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BioMed Research International
Volume 2015 (2015), Article ID 102419, 15 pages
http://dx.doi.org/10.1155/2015/102419
Research Article

Astroglia-Microglia Cross Talk during Neurodegeneration in the Rat Hippocampus

1Unitat de Bioquímica i Biologia Molecular, Facultat de Medicina, Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona and Centro de Investigación Biomédica en Red Sobre Enfermedades Neurodegenerativas (CIBERNED), C/Casanova 143, 08036 Barcelona, Spain
2Istituto di Anatomia Umana e Biologia Cellulare, Facoltà di Medicina e Chirurgia, Università Cattolica del Sacro Cuore, 00168 Roma, Italy
3Vall d’Hebron Institute of Research (VHIR), Passeig de la Vall d’Hebron 119, 08035 Barcelona, Spain

Received 13 October 2014; Revised 16 January 2015; Accepted 9 March 2015

Academic Editor: Liliana Bernardino

Copyright © 2015 Montserrat Batlle 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. K. Helmut, U.-K. Hanisch, M. Noda, and A. Verkhratsky, “Physiology of microglia,” Physiological Reviews, vol. 91, no. 2, pp. 461–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. F. J. Ortega, J. M. Vidal-Taboada, N. Mahy, and M. J. Rodríguez, “Molecular mechanisms of acute brain injury and ensuing neurodegeneration,” in Brain Damage—Bridging between Basic Research and Clinics, A. González-Quevedo, Ed., pp. 163–186, InTech, Rijeka, Croatia, 2012. View at Google Scholar
  3. J. Gimeno-Bayón, A. López-López, M. J. Rodríguez, and N. Mahy, “Glucose pathways adaptation supports acquisition of activated microglia phenotype,” Journal of Neuroscience Research, vol. 92, no. 6, pp. 723–731, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. W.-S. Qu, D.-S. Tian, Z.-B. Guo et al., “Inhibition of EGFR/MAPK signaling reduces microglial inflammatory response and the associated secondary damage in rats after spinal cord injury,” Journal of Neuroinflammation, vol. 9, article 178, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Hellwig, A. Heinrich, and K. Biber, “The brain's best friend: microglial neurotoxicity revisited,” Frontiers in Cellular Neuroscience, vol. 7, article 71, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Prokop, K. R. Miller, and F. L. Heppner, “Microglia actions in Alzheimer's disease,” Acta Neuropathologica, vol. 126, no. 4, pp. 461–477, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. F. J. Ortega, J. Jolkkonen, N. Mahy, and M. J. Rodríguez, “Glibenclamide enhances neurogenesis and improves long-term functional recovery after transient focal cerebral ischemia,” Journal of Cerebral Blood Flow & Metabolism, vol. 33, no. 3, pp. 356–364, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Domercq, N. Vázquez-Villoldo, and C. Matute, “Neurotransmitter signaling in the pathophysiology of microglia,” Frontiers in Cellular Neuroscience, vol. 7, article 49, 2013. View at Publisher · View at Google Scholar
  9. S.-I. Hung, A. C. Chang, I. Kato, and N.-C. A. Chang, “Transient expression of Ym1, a heparin-binding lectin, during developmental hematopoiesis and inflammation,” Journal of Leukocyte Biology, vol. 72, no. 1, pp. 72–82, 2002. View at Google Scholar · View at Scopus
  10. G. Stoll, S. Jander, and M. Schroeter, “Detrimental and beneficial effects of injury-induced inflammation and cytokine expression in the nervous system,” Advances in Experimental Medicine and Biology, vol. 513, pp. 87–113, 2002. View at Google Scholar · View at Scopus
  11. B. Liao, W. Zhao, D. R. Beers, J. S. Henkel, and S. H. Appel, “Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS,” Experimental Neurology, vol. 237, no. 1, pp. 147–152, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. M. J. Rodríguez, M. Martínez-Moreno, F. J. Ortega, and N. Mahy, “Targeting microglial KATP channels to treat neurodegenerative diseases: a mitochondrial issue,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 194546, 13 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Tanuma, H. Sakuma, A. Sasaki, and Y. Matsumoto, “Chemokine expression by astrocytes plays a role in microglia/macrophage activation and subsequent neurodegeneration in secondary progressive multiple sclerosis,” Acta neuropathologica, vol. 112, no. 2, pp. 195–204, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. S. F. Sorrells and R. M. Sapolsky, “An inflammatory review of glucocorticoid actions in the CNS,” Brain, Behavior, and Immunity, vol. 21, no. 3, pp. 259–272, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Sierra, A. Gottfried-Blackmore, T. A. Milner, B. S. McEwen, and K. Bulloch, “Steroid hormone receptor expression and function in microglia,” Glia, vol. 56, no. 6, pp. 659–674, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. L. J. van Eldik and M. S. Wainwright, “The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain,” Restorative Neurology and Neuroscience, vol. 21, no. 3-4, pp. 97–108, 2003. View at Google Scholar · View at Scopus
