Effects of Microglia on Neurogenesis

GLIA

Volumn 63, Issue 8, 2015, Pages 1394-1405

  Sato, Kaoru ^a  

^a NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

Cytokine; Microglia; Neurogenesis; Subgranular zone; Subventricular zone

Indexed keywords

BRAIN REGION; CELL FUNCTION; EXPERIMENTAL DESIGN; HIPPOCAMPUS; HUMAN; LATERAL BRAIN VENTRICLE; MICROGLIA; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS; SUBVENTRICULAR ZONE; ANIMAL; BRAIN; GROWTH, DEVELOPMENT AND AGING; NEURAL STEM CELL; PHYSIOLOGY; STEM CELL NICHE;

ANIMALS; BRAIN; HUMANS; MICROGLIA; NEURAL STEM CELLS; NEUROGENESIS; STEM CELL NICHE;

EID: 84930870757     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22858     Document Type: Review

References (158)

1. Aarum J, Sandberg K, Haeberlein SL, Persson MA. 2003. Migration and differentiation of neural precursor cells can be directed by microglia. Proc Natl Acad Sci USA 100:15983-15988.
2. Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, Degen JL, Akassoglou K. 2007. The fibrin-derived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 204:571-582.
3. Aguilar-Valles A, Poole S, Mistry Y, Williams S, Luheshi GN. 2007. Attenuated fever in rats during late pregnancy is linked to suppressed interleukin-6 production after localized inflammation with turpentine. J Physiol 583:391-403.
4. Aimone JB, Wiles J, Gage FH. 2006. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9:723-727.
5. Aimone JB, Deng W, Gage FH. 2011. Resolving new memories: A critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70:589-596.
6. Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FM. 2011. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 14:1142-1149.
7. Arno B, Grassivaro F, Rossi C, Bergamaschi A, Castiglioni V, Furlan R, Greter M, Favaro R, Comi G, Becher B, Martino G, Muzio L, et al. 2014. Neural progenitor cells orchestrate microglia migration and positioning into the developing cortex. Nat Commun 5:5611.
8. Ashdown H, Poole S, Boksa P, Luheshi GN. 2007. Interleukin-1 receptor antagonist as a modulator of gender differences in the febrile response to lipopolysaccharide in rats. Am J Physiol Regul Integr Comp Physiol 292:R1667-R1674.
9. Bachstetter AD, Morganti JM, Jernberg J, Schlunk A, Mitchell SH, Brewster KW, Hudson CE, Cole MJ, Harrison JK, Bickford PC, et al. 2009. Fractalkine and CX 3 cr1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiol Aging 32:2030-2044.
10. Bao AM, Swaab DF. 2010. Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 16:550-565.
11. Barrientos SA, Martinez NW, Yoo S, Jara JS, Zamorano S, Hetz C, Twiss JL, Alvarez J, Court FA. 2011. Axonal degeneration is mediated by the mitochondrial permeability transition pore. J Neurosci 31:966-978.
12. Bechmann I, Galea I, Perry VH. 2007. What is the blood-brain barrier (not)? Trends Immunol 28:5-11.
13. Ben-Hur T, Ben-Menachem O, Furer V, Einstein O, Mizrachi-Kol R, Grigoriadis N. 2003. Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol Cell Neurosci 24:623-631.
14. Bernardino L, Agasse F, Silva B, Ferreira R, Grade S, Malva JO. 2008. Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells 26:2361-2371.
15. Bizon JL, Lee HJ, Gallagher M. 2004. Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 3:227-234.
16. Bonde S, Ekdahl CT, Lindvall O. 2006. Long-term neuronal replacement in adult rat hippocampus after status epilepticus despite chronic inflammation. Eur J Neurosci 23:965-974.
17. Bouchard-Cannon P, Mendoza-Viveros L, Yuen A, Kærn M, Cheng HY. 2013. The circadian molecular clock regulates adult hippocampal neurogenesis by controlling the timing of cell-cycle entry and exit. Cell Rep 5:961-973.
18. Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, Yang R, Lepier A, Gascon S, Erdelyi F, Szabo G, et al. 2009. Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12:1524-1533.
19. Burns CE, Traver D, Mayhall E, Shepard JL, Zon LI. 2005. Hematopoietic stem cell fate is established by the Notch-runx pathway. Genes Dev 19:2331-2342.
20. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, et al. 2014. Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat Neurosci 17:131-143.
21. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M. 2006. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149-160.
