Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2014, Article ID 610343, 15 pages
http://dx.doi.org/10.1155/2014/610343
Review Article

Surveillance, Phagocytosis, and Inflammation: How Never-Resting Microglia Influence Adult Hippocampal Neurogenesis

1Ikerbasque Foundation, 48011 Bilbao, Spain
2Achucarro Basque Center for Neuroscience, Bizkaia Science and Technology Park, 48170 Zamudio, Spain
3Department of Neurosciences, University of the Basque Country, 48940 Leioa, Spain
4Centre de Recherche du CHU de Québec, Axe Neurosciences, Canada G1P 4C7
5Département de Médecine Moléculaire, Université Laval, Canada G1V 4G2

Received 10 December 2013; Accepted 11 February 2014; Published 19 March 2014

Academic Editor: Carlos Fitzsimons

Copyright © 2014 Amanda Sierra 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. P. Rezaie and D. Male, “Mesoglia and microglia—a historical review of the concept of mononuclear phagocytes within the central nervous system,” Journal of the History of the Neurosciences, vol. 11, no. 4, pp. 325–374, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. F. Ginhoux, S. Lim, G. Hoeffel, D. Low, and T. Huber, “Origin and differentiation of microglia,” Frontiers in Cellular Neuroscience, vol. 7, article 45, 2013. View at Publisher · View at Google Scholar
  3. E. Gomez Perdiguero, C. Schulz, and F. Geissmann, “Development and homeostasis of “resident” myeloid cells: the case of the microglia,” GLIA, vol. 61, no. 1, pp. 112–120, 2013. View at Publisher · View at Google Scholar
  4. H. Kettenmann, F. Kirchhoff, and A. Verkhratsky, “Microglia: new roles for the synaptic stripper,” Neuron, vol. 77, no. 1, pp. 10–18, 2013. View at Publisher · View at Google Scholar
  5. A. Aguzzi, B. A. Barres, and M. L. Bennett, “Microglia: scapegoat, saboteur, or something else?” Science, vol. 339, no. 6116, pp. 156–161, 2013. View at Publisher · View at Google Scholar
  6. 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
  7. M. È. Tremblay, B. Stevens, A. Sierra, H. Wake, A. Bessis, and A. Nimmerjahn, “The role of microglia in the healthy brain,” Journal of Neuroscience, vol. 31, no. 45, pp. 16064–16069, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Miyamoto, H. Wake, A. J. Moorhouse, and J. Nabekura, “Microglia and synapse interactions: fine tuaning neural circuits and candidate molecules,” Frontiers in Cellular Neuroscience, vol. 7, article 70, 2013. View at Publisher · View at Google Scholar
  9. C. Bechade, Y. Cantaut-Belarif, and A. Bessis, “Microglial control of neuronal activity,” Frontiers in Cellular Neuroscience, vol. 7, article 32, 2013. View at Publisher · View at Google Scholar
  10. A. Sierra, O. Abiega, A. Shahraz, and H. Neumann, “Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis,” Frontiers in Cellular Neuroscience, vol. 7, article 6, 2013. View at Publisher · View at Google Scholar
  11. 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
  12. J. M. Encinas, T. V. Michurina, N. Peunova et al., “Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus,” Cell Stem Cell, vol. 8, no. 5, pp. 566–579, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. 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
  14. J. J. Breunig, J. I. Arellano, J. D. Macklis, and P. Rakic, “Everything that glitters isn't gold: a critical review of postnatal neural precursor analyses,” Cell Stem Cell, vol. 1, no. 6, pp. 612–627, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. L. S. Overstreet-Wadiche and G. L. Westbrook, “Functional maturation of adult-generated granule cells,” Hippocampus, vol. 16, no. 3, pp. 208–215, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Ge, C. H. Yang, K. S. Hsu, G. L. Ming, and H. Song, “A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain,” Neuron, vol. 54, no. 4, pp. 559–566, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Bruel-Jungerman, C. Rampon, and S. Laroche, “Adult hippocampal neurogenesis, synaptic plasticity and memory: facts and hypotheses,” Reviews in the Neurosciences, vol. 18, no. 2, pp. 93–114, 2007. View at Google Scholar · View at Scopus
  18. K. Nakajima, S. Honda, Y. Tohyama, Y. Imai, S. Kohsaka, and T. Kurihara, “Neurotrophin secretion from cultured microglia,” Journal of Neuroscience Research, vol. 65, no. 4, pp. 322–331, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Krampert, S. R. Chirasani, F. P. Wachs et al., “Smad7 regulates the adult neural stem/progenitor cell pool in a transforming growth factor β- and bone morphogenetic protein-independent manner,” Molecular and Cellular Biology, vol. 30, no. 14, pp. 3685–3694, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. K. I. Mosher, R. H. Andres, T. Fukuhara et al., “Neural progenitor cells regulate microglia functions and activity,” Nature Neuroscience, vol. 15, no. 11, pp. 1485–1487, 2012. View at Publisher · View at Google Scholar
