Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2016 (2016), Article ID 9839348, 13 pages
http://dx.doi.org/10.1155/2016/9839348
Research Article

Wnt5a Increases the Glycolytic Rate and the Activity of the Pentose Phosphate Pathway in Cortical Neurons

1CARE Biomedical Research Center, Faculty of Biological Sciences, Pontificia Universidad Católica de Chile, Alameda 340, P.O. Box 114-D, Santiago, Chile
2Facultad de Ciencias Naturales, Departamento de Química y Biología, Universidad de Atacama, Copayapu 485, Copiapó, Chile
3Centro de Estudios Científicos (CECs), Casilla 1469, Valdivia, Chile
4Centre for Healthy Brain Ageing, School of Psychiatry, Faculty of Medicine, University of New South Wales, Sydney, NSW, Australia
5Centro de Excelencia en Biomedicina de Magallanes (CEBIMA), Universidad de Magallanes, Punta Arenas, Chile

Received 21 April 2016; Accepted 10 July 2016

Academic Editor: Jordi Duran

Copyright © 2016 Pedro Cisternas et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Nusse and H. Varmus, “Three decades of Wnts: a personal perspective on how a scientific field developed,” EMBO Journal, vol. 31, no. 12, pp. 2670–2684, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. M. S. Arrázola, C. Silva-Alvarez, and N. C. Inestrosa, “How the Wnt signaling pathway protects from neurodegeneration: the mitochondrial scenario,” Frontiers in Cellular Neuroscience, vol. 9, article 166, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. J. F. Codocedo and N. C. Inestrosa, “Wnt-5a-regulated miR-101b controls COX2 expression in hippocampal neurons,” Biological Research, vol. 49, no. 1, article 9, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. J. F. Codocedo, C. Montecinos-Oliva, and N. C. Inestrosa, “Wnt-related synGAP1 is a neuroprotective factor of glutamatergic synapses against Aβ oligomers,” Frontiers in Cellular Neuroscience, vol. 9, article 227, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Parodi, C. Montecinos-Oliva, R. Varas et al., “Wnt5a inhibits K+ currents in hippocampal synapses through nitric oxide production,” Molecular and Cellular Neuroscience, vol. 68, pp. 314–322, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. V. T. Ramírez, E. Ramos-Fernández, and N. C. Inestrosa, “The Gαo activator mastoparan-7 promotes dendritic spine formation in hippocampal neurons,” Neural Plasticity, vol. 2016, Article ID 4258171, 11 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. J. A. Ríos, P. Cisternas, M. Arrese, S. Barja, and N. C. Inestrosa, “Is Alzheimer's disease related to metabolic syndrome? A Wnt signaling conundrum,” Progress in Neurobiology, vol. 121, pp. 125–146, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. J. N. Anastas and R. T. Moon, “WNT signalling pathways as therapeutic targets in cancer,” Nature Reviews Cancer, vol. 13, no. 1, pp. 11–26, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. C. B. Thompson, “Wnt meets Warburg: another piece in the puzzle?” The EMBO Journal, vol. 33, no. 13, pp. 1420–1422, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. K. T. Pate, C. Stringari, S. Sprowl-Tanio et al., “Wnt signaling directs a metabolic program of glycolysis and angiogenesis in colon cancer,” The EMBO Journal, vol. 33, no. 13, pp. 1454–1473, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. J. A. Godoy, J. A. Rios, J. M. Zolezzi, N. Braidy, and N. C. Inestrosa, “Signaling pathway cross talk in Alzheimer's disease,” Cell Communication and Signaling, vol. 12, article 23, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. D. G. Hardie, “AMPK: a key regulator of energy balance in the single cell and the whole organism,” International Journal of Obesity, vol. 32, supplement 4, pp. S7–S12, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Attwell and S. B. Laughlin, “An energy budget for signaling in the grey matter of the brain,” Journal of Cerebral Blood Flow and Metabolism, vol. 21, no. 10, pp. 1133–1145, 2001. View at Google Scholar · View at Scopus