  17. M. M. Edwards and S. R. Robinson, “TNF alpha affects the expression of GFAP and S100B: implications for Alzheimer's disease,” Journal of Neural Transmission, vol. 113, no. 11, pp. 1709–1715, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Reali, F. Scintu, R. Pillai, R. Donato, F. Michetti, and V. Sogos, “S100β counteracts effects of the neurotoxicant trimethyltin on astrocytes and microglia,” Journal of Neuroscience Research, vol. 81, no. 5, pp. 677–686, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Tramontina, A. C. Tramontina, D. F. Souza et al., “Glutamate uptake is stimulated by extracellular S100B in hippocampal astrocytes,” Cellular and Molecular Neurobiology, vol. 26, no. 1, pp. 81–86, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. V. Blais and S. Rivest, “Effects of TNF-α and IFN-γ on nitric oxide-induced neurotoxicity in the mouse brain,” Journal of Immunology, vol. 172, no. 11, pp. 7043–7052, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. G. J. Liu, R. J. Middleton, C. R. Hatty et al., “The 18 kDa translocator protein, microglia and neuroinflammation,” Brain Pathology, vol. 24, no. 6, pp. 631–653, 2014. View at Publisher · View at Google Scholar
  22. Q. X. Feng, W. Wang, X. Y. Feng et al., “Astrocytic activation in thoracic spinal cord contributes to persistent pain in rat model of chronic pancreatitis,” Neuroscience, vol. 167, no. 2, pp. 501–509, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. J. A. Filosa, M. T. Nelson, and L. V. G. Bosc, “Activity-dependent NFATc3 nuclear accumulation in pericytes from cortical parenchymal microvessels,” The American Journal of Physiology—Cell Physiology, vol. 293, no. 6, pp. C1797–C1805, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. M. J. Rodríguez, M. Martínez-Sánchez, F. Bernal, and N. Mahy, “Heterogeneity between hippocampal and septal astroglia as a contributing factor to differential in vivo AMPA excitotoxicity,” Journal of Neuroscience Research, vol. 77, no. 3, pp. 344–353, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. W. Wang, X. Mei, J. Huang et al., “Crosstalk between spinal astrocytes and neurons in nerve injury-induced neuropathic pain,” PLoS ONE, vol. 4, no. 9, Article ID e6973, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. R. J. Bridges, C. G. Hatalski, S. N. Shim et al., “Gliotoxic actions of excitatory amino acids,” Neuropharmacology, vol. 31, no. 9, pp. 899–907, 1992. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Sugawara, K. Torigoe, S. Okoyama, K. Negishi, and S. Kato, “Neurotoxic effects of l-α-aminoadipic acid on the carp retina: a long term observation,” Neuroscience, vol. 36, no. 1, pp. 155–163, 1990. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates, Academic Press, San Diego, Calif, USA, 1986.
  29. F. Bernal, J. Saura, J. Ojuel, and N. Mahy, “Differential vulnerability of hippocampus, basal ganglia, and prefrontal cortex to long-term NMDA excitotoxicity,” Experimental Neurology, vol. 161, no. 2, pp. 686–695, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. M. E. Dailey and M. Waite, “Confocal imaging of microglial cell dynamics in hippocampal slice cultures,” Methods: A Companion to Methods in Enzymology, vol. 18, no. 2, pp. 222–230, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. M. J. Rodríguez, J. Saura, C. C. Finch, N. Mahy, and E. E. Billett, “Localization of monoamine oxidase A and B in human pancreas, thyroid, and adrenal glands,” Journal of Histochemistry and Cytochemistry, vol. 48, no. 1, pp. 147–151, 2000. View at Google Scholar · View at Scopus