  21. V. Tropepe, M. Sibilia, B. G. Ciruna, J. Rossant, E. F. Wagner, and D. van der Kooy, “Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon,” Developmental Biology, vol. 208, no. 1, pp. 166–188, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. S. U. Kim and J. De Vellis, “Microglia in health and disease,” Journal of Neuroscience Research, vol. 81, no. 3, pp. 302–313, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. B. A. Reynolds and R. L. Rietze, “Neural stem cells and neurospheres—re-evaluating the relationship,” Nature Methods, vol. 2, no. 5, pp. 333–336, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Satake, Y. Matsuyama, M. Kamiya et al., “Up-regulation of glial cell line-derived neurotrophic factor (GDNF) following traumatic spinal cord injury,” NeuroReport, vol. 11, no. 17, pp. 3877–3881, 2000. View at Google Scholar · View at Scopus
  25. Y. M. Yoo, C. J. Lee, and Y. J. Kim, “Exogenous GDNF increases the migration of the neural stem cells with no protection against kainic acid-induced excitotoxic cell death in rats,” Brain Research, vol. 1486, pp. 27–38, 2012. View at Publisher · View at Google Scholar
  26. J. L. Trejo, E. Carro, and I. Torres-Alemán, “Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus,” Journal of Neuroscience, vol. 21, no. 5, pp. 1628–1634, 2001. View at Google Scholar · View at Scopus
  27. K. Striedinger and E. Scemes, “Interleukin-1β affects calcium signaling and in vitro cell migration of astrocyte progenitors,” Journal of Neuroimmunology, vol. 196, no. 1-2, pp. 116–123, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. B. Lee, A. Nagai, and S. U. Kim, “Cytokines, chemokines, and cytokine receptors in human microglia,” Journal of Neuroscience Research, vol. 69, no. 1, pp. 94–103, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Kempermann and H. Neumann, “Microglia: the enemy within?” Science, vol. 302, no. 5651, pp. 1689–1690, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. M. F. Mehler, R. Rozental, M. Dougherty, D. C. Spray, and J. A. Kessler, “Cytokine regulation of neuronal differentiation of hippocampal progenitor cells,” Nature, vol. 362, no. 6415, pp. 62–65, 1993. View at Publisher · View at Google Scholar · View at Scopus
  31. U. Gurok, C. Steinhoff, B. Lipkowitz, H. H. Ropers, C. Scharff, and U. A. Nuber, “Gene expression changes in the course of neural progenitor cell differentiation,” Journal of Neuroscience, vol. 24, no. 26, pp. 5982–6002, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. J. B. Demoulin, M. Enarsson, J. Larsson, A. Essaghir, C. H. Heldin, and K. Forsberg-Nilsson, “The gene expression profile of PDGF-treated neural stem cells corresponds to partially differentiated neurons and glia,” Growth Factors, vol. 24, no. 3, pp. 184–196, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. F. C. Mansergh, M. A. Wride, and D. E. Rancourt, “Neurons from stem cells: implications for understanding nervous system development and repair,” Biochemistry and Cell Biology, vol. 78, no. 5, pp. 613–628, 2000. View at Google Scholar · View at Scopus
  34. F. C. Alcantara Gomes, V. De Oliveira Sousa, and L. Romão, “Emerging roles for TGF-β1 in nervous system development,” International Journal of Developmental Neuroscience, vol. 23, no. 5, pp. 413–424, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Elkabes, E. M. DiCicco-Bloom, and I. B. Black, “Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function,” Journal of Neuroscience, vol. 16, no. 8, pp. 2508–2521, 1996. View at Google Scholar · View at Scopus
  36. U. K. Hanisch and H. Kettenmann, “Microglia: active sensor and versatile effector cells in the normal and pathologic brain,” Nature Neuroscience, vol. 10, no. 11, pp. 1387–1394, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. H. J. Klassen, T. F. Ng, Y. Kurimoto et al., “Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior,” Investigative Ophthalmology and Visual Science, vol. 45, no. 11, pp. 4167–4173, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. W. J. Streit, S. D. Hurley, T. S. McGraw, and S. L. Semple-Rowland, “Comparative evaluation of cytokine profiles and reactive gliosis supports a critical role for interleukin-6 in neuron-glia signaling during regeneration,” Journal of Neuroscience Research, vol. 61, no. 1, pp. 10–20, 2000. View at Google Scholar
  39. A. Suzumura, M. Sawada, H. Yamamoto, and T. Marunouchi, “Effects of colony stimulating factors on isolated microglia in vitro,” Journal of Neuroimmunology, vol. 30, no. 2-3, pp. 111–120, 1990. View at Google Scholar · View at Scopus
  40. Z. Lu, M. R. Elliott, Y. Chen et al., “Phagocytic activity of neuronal progenitors regulates adult neurogenesis,” Nature Cell Biology, vol. 13, no. 9, pp. 1076–1084, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Nakajima, Y. Kikuchi, E. Ikoma et al., “Neurotrophins regulate the function of cultured microglia,” GLIA, vol. 24, no. 3, pp. 272–289, 1998. View at Google Scholar
