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Stem Cells International
Volume 2012, Article ID 820790, 10 pages
http://dx.doi.org/10.1155/2012/820790
Review Article

Neural Stem Cells in the Diabetic Brain

Medicina Celular y Molecular, Facultad de Ciencias Biomédicas, Universidad Austral, Buenos Aires, B1629AHJ Pilar, Argentina

Received 4 August 2012; Accepted 15 October 2012

Academic Editor: Branden R. Nelson

Copyright © 2012 Tomás P. Bachor and Angela M. Suburo. 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. J. Altman and G. D. Das, “Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats,” Journal of Comparative Neurology, vol. 124, no. 3, pp. 319–335, 1965. View at Google Scholar · View at Scopus
  2. S. A. Bayer, J. W. Yackel, and P. S. Puri, “Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life,” Science, vol. 216, no. 4548, pp. 890–892, 1982. View at Google Scholar · View at Scopus
  3. L. Bonfanti and P. Peretto, “Adult neurogenesis in mammals–a theme with many variations,” European Journal of Neuroscience, vol. 34, no. 6, pp. 930–950, 2011. View at Google Scholar
  4. F. H. Gage, G. Kempermann, T. D. Palmer, D. A. Peterson, and J. Ray, “Multipotent progenitor cells in the adult dentate gyrus,” Journal of Neurobiology, vol. 36, no. 2, pp. 249–266, 1998. View at Google Scholar
  5. P. S. Eriksson, E. Perfilieva, T. Björk-Eriksson et al., “Neurogenesis in the adult human hippocampus,” Nature Medicine, vol. 4, no. 11, pp. 1313–1317, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. M. A. Curtis, R. L. M. Faull, and P. S. Eriksson, “The effect of neurodegenerative diseases on the subventricular zone,” Nature Reviews Neuroscience, vol. 8, no. 9, pp. 712–723, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Kam, M. A. Curtis, S. R. McGlashan, B. Connor, U. Nannmark, and R. L. M. Faull, “The cellular composition and morphological organization of the rostral migratory stream in the adult human brain,” Journal of Chemical Neuroanatomy, vol. 37, no. 3, pp. 196–205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. P. J. Bernier, J. Vinet, M. Cossette, and A. Parent, “Characterization of the subventricular zone of the adult human brain: evidence for the involvement of Bcl-2,” Neuroscience Research, vol. 37, no. 1, pp. 67–78, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Quiñones-Hinojosa, N. Sanai, O. Gonzalez-Perez, and J. M. Garcia-Verdugo, “The human brain subventricular zone: stem cells in this niche and its organization,” Neurosurgery Clinics of North America, vol. 18, no. 1, pp. 15–20, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Wang, F. Liu, Y. Y. Liu et al., “Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain,” Cell Research, vol. 21, no. 11, pp. 1534–1550, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. M. A. Curtis, V. F. Low, and R. L. Faull, “Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation,” Developmental Neurobiology, vol. 72, no. 7, pp. 990–1005, 2012. View at Google Scholar
  12. D. Ehninger and G. Kempermann, “Neurogenesis in the adult hippocampus,” Cell and Tissue Research, vol. 331, no. 1, pp. 243–250, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. B. Steiner, G. Kronenberg, S. Jessberger, M. D. Brandt, K. Reuter, and G. Kempermann, “Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice,” GLIA, vol. 46, no. 1, pp. 41–52, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Bonaguidi, M. A. Wheeler, J. S. Shapiro et al., “In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics,” Cell, vol. 145, no. 7, pp. 1142–1155, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Kempermann, S. Jessberger, B. Steiner, and G. Kronenberg, “Milestones of neuronal development in the adult hippocampus,” Trends in Neurosciences, vol. 27, no. 8, pp. 447–452, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Namba, H. Mochizuki, R. Suzuki et al., “Time-lapse imaging reveals symmetric neurogenic cell division of GFAP-expressing progenitors for expansion of postnatal dentate granule neurons,” PLoS ONE, vol. 6, no. 9, Article ID e25303, 2011. View at Google Scholar
