Prophylactic Chronic Zinc Administration Increases Neuroinflammation in a Hypoxia-Ischemia Model

Journal of Immunology Research

Volumn 2016, Issue , 2016, Pages

  Tomas Sanchez, Constantino ^a   Blanco Alvarez, Victor Manuel ^a   Gonzalez Barrios, Juan Antonio ^b   Martinez Fong, Daniel ^c   Garcia Robles, Guadalupe ^a   Soto Rodriguez, Guadalupe ^c   Brambila, Eduardo ^a   Torres Soto, Maricela ^a   Gonzalez Vazquez, Alejandro ^a   Aguilar Peralta, Ana Karina ^a   Garate Morales, José Luis ^a   Aguilar Carrasco, Luis Angel ^a   Limón, Daniel I ^a   Cebada, Jorge ^a   Leon Chavez, Bertha Alicia ^a  

^a BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

^b HOSPITAL REGIONAL 1 DE OCTUBRE   (Mexico)

^c DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR8; CHEMOKINE RECEPTOR CXCR2; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; CHEMOKINE RECEPTOR CXCR6; CHEMOKINE RECEPTOR CXCR7; CXCL13 CHEMOKINE; EOTAXIN; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; FIBROBLAST GROWTH FACTOR 2; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 5; NITRITE; RANTES; STROMAL CELL DERIVED FACTOR 1; TUMOR NECROSIS FACTOR; VASCULOTROPIN A; ZINC; CHEMOKINE; CHEMOKINE RECEPTOR; CHLORIDE; NEUROPROTECTIVE AGENT; ZINC CHLORIDE; ZINC DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HIPPOCAMPUS; HYPOXIC ISCHEMIC ENCEPHALOPATHY; LIPID PEROXIDATION; LONG TERM MEMORY; MALE; NERVOUS SYSTEM INFLAMMATION; NITROSATIVE STRESS; NONHUMAN; RAT; TEMPOROPARIETAL JUNCTION; UPREGULATION; ANIMAL; BLOOD; DISEASE MODEL; DRUG ADMINISTRATION; DRUG EFFECTS; GENETICS; HYPOXIA-ISCHEMIA, BRAIN; IMMUNOLOGY; IMMUNOMODULATION; MAZE TEST; MEMORY; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; WISTAR RAT;

ANIMALS; CHEMOKINES; CHLORIDES; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; FIBROBLAST GROWTH FACTOR 2; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; MALE; MAZE LEARNING; MEMORY; NEUROIMMUNOMODULATION; NEURONS; NEUROPROTECTIVE AGENTS; NITRITES; RATS; RATS, WISTAR; RECEPTORS, CHEMOKINE; ZINC COMPOUNDS;

EID: 84984701752     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2016/4039837     Document Type: Article

References (93)

1. S. C. Johnston, S. Mendis, and C. D. Mathers, "Global variation in stroke burden and mortality: estimates from monitoring, surveillance, and modelling," The Lancet Neurology, vol. 8, no. 4, pp. 345-354, 2009.
2. A. Tuttolomondo, D. Di Raimondo, R. di Sciacca, A. Pinto, and G. Licata, "Inflammatory cytokines in acute ischemic stroke," Current Pharmaceutical Design, vol. 14, no. 33, pp. 3574-3589, 2008.
3. M. I. Cuartero, I. Ballesteros, I. Lizasoain, and M. A. Moro, "Complexity of the cell-cell interactions in the innate immune response after cerebral ischemia," Brain Research, vol. 1623, pp. 53-62, 2015.
4. M. Mirabelli-Badenier, V. Braunersreuther, G. L. Viviani et al., "CC and CXC chemokines are pivotal mediators of cerebral injury in ischaemic stroke," Thrombosis and Haemostasis, vol. 105, no. 3, pp. 409-420, 2011.
5. A. Zlotnik and O. Yoshie, "Chemokines: a new classification system and their role in immunity," Immunity, vol. 12, no. 2, pp. 121-127, 2000.
6. R. J. Gordon, A. L. McGregor, and B. Connor, "Chemokines direct neural progenitor cell migration following striatal cell loss,"Molecular and CellularNeuroscience, vol. 41,no. 2, pp. 219-232, 2009.
