MHCI requires MEF2 transcription factors to negatively regulate synapse density during development and in disease

Journal of Neuroscience

Volumn 33, Issue 34, 2013, Pages 13791-13804

  Elmer, Bradford M ^a   Estes, Myka L ^a   Barrow, Stephanie L ^a   McAllister, A Kimberley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; GLUTAMATE RECEPTOR 1; IONOTROPIC RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MYOCYTE ENHANCER FACTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CONNECTOME; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; FLOW CYTOMETRY; IMMUNE DYSREGULATION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NEUROLOGIC EXAMINATION; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RISK FACTOR; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; CALCINEURIN; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTOCOMPATIBILITY ANTIGENS CLASS I; MALE; MICE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; MYOGENIC REGULATORY FACTORS; NERVE TISSUE PROTEINS; NEURONS; OCCIPITAL LOBE; POLY I-C; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC POTENTIALS;

EID: 84882620367     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2366-13.2013     Document Type: Article

References (100)

1. Adelson JD, Barreto GE, Xu L, Kim T, Brott BK, Ouyang YB, Naserke T, Djurisic M, Xiong X, Shatz CJ, Giffard RG (2012) Neuroprotection from stroke in the absence of MHCI or PirB. Neuron 73:1100-1107.
2. Akhtar MW, Kim MS, Adachi M, Morris MJ, Qi X, Richardson JA, Bassel-Duby R, Olson EN, Kavalali ET, Monteggia LM (2012) In vivo analysis of MEF2 transcription factors in synapse regulation and neuronal survival. PLoS One 7:e34863.
3. Andreassen OA, Thompson WK, Schork AJ, Ripke S, Mattingsdal M, Kelsoe JR, Kendler KS, ODonovan MC, Rujescu D, Werge T, Sklar P, Roddey JC, Chen CH, McEvoy L, Desikan RS, Djurovic S, Dale AM (2013) Improved detection of common variants associated with schizophrenia and bipolar disorder using pleiotropy-informed conditional false discovery rate. PLoS Genet 9:e1003455.
4. Aramburu J, Yaffe MB, Lopez-Rodriguez C, Cantley LC, Hogan PG, Rao A (1999) Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 285:2129-2133.
5. Arnold MA, Kim Y, Czubryt MP, Phan D, McAnally J, Qi X, Shelton JM, Richardson JA, Bassel-Duby R, Olson EN (2007) MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev Cell 12:377-389.
6. Arosa FA, Santos SG, Powis SJ (2007) Open conformers: the hidden face of MHC-I molecules. Trends Immunol 28:115-123.
7. Arrode-Bruses G, Bruses JL (2012) Maternal immune activation by poly(I:C) induces expression of cytokines IL-1beta and IL-13, chemokine MCP-1 and colony stimulating factor VEGF in fetal mouse brain. J Neu-roinflammation 9:83.
8. Atladottir HO, Thorsen P, Østergaard L, Schendel DE, Lemcke S, Abdallah M, Parner ET (2010) Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord 40:1423-1430.
9. Atladottir HO, Henriksen TB, Schendel DE, Parner ET (2012) Autism after infection, febrile episodes, and antibiotic use during pregnancy: an exploratory study. Pediatrics 130:e1447-1454.
10. Barbosa AC, Olson EN, Kim MS, Ertunc M, Adachi M, Nelson ED, McAnally J, Richardson JA, Kavalali ET, Monteggia LM, Bassel-Duby R (2008) MEF2C, a transcription factor that facilitates learning and memory by negative regulation of synapse numbers and function. Proc Natl Acad Sci USA 105:9391-9396.
11. Bilousova T, Dang H, Xu W, Gustafson S, Jin Y, Wickramasinghe L, Won T, Bobarnac G, Middleton B, Tian J, Kaufman DL (2012) Major histocompatibility complex class I molecules modulate embryonic neuritogenesis and neuronal polarization. J Neuroimmunol 247:1-8.
12. Black BL, Ligon KL, Zhang Y, Olson EN (1996) Cooperative transcriptional activation by the neurogenic basic helix-loop-helix protein MASH1 and members of the myocyte enhancer factor-2 (MEF2) family. J Biol Chem 271:26659-26663.
13. Blaeser F, Ho N, Prywes R, Chatila TA (2000) Ca(2 +)-dependent gene expression mediated by MEF2 transcription factors. J Biol Chem 275:197-209.
14. Brown AS (2012) Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev Neurobiol 72:1272-1276.
15. Brown AS, Patterson PH (2011) Maternal infection and schizophrenia: implications for prevention. Schizophr Bulle 37:284-290.