  42. P. A. Lodge and S. Sriram, “Regulation of microglial activation by TGF-β, IL-10, and CSF-1,” Journal of Leukocyte Biology, vol. 60, no. 4, pp. 502–508, 1996. View at Google Scholar · View at Scopus
  43. W. S. Sheng, S. Hu, F. H. Kravitz, P. K. Peterson, and C. C. Chao, “Tumor necrosis factor alpha upregulates human microglial cell production of interleukin-10 in vitro,” Clinical and Diagnostic Laboratory Immunology, vol. 2, no. 5, pp. 604–608, 1995. View at Google Scholar · View at Scopus
  44. G. L. Ming and H. Song, “Adult neurogenesis in the mammalian brain: significant answers and significant questions,” Neuron, vol. 70, no. 4, pp. 687–702, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Bruel-Jungerman, S. Davis, C. Rampon, and S. Laroche, “Long-term potentiation enhances neurogenesis in the adult dentate gyrus,” Journal of Neuroscience, vol. 26, no. 22, pp. 5888–5893, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Drapeau, M. F. Montaron, S. Aguerre, and D. N. Abrous, “Learning-induced survival of new neurons depends on the cognitive status of aged rats,” Journal of Neuroscience, vol. 27, no. 22, pp. 6037–6044, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Mouret, G. Gheusi, M. M. Gabellec, F. De Chaumont, J. C. Olivo-Marin, and P. M. Lledo, “Learning and survival of newly generated neurons: when time matters,” Journal of Neuroscience, vol. 28, no. 45, pp. 11511–11516, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Kee, C. M. Teixeira, A. H. Wang, and P. W. Frankland, “Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus,” Nature Neuroscience, vol. 10, no. 3, pp. 355–362, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Massa, M. Koelh, T. Wiesner et al., “Conditional reduction of adult neurogenesis impairs bidirectional hippocampal synaptic plasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 16, pp. 6644–6649, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. T. J. Shors, G. Miesegaes, A. Beylin, M. Zhao, T. Rydel, and E. Gould, “Neurogenesis in the adult is involved in the formation of trace memories,” Nature, vol. 410, no. 6826, pp. 372–376, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. W. Deng, M. D. Saxe, I. S. Gallina, and F. H. Gage, “Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain,” Journal of Neuroscience, vol. 29, no. 43, pp. 13532–13542, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Arruda-Carvalho, M. Sakaguchi, K. G. Akers, S. A. Josselyn, and P. W. Frankland, “Posttraining ablation of adult-generated neurons degrades previously acquired memories,” Journal of Neuroscience, vol. 31, no. 42, pp. 15113–15127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Sahay, K. N. Scobie, A. S. Hill et al., “Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation,” Nature, vol. 472, no. 7344, pp. 466–470, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. G. L. Ming and H. Song, “Adult neurogenesis in the mammalian central nervous system,” Annual Review of Neuroscience, vol. 28, pp. 223–250, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Newton and V. M. Dixit, “Signaling in innate immunity and inflammation,” Cold Spring Harbor Perspectives in Biology, vol. 4, no. 3, 2012. View at Publisher · View at Google Scholar
  56. H. K. Jeong, K. Ji, K. Min, and E. H. Joe, “Brain inflammation and microglia: facts and misconceptions,” Experimental Neurobiology, vol. 22, no. 2, pp. 59–67, 2013. View at Publisher · View at Google Scholar
  57. D. Stellwagen and R. C. Malenka, “Synaptic scaling mediated by glial TNF-α,” Nature, vol. 440, no. 7087, pp. 1054–1059, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Pickering, D. Cumiskey, and J. J. O'Connor, “Actions of TNF-α on glutamatergic synaptic transmission in the central nervous system,” Experimental Physiology, vol. 90, no. 5, pp. 663–670, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. K. Belarbi, T. Jopson, D. Tweedie et al., “TNF-α protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation,” Journal of Neuroinflammation, vol. 9, article 23, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. C. T. Ekdahl, J. H. Claasen, S. Bonde, Z. Kokaia, and O. Lindvall, “Inflammation is detrimental for neurogenesis in adult brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 23, pp. 13632–13637, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. M. L. Monje, H. Toda, and T. D. Palmer, “Inflammatory blockade restores adult hippocampal neurogenesis,” Science, vol. 302, no. 5651, pp. 1760–1765, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Sierra, J. M. Encinas, J. J. P. Deudero et al., “Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis,” Cell Stem Cell, vol. 7, no. 4, pp. 483–495, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Chugh, P. Nilsson, S. A. Afjei, A. Bakochi, and C. T. Ekdahl, “Brain inflammation induces post-synaptic changes during early synapse formation in adult-born hippocampal neurons,” Experimental Neurobiology, vol. 250, pp. 176–188, 2013. View at Publisher · View at Google Scholar
