The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
권호 표지
DOI QR코드

DOI QR Code

Synaptic Plasticity in Mouse Models of Autism Spectrum Disorders

  • Chung, Leeyup (Department of Pediatrics, Duke University School of Medicine) ;
  • Bey, Alexandra L. (Department of Neurobiology, Duke University School of Medicine) ;
  • Jiang, Yong-Hui (Department of Pediatrics, Duke University School of Medicine)
  • Received : 2012.09.26
  • Accepted : 2012.10.28
  • Published : 2012.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Analysis of synaptic plasticity together with behavioral and molecular studies have become a popular approach to model autism spectrum disorders in order to gain insight into the pathosphysiological mechanisms and to find therapeutic targets. Abnormalities of specific types of synaptic plasticity have been revealed in numerous genetically modified mice that have molecular construct validity to human autism spectrum disorders. Constrained by the feasibility of technique, the common regions analyzed in most studies are hippocampus and visual cortex. The relevance of the synaptic defects in these regions to the behavioral abnormalities of autistic like behaviors is still a subject of debate. Because the exact regions or circuits responsible for the core features of autistic behaviors in humans are still poorly understood, investigation using region-specific conditional mutant mice may help to provide the insight into the neuroanatomical basis of autism in the future.

Keywords

References

  1. Bliss TV, Collingridge GL. A synaptic model of memory: longterm potentiation in the hippocampus. Nature. 1993;361:31-39. https://doi.org/10.1038/361031a0
  2. Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science. 2001;294:1030-1038. https://doi.org/10.1126/science.1067020
  3. Collingridge GL, Peineau S, Howland JG, Wang YT. Longterm depression in the CNS. Nat Rev Neurosci. 2010;11:459-473.
  4. Nicoll RA. Expression mechanisms underlying long-term potentiation: a postsynaptic view. Philos Trans R Soc Lond B Biol Sci. 2003;358:721-726. https://doi.org/10.1098/rstb.2002.1228
  5. Zoghbi HY, Bear MF. Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb Perspect Biol. 2012;4.
  6. Ting JT, Peça J, Feng G. Functional consequences of mutations in postsynaptic scaffolding proteins and relevance to psychiatric disorders. Annu Rev Neurosci. 2012;35:49-71. https://doi.org/10.1146/annurev-neuro-062111-150442
  7. Dagli A, Buiting K, Williams CA. Molecular and Clinical Aspects of Angelman Syndrome. Mol Syndromol. 2012;2:100-112.
  8. Williams CA, Beaudet AL, Clayton-Smith J, Knoll JH, Kyllerman M, Laan LA, Magenis RE, Moncla A, Schinzel AA, Summers JA, Wagstaff J. Angelman syndrome 2005: updated consensus for diagnostic criteria. Am J Med Genet A. 2006; 140:413-418.
  9. Jiang Y, Lev-Lehman E, Bressler J, Tsai TF, Beaudet AL. Genetics of Angelman syndrome. Am J Hum Genet. 1999;65: 1-6. https://doi.org/10.1086/302473
  10. Kishino T, Lalande M, Wagstaff J. UBE3A/E6-AP mutations cause Angelman syndrome. Nat Genet. 1997;15:70-73. https://doi.org/10.1038/ng0197-70
  11. Matsuura T, Sutcliffe JS, Fang P, Galjaard RJ, Jiang YH, Benton CS, Rommens JM, Beaudet AL. De novo truncating mutations in E6-AP ubiquitin-protein ligase gene (UBE3A) in Angelman syndrome. Nat Genet. 1997;15:74-77.
  12. Jiang YH, Armstrong D, Albrecht U, Atkins CM, Noebels JL, Eichele G, Sweatt JD, Beaudet AL. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron. 1998;21:799-811. https://doi.org/10.1016/S0896-6273(00)80596-6
  13. Miura K, Kishino T, Li E, Webber H, Dikkes P, Holmes GL, Wagstaff J. Neurobehavioral and electroencephalographic abnormalities in Ube3a maternal-deficient mice. Neurobiol Dis. 2002;9:149-159. https://doi.org/10.1006/nbdi.2001.0463
  14. Jiang YH, Pan Y, Zhu L, Landa L, Yoo J, Spencer C, Lorenzo I, Brilliant M, Noebels J, Beaudet AL. Altered ultrasonic vocalization and impaired learning and memory in Angelman syndrome mouse model with a large maternal deletion from Ube3a to Gabrb3. PLoS One. 2010;5:e12278. https://doi.org/10.1371/journal.pone.0012278
  15. Weeber EJ, Jiang YH, Elgersma Y, Varga AW, Carrasquillo Y, Brown SE, Christian JM, Mirnikjoo B, Silva A, Beaudet AL, Sweatt JD. Derangements of hippocampal calcium/calmodulin- dependent protein kinase II in a mouse model for Angelman mental retardation syndrome. J Neurosci. 2003;23:2634-2644.