  17. W. J. Zhang, Y. F. Tan, J. T. Y. Yue, M. Vranic, and J. M. Wojtowicz, “Impairment of hippocampal neurogenesis in streptozotocin-treated diabetic rats,” Acta Neurologica Scandinavica, vol. 117, no. 3, pp. 205–210, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. I. K. Hwang, S. S. Yi, W. Song, M. H. Won, Y. S. Yoon, and J. K. Seong, “Effects of age and treadmill exercise in chronic diabetic stages on neuroblast differentiation in a rat model of type 2 diabetes,” Brain Research, vol. 1341, pp. 63–71, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. O. von Bohlen Und Halbach, “Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus,” Cell and Tissue Research, vol. 345, no. 1, pp. 1–19, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Jessberger, B. Römer, H. Babu, and G. Kempermann, “Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells,” Experimental Neurology, vol. 196, no. 2, pp. 342–351, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Toni, E. M. Teng, E. A. Bushong et al., “Synapse formation on neurons born in the adult hippocampus,” Nature Neuroscience, vol. 10, no. 6, pp. 727–734, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Stangl and S. Thuret, “Impact of diet on adult hippocampal neurogenesis,” Genes and Nutrition, vol. 4, no. 4, pp. 271–282, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Koehl and D. N. Abrous, “A new chapter in the field of memory: adult hippocampal neurogenesis,” European Journal of Neuroscience, vol. 33, no. 6, pp. 1101–1114, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Garthe, J. Behr, and G. Kempermann, “Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies,” PLoS ONE, vol. 4, no. 5, Article ID e5464, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Doetsch, I. Caille, D. A. Lim, J. M. Garcia-Verdugo, and A. Alvarez-Buylla, “Subventricular zone astrocytes are neural stem cells in the adult mammalian brain,” Cell, vol. 97, no. 6, pp. 703–716, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Seri, J. M. García-Verdugo, B. S. McEwen, and A. Alvarez-Buylla, “Astrocytes give rise to new neurons in the adult mammalian hippocampus,” The Journal of Neuroscience, vol. 21, no. 18, pp. 7153–7160, 2001. View at Google Scholar · View at Scopus
  27. M. Alonso, I. Ortega-Pérez, M. S. Grubb, J. P. Bourgeois, P. Charneau, and P. M. Lledo, “Turning astrocytes from the rostral migratory stream into neurons: a role for the olfactory sensory organ,” The Journal of Neuroscience, vol. 28, no. 43, pp. 11089–11102, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Kriegstein and A. Alvarez-Buylla, “The glial nature of embryonic and adult neural stem cells,” Annual Review of Neuroscience, vol. 32, pp. 149–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. L. C. Fuentealba, K. Obernier, and A. Alvarez-Buylla, “Adult neural stem cells bridge their niche,” Cell Stem Cell, vol. 10, no. 6, pp. 698–708, 2012. View at Google Scholar
  30. Z. Mirzadeh, F. T. Merkle, M. Soriano-Navarro, J. M. Garcia-Verdugo, and A. Alvarez-Buylla, “Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain,” Cell Stem Cell, vol. 3, no. 3, pp. 265–278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. Q. Shen, Y. Wang, E. Kokovay et al., “Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions,” Cell Stem Cell, vol. 3, no. 3, pp. 289–300, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. X. Duan, E. Kang, C. Y. Liu, G. L. Ming, and H. Song, “Development of neural stem cell in the adult brain,” Current Opinion in Neurobiology, vol. 18, no. 1, pp. 108–115, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. A. K. Chojnacki, G. K. Mak, and S. Weiss, “Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both?” Nature Reviews Neuroscience, vol. 10, no. 2, pp. 153–163, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Coskun, H. Wu, B. Blanchi et al., “CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 3, pp. 