256–5264PubMedCrossRefGoogle Scholar
  59. Kickstein E, Krauss S, Thornhill P, Rutschow D, Zeller R, Sharkey J, Williamson R, Fuchs M, Kohler A, Glossmann H, Schneider R, Sutherland C, Schweiger S (2010) Biguanide metformin acts on tau phosphorylation via mTOR/protein phosphatase 2A (PP2A) signaling. Proc Natl Acad Sci USA 107(50):21830–21835PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13(2):132–141PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kim TW, Cho HM, Choi SY, Suguira Y, Hayasaka T, Setou M, Koh HC, Hwang EM, Park JY, Kang SJ, Kim HS, Kim H, Sun W (2013) (ADP-ribose) polymerase 1 and AMP-activated protein kinase mediate progressive dopaminergic neuronal degeneration in a mouse model of Parkinson’s disease. Cell Death Dis 4:e919PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kim B, Figueroa-Romero C, Pacut C, Backus C, Feldman EL (2015) Insulin resistance prevents AMPK-induced tau dephosphorylation through Akt-mediated increase in AMPKSer-485 phosphorylation. J Biol Chem 290(31):19146–19157PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kish SJ, Lopes-Cendes I, Guttman M, Furukawa Y, Pandolfo M, Rouleau GA, Ross BM, Nance M, Schut L, Ang L, DiStefano L (1998) Brain glyceraldehyde-3-phosphate dehydrogenase activity in human trinucleotide repeat disorders. Arch Neurol 55(10):1299–1304PubMedCrossRefGoogle Scholar
  64. Kobilo T, Yuan C, van Praag H (2011) Endurance factors improve hippocampal neurogenesis and spatial memory in mice. Learn Mem 18(2):103–107PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kobilo T, Guerrieri D, Zhang Y, Collica SC, Becker KG, van Praag H (2014) AMPK agonist AICAR improves cognition and motor coordination in young and aged mice. Learn Mem 21(2):119–126PubMedPubMedCentralCrossRefGoogle Scholar
  66. Lambert JC, Heath S, Even G, Campion D, Sleegers K, Hiltunen M, Combarros O, Zelenika D, Bullido MJ, Tavernier B, Letenneur L, Bettens K, Berr C, Pasquier F, Fievet N, Barberger-Gateau P, Engelborghs S, De Deyn P, Mateo I, Franck A, Helisalmi S, Porcellini E, Hanon O, European Alzheimer’s Disease Initiative Investigators, de Pancorbo MM, Lendon C, Dufouil C, Jaillard C, Leveillard T, Alvarez V, Bosco P, Mancuso M, Panza F, Nacmias B, Bossu P, Piccardi P, Annoni G, Seripa D, Galimberti D, Hannequin D, Licastro F, Soininen H, Ritchie K, Blanche H, Dartigues JF, Tzourio C, Gut I, Van Broeckhoven C, Alperovitch A, Lathrop M, Amouyel P (2009) Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer’s disease. Nat Genet 41(10):1094–1099PubMedCrossRefGoogle Scholar
  67. Leuner K, Schutt T, Kurz C, Eckert SH, Schiller C, Occhipinti A, Mai S, Jendrach M, Eckert GP, Kruse SE, Palmiter RD, Brandt U, Drose S, Wittig I, Willem M, Haass C, Reichert AS, Muller WE (2012) Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation. Antioxid Redox Signal 16(12):1421–1433PubMedPubMedCentralCrossRefGoogle Scholar
