Postnatal Loss of Mef2c Results in Dissociation of Effects on Synapse Number and Learning and Memory

Biological Psychiatry

Volumn 80, Issue 2, 2016, Pages 140-148

  Adachi, Megumi ^a   Lin, Pei Yi ^a   Pranav, Heena ^a   Monteggia, Lisa M ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Autism; Behavior; Fear conditioning; MEF2C; Postnatal brain; Synaptic plasticity

Indexed keywords

MYOCYTE ENHANCER FACTOR 2; MEF2C PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; AUTISM; BEHAVIOR; BRAIN FUNCTION; COMPULSION; CONTROLLED STUDY; DISSOCIATION; EMBRYO DEVELOPMENT; GENE DELETION; GENETIC MANIPULATION; HIPPOCAMPUS; KNOCKOUT MOUSE; LEARNING; LOCOMOTION; LONG TERM POTENTIATION; MEMORY; MOTOR COORDINATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SOCIAL BEHAVIOR; SYNAPSE; SYNAPTOGENESIS; ANIMAL; ANIMAL BEHAVIOR; DENDRITIC SPINE; DISEASE MODEL; GENETICS; MOTOR ACTIVITY; PHYSIOLOGY;

ANIMALS; AUTISM SPECTRUM DISORDER; BEHAVIOR, ANIMAL; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; LEARNING; MEF2 TRANSCRIPTION FACTORS; MEMORY; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURONAL PLASTICITY;

EID: 84948807648     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2015.09.018     Document Type: Article

References (41)