1026–1031, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. M. Castañeda, M. A. Cubilla, M. M. López-Vicchi, and A. M. Suburo, “Endothelinergic cells in the subependymal region of mice,” Brain Research, vol. 1321, pp. 20–30, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Ahmed, “The culture of neural stem cells,” Journal of Cellular Biochemistry, vol. 106, no. 1, pp. 1–6, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Y. Maslov, T. A. Barone, R. J. Plunkett, and S. C. Pruitt, “Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice,” The Journal of Neuroscience, vol. 24, no. 7, pp. 1726–1733, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. R. L. Zhang, Z. G. Zhang, M. Lu, Y. Wang, J. J. Yang, and M. Chopp, “Reduction of the cell cycle length by decreasing G1 phase and cell cycle reentry expand neuronal progenitor cells in the subventricular zone of adult rat after stroke,” Journal of Cerebral Blood Flow and Metabolism, vol. 26, no. 6, pp. 857–863, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. D. N. Abrous, M. Koehl, and M. Le Moal, “Adult neurogenesis: from precursors to network and physiology,” Physiological Reviews, vol. 85, no. 2, pp. 523–569, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Colak, T. Mori, M. S. Brill et al., “Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells,” The Journal of Neuroscience, vol. 28, no. 2, pp. 434–446, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. M. M. Castañeda, M. A. Cubilla, T. Bachor, and A. M. Suburo, “Endothelinergic signaling during recovery of brain cortical lesions,” Journal of Neurological Research, vol. 33, no. 2, pp. 137–144, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. S. P. J. Fancy, C. Zhao, and R. J. M. Franklin, “Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS,” Molecular and Cellular Neuroscience, vol. 27, no. 3, pp. 247–254, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Menn, J. M. Garcia-Verdugo, C. Yaschine, O. Gonzalez-Perez, D. Rowitch, and A. Alvarez-Buylla, “Origin of oligodendrocytes in the subventricular zone of the adult brain,” The Journal of Neuroscience, vol. 26, no. 30, pp. 7907–7918, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Jablonska, A. Aguirre, M. Raymond et al., “Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination,” Nature Neuroscience, vol. 13, no. 5, pp. 541–550, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. O. Gonzalez-Perez and A. Alvarez-Buylla, “Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor,” Brain Research Reviews, vol. 67, no. 1-2, pp. 147–156, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. C. A. G. Marshall, S. O. Suzuki, and J. E. Goldman, “Gliogenic and neurogenic progenitors of the subventricular zone: who are they, where did they come from, and where are they going?” GLIA, vol. 43, no. 1, pp. 52–61, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. E. Raponi, F. Agenes, C. Delphin et al., “S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage,” GLIA, vol. 55, no. 2, pp. 165–177, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. M. F. Mehler and S. Gokhan, “Postnatal cerebral cortical multipotent progenitors: regulatory mechanisms and potential role in the development of novel neural regenerative strategies,” Brain Pathology, vol. 9, no. 3, pp. 515–526, 1999. View at Google Scholar · View at Scopus
  49. W. P. Ge, A. Miyawaki, F. H. Gage, Y. N. Jan, and L. Y. Jan, “Local generation of glia is a major astrocyte source in postnatal cortex,” Nature, vol. 484, no. 7394, pp. 376–380, 2012. View at Google Scholar
  50. I. Malandrucco, P. Pasqualetti, I. Giordani et al., “Very-low-calorie diet: a quick therapeutic tool to improve beta cell function in morbidly obese patients with type 2 diabetes,” The American Journal of Clinical Nutrition, vol. 95, no. 3, pp. 609–613, 2012. View at Google Scholar
  51. W. M. Teeuwisse, R. L. Widya, M. Paulides et al., “Short-term caloric restriction normalizes hypothalamic neuronal responsiveness to glucose ingestion in patients with type 2 diabetes,” Diabetes. In press.