  68. Li Y, Xu S, Mihaylova MM, Zheng B, Hou X, Jiang B, Park O, Luo Z, Lefai E, Shyy JY, Gao B, Wierzbicki M, Verbeuren TJ, Shaw RJ, Cohen RA, Zang M (2011) AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metab 13(4):376–388PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lim MA, Selak MA, Xiang Z, Krainc D, Neve RL, Kraemer BC, Watts JL, Kalb RG (2012) Reduced activity of AMP-activated protein kinase protects against genetic models of motor neuron disease. J Neurosci 32(3):1123–1141PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lin YT, Cheng JT, Liang LC, Ko CY, Lo YK, Lu PJ (2007) The binding and phosphorylation of Thr231 is critical for Tau’s hyperphosphorylation and functional regulation by glycogen synthase kinase 3beta. J Neurochem 103(2):802–813PubMedCrossRefGoogle Scholar
  71. Liu YJ, Ju TC, Chen HM, Jang YS, Lee LM, Lai HL, Tai HC, Fang JM, Lin YL, Tu PH, Chern Y (2015a) Activation of AMP-activated protein kinase alpha1 mediates mislocalization of TDP-43 in amyotrophic lateral sclerosis. Hum Mol Genet 24(3):787–801PubMedCrossRefGoogle Scholar
  72. Liu YJ, Lee LM, Lai HL, Chern Y (2015b) Aberrant activation of AMP-activated protein kinase contributes to the abnormal distribution of HuR in amyotrophic lateral sclerosis. FEBS Lett 589(4):432–439PubMedCrossRefGoogle Scholar
  73. Lu L, Zheng L, Si Y, Luo W, Dujardin G, Kwan T, Potochick NR, Thompson SR, Schneider DA, King PH (2014) Hu antigen R (HuR) is a positive regulator of the RNA-binding proteins TDP-43 and FUS/TLS: implications for amyotrophic lateral sclerosis. J Biol Chem 289(46):31792–31804PubMedPubMedCentralCrossRefGoogle Scholar
  74. Ma TC, Buescher JL, Oatis B, Funk JA, Nash AJ, Carrier RL, Hoyt KR (2007) Metformin therapy in a transgenic mouse model of Huntington’s disease. Neurosci Lett 411(2):98–103PubMedCrossRefGoogle Scholar
  75. Ma T, Chen Y, Vingtdeux V, Zhao H, Viollet B, Marambaud P, Klann E (2014) Inhibition of AMP-activated protein kinase signaling alleviates impairments in hippocampal synaptic plasticity induced by amyloid beta. J Neurosci 34(36):12230–12238PubMedPubMedCentralCrossRefGoogle Scholar
  76. Mairet-Coello G, Courchet J, Pieraut S, Courchet V, Maximov A, Polleux F (2013) The CAMKK2-AMPK kinase pathway mediates the synaptotoxic effects of Abeta oligomers through Tau phosphorylation. Neuron 78(1):94–108PubMedPubMedCentralCrossRefGoogle Scholar
  77. Mancuso R, del Valle J, Modol L, Martinez A, Granado-Serrano AB, Ramirez-Nunez O, Pallas M, Portero-Otin M, Osta R, Navarro X (2014) Resveratrol improves motoneuron function and extends survival in SOD1(G93A) ALS mice. Neurotherapeutics 11(2):419–432PubMedPubMedCentralGoogle Scholar
  78. Manwani B, McCullough LD (2013) Function of the master energy regulator adenosine monophosphate-activated protein kinase in stroke. J Neurosci Res 91(8):1018–1029PubMedPubMedCentralCrossRefGoogle Scholar
  79. Marangos PJ, Loftus T, Wiesner J, Lowe T, Rossi E, Browne CE, Gruber HE (1990) Adenosinergic modulation of homocysteine-induced seizures in mice. Epilepsia 31(3):239–246PubMedCrossRefGoogle Scholar
  80. Marsin AS, Bertrand L, Rider MH, Deprez J, Beauloye C, Vincent MF, Van den Berghe G, Carling D, Hue L (2000) Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol 10(20):1247–1255PubMedCrossRefGoogle Scholar
  81. Martin LJ, Pan Y, Price AC, Sterling W, Copeland NG, Jenkins NA, Price DL, Lee MK (2006) Parkinson’s disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. J Neurosci 26(1):41–50PubMedCrossRefGoogle Scholar
  82. Mattson MP (2007) Calcium and neurodegeneration. Aging Cell 6(3):337–350PubMedCrossRefGoogle Scholar