22. Cacci E, Ajmone-Cat MA, Anelli T, Biagioni S, Minghetti L. 2008. In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia 56:412-425.
23. Cao Q, Lu J, Kaur C, Sivakumar V, Li F, Cheah PS, Dheen ST, Ling EA. 2008. Expression of Notch-1 receptor and its ligands Jagged-1 and Delta-1 in amoeboid microglia in postnatal rat brain and murine BV-2 cells. Glia 56:1224-1237.
24. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, et al. 2006. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924.
25. Chan WY, Kohsaka S, Rezaie P. 2007. The origin and cell lineage of microglia: New concepts. Brain Res Rev 53:344-354.
26. Chapman GA, Moores K, Harrison D, Campbell CA, Stewart BR, Strijbos PJ. 2000. Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J Neurosci 20:RC87.
27. Chen SK, Tvrdik P, Peden E, Cho S, Wu S, Spangrude G, Capecchi MR. 2010. Hematopoietic origin of pathological grooming in hoxb8 mutant mice. Cell 141:775-785.
28. Chen Z, Palmer TD. 2013. Differential roles of tnfr1 and tnfr2 signaling in adult hippocampal neurogenesis. Brain Behav Immun 30:45-53.
29. Choi YS, Cho HY, Hoyt KR, Naegele JR, Obrietan K. 2008. IGF-1 receptor-mediated ERK/MAPK signaling couples status epilepticus to progenitor cell proliferation in the subgranular layer of the dentate gyrus. Glia 56:791-800.
30. Chrysis D, Calikoglu AS, Ye P, D'Ercole AJ. 2001. Insulin-like growth factor-I overexpression attenuates cerebellar apoptosis by altering the expression of bcl family proteins in a developmentally specific manner. J Neurosci 21:1481-1489.
31. Clark IA. 2007. The advent of the cytokine storm. Immunol Cell Biol 85:271-273.
32. Crain JM, Nikodemova M, Watters JJ. 2013. Microglia express distinct m1 and m2 phenotypic markers in the postnatal and adult central nervous system in male and female mice. J Neurosci Res 91:1143-1151.
33. Cunningham CL, Martinez-Cerdeno V, Noctor SC. 2013. Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J Neurosci 33:4216-4233.
34. Dahlstrand J, Lardelli M, Lendahl U. 1995. Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system. Brain Res Dev Brain Res 84:109-129.
35. Das S, Basu A. 2008. Inflammation: A new candidate in modulating adult neurogenesis. J Neurosci Res 86:1199-1208.
36. De S, Nagarajan N, Xu B, Peden E, Tbrdik P, Capecchi M. 2013. Hoxb8-positive microglia have distinct developmental and physiological properties. Sc. Neurosci., Abstract.
37. Diamond MC, Ingham CA, Johnson RE, Bennett EL, Rosenzweig MR. 1976. Effects of environment on morphology of rat cerebral cortex and hippocampus. J Neurobiol 7:75-85.
38. Dilger RN, Johnson RW. 2008. Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system. J Leukoc Biol 84:932-939.
39. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
40. Dorr A, Sled JG, Kabani N. 2007. Three-dimensional cerebral vasculature of the CBA mouse brain: A magnetic resonance imaging and micro computed tomography study. Neuroimage 35:1409-1423.
41. Dranovsky A, Picchini AM, Moadel T, Sisti AC, Yamada A, Kimura S, Leonardo ED, Hen R. 2011. Experience dictates stem cell fate in the adult hippocampus. Neuron 70:908-923.
42. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. 2003. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 100:14385-14390.
43. Durafourt BA, Moore CS, Zammit DA, Johnson TA, Zaguia F, Guiot MC, Bar-Or A, Antel JP. 2012. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia 60:717-727.
44. Eckenhoff MF, Rakic P. 1988. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci 8:2729-2747.
45. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O. 2003. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100:13632-13637.
46. Elkabes S, DiCicco-Bloom EM, Black IB. 1996. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16:2508-2521.
47. Erblich B, Zhu L, Etgen AM, Dobrenis K, Pollard JW. 2011. Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS One 6:e26317.
48. Gage FH, Kempermann G, Palmer TD, Peterson DA, Ray J. 1998. Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 36:249-266.
49. Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A. 1998. Architecture and cell types of the adult subventricular zone: In search of the stem cells. J Neurobiol 36:234-248.