  14. S. Jang, J. C. Nelson, E. G. Bend et al., “Glycolytic enzymes localize to synapses under energy stress to support synaptic function,” Neuron, vol. 90, no. 2, pp. 278–291, 2016. View at Publisher · View at Google Scholar
  15. Z. Chen and C. Zhong, “Decoding Alzheimer's disease from perturbed cerebral glucose metabolism: implications for diagnostic and therapeutic strategies,” Progress in Neurobiology, vol. 108, pp. 21–43, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. E. A. Winkler, Y. Nishida, A. P. Sagare et al., “GLUT1 reductions exacerbate Alzheimer's disease vasculo-neuronal dysfunction and degeneration,” Nature Neuroscience, vol. 18, no. 4, pp. 521–530, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. S. M. Euser, N. Sattar, J. C. M. Witteman et al., “A prospective analysis of elevated fasting glucose levels and cognitive function in older people: results from PROSPER and the Rotterdam Study,” Diabetes, vol. 59, no. 7, pp. 1601–1607, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Craft, “Insulin resistance syndrome and Alzheimer's disease: age- and obesity-related effects on memory, amyloid, and inflammation,” Neurobiology of Aging, vol. 26, supplement 1, pp. S65–S69, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. J. P. Schroeder and M. G. Packard, “Systemic or intra-amygdala injections of glucose facilitate memory consolidation for extinction of drug-induced conditioned reward,” European Journal of Neuroscience, vol. 17, no. 7, pp. 1482–1488, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Varela-Nallar, I. E. Alfaro, F. G. Serrano, J. Parodi, and N. C. Inestrosa, “Wingless-type family member 5A (Wnt-5a) stimulates synaptic differentiation and function of glutamatergic synapses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 49, pp. 21164–21169, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Varela-Nallar, J. Parodi, G. G. Farías, and N. C. Inestrosa, “Wnt-5a is a synaptogenic factor with neuroprotective properties against Aβ toxicity,” Neurodegenerative Diseases, vol. 10, no. 1–4, pp. 23–26, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Y. Vargas, J. Ahumada, M. S. Arrázola, M. Fuenzalida, and N. C. Inestrosa, “WASP-1, a canonical Wnt signaling potentiator, rescues hippocampal synaptic impairments induced by Aβ oligomers,” Experimental Neurology, vol. 264, pp. 14–25, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Willert, J. D. Brown, E. Danenberg et al., “Wnt proteins are lipid-modified and can act as stem cell growth factors,” Nature, vol. 423, no. 6938, pp. 448–452, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. W. Chen, D. Ten Berge, J. Brown et al., “Dishevelled 2 recruits β-arrestin 2 to mediate Wnt5A-stimulated endocytosis of frizzled 4,” Science, vol. 301, no. 5638, pp. 1391–1394, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. G. G. Farías, I. E. Alfaro, W. Cerpa et al., “Wnt-5a/JNK signaling promotes the clustering of PSD-95 in hippocampal neurons,” The Journal of Biological Chemistry, vol. 284, no. 23, pp. 15857–15866, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. G. V. De Ferrari, M. A. Chacón, M. I. Barría et al., “Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by β-amyloid fibrils,” Molecular Psychiatry, vol. 8, no. 2, pp. 195–208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Y. Jung and A. L. Rampal, “Cytochalasin B binding sites and glucose transport carrier in human erythrocyte ghosts,” The Journal of Biological Chemistry, vol. 252, no. 15, pp. 5456–5463, 1977. View at Google Scholar · View at Scopus
  28. J. M. Bertoni, “Competitive inhibition of rat brain hexokinase by 2-deoxyglucose, glucosamine, and metrizamide,” Journal of Neurochemistry, vol. 37, no. 6, pp. 1523–1528, 1981. View at Publisher · View at Google Scholar · View at Scopus
