Microglia are essential to masculinization of brain and behavior

Journal of Neuroscience

Volumn 33, Issue 7, 2013, Pages 2761-2772

  Lenz, Kathryn M ^a   Nugent, Bridget M ^a   Haliyur, Rachana ^a   McCarthy, Margaret M ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; INDOMETACIN; MINOCYCLINE; PROSTAGLANDIN E2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL STRUCTURE; CONTROLLED STUDY; COPULATION; DENDRITIC SPINE; ENZYME IMMUNOASSAY; FEMALE; GENDER; IMMUNOHISTOCHEMISTRY; LATENT PERIOD; MALE; MICROGLIA; NERVE CELL INHIBITION; NEWBORN; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; RAT; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; UPREGULATION;

ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN; BRAIN CHEMISTRY; CELL COUNT; CELLS, CULTURED; DENDRITIC SPINES; DINOPROSTONE; ESTRADIOL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MINOCYCLINE; NERVE TISSUE PROTEINS; PREOPTIC AREA; RATS; SEX DIFFERENTIATION; SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION;

EID: 84873693906     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1268-12.2013     Document Type: Article

References (47)

1. Amateau SK, McCarthy MM (2002a) A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2. J Neurosci 22:8586-8596. Medline
2. Amateau SK, McCarthy MM (2002b) Sexual differentiation of astrocyte morphology in the developing rat preoptic area. J Neuroendocrinol 14: 904-910. CrossRef Medline
3. Amateau SK, McCarthy MM (2004) Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat Neurosci 7:643-650. CrossRef Medline
4. Bilousova TV, Dansie L, Ngo M, Aye J, Charles JR, Ethell DW, Ethell IM (2009) Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. J Med Genet 46:94-102. Medline
5. Burudi EM, Régnier-Vigouroux A (2001) Regional and cellular expression of the mannose receptor in the post-natal developing mouse brain. Cell Tissue Res 303:307-317. CrossRef Medline
6. Crain JM, Watters JJ (2010) Estrogen and P2 purinergic receptor systems in microglia: therapeutic targets for neuroprotection. Open Drug Discov J 2:148-167. Medline
7. Dalmau I, Finsen B, Tønder N, Zimmer J, González B, Castellano B (1997) Development of microglia in the prenatal rat hippocampus. J Comp Neurol 377:70-84. CrossRef Medline
8. Davis EC, Popper P, Gorski RA (1996) The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Res 734:10-18. CrossRef Medline
9. Fatemi SH, Folsom TD (2009) The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr Bull 35:528-548. CrossRef Medline
10. Gehrmann J, Matsumoto Y, Kreutzberg GW (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res Brain Res Rev 20:269-287. CrossRef Medline
11. Giulian D, Young DG, Woodward J, Brown DC, Lachman LB (1988) Interleukin-1 is an astroglial growth factor in the developing brain. J Neurosci 8:709-714. Medline
12. Gorski RA, Gordon JH, Shryne JE, Southam AM (1978) Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res 148:333-346. CrossRef Medline
13. Kim OS, Lee CS, Kim HY, Joe EH, Jou I (2005) Characterization of new microglia-like cells obtained from neonatal rat brain. Biochem Biophys Res Commun 328:281-287. CrossRef Medline
14. Kingham PJ, Cuzner ML, Pocock JM (1999) Apoptotic pathways mobilized in microglia and neurones as a consequence of chromogranin A-induced microglial activation. J Neurochem 73:538-547. CrossRef Medline
15. Kloss CU, Bohatschek M, Kreutzberg GW, Raivich G (2001) Effect of lipopolysaccharide on the morphology and integrin immunoreactivity of ramified microglia in the mouse brain and in cell culture. Exp Neurol 168:32-46. CrossRef Medline
16. Krishnan S, Intlekofer KA, Aggison LK, Petersen SL (2009) Central role of TRAF-interacting protein in a new model of brain sexual differentiation. Proc Natl Acad Sci U S A 106:16692-16697. CrossRef Medline
17. Ling EA, Wong WC (1993) The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7:9-18. CrossRef Medline
18. Ling EA, Kaur LC, Yick TY, Wong WC (1990) Immunocytochemical localization of CR3 complement receptors with OX-42 in amoeboid microglia in postnatal rats. Anat Embryol (Berl) 182:481-486. CrossRef Medline
19. Mallat M, Marín-Teva JL, Chéret C (2005) Phagocytosis in the developing CNS: more than clearing the corpses. Curr Opin Neurobiol 15:101-107. CrossRef Medline
20. Marchetti B, Serra PA, L'Episcopo F, Tirolo C, Caniglia S, Testa N, Cioni S, Gennuso F, Rocchitta G, Desole MS, Mazzarino MC, Miele E, Morale MC (2005) Hormones are key actors in gene environment interactions programming the vulnerability to Parkinson's disease: glia as a common final pathway. Ann N Y Acad Sci 1057:296-318. CrossRef Medline