  52. S. Kumar, J. Parkash, H. Kataria, and G. Kaur, “Interactive effect of excitotoxic injury and dietary restriction on neurogenesis and neurotrophic factors in adult male rat brain,” Neuroscience Research, vol. 65, no. 4, pp. 367–374, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. P. Rivera, Y. Romero-Zerbo, F. J. Pavon et al., “Obesity-dependent cannabinoid modulation of proliferation in adult neurogenic regions,” European Journal of Neuroscience, vol. 33, no. 9, pp. 1577–1586, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. S. G. Kernie and J. M. Parent, “Forebrain neurogenesis after focal Ischemic and traumatic brain injury,” Neurobiology of Disease, vol. 37, no. 2, pp. 267–274, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. J. E. Gotts and M. F. Chesselet, “Migration and fate of newly born cells after focal cortical ischemia in adult rats,” Journal of Neuroscience Research, vol. 80, no. 2, pp. 160–171, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. L. Z. Rui, Y. LeTourneau, S. R. Gregg et al., “Neuroblast division during migration toward the ischemic striatum: a study of dynamic migratory and proliferative characteristics of neuroblasts from the subventricular zone,” The Journal of Neuroscience, vol. 27, no. 12, pp. 3157–3162, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. M. V. Kokoeva, H. Yin, and J. S. Flier, “Evidence for constitutive neural cell proliferation in the adult murine hypothalamus,” Journal of Comparative Neurology, vol. 505, no. 2, pp. 209–220, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. K. Matsuzaki, M. Katakura, T. Hara, G. Li, M. Hashimoto, and O. Shido, “Proliferation of neuronal progenitor cells and neuronal differentiation in the hypothalamus are enhanced in heat-acclimated rats,” Pflugers Archiv European Journal of Physiology, vol. 458, no. 4, pp. 661–673, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Perez-Martin, M. Cifuentes, J. M. Grondona et al., “IGF-I stimulates neurogenesis in the hypothalamus of adult rats,” European Journal of Neuroscience, vol. 31, no. 9, pp. 1533–1548, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. D. A. Lee, J. L. Bedont, T. Pak et al., “Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche,” Nature Neuroscience, vol. 15, no. 5, pp. 700–702, 2012. View at Google Scholar
  61. A. A. Pierce and A. W. Xu, “De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance,” The Journal of Neuroscience, vol. 30, no. 2, pp. 723–730, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. M. V. Kokoeva, H. Yin, and J. S. Flier, “Neurogenesis in the hypothalamus of adult mice: potential role in energy balance,” Science, vol. 310, no. 5748, pp. 679–683, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. D. E. McNay, N. Briancon, M. V. Kokoeva, E. Maratos-Flier, and J. S. Flier, “Remodeling of the arcuate nucleus energy-balance circuit is inhibited in obese mice,” The Journal of Clinical Investigation, vol. 122, no. 1, pp. 142–152, 2012. View at Google Scholar
  64. International Diabetes Federation (IDF), “Diabetes Prevalence,” 2007.
  65. C. C. Cowie, K. F. Rust, E. S. Ford et al., “Full accounting of diabetes and pre-diabetes in the U.S. population in 1988–1994 and 2005-2006,” Diabetes Care, vol. 32, no. 2, pp. 287–294, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. WHO, Obesity and Overweight, Fact Sheet 311, 2011.
  67. R. Chilton, J. Wyatt, S. Nandish, R. Oliveros, and M. Lujan, “Cardiovascular comorbidities of type 2 diabetes mellitus: defining the potential of glucagonlike peptide1-based therapies,” American Journal of Medicine, vol. 124, no. 1, supplement, pp. S35–S53, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. M. W. J. Strachan, R. M. Reynolds, R. E. Marioni, and J. F. Price, “Cognitive function, dementia and type 2 diabetes mellitus in the elderly,” Nature Reviews Endocrinology, vol. 7, no. 2, pp. 108–114, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. G. Cheng, C. Huang, H. Deng, and H. Wang, “Diabetes as a risk factor for dementia and mild cognitive impairment: a meta-analysis of longitudinal studies,” Internal Medicine Journal, vol. 42, no. 5, pp. 484–491, 2012. View at Google Scholar