7. T. Liu, P. R. Young, P. C. McDonnell, R. F. White, F. C. Barone, and G. Z. Feuerstein, "Cytokine-induced neutrophil chemoattractant mRNA expressed in cerebral ischemia," Neuroscience Letters, vol. 164, no. 1-2, pp. 125-128, 1993.
8. 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 brainmacrophages in ischemic rat brain lesions," Journal of Neuroscience Research, vol. 91, no. 5, pp. 681-693, 2013.
9. B. Yang, X. Xi, J. Aronowski, and S. I. Savitz, "Ischemic strokemay activate bonemarrowmononuclear cells to enhance recovery after stroke," Stem Cells and Development, vol. 21, no. 18, pp. 3332-3340, 2012.
10. T. Zhang and P. Li, "Expression and significance of mRNA for MIP-1alpha in cerebral tissue of newborn rat with hypoxicischemic brain damage," Sichuan Da Xue Xue Bao Yi Xue Ban, vol. 36, pp. 240-242, 2005.
11. S. Takami, H. Nishikawa, M. Minami et al., "Induction of macrophage inflammatory protein MIP-1αmRNA on glial cells after focal cerebral ischemia in the rat,"Neuroscience Letters, vol. 227, no. 3, pp. 173-176, 1997.
12. S. Terao, G. Yilmaz, K. Y. Stokes et al., "Blood cell-derived RANTES mediates cerebral microvascular dysfunction, inflammation, and tissue injury after focal ischemia-reperfusion," Stroke, vol. 39, no. 9, pp. 2560-2570, 2008.
13. M. Li, J. S. Hale, J. N. Rich, R. M. Ransohoff, and J. D. Lathia, "Chemokine CXCL12 in neurodegenerative diseases: an SOS signal for stem cell-based repair," Trends in Neurosciences, vol. 35, no. 10, pp. 619-628, 2012.
14. 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.
15. W.-Q. Shi, G.-Y. Zheng, X.-D. Chen, Y.-G. Zhu, J. Zhang, and Q. Jiang, "The expression of bFGF, GAP-43 and neurogenesis after cerebral ischemia/reperfusion in rats," Zhongguo Ying Yong Sheng Li Xue Za Zhi, vol. 29, no. 1, pp. 63-67, 2013.
16. H. Haase and L. Rink, "Multiple impacts of zinc on immune function,"Metallomics: Integrated Biometal Science, vol. 6, no. 7, pp. 1175-1180, 2014.
17. H. Haase and L. Rink, "Zinc signals and immune function," BioFactors, vol. 40, no. 1, pp. 27-40, 2014.
18. M. Foster and S. Samman, "Zinc and Regulation of inflammatory cytokines: implications for cardiometabolic disease," Nutrients, vol. 4, no. 7, pp. 676-694, 2012.
19. L. Rink andH. Haase, "Zinc homeostasis and immunity," Trends in Immunology, vol. 28, no. 1, pp. 1-4, 2007.
20. L. S. Mayer, P. Uciechowski, S. Meyer, T. Schwerdtle, L. Rink, and H. Haase, "Differential impact of zinc deficiency on phagocytosis, oxidative burst, and production of pro-inflammatory cytokines by human monocytes," Metallomics, vol. 6, no. 7, pp. 1288-1295, 2014.
21. Y. Yamasaki, T. Suzuki, H. Yamaya, N. Matsuura, H. Onodera, and K. Kogure, "Possible involvement of interleukin-1 in ischemic brain edema formation," Neuroscience Letters, vol. 142, no. 1, pp. 45-47, 1992.
22. 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.
23. V. M. Blanco-Alvarez, G. Soto-Rodriguez, J. A. Gonzalez-Barrios et al., "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," Neural Plasticity, vol. 2015, Article ID 375391, 15 pages, 2015.
24. X. Luo, X. Zhang, W. Shao, Y. Yin, and J. Zhou, "Crucial roles of MZF-1 in the transcriptional regulation of apomorphineinducedmodulation of FGF-2 expression in astrocytic cultures," Journal of Neurochemistry, vol. 108, no. 4, pp. 952-961, 2009.
25. C. Yamamoto, N. Fukuda, T. Matsumoto, T. Higuchi, T. Ueno, and K. Matsumoto, "Zinc-finger transcriptional factor Sall1 induces angiogenesis by activation of the gene for VEGF-A," Hypertension Research, vol. 33, no. 2, pp. 143-148, 2010.