  64. K. Belarbi, C. Arellano, R. Ferguson, T. Jopson, and S. Rosi, “Chronic neuroinflammation impacts the recruitment of adult-born neurons into behaviorally relevant hippocampal networks,” Brain, Behavior, and Immunity, vol. 26, no. 1, pp. 18–23, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Johann, E. Kampmann, B. Denecke et al., “Expression of enzymes involved in the prostanoid metabolism by cortical astrocytes after LPS-induced inflammation,” Journal of Molecular Neuroscience, vol. 34, no. 2, pp. 177–185, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. P. V. B. Reddy, K. V. Rama Rao, and M. D. Norenberg, “Inhibitors of the mitochondrial permeability transition reduce ammonia-induced cell swelling in cultured astrocytes,” Journal of Neuroscience Research, vol. 87, no. 12, pp. 2677–2685, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Nie, H. Zhang, and H. R. Weng, “Minocycline prevents impaired glial glutamate uptake in the spinal sensory synapses of neuropathic rats,” Neuroscience, vol. 170, no. 3, pp. 901–912, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. F. Cerbai, D. Lana, D. Nosi et al., “The neuron-astrocyte-microglia triad in normal brain ageing and in a model of neuroinflammation in the rat hippocampus,” PLoS ONE, vol. 7, no. 9, Article ID e45250, 2012. View at Publisher · View at Google Scholar
  69. W. J. Jin, S. W. Feng, Z. Feng, S. M. Lu, T. Qi, and Y. N. Qian, “Minocycline improves postoperative cognitive impairment in aged mice by inhibiting astrocytic activation,” NeuroReport, 2013. View at Publisher · View at Google Scholar
  70. K. A. Ji, M. S. Yang, H. K. Jeong et al., “Resident microglia die and infiltrated neutrophils and monocytes become major inflammatory cells in lipopolysaccharide-injected brain,” GLIA, vol. 55, no. 15, pp. 1577–1588, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. N. J. van Wagoner, J. W. Oh, P. Repovic, and E. N. Benveniste, “Interleukin-6 (IL-6) production by astrocytes: autocrine regulation by IL-6 and the soluble IL-6 receptor,” Journal of Neuroscience, vol. 19, no. 13, pp. 5236–5244, 1999. View at Google Scholar · View at Scopus
  72. L. Valliéres, I. L. Campbell, F. H. Gage, and P. E. Sawchenko, “Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6,” Journal of Neuroscience, vol. 22, no. 2, pp. 486–492, 2002. View at Google Scholar · View at Scopus
  73. B. S. McEwen, “Physiology and neurobiology of stress and adaptation: central role of the brain,” Physiological Reviews, vol. 87, no. 3, pp. 873–904, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. V. Luine, M. Villegas, C. Martinez, and B. S. McEwen, “Repeated stress causes reversible impairments of spatial memory performance,” Brain Research, vol. 639, no. 1, pp. 167–170, 1994. View at Publisher · View at Google Scholar · View at Scopus
  75. 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
  76. S. Nadeau and S. Rivest, “Endotoxemia prevents the cerebral inflammatory wave induced by intraparenchymal lipopolysaccharide injection: role of glucocorticoids and CD14,” Journal of Immunology, vol. 169, no. 6, pp. 3370–3381, 2002. View at Google Scholar · View at Scopus
  77. 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
  78. C. Liston and W. B. Gan, “Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 38, pp. 16074–16079, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. C. Liston, J. M. Cichon, F. Jeanneteau, Z. Jia, M. V. Chao, and W. B. Gan, “Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance,” Nature Neuroscience, vol. 16, no. 6, pp. 698–705, 2013. View at Publisher · View at Google Scholar
  80. M. A. Carrillo-de Sauvage, L. Maatouk, I. Arnoux et al., “Potent and multiple regulatory actions of microglial glucocorticoid receptors during CNS inflammation,” Cell Death & Differentiation, vol. 20, no. 11, pp. 1546–1557, 2013. View at Publisher · View at Google Scholar
  81. S. F. Sorrells, J. R. Caso, C. D. Munhoz, and R. M. Sapolsky, “The stressed CNS: when glucocorticoids aggravate inflammation,” Neuron, vol. 64, no. 1, pp. 33–39, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. M. A. Bellavance and S. Rivest, “The neuroendocrine control of the innate immune system in health and brain diseases,” Immunological Reviews, vol. 248, no. 1, pp. 36–55, 2012. View at Publisher · View at Google Scholar
