Microglial regulation of cholinergic differentiation in the basal forebrain

Developmental Neurobiology

Volumn 72, Issue 6, 2012, Pages 857-864

  Jonakait, G Miller ^a   Pratt, Lorelei ^b   Acevedo, Giselles ^b   Ni, Li ^a  

^a NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Basal forebrain; Cholinergic; Cytokines; Growth factors; Microglia

Indexed keywords

ACETYLCHOLINESTERASE; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 9; CYTOKINE; INTERLEUKIN 6; MESSENGER RNA; NERVE GROWTH FACTOR; RECOMBINANT BRAIN DERIVED NEUROTROPHIC FACTOR; RECOMBINANT NERVE GROWTH FACTOR;

ANIMAL CELL; ARTICLE; AUTISM; BIOSYNTHESIS; CELL DIFFERENTIATION; CHO CELL; CHOLINERGIC NERVE CELL; CYTOKINE PRODUCTION; EMBRYO; ENZYME ACTIVITY; FOREBRAIN; IMMUNE SYSTEM; INFECTION; INFLAMMATION; MICROGLIA; NERVE CELL CULTURE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHIZOPHRENIA;

ANIMALS; CELL COUNT; CELL DIFFERENTIATION; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC NEURONS; INTERFERON-GAMMA; INTERLEUKIN-6; MICROGLIA; NERVE GROWTH FACTOR; PROSENCEPHALON; RATS;

EID: 84860898158     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20969     Document Type: Article

References (55)

1. Ashwell K. 1990. Microglia and cell death in the developing mouse cerebellum. Brain Res Dev Brain Res 55: 219-230.
2. Ashwell K. 1991. The distribution of microglia and cell death in the fetal rat forebrain. Dev Brain Res 68: 1-12.
3. Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Pessah I, Van de Water J. 2011. Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome. Brain Behav Immun 25: 40-45.
4. Bauman M, Kemper TL. 2005. Neuroanatomic observations of the brain in autism: A review and future directions. Int J Dev Neurosci 23: 183-187.
5. Beattie MS, Harrington AW, Lee R, Kim JY, Boyce SL, Longo FM, Bresnahan JC, et al. 2002. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36: 375-386.
6. Bell MJ, Hallenbeck JM. 2002. Effects of intrauterine inflammation on developing rat brain. J Neurosci Res 70: 570-579.
7. Cai Z, Pan ZL, Pang Y, Evans OB, Rhodes PG. 2000. Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr Res 47: 64-72.
8. Carson MJ, Thrash JC, Lo D. 2004. Analysis of microglial gene expression: Identifying targets for CNS neurodegenerative and autoimmune disease. Am J Pharmacogenomics 4: 321-330.
9. Cheepsunthorn P, Radov L, Menzies S, Reid J, Connor JR. 2001. Characterization of a novel brain-derived microglial cell line isolated from neonatal rat brain. Glia 35: 53-62.
10. Duncan JR, Cock ML, Scheerlinck JP, Westcott KT, McLean C, Harding R, et al. 2002. White matter injury after repeated endotoxin exposure in the preterm ovine fetus. Pediatr Res 52: 941-949.
11. 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.
12. Friedman WJ. 2000. Neurotrophins induce death of hippocampal neurons via the p75 receptor. J Neurosci 20: 6340-6346.
13. Gross RE, Mehler MF, Mabie PC, Zang Z, Santschi L, Kessler JA. 1996. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17: 595-606.
14. Hagberg H, Mallard C. 2005. Effect of inflammation on central nervous system development and vulnerability: Review. Curr Opin Neurol 18: 117-123.
15. Hallmayer J, Cleveland S, Torres A, Phillips J, Cohen B, Torigoe T, Miller J, et al. 2011. Genetic heritability and shared environmental factors among twin pairs with autism. Arch Gen Psychiatry doi:10.1001/archgenpsychiatry. 2011.76.
16. Harrington AW, Leiner B, Blechschmitt C, Arevalo JC, Lee R, Morl K, Meyer M, et al. 2004. Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc Natl Acad Sci USA 101: 6226-6230.
17. Heyen JR, Ye S, Finck BN, Johnson RW. 2000. Interleukin (IL)-10 inhibits IL-6 production in microglia by preventing activation of NF-kappa B. Brain Res Mol Brain Res 77: 138-147.
18. Hirasawa T, Ohsawa K, Imai Y, Ondo Y, Akazawa C, Uchino S, Kohsaka S. 2005. Visualization of microglia in living tissues using Iba1-EGFP transgenic mice. J Neurosci Res 81: 357-362.
19. Hohmann CF, Berger-Sweeney J. 1998. Cholinergic regulation of cortical development and plasticity. New twists to an old story. Perspect Dev Neurobiol 5: 401-425.
20. Hornig M, Weissenbock H, Horscroft N, Lipkin WI. 1999. An infection-based model of neurodevelopmental damage. Proc Natl Acad Sci USA 96: 12102-12107.
21. Jonakait GM. 2007. The effects of maternal inflammation on neuronal development: Possible mechanisms. Int J Dev Neurosci 25: 415-425.
22. Jonakait GM, Luskin MB, Ni L. 1998. Transforming growth factor-α expands progenitor cells of the basal forebrain, but does not promote cholinergic differentiation. J Neurobiol 37: 405-412.
23. Jonakait GM, Luskin MB, Wei R, Tian X-F, Ni L. 1996. Conditioned medium from activated microglia promotes cholinergic differentiation in the basal forebrain in vitro. Dev Biol 177: 85-95.
24. Jonakait GM, Wei R, Sheng Z-L, Hart RP, Li N. 1994. Interferon-γ promotes cholinergic differentiation of embryonic septal nuclei and adjacent basal forebrain. Neuron 12: 1149-1159.
25. Jonakait GM, Wen Y, Wan Y, Ni L. 2000. Macrophage cell-conditioned medium promotes cholinergic differentiation of undifferentiated progenitors and synergizes with nerve growth factor action in the developing basal forebrain. Exp Neurol 161: 285-296.
26. Jyonouchi H, Sun S, Le H. 2001. Proinflammatory and regulatory cytokine production associated with innate and adaptive immune responses in children with autism spectrum disorders and developmental regression. J Neuroimmunol 120: 170-179.
27. Lee R, Kermani P, Teng KK, Hempstead BL. 2001. Regulation of cell survival by secreted proneurotrophins. Science 294: 1945-1948.
28. Li W, Cogswell CA, LoTurco JJ. 1998. Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J Neurosci 18: 8853-8862.
29. Li X, Chauhan A, Sheikh AM, Patil S, Chauhan V, Li XM, Ji L, et al. 2009. Elevated immune response in the brain of autistic patients. J Neuroimmunol 207: 111-116.
30. Ling E-A, Wong W-C. 1993. The origin and nature of ramified and amoeboid microglia: A historical review and current concepts. Glia 7: 9-18.
31. Lopez-Coviella I, Berse B, Krauss R, Thies RS, Blusztajn JK. 2000. Induction and maintenance of the neuronal cholinergic phenotype in the central nervous system by BMP-9. Science 289: 313-316.
32. Mallat M, Houlgatte R, Brachet OP, Prochiantz A. 1989. Lipopolysaccharide-stimulated rat brain macrophages release NGF in vitro. Dev Biol 133: 309-311.
33. Marin-Teva JL, Dusart I, Colin C, Gervais A, van Rooijen N, Mallat M. 2004. Microglia promote the death of developing Purkinje cells. Neuron 41: 535-547.
34. Martinez HJ, Dreyfus CF, Jonakait GM, Black IB. 1987. Nerve growth factor selectively increases cholinergic markers but not neuropeptides in rat basal forebrain in culture. Brain Res 412: 295-301.
35. Mehler MF, Marmur R, Gross R, Mabie PC, Zang Z, Papavasiliou A, et al. 1995. Cytokines regulate the cellular phenotype of developing neural lineage species. Int J Dev Neurosci 13: 213-240.
36. Murphy GMJr, Song Y, Ong E, Lee YL, Schmidt KG, Bocchini V, Eng LF. 1995. Leukemia inhibitory factor mRNA is expressed in cortical astrocyte cultures but not in an immortalized microglial cell line. Neurosci Lett 184: 48-51.
37. Narita N, Kato M, Tazoe M, Miyazaki K, Narita M, Okado N. 2002. Increased monoamine concentration in the brain and blood of fetal thalidomide- and valproic acid-exposed rat: Putative animal models for autism. Pediatr Res 52: 576-579.
38. Navascues J, Calvente R, Marin-Teva JL, Cuadros MA. 2000. Entry, dispersion and differentiation of microglia in the developing central nervous system. An Acad Bras Cienc 72: 91-102.
39. Ni L, Acevedo G, Muralidharan B, Padala N, To J, Jonakait GM. 2007. Toll-like receptor ligands and CD154 stimulate microglia to produce a factor(s) that promotes excess cholinergic differentiation in the developing rat basal forebrain: implications for neurodevelopmental disorders. Pediatr Res 61: 15-20.
40. O'Keefe GM, Nguyen VT, Benveniste EN. 1999. Class II transactivator and class II MHC gene expression in microglia: Modulation by the cytokines TGF-beta, IL-4, IL-13 and IL-10. Eur J Immunol 29: 1275-1285.
41. Patterson PH. 2002. Maternal infection: Window on neuroimmune interactions in fetal brain development and mental illness. Curr Opin Neurobiol 12: 115-118.
42. Pedraza CE, Podlesniy P, Vidal N, Arevalo JC, Lee R, Hempstead B, Ferrer I, et al. 2005. Pro-NGF isolated from the human brain affected by Alzheimer's disease induces neuronal apoptosis mediated by p75NTR. Am J Pathol 166: 533-543.
43. Perry EK, Lee ML, Martin-Ruiz CM, Court JA, Volsen SG, Merrit J, Folly E, et al. 2001. Cholinergic activity in autism: Abnormalities in the cerebral cortex and basal forebrain. Am J Psychiatry 158: 1058-1066.
44. Rezaie P, Dean A, Male D, Ulfig N. 2005. Microglia in the cerebral wall of the human telencephalon at second trimester. Cereb Cortex 15: 938-949.
45. Sebire G, Emilie D, Wallon C, Hery C, Devergne O, Delfraissy JF, Galanaud P, et al. 1993. In vitro production of IL-6, IL-1 beta, and tumor necrosis factor-alpha by human embryonic microglial and neural cells. J Immunol 150: 1517-1523.
46. Smith SEP, Li J, Garbett K, Mirnics K, Patterson PH. 2007. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 27: 10695-10702.
47. Sweeten TL, Posey DJ, Shankar S, McDougle CJ. 2004. High nitric oxide production in autistic disorder: A possible role for interferon-gamma. Biol Psychiatry 55: 434-437.
48. Takahashi K, Yamamurra F, Naito M. 1989. Differentiation, maturation, and proliferation of macrophages in the mouse yolk sac: A light-microscopic, enzyme-cytochemical, immunohistochemical, and ultrastructural study. JLeukoc Biol 45: 87-96.
49. Temple S, Raff MC. 1985. Differentiation of a bipotential glial progenitor cell in a single cell microculture. Nature 313: 223-225.
50. Urakubo A, Jarskog LF, Lieberman JA, Gilmore JH. 2001. Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain. Schizophr Res 47: 27-36.
51. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA. 2005. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57: 67-81.
52. Volosin M, Song W, Almeida RD, Kaplan DR, Hempstead BL, Friedman WJ. 2006. Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. J Neurosci 26: 7756-7766.
53. Wei H, Zou H, Sheikh AM, Malik M, Dobkin C, Brown WT, Li X. 2011. IL-6 is increased in the cerebellum of autistic brain and alters neural cell adhesion, migration and synaptic formation. J Neuroinflammation 8: 52. [Epub ahead of print].
54. Woodroofe MN, Sarna GS, Wadhwa M, Hayes GM, Loughlin AJ, Tinker A, Cuzner ML. 1991. Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: Evidence of a role for microglia in cytokine production. J Neuroimmunol 33: 227-236.
55. Zuckerman L, Rehavi M, Nachman R, Weiner I. 2003. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: A novel neurodevelopmental model of schizophrenia. Neuropsychopharm 28: 1778-1789.