Sex differences in microglial colonization of the developing rat brain

Journal of Neurochemistry

Volumn 120, Issue 6, 2012, Pages 948-963

  Schwarz, Jaclyn M ^a   Sholar, Paige W ^a   Bilbo, Staci D ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Chemokines; Cytokines; Female; Glia; Male

Indexed keywords

CHEMOKINE; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 1BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; BRAIN SIZE; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; STEREOLOGY;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN; CALCIUM-BINDING PROTEINS; CELL COUNT; CHEMOKINE CXCL9; EMBRYO, MAMMALIAN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERLEUKIN-10; INTERLEUKIN-1BETA; MALE; MICROFILAMENT PROTEINS; MICROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SEX CHARACTERISTICS;

RATTUS;

EID: 84857917135     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07630.x     Document Type: Article

References (56)

1. Adler M. W., Geller E. B., Chen X. and Rogers T. J. (2006) Viewing chemokines as a third major system of communication in the brain. AAPS J. 7, E865-E870.
2. Arias C., Zepeda A., Hernandez-Ortega K., Leal-Galicia P., Lojero C. and Camacho-Arroyo I. (2009) Sex and estrous cycle-dependent differences in glial fibrillary acidic protein immunoreactivity in the adult rat hippocampus. Horm. Behav. 55, 257-263.
3. Arnold A. P., Xu J., Grisham W., Chen X., Kim Y. H. and Itoh Y. (2004) Minireview: sex chromosomes and brain sexual differentiation. Endocrinology 145, 1057-1062. (Pubitemid 38280982)
4. Ashwell K. (1990) Microglia and cell death in the developing mouse cerebellum. Brain Res. Dev. Brain Res. 55, 219-230.
5. Ashwell K. (1991) The distribution of microglia and cell death in the fetal rat forebrain. Brain Res. Dev. Brain Res. 58, 1-12.
6. Baker A. E., Brautigam V. M. and Watters J. J. (2004) Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor beta. Endocrinology 145, 5021-5032. (Pubitemid 39551121)
7. Bao A. M. and Swaab D. F. (2010) Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 16, 550-565.
8. Bilbo S. D., Levkoff L. H., Mahoney J. H., Watkins L. R., Rudy J. W. and Maier S. F. (2005) Neonatal infection induces memory impairments following an immune challenge in adulthood. Behav. Neurosci. 119, 293-301. (Pubitemid 40279518)
9. Bilbo S. D., Rudy J. W., Watkins L. R. and Maier S. F. (2006) A behavioural characterization of neonatal infection-facilitated memory impairment in adult rats. Behav. Brain Res. 169, 39-47. (Pubitemid 43277469)
10. Bilbo S. D., Barrientos R. M., Eads A. S., Northcutt A., Watkins L. R., Rudy J. W. and Maier S. F. (2008) Early-life infection leads to altered BDNF and IL-1beta mRNA expression in rat hippocampus following learning in adulthood. Brain Behav. Immun. 22, 451-455. (Pubitemid 351451825)
11. Bilbo S. D., Wieseler J. L., Barrientos R. M., Tsang V., Watkins L. R. and Maier S. F. (2010) Neonatal bacterial infection alters fever to live and simulated infections in adulthood. Psychoneuroendocrinology 35, 369-381.
12. Bilbo S. D., Smith S. H. and Schwarz J. M. (2011) A Lifespan Approach to Neuroinflammatory and Cognitive Disorders: A Critical Role for Glia. J. Neuroimmune Pharmacol. PMID: 21822589. [Epub ahead of print].
13. Boulanger L. M. (2009) Immune proteins in brain development and synaptic plasticity. Neuron 64, 93-109.
14. Cowell R. M. and Silverstein F. S. (2003) Developmental changes in the expression of chemokine receptor CCR1 in the rat cerebellum. J. Comp. Neurol. 457, 7-23. (Pubitemid 36172569)
15. Cowell R. M., Xu H., Parent J. M. and Silverstein F. S. (2006) Microglial expression of chemokine receptor CCR5 during rat forebrain development and after perinatal hypoxia-ischemia. J. Neuroimmunol. 173, 155-165.