  83. Mochel F, Durant B, Meng X, O’Callaghan J, Yu H, Brouillet E, Wheeler VC, Humbert S, Schiffmann R, Durr A (2012) Early alterations of brain cellular energy homeostasis in Huntington disease models. J Biol Chem 287(2):1361–1370PubMedCrossRefGoogle Scholar
  84. Momcilovic M, Hong SP, Carlson M (2006) Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem 281(35):25336–25343PubMedCrossRefGoogle Scholar
  85. Mosconi L (2005) Brain glucose metabolism in the early and specific diagnosis of Alzheimer’s disease. FDG-PET studies in MCI and AD. Eur J Nucl Med Mol Imaging 32(4):486–510PubMedCrossRefGoogle Scholar
  86. Narendra D, Tanaka A, Suen DF, Youle RJ (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183(5):795–803PubMedPubMedCentralCrossRefGoogle Scholar
  87. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8(1):e1000298PubMedPubMedCentralCrossRefGoogle Scholar
  88. Ng CH, Guan MS, Koh C, Ouyang X, Yu F, Tan EK, O’Neill SP, Zhang X, Chung J, Lim KL (2012) AMP kinase activation mitigates dopaminergic dysfunction and mitochondrial abnormalities in Drosophila models of Parkinson’s disease. J Neurosci 32(41):14311–14317PubMedCrossRefGoogle Scholar
  89. Nixon RA, Yang DS (2011) Autophagy failure in Alzheimer’s disease—locating the primary defect. Neurobiol Dis 43(1):38–45PubMedPubMedCentralCrossRefGoogle Scholar
  90. Olah J, Klivenyi P, Gardian G, Vecsei L, Orosz F, Kovacs GG, Westerhoff HV, Ovadi J (2008) Increased glucose metabolism and ATP level in brain tissue of Huntington’s disease transgenic mice. FEBS J 275(19):4740–4755PubMedCrossRefGoogle Scholar
  91. Olanow CW, Tatton WG (1999) Etiology and pathogenesis of Parkinson’s disease. Annu Rev Neurosci 22:123–144PubMedCrossRefGoogle Scholar
  92. Perera ND, Sheean RK, Scott JW, Kemp BE, Horne MK, Turner BJ (2014) Mutant TDP-43 deregulates AMPK activation by PP2A in ALS models. PLoS One 9(4):e95549PubMedCrossRefGoogle Scholar
  93. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 118(6):2190–2199PubMedPubMedCentralGoogle Scholar
  94. Potter WB, O’Riordan KJ, Barnett D, Osting SM, Wagoner M, Burger C, Roopra A (2010) Metabolic regulation of neuronal plasticity by the energy sensor AMPK. PLoS One 5(2):e8996PubMedPubMedCentralCrossRefGoogle Scholar
  95. Powers WJ, Videen TO, Markham J, McGee-Minnich L, Antenor-Dorsey JV, Hershey T, Perlmutter JS (2007) Selective defect of in vivo glycolysis in early Huntington’s disease striatum. Proc Natl Acad Sci USA 104(8):2945–2949PubMedPubMedCentralCrossRefGoogle Scholar
  96. Reddy PH (2011) Abnormal tau, mitochondrial dysfunction, impaired axonal transport of mitochondria, and synaptic deprivation in Alzheimer’s disease. Brain Res 1415:136–148PubMedPubMedCentralCrossRefGoogle Scholar
  97. Renton AE, Chio A, Traynor BJ (2014) State of play in amyotrophic lateral sclerosis genetics. Nat Neurosci 17(1):17–23PubMedCrossRefGoogle Scholar
  98. Rowland LP, Shneider NA (2001) Amyotrophic lateral sclerosis. N Engl J Med 344(22):1688–1700PubMedCrossRefGoogle Scholar
  99. Russell RR 3rd, Bergeron R, Shulman GI, Young LH (1999) Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol 277(2 Pt 2):H643–H649PubMedGoogle Scholar