  70. R. J. McCrimmon, C. M. Ryan, and B. M. Frier, “Diabetes and cognitive dysfunction,” The Lancet, vol. 379, no. 9833, pp. 2291–2299, 2012. View at Google Scholar
  71. Y. Ozawa, T. Kurihara, M. Sasaki et al., “Neural degeneration in the retina of the streptozotocin-induced type 1 diabetes model,” Experimental Diabetes Research, vol. 2011, Article ID 108328, 7 pages, 2011. View at Publisher · View at Google Scholar
  72. B. Winner, Z. Kohl, and F. H. Gage, “Neurodegenerative disease and adult neurogenesis,” European Journal of Neuroscience, vol. 33, no. 6, pp. 1139–1151, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Mu and F. H. Gage, “Adult hippocampal neurogenesis and its role in Alzheimer's disease,” Molecular Neurodegeneration, vol. 6, article 85, 2011. View at Google Scholar
  74. A. Nouwen, G. Nefs, I. Caramlau et al., “Prevalence of depression in individuals with impaired glucose metabolism or undiagnosed diabetes: a systematic review and meta-analysis of the European Depression in Diabetes (EDID) research consortium,” Diabetes Care, vol. 34, no. 3, pp. 752–762, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Fotuhi, D. Do, and C. Jack, “Modifiable factors that alter the size of the hippocampus with ageing,” Nature Reviews Neurology, vol. 8, no. 4, pp. 189–202, 2012. View at Google Scholar
  76. A. Junod, A. E. Lambert, W. Stauffacher, and A. E. Renold, “Diabetogenic action of streptozotocin: relationship of dose to metabolic response,” The Journal of Clinical Investigation, vol. 48, no. 11, pp. 2129–2139, 1969. View at Google Scholar · View at Scopus
  77. R. S. Surwit, M. N. Feinglos, J. Rodin et al., “Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J mice,” Metabolism, vol. 44, no. 5, pp. 645–651, 1995. View at Google Scholar · View at Scopus
  78. M. J. Soler, M. Riera, and D. Batlle, “New experimental models of diabetic nephropathy in mice models of type 2 diabetes: efforts to replicate human nephropathy,” Experimental Diabetes Research, vol. 2012, Article ID 616313, 9 pages, 2012. View at Publisher · View at Google Scholar
  79. M. S. Islam and T. Loots du, “Experimental rodent models of type 2 diabetes: a review,” Methods and Findings in Experimental and Clinical Pharmacology, vol. 31, no. 4, pp. 249–261, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. T. Nakamura, T. Terajima, T. Ogata et al., “Establishment and pathophysiological characterization of type 2 diabetic mouse model produced by streptozotocin and nicotinamide,” Biological and Pharmaceutical Bulletin, vol. 29, no. 6, pp. 1167–1174, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. NIDDK, Diabetic Complications Consortium, National Institute of Diabetes, Digestive and Kidney Diseases (NIDDK), 2012.
  82. F. Saravia, Y. Revsin, V. Lux-Lantos, J. Beauquis, F. Homo-Delarche, and A. F. De Nicola, “Oestradiol restores cell proliferation in dentate gyrus and subventricular zone of streptozotocin-diabetic mice,” Journal of Neuroendocrinology, vol. 16, no. 8, pp. 704–710, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. J. Jackson-Guilford, J. D. Leander, and L. K. Nisenbaum, “The effect of streptozotocin-induced diabetes on cell proliferation in the rat dentate gyrus,” Neuroscience Letters, vol. 293, no. 2, pp. 91–94, 2000. View at Publisher · View at Google Scholar · View at Scopus
  84. J. Beauquis, P. Roig, F. Homo-Delarche, A. De Nicola, and F. Saravia, “Reduced hippocampal neurogenesis and number of hilar neurones in streptozotocin-induced diabetic mice: reversion by antidepressant treatment,” European Journal of Neuroscience, vol. 23, no. 6, pp. 1539–1546, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. F. E. Saravia, Y. Revsin, M. C. Gonzalez Deniselle et al., “Increased astrocyte reactivity in the hippocampus of murine models of type 1 diabetes: the nonobese diabetic (NOD) and streptozotocin-treated mice,” Brain Research, vol. 957, no. 2, pp. 345–353, 2002. View at Publisher · View at Google Scholar · View at Scopus