  16. van Woerden GM, Harris KD, Hojjati MR, Gustin RM, Qiu S, de Avila Freire R, Jiang YH, Elgersma Y, Weeber EJ. Rescue of neurological deficits in a mouse model for Angelman syndrome by reduction of alphaCaMKII inhibitory phosphorylation. Nat Neurosci. 2007;10:280-282. https://doi.org/10.1038/nn1845
  17. Yashiro K, Riday TT, Condon KH, Roberts AC, Bernardo DR, Prakash R, Weinberg RJ, Ehlers MD, Philpot BD. Ube3a is required for experience-dependent maturation of the neocortex. Nat Neurosci. 2009;12:777-783. https://doi.org/10.1038/nn.2327
  18. Sato M, Stryker MP. Genomic imprinting of experience-dependent cortical plasticity by the ubiquitin ligase gene Ube3a. Proc Natl Acad Sci USA. 2010;107:5611-5616. https://doi.org/10.1073/pnas.1001281107
  19. Mabb AM, Judson MC, Zylka MJ, Philpot BD. Angelman syndrome: insights into genomic imprinting and neurodevelopmental phenotypes. Trends Neurosci. 2011;34:293-303. https://doi.org/10.1016/j.tins.2011.04.001
  20. Huang HS, Allen JA, Mabb AM, King IF, Miriyala J, Taylor- Blake B, Sciaky N, Dutton JW Jr, Lee HM, Chen X, Jin J, Bridges AS, Zylka MJ, Roth BL, Philpot BD. Topoisomerase inhibitors unsilence the dormant allele of Ube3a in neurons. Nature. 2011;481:185-189. https://doi.org/10.1038/nature10726
  21. Beaudet AL. Angelman syndrome: Drugs to awaken a paternal gene. Nature. 2011;481:150-152.
  22. Daily JL, Nash K, Jinwal U, Golde T, Rogers J, Peters MM, Burdine RD, Dickey C, Banko JL, Weeber EJ. Adeno-associated virus-mediated rescue of the cognitive defects in a mouse model for Angelman syndrome. PLoS One. 2011;6:e27221. https://doi.org/10.1371/journal.pone.0027221
  23. Kaphzan H, Hernandez P, Jung JI, Cowansage KK, Deinhardt K, Chao MV, Abel T, Klann E. Reversal of impaired hippocampal long-term potentiation and contextual fear memory deficits in Angelman syndrome model mice by ErbB inhibitors. Biol Psychiatry. 2012;72:182-190. https://doi.org/10.1016/j.biopsych.2012.01.021
  24. Guy J, Gan J, Selfridge J, Cobb S, Bird A. Reversal of neurological defects in a mouse model of Rett syndrome. Science. 2007;315:1143-1147. https://doi.org/10.1126/science.1138389
  25. Gadalla KK, Bailey ME, Cobb SR. MeCP2 and Rett syndrome: reversibility and potential avenues for therapy. Biochem J. 2011;439:1-14. https://doi.org/10.1042/BJ20110648
  26. Williams CA. The behavioral phenotype of the Angelman syndrome. Am J Med Genet C Semin Med Genet. 2010;154C: 432-437. https://doi.org/10.1002/ajmg.c.30278
  27. Allensworth M, Saha A, Reiter LT, Heck DH. Normal social seeking behavior, hypoactivity and reduced exploratory range in a mouse model of Angelman syndrome. BMC Genet. 2011; 12:7.