  83. R. J. Tynan, S. Naicker, M. Hinwood et al., “Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions,” Brain, Behavior, and Immunity, vol. 24, no. 7, pp. 1058–1068, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. E. S. Wohleb, N. D. Powell, J. P. Godbout, and J. F. Sheridan, “Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior,” The Journal of Neuroscience, vol. 33, no. 34, pp. 13820–13833, 2013. View at Publisher · View at Google Scholar
  85. Y. Diz-Chaves, M. Astiz, M. J. Bellini, and L. M. Garcia-Segura, “Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice,” Brain, Behavior, and Immunity, vol. 28, pp. 196–206, 2013. View at Publisher · View at Google Scholar
  86. E. S. Wohleb, A. M. Fenn, A. M. Pacenta, N. D. Powell, J. F. Sheridan, and J. P. Godbout, “Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice,” Psychoneuroendocrinology, vol. 37, no. 9, pp. 1491–1505, 2012. View at Publisher · View at Google Scholar · View at Scopus
  87. C. Mirescu and E. Gould, “Stress and adult neurogenesis,” Hippocampus, vol. 16, no. 3, pp. 233–238, 2006. View at Publisher · View at Google Scholar · View at Scopus
  88. J. L. Warner-Schmidt and R. S. Duman, “Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment,” Hippocampus, vol. 16, no. 3, pp. 239–249, 2006. View at Publisher · View at Google Scholar · View at Scopus
  89. N. D. Hanson, M. J. Owens, K. A. Boss-Williams, J. M. Weiss, and C. B. Nemeroff, “Several stressors fail to reduce adult hippocampal neurogenesis,” Psychoneuroendocrinology, vol. 36, no. 10, pp. 1520–1529, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. E. Gould, B. S. McEwen, P. Tanapat, L. A. M. Galea, and E. Fuchs, “Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation,” Journal of Neuroscience, vol. 17, no. 7, pp. 2492–2498, 1997. View at Google Scholar · View at Scopus
  91. J. W. Koo and R. S. Duman, “IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 2, pp. 751–756, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. D. C. Lagace, M. H. Donovan, N. A. Decarolis et al., “Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 9, pp. 4436–4441, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. G. Kronenberg, I. Kirste, D. Inta et al., “Reduced hippocampal neurogenesis in the GR+/- genetic mouse model of depression,” European Archives of Psychiatry and Clinical Neuroscience, vol. 259, no. 8, pp. 499–504, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. M. B. Howren, D. M. Lamkin, and J. Suls, “Associations of depression with c-reactive protein, IL-1, and IL-6: a meta-analysis,” Psychosomatic Medicine, vol. 71, no. 2, pp. 171–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. J. W. Koo, S. J. Russo, D. Ferguson, E. J. Nestler, and R. S. Duman, “Nuclear factor-κB is a critical mediator of stress-impaired neurogenesis and depressive behavior,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 6, pp. 2669–2674, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. I. Goshen, T. Kreisel, O. Ben-Menachem-Zidon et al., “Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression,” Molecular Psychiatry, vol. 13, no. 7, pp. 717–728, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. C. D. Munhoz, L. B. Lepsch, E. M. Kawamoto et al., “Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-κB in the frontal cortex and hippocampus via glucocorticoid secretion,” Journal of Neuroscience, vol. 26, no. 14, pp. 3813–3820, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. S. J. Sukoff Rizzo, S. J. Neal, Z. A. Hughes et al., “Evidence for sustained elevation of IL-6 in the CNS as a key contributor of depressive-like phenotypes,” Translational Psychiatry, vol. 2, article e199, 2012. View at Publisher · View at Google Scholar
  99. A. Garcia, B. Steiner, G. Kronenberg, A. Bick-Sander, and G. Kempermann, “Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus,” Aging Cell, vol. 3, no. 6, pp. 363–371, 2004. View at Publisher · View at Google Scholar · View at Scopus
  100. M. G. Frank, B. M. Thompson, L. R. Watkins, and S. F. Maier, “Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses,” Brain, Behavior, and Immunity, vol. 26, no. 2, pp. 337–345, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. S. Sugama, M. Fujita, M. Hashimoto, and B. Conti, “Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18,” Neuroscience, vol. 146, no. 3, pp. 1388–1399, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. A. Sierra, J. M. Encinas, and M. Maletic-Savatic, “Adult human neurogenesis: from microscopy to magnetic resonance imaging,” Frontiers in Neuroscience, vol. 5, article 47, 2011. View at Google Scholar
  103. 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,” Journal of Neuroscience, vol. 16, no. 6, pp. 2027–2033, 1996. View at Google Scholar · View at Scopus
  104. L. N. Manganas, X. Zhang, Y. Li et al., “Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain,” Science, vol. 318, no. 5852, pp. 980–985, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. K. L. Spalding, O. Bergmann, K. Alkass et al., “Dynamics of hippocampal neurogenesis in adult humans,” Cell, vol. 153, no. 6, pp. 1219–1227, 2013. View at Publisher · View at Google Scholar