26. R. S. MacDonald, "The role of zinc in growth and cell proliferation," Journal of Nutrition, vol. 130, supplement 5, pp. 1500S-1508S, 2000.
27. G.-H. Zhao, P. Yu, X.-S. Hu, and L. Zhao, "Effect of Zn(II) on the structure and biological activity of natural β-NGF," Acta Biochimica et Biophysica Sinica, vol. 36, no. 2, pp. 99-104, 2004.
28. K. Vogt, J. Mellor, G. Tong, and R. Nicoll, "The actions of synaptically released zinc at hippocampalmossy fiber synapses," Neuron, vol. 26, no. 1, pp. 187-196, 2000.
29. J. K. Ketterman and Y. V. Li, "Presynaptic evidence for zinc release at the mossy fiber synapse of rat hippocampus," Journal of Neuroscience Research, vol. 86, no. 2, pp. 422-434, 2008.
30. T. D. Palmer,A. R. Willhoite, and F. H. Gage, "Vascular niche for adult hippocampal neurogenesis," The Journal of Comparative Neurology, vol. 425, no. 4, pp. 479-494, 2000.
31. Y. Yang, X.-P. Jing, S.-P. Zhang et al., "High dose zinc supplementation induces hippocampal zinc deficiency and memory impairment with inhibition ofBDNF signaling," PLoSONE, vol. 8, article e55384, 2013.
32. A. Piechal, K. Blecharz-Klin, J. Pyrzanowska, and E. Widy-Tyszkiewicz, "Maternal zinc supplementation improves spatial memory in rat pups," Biological Trace Element Research, vol. 147, no. 1-3, pp. 299-308, 2012.
33. A. Adamcakova-Dodd, L. V. Stebounova, J. S. Kim et al., "Toxicity assessment of zinc oxide nanoparticles using subacute and sub-chronic murine inhalation models," Particle and Fibre Toxicology, vol. 11, no. 1, article 15, 2014.
34. H. Yorulmaz, F. B. Seker, G. Demir, I. E. Yalcin, and B. Oztas, "The effects of zinc treatment on the blood-brain barrier permeability and brain element levels during convulsions," Biological Trace Element Research, vol. 151, no. 2, pp. 256-262, 2013.
35. M. Sowa-Kucma, M. Kowalska, M. Szlósarczyk et al., "Chronic treatment with zinc and antidepressants induces enhancement of presynaptic/extracellular zinc concentration in the rat prefrontal cortex," Amino Acids, vol. 40, no. 1, pp. 249-258, 2011.
36. E. Brambila, J. L. Munoz-Sánchez, A. Albores, and M. Waalkes, "Early effects of surgery on zinc and metallothionein levels in female rats," Biological Trace Element Research, vol. 70, no. 2, pp. 173-182, 1999.
37. B. A. León-Chávez, J. A. Gonzalez-Barrios, A. Ugarte, M. A. Meraz, and D. Martinez-Fong, "Evidence in vitro of glial cell priming in the taiep rat," Brain Research, vol. 965, no. 1-2, pp. 274-278, 2003.
38. D. Gerard-Monnier, I. Erdelmeier, K. Regnard, N. Moze-Henry, J. C. Yadan, and J. Chaudiere, "Reactions of 1-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Analytical applications to a colorimetric assay of lipid peroxidation," Chemical Research in Toxicology, vol. 11, no. 10, pp. 1176-1183, 1998.
39. B. Alicia Leon-Chavez, P. Aguilar-Alonso, J. Antonio 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.
40. 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.
41. S. Elmore, "Apoptosis: a review of programmed cell death," Toxicologic Pathology, vol. 35, no. 4, pp. 495-516, 2007.
42. 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.
43. M. A. Erickson, Y. Morofuji, J. B. Owen, and W. A. Banks, "Rapid transport of CCL11 across the blood-brain barrier: regional variation and importance of blood cells," The Journal of Pharmacology and ExperimentalTherapeutics, vol. 349, no. 3, pp. 497-507, 2014.
44. S. Beaulieu, D. F. Robbiani, X. Du et al., "Expression of a functional eotaxin (CC chemokine ligand 11) receptor CCR3 by human dendritic cells," The Journal of Immunology, vol. 169, pp. 2925-2936, 2002.
45. J. L. Williams, D. W. Holman, and R. S. Klein, "Chemokines in the balance: maintenance of homeostasis and protection at CNS barriers," Frontiers in Cellular Neuroscience, vol. 8, article 154, 2014.