  86. J. Beauquis, F. Saravia, J. Coulaud et al., “Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse,” Experimental Neurology, vol. 210, no. 2, pp. 359–367, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. S. S. Yi, I. K. Hwang, K. Y. Yoo et al., “Effects of treadmill exercise on cell proliferation and differentiation in the subgranular zone of the dentate gyrus in a rat model of type ii diabetes,” Neurochemical Research, vol. 34, no. 6, pp. 1039–1046, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. J. Beauquis, F. Homo-Delarche, M. H. Giroix et al., “Hippocampal neurovascular and hypothalamic-pituitary-adrenal axis alterations in spontaneously type 2 diabetic GK rats,” Experimental Neurology, vol. 222, no. 1, pp. 125–134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. B. T. Lang, Y. Yan, R. J. Dempsey, and R. Vemuganti, “Impaired neurogenesis in adult type-2 diabetic rats,” Brain Research, vol. 1258, pp. 25–33, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Granado, C. García-Cáceres, M. Tuda, L. M. Frago, J. A. Chowen, and J. Argente, “Insulin and growth hormone-releasing peptide-6 (GHRP-6) have differential beneficial effects on cell turnover in the pituitary, hypothalamus and cerebellum of streptozotocin (STZ)-induced diabetic rats,” Molecular and Cellular Endocrinology, vol. 337, no. 1-2, pp. 101–113, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. C. García-Cáceres, A. Lechuga-Sancho, J. Argente, L. M. Frago, and J. A. Chowen, “Death of hypothalamic astrocytes in poorly controlled diabetic rats is associated with nuclear translocation of apoptosis inducing factor,” Journal of Neuroendocrinology, vol. 20, no. 12, pp. 1348–1360, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. Z. H. Afsari, W. M. Renno, and E. Adb-El-Basset, “Alteration of glial fibrillary acidic proteins immunoreactivity in astrocytes of the spinal cord diabetic rats,” Anatomical Record, vol. 291, no. 4, pp. 390–399, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. E. S. Coleman, J. C. Dennis, T. D. Braden, R. L. Judd, and P. Posner, “Insulin treatment prevents diabetes-induced alterations in astrocyte glutamate uptake and GFAP content in rats at 4 and 8weeks of diabetes duration,” Brain Research, vol. 1306, pp. 131–141, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. E. Cacci, M. A. Ajmone-Cat, T. Anelli, S. Biagioni, and L. Minghetti, “In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia,” GLIA, vol. 56, no. 4, pp. 412–425, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. I. Russo, S. Barlati, and F. Bosetti, “Effects of neuroinflammation on the regenerative capacity of brain stem cells,” Journal of Neurochemistry, vol. 116, no. 6, pp. 947–956, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. A. M. Stranahan, T. V. Arumugam, R. G. Cutler, K. Lee, J. M. Egan, and M. P. Mattson, “Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons,” Nature Neuroscience, vol. 11, no. 3, pp. 309–317, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Mansouri, H. Ortsater, O. Pintor Gallego, V. Darsalia, A. Sjoholm, and C. Patrone, “Pituitary adenylate cyclase-activating polypeptide counteracts the impaired adult neural stem cell viability induced by palmitate,” Journal of Neuroscience Research, vol. 90, no. 4, pp. 759–768, 2012. View at Google Scholar
  98. M. W. J. Strachan, R. M. Reynolds, B. M. Frier, R. J. Mitchell, and J. F. Price, “The role of metabolic derangements and glucocorticoid excess in the aetiology of cognitive impairment in type 2 diabetes. Implications for future therapeutic strategies,” Diabetes, Obesity and Metabolism, vol. 11, no. 5, pp. 407–414, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. T. J. Schoenfeld and E. Gould, “Stress, stress hormones, and adult neurogenesis,” Experimental Neurology, vol. 233, no. 1, pp. 12–21, 2012. View at Google Scholar
  100. S. Brummelte and L. A. M. Galea, “Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats,” Neuroscience, vol. 168, no. 3, pp. 680–690, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. J. Beauquis, P. Roig, A. F. de Nicola, and F. Saravia, “Short-term environmental enrichment enhances adult neurogenesis, vascular network and dendritic complexity in the hippocampus of type 1 diabetic mice,” PLoS ONE, vol. 5, no. 11, Article ID e13993, 2010. View at Publisher · View at Google Scholar · View at Scopus