  106. J. M. Encinas and A. Sierra, “Neural stem cell deforestation as the main force driving the age-related decline in adult hippocampal neurogenesis,” Behavioural Brain Research, vol. 227, no. 2, pp. 433–439, 2012. View at Publisher · View at Google Scholar · View at Scopus
  107. K. S. Krabbe, M. Pedersen, and H. Bruunsgaard, “Inflammatory mediators in the elderly,” Experimental Gerontology, vol. 39, no. 5, pp. 687–699, 2004. View at Publisher · View at Google Scholar · View at Scopus
  108. B. S. Diniz, A. L. Teixeira, L. Talib, W. F. Gattaz, and O. V. Forlenza, “Interleukin-1β serum levels is increased in antidepressant-free elderly depressed patients,” American Journal of Geriatric Psychiatry, vol. 18, no. 2, pp. 172–176, 2010. View at Publisher · View at Google Scholar · View at Scopus
  109. A. Sierra, A. C. Gottfried-Blackmore, B. S. Mcewen, and K. Bulloch, “Microglia derived from aging mice exhibit an altered inflammatory profile,” GLIA, vol. 55, no. 4, pp. 412–424, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. C. Franceschi, M. Bonafè, S. Valensin et al., “Inflamm-aging. An evolutionary perspective on immunosenescence,” Annals of the New York Academy of Sciences, vol. 908, pp. 244–254, 2000. View at Google Scholar · View at Scopus
  111. R. Sano and J. C. Reed, “ER stress-induced cell death mechanisms,” Biochimica et Biophysica Acta, vol. 1833, no. 12, pp. 3460–3470, 2013. View at Google Scholar
  112. S. Z. Hasnain, R. Lourie, I. Das, A. C. H. Chen, and M. A. McGuckin, “The interplay between endoplasmic reticulum stress and inflammation,” Immunology and Cell Biology, vol. 90, no. 3, pp. 260–270, 2012. View at Publisher · View at Google Scholar · View at Scopus
  113. S. Matus, L. H. Glimcher, and C. Hetz, “Protein folding stress in neurodegenerative diseases: a glimpse into the ER,” Current Opinion in Cell Biology, vol. 23, no. 2, pp. 239–252, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. Y. Ito, M. Yamada, H. Tanaka et al., “Involvement of CHOP, an ER-stress apoptotic mediator, in both human sporadic ALS and ALS model mice,” Neurobiology of Disease, vol. 36, no. 3, pp. 470–476, 2009. View at Publisher · View at Google Scholar · View at Scopus
  115. D. Papadimitriou, V. Le Verche, A. Jacquier, B. Ikiz, S. Przedborski, and D. B. Re, “Inflammation in ALS and SMA: sorting out the good from the evil,” Neurobiology of Disease, vol. 37, no. 3, pp. 493–502, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. A. R. Johnson, J. J. Milner, and L. Makowski, “The inflammation highway: metabolism accelerates inflammatory traffic in obesity,” Immunological Reviews, vol. 249, no. 1, pp. 218–238, 2012. View at Google Scholar
  117. S. Buch, H. Yao, M. Guo et al., “Cocaine and HIV-1 interplay in CNS: cellular and molecular mechanisms,” Current HIV Research, vol. 10, no. 5, pp. 425–428, 2012. View at Google Scholar
  118. M. K. Brown and N. Naidoo, “The endoplasmic reticulum stress response in aging and age-related diseases,” Frontiers in Physiology, vol. 3, article 263, 2012. View at Google Scholar
  119. G. Castro, C. Areias MF, L. Weissmann et al., “Diet-induced obesity induces endoplasmic reticulum stress and insulin resistance in the amygdala of rats,” FEBS Open Bio, vol. 3, pp. 443–449, 2013. View at Publisher · View at Google Scholar
  120. A. A. Pavlovsky, D. Boehning, D. Li, Y. Zhang, X. Fan, and T. A. Green, “Psychological stress, cocaine and natural reward each induce endoplasmic reticulum stress genes in rat brain,” Neuroscience, vol. 246, pp. 160–169, 2013. View at Publisher · View at Google Scholar
  121. G. Gargiulo, M. Cesaroni, M. Serresi et al., “In vivo RNAi screen for BMI1 targets identifies TGF-beta/BMP-ER stress pathways as key regulators of neural- and malignant glioma-stem cell homeostasis,” Cancer Cell, vol. 23, no. 5, pp. 660–676, 2013. View at Publisher · View at Google Scholar
  122. A. Salminen, K. Kaarniranta, and A. Kauppinen, “Inflammaging: disturbed interplay between autophagy and inflammasomes,” Aging, vol. 4, no. 3, pp. 166–175, 2012. View at Google Scholar
  123. E. Latz, T. S. Xiao, and A. Stutz, “Activation and regulation of the inflammasomes,” Nature Reviews Immunology, vol. 13, no. 6, pp. 397–411, 2013. View at Publisher · View at Google Scholar
  124. C. Gemma, A. D. Bachstetter, M. J. Cole, M. Fister, C. Hudson, and P. C. Bickford, “Blockade of caspase-1 increases neurogenesis in the aged hippocampus,” European Journal of Neuroscience, vol. 26, no. 10, pp. 2795–2803, 2007. View at Publisher · View at Google Scholar · View at Scopus
