Insulin and IGF-1 regularize energy metabolites in neural cells expressing full-length mutant huntingtin

Neuropeptides

Volumn 58, Issue , 2016, Pages 73-81

  Naia, Luana ^a,b   Ribeiro, Márcio ^a   Rodrigues, Joana ^a   Duarte, Ana I ^a,c   Lopes, Carla ^a,c   Rosenstock, Tatiana R ^a,c   Hayden, Michael R ^d   Rego, A Cristina ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Energy metabolism; Huntington's disease; IGF 1; Insulin; Lactate; Lactate dehydrogenase; Pyruvate dehydrogenase

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CREATINE PHOSPHATE; HUNTINGTIN; INSULIN; LACTATE DEHYDROGENASE; LACTIC ACID; MESSENGER RNA; PROTEIN; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE E1ALPHA SUBUNIT; PYRUVIC ACID; SOMATOMEDIN C; UNCLASSIFIED DRUG; HTT PROTEIN, HUMAN;

ADENOSINE TRIPHOSPHATE ADENOSINE DIPHOSPHATE RATIO; ANALYTICAL PARAMETERS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CELL CULTURE; BRAIN METABOLISM; CELL MUTANT; CONTROLLED STUDY; CORPUS STRIATUM; DOWN REGULATION; EMBRYO; ENERGY METABOLISM; ENZYME ACTIVITY; ENZYME INACTIVATION; HUNTINGTON CHOREA; METABOLIC DISORDER; METABOLIC REGULATION; MOUSE; NERVE CELL; NONHUMAN; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STRIATAL CELL; ANIMAL; BRAIN CORTEX; CELL LINE; DISEASE MODEL; DRUG EFFECTS; GENE TARGETING; GENETICS; HUMAN; METABOLISM; MUTATION;

ANIMALS; CELL LINE; CEREBRAL CORTEX; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; GENE KNOCK-IN TECHNIQUES; HUMANS; HUNTINGTIN PROTEIN; HUNTINGTON DISEASE; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MICE; MUTATION; NEURONS;

EID: 84957398906     PISSN: 01434179     EISSN: 15322785     Source Type: Journal    
DOI: 10.1016/j.npep.2016.01.009     Document Type: Article

References (52)