50. Gebara E, Sultan S, Kocher-Braissant J, Toni N. 2013. Adult hippocampal neurogenesis inversely correlates with microglia in conditions of voluntary running and aging. Front Neurosci 7:145-
51. Geissmann F, Gordon S, Hume DA, Mowat AM, Randolph GJ. 2010. Unravelling mononuclear phagocyte heterogeneity. Nat Rev Immunol 10:453-460.
52. Gemma C, Bachstetter AD, Cole MJ, Fister M, Hudson C, Bickford PC. 2007. Blockade of caspase-1 increases neurogenesis in the aged hippocampus. Eur J Neurosci 26:2795-2803.
53. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, et al. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330:841-845.
54. Godbout JP, Chen J, Abraham J, Richwine AF, Berg BM, Kelley KW, Johnson RW. 2005. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J 19:1329-1331.
55. Goings GE, Kozlowski DA, Szele FG. 2006. Differential activation of microglia in neurogenic versus non-neurogenic regions of the forebrain. Glia 54:329-342.
56. Goldberg JS, Hirschi KK. 2009. Diverse roles of the vasculature within the neural stem cell niche. Regen Med 4:879-897.
57. Gonzalez-Perez O, Alvarez-Buylla A. 2011. Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res Rev 67:147-156.
58. Greter M, Lelios I, Pelczar P, Hoeffel G, Price J, Leboeuf M, Kundig TM, Frei K, Ginhoux F, Merad M, et al. 2012. Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity 37:1050-1060.
59. Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo PM, Gotz M. 2005. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8:865-872.
60. Hamilton JA. 2008. Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol 8:533-544.
61. Hanisch UK, Kettenmann H. 2007. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394.
62. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, McNamara RK, Streit WJ, Salafranca MN, Adhikari S, Thompson DA, et al. 1998. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci USA 95:10896-10901.
63. Hodge RD, D'Ercole AJ, O'Kusky JR. 2004. Insulin-like growth factor-I accelerates the cell cycle by decreasing g1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J Neurosci 24:10201-10210.
64. Ihrie RA, Alvarez-Buylla A. 2011. Lake-front property: A unique germinal niche by the lateral ventricles of the adult brain. Neuron 70:674-686.
65. Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S, Kokaia Z, Jacobsen SE, Lindvall O. 2006. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 26:9703-9712.
66. Islam O, Gong X, Rose-John S, Heese K. 2009. Interleukin-6 and neural stem cells: More than gliogenesis. Mol Biol Cell 20:188-199.
67. Jessberger S, Nakashima K, Clemenson GD Jr, Mejia E, Mathews E, Ure K, Ogawa S, Sinton CM, Gage FH, Hsieh J. 2007. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 27:5967-5975.
68. Kaplan MS, Hinds JW. 1977. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 197:1092-1094.
69. Kempermann G, Gast D, Gage FH. 2002. Neuroplasticity in old age: Sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135-143.
70. Kempermann G, Kuhn HG, Gage FH. 1998. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206-3212.
71. Kempermann G, Wiskott L, Gage FH. 2004. Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186-191.
72. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. 2011. Physiology of microglia. Physiol Rev 91:461-553.
73. Kohman RA, DeYoung EK, Bhattacharya TK, Lindsey N, Peterson LN, Rhodes JS. 2012. Wheel running attenuates microglia proliferation and increases expression of a proneurogenic phenotype in the hippocampus of aged mice. Brain Behav Immun 26:803-810.
74. Kohman RA, Rodriguez-Zas SL, Southey BR, Kelley KW, Dantzer R, Rhodes JS. 2011b. Voluntary wheel running reverses age-induced changes in hippocampal gene expression. PLoS One 6:e22654.
75. Kohman RA, Tarr AJ, Byler SL, Boehm GW. 2007. Age increases vulnerability to bacterial endotoxin-induced behavioral decrements. Physiol Behav 91:561-565.
76. Koo JW, Duman RS. 2008. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci USA 105:751-756.
77. Lawson LJ, Perry VH, Dri P, Gordon S. 1990. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39:151-170.
78. Lee B, Dziema H, Lee KH, Choi YS, Obrietan K. 2007. CRE-mediated transcription and COX-2 expression in the pilocarpine model of status epilepticus. Neurobiol Dis 25:80-91.
79. Li G, Fang L, Fernández G, Pleasure SJ. 2013. The ventral hippocampus is the embryonic origin for adult neural stem cells in the dentate gyrus. Neuron 78:658-672.
80. Li L, Walker TL, Zhang Y, Mackay EW, Bartlett PF. 2010. Endogenous interferon gamma directly regulates neural precursors in the non-inflammatory brain. J Neurosci 30:9038-9050.
81. Lie DC, Song H, Colamarino SA, Ming GL, Gage FH. 2004. Neurogenesis in the adult brain: New strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 44:399-421.
82. Lie DC, Colamarino SA, Song HJ, Désiré L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH. 2005. Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375.
83. Lin H, Lee E, Hestir K, Leo C, Huang M, Bosch E, Halenbeck R, Wu G, Zhou A, Behrens D, et al. 2008. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science 320:807-811.
84. Lledo PM, Alonso M, Grubb MS. 2006. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179-193.
85. Logan TT, Villapol S, Symes AJ. 2013. TGF-beta superfamily gene expression and induction of the runx1 transcription factor in adult neurogenic regions after brain injury. PLoS One 8:e59250-
86. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
87. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. 2002. Macrophage polarization: Tumor-associated macrophages as a paradigm for polarized m2 mononuclear phagocytes. Trends Immunol 23:549-555.
88. Marshall GP II, Deleyrolle LP, Reynolds BA, Steindler DA Laywell ED. 2014. Microglia from neurogenic and non-neurogenic regions display differential proliferative potential and neuroblast support. Front Cell Neurosci 8:180.
89. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. 2006. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26:7907-7918.
90. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. 2007. Mosaic organization of neural stem cells in the adult brain. Science 317:381-384.
91. Merrill DA, Karim R, Darraq M, Chiba AA, Tuszynski MH. 2003. Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J Comp Neurol 459:201-207.
92. Mesiano S, Welsh TN. 2007. Steroid hormone control of myometrial contractility and parturition. Semin Cell Dev Biol 18:321-331.
93. Miller JA, Nathanson J, Franjic D, Shim S, Dalley RA, Shapouri S, Smith KA, Sunkin SM, Bernard A, Bennett JL, Lee CK, Hawrylycz MJ, Jones AR, Amaral DG, Šestan N, Gage FH, Lein ES. 2013. Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates. Development 140:4633-4644.
94. Mills CD. 2012. M1 and M2 macrophages: Oracles of health and disease. Crit Rev Immunol 32:463-488.
95. Ming GL, Song H. 2011. Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron 70:687-702.
96. Monje ML, Toda H, Palmer TD. 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760-1765.
97. Mosher KI, Andres RH, Fukuhara T, Bieri G, Hasegawa-Moriyama M, He Y, Guzman R, Wyss-Coray T. 2012. Neural progenitor cells regulate microglia functions and activity. Nat Neurosci 15:1485-1487.
98. Nakahira E, Yuasa S. 2005. Neuronal generation, migration, and differentiation in the mouse hippocampal primoridium as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J Comp Neurol 483:329-340.
99. Neiva I, Malva JO, Valero J. 2014. Can we talk about microglia without neurons? A discussion of microglial cell autonomous properties in culture. Front Cell Neurosci 8:202.
100. Neumann H, Kotter MR, Franklin RJ. 2009. Debris clearance by microglia: An essential link between degeneration and regeneration. Brain 132:288-295.
101. Nunan R, Sivasathiaseelan H, Khan D, Zaben M, Gray W. 2014. Microglial VPAC1R mediates a novel mechanism of neuroimmune-modulation of hippocampal precursor cells via IL-4 release. Glia 62:1313-1327.
102. Olah M, Biber K, Vinet J, Boddeke HW. 2011. Microglia phenotype diversity. CNS Neurol Disord Drug Targets 10:108-118.
103. Olah M, Ping G, De Haas AH, Brouwer N, Meerlo P, Van Der Zee EA, Biber K, Boddeke HW. 2009. Enhanced hippocampal neurogenesis in the absence of microglia T cell interaction and microglia activation in the murine running wheel model. Glia 57:1046-1061.
104. Ortega F, Gascon S, Masserdotti G, Deshpande A, Simon C, Fischer J, Dimou L, Chichung Lie D, Schroeder T, Berninger B. 2013. Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to wnt signalling. Nat Cell Biol 15:602-613.
105. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, et al. 2011. Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456-1458.
106. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR III, Lafaille JJ, Hempstead BL, Littman DR Gan WB. 2013. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155:1596-1609.
107. Pelvig DP, Pakkenberg H, Stark AK, Pakkenberg B. 2008. Neocortical glial cell numbers in human brains. Neurobiol Aging 29:1754-1762.
108. Pervaiz N, Hoffman-Goetz L. 2011. Freewheel training alters mouse hippocampal cytokines. Int J Sports Med 32:889-895.
109. Pocock JM, Kettenmann H. 2007. Neurotransmitter receptors on microglia. Trends Neurosci 30:527-535.
110. Prinz M, Mildner A. 2011. Microglia in the CNS: Immigrants from another world. Glia 59:177-187.
111. Quaegebeur A, Lange C, Carmeliet P. 2011. The neurovascular link in health and disease: Molecular mechanisms and therapeutic implications. Neuron 71:406-424.
112. Ransohoff RM, Cardona AE. 2010. The myeloid cells of the central nervous system parenchyma. Nature 468:253-262.
113. Ransohoff RM, Perry VH. 2009. Microglial physiology: Unique stimuli, specialized responses. Annu Rev Immunol 27:119-145.
114. Rao MS, Hattiangady B, Shetty AK. 2006. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5:545-558.
115. Ravichandran KS. 2003. "recruitment signals" from apoptotic cells: Invitation to a quiet meal. Cell 113:817-820.
116. Ren L, Lubrich B, Biber K, Gebicke-Haerter PJ. 1999. Differential expression of inflammatory mediators in rat microglia cultured from different brain regions. Brain Res Mol Brain Res 65:198-205.
117. Reshef R, Kreisel T, Beroukhim Kay D, Yirmiya R. 2014. Microglia and their cx3cr1 signaling are involved in hippocampal- but not olfactory bulb-related memory and neurogenesis. Brain Behav Immun 41:239-250.
118. Rogers JT, Morganti JM, Bachstetter AD, Hudson CE, Peters MM, Grimmig BA, Weeber EJ, Bickford PC, Gemma C. 2011. Cx3cr1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J Neurosci 31:16241-16250.
119. Russo I, Barlati S, Bosetti F. 2011. Effects of neuroinflammation on the regenerative capacity of brain stem cells. J Neurochem 116:947-956.
120. Ryu JK, Davalos D, Akassoglou K. 2009. Fibrinogen signal transduction in the nervous system. J Thromb Haemost 7 Suppl 1:151-154.
121. Scheffel J, Regen T, Van Rossum D, Seifert S, Ribes S, Nau R, Parsa R, Harris RA, Boddeke HW, Chuang HN, et al. 2012. Toll-like receptor activation reveals developmental reorganization and unmasks responder subsets of microglia. Glia 60:1930-1943.
122. Schlegelmilch T, Henke K, Peri F. 2011. Microglia in the developing brain: From immunity to behaviour. Curr Opin Neurobiol 21:5-10.
123. Schmid CD, Melchior B, Masek K, Puntambekar SS, Danielson PE, Lo DD, Sutcliffe JG, Carson MJ. 2009. Differential gene expression in LPS/IFNgamma activated microglia and macrophages: In vitro versus in vivo. J Neurochem 109 Suppl 1:117-125.
124. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, et al. 2012. A lineage of myeloid cells independent of myb and hematopoietic stem cells. Science 336:86-90.
125. Schwarz JM, Bilbo SD. 2012. Sex, glia, and development: Interactions in health and disease. Horm Behav 62:243-253.
126. Schwarz JM, Sholar PW, Bilbo SD. 2011. Sex differences in microglial colonization of the developing rat brain. J Neurochem 120:948-963.
127. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S. 2004. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338-1340.
128. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S. 2008. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3:289-300.
129. Sheridan GK, Murphy KJ. 2013. Neuron-glia crosstalk in health and disease: Fractalkine and cx3cr1 take centre stage. Open Biol 3:130181-
130. Shigemoto-Mogami Y, Hoshikawa K, Goldman JE, Sekino Y, Sato K. 2014. Microglia enhance neurogenesis and oligodendrogenesis in the early postnatal subventricular zone. J Neurosci 34:2231-2243.
131. Sica A, Mantovani A. 2012. Macrophage plasticity and polarization: In vivo veritas. J Clin Invest 122:787-795.
132. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M. 2010. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483-495.
133. Sminia T, de Groot CJ, Dijkstra CD, Koetsier JC, Polman CH. 1987. Macrophages in the central nervous system of the rat. Immunobiology 174:43-50.
134. Smith PL, Hagberg H, Naylor AS, Mallard C. 2014. Neonatal peripheral immune challenge activates microglia and inhibits neurogenesis in the developing murine hippocampus. Dev Neurosci 36:119-131.
135. Spencer SJ, Mouihate A, Galic MA, Pittman QJ. 2008. Central and peripheral neuroimmune responses: Hyporesponsiveness during pregnancy. J Physiol 586:399-406.
136. Squarzoni P, Oller G, Hoeffel G, Pont-Lezica L, Rostaing P, Low D, Bessis A, Ginhoux F, Garel S. 2014. Microglia modulate wiring of the embryonic forebrain. Cell Rep 8:1271-1279.
137. Sultan S, Gebara E, Toni N. 2013. Doxycycline increases neurogenesis and reduces microglia in the adult hippocampus. Front Neurosci 7:131.
138. Taupin P, editor. 2008. Development of the hippocampus. New York: Nova Biomedical Books. p 93.
139. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F. 2008. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279-288.
140. Tong L, Shen H, Perreau VM, Balazs R, Cotman CW. 2001. Effects of exercise on gene-expression profile in the rat hippocampus. Neurobiol Dis 8:1046-1056.
141. Tropepe V, Craig CG, Morshead CM, van der Kooy D. 1997. Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 17:7850-7859.
142. Tyler WA, Haydar TF. 2013. Multiplex genetic fate mapping reveals a novel route of neocortical neurogenesis, which is altered in the Ts65Dn mouse model of down syndrome. J Neurosci 33:5106-5119.
143. Ueno M, Yamashita T. 2014. Bidirectional tuning of microglia in the developing brain: From neurogenesis to neural circuit formation. Curr Opin Neurobiol 27:8-15.
144. van Praag H, Kempermann G, Gage FH. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
145. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
146. van Praag H, Shubert T, Zhao C, Gage FH. 2005. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680-8685.
147. Varela-Nallar L, Inestrosa NC. 2013. Wnt signaling in the regulation of adult hippocampal neurogenesis. Front Cell Neurosci 7:100.
148. Vukovic J, Colditz MJ, Blackmore DG, Ruitenberg MJ, Bartlett PF. 2012. Microglia modulate hippocampal neural precursor activity in response to exercise and aging. J Neurosci 32:6435-6443.
149. Wakselman S, Bechade C, Roumier A, Bernard D, Triller A, Bessis A. 2008. Developmental neuronal death in hippocampus requires the microglial CD11b integrin and dap12 immunoreceptor. J Neurosci 28:8138-8143.
150. Walter J, Keiner S, Witte OW, Redecker C. 2011. Age-related effects on hippocampal precursor cell subpopulations and neurogenesis. Neurobiol Aging 32:1906-1914.
151. Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM, Marshall GP II, Scheffler B Steindler DA. 2006. Microglia instruct subventricular zone neurogenesis. Glia 54:815-825.
152. Wang X, Fu S, Wang Y, Yu P, Hu J, Gu W, Xu XM, Lu P. 2007. Interleukin-1beta mediates proliferation and differentiation of multipotent neural precursor cells through the activation of SAPK/JNK pathway. Mol Cell Neurosci 36:343-354.
153. Wei S, Nandi S, Chitu V, Yeung YG, Yu W, Huang M, Williams LT, Lin H, Stanley ER. 2010. Functional overlap but differential expression of CSF-1 and IL-34 in their CSF-1 receptor-mediated regulation of myeloid cells. J Leukoc Biol 88:495-505.
154. Williamson LL, Chao A, Bilbo SD. 2012. Environmental enrichment alters glial antigen expression and neuroimmune function in the adult rat hippocampus. Brain Behav Immun 26:500-510.
155. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M. 2006. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9:268-275.
156. Ziv Y, Schwartz M. 2008a. Immune-based regulation of adult neurogenesis: Implications for learning and memory. Brain Behav Immun 22:167-176.
157. Ziv Y, Schwartz M. 2008b. Orchestrating brain-cell renewal: The role of immune cells in adult neurogenesis in health and disease. Trends Mol Med 14:471-478.
158. Zusso M, Methot L, Lo R, Greenhalgh AD, David S, Stifani S. 2012. Regulation of postnatal forebrain amoeboid microglial cell proliferation and development by the transcription factor runx1. J Neurosci 32:11285-11298.