  125. M. D. Wu, A. M. Hein, M. J. Moravan, S. S. Shaftel, J. A. Olschowka, and M. K. O'Banion, “Adult murine hippocampal neurogenesis is inhibited by sustained IL-1β and not rescued by voluntary running,” Brain, Behavior, and Immunity, vol. 26, no. 2, pp. 292–300, 2012. View at Publisher · View at Google Scholar · View at Scopus
  126. Y. Wolf, S. Yona, K. W. Kim, and S. Jung, “Microglia, seen from the CX3CR1 angle,” Frontiers in Cellular Neuroscience, vol. 7, article 26, 2013. View at Publisher · View at Google Scholar
  127. A. E. Cardona, E. P. Pioro, M. E. Sasse et al., “Control of microglial neurotoxicity by the fractalkine receptor,” Nature Neuroscience, vol. 9, no. 7, pp. 917–924, 2006. View at Publisher · View at Google Scholar · View at Scopus
  128. K. Bhaskar, M. Konerth, O. N. Kokiko-Cochran, A. Cardona, R. M. Ransohoff, and B. T. Lamb, “Regulation of tau pathology by the microglial fractalkine receptor,” Neuron, vol. 68, no. 1, pp. 19–31, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. A. D. Bachstetter, J. M. Morganti, J. Jernberg et al., “Fractalkine and CX3CR1 regulate hippocampal neurogenesis in adult and aged rats,” Neurobiology of Aging, vol. 32, no. 11, pp. 2030–2044, 2011. View at Publisher · View at Google Scholar · View at Scopus
  130. S. Jung, J. Aliberti, P. Graemmel et al., “Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion,” Molecular and Cellular Biology, vol. 20, no. 11, pp. 4106–4114, 2000. View at Publisher · View at Google Scholar · View at Scopus
  131. J. T. Rogers, J. M. Morganti, A. D. Bachstetter et al., “CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity,” Journal of Neuroscience, vol. 31, no. 45, pp. 16241–16250, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. W. S. T. Griffin, L. C. Stanley, C. Ling et al., “Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 19, pp. 7611–7615, 1989. View at Google Scholar · View at Scopus
  133. W. C. Benzing, J. R. Wujek, E. K. Ward et al., “Evidence for glial-mediated inflammation in aged APP(SW) transgenic mice,” Neurobiology of Aging, vol. 20, no. 6, pp. 581–589, 1999. View at Publisher · View at Google Scholar · View at Scopus
  134. T. J. Seabrook, L. Jiang, M. Maier, and C. A. Lemere, “Minocycline affects microglia activation, Aβ deposition, and behavior in APP-tg mice,” GLIA, vol. 53, no. 7, pp. 776–782, 2006. View at Publisher · View at Google Scholar · View at Scopus
  135. B. Biscaro, O. Lindvall, G. Tesco, C. T. Ekdahl, and R. M. Nitsch, “Inhibition of microglial activation protects hippocampal neurogenesis and improves cognitive deficits in a transgenic mouse model for Alzheimer's disease,” Neurodegenerative Diseases, vol. 9, no. 4, pp. 187–198, 2012. View at Publisher · View at Google Scholar
  136. P. A. Zunszain, C. Anacker, A. Cattaneo et al., “Interleukin-1β: a new regulator of the kynurenine pathway affecting human hippocampal neurogenesis,” Neuropsychopharmacology, vol. 37, no. 4, pp. 939–949, 2012. View at Publisher · View at Google Scholar · View at Scopus
  137. R. De Simone, M. Antonietta Ajmone-Cat, P. Tirassa, and L. Minghetti, “Apoptotic PC12 cells exposing phosphatidylserine promote the production of anti-inflammatory and neuroprotective molecules by microglial cells,” Journal of Neuropathology and Experimental Neurology, vol. 62, no. 2, pp. 208–216, 2003. View at Google Scholar · View at Scopus
  138. M. S. Buckwalter, M. Yamane, B. S. Coleman et al., “Chronically increased transforming growth factor-β1 strongly inhibits hippocampal neurogenesis in aged mice,” American Journal of Pathology, vol. 169, no. 1, pp. 154–164, 2006. View at Publisher · View at Google Scholar · View at Scopus
  139. O. Butovsky, Y. Ziv, A. Schwartz et al., “Microglia activated by IL-4 or IFN-γ differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells,” Molecular and Cellular Neuroscience, vol. 31, no. 1, pp. 149–160, 2006. View at Publisher · View at Google Scholar · View at Scopus
  140. C. T. Ekdahl, “Microglial activation—tuning and pruning adult neurogenesis,” Frontiers in Pharmacology, vol. 3, article 41, 2012. View at Google Scholar
  141. H. Wake, A. J. Moorhouse, S. Jinno, S. Kohsaka, and J. Nabekura, “Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals,” Journal of Neuroscience, vol. 29, no. 13, pp. 3974–3980, 2009. View at Publisher · View at Google Scholar · View at Scopus
  142. M. È. Tremblay, R. L. Lowery, and A. K. Majewska, “Microglial interactions with synapses are modulated by visual experience,” PLoS Biology, vol. 8, no. 11, Article ID e1000527, 2010. View at Publisher · View at Google Scholar · View at Scopus
  143. M. È. Tremblay, M. L. Zettel, J. R. Ison, P. D. Allen, and A. K. Majewska, “Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices,” GLIA, vol. 60, no. 4, pp. 541–558, 2012. View at Publisher · View at Google Scholar · View at Scopus
  144. D. P. Schafer, E. K. Lehrman, A. G. Kautzman et al., “Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner,” Neuron, vol. 74, no. 4, pp. 691–705, 2012. View at Publisher · View at Google Scholar