1. Andreassen, O.A., Dedeoglu, A., Stanojevic, V., Hughes, D.B., Browne, S.E., Leech, C.A., Ferrante, R.J., Habener, J.F., Beal, M.F., Thomas, M.K., Huntington's disease of the endocrine pancreas: insulin deficiency and diabetes mellitus due to impaired insulin gene expression. Neurobiol. Dis. 11 (2002), 410–424.
2. Butterworth, J., Changes in nine enzyme markers for neurons, glia, and endothelial cells in agonal state and Huntington's disease caudate nucleus. J. Neurochem. 47 (1986), 583–587.
3. Carro, E., Trejo, J.L., Gomez-Isla, T., LeRoith, D., Torres-Aleman, I., Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat. Med. 8 (2002), 1390–1397.
4. Carter, C.J., Increased alanine aminotransferase activity in the Huntington's disease putamen. J. Neurol. Sci. 66 (1984), 27–32.
5. Cohen, E., Bieschke, J., Perciavalle, R.M., Kelly, J.W., Dillin, A., Opposing activities protect against age-onset proteotoxicity. Science 313:5793 (2006 Sep 15), 1604–1610.
6. Dedeoglu, A., Kubilus, J.K., Yang, L., Ferrante, K.L., Hersch, S.M., Beal, M.F., Ferrante, R.J., Creatine therapy provides neuroprotection after onset of clinical symptoms in Huntington's disease transgenic mice. J. Neurochem. 85 (2002), 1359–1367.
7. D'Ercole, A.J., Ye, P., O'Kusky, J.R., Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides 36:2–3 (2002), 209–220.
8. Duarte, A.I., Santos, P., Oliveira, C.R., Santos, M.S., Rego, A.C., Insulin neuroprotection against oxidative stress is mediated by Akt and GSK-3β signaling pathways and changes in protein expression. Biochim. Biophys. Acta 1783 (2008), 994–1002, 10.1016/j.bbamcr.2008.02.016.
9. Duarte, A.I., Petit, G.H., Ranganathan, S., Li, J.Y., Oliveira, C.R., Brundin, P., Björkqvist, M., Rego, A.C., IGF-1 protects against diabetic features in an in vivo model of Huntington's disease. Exp. Neurol. 231 (2011), 314–319, 10.1016/j.expneurol.2011.06.016.
10. Ferreira, I.L., Cunha-Oliveira, T., Nascimento, M.V., Ribeiro, M., Proença, M.T., Januário, C., Oliveira, C.R., Rego, A.C., Bioenergetic dysfunction in Huntington's disease human cybrids. Exp. Neurol. 231 (2011), 127–134, 10.1016/j.expneurol.2011.05.024.
11. Gårseth, M., Sonnewald, U., White, L.R., Rød, M., Zwart, J.A., Nygaard, O., Aasly, J., Proton magnetic resonance spectroscopy of cerebrospinal fluid in neurodegenerative disease: indication of glial energy impairment in Huntington chorea, but not Parkinson disease. J. Neurosci. Res. 60 (2000), 779–782.
12. Gil, J.M., Rego, A.C., Mechanisms of neurodegeneration in Huntington's disease. Eur. J. Neurosci. 27 (2008), 2803–2820, 10.1111/j.1460-9568.2008.06310.x.
13. Gines, S., Seong, I.S., Fossale, E., Ivanova, E., Trettel, F., Gusella, J.F., Wheeler, V.C., Persichetti, F., MacDonald, M.E., Specific progressive cAMP reduction implicates energy deficit in presymptomatic Huntington's disease knock-in mice. Hum. Mol. Genet. 12 (2003), 497–508.
14. Holzenberger, M., Dupont, J., Ducos, B., Leneuve, P., Géloën, A., Even, P.C., Cervera, P., Le Bouc, Y., IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421 (2003), 182–187.
15. Humbert, S., Bryson, E.A., Cordelières, F.P., Connors, N.C., Datta, S.R., Finkbeiner, S., Greenberg, M.E., Saudou, F., The IGF-1/Akt pathway is neuroprotective in Huntington's disease and involves Huntingtin phosphorylation by Akt. Dev. Cell 2 (2002), 831–837.
16. Jakubik, M., Floriddia, E.M., Nicotera, P., Bano, D., Heterozygous Igf1r deletion does not ameliorate pathological features associated with polyglutamine-containing huntingtin fragment. Neurosci. Lett. 580 (2014), 52–55, 10.1016/j.neulet.2014.07.049.
17. Jenkins, B.G., Koroshetz, W.J., Beal, M.F., Rosen, B.R., Evidence for impairment of energy metabolism in vivo in Huntington's disease using localized 1 H NMR spectroscopy. Neurology 43 (1993), 2689–2695.
18. Jenkins, B.G., Rosas, H.D., Chen, Y.C., Makabe, T., Myers, R., MacDonald, M., Rosen, B.R., Beal, M.F., Koroshetz, W.J., 1 H NMR spectroscopy studies of Huntington's disease: correlations with CAG repeat numbers. Neurology 50 (1998), 1357–1365.