16. Chacon MA, Boulanger LM (2013) MHC class I protein is expressed by neurons and neural progenitors in mid-gestation mouse brain. Mol Cell Neurosci 52:117-127.
17. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320:1224-1229.
18. Chen SX, Cherry A, Tari PK, Podgorski K, Kwong YK, Haas K (2012) The transcription factor MEF2 directs developmental visually driven functional and structural metaplasticity. Cell 151:41-55.
19. Chen Y, Stevens B, Chang J, Milbrandt J, Barres BA, Hell JW (2008) NS21: redefined and modified supplement B27 for neuronal cultures. J Neurosci Methods 171:239-247.
20. Cole CJ, Mercaldo V, Restivo L, Yiu AP, Sekeres MJ, Han JH, Vetere G, Pekar T, Ross PJ, Neve RL, Frankland PW, Josselyn SA (2012) MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nat Neurosci 15:1255-1264.
21. Corriveau R, Huh GS, Shatz CJ (1998) Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 21:505-520.
22. Datwani A, McConnell MJ, Kanold PO, Micheva KD, Busse B, Shamloo M, Smith SJ, Shatz CJ (2009) Classical MHCI molecules regulate retino-geniculate refinement and limit ocular dominance plasticity. Neuron 64: 463-470.
23. Dietrich JB (2013) The MEF2 family and the brain: from molecules to memory. Cell Tissue Res 352:179-190.
24. Dissing S, Geisler C, Rubin B, Plesner T, Claesson MH (1990) T cell activation: II. Activation of human T lymphoma cells by cross-linking of their MHC class I antigens. Cell Immunol 126:196-210.
25. Elmer BM, McAllister AK (2012) Major histocompatibility complex class I proteins in brain development and plasticity. Trends Neurosci 35:660- 670.
26. Fatemi SH, Reutiman TJ, Folsom TD, Huang H, Oishi K, Mori S, Smee DF, Pearce DA, Winter C, Sohr R, Juckel G (2008) Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: implications for genesis of neurodevelopmental disorders. Schizophr Res 99:56-70.
27. Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G (2009) Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 28:697-710.
28. Flavell SW, Cowan CW, Kim TK, Greer PL, Lin Y, Paradis S, Griffith EC, Hu LS, Chen C, Greenberg ME (2006) Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311:1008-1012.
29. Flavell SW, Kim TK, Gray JM, Harmin DA, Hemberg M, Hong EJ, Markenscoff-Papadimitriou E, Bear DM, Greenberg ME (2008) Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60:1022-1038.
30. Fourgeaud L, Davenport CM, Tyler CM, Cheng TT, Spencer MB, Boulanger LM (2010) MHC class I modulates NMDA receptor function and AMPA receptor trafficking. Proc Natl Acad Sci USA 107:22278-22283.
31. Garay PA, Hsiao EY, Patterson PH, McAllister AK (2013) Maternal immune activation causes age- and region-specific changes in brain cytokines in offspring throughout development. Brain Behav Immun 31:54-68.
32. Gilliland LK, Norris NA, Grosmaire LS, Ferrone S, Gladstone P, Ledbetter JA (1989) Signal transduction in lymphocyte activation through cross linking of HLA class I molecules. Hum Immunol 25:269-289.
33. Giovanoli S, Engler H, Engler A, Richetto J, Voget M, Willi R, Winter C, Riva MA, Mortensen PB, Schedlowski M, Meyer U (2013) Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science 339:1095-1099.
34. Glynn MW, McAllister AK (2006) Immunocytochemistry and quantification of protein colocalization in cultured neurons. Nat Protoc 1:1287-1296.
35. Glynn MW, Elmer BM, Garay PA, Liu XB, Needleman LA, El-Sabeawy F, McAllister AK (2011) MHCI negatively regulates synapse density during the establishment of cortical connections. Nat Neurosci 14:442-451.
36. Goddard CA, Butts DA, Shatz CJ (2007) Regulation of CNS synapses by neuronal MHC class I. Proc Natl Acad Sci U S A 104:6828-6833.
37. Groth RD, Dunbar RL, Mermelstein PG (2003) Calcineurin regulation of neuronal plasticity. Biochem Biophys Res Commun 311:1159-1171.
38. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, Shatz CJ (2000) Functional requirement for class I MHC in CNS development and plasticity. Science 290:2155-2159.