21. Marín-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. CrossRef Medline
22. Marzolo MP, von Bernhardi R, Inestrosa NC (1999) Mannose receptor is present in a functional state in rat microglial cells. J Neurosci Res 58:387-395. CrossRef Medline
23. McCarthy MM, Wright CL, Schwarz JM (2009) New tricks by an old dogma: mechanisms of the Organizational/Activational Hypothesis of steroid-mediated sexual differentiation of brain and behavior. Horm Behav 55:655-665. CrossRef Medline
24. Meda L, Cassatella MA, Szendrei GI, Otvos L Jr, Baron P, Villalba M, Ferrari D, Rossi F (1995) Activation of microglial cells by β-amyloid protein and interferon. Nature 374:647-650. CrossRef Medline
25. Minghetti L, Levi G (1998) Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog Neurobiol 54:99-125. CrossRef Medline
26. Minghetti L, Nicolini A, Polazzi E, Créminon C, Maclouf J, Levi G (1997) Prostaglandin E2 downregulates inducible nitric oxide synthase expression in microglia by increasing cAMP levels. Adv Exp Med Biol 433:181-184. Medline
27. Mong JA, McCarthy MM (1999) Steroid-induced developmental plasticity in hypothalamic astrocytes: implications for synaptic patterning. J Neurobiol 40:602-619. CrossRef Medline
28. Morale MC, Serra PA, L'Episcopo F, Tirolo C, Caniglia S, Testa N, Gennuso F, Giaquinta G, Rocchitta G, Desole MS, Miele E, Marchetti B (2006) Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. Neuroscience 138:869-878. CrossRef Medline
29. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958-969. CrossRef Medline
30. Munn NA (2000) Microglia dysfunction in schizophrenia: an integrative theory. Med Hypotheses 54:198-202. CrossRef Medline
31. Nawa H, Takei N (2006) Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines. Neurosci Res 56:2-13. CrossRef Medline
32. Olesen KM, Auger AP (2005) Sex differences in Fos protein expression in the neonatal rat brain. J Neuroendocrinol 17:255-261. CrossRef Medline
33. Orikasa C, Kondo Y, Hayashi S, McEwen BS, Sakuma Y (2002) Sexually dimorphic expression of estrogen receptor β in the anteroventral periventricular nucleus of the rat preoptic area: implication in luteinizing hormone surge. Proc Natl Acad Sci U S A 99:3306-3311. CrossRef Medline
34. Park JH, Bonthius PJ, Tsai HW, Bekiranov S, Rissman EF (2010) Amyloid β precursor protein regulates male sexual behavior. J Neurosci 30:9967-9972. CrossRef Medline
35. Polazzi E, Contestabile A (2002) Reciprocal interactions between microglia and neurons: from survival to neuropathology. Rev Neurosci 13:221-242. Medline
36. Saijo K, Collier JG, Li AC, Katzenellenbogen JA, Glass CK (2011) An ADIOL-ERβ-CtBP transrepression pathway negatively regulates microglia-mediated inflammation. Cell 145:584-595. CrossRef Medline
37. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complementdependent manner. Neuron 74:691-705. CrossRef Medline
38. Schwarz JM, Sholar PW, Bilbo SD (2012) Sex differences in microglial colonization of the developing rat brain. J Neurochem 120:948-963. CrossRef Medline
39. Stence N, Waite M, Dailey ME (2001) Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia 33:256-266. CrossRef Medline
40. Streit WJ, Conde JR, Fendrick SE, Flanary BE, Mariani CL (2005) Role of microglia in the central nervous system's immune response. Neurol Res 27:685-691. CrossRef Medline
41. Tremblay ME, Stevens B, Sierra A, Wake H, Bessis A, Nimmerjahn A (2011) The role of microglia in the healthy brain. J Neurosci 31:16064-16069. CrossRef Medline
42. 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. CrossRef Medline
43. Vegeto E, Bonincontro C, Pollio G, Sala A, Viappiani S, Nardi F, Brusadelli A, Viviani B, Ciana P, Maggi A (2001) Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. J Neurosci 21:1809-1818. Medline
44. World Health Organization (2001) Mental and neurological disorders [fact sheet]. Retrieved from http://www.who.int/whr/2001/media_centre/en/whr01_fact_sheet1_en.pdf
45. Wright CL, McCarthy MM (2009) Prostaglandin E2-induced masculinization of brain and behavior requires protein kinase A, AMPA/kainate, and metabotropic glutamate receptor signaling. J Neurosci 29:13274-13282. CrossRef Medline
46. Wu CH, Wen CY, Shieh JY, Ling EA (1992) A quantitative and morphometric study of the transformation of amoeboid microglia into ramified microglia in the developing corpus callosum in rats. J Anat 181:423-430. Medline
47. Yokosuka M, Okamura H, Hayashi S (1997) Postnatal development and sex difference in neurons containing estrogen receptor-immunoreactivity in the preoptic brain, the diencephalon, and the amygdala in the rat. J Comp Neurol 389:81-93. CrossRef Medline