19. Kapperler, L., De Magalhães, Filho C., Dupont, J., Leneuve, P., Cervera, P., Périn, L., Loudes, C., Blaise, A., Klein, R., Le Bouc Y, Epelbaum, Holzenberger, M., Brain IGF-1 receptors control mammalian growth and lifespan through a neuroendrocrine mechanism. PLoS Biol., 6, 2008, e254, 10.1371/journal.pbio.0060254.
20. Kenyon, C., Chang, J., Gensch, E., Rudner, A., Tabtiang, R., A C. elegans mutant that lives twice as long as wild type. Nature 366:6454 (1993), 461–464.
21. Koroshetz, W.J., Jenkins, B.G., Rosen, B.R., Beal, M.F., Energy metabolism defects in Huntington's disease and effects of coenzyme Q10. Ann. Neurol. 41 (1997), 160–165.
22. Lamprecht, W., Stein, P., Heinz, F., H:, Weissner, Creatine phosphate. Methods of Enzymatic Analysis (Bergmeyer Hu), 4, 1974, Academic Press, N. Y., 1777–1781.
23. Lee, W., Reyes, R.C., Gottipati, M.K., Lewis, K., Lesort, M., Parpura, V., Gray, M., Enhanced Ca(2 +)-dependent glutamate release from astrocytes of the BACHD Huntington's disease mouse model. Neurobiol. Dis. 58 (2013), 192–199, 10.1016/j.nbd.2013.06.002.
24. Lodi, R., Schapira, A.H., Manners, D., Styles, P., Wood, N.W., Taylor, D.J., Warner, T.T., Abnormal in vivo skeletal muscle energy metabolism in Huntington's disease and dentatorubropal-lidoluysian atrophy. Ann. Neurol. 48 (2000), 72–76.
25. Lopes, C., Ribeiro, M., Duarte, A.I., Humbert, S., Saudou, F., de Almeida L, Pereira, Hayden, M., AC, Rego, IGF-1 intranasal administration rescues Huntington's disease phenotypes in YAC128 mice. Mol. Neurobiol. 49 (2014), 1126–1142, 10.1007/s12035-013-8585-5.
26. Martin, W.R., Wieler, M., Hanstock, C.C., Is brain lactate increased in Huntington's disease?. J. Neurol. Sci. 263 (2007), 70–74.
27. Milakovic, T., Johnson, G.V., Mitochondrial respiration and ATP production are significantly impaired in striatal cells expressing mutant huntingtin. J. Biol. Chem. 280 (2005), 30773–30782.
28. Mochel, F., Durant, B., Meng, X., O'Callaghan, J., Yu, H., Brouillet, E., Wheeler, V.C., Humbert, S., Schiffmann, R., Durr, A., Early alterations of brain cellular energy homeostasis in Huntington's disease models. J. Biol. Chem. 287 (2012), 1361–1370, 10.1074/jbc.M111.309849.
29. Morley, J.F., Brignull, H.R., Weyers, J.J., Morimoto, R.I., The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 10417–10422.
30. Naia, L., Ribeiro, M.J., Rego, A.C., Mitochondrial and metabolic-based protective strategies in Huntington's disease: the case of creatine and coenzyme Q. Rev. Neurosci. 23 (2011), 13–28, 10.1515/RNS.2011.060.
31. Naia, L., Ferreira, I.L., Cunha-Oliveira, T., Duarte, A.I., Ribeiro, R., Rosenstock, T.R., Laço, M.N., Ribeiro, M.J., Oliveira, C.R., Saudou, F., Humbert, S., Rego, A.C., Activation of IGF-1 and insulin signaling pathways ameliorate mitochondrial function and energy metabolism in Huntington's disease human lymphoblasts. Mol. Neurobiol. 51 (2015), 331–348, 10.1007/s12035-014-8735-4.
32. Perluigi, M., Poon, H.F., Maragos, W., Pierce, W.M., Klein, J.B., Calabrese, V., Cini, C., De Marco, C., Butterfield, D.A., Proteomic analysis of protein expression and oxidative modification in R6/2 transgenic mice: a model of Huntington disease. Mol. Cell. Proteomics 4 (2005), 1849–1861.
33. Pouladi, M.A., Xie, Y., Skotte, N.H., Ehrnhoefer, D.E., Graham, R.K., Kim, J.E., Bissada, N., Yang, X.W., Paganetti, P., Friedlander, R.M., Leavitt, B.R., Hayden, M.R., Full-length huntingtin levels modulate body weight by influencing insulin-like growth factor 1 expression. Hum. Mol. Genet. 19 (2010), 1528–1538, 10.1093/hmg/ddq026.
34. Rampersad, S.N., Multiple applications of Alamar Blue as an indicator of metabolic function and cellular health in cell viability bioassays. Sensors (Basel) 12 (2012), 12347–12360, 10.3390/s120912347.
35. Rechler, M.M., Zapf, J., Nissley, S.P., Froesch, E.R., Moses, A.C., Podskalny, J.M., Schilling, E.E., Humbel, R.E., Interactions of insulin-like growth factors I and II and multiplication-stimulating activity with receptors and serum carrier proteins. Endocrinology 107 (1980), 1451–1459.