  28. Bhakar AL, Dolen G, Bear MF. The pathophysiology of fragile X (and what it teaches us about synapses). Annu Rev Neurosci. 2012;35:417-443. https://doi.org/10.1146/annurev-neuro-060909-153138
  29. Martin JP, Bell J. A pedigree of mental defect showing sex-linkage. J Neurol Psychiatry. 1943;6:154-157. https://doi.org/10.1136/jnnp.6.3-4.154
  30. Pieretti M, Zhang FP, Fu YH, Warren ST, Oostra BA, Caskey CT, Nelson DL. Absence of expression of the FMR-1 gene in fragile X syndrome. Cell. 1991;66:817-822. https://doi.org/10.1016/0092-8674(91)90125-I
  31. Verkerk AJ, Pieretti M, Sutcliffe JS, Fu YH, Kuhl DP, Pizzuti A, Reiner O, Richards S, Victoria MF, Zhang FP, et al. Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell. 1991;65:905-914. https://doi.org/10.1016/0092-8674(91)90397-H
  32. Sutcliffe JS, Nelson DL, Zhang F, Pieretti M, Caskey CT, Saxe D, Warren ST. DNA methylation represses FMR-1 transcription in fragile X syndrome. Hum Mol Genet. 1992;1:397-400. https://doi.org/10.1093/hmg/1.6.397
  33. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A, Fischer U. Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet. 2001; 10:329-338. https://doi.org/10.1093/hmg/10.4.329
  34. Li Z, Zhang Y, Ku L, Wilkinson KD, Warren ST, Feng Y. The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res. 2001;29:2276-2283. https://doi.org/10.1093/nar/29.11.2276
  35. Fmr1 knockout mice: a model to study fragile X mental retardation. The Dutch-Belgian Fragile X Consortium. Cell. 1994;78:23-33.
  36. Santoro MR, Bray SM, Warren ST. Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu Rev Pathol. 2012;7:219-245. https://doi.org/10.1146/annurev-pathol-011811-132457
  37. Godfraind JM, Reyniers E, De Boulle K, D'Hooge R, De Deyn PP, Bakker CE, Oostra BA, Kooy RF, Willems PJ. Long-term potentiation in the hippocampus of fragile X knockout mice. Am J Med Genet. 1996;64:246-251. https://doi.org/10.1002/(SICI)1096-8628(19960809)64:2<246::AID-AJMG2>3.0.CO;2-S
  38. Paradee W, Melikian HE, Rasmussen DL, Kenneson A, Conn PJ, Warren ST. Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience. 1999;94:185-192. https://doi.org/10.1016/S0306-4522(99)00285-7
  39. Li J, Pelletier MR, Perez Velazquez JL, Carlen PL. Reduced cortical synaptic plasticity and GluR1 expression associated with fragile X mental retardation protein deficiency. Mol Cell Neurosci. 2002;19:138-151. https://doi.org/10.1006/mcne.2001.1085
  40. Larson J, Jessen RE, Kim D, Fine AK, du Hoffmann J. Age-dependent and selective impairment of long-term potentiation in the anterior piriform cortex of mice lacking the fragile X mental retardation protein. J Neurosci. 2005;25: 9460-9469. https://doi.org/10.1523/JNEUROSCI.2638-05.2005
  41. Lauterborn JC, Rex CS, Kramar E, Chen LY, Pandyarajan V, Lynch G, Gall CM. Brain-derived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome. J Neurosci. 2007;27:10685-10694. https://doi.org/10.1523/JNEUROSCI.2624-07.2007
  42. Lee HY, Ge WP, Huang W, He Y, Wang GX, Rowson-Baldwin A, Smith SJ, Jan YN, Jan LY. Bidirectional regulation of dendritic voltage-gated potassium channels by the fragile X mental retardation protein. Neuron. 2011;72:630-642. https://doi.org/10.1016/j.neuron.2011.09.033
  43. Zhao MG, Toyoda H, Ko SW, Ding HK, Wu LJ, Zhuo M. Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. J Neurosci. 2005;25: 7385-7392. https://doi.org/10.1523/JNEUROSCI.1520-05.2005