46. J. P. Warrington, "Placental ischemia increases seizure susceptibility and cerebrospinal fluid cytokines," Physiological Reports, vol. 3, no. 11, article e12634, 2015.
47. S. J. Collington, J. Westwick, T. J. Williams, and C. L. Weller, "The function of CCR3 on mouse bone marrow-derived mast cells in vitro," Immunology, vol. 129, no. 1, pp. 115-124, 2010.
48. F. Sallusto, D. Impellizzieri, C. Basso et al., "T-cell trafficking in the central nervous system," Immunological Reviews, vol. 248, no. 1, pp. 216-227, 2012.
49. Y. Terao, H. Ohta, A. Oda, Y. Nakagaito, Y. Kiyota, and Y. Shintani, "Macrophage inflammatory protein-3alpha plays a key role in the inflammatory cascade in rat focal cerebral ischemia," Neuroscience Research, vol. 64, no. 1, pp. 75-82, 2009.
50. J. Zaremba, P. Skrobánski, and J. Losy, "The level of chemokine CXCL5 in the cerebrospinal fluid is increased during the first 24 hours of ischaemic stroke and correlates with the size of early brain damage," Folia Morphologica, vol. 65, no. 1, pp. 1-5, 2006.
51. L.-Y. Wang, Y.-F. Tu, Y.-C. Lin, and C.-C. Huang, "CXCL5 signaling is a shared pathway of neuroinflammation and bloodbrain barrier injury contributing to white matter injury in the immature brain," Journal of Neuroinflammation, vol. 13, no. 1, article 6, 2016.
52. J. H. Shin, Y. M. Park, D. H. Kim et al., "Ischemic brain extract increases SDF-1 expression in astrocytes through the CXCR2/miR-223/miR-27b pathway," Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, vol. 1839, no. 9, pp. 826-836, 2014.
53. J. Yoo, J.-J. Seo, J.-H. Eom, and D.-Y. Hwang, "Effects of stromal cell-derived factor 1αdelivered at different phases of transient focal ischemia in rats," Neuroscience, vol. 209, pp. 171-186, 2012.
54. A. A. Ardelt, B. J. Bhattacharyya, A. Belmadani, D. Ren, and R. J. Miller, "Stromal derived growth factor-1 (CXCL12) modulates synaptic transmission to immature neurons during post-ischemic cerebral repair," Experimental Neurology, vol. 248, pp. 246-253, 2013.
55. L. Cui, H. Qu, T. Xiao, M. Zhao, J. Jolkkonen, and C. Zhao, "Stromal cell-derived factor-1 and its receptor CXCR4 in adult neurogenesis after cerebral ischemia," RestorativeNeurology and Neuroscience, vol. 31, no. 3, pp. 239-251, 2013.
56. S. Ge, L. Song, D. R. Serwanski, W. A. Kuziel, and J. S. Pachter, "Transcellular transport of CCL2 across brain microvascular endothelial cells," Journal of Neurochemistry, vol. 104, no. 5, pp. 1219-1232, 2008.
57. 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.
58. 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.
59. 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.
60. F. Dong,M. Khalil, M. Kiedrowski et al., "Critical role for leukocyte hypoxia inducible factor-1αexpression in post-myocardial infarction left ventricular remodeling," Circulation Research, vol. 106, no. 3, pp. 601-610, 2010.
61. X. Wang, X. Li, D. B. Schmidt et al., "Identification and molecular characterization of rat CXCR3: receptor expression and interferon-inducible protein-10 binding are increased in focal stroke," Molecular Pharmacology, vol. 57, no. 6, pp. 1190-1198, 2000.
62. A. Song, A. Patel, K. Thamatrakoln et al., "Functional domains andDNA-binding sequences of RFLAT-1/KLF13, aKrüppel-like transcription factor of activated T lymphocytes," The Journal of Biological Chemistry, vol. 277, no. 33, pp. 30055-30065, 2002.
63. P. Wolinski and A. Glabinski, "Chemokines and neurodegeneration in the early stage of experimental ischemic stroke," Mediators of Inflammation, vol. 2013,Article ID727189, 9 pages, 2013.
64. H. Tokami, T. Ago, H. Sugimori et al., "RANTES has a potential to play a neuroprotective role in an autocrine/paracrinemanner after ischemic stroke," Brain Research, vol. 1517, pp. 122-132, 2013.
