Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2015, Article ID 451512, 14 pages
http://dx.doi.org/10.1155/2015/451512
Research Article

Nitric Oxide Regulates Neurogenesis in the Hippocampus following Seizures

1Center for Neuroscience and Cell Biology, Neuroendocrinology and Neurogenesis Group, University of Coimbra, 3004-517 Coimbra, Portugal
2Regenerative Medicine Program, Department of Biomedical Sciences and Medicine, University of Algarve, 8005-139 Faro, Portugal
3Center for Biomedical Research (CBMR), University of Algarve, 8005-139 Faro, Portugal

Received 30 April 2015; Accepted 18 May 2015

Academic Editor: Renata Santos

Copyright © 2015 Bruno P. Carreira 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. F. H. Gage, “Mammalian neural stem cells,” Science, vol. 287, no. 5457, pp. 1433–1438, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Götz and W. B. Huttner, “The cell biology of neurogenesis,” Nature Reviews Molecular Cell Biology, vol. 6, no. 10, pp. 777–788, 2005. View at Publisher · View at Google Scholar
  3. 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
  4. F. H. Gage, P. W. Coates, T. D. Palmer et al., “Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 25, pp. 11879–11883, 1995. View at Publisher · View at Google Scholar · View at Scopus
  5. B. B. Stanfield and J. E. Trice, “Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections,” Experimental Brain Research, vol. 72, no. 2, pp. 399–406, 1988. View at Google Scholar · View at Scopus
  6. E. A. Markakis and F. H. Gage, “Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles,” The Journal of Comparative Neurology, vol. 406, no. 4, pp. 449–460, 1999. View at Google Scholar · View at Scopus
  7. F. Doetsch, L. Petreanu, I. Caille, J.-M. Garcia-Verdugo, and A. Alvarez-Buylla, “EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells,” Neuron, vol. 36, no. 6, pp. 1021–1034, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Shingo, C. Gregg, E. Enwere et al., “Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin,” Science, vol. 299, no. 5603, pp. 117–120, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. B. P. Carreira, M. I. Morte, A. S. Lourenço et al., “Differential contribution of the guanylyl cyclase-cyclic GMP-Protein kinase G pathway to the proliferation of neural stem cells stimulated by nitric oxide,” NeuroSignals, vol. 21, no. 1-2, pp. 1–13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. H. G. Kuhn, H. Dickinson-Anson, and F. H. Gage, “Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation,” The Journal of Neuroscience, vol. 16, no. 6, pp. 2027–2033, 1996. View at Google Scholar · View at Scopus
  11. S. M. Rothman and M. P. Mattson, “Adverse stress, hippocampal networks, and Alzheimer's disease,” NeuroMolecular Medicine, vol. 12, no. 1, pp. 56–70, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. J. Vukovic, D. G. Blackmore, D. Jhaveri, and P. F. Bartlett, “Activation of neural precursors in the adult neurogenic niches,” Neurochemistry International, vol. 59, no. 3, pp. 341–346, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. N. P. Whitney, T. M. Eidem, H. Peng, Y. Huang, and J. C. Zheng, “Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders,” Journal of Neurochemistry, vol. 108, no. 6, pp. 1343–1359, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. V. W. T. Liu and P. L. Huang, “Cardiovascular roles of nitric oxide: a review of insights from nitric oxide synthase gene disrupted mice,” Cardiovascular Research, vol. 77, no. 1, pp. 19–29, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. B. P. Carreira, M. I. Morte, Â. Inácio et al., “Nitric oxide stimulates the proliferation of neural stem cells bypassing the epidermal growth factor receptor,” Stem Cells, vol. 28, no. 7, pp. 1219–1230, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Bengzon, Z. Kokaia, E. Elmer, A. Nanobashvili, M. Kokaia, and O. Lindvall, “Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 19, pp. 10432–10437, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. J. M. Parent, T. W. Yu, R. T. Leibowitz, D. H. Geschwind, R. S. Sloviter, and D. H. Lowenstein, “Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus,” The Journal of Neuroscience, vol. 17, no. 10, pp. 3727–3738, 1997. View at Google Scholar · View at Scopus
  18. P. E. Schauwecker and O. Steward, “Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 8, pp. 4103–4108, 1997. View at Publisher · View at Google Scholar · View at Scopus
  19. W. P. Gray and L. E. Sundstrom, “Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat,” Brain Research, vol. 790, no. 1-2, pp. 52–59, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. J. M. Parent, “Adult neurogenesis in the intact and epileptic dentate gyrus,” Progress in Brain Research, vol. 163, pp. 529–817, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. J. M. Parent, “Injury-induced neurogenesis in the adult mammalian brain,” The Neuroscientist, vol. 9, no. 4, pp. 261–272, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Y. Zhu, S. H. Liu, H. S. Sun, and Y. M. Lu, “Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus,” The Journal of Neuroscience, vol. 23, no. 1, pp. 223–229, 2003. View at Google Scholar · View at Scopus
  23. P. K. Dash, S. A. Mach, and A. N. Moore, “Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury,” Journal of Neuroscience Research, vol. 63, no. 4, pp. 313–319, 2001. View at Publisher · View at Google Scholar
  24. A. C. Rice, A. Khaldi, H. B. Harvey et al., “Proliferation and neuronal differentiation of mitotically active cells following traumatic brain injury,” Experimental Neurology, vol. 183, no. 2, pp. 406–417, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Yoneyama, K. Kawada, Y. Gotoh, T. Shiba, and K. Ogita, “Endogenous reactive oxygen species are essential for proliferation of neural stem/progenitor cells,” Neurochemistry International, vol. 56, no. 6-7, pp. 740–746, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. B. P. Carreira, C. M. Carvalho, and I. M. Araújo, “Regulation of injury-induced neurogenesis by Nitric oxide,” Stem Cells International, vol. 2012, Article ID 895659, 15 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. O. W. Howell, K. Doyle, J. H. Goodman et al., “Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus,” Journal of Neurochemistry, vol. 93, no. 3, pp. 560–570, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Agasse, L. Bernardino, H. Kristiansen et al., “Neuropeptide Y promotes neurogenesis in murine subventricular zone,” Stem Cells, vol. 26, no. 6, pp. 1636–1645, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Cheung, P. L. Newland, M. Zaben, G. S. Attard, and W. P. Gray, “Intracellular nitric oxide mediates neuroproliferative effect of neuropeptide Y on postnatal hippocampal precursor cells,” The Journal of Biological Chemistry, vol. 287, no. 24, pp. 20187–20196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. Y.-S. Choi, H.-Y. Cho, K. R. Hoyt, J. R. Naegele, and K. Obrietan, “IGF-1 receptor-mediated ERK/MAPK signaling couples status epilepticus to progenitor cell proliferation in the subgranular layer of the dentate gyrus,” Glia, vol. 56, no. 7, pp. 791–800, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Nacher, C. Crespo, and B. S. McEwen, “Doublecortin expression in the adult rat telencephalon,” European Journal of Neuroscience, vol. 14, no. 4, pp. 629–644, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. A. S. Cosgrave, J. S. McKay, R. Morris, J. P. Quinn, and T. Thippeswamy, “The effects of nitric oxide inhibition prior to kainic acid treatment on neuro- and gliogenesis in the rat dentate gyrus in vivo and in vitro,” Histology and Histopathology, vol. 25, no. 7, pp. 841–856, 2010. View at Google Scholar · View at Scopus
  33. J. Chen, J. Qin, X. Liu et al., “Nitric oxide-mediated neuronal apoptosis in rats with recurrent febrile seizures through endoplasmic reticulum stress pathway,” Neuroscience Letters, vol. 443, no. 3, pp. 134–139, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Ishida, T. Sasaguri, C. Kosaka, H. Nojima, and J. Ogata, “Induction of the cyclin-dependent kinase inhibitor p21Sdi1/Cip1/Waf1 by nitric oxide-generating vasodilator in vascular smooth muscle cells,” The Journal of Biological Chemistry, vol. 272, no. 15, pp. 10050–10057, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Nakaya, S. W. Lowe, Y. Taya, A. Chenchik, and G. Enikolopov, “Specific pattern of p53 phosphorylation during nitric oxide-induced cell cycle arrest,” Oncogene, vol. 19, no. 54, pp. 6369–6375, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Covacu, A. I. Danilov, B. S. Rasmussen et al., “Nitric oxide exposure diverts neural stem cell fate from neurogenesis towards astrogliogenesis,” Stem Cells, vol. 24, no. 12, pp. 2792–2800, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. M. A. Packer, Y. Stasiv, A. Benraiss et al., “Nitric oxide negatively regulates mammalian adult neurogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 16, pp. 9566–9571, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Torroglosa, M. Murillo-Carretero, C. Romero-Grimaldi, E. R. Matarredona, A. Campos-Caro, and C. Estrada, “Nitric oxide decreases subventricular zone stem cell proliferation by inhibition of epidermal growth factor receptor and phosphoinositide-3-kinase/Akt pathway,” Stem Cells, vol. 25, no. 1, pp. 88–97, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. B. Moreno-López, C. Romero-Grimaldi, J. A. Noval, M. Murillo-Carretero, E. R. Matarredona, and C. Estrada, “Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb,” Journal of Neuroscience, vol. 24, no. 1, pp. 85–95, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Hua, X.-Y. Huang, L. Zhou et al., “DETA/NONOate, a nitric oxide donor, produces antidepressant effects by promoting hippocampal neurogenesis,” Psychopharmacology, vol. 200, no. 2, pp. 231–242, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Ciani, “Proliferation of cerebellar precursor cells is negatively regulated by nitric oxide in newborn rat,” Journal of Cell Science, vol. 119, no. 15, pp. 3161–3170, 2006. View at Publisher · View at Google Scholar