  100. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D (2007) Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 403(1):139–148PubMedPubMedCentralCrossRefGoogle Scholar
  101. Sato-Harada R, Okabe S, Umeyama T, Kanai Y, Hirokawa N (1996) Microtubule-associated proteins regulate microtubule function as the track for intracellular membrane organelle transports. Cell Struct Funct 21(5):283–295PubMedCrossRefGoogle Scholar
  102. Sayre LM, Perry G, Smith MA (2008) Oxidative stress and neurotoxicity. Chem Res Toxicol 21(1):172–188PubMedCrossRefGoogle Scholar
  103. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, Marsden CD (1990) Mitochondrial complex I deficiency in Parkinson’s disease. J Neurochem 54(3):823–827PubMedCrossRefGoogle Scholar
  104. Seshadri S, Fitzpatrick AL, Ikram MA, DeStefano AL, Gudnason V, Boada M, Bis JC, Smith AV, Carassquillo MM, Lambert JC, Harold D, Schrijvers EM, Ramirez-Lorca R, Debette S, Longstreth WT Jr, Janssens AC, Pankratz VS, Dartigues JF, Hollingworth P, Aspelund T, Hernandez I, Beiser A, Kuller LH, Koudstaal PJ, Dickson DW, Tzourio C, Abraham R, Antunez C, Du Y, Rotter JI, Aulchenko YS, Harris TB, Petersen RC, Berr C, Owen MJ, Lopez-Arrieta J, Varadarajan BN, Becker JT, Rivadeneira F, Nalls MA, Graff-Radford NR, Campion D, Auerbach S, Rice K, Hofman A, Jonsson PV, Schmidt H, Lathrop M, Mosley TH, Au R, Psaty BM, Uitterlinden AG, Farrer LA, Lumley T, Ruiz A, Williams J, Amouyel P, Younkin SG, Wolf PA, Launer LJ, Lopez OL, van Duijn CM, Breteler MM, CHARGE Consortium, GERAD1 Consortium, EADI1 Consortium (2010) Genome-wide analysis of genetic loci associated with Alzheimer disease. JAMA 303(18):1832–1840PubMedPubMedCentralCrossRefGoogle Scholar
  105. Shaw RJ (2009) LKB1 and AMP-activated protein kinase control of mTOR signalling and growth. Acta Physiol (Oxf) 196(1):65–80CrossRefGoogle Scholar
  106. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, Cantley LC (2004) The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 101(10):3329–3335PubMedPubMedCentralCrossRefGoogle Scholar
  107. Sheng ZH (2014) Mitochondrial trafficking and anchoring in neurons: new insight and implications. J Cell Biol 204(7):1087–1098PubMedPubMedCentralCrossRefGoogle Scholar
  108. Sherer TB, Betarbet R, Greenamyre JT (2002) Environment, mitochondria, and Parkinson’s disease. Neuroscientist 8(3):192–197PubMedGoogle Scholar
  109. Shin H, Kim MH, Lee SJ, Lee KH, Kim MJ, Kim JS, Cho JW (2013) Decreased metabolism in the cerebral cortex in early-stage Huntington’s disease: a possible biomarker of disease progression? J Clin Neurol 9(1):21–25PubMedPubMedCentralCrossRefGoogle Scholar
  110. Shirendeb U, Reddy AP, Manczak M, Calkins MJ, Mao P, Tagle DA, Reddy PH (2011) Abnormal mitochondrial dynamics, mitochondrial loss and mutant huntingtin oligomers in Huntington’s disease: implications for selective neuronal damage. Hum Mol Genet 20(7):1438–1455PubMedPubMedCentralCrossRefGoogle Scholar
  111. Smith R, Bacos K, Fedele V, Soulet D, Walz HA, Obermuller S, Lindqvist A, Bjorkqvist M, Klein P, Onnerfjord P, Brundin P, Mulder H, Li JY (2009) Mutant huntingtin interacts with {beta}-tubulin and disrupts vesicular transport and insulin secretion. Hum Mol Genet 18(20):3942–3954PubMedCrossRefGoogle Scholar