  145. H. Nakanishi, “Microglial functions and proteases,” Molecular Neurobiology, vol. 27, no. 2, pp. 163–176, 2003. View at Publisher · View at Google Scholar · View at Scopus
  146. M. È. Tremblay and A. K. Majewska, “A role for microglia in synaptic plasticity?” Communicative and Integrative Biology, vol. 4, no. 2, pp. 220–222, 2011. View at Publisher · View at Google Scholar · View at Scopus
  147. R. C. Paolicelli, G. Bolasco, F. Pagani et al., “Synaptic pruning by microglia is necessary for normal brain development,” Science, vol. 333, no. 6048, pp. 1456–1458, 2011. View at Publisher · View at Google Scholar · View at Scopus
  148. G. Kempermann, H. G. Kuhn, and F. H. Gage, “More hippocampal neurons in adult mice living in an enriched environment,” Nature, vol. 386, no. 6624, pp. 493–495, 1997. View at Publisher · View at Google Scholar · View at Scopus
  149. M. Nilsson, E. Perfilieva, U. Johansson, O. Orwar, and P. S. Eriksson, “Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory,” Journal of Neurobiology, vol. 39, no. 4, pp. 569–578, 1999. View at Google Scholar
  150. H. van Praag, G. Kempermann, and F. H. Gage, “Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus,” Nature Neuroscience, vol. 2, no. 3, pp. 266–270, 1999. View at Publisher · View at Google Scholar · View at Scopus
  151. D. Young, P. A. Lawlor, P. Leone, M. Dragunow, and M. J. During, “Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective,” Nature Medicine, vol. 5, no. 4, pp. 448–453, 1999. View at Publisher · View at Google Scholar · View at Scopus
  152. L. L. Williamson, A. Chao, and S. D. Bilbo, “Environmental enrichment alters glial antigen expression and neuroimmune function in the adult rat hippocampus,” Brain, Behavior, and Immunity, vol. 26, no. 3, pp. 500–510, 2012. View at Publisher · View at Google Scholar · View at Scopus
  153. L. Maggi, M. Scianni, I. Branchi, I. D'Andrea, C. Lauro, and C. Limatola, “CX(3)CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment,” Frontiers in Cellular Neuroscience, vol. 5, article 22, 2011. View at Publisher · View at Google Scholar
  154. I. Goshen, A. Avital, T. Kreisel, T. Licht, M. Segal, and R. Yirmiya, “Environmental enrichment restores memory functioning in mice with impaired IL-1 signaling via reinstatement of long-term potentiation and spine size enlargement,” Journal of Neuroscience, vol. 29, no. 11, pp. 3395–3403, 2009. View at Publisher · View at Google Scholar · View at Scopus
  155. Y. Ziv, N. Ron, O. Butovsky et al., “Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood,” Nature Neuroscience, vol. 9, no. 2, pp. 268–275, 2006. View at Publisher · View at Google Scholar · View at Scopus
  156. J. Kipnis, H. Cohen, M. Cardon, Y. Ziv, and M. Schwartz, “T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 21, pp. 8180–8185, 2004. View at Publisher · View at Google Scholar · View at Scopus
  157. S. A. Wolf, B. Steiner, A. Akpinarli et al., “CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis,” Journal of Immunology, vol. 182, no. 7, pp. 3979–3984, 2009. View at Publisher · View at Google Scholar · View at Scopus
  158. G. J. Huang, A. L. Smith, D. H. D. Gray et al., “A genetic and functional relationship between T cells and cellular proliferation in the adult hippocampus,” PLOS Biology, vol. 8, no. 12, Article ID e1000561, 2010. View at Publisher · View at Google Scholar
  159. R. M. Ransohoff and B. Engelhardt, “The anatomical and cellular basis of immune surveillance in the central nervous system,” Nature Reviews Immunology, vol. 12, no. 9, pp. 623–635, 2012. View at Publisher · View at Google Scholar
  160. M. Olah, G. Ping, A. H. De Haas et al., “Enhanced hippocampal neurogenesis in the absence of microglia T cell interaction and microglia activation in the murine running wheel model,” GLIA, vol. 57, no. 10, pp. 1046–1061, 2009. View at Publisher · View at Google Scholar · View at Scopus
  161. E. Gebara, S. Sultan, J. Kocher-Braissant, and N. Toni, “Adult hippocampal neurogenesis inversely correlates with microglia in conditions of voluntary running and aging,” Frontiers in Neuroscience, vol. 7, article 145, 2013. View at Publisher · View at Google Scholar
  162. R. Aharoni, B. Kayhan, R. Eilam, M. Sela, and R. Arnon, “Glatiramer acetate-specific T cells in the brain express T helper 2/3 cytokines and brain-derived neurotrophic factor in situ,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 14157–14162, 2003. View at Publisher · View at Google Scholar · View at Scopus
  163. C. Rossi, A. Angelucci, L. Costantin et al., “Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment,” European Journal of Neuroscience, vol. 24, no. 7, pp. 1850–1856, 2006. View at Publisher · View at Google Scholar · View at Scopus