39. Irish Schizophrenia Genomics Consortium and the Wellcome Trust Case Control Consortium 2 (2012) Genome-wide association study implicates HLA-C*01:02 as a risk factor at the major histocompatibility complex locus in schizophrenia. Biol Psychiatry 72:620-628.
40. Ito HT, Smith SE, Hsiao E, Patterson PH (2010) Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain Behav Immun 24:930-941.
41. Jia P, Wang L, Fanous AH, Chen X, Kendler KS, Zhao Z (2012) A bias-reducing pathway enrichment analysis of genome-wide association data confirmed association of the MHC region with schizophrenia. J Med Genet 49:96-103.
42. Jin YP, Fishbein MC, Said JW, Jindra PT, Rajalingam R, Rozengurt E, Reed EF (2004) Anti-HLA class I antibody-mediated activation of the PI3K/Akt signaling pathway and induction of Bcl-2 and Bcl-xL expression in endo-thelial cells. Hum Immunol 65:291-302.
43. Johnson DR (2003) Locus-specific constitutive and cytokine-induced HLA class I gene expression. J Immunol 170:1894-1902.
44. Kano S, Nwulia E, Niwa M, Chen Y, Sawa A, Cascella N (2011) Altered MHC class I expression in dorsolateral prefrontal cortex of nonsmoker patients with schizophrenia. Neurosci Res 71:289-293.
45. Li H, Radford JC, Ragusa MJ, Shea KL, McKercher SR, Zaremba JD, Soussou W, Nie Z, Kang YJ, Nakanishi N, Okamoto S, Roberts AJ, Schwarz JJ, Lipton SA (2008) Transcription factor MEF2C influences neural stem/ progenitor cell differentiation and maturation in vivo. Proc Natl Acad Sci USA 105:9397-9402.
46. Li T, Li Z, Chen P, Zhao Q, Wang T, Huang K, Li J, Li Y, Liu J, Zeng Z, Feng G, He L, Shi Y (2010) Common variants in major histocompatibility complex region and TCF4 gene are significantly associated with schizophrenia in Han Chinese. Biol Psychiatry 68:671-673.
47. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 30:126-134.
48. Lyons GE, Micales BK, Schwarz J, Martin JF, Olson EN (1995) Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J Neurosci 15:5727-5738.
49. Lyons MR, Schwarz CM, West AE (2012) Members of the myocyte enhancer factor 2 transcription factor family differentially regulate Bdnf transcription in response to neuronal depolarization. J Neurosci 32: 12780-12785.
50. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
51. Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH (2012) Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun 26:607-616.
52. Mao Z, Bonni A, Xia F, Nadal-Vicens M, Greenberg ME (1999) Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286:785-790.
53. McConnell MJ, Huang YH, Datwani A, Shatz CJ (2009) H2-K(b) and H2-D(b) regulate cerebellar long-term depression and limit motor learning. Proc Natl Acad Sci USA 106:6784-6789.
54. Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I, Yee BK, Feldon J (2006) The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci 26:4752-4762.
55. Meyer U, Nyffeler M, Yee BK, Knuesel I, Feldon J (2008a) Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav Immun 22:469-486.
56. Meyer U, Nyffeler M, Schwendener S, Knuesel I, Yee BK, Feldon J (2008b) Relative prenatal and postnatal maternal contributions to schizophrenia-related neurochemical dysfunction after in utero immune challenge. Neuropsychopharmacology 33:441-456.
57. Meyer U, Feldon J, Fatemi SH (2009) In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurode-velopmental brain disorders. Neurosci Biobehav Rev 33:1061-1079.
58. Meyer U, Feldon J, Dammann O (2011) Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation? Pediatr Res 69:26R-33R.
59. Michel M, Schmidt MJ, Mirnics K (2012) Immune system gene dysregula-tion in autism and schizophrenia. DevNeurobiol 72:1277-1287.
60. Micheva KD, Busse B, Weiler NC, ORourke N, Smith SJ (2010) Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. Neuron 68:639-653.
61. Mikhail FM, Lose EJ, Robin NH, Descartes MD, Rutledge KD, Rutledge SL, Korf BR, Carroll AJ (2011) Clinically relevant single gene or intragenic deletions encompassing critical neurodevelopmental genes in patients with developmental delay, mental retardation, and/or autism spectrum disorders. Am J Med Genet A 155A:2386-2396.
62. Morrow EM, Yoo SY, Flavell SW, Kim TK, Lin Y, Hill RS, Mukaddes NM, Balkhy S, Gascon G, Hashmi A, Al-Saad S, Ware J, Joseph RM, Greenblatt R, Gleason D, Ertelt JA, Apse KA, Bodell A, Partlow JN, Barry B, et al. (2008) Identifying autism loci and genes by tracing recent shared ancestry. Science 321:218-223.
63. Mostafa GA, Shehab AA, Al-Ayadhi LY (2013) The link between some alleles on human leukocyte antigen system and autism in children. J Neu-roimmunol 255:70-74.
64. Neale BM, Kou Y, Liu L, Maayan A, Samocha KE, Sabo A, Lin CF, Stevens C, Wang LS, Makarov V, Polak P, Yoon S, Maguire J, Crawford EL, Campbell NG, Geller ET, Valladares O, Schafer C, Liu H, Zhao T, et al. (2012) Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 485:242-245.
65. Needleman LA, McAllister AK (2012) The major histocompatibility complex and autism spectrum disorder. Dev Neurobiol 72:1288-1301.
66. Needleman LA, Liu XB, El-Sabeawy F, Jones EG, McAllister AK (2010) MHC class I molecules are present both pre- and postsynaptically in the visual cortex during postnatal development and in adulthood. Proc Natl Acad Sci U S A 107:16999-17004.
67. Novara F, Beri S, Giorda R, Ortibus E, Nageshappa S, Darra F, Dalla Bernardina B, Zuffardi O, Van Esch H (2010) Refining the phenotype associated with MEF2C haploinsufficiency. Clin Genet 78:471-477.
68. Okamoto S, Krainc D, Sherman K, Lipton SA (2000) Antiapoptotic role of the p38 mitogen-activated protein kinase-myocyte enhancer factor 2 transcription factor pathway during neuronal differentiation. Proc Natl Acad Sci U S A 97:7561-7566.
69. Patterson PH (2011) Maternal infection and immune involvement in autism. Trends Mol Med 17:389-394.
70. Pazyra-Murphy MF, Hans A, Courchesne SL, Karch C, Cosker KE, Heerssen HM, Watson FL, Kim T, Greenberg ME, Segal RA (2009) A retrograde neuronal survival response: target-derived neurotrophins regulate MEF2D and bcl-w. J Neurosci 29:6700-6709.
71. Pedersen AE, Skov S, Bregenholt S, Ruhwald M, Claesson MH (1999) Signal transduction by the major histocompatibility complex class I molecule. APMIS 107:887-895.
72. Pereira AH, Clemente CF, Cardoso AC, Theizen TH, Rocco SA, Judice CC, Guido MC, Pascoal VD, Lopes-Cendes I, Souza JR, Franchini KG (2009) MEF2C silencing attenuates load-induced left ventricular hypertrophy by modulating mTOR/S6K pathway in mice. PLoS One 4:e8472.
73. Pfeiffer BE, Zang T, Wilkerson JR, Taniguchi M, Maksimova MA, Smith LN, Cowan CW, Huber KM (2010) Fragile X mental retardation protein is required for synapse elimination by the activity-dependent transcription factor MEF2. Neuron 66:191-197.
74. Potthoff MJ, Olson EN (2007) MEF2: A central regulator of diverse developmental programs. Development 134:4131-4140.
75. Pulipparacharuvil S, Renthal W, Hale CF, Taniguchi M, Xiao G, Kumar A, Russo SJ, Sikder D, Dewey CM, Davis MM, Greengard P, Nairn AC, Nestler EJ, Cowan CW (2008) Cocaine regulates MEF2 to control syn-aptic and behavioral plasticity. Neuron 59:621-633.
76. Purcell SM, Wray NR, Stone JL, Visscher PM, ODonovan MC, Sullivan PF, Sklar P (2009) Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 460:748-752.
77. Ribic A, Flügge G, Schlumbohm C, Mätz-Rensing K, Walter L, Fuchs E (2011) Activity-dependent regulation of MHC class I expression in the developing primary visual cortex of the common marmoset monkey. Behav Brain Funct 7:1.
78. Shalizi AK, Bonni A (2005) brawn for brains: the role of MEF2 proteins in the developing nervous system. Curr Top Dev Biol 69:239-266.
79. Shalizi A, Lehtinen M, Gaudilliere B, Donovan N, Han J, Konishi Y, Bonni A (2003) Characterization of a neurotrophin signaling mechanism that mediates neuron survival in a temporally specific pattern. J Neurosci 23:7326-7336.
80. Shalizi A, Gaudillière B, Yuan Z, Stegmüller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW, Bonni A (2006) A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311: 1012-1017.
81. Shalizi A, Bilimoria PM, Stegmuller J, Gaudillière B, Yang Y, Shuai K, Bonni A (2007) PIASx is a MEF2 SUMO E3 ligase that promotes postsynaptic dendritic morphogenesis. J Neurosci 27:10037-10046.
82. Shi J, Levinson DF, Duan J, Sanders AR, Zhang Y, Peer I, Dudbridge F, Holmans PA, Whittemore AS, Mowry BJ, Olincy A, Amin F, Cloninger CR, Silverman JM, Bocola NG, Byerley WF, Black DW, Crowe RR, Oksenberg JR, Mirel DB, et al. (2009) Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 460:753-757.
83. Shi L, Fatemi SH, Sidwell RW, Patterson PH (2003) Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 23:297-302.
84. Shi L, Tu N, Patterson PH (2005) Maternal influenza infection is likely to alter fetal brain development indirectly: the virus is not detected in the fetus. Int J Dev Neurosci 23:299-305.
85. Skov S, Odum N, Claesson MH (1995) MHC class I signaling in T cells leads to tyrosine kinase activity and PLC-gamma 1 phosphorylation. J Immunol 154:1167-1176.
86. Skov S, Bregenholt S, Claesson MH (1997) MHC classIligation of human T cells activates the ZAP70 and p56lck tyrosine kinases, leads to an alternative phenotype of the TCR/CD3 zeta-chain, and induces apoptosis. J Immunol 158:3189-3196.
87. Stefansson H, et al. (2009) Common variants conferring risk of schizophrenia. Nature 460:744-747.
88. Sun L, Youn HD, Loh C, Stolow M, He W, Liu JO (1998) Cabin 1, a negative regulator for calcineurin signaling in T lymphocytes. Immunity 8:703-711.
89. Swanson GT, Kamboj SK, Cull-Candy SG (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17:58-69.
90. Syken J, Grandpre T, Kanold PO, Shatz CJ (2006) PirB restricts ocular-dominance plasticity in visual cortex. Science 313:1795-1800.
91. Tian X, Kai L, Hockberger PE, Wokosin DL, Surmeier DJ (2010) MEF-2 regulates activity-dependent spine loss in striatopallidal medium spiny neurons. Mol Cell Neurosci 44:94-108.
92. Torres AR, Westover JB, Rosenspire AJ (2012a) HLA immune function genes in autism. Autism Res Treat 2012:959073.
93. Torres AR, Westover JB, Gibbons C, Johnson RC, Ward DC (2012b) Activating killer-cell immunoglobulin-like receptors (KIR) and their cognate HLA ligands are significantly increased in autism. Brain Behav Immun 26:1122-1127.
94. Tsai NP, Wilkerson JR, Guo W, Maksimova MA, DeMartino GN, Cowan CW, Huber KM (2012) Multiple autism-linked genes mediate synapse elimination via proteasomal degradation of a synaptic scaffold PSD-95. Cell 151:1581-1594.
95. Vetere G, Restivo L, Cole CJ, Ross PJ, Ammassari-Teule M, Josselyn SA, Frankland PW (2011) Spine growth in the anterior cingulate cortex is necessary for the consolidation of contextual fear memory. Proc Natl Acad Sci U S A 108:8456-8460.
96. Vuillermot S, Weber L, Feldon J, Meyer U (2010) A longitudinal examination of the neuro developmental impact of prenatal immune activation in mice reveals primary defects in dopaminergic development relevant to schizophrenia. J Neurosci 30:1270-1287.
97. Washburn LR, Zekzer D, Eitan S, Lu Y, Dang H, Middleton B, Evans CJ, Tian J, Kaufman DL (2011) A potential role for shed soluble major histocom-patibility class I molecules as modulators of neurite outgrowth. PLoS One 6:e18439.
98. Wu ZP, Washburn L, Bilousova TV, Boudzinskaia M, Escande-Beillard N, Querubin J, Dang H, Xie CW, Tian J, Kaufman DL (2011) Enhanced neuronal expression of major histocompatibility complex class I leads to aberrations in neurodevelopment and neurorepair. J Neuroimmunol 232:8-16.
99. Yamada T, Yang Y, Huang J, Coppola G, Geschwind DH, Bonni A (2013) Sumoylated MEF2A coordinately eliminates orphan presynaptic sites and promotes maturation of presynaptic boutons. J Neurosci 33:4726-4740.
100. Zang T, Maksimova MA, Cowan CW, Bassel-Duby R, Olson EN, Huber KM (2013) Postsynaptic FMRP bidirectionally regulates excitatory synapses as a function of developmental age and MEF2 activity. Mol Cell Neurosci 56C:39-49.