  44. Wilson BM, Cox CL. Absence of metabotropic glutamate receptor-mediated plasticity in the neocortex of fragile X mice. Proc Natl Acad Sci USA. 2007;104:2454-2459. https://doi.org/10.1073/pnas.0610875104
  45. Suvrathan A, Hoeffer CA, Wong H, Klann E, Chattarji S. Characterization and reversal of synaptic defects in the amygdala in a mouse model of fragile X syndrome. Proc Natl Acad Sci USA. 2010;107:11591-11596. https://doi.org/10.1073/pnas.1002262107
  46. Huber KM, Gallagher SM, Warren ST, Bear MF. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA. 2002;99:7746-7750. https://doi.org/10.1073/pnas.122205699
  47. Koekkoek SK, Yamaguchi K, Milojkovic BA, Dortland BR, Ruigrok TJ, Maex R, De Graaf W, Smit AE, VanderWerf F, Bakker CE, Willemsen R, Ikeda T, Kakizawa S, Onodera K, Nelson DL, Mientjes E, Joosten M, De Schutter E, Oostra BA, Ito M, De Zeeuw CI. Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron. 2005;47:339-352. https://doi.org/10.1016/j.neuron.2005.07.005
  48. Bear MF, Huber KM, Warren ST. The mGluR theory of fragile X mental retardation. Trends Neurosci. 2004;27:370-377. https://doi.org/10.1016/j.tins.2004.04.009
  49. Gallagher SM, Daly CA, Bear MF, Huber KM. Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J Neurosci. 2004;24:4859-4864. https://doi.org/10.1523/JNEUROSCI.5407-03.2004
  50. Hou L, Klann E. Activation of the phosphoinositide 3-kinase- Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci. 2004;24:6352-6361. https://doi.org/10.1523/JNEUROSCI.0995-04.2004
  51. Osterweil EK, Krueger DD, Reinhold K, Bear MF. Hypersensitivity to mGluR5 and ERK1/2 leads to excessive protein synthesis in the hippocampus of a mouse model of fragile X syndrome. J Neurosci. 2010;30:15616-15627. https://doi.org/10.1523/JNEUROSCI.3888-10.2010
  52. Bassell GJ, Warren ST. Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron. 2008;60:201-214. https://doi.org/10.1016/j.neuron.2008.10.004
  53. Ronesi JA, Huber KM. Homer interactions are necessary for metabotropic glutamate receptor-induced long-term depression and translational activation. J Neurosci. 2008;28:543-547. https://doi.org/10.1523/JNEUROSCI.5019-07.2008
  54. Dolen G, Osterweil E, Rao BS, Smith GB, Auerbach BD, Chattarji S, Bear MF. Correction of fragile X syndrome in mice. Neuron. 2007;56:955-962. https://doi.org/10.1016/j.neuron.2007.12.001
  55. Michalon A, Sidorov M, Ballard TM, Ozmen L, Spooren W, Wettstein JG, Jaeschke G, Bear MF, Lindemann L. Chronic pharmacological mGlu5 inhibition corrects fragile X in adult mice. Neuron. 2012;74:49-56. https://doi.org/10.1016/j.neuron.2012.03.009
  56. Ronesi JA, Collins KA, Hays SA, Tsai NP, Guo W, Birnbaum SG, Hu JH, Worley PF, Gibson JR, Huber KM. Disrupted Homer scaffolds mediate abnormal mGluR5 function in a mouse model of fragile X syndrome. Nat Neurosci. 2012;15: 431-440. https://doi.org/10.1038/nn.3033
  57. Spencer CM, Alekseyenko O, Serysheva E, Yuva-Paylor LA, Paylor R. Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav. 2005;4:420-430. https://doi.org/10.1111/j.1601-183X.2005.00123.x
  58. McNaughton CH, Moon J, Strawderman MS, Maclean KN, Evans J, Strupp BJ. Evidence for social anxiety and impaired social cognition in a mouse model of fragile X syndrome. Behav Neurosci. 2008;122:293-300.
  59. Thomas AM, Bui N, Graham D, Perkins JR, Yuva-Paylor LA, Paylor R. Genetic reduction of group 1 metabotropic glutamate receptors alters select behaviors in a mouse model for fragile X syndrome. Behav Brain Res. 2011;223:310-321. https://doi.org/10.1016/j.bbr.2011.04.049
  60. Bhattacharya A, Kaphzan H, Alvarez-Dieppa AC, Murphy JP, Pierre P, Klann E. Genetic Removal of p70 S6 Kinase 1 Corrects Molecular, Synaptic, and Behavioral Phenotypes in Fragile X Syndrome Mice. Neuron. 2012;76:325-337. https://doi.org/10.1016/j.neuron.2012.07.022
  61. Crino PB, Nathanson KL, Henske EP. The tuberous sclerosis complex. N Engl J Med. 2006;355:1345-1356. https://doi.org/10.1056/NEJMra055323
  62. Curatolo P, Bombardieri R, Jozwiak S. Tuberous sclerosis. Lancet. 2008;372:657-668. https://doi.org/10.1016/S0140-6736(08)61279-9
  63. Kandt RS, Haines JL, Smith M, Northrup H, Gardner RJ, Short MP, Dumars K, Roach ES, Steingold S, Wall S, et al. Linkage of an important gene locus for tuberous sclerosis to a chromosome 16 marker for polycystic kidney disease. Nat Genet. 1992;2:37-41. https://doi.org/10.1038/ng0992-37
  64. van Slegtenhorst M, de Hoogt R, Hermans C, Nellist M, Janssen B, Verhoef S, Lindhout D, van den Ouweland A, Halley D, Young J, Burley M, Jeremiah S, Woodward K, Nahmias J, Fox M, Ekong R, Osborne J, Wolfe J, Povey S, Snell RG, Cheadle JP, Jones AC, Tachataki M, Ravine D, Sampson JR, Reeve MP, Richardson P, Wilmer F, Munro C, Hawkins TL, Sepp T, Ali JB, Ward S, Green AJ, Yates JR, Kwiatkowska J, Henske EP, Short MP, Haines JH, Jozwiak S, Kwiatkowski DJ. Identification of the tuberous sclerosis gene TSC1 on chromosome 9q34. Science. 1997;277:805-808. https://doi.org/10.1126/science.277.5327.805
  65. Plank TL, Yeung RS, Henske EP. Hamartin, the product of the tuberous sclerosis 1 (TSC1) gene, interacts with tuberin and appears to be localized to cytoplasmic vesicles. Cancer Res. 1998;58:4766-4770.
  66. van Slegtenhorst M, Nellist M, Nagelkerken B, Cheadle J, Snell R, van den Ouweland A, Reuser A, Sampson J, Halley D, van der Sluijs P. Interaction between hamartin and tuberin, the TSC1 and TSC2 gene products. Hum Mol Genet. 1998;7:1053-1057. https://doi.org/10.1093/hmg/7.6.1053
  67. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J. Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol. 2003;13:1259-1268. https://doi.org/10.1016/S0960-9822(03)00506-2
  68. de Vries PJ, Howe CJ. The tuberous sclerosis complex proteins-- a GRIPP on cognition and neurodevelopment. Trends Mol Med. 2007;13:319-326. https://doi.org/10.1016/j.molmed.2007.06.003
  69. Onda H, Lueck A, Marks PW, Warren HB, Kwiatkowski DJ. Tsc2(+/-) mice develop tumors in multiple sites that express gelsolin and are influenced by genetic background. J Clin Invest. 1999;104:687-695. https://doi.org/10.1172/JCI7319
  70. Kobayashi T, Minowa O, Kuno J, Mitani H, Hino O, Noda T. Renal carcinogenesis, hepatic hemangiomatosis, and embryonic lethality caused by a germ-line Tsc2 mutation in mice. Cancer Res. 1999;59:1206-1211.
  71. Kobayashi T, Minowa O, Sugitani Y, Takai S, Mitani H, Kobayashi E, Noda T, Hino O. A germ-line Tsc1 mutation causes tumor development and embryonic lethality that are similar, but not identical to, those caused by Tsc2 mutation in mice. Proc Natl Acad Sci USA. 2001;98:8762-8767. https://doi.org/10.1073/pnas.151033798
  72. Ehninger D, Han S, Shilyansky C, Zhou Y, Li W, Kwiatkowski DJ, Ramesh V, Silva AJ. Reversal of learning deficits in a Tsc2+/－ mouse model of tuberous sclerosis. Nat Med. 2008; 14:843-848. https://doi.org/10.1038/nm1788
  73. Goorden SM, van Woerden GM, van der Weerd L, Cheadle JP, Elgersma Y. Cognitive deficits in Tsc1+/- mice in the absence of cerebral lesions and seizures. Ann Neurol. 2007;62: 648-655. https://doi.org/10.1002/ana.21317
  74. von der Brelie C, Waltereit R, Zhang L, Beck H, Kirschstein T. Impaired synaptic plasticity in a rat model of tuberous sclerