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Neural Plasticity
Volume 2015, Article ID 375391, 15 pages
http://dx.doi.org/10.1155/2015/375391
Research Article

Prophylactic Subacute Administration of Zinc Increases CCL2, CCR2, FGF2, and IGF-1 Expression and Prevents the Long-Term Memory Loss in a Rat Model of Cerebral Hypoxia-Ischemia

1Facultad de Ciencias Químicas, BUAP, 14 Sur y Avenida San Claudio, 72570 Puebla, PUE, Mexico
2Laboratorio de Medicina Genómica, Hospital Regional 1° de Octubre, ISSSTE, Avenida Instituto Politécnico Nacional No. 1669, 07760 México, DF, Mexico
3Departamento de Fisiología, Biofísica y Neurociencias, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Apartado Postal 14-740, 07000 México, DF, Mexico
4Instituto de Fisiología, BUAP, 14 Sur 6301, 72570 Puebla, PUE, Mexico

Received 6 February 2015; Revised 30 May 2015; Accepted 1 June 2015

Academic Editor: Preston E. Garraghty

Copyright © 2015 Victor Manuel Blanco-Alvarez 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. V. M. Blanco-Alvarez, P. Lopez-Moreno, G. Soto-Rodriguez et al., “Subacute zinc administration and L-name caused an increase of NO, Zinc, lipoperoxidation, and caspase-3 during a cerebral hypoxia-ischemia process in the rat,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 240560, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. Kitamura, Y. Iida, J. Abe et al., “Protective effect of zinc against ischemic neuronal injury in a middle cerebral artery occlusion model,” Journal of Pharmacological Sciences, vol. 100, no. 2, pp. 142–148, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Matsushita, K. Kitagawa, T. Matsuyama et al., “Effect of systemic zinc administration on delayed neuronal death in the gerbil hippocampus,” Brain Research, vol. 743, no. 1-2, pp. 362–365, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Miyawaki, H. Yokota, K. Oguro, K. Kato, and K. Shimazaki, “Ischemic preconditioning decreases intracellular zinc accumulation induced by oxygen-glucose deprivation in gerbil hippocampal CA1 neurons,” Neuroscience Letters, vol. 362, no. 3, pp. 216–219, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Xu, Z. Gong, W.-Z. Zhu et al., “Remote ischemic preconditioning protects neurocognitive function of rats following cerebral hypoperfusion,” Medical Science Monitor, vol. 17, no. 11, pp. 299–304, 2011. View at Google Scholar · View at Scopus
  6. J.-Y. Lee, Y.-J. Kim, T.-Y. Kim, J.-Y. Koh, and Y.-H. Kim, “Essential role for zinc-triggered p75NTR activation in preconditioning neuroprotection,” Journal of Neuroscience, vol. 28, no. 43, pp. 10919–10927, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. C. J. Frederickson, J.-Y. Koh, and A. I. Bush, “The neurobiology of zinc in health and disease,” Nature Reviews Neuroscience, vol. 6, no. 6, pp. 449–462, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. C. J. Frederickson, L. J. Giblin, A. Krezel et al., “Concentrations of extracellular free zinc (pZn)e in the central nervous system during simple anesthetization, ischemia and reperfusion,” Experimental Neurology, vol. 198, no. 2, pp. 285–293, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. M. A. Aras, H. Hara, K. A. Hartnett, K. Kandler, and E. Aizenman, “Protein kinase C regulation of neuronal zinc signaling mediates survival during preconditioning,” Journal of Neurochemistry, vol. 110, no. 1, pp. 106–117, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. G.-Q. Huang, J.-N. Wang, J.-M. Tang et al., “The combined transduction of copper, zinc-superoxide dismutase and catalase mediated by cell-penetrating peptide, PEP-1, to protect myocardium from ischemia-reperfusion injury,” Journal of Translational Medicine, vol. 9, article 73, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. Y.-E. Zhang, S.-Z. Fu, X.-Q. Li et al., “PEP-1-SOD1 protects brain from ischemic insult following asphyxial cardiac arrest in rats,” Resuscitation, vol. 82, no. 8, pp. 1081–1086, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. P. H. Chan, “Antioxidant-dependent amelioration of brain injury: role of CuZn-superoxide dismutase,” Journal of Neurotrauma, vol. 9, supplement 2, pp. S417–S423, 1992. View at Google Scholar · View at Scopus
  13. C. X. Alves, S. H. L. Vale, M. M. G. Dantas et al., “Positive effects of zinc supplementation on growth, GH, IGF1, and IGFBP3 in eutrophic children,” Journal of Pediatric Endocrinology and Metabolism, vol. 25, no. 9-10, pp. 881–887, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Aras and E. Aizenman, “Redox regulation of intracellular zinc: molecular signaling in the life and death of neurons,” Antioxidants and Redox Signaling, vol. 15, no. 8, pp. 2249–2263, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. G. K. Helal, “Systemic administration of Zn2+ during the reperfusion phase of transient cerebral ischaemia protects rat hippocampus against iron-catalysed postischaemic injury,” Clinical and Experimental Pharmacology and Physiology, vol. 35, no. 7, pp. 775–781, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Bao, A. S. Prasad, F. W. J. Beck et al., “Zinc decreases C-reactive protein, lipid peroxidation, and inflammatory cytokines in elderly subjects: a potential implication of zinc as an atheroprotective agent,” The American Journal of Clinical Nutrition, vol. 91, no. 6, pp. 1634–1641, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Xie, S. Chen, Y. Wu, and T. H. Murphy, “Prolonged deficits in parvalbumin neuron stimulation-evoked network activity despite recovery of dendritic structure and excitability in the somatosensory cortex following global ischemia in mice,” The Journal of Neuroscience, vol. 34, no. 45, pp. 14890–14900, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. A. M. Vergnano, N. Rebola, L. P. Savtchenko et al., “Zinc dynamics and action at excitatory synapses,” Neuron, vol. 82, no. 5, pp. 1101–1114, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Prakash, K. Bharti, and A. B. Majeed, “Zinc: indications in brain disorders,” Fundamental & Clinical Pharmacology, vol. 29, no. 2, pp. 131–149, 2015. View at Publisher · View at Google Scholar
  20. T. Nishi, C. M. Maier, T. Hayashi, A. Saito, and P. H. Chan, “Superoxide dismutase 1 overexpression reduces MCP-1 and MIP-1α expression after transient focal cerebral ischemia,” Journal of Cerebral Blood Flow and Metabolism, vol. 25, no. 10, pp. 1312–1324, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Losy and J. Zaremba, “Monocyte chemoattractant protein-1 is increased in the cerebrospinal fluid of patients with ischemic stroke,” Stroke, vol. 32, no. 11, pp. 2695–2696, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Zaremba, J. Ilkowski, and J. Losy, “Serial measurements of levels of the chemokines CCL2, CCL3 and CCL5 in serum of patients with acute ischaemic stroke,” Folia Neuropathologica, vol. 44, no. 4, pp. 282–289, 2006. View at Google Scholar · View at Scopus
  23. J. Losy, J. Zaremba, and P. Skrobański, “CXCL1 (GRO-alpha) chemokine in acute ischaemic stroke patients,” Folia Neuropathologica, vol. 43, no. 2, pp. 97–102, 2005. View at Google Scholar · View at Scopus
  24. J. Mojsilovic-Petrovic, D. Callaghan, H. Cui, C. Dean, D. B. Stanimirovic, and W. Zhang, “Hypoxia-inducible factor-1 (HIF-1) is involved in the regulation of hypoxia-stimulated expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) and MCP-5 (Ccl12) in astrocytes,” Journal of Neuroinflammation, vol. 4, article 12, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. X. Che, W. Ye, L. Panga, D.-C. Wu, and G.-Y. Yang, “Monocyte chemoattractant protein-1 expressed in neurons and astrocytes during focal ischemia in mice,” Brain Research, vol. 902, no. 2, pp. 171–177, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Liu, L. Zhang, Q. Wu, and T. Wang, “Chemokine CCL2 induces apoptosis in cortex following traumatic brain injury,” Journal of Molecular Neuroscience, vol. 51, no. 3, pp. 1021–1029, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Chen, J. M. Hallenbeck, C. Ruetzler et al., “Overexpression of monocyte chemoattractant protein 1 in the brain exacerbates ischemic brain injury and is associated with recruitment of inflammatory cells,” Journal of Cerebral Blood Flow and Metabolism, vol. 23, no. 6, pp. 748–755, 2003. View at Google Scholar · View at Scopus
  28. A. Stålman, D. Bring, and P. W. Ackermann, “Chemokine expression of CCL2, CCL3, CCL5 and CXCL10 during early inflammatory tendon healing precedes nerve regeneration: an immunohistochemical study in the rat,” Knee Surgery, Sports Traumatology, Arthroscopy, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. A. N. Kalehua, J. E. Nagel, L. M. Whelchel et al., “Monocyte chemoattractant protein-1 and macrophage inflammatory protein-2 are involved in both excitotoxin-induced neurodegeneration and regeneration,” Experimental Cell Research, vol. 297, no. 1, pp. 197–211, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. H. S. G. Kalluri, R. Vemuganti, and R. J. Dempsey, “Mechanism of insulin-like growth factor I-mediated proliferation of adult neural progenitor cells: role of Akt,” European Journal of Neuroscience, vol. 25, no. 4, pp. 1041–1048, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. H. S. G. Kalluri and R. J. Dempsey, “Growth factors, stem cells, and stroke,” Neurosurgical Focus, vol. 24, no. 3-4, p. E13, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Ruan, B. Wang, Q. ZhuGe, and K. Jin, “Coupling of neurogenesis and angiogenesis after ischemic stroke,” Brain Research, 2015. View at Publisher · View at Google Scholar
  33. S. Mélik-Parsadaniantz, “CCL2 chemokine and transmission of nociceptive information,” Biologie Aujourd'hui, vol. 204, no. 4, pp. 301–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. J. G. Bray, K. C. Reyes, A. J. Roberts, R. M. Ransohoff, and D. L. Gruol, “Synaptic plasticity in the hippocampus shows resistance to acute ethanol exposure in transgenic mice with astrocyte-targeted enhanced CCL2 expression,” Neuropharmacology, vol. 67, pp. 115–125, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Sakurai-Yamashita, K. Shigematsu, K. Yamashita, and M. Niwa, “Expression of MCP-1 in the hippocampus of SHRSP with ischemia-related delayed neuronal death,” Cellular and Molecular Neurobiology, vol. 26, no. 4–6, pp. 823–831, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. N. Tei, J. Tanaka, K. Sugimoto et al., “Expression of MCP-1 and fractalkine on endothelial cells and astrocytes may contribute to the invasion and migration of brain macrophages in ischemic rat brain lesions,” Journal of Neuroscience Research, vol. 91, no. 5, pp. 681–693, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Yamagami, M. Tamura, M. Hayashi et al., “Differential production of MCP-1 and cytokine-induced neutrophil chemoattractant in the ischemic brain after transient focal ischemia in rats,” Journal of Leukocyte Biology, vol. 65, no. 6, pp. 744–749, 1999. View at Google Scholar · View at Scopus
  38. O. B. Dimitrijevic, S. M. Stamatovic, R. F. Keep, and A. V. Andjelkovic, “Effects of the chemokine CCL2 on blood-brain barrier permeability during ischemia-reperfusion injury,” Journal of Cerebral Blood Flow & Metabolism, vol. 26, no. 6, pp. 797–810, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. O. B. Dimitrijevic, S. M. Stamatovic, R. F. Keep, and A. V. Andjelkovic, “Absence of the chemokine receptor CCR2 protects against cerebral ischemia/reperfusion injury in mice,” Stroke, vol. 38, no. 4, pp. 1345–1353, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. A. M. Stowe, B. K. Wacker, P. D. Cravens et al., “CCL2 upregulation triggers hypoxic preconditioning-induced protection from stroke,” Journal of Neuroinflammation, vol. 9, article 33, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. A. K. Rehni and T. G. Singh, “Involvement of CCR-2 chemokine receptor activation in ischemic preconditioning and postconditioning of brain in mice,” Cytokine, vol. 60, no. 1, pp. 83–89, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. O. Gonzalez-Perez, F. Jauregui-Huerta, and A. Y. Galvez-Contreras, “Immune system modulates the function of adult neural stem cells,” Current Immunology Reviews, vol. 6, no. 3, pp. 167–173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Naylor, K. K. Bowen, K. A. Sailor, R. J. Dempsey, and R. Vemuganti, “Preconditioning-induced ischemic tolerance stimulates growth factor expression and neurogenesis in adult rat hippocampus,” Neurochemistry International, vol. 47, no. 8, pp. 565–572, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. J. L. Herrmann, Y. Wang, A. M. Abarbanell, B. R. Weil, J. Tan, and D. R. Meldrum, “Preconditioning mesenchymal stem cells with transforming growth factor-alpha improves mesenchymal stem cell-mediated cardioprotection,” Shock, vol. 33, no. 1, pp. 24–30, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. H.-C. Chang, Y.-R. Yang, P. S. Wang, C.-H. Kuo, and R.-Y. Wang, “The neuroprotective effects of intramuscular insulin-like growth factor-I treatment in brain ischemic rats,” PLoS ONE, vol. 8, no. 5, Article ID e64015, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. D. De Geyter, W. Stoop, S. Sarre, J. De Keyser, and R. Kooijman, “Neuroprotective efficacy of subcutaneous insulin-like growth factor-I administration in normotensive and hypertensive rats with an ischemic stroke,” Neuroscience, vol. 250, pp. 253–262, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Jin-qiao, S. Bin, Z. Wen-hao, and Y. Yi, “Basic fibroblast growth factor stimulates the proliferation and differentiation of neural stem cells in neonatal rats after ischemic brain injury,” Brain and Development, vol. 31, no. 5, pp. 331–340, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Kooijman, S. Sarre, Y. Michotte, and J. D. Keyser, “Insulin-like growth factor I: a potential neuroprotective compound for the treatment of acute ischemic stroke?” Stroke, vol. 40, no. 4, pp. e83–e88, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. Z. Wang, H. Zhang, X. Xu et al., “BFGF inhibits ER stress induced by ischemic oxidative injury via activation of the PI3K/Akt and ERK1/2 pathways,” Toxicology Letters, vol. 212, no. 2, pp. 137–146, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. Z.-L. Wang, S.-M. Cheng, M.-M. Ma et al., “Intranasally delivered bFGF enhances neurogenesis in adult rats following cerebral ischemia,” Neuroscience Letters, vol. 446, no. 1, pp. 30–35, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Elkabes and A. B. Nicot, “Sex steroids and neuroprotection in spinal cord injury: a review of preclinical investigations.,” Experimental neurology, vol. 259, pp. 28–37, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. B. Gürer, H. Kertmen, E. Kasim et al., “Neuroprotective effects of testosterone on ischemia/reperfusion injury of the rabbit spinal cord,” Injury, vol. 46, no. 2, pp. 240–248, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Beltramini, P. Zambenedetti, W. Wittkowski, and P. Zatta, “Effects of steroid hormones on the Zn, Cu and MTI/II levels in the mouse brain,” Brain Research, vol. 1013, no. 1, pp. 134–141, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. B. Alicia Leon-Chavez, P. Aguilar-Alonso, J. A. Gonzalez-Barrios et al., “Increased nitric oxide levels and nitric oxide synthase isoform expression in the cerebellum of the taiep rat during its severe demyelination stage,” Brain Research, vol. 1121, no. 1, pp. 221–230, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. J. J. Sedmak and S. E. Grossberg, “A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G250,” Analytical Biochemistry, vol. 79, no. 1-2, pp. 544–552, 1977. View at Publisher · View at Google Scholar · View at Scopus
  56. J. A. Gonzalez-Barrios, B. Escalante, J. Valdés, B. A. León-Chávez, and D. Martinez-Fong, “Nitric oxide and nitric oxide synthases in the fetal cerebral cortex of rats following transient uteroplacental ischemia,” Brain Research, vol. 945, no. 1, pp. 114–122, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Morris, “Developments of a water-maze procedure for studying spatial learning in the rat,” Journal of Neuroscience Methods, vol. 11, no. 1, pp. 47–60, 1984. View at Publisher · View at Google Scholar · View at Scopus
  58. J. E. Ramsey and J. D. Fontes, “The zinc finger transcription factor ZXDC activates CCL2 gene expression by opposing BCL6-mediated repression,” Molecular Immunology, vol. 56, no. 4, pp. 768–780, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. R. P. Panganiban, B. M. Vonakis, F. T. Ishmael, and C. Stellato, “Coordinated post-transcriptional regulation of the chemokine system: messages from CCL2,” Journal of Interferon and Cytokine Research, vol. 34, no. 4, pp. 255–266, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Fan, N. M. Heller, M. Gorospe, U. Atasoy, and C. Stellato, “The role of post-transcriptional regulation in chemokine gene expression in inflammation and allergy,” European Respiratory Journal, vol. 26, no. 5, pp. 933–947, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. T. Hamilton, M. Novotny, P. J. Pavicic et al., “Diversity in post-transcriptional control of neutrophil chemoattractant cytokine gene expression,” Cytokine, vol. 52, no. 1-2, pp. 116–122, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. P. E. Kolattukudy and J. Niu, “Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/CCR2 pathway,” Circulation Research, vol. 110, no. 1, pp. 174–189, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Schilling, J.-K. Strecker, W.-R. Schäbitz, E. B. Ringelstein, and R. Kiefer, “Effects of monocyte chemoattractant protein 1 on blood-borne cell recruitment after transient focal cerebral ischemia in mice,” Neuroscience, vol. 161, no. 3, pp. 806–812, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. J. Niu and P. E. Kolattukudy, “Role of MCP-1 in cardiovascular disease: molecular mechanisms and clinical implications,” Clinical Science, vol. 117, no. 3, pp. 95–109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. H.-M. Woo, J.-H. Kang, T. Kawada, H. Yoo, M.-K. Sung, and R. Yu, “Active spice-derived components can inhibit inflammatory responses of adipose tissue in obesity by suppressing inflammatory actions of macrophages and release of monocyte chemoattractant protein-1 from adipocytes,” Life Sciences, vol. 80, no. 10, pp. 926–931, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. R. H. Andres, R. Choi, A. V. Pendharkar et al., “The CCR2/CCL2 interaction mediates the transendothelial recruitment of intravascularly delivered neural stem cells to the ischemic brain,” Stroke, vol. 42, no. 10, pp. 2923–2931, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. R. J. Gordon, A. L. McGregor, and B. Connor, “Chemokines direct neural progenitor cell migration following striatal cell loss,” Molecular and Cellular Neuroscience, vol. 41, no. 2, pp. 219–232, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. S. K. Tang, R. A. Knobloch, C. Maucksch, and B. Connor, “Redirection of doublecortin-positive cell migration by over-expression of the chemokines MCP-1, MIP-1alpha and GRO-alpha in the adult rat brain,” Neuroscience, vol. 260, pp. 240–248, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. A. E. Hinojosa, B. Garcia-Bueno, J. C. Leza, and J. L. M. Madrigal, “CCL2/MCP-1 modulation of microglial activation and proliferation,” Journal of Neuroinflammation, vol. 8, article 77, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. X. Luo, X. Zhang, W. Shao, Y. Yin, and J. Zhou, “Crucial roles of MZF-1 in the transcriptional regulation of apomorphine-induced modulation of FGF-2 expression in astrocytic cultures,” Journal of Neurochemistry, vol. 108, no. 4, pp. 952–961, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Fujiwara and T. Kaji, “Zinc potentiates the stimulation by basic and acidic fibroblast growth factors on the proliferation of cultured vascular smooth muscle cells,” Research Communications in Molecular Pathology and Pharmacology, vol. 97, no. 1, pp. 95–106, 1997. View at Google Scholar · View at Scopus
  72. S. Bake, A. Selvamani, J. Cherry, and F. Sohrabji, “Blood brain barrier and neuroinflammation are critical targets of IGF-1-mediated neuroprotection in stroke for middle-aged female rats,” PLoS ONE, vol. 9, no. 3, Article ID e91427, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. G. Koçer, M. Nazıroğlu, Ö. Çelik et al., “Basic fibroblast growth factor attenuates bisphosphonate-induced oxidative injury but decreases zinc and copper levels in oral epithelium of rat,” Biological Trace Element Research, vol. 153, no. 1–3, pp. 251–256, 2013. View at Publisher · View at Google Scholar
  74. E. Yoshida, T. G. Atkinson, and B. Chakravarthy, “Neuroprotective gene expression profiles in ischemic cortical cultures preconditioned with IGF-1 or bFGF,” Molecular Brain Research, vol. 131, no. 1-2, pp. 33–50, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. M. M. Adams, T. D. Smith, D. Moga et al., “Hippocampal dependent learning ability correlates with N-methyl-D-aspartate (NMDA) receptor levels in CA3 neurons of young and aged rats,” Journal of Comparative Neurology, vol. 432, no. 2, pp. 230–243, 2001. View at Publisher · View at Google Scholar · View at Scopus
  76. V. Ramíarez-Amaya, I. Balderas, J. Sandoval, M. L. Escobar, and F. Bermúdez-Rattoni, “Spatial long-term memory is related to mossy fiber synaptogenesis,” Journal of Neuroscience, vol. 21, no. 18, pp. 7340–7348, 2001. View at Google Scholar · View at Scopus
  77. K. M. Frick, M. G. Baxter, A. L. Markowska, D. S. Olton, and D. L. Price, “Age-related spatial reference and working memory deficits assessed in the water maze,” Neurobiology of Aging, vol. 16, no. 2, pp. 149–160, 1995. View at Publisher · View at Google Scholar · View at Scopus
  78. E. C. Cope, D. R. Morris, A. G. Scrimgeour, and C. W. Levenson, “Use of zinc as a treatment for traumatic brain injury in the rat: effects on cognitive and behavioral outcomes,” Neurorehabilitation and Neural Repair, vol. 26, no. 7, pp. 907–913, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. S. T. Boroujeni, N. Naghdi, M. Shahbazi et al., “The effect of severe zinc deficiency and zinc supplement on spatial learning and memory,” Biological Trace Element Research, vol. 130, no. 1, pp. 48–61, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. Y. Xie, Y. Wang, T. Zhang, G. Ren, and Z. Yang, “Effects of nanoparticle zinc oxide on spatial cognition and synaptic plasticity in mice with depressive-like behaviors,” Journal of Biomedical Science, vol. 19, no. 1, pp. 1–11, 2012. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Ceccom, E. Bouhsira, H. Halley, S. Daumas, and J. M. Lassalle, “Differential needs of zinc in the CA3 area of dorsal hippocampus for the consolidation of contextual fear and spatial memories,” Learning & Memory, vol. 20, no. 7, pp. 348–351, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Zechel, S. Werner, K. Unsicker, and O. von Bohlen und Halbach, “Expression and functions of fibroblast growth factor 2 (FGF-2) in hippocampal formation,” Neuroscientist, vol. 16, no. 4, pp. 357–373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. Q. Ding, S. Vaynman, M. Akhavan, Z. Ying, and F. Gomez-Pinilla, “Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function,” Neuroscience, vol. 140, no. 3, pp. 823–833, 2006. View at Publisher · View at Google Scholar · View at Scopus