  112. Son SM, Jung ES, Shin HJ, Byun J, Mook-Jung I (2012) Abeta-induced formation of autophagosomes is mediated by RAGE-CaMKKbeta-AMPK signaling. Neurobiol Aging 33(5):1006e11–1006e23CrossRefGoogle Scholar
  113. Song W, Chen J, Petrilli A, Liot G, Klinglmayr E, Zhou Y, Poquiz P, Tjong J, Pouladi MA, Hayden MR, Masliah E, Ellisman M, Rouiller I, Schwarzenbacher R, Bossy B, Perkins G, Bossy-Wetzel E (2011) Mutant huntingtin binds the mitochondrial fission GTPase dynamin-related protein-1 and increases its enzymatic activity. Nat Med 17(3):377–382PubMedPubMedCentralCrossRefGoogle Scholar
  114. Song L, Chen L, Zhang X, Li J, Le W (2014) Resveratrol ameliorates motor neuron degeneration and improves survival in SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Biomed Res Int 2014:483501PubMedPubMedCentralGoogle Scholar
  115. Spasic MR, Callaerts P, Norga KK (2008) Drosophila alicorn is a neuronal maintenance factor protecting against activity-induced retinal degeneration. J Neurosci 28(25):6419–6429PubMedCrossRefGoogle Scholar
  116. Sui Y, Zhao Z, Liu R, Cai B, Fan D (2014) Adenosine monophosphate-activated protein kinase activation enhances embryonic neural stem cell apoptosis in a mouse model of amyotrophic lateral sclerosis. Neural Regen Res 9(19):1770–1778PubMedPubMedCentralCrossRefGoogle Scholar
  117. Tabrizi SJ, Cleeter MW, Xuereb J, Taanman JW, Cooper JM, Schapira AH (1999) Biochemical abnormalities and excitotoxicity in Huntington’s disease brain. Ann Neurol 45(1):25–32PubMedCrossRefGoogle Scholar
  118. Tenreiro S, Reimao-Pinto MM, Antas P, Rino J, Wawrzycka D, Macedo D, Rosado-Ramos R, Amen T, Waiss M, Magalhaes F, Gomes A, Santos CN, Kaganovich D, Outeiro TF (2014) Phosphorylation modulates clearance of alpha-synuclein inclusions in a yeast model of Parkinson’s disease. PLoS Genet 10(5):e1004302PubMedPubMedCentralCrossRefGoogle Scholar
  119. The Huntington’s Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cell 72(6):971–983CrossRefGoogle Scholar
  120. Thornton C, Bright NJ, Sastre M, Muckett PJ, Carling D (2011) AMP-activated protein kinase (AMPK) is a tau kinase, activated in response to amyloid beta-peptide exposure. Biochem J 434(3):503–512PubMedCrossRefGoogle Scholar
  121. Tian J, Yan YP, Zhou R, Lou HF, Rong Y, Zhang BR (2014) Soluble N-terminal fragment of mutant Huntingtin protein impairs mitochondrial axonal transport in cultured hippocampal neurons. Neurosci Bull 30(1):74–80PubMedCrossRefGoogle Scholar
  122. Tschape JA, Hammerschmied C, Muhlig-Versen M, Athenstaedt K, Daum G, Kretzschmar D (2002) The neurodegeneration mutant lochrig interferes with cholesterol homeostasis and Appl processing. EMBO J 21(23):6367–6376PubMedPubMedCentralCrossRefGoogle Scholar
  123. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, Gonzalez-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, Auburger G, Wood NW (2004) Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science 304(5674):1158–1160PubMedCrossRefGoogle Scholar
  124. Vergouts M, Marinangeli C, Ingelbrecht C, Genard G, Schakman O, Sternotte A, Calas AG, Hermans E (2015) Early ALS-type gait abnormalities in AMP-dependent protein kinase-deficient mice suggest a role for this metabolic sensor in early stages of the disease. Metab Brain Dis 30(6):1369–1377PubMedCrossRefGoogle Scholar