16. Cross A. K. and Woodroofe M. N. (1999) Chemokines induce migration and changes in actin polymerization in adult rat brain microglia and a human fetal microglial cell line in vitro. J. Neurosci. Res. 55, 17-23. (Pubitemid 29014407)
17. Cuadros M. A. and Navascués J. (1998) The origin and differentiation of microglial cells during development. Prog. Neurobiol. 56, 173-189. (Pubitemid 28432564)
18. Deverman B. E. and Patterson P. H. (2009) Cytokines and CNS development. Neuron 64, 61-78.
19. Drew P. D. and Chavis J. A. (2000) Female sex steroids: effects upon microglial cell activation. J. Neuroimmunol. 111, 77-85.
20. Drew P. D., Chavis J. A. and Bhatt R. (2003) Sex steroid regulation of microglial cell activation: relevance to multiple sclerosis. Ann. N Y Acad. Sci. 1007, 329-334. (Pubitemid 38253678)
21. Forger N. G. (2006) Cell death and sexual differentiation of the nervous system. Neuroscience 138, 929-938.
22. Forger N. G., Rosen G. J., Waters E. M., Jacob D., Simerly R. B. and de Vries G. J. (2004) Deletion of Bax eliminates sex differences in the mouse forebrain. Proc. Natl. Acad. Sci. USA 101, 13666-13671. (Pubitemid 39238460)
23. Frank M. G., Wieseler-Frank J. L., Watkins L. R. and Maier S. F. (2006) Rapid isolation of highly enriched and quiescent microglia from adult rat hippocampus: Immunophenotypic and functional characteristics. J. Neurosci. Methods 151, 121-130. (Pubitemid 43294435)
24. Garay P. A. and McAllister A. K. (2010) Novel roles for immune molecules in neural development: implications for neurodevelopmental disorders. Front. Synaptic Neurosci. 2, 136.
25. Ginhoux F., Greter M., Leboeuf M. et al. (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845.
26. Glaser J., Green G. and Hendricks S. (2007) Stereology for biological research. MBF Press, Williston, VT.
27. Gomez-Gonzalez B. and Escobar A. (2010) Prenatal stress alters microglial development and distribution in postnatal rat brain. Acta Neuropathol. 119, 303-315.
28. Hahn Y. K., Vo P., Fitting S., Block M. L., Hauser K. F. and Knapp P. E. (2010) beta-Chemokine production by neural and glial progenitor cells is enhanced by HIV-1 Tat: effects on microglial migration. J. Neurochem. 114, 97-109.
29. Harry G. J. and Kraft A. D. (2008) Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment. Expert Opin. Drug Metab. Toxicol. 4, 1265-1277.
30. Hilton G. D., Nunez J. L. and McCarthy M. M. (2003) Sex differences in response to kainic acid and estradiol in the hippocampus of newborn rats. Neuroscience 116, 383-391. (Pubitemid 36139910)
31. Hodgson D. M. and Knott B. (2002) Potentiation of tumor metastasis in adulthood by neonatal endotoxin exposure: sex differences. Psychoneuroendocrinology 27, 791-804. (Pubitemid 35340807)
32. Johnson R. T., Breedlove S. M. and Jordan C. L. (2008) Sex differences and laterality in astrocyte number and complexity in the adult rat medial amygdala. J. Comp. Neurol. 511, 599-609.
33. Kipp M., Karakaya S., Johann S., Kampmann E., Mey J. and Beyer C. (2007) Oestrogen and progesterone reduce lipopolysaccharide-induced expression of tumour necrosis factor-alpha and interleukin-18 in midbrain astrocytes. J. Neuroendocrinol. 19, 819-822. (Pubitemid 47386883)
34. Krebs-Kraft D. L., Hill M. N., Hillard C. J. and McCarthy M. M. (2010) Sex difference in cell proliferation in developing rat amygdala mediated by endocannabinoids has implications for social behavior. Proc. Natl. Acad. Sci. USA 107, 20535-20540.
35. Kreutzberg G. W. (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318.
36. Llorente R., Gallardo M. L., Berzal A. L., Prada C., Garcia-Segura L. M. and Viveros M. P. (2009) Early maternal deprivation in rats induces gender-dependent effects on developing hippocampal and cerebellar cells. Int. J. Dev. Neurosci. 27, 233-241.
37. McKimmie C. S. and Graham G. J. (2010) Astrocytes modulate the chemokine network in a pathogen-specific manner. Biochem. Biophys. Res. Commun. 394, 1006-1011.
38. Mong J. A., Glaser E. and McCarthy M. M. (1999) Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regionally specific manner. J. Neurosci. 19, 1464-1472. (Pubitemid 29088927)
39. Mouton P. R. (2002) Principles and practices of unbiased stereology: an introduction for bioscientists. The Johns Hopkins University Press, Baltimore, MD.
40. Nishiyori A., Minami M., Ohtani Y., Takami S., Yamamoto J., Kawaguchi N., Kume T., Akaike A. and Satoh M. (1998) Localization of fractalkine and CX3CR1 mRNAs in rat brain: does fractalkine play a role in signaling from neuron to microglia? FEBS Lett. 429, 167-172. (Pubitemid 28288203)
41. Nunez J. L., Alt J. J. and McCarthy M. M. (2003) A novel model for prenatal brain damage. II. Long-term deficits in hippocampal cell number and hippocampal-dependent behavior following neonatal GABAA receptor activation. Exp. Neurol. 181, 270-280. (Pubitemid 36629247)
42. Ransohoff R. M. and Perry V. H. (2009) Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27, 119-145.
43. Reyna-Neyra A., Arias C., Ferrera P., Morimoto S. and Camacho-Arroyo I. (2004) Changes in the content and distribution of microtubule associated protein 2 in the hippocampus of the rat during the estrous cycle. J. Neurobiol. 60, 473-480. (Pubitemid 39108887)
44. Rezaie P., Trillo-Pazos G., Everall I. P. and Male D. K. (2002) Expression of beta-chemokines and chemokine receptors in human fetal astrocyte and microglial co-cultures: potential role of chemokines in the developing CNS. Glia 37, 64-75. (Pubitemid 34103095)
45. Santos-Galindo M., Acaz-Fonseca E., Bellini M. J. and Garcia-Segura L. M. (2011) Sex differences in the inflammatory response of primary astrocytes to lipopolysaccharide. Biol. Sex. Differ. 2, 7.
46. Schwarz J. M. and McCarthy M. M. (2008) Steroid-induced sexual differentiation of the developing brain: multiple pathways, one goal. J. Neurochem. 105, 1561-1572. (Pubitemid 351678518)
47. Sisk C. L. and Zehr J. L. (2005) Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 26, 163-174. (Pubitemid 41772653)
48. Soucy G., Boivin G., Labrie F. and Rivest S. (2005) Estradiol is required for a proper immune response to bacterial and viral pathogens in the female brain. J. Immunol. 174, 6391-6398. (Pubitemid 40663832)
49. Stevens B., Allen N. J., Vazquez L. E. et al. (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164-1178. (Pubitemid 350235022)
50. Wang C., Wu C., Shieh J. and Wen C. (2002) Microglial distribution and apoptosis in fetal rat brain. Dev. Brain Res. 139, 337-342. (Pubitemid 35453922)
51. Williamson L. L., Sholar P. W., Mistry R. M., Smith S. H. and Bilbo S. D. (2011) Microglia and memory: modulation by early-life infection. J. Neurosci. 31, 15511-15521.
52. Wu C. H., Wen C. Y., Shieh J. Y. and Ling E. A. (1992) A quantitative and morphometric study of the transformation of amoeboid microglia into ramified microglia in the developing corpus callosum in rats. J. Anat. 181(Pt 3), 423-430. (Pubitemid 23108134)
53. Wu C. H., Wen C. Y., Shieh J. Y. and Ling E. A. (1993) A quantitative study of the differentiation of microglial cells in the developing cerebral cortex in rats. J. Anat. 182(Pt 3), 403-413. (Pubitemid 23241207)
54. Wynne O., Horvat J. C., Osei-Kumah A., Smith R., Hansbro P. M., Clifton V. L. and Hodgson D. M. (2011) Early life infection alters adult BALB/c hippocampal gene expression in a sex specific manner. Stress 14, 247-261.
55. Xu J., Kaur C. and Ling E. A. (1993) Variation with age in the labelling of amoeboid microglial cells in rats following intraperitoneal or intravenous injection of a fluorescent dye. J. Anat. 182(Pt 1), 55-63. (Pubitemid 23124877)
56. Zehr J. L., Todd B. J., Schulz K. M., McCarthy M. M. and Sisk C. L. (2006) Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster. J. Neurobiol. 66, 578-590.