36. Ribeiro, M., Rosenstock, T.R., Oliveira, A.M., Oliveira, C.R., Rego, A.C., Insulin and IGF-1 improve mitochondrial function in a PI-3K/Akt-dependent manner and reduce mitochondrial generation of reactive oxygen species in Huntington's disease knock-in striatal cells. Free Radic. Biol. Med. 74 (2014), 129–144, 10.1016/j.freeradbiomed.2014.06.023.
37. Rosas, H.D., Hevelone, N.D., Zaleta, A.K., Greve, D.N., Salat, D.H., Fischl, B., Regional cortical thinning in preclinical Huntington disease and its relationship to cognition. Neurology 65 (2005), 745–747.
38. Ryu, H., Rosas, H.D., Hersch, S.M., Ferrante, R.J., The therapeutic role of creatine in Huntington's disease. Pharmacol. Ther. 108 (2005), 193–207.
39. Sadagursky, M., Cheng, Z., Rozzo, A., Palazzolo, I., Kelley, G.R., Dong, X., Krainc, D., White, M.F., IRS2 increases mitochondrial dysfunction and oxidative stress in a mouse model of Huntington disease. J. Clin. Invest. 121 (2011), 4070–4081, 10.1172/JCI46305.
40. Saleh, N., Moutereau, S., Azulay, J.P., Verny, C., Simonin, C., Tranchant, C., El Hawajri, N., Bachoud-Lévi, A.C., Maison, P., High insulin like growth factor I is associated with cognitive decline in Huntington disease. Neurology 75 (2010), 57–63, 10.1212/WNL.0b013e3181e62076.
41. Seong, I.S., Ivanova, E., Lee, J.M., Choo, Y.S., Fossale, E., Anderson, M., Gusella, J.F., Laramie, J.M., Myers, R.H., Lesort, M., MacDonald, M.E., HD CAG repeat implicates a dominant property of huntingtin in mitochondrial energy metabolism. Hum. Mol. Genet. 14 (2005), 2871–2880.
42. Silva, A.C., Almeida, S., Laço, M., Duarte, A.I., Domingues, J., Oliveira, C.R., Januário, C., Rego, A.C., Mitochondrial respiratory chain complex activity and bioenergetic alterations in human platelets derived from pre-symptomatic and symptomatic Huntington's disease carriers. Mitochondrion 13 (2013), 801–809, 10.1016/j.mito.2013.05.006.
43. Slow, E.J., van Raamsdonk, J., Rogers, D., Coleman, S.H., Graham, R.K., Deng, Y., Oh, R., Bissada, N., Hossain, S.M., Yang, Y.Z., Li, X.-J., Simpson, E.M., Gutekunst, C.-A., Leavitt, B.R., Hayden, M.R., Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum. Mol. Genet. 12 (2003), 1555–1567.
44. Stocchi, V., Cucchiarini, L., Magnani, M., Chiarantini, L., Palma, P., Crescentini, G., Simultaneous extraction and reverse-phase high-performance liquid chromatographic determination of adenine and pyridine nucleotides in human red blood cells. Anal. Biochem. 146 (1985), 118–124.
45. Tabrizi, S.J., Workman, J., Hart, P.E., Mangiarini, L., Mahal, A., Bates, G., Cooper, J.M., Schapira, A.H., Mitochondrial dysfunction and free radical damage in the Huntington R6/2 trans- genic mouse. Ann. Neurol. 47 (2000), 80–86.
46. Teixeira-Castro, A., Ailion, M., Jalles, A., Brignull, H.R., Vilaça, J.L., Dias, N., Rodrigues, P., Oliveira, J.F., Neves-Carvalho, A., Morimoto, R.I., Maciel, P., Neuron-specific proteotoxicity of mutant ataxin-3 in C. elegans: rescue by the DAF-16 and HSF-1 pathways. Hum. Mol. Genet. 20 (2011), 2996–3009, 10.1093/hmg/ddr203.
47. Trettel, F., Rigamonti, D., Hilditch-Maguire, P., Wheeler, V.C., Sharp, A.H., Persichetti, F., Cattaneo, E., MacDonald, M.E., Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum. Mol. Genet. 9 (2000), 2799–2809.
48. Tsang, T.M., Woodman, B., McLoughlin, G.A., Griffin, J.L., Tabrizi, S.J., Bates, G.P., Holmes, E., Metabolic characterization of the R6/2 transgenic mouse model of Huntington's disease by high-resolution MAS 1 H NMR spectroscopy. J. Proteome Res. 5 (2006), 483–492.
49. Vonsattel, J.P., DiFiglia, M., Huntington disease. J. Neuropathol. Exp. Neurol. 57 (1998), 369–384.
50. Wolf, A., Agnihotri, S., Micallef, J., Mukherjee, J., Sabha, N., Cairns, R., Hawkins, C., Guha, A., Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme. J. Exp. Med. 208 (2011), 313–326, 10.1084/jem.20101470.
51. Zemva, J., Schubert, M., The role of neuronal insulin/insulin-like growth factor-1 signaling for the pathogenesis of Alzheimer's disease: possible therapeutic implications. CNS Neurol. Disord. Drug Targets 13 (2014), 322–337.
52. Zhou, Q., Lam, P.Y., Han, D., Cadenas, E., c-Jun N-terminal kinase regulates mitochondrial bioenergetics by modulating pyruvate dehydrogenase activity in primary cortical neurons. J. Neurochem. 104 (2008), 325–335.