1. 1 Potthoff, M.J., Olson, E.N., MEF2: A central regulator of diverse developmental programs. Development 134 (2007), 4131–4140.
2. 2 Lyons, G.E., Micales, B.K., Schwarz, J., Martin, J.F., Olson, E.N., Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J Neurosci 15 (1995), 5727–5738.
3. 3 Leifer, D., Golden, J., Kowall, N.W., Myocyte-specific enhancer binding factor 2C expression in human brain development. Neuroscience 63 (1994), 1067–1079.
4. 4 Black, B., Cripps, R., Myocyte enhancer factor-2 transcription factors in heart development and disease. Heart Development and Regeneration 2 (2010), 673–699.
5. 5 Flavell, S.W., Cowan, C.W., Kim, T.K., Greer, P.L., Lin, Y., Paradis, S., et al. Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311 (2006), 1008–1012.
6. 6 Cole, C.J., Mercaldo, V., Restivo, L., Yiu, A.P., Sekeres, M.J., Han, J.H., et al. MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nat Neurosci 15 (2012), 1255–1264.
7. 7 Rashid, A.J., Cole, C.J., Josselyn, S.A., Emerging roles for MEF2 transcription factors in memory. Genes Brain Behav 13 (2014), 118–125.
8. 8 Naya, F.J., Black, B.L., Wu, H., Bassel-Duby, R., Richardson, J.A., Hill, J.A., et al. Mitochondrial deficiency and cardiac sudden death in mice lacking the MEF2A transcription factor. Nat Med 8 (2002), 1303–1309.
9. 9 Phan, D., Rasmussen, T.L., Nakagawa, O., McAnally, J., Gottlieb, P.D., Tucker, P.W., et al. BOP, a regulator of right ventricular heart development, is a direct transcriptional target of MEF2C in the developing heart. Development 132 (2005), 2669–2678.
10. 10 Akhtar, M.W., Kim, M.S., Adachi, M., Morris, M.J., Qi, X., Richardson, J.A., et al. In vivo analysis of MEF2 transcription factors in synapse regulation and neuronal survival. PLoS One, 7, 2012, e34863.
11. 11 Barbosa, A.C., Kim, M.S., Ertunc, M., Adachi, M., Nelson, E.D., McAnally, J., et al. MEF2C, a transcription factor that facilitates learning and memory by negative regulation of synapse numbers and function. Proc Natl Acad Sci U S A 105 (2008), 9391–9396.
12. 12 Akbarian, S., Rios, M., Liu, R.J., Gold, S.J., Fong, H.F., Zeiler, S., et al. Brain-derived neurotrophic factor is essential for opiate-induced plasticity of noradrenergic neurons. J Neurosci 22 (2002), 4153–4162.
13. 13 Chen, R.Z., Akbarian, S., Tudor, M., Jaenisch, R., Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 27 (2001), 327–331.
14. 14 Luikart, B.W., Nef, S., Virmani, T., Lush, M.E., Liu, Y., Kavalali, E.T., et al. TrkB has a cell-autonomous role in the establishment of hippocampal Schaffer collateral synapses. J Neurosci 25 (2005), 3774–3786.
15. 15 Arnold, M.A., Kim, Y., Czubryt, M.P., Phan, D., McAnally, J., Qi, X., et al. MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev Cell 12 (2007), 377–389.
16. 16 Lin, Q., Schwarz, J., Bucana, C., Olson, E.N., Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276 (1997), 1404–1407.
17. 17 Adachi, M., Autry, A.E., Covington, H.E. 3rd, Monteggia, L.M., MeCP2-mediated transcription repression in the basolateral amygdala may underlie heightened anxiety in a mouse model of Rett syndrome. J Neurosci 29 (2009), 4218–4227.
18. 18 Gemelli, T., Berton, O., Nelson, E.D., Perrotti, L.I., Jaenisch, R., Monteggia, L.M., Postnatal loss of methyl-CpG binding protein 2 in the forebrain is sufficient to mediate behavioral aspects of Rett syndrome in mice. Biol Psychiatry 59 (2006), 468–476.
19. 19 Lange, N., Hamann, M., Shashidharan, P., Richter, A., Behavioural and pharmacological examinations in a transgenic mouse model of early-onset torsion dystonia. Pharmacol Biochem Behav 97 (2011), 647–655.
20. 20 Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
21. 21 Neale, B.M., Kou, Y., Liu, L., Ma'ayan, A., Samocha, K.E., Sabo, A., et al. Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 485 (2012), 242–245.
22. 22 Novara, F., Beri, S., Giorda, R., Ortibus, E., Nageshappa, S., Darra, F., et al. Refining the phenotype associated with MEF2C haploinsufficiency. Clin Genet 78 (2010), 471–477.
23. 23 Chao, H.T., Chen, H., Samaco, R.C., Xue, M., Chahrour, M., Yoo, J., et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468 (2010), 263–269.
24. 24 Bi, R., Foy, M.R., Vouimba, R.M., Thompson, R.F., Baudry, M., Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc Natl Acad Sci U S A 98 (2001), 13391–13395.
25. 25 Gould, E., Woolley, C.S., Frankfurt, M., McEwen, B.S., Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10 (1990), 1286–1291.
26. 26 Smith, C.C., McMahon, L.L., Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J Neurosci 25 (2005), 7780–7791.
27. 27 Monteggia, L.M., Barrot, M., Powell, C.M., Berton, O., Galanis, V., Gemelli, T., et al. Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc Natl Acad Sci U S A 101 (2004), 10827–10832.
28. 28 Garcia, A.D., Doan, N.B., Imura, T., Bush, T.G., Sofroniew, M.V., GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7 (2004), 1233–1241.
29. 29 Lin, X., Shah, S., Bulleit, R.F., The expression of MEF2 genes is implicated in CNS neuronal differentiation. Brain Res Mol Brain Res 42 (1996), 307–316.
30. 30 Berland, S., Houge, G., Late-onset gain of skills and peculiar jugular pit in an 11-year-old girl with 5q14.3 microdeletion including MEF2C. Clin Dysmorphol 19 (2010), 222–224.
31. 31 Carr, C.W., Zimmerman, H.H., Martin, C.L., Vikkula, M., Byrd, A.C., Abdul-Rahman, O.A., 5q14.3 neurocutaneous syndrome: A novel continguous gene syndrome caused by simultaneous deletion of RASA1 and MEF2C. Am J Med Genet A 155A (2011), 1640–1645.
32. 32 Engels, H., Wohlleber, E., Zink, A., Hoyer, J., Ludwig, K.U., Brockschmidt, F.F., et al. A novel microdeletion syndrome involving 5q14.3-q15: Clinical and molecular cytogenetic characterization of three patients. Eur J Hum Genet 17 (2009), 1592–1599.
33. 33 Le Meur, N., Holder-Espinasse, M., Jaillard, S., Goldenberg, A., Joriot, S., Amati-Bonneau, P., et al. MEF2C haploinsufficiency caused by either microdeletion of the 5q14.3 region or mutation is responsible for severe mental retardation with stereotypic movements, epilepsy and/or cerebral malformations. J Med Genet 47 (2010), 22–29.
34. 34 Mikhail, F.M., Lose, E.J., Robin, N.H., Descartes, M.D., Rutledge, K.D., Rutledge, S.L., et al. 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 (2011), 2386–2396.
35. 35 Nowakowska, B.A., Obersztyn, E., Szymanska, K., Bekiesinska-Figatowska, M., Xia, Z., Ricks, C.B., et al. Severe mental retardation, seizures, and hypotonia due to deletions of MEF2C. Am J Med Genet B Neuropsychiatr Genet 153B (2010), 1042–1051.
36. 36 Paciorkowski, A.R., Traylor, R.N., Rosenfeld, J.A., Hoover, J.M., Harris, C.J., Winter, S., et al. MEF2C haploinsufficiency features consistent hyperkinesis, variable epilepsy, and has a role in dorsal and ventral neuronal developmental pathways. Neurogenetics 14 (2013), 99–111.
37. 37 Zweier, M., Gregor, A., Zweier, C., Engels, H., Sticht, H., Wohlleber, E., et al. Mutations in MEF2C from the 5q14.3q15 microdeletion syndrome region are a frequent cause of severe mental retardation and diminish MECP2 and CDKL5 expression. Hum Mutat 31 (2010), 722–733.
38. 38 Morrow, E.M., Yoo, S.Y., Flavell, S.W., Kim, T.K., Lin, Y., Hill, R.S., et al. Identifying autism loci and genes by tracing recent shared ancestry. Science 321 (2008), 218–223.
39. 39 Li, H., Radford, J.C., Ragusa, M.J., Shea, K.L., McKercher, S.R., Zaremba, J.D., et al. Transcription factor MEF2C influences neural stem/progenitor cell differentiation and maturation in vivo. Proc Natl Acad Sci U S A 105 (2008), 9397–9402.
40. 40 Vetere, G., Restivo, L., Cole, C.J., Ross, P.J., Ammassari-Teule, M., Josselyn, S.A., et al. Spine growth in the anterior cingulate cortex is necessary for the consolidation of contextual fear memory. Proc Natl Acad Sci U S A 108 (2011), 8456–8460.
41. 41 Pulipparacharuvil, S., Renthal, W., Hale, C.F., Taniguchi, M., Xiao, G., Kumar, A., et al. Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59 (2008), 621–633.