65. A. M. Robin, Z. G. Zhang, L. Wang et al., "Stromal cellderived factor 1αmediates neural progenitor cell motility after focal cerebral ischemia," Journal of Cerebral Blood Flow and Metabolism, vol. 26, no. 1, pp. 125-134, 2006.
66. Y. Wu, H. Peng, M. Cui, N. P. Whitney, Y. Huang, and J. C. Zheng, "CXCL12 increases human neural progenitor cell proliferation through Akt-1/FOXO3a signaling pathway," Journal of Neurochemistry, vol. 109, no. 4, pp. 1157-1167, 2009.
67. J. J. Merino, V. Bellver-Landete, M. J. Oset-Gasque, and B. Cubelos, "CXCR4/CXCR7 molecular involvement in neuronal and neural progenitor migration: focus in CNS repair," Journal of Cellular Physiology, vol. 230, no. 1, pp. 27-42, 2015.
68. U. M. Selvaraj, S. B. Ortega, R. Hu et al., "Preconditioninginduced CXCL12 upregulation minimizes leukocyte infiltration after stroke in ischemia-tolerant mice," Journal of Cerebral Blood Flow & Metabolism, 2016.
69. Q. Yu, L. Zhou, L. Liu et al., "Stromal cell-derived factor-1 alpha alleviates hypoxic-ischemic brain damage in mice," Biochemical and Biophysical Research Communications, vol. 464, no. 2, pp. 447-452, 2015.
70. Y. Li, G. Tang, Y. Liu et al., "CXCL12 gene therapy ameliorates ischemia-induced white matter injury in mouse brain," Stem Cells Translational Medicine, vol. 4, no. 10, pp. 1122-1130, 2015.
71. S. Shahrara, C. C. Park, V. Temkin, J. W. Jarvis, M. V. Volin, and R. M. Pope, "RANTES modulates TLR4-induced cytokine secretion in human peripheral blood monocytes," The Journal of Immunology, vol. 177, no. 8, pp. 5077-5087, 2006.
72. S. Abi-Younes, A. Sauty, F. Mach, G. K. Sukhova, P. Libby, and A. D. Luster, "The stromal cell-derived factor-1 chemokine is a potent platelet agonist highly expressed in atherosclerotic plaques," Circulation Research, vol. 86, no. 2, pp. 131-138, 2000.
73. B. Schönemeier, S. Schulz, V. Hoellt, and R. Stumm, "Enhanced expression of the CXCl12/SDF-1 chemokine receptor CXCR7 after cerebral ischemia in the rat brain," Journal of Neuroimmunology, vol. 198, no. 1-2, pp. 39-45, 2008.
74. Y. Wang, W. Fu, S. Zhang et al., "CXCR-7 receptor promotes SDF-1α-induced migration of bone marrow mesenchymal stem cells in the transient cerebral ischemia/reperfusion rat hippocampus," Brain Research, vol. 1575, no. 1, pp. 78-86, 2014.
75. L. Wang, Q. Chen, G. Li, and D. Ke, "Ghrelin stimulates angiogenesis via GHSR1a-dependent MEK/ERK and PI3K/Akt signal pathways in rat cardiac microvascular endothelial cells," Peptides, vol. 33, no. 1, pp. 92-100, 2012.
76. J. H. Seo, J. H. Yu,H. Suh,M.-S. Kim, and S.-R. Cho, "Fibroblast growth factor-2 induced by enriched environment enhances angiogenesis and motor function in chronic hypoxic-ischemic brain injury," PLoS ONE, vol. 8, no. 9,Article ID e74405, 2013.
77. Q. Ruan, C. Zhao, Z. Ye, J. Ruan,Q. Xie, and W. Xie, "Effect and possiblemechanismofmonocyte-derivedVEGF onmonocyteendothelial cellular adhesion after electrical burns," Burns, vol. 41, no. 4, pp. 825-832, 2015.
78. J. Yang, Y. Yao, T. Chen, and T. Zhang, "VEGF ameliorates cognitive impairment in in vivo and in vitro ischemia via improving neuronal viability and function," NeuroMolecular Medicine, vol. 16, no. 2, pp. 376-388, 2014.
79. A. Pikula, A. S. Beiser, T. C. Chen et al., "Serum brain-derived neurotrophic factor and vascular endothelial growth factor levels are associatedwith risk of stroke and vascular brain injury framingham study," Stroke, vol. 44, no. 10, pp. 2768-2775, 2013.
80. X.-J. Ke and J.-J. Zhang, "Changes in HIF-1α, VEGF, NGF and BDNF levels in cerebrospinal fluid and their relationship with cognitive impairment in patients with cerebral infarction," Journal of Huazhong University of Science and Technology: Medical Sciences, vol. 33, no. 3, pp. 433-437, 2013.
81. B. Bielecki, A. Mazurek, P. Wolinski, and A. Glabinski, "Expression of chemokine receptors CCR7 and CCR8 in the CNS during ChREAE," Scandinavian Journal of Immunology, vol. 66, no. 4, pp. 383-392, 2007.
82. J. X. Liu,X. Cao,Y. C. Tang, Y. Liu, andF. R. Tang, "CCR7, CCR8, CCR9 and CCR10 in the mouse hippocampal CA1 area and the dentate gyrus during and after pilocarpine-induced status epilepticus," Journal of Neurochemistry, vol. 100, no. 4, pp. 1072-1088, 2007.
83. V. H. Brait, J. Rivera, B. R. S. Broughton, S. Lee, G. R. Drummond, and C. G. Sobey, "Chemokine-related gene expression in the brain following ischemic stroke: no role for CXCR2 in outcome," Brain Research, vol. 1372, pp. 169-179, 2011.
84. B. K. Popivanova, K. Koike, A. B. Tonchev et al., "Accumulation of microglial cells expressing ELR motif-positive CXC chemokines and their receptor CXCR2 in monkey hippocampus after ischemia-reperfusion," Brain Research, vol. 970, no. 1-2, pp. 195-204, 2003.
85. N. L. Monson, S. B. Ortega, S. J. Ireland et al., "Repetitive hypoxic preconditioning induces an immunosuppressed B cell phenotype during endogenous protection from stroke," Journal of Neuroinflammation, vol. 11, article no. 22, 2014.
86. W. L. Thompson and L. J. Van Eldik, "Inflammatory cytokines stimulate the chemokines CCL2/MCP-1 and CCL7/MCP-3 through NFB and MAPK dependent pathways in rat astrocytes," Brain Research, vol. 1287, pp. 47-57, 2009.
87. C. E. Repeke, S. B. Ferreira, M. Claudino et al., "Evidences of the cooperative role of the chemokines CCL3, CCL4 and CCL5 and its receptors CCR1+ and CCR5+ in RANKL+ cell migration throughout experimental periodontitis in mice," Bone, vol. 46, no. 4, pp. 1122-1130, 2010.
88. M. Li and R. M. Ransohoff, "Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology," Progress inNeurobiology, vol. 84, no. 2, pp. 116-131, 2008.
89. Y. S. Song, Y.-S. Lee, P. Narasimhan, and P. H. Chan, "Reduced oxidative stress promotes NF-κB-mediated neuroprotective gene expression after transient focal cerebral ischemia: lymphocytotrophic cytokines and antiapoptotic factors," Journal of Cerebral Blood Flow & Metabolism, vol. 27, no. 4, pp. 764-775, 2007.
90. T. Nishi, C. M. Maier, T. Hayashi, A. Saito, and P. H. Chan, "Superoxide dismutase 1 overexpression reduces MCP-1 and MIP-1αexpression after transient focal cerebral ischemia," Journal of Cerebral Blood Flow and Metabolism, vol. 25, no. 10, pp. 1312-1324, 2005.
91. M. H. Kim and H. J. Jeong, "Zinc oxide nanoparticles suppress LPS-induced NF-κB activation by Inducing A20, a negative regulator of NF-κB, in RAW 264. 7 macrophages," Journal of Nanoscience and Nanotechnology, vol. 15, no. 9, pp. 6509-6515, 2015.
92. C. J. Stork and Y. V. Li, "Elevated cytoplasmic free zinc and increased reactive oxygen species generation in the context of brain injury," Acta Neurochirurgica. Supplement, vol. 121, pp. 347-353, 2016.
93. W.-M. Wang, Z. Liu, A.-J. Liu et al., "The Zinc Ion chelating agent TPEN attenuates neuronal death/apoptosis caused by hypoxia/ischemia viamediating the pathophysiological cascade including excitotoxicity, oxidative stress, and inflammation," CNS Neuroscience and Therapeutics, vol. 21, no. 9, pp. 708-717, 2015.