  125. Verstraeten A, Theuns J, Van Broeckhoven C (2015) Progress in unraveling the genetic etiology of Parkinson disease in a genomic era. Trends Genet 31(3):140–149PubMedCrossRefGoogle Scholar
  126. Vingtdeux V, Giliberto L, Zhao H, Chandakkar P, Wu Q, Simon JE, Janle EM, Lobo J, Ferruzzi MG, Davies P, Marambaud P (2010) AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J Biol Chem 285(12):9100–9113PubMedPubMedCentralCrossRefGoogle Scholar
  127. Vingtdeux V, Chandakkar P, Zhao H, d’Abramo C, Davies P, Marambaud P (2011a) Novel synthetic small-molecule activators of AMPK as enhancers of autophagy and amyloid-beta peptide degradation. FASEB J 25(1):219–231PubMedPubMedCentralCrossRefGoogle Scholar
  128. Vingtdeux V, Davies P, Dickson DW, Marambaud P (2011b) AMPK is abnormally activated in tangle- and pre-tangle-bearing neurons in Alzheimer’s disease and other tauopathies. Acta Neuropathol 121(3):337–349PubMedCrossRefGoogle Scholar
  129. Walker FO (2007) Huntington’s disease. Lancet 369(9557):218–228PubMedCrossRefGoogle Scholar
  130. Wang Y, Martinez-Vicente M, Kruger U, Kaushik S, Wong E, Mandelkow EM, Cuervo AM, Mandelkow E (2010) Synergy and antagonism of macroautophagy and chaperone-mediated autophagy in a cell model of pathological tau aggregation. Autophagy 6(1):182–183PubMedCrossRefGoogle Scholar
  131. Wang ZX, Tan L, Yu JT (2015) Axonal transport defects in Alzheimer’s disease. Mol Neurobiol 51(3):1309–1321PubMedCrossRefGoogle Scholar
  132. Weisova P, Concannon CG, Devocelle M, Prehn JH, Ward MW (2009) Regulation of glucose transporter 3 surface expression by the AMP-activated protein kinase mediates tolerance to glutamate excitation in neurons. J Neurosci 29(9):2997–3008PubMedCrossRefGoogle Scholar
  133. Weisova P, Davila D, Tuffy LP, Ward MW, Concannon CG, Prehn JH (2011) Role of 5′-adenosine monophosphate-activated protein kinase in cell survival and death responses in neurons. Antioxid Redox Signal 14(10):1863–1876PubMedCrossRefGoogle Scholar
  134. Weisova P, Alvarez SP, Kilbride SM, Anilkumar U, Baumann B, Jordan J, Bernas T, Huber HJ, Dussmann H, Prehn JH (2013) Latrepirdine is a potent activator of AMP-activated protein kinase and reduces neuronal excitability. Transl Psychiatry 3:e317PubMedPubMedCentralCrossRefGoogle Scholar
  135. Won JS, Im YB, Kim J, Singh AK, Singh I (2010) Involvement of AMP-activated-protein-kinase (AMPK) in neuronal amyloidogenesis. Biochem Biophys Res Commun 399(4):487–491PubMedPubMedCentralCrossRefGoogle Scholar
  136. Wong YC, Holzbaur EL (2014) The regulation of autophagosome dynamics by huntingtin and HAP1 is disrupted by expression of mutant huntingtin, leading to defective cargo degradation. J Neurosci 34(4):1293–1305PubMedPubMedCentralCrossRefGoogle Scholar
  137. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, Schlattner U, Wallimann T, Carlson M, Carling D (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13(22):2004–2008PubMedCrossRefGoogle Scholar
  138. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D (2005) Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2(1):21–33PubMedCrossRefGoogle Scholar