  102. S. D. Jordan, A. C. Könner, and J. C. Brüning, “Sensing the fuels: glucose and lipid signaling in the CNS controlling energy homeostasis,” Cellular and Molecular Life Sciences, vol. 67, no. 19, pp. 3255–3273, 2010. View at Publisher · View at Google Scholar · View at Scopus
  103. A. Lindqvist, P. Mohapel, B. Bouter et al., “High-fat diet impairs hippocampal neurogenesis in male rats,” European Journal of Neurology, vol. 13, no. 12, pp. 1385–1388, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. H. R. Park, M. Park, J. Choi, K. Y. Park, H. Y. Chung, and J. Lee, “A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor,” Neuroscience Letters, vol. 482, no. 3, pp. 235–239, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. J. Lee, W. Duan, and M. P. Mattson, “Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice,” Journal of Neurochemistry, vol. 82, no. 6, pp. 1367–1375, 2002. View at Publisher · View at Google Scholar · View at Scopus
  106. K. van der Borght, R. Köhnke, N. Göransson et al., “Reduced neurogenesis in the rat hippocampus following high fructose consumption,” Regulatory Peptides, vol. 167, no. 1, pp. 26–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  107. G. Bertilsson, C. Patrone, O. Zachrisson et al., “Peptide hormone exendin-4 stimulates subventricular zone neurogenesis in the adult rodent brain and induces recovery in an animal model of Parkinson's disease,” Journal of Neuroscience Research, vol. 86, no. 2, pp. 326–338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. H. Li, C. H. Lee, K. Y. Yoo et al., “Chronic treatment of exendin-4 affects cell proliferation and neuroblast differentiation in the adult mouse hippocampal dentate gyrus,” Neuroscience Letters, vol. 486, no. 1, pp. 38–42, 2010. View at Publisher · View at Google Scholar · View at Scopus
  109. A. Hamilton, S. Patterson, D. Porter, V. A. Gault, and C. Holscher, “Novel GLP-1 mimetics developed to treat type 2 diabetes promote progenitor cell proliferation in the brain,” Journal of Neuroscience Research, vol. 89, no. 4, pp. 481–489, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. E. Faivre, V. A. Gault, B. Thorens, and C. Hölscher, “Glucose-dependent insulinotropic polypeptide receptor knockout mice are impaired in learning, synaptic plasticity, and neurogenesis,” Journal of Neurophysiology, vol. 105, no. 4, pp. 1574–1580, 2011. View at Publisher · View at Google Scholar · View at Scopus
  111. E. Faivre, A. Hamilton, and C. Holscher, “Effects of acute and chronic administration of GIP analogues on cognition, synaptic plasticity and neurogenesis in mice,” European Journal of Pharmacology, vol. 674, no. 2-3, pp. 294–306, 2012. View at Google Scholar
  112. J. Wang, D. Gallagher, L. M. Devito et al., “Metformin activates an atypical PKC-CBP pathway to promote neurogenesis and enhance spatial memory formation,” Cell Stem Cell, vol. 11, no. 1, pp. 23–35, 2012. View at Google Scholar
  113. M. A. Pierotti, F. Berrino, M. Gariboldi et al., “Targeting metabolism for cancer treatment and prevention: metformin, an old drug with multi-faceted effects,” Oncogene. In press.
  114. L. He, A. Sabet, S. Djedjos et al., “Metformin and insulin suppress hepatic gluconeogenesis through phosphorylation of CREB binding protein,” Cell, vol. 137, no. 4, pp. 635–646, 2009. View at Publisher · View at Google Scholar · View at Scopus
  115. M. Tavazoie, L. Van der Veken, V. Silva-Vargas et al., “A specialized vascular niche for adult neural stem cells,” Cell Stem Cell, vol. 3, no. 3, pp. 279–288, 2008. View at Publisher · View at Google Scholar · View at Scopus
  116. E. Kokovay, S. Goderie, Y. Wang et al., “Adult svz lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling,” Cell Stem Cell, vol. 7, no. 2, pp. 163–173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. M. V. Gomez-Gaviro, C. E. Scott, A. K. Sesay et al., “Betacellulin promotes cell proliferation in the neural stem cell niche and stimulates neurogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 4, pp. 1317–1322, 2012. View at Google Scholar
  118. R. Prakash, P. R. Somanath, A. B. El-Remessy et al., “Enhanced cerebral but not peripheral angiogenesis in the Goto-Kakizaki model of type 2 diabetes involves VEGF and peroxynitrite signaling,” Diabetes, vol. 61, no. 6, pp. 1533–1542, 2012. View at Google Scholar
  119. J. M. Parent, Z. S. Vexler, C. Gong, N. Derugin, and D. M. Ferriero, “Rat forebrain neurogenesis and striatal neuron replacement after focal stroke,” Annals of Neurology, vol. 52, no. 6, pp. 802–813, 2002. View at Publisher · View at Google Scholar · View at Scopus
  120. D. Nakayama, T. Matsuyama, H. Ishibashi-Ueda et al., “Injury-induced neural stem/progenitor cells in post-stroke human cerebral cortex,” European Journal of Neuroscience, vol. 31, no. 1, pp. 90–98, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. D. Sander and M. T. Kearney, “Reducing the risk of stroke in type 2 diabetes: pathophysiological and therapeutic perspectives,” Journal of Neurology, vol. 256, no. 10, pp. 1603–1619, 2009. View at Publisher · View at Google Scholar · View at Scopus
  122. V. Darsalia, S. Mansouri, H. Ortsater et al., “Glucagon-like peptide-1 receptor activation reduces ischaemic brain damage following stroke in Type 2 diabetic rats,” Clinical Science, vol. 122, no. 10, pp. 473–483, 2012. View at Google Scholar
  123. O. Lazarov and R. A. Marr, “Neurogenesis and Alzheimer's disease: at the crossroads,” Experimental Neurology, vol. 223, no. 2, pp. 267–281, 2010. View at Publisher · View at Google Scholar · View at Scopus
  124. L. G. Exalto, R. A. Whitmer, L. J. Kappele, and G. J. Biessels, “An update on type 2 diabetes,” Experimental Gerontology, vol. 47, no. 11, pp. 858–864, 2012. View at Google Scholar
  125. T. Ma, X. Du, J. E. Pick, G. Sui, M. Brownlee, and E. Klann, “Glucagon-like peptide-1 cleavage product GLP-1(9-36) amide rescues synaptic plasticity and memory deficits in Alzheimer's disease model mice,” The Journal of Neuroscience, vol. 32, no. 40, pp. 13701–13708, 2012. View at Google Scholar
  126. E. J. Rivera, A. Goldin, N. Fulmer, R. Tavares, J. R. Wands, and S. M. de la Monte, “Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine,” Journal of Alzheimer's Disease, vol. 8, no. 3, pp. 247–268, 2005. View at Google Scholar · View at Scopus
  127. S. M. de la Monte, “Contributions of brain insulin resistance and deficiency in amyloid-related neurodegeneration in Alzheimer's disease,” Drugs, vol. 72, no. 1, pp. 49–66, 2012. View at Google Scholar
  128. A. M. Moloney, R. J. Griffin, S. Timmons, R. O'Connor, R. Ravid, and C. O'Neill, “Defects in IGF-1 receptor, insulin receptor and IRS-1/2 in Alzheimer's disease indicate possible resistance to IGF-1 and insulin signalling,” Neurobiology of Aging, vol. 31, no. 2, pp. 224–243, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. P. Imfeld, M. Bodmer, S. S. Jick, and C. R. Meier, “Metformin, other antidiabetic drugs, and risk of Alzheimer's disease: a population-based case-control study,” Journal of the American Geriatrics Society, vol. 60, no. 5, pp. 916–921, 2012. View at Google Scholar
  130. E. Cereda, M. Barichella, C. Pedrolli et al., “Diabetes and risk of Parkinson's disease,” Movement Disorders. In press.
  131. Q. Xu, Y. Park, X. Huang et al., “Diabetes and risk of Parkinson's disease,” Diabetes Care, vol. 34, no. 4, pp. 910–915, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. K. M. Fox, R. A. Gerber Pharmd, B. Bolinder, J. Chen, and S. Kumar, “Prevalence of inadequate glycemic control among patients with type 2 diabetes in the United Kingdom general practice research database: a series of retrospective analyses of data from 1998 through 2002,” Clinical Therapeutics, vol. 28, no. 3, pp. 388–395, 2006. View at Publisher · View at Google Scholar · View at Scopus
  133. A. Cherubini, I. Spoletini, P. Péran et al., “A multimodal MRI investigation of the subventricular zone in mild cognitive impairment and Alzheimer's disease patients,” Neuroscience Letters, vol. 469, no. 2, pp. 214–218, 2010. View at Publisher · View at Google Scholar · View at Scopus
  134. S. Gluth, J. Rieskamp, and C. Buchel, “Deciding when to decide: time-variant sequential sampling models explain the emergence of value-based decisions in the human brain,” The Journal of Neuroscience, vol. 32, no. 31, pp. 10686–10698, 2012. View at Google Scholar