  32. M. J. Rodríguez, A. Prats, Y. Malpesa et al., “Pattern of injury with a graded excitotoxic insult and ensuing chronic medial septal damage in the rat brain,” Journal of Neurotrauma, vol. 26, no. 10, pp. 1823–1834, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. I. K. Hwang, Y.-B. Lee, K.-Y. Yoo et al., “Seizure-induced changes of mineralocorticoid and glucocorticoid receptors in the hippocampus in seizure sensitive gerbils,” Neuroscience Research, vol. 53, no. 1, pp. 14–24, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Andrés, A. Marino, J. M. Macarulla, and M. Trueba, “Characterization of specific corticosterone binding sites in adrenal cortex plasma membrane and their localization by autoradiographic studies,” Cellular and Molecular Life Sciences, vol. 53, no. 8, pp. 673–680, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. S. J. Bolton and V. H. Perry, “Differential blood–brain barrier breakdown and leucocyte recruitment following excitotoxic lesions in juvenile and adult rats,” Experimental Neurology, vol. 154, no. 1, pp. 231–240, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. N. Virgili, J. F. Espinosa-Parrilla, P. Mancera et al., “Oral administration of the KATP channel opener diazoxide ameliorates disease progression in a murine model of multiple sclerosis,” Journal of Neuroinflammation, vol. 8, article 149, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. N. Virgili, P. Mancera, C. Chanvillard et al., “Diazoxide attenuates autoimmune encephalomyelitis and modulates lymphocyte proliferation and dendritic cell functionality,” Journal of Neuroimmune Pharmacology, vol. 9, no. 4, pp. 558–568, 2014. View at Publisher · View at Google Scholar
  38. L. de Yebra, Y. Malpesa, G. Ursu et al., “Dissociation between hippocampal neuronal loss, astroglial and microglial reactivity after pharmacologically induced reverse glutamate transport,” Neurochemistry International, vol. 49, no. 7, pp. 691–697, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Giannetti, E. Moyse, A. Ducray et al., “Accumulation of Ym1/2 protein in the mouse olfactory epithelium during regeneration and aging,” Neuroscience, vol. 123, no. 4, pp. 907–917, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. M. V. Sofroniew and H. V. Vinters, “Astrocytes: biology and pathology,” Acta Neuropathologica, vol. 119, no. 1, pp. 7–35, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Suzumura, H. Takeuchi, G. Zhang, R. Kuno, and T. Mizuno, “Roles of glia-derived cytokines on neuronal degeneration and regeneration,” Annals of the New York Academy of Sciences, vol. 1088, pp. 219–229, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. V. Fontaine, S. Mohand-Said, N. Hanoteau, C. Fuchs, K. Pfizenmaier, and U. Eisel, “Neurodegenerative and neuroprotective effects of tumor Necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2,” The Journal of Neuroscience, vol. 22, no. 7, Article ID RC216, 2002. View at Google Scholar · View at Scopus
  43. L. Bernardino, F. Agasse, B. Silva, R. Ferreira, S. Grade, and J. O. Malva, “Tumor necrosis factor-α modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures,” Stem Cells, vol. 26, no. 9, pp. 2361–2371, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Rivest, “Molecular insights on the cerebral innate immune system,” Brain, Behavior, and Immunity, vol. 17, no. 1, pp. 13–19, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Bianchi, I. Giambanco, and R. Donato, “S100B/RAGE-dependent activation of microglia via NF-kappaB and AP-1. Co-regulation of COX-2 expression by S100B, IL-1beta and TNF-alpha,” Neurobiology of Aging, vol. 31, no. 4, pp. 665–677, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. F. J. Ortega, J. Gimeno-Bayon, J. F. Espinosa-Parrilla et al., “ATP-dependent potassium channel blockade strengthens microglial neuroprotection after hypoxia-ischemia in rats,” Experimental Neurology, vol. 235, no. 1, pp. 282–296, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Chrétien, A.-V. Vallat-Decouvelaere, C. Bossuet et al., “Expression of excitatory amino acid transporter-2 (EAAT-2) and glutamine synthetase (GS) in brain macrophages and microglia of SIVmac251-infected macaques,” Neuropathology & Applied Neurobiology, vol. 28, no. 5, pp. 410–417, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. F. K. H. van Landeghem, J. F. Stover, I. Bechmann et al., “Early expression of glutamate transporter proteins in ramified microglia after controlled cortical impact injury in the rat,” Glia, vol. 35, no. 3, pp. 167–179, 2001. View at Publisher · View at Google Scholar · View at Scopus