  139. Wu Y, Li X, Zhu JX, Xie W, Le W, Fan Z, Jankovic J, Pan T (2011) Resveratrol-activated AMPK/SIRT1/autophagy in cellular models of Parkinson’s disease. Neurosignals 19(3):163–174PubMedPubMedCentralCrossRefGoogle Scholar
  140. Wu CA, Chao Y, Shiah SG, Lin WW (2013) Nutrient deprivation induces the Warburg effect through ROS/AMPK-dependent activation of pyruvate dehydrogenase kinase. Biochim Biophys Acta 1833(5):1147–1156PubMedCrossRefGoogle Scholar
  141. Xiao B, Sanders MJ, Underwood E, Heath R, Mayer FV, Carmena D, Jing C, Walker PA, Eccleston JF, Haire LF, Saiu P, Howell SA, Aasland R, Martin SR, Carling D, Gamblin SJ (2011) Structure of mammalian AMPK and its regulation by ADP. Nature 472(7342):230–233PubMedPubMedCentralCrossRefGoogle Scholar
  142. Xu Y, Liu C, Chen S, Ye Y, Guo M, Ren Q, Liu L, Zhang H, Xu C, Zhou Q, Huang S, Chen L (2014) Activation of AMPK and inactivation of Akt result in suppression of mTOR-mediated S6K1 and 4E-BP1 pathways leading to neuronal cell death in in vitro models of Parkinson’s disease. Cell Signal 26(8):1680–1689PubMedPubMedCentralCrossRefGoogle Scholar
  143. Yang TT, Shih YS, Chen YW, Kuo YM, Lee CW (2015) Glucose regulates amyloid beta production via AMPK. J Neural Transm 122(10):1381–1390PubMedCrossRefGoogle Scholar
  144. Yoon SO, Park DJ, Ryu JC, Ozer HG, Tep C, Shin YJ, Lim TH, Pastorino L, Kunwar AJ, Walton JC, Nagahara AH, Lu KP, Nelson RJ, Tuszynski MH, Huang K (2012) JNK3 perpetuates metabolic stress induced by Abeta peptides. Neuron 75(5):824–837PubMedPubMedCentralCrossRefGoogle Scholar
  145. Youle RJ, Narendra DP (2011) Mechanisms of mitophagy. Nat Rev Mol Cell Biol 12(1):9–14PubMedPubMedCentralCrossRefGoogle Scholar
  146. Yu WH, Cuervo AM, Kumar A, Peterhoff CM, Schmidt SD, Lee JH, Mohan PS, Mercken M, Farmery MR, Tjernberg LO, Jiang Y, Duff K, Uchiyama Y, Naslund J, Mathews PM, Cataldo AM, Nixon RA (2005) Macroautophagy—a novel Beta-amyloid peptide-generating pathway activated in Alzheimer’s disease. J Cell Biol 171(1):87–98PubMedPubMedCentralCrossRefGoogle Scholar
  147. Zala D, Hinckelmann MV, Yu H, Lyra da Cunha MM, Liot G, Cordelieres FP, Marco S, Saudou F (2013) Vesicular glycolysis provides on-board energy for fast axonal transport. Cell 152(3):479–491PubMedCrossRefGoogle Scholar
  148. Zarei S, Carr K, Reiley L, Diaz K, Guerra O, Altamirano PF, Pagani W, Lodin D, Orozco G, Chinea A (2015) A comprehensive review of amyotrophic lateral sclerosis. Surg Neurol Int 6:171PubMedPubMedCentralCrossRefGoogle Scholar
  149. Zhao Z, Sui Y, Gao W, Cai B, Fan D (2015) Effects of diet on adenosine monophosphate-activated protein kinase activity and disease progression in an amyotrophic lateral sclerosis model. J Int Med Res 43(1):67–79PubMedCrossRefGoogle Scholar
  150. Zheng D, MacLean PS, Pohnert SC, Knight JB, Olson AL, Winder WW, Dohm GL (2001) Regulation of muscle GLUT-4 transcription by AMP-activated protein kinase. J Appl Physiol (1985) 91(3):1073–1083Google Scholar
  151. Zuccato C, Valenza M, Cattaneo E (2010) Molecular mechanisms and potential therapeutical targets in Huntington’s disease. Physiol Rev 90(3):905–981PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Univ. Lille, Inserm, CHU Lille, UMR-S 1172 – JPArc – Centre de Recherche Jean-Pierre AUBERTLilleFrance

Personalised recommendations