  29. W. Y. Sanchez, S. L. McGee, T. Connor et al., “Dichloroacetate inhibits aerobic glycolysis in multiple myeloma cells and increases sensitivity to bortezomib,” British Journal of Cancer, vol. 108, no. 8, pp. 1624–1633, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. P. Cisternas, C. Silva-Alvarez, F. Martínez et al., “The oxidized form of vitamin C, dehydroascorbic acid, regulates neuronal energy metabolism,” Journal of Neurochemistry, vol. 129, no. 4, pp. 663–671, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. L. F. Barros, C. X. Bittner, A. Loaiza et al., “Kinetic validation of 6-NBDG as a probe for the glucose transporter GLUT1 in astrocytes,” Journal of Neurochemistry, vol. 109, no. 1, pp. 94–100, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. C. S. Tsai and Q. Chen, “Purification and kinetic characterization of hexokinase and glucose-6- phosphate dehydrogenase from Schizosaccharomyces pombe,” Biochemistry and Cell Biology, vol. 76, no. 1, pp. 107–113, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Herrero-Mendez, A. Almeida, E. Fernández, C. Maestre, S. Moncada, and J. P. Bolaños, “The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1,” Nature Cell Biology, vol. 11, no. 6, pp. 747–752, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. J. S. Hothersall, N. Z. Baquer, A. L. Greenbaum, and P. McLean, “Alternative pathways of glucose utilization in brain. Changes in the pattern of glucose utilization in brain during development and the effect of phenazine methosulfate on the integration of metabolic routes,” Archives of Biochemistry and Biophysics, vol. 198, no. 2, pp. 478–492, 1979. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Konagaya, Y. Konagaya, H. Horikawa, and M. Iida, “Pentose phosphate pathway in neuromuscular diseases—evaluation of muscular glucose 6-phosphate dehydrogenase activity and RNA content,” Rinsho Shinkeigaku, vol. 30, no. 10, pp. 1078–1083, 1990. View at Google Scholar · View at Scopus
  36. M. G. Larrabee, “Evaluation of the pentose phosphate pathway from 14CO2 data. Fallibility of a classic equation when applied to non-homogeneous tissues,” Biochemical Journal, vol. 272, no. 1, pp. 127–132, 1990. View at Publisher · View at Google Scholar · View at Scopus
  37. M. J. Calkins, M. Manczak, P. Mao, U. Shirendeb, and P. H. Reddy, “Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer's disease,” Human Molecular Genetics, vol. 20, no. 23, pp. 4515–4529, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. W. Cerpa, J. A. Godoy, I. Alfaro et al., “Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons,” The Journal of Biological Chemistry, vol. 283, no. 9, pp. 5918–5927, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Bonansco, A. Couve, G. Perea, C. Á. Ferradas, M. Roncagliolo, and M. Fuenzalida, “Glutamate released spontaneously from astrocytes sets the threshold for synaptic plasticity,” European Journal of Neuroscience, vol. 33, no. 8, pp. 1483–1492, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. E. P. Murono, T. Lin, and J. Osterman, “[14C]-2-deoxyglucose uptake studies in Leydig cells,” Andrologia, vol. 18, no. 6, pp. 587–594, 1986. View at Google Scholar · View at Scopus
  41. F. J. Muñoz, J. A. Godoy, W. Cerpa, I. M. Poblete, J. P. Huidobro-Toro, and N. C. Inestrosa, “Wnt-5a increases NO and modulates NMDA receptor in rat hippocampal neurons,” Biochemical and Biophysical Research Communications, vol. 444, no. 2, pp. 189–194, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. R. C. Babbedge, P. A. Bland-Ward, S. L. Hart, and P. K. Moore, “Inhibition of rat cerebellar nitric oxide synthase by 7-nitro indazole and related substituted indazoles,” British Journal of Pharmacology, vol. 110, no. 1, pp. 225–228, 1993. View at Publisher · View at Google Scholar · View at Scopus
  43. J. E. Wilson, “Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function,” Journal of Experimental Biology, vol. 206, no. 12, pp. 2049–2057, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. M. D. Gordon and R. Nusse, “Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors,” The Journal of Biological Chemistry, vol. 281, no. 32, pp. 22429–22433, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. N. C. Inestrosa and E. Arenas, “Emerging roles of Wnts in the adult nervous system,” Nature Reviews Neuroscience, vol. 11, no. 2, pp. 77–86, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. N. C. Inestrosa and L. Varela-Nallar, “Wnt signaling in the nervous system and in Alzheimer's disease,” Journal of Molecular Cell Biology, vol. 6, no. 1, pp. 64–74, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. R. van Amerongen, “Alternative Wnt pathways and receptors,” Cold Spring Harbor Perspectives in Biology, vol. 4, no. 10, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. I. Llorente-Folch, C. B. Rueda, B. Pardo, G. Szabadkai, M. R. Duchen, and J. Satrustegui, “The regulation of neuronal mitochondrial metabolism by calcium,” The Journal of Physiology, vol. 593, no. 16, pp. 3447–3462, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. A. I. Ivanov, A. E. Malkov, T. Waseem et al., “Glycolysis and oxidative phosphorylation in neurons and astrocytes during network activity in hippocampal slices,” Journal of Cerebral Blood Flow and Metabolism, vol. 34, no. 3, pp. 397–407, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. J. P. Bolaños and A. Almeida, “Modulation of astroglial energy metabolism by nitric oxide,” Antioxidants and Redox Signaling, vol. 8, no. 5-6, pp. 955–965, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Almeida, P. Cidad, M. Delgado-Esteban, E. Fernández, P. García-Nogales, and J. P. Bolaños, “Inhibition of mitochondrial respiration by nitric oxide: its role in glucose metabolism and neuroprotection,” Journal of Neuroscience Research, vol. 79, no. 1-2, pp. 166–171, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Schinner, “Wnt-signalling and the metabolic syndrome,” Hormone and Metabolic Research, vol. 41, no. 2, pp. 159–163, 2009. View at Publisher · View at Google Scholar
  53. V. Lyssenko, “The transcription factor 7-like 2 gene and increased risk of type 2 diabetes: an update,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 11, no. 4, pp. 385–392, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. D. Zeve, J. Seo, J. M. Suh et al., “Wnt signaling activation in adipose progenitors promotes insulin-independent muscle glucose uptake,” Cell Metabolism, vol. 15, no. 4, pp. 492–504, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. Y.-C. Lu, C.-P. Wang, C.-C. Hsu et al., “Circulating secreted frizzled-related protein 5 (Sfrp5) and wingless-type MMTV integration site family member 5a (Wnt5a) levels in patients with type 2 diabetes mellitus,” Diabetes/Metabolism Research and Reviews, vol. 29, no. 7, pp. 551–556, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Silva-Alvarez, M. S. Arrázola, J. A. Godoy, D. Ordenes, and N. C. Inestrosa, “Canonical Wnt signaling protects hippocampal neurons from Aβ oligomers: role of non-canonical Wnt-5a/Ca2+ in mitochondrial dynamics,” Frontiers in Cellular Neuroscience, vol. 7, article 97, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Kristián, “Metabolic stages, mitochondria and calcium in hypoxic/ischemic brain damage,” Cell Calcium, vol. 36, no. 3-4, pp. 221–233, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. L. Sokoloff, “Local cerebral energy metabolism: its relationships to local functional activity and blood flow,” Ciba Foundation Symposium, no. 56, pp. 171–197, 1978. View at Google Scholar
  59. P. J. Magistretti and I. Allaman, “A cellular perspective on brain energy metabolism and functional imaging,” Neuron, vol. 86, no. 4, pp. 883–901, 2015. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Mueckler, “Facilitative glucose transporters,” European Journal of Biochemistry, vol. 219, no. 3, pp. 713–725, 1994. View at Publisher · View at Google Scholar · View at Scopus
  61. J. P. Bolaños and A. Almeida, “The pentose-phosphate pathway in neuronal survival against nitrosative stress,” IUBMB Life, vol. 62, no. 1, pp. 14–18, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. J. P. Bolaños, M. Delgado-Esteban, A. Herrero-Mendez, S. Fernandez-Fernandez, and A. Almeida, “Regulation of glycolysis and pentose-phosphate pathway by nitric oxide: impact on neuronal survival,” Biochimica et Biophysica Acta—Bioenergetics, vol. 1777, no. 7-8, pp. 789–793, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. A. M. Brown, “Brain glycogen re-awakened,” Journal of Neurochemistry, vol. 89, no. 3, pp. 537–552, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. J. Valles-Ortega, J. Duran, M. Garcia-Rocha et al., “Neurodegeneration and functional impairments associated with glycogen synthase accumulation in a mouse model of Lafora disease,” EMBO Molecular Medicine, vol. 3, no. 11, pp. 667–681, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. D. Vilchez, S. Ros, D. Cifuentes et al., “Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy,” Nature Neuroscience, vol. 10, no. 11, pp. 1407–1413, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. I. Saez, J. Duran, C. Sinadinos et al., “Neurons have an active glycogen metabolism that contributes to tolerance to hypoxia,” Journal of Cerebral Blood Flow and Metabolism, vol. 34, no. 6, pp. 945–955, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Duran and J. J. Guinovart, “Brain glycogen in health and disease,” Molecular Aspects of Medicine, vol. 46, pp. 70–77, 2015. View at Publisher · View at Google Scholar · View at Scopus
  68. C. Sinadinos, J. Valles-Ortega, L. Boulan et al., “Neuronal glycogen synthesis contributes to physiological aging,” Aging Cell, vol. 13, no. 5, pp. 935–945, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. J. C. López-Ramos, J. Duran, A. Gruart, J. J. Guinovart, and J. M. Delgado-García, “Role of brain glycogen in the response to hypoxia and in susceptibility to epilepsy,” Frontiers in Cellular Neuroscience, vol. 9, article 431, 2015. View at Publisher · View at Google Scholar · View at Scopus
  70. G. Wu, Y.-Z. Fang, S. Yang, J. R. Lupton, and N. D. Turner, “Glutathione metabolism and its implications for health,” Journal of Nutrition, vol. 134, no. 3, pp. 489–492, 2004. View at Google Scholar · View at Scopus
  71. U. Müller and G. Bicker, “Calcium-activated release of nitric oxide and cellular distribution of nitric oxide-synthesizing neurons in the nervous system of the locust,” The Journal of Neuroscience, vol. 14, no. 12, pp. 7521–7528, 1994. View at Google Scholar · View at Scopus
  72. J. P. Bolaños, A. Herrero-Mendez, S. Fernandez-Fernandez, and A. Almeida, “Linking glycolysis with oxidative stress in neural cells: a regulatory role for nitric oxide,” Biochemical Society Transactions, vol. 35, part 5, pp. 1224–1227, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. J. P. Bolaños, M. Delgado-Esteban, A. Herrero-Mendez, S. Fernandez-Fernandez, and A. Almeida, “Regulation of glycolysis and pentose-phosphate pathway by nitric oxide: impact on neuronal survival,” Biochimica et Biophysica Acta, vol. 1777, no. 7-8, pp. 789–793, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. A.-K. Bouzier-Sore and L. Pellerin, “Unraveling the complex metabolic nature of astrocytes,” Frontiers in Cellular Neuroscience, vol. 7, article 179, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. G. A. Dienel, “The metabolic trinity, glucose-glycogen-lactate, links astrocytes and neurons in brain energetics, signaling, memory, and gene expression,” Neuroscience Letters, 2015. View at Publisher · View at Google Scholar · View at Scopus
  76. L. F. Barros, “Metabolic signaling by lactate in the brain,” Trends in Neurosciences, vol. 36, no. 7, pp. 396–404, 2013. View at Publisher · View at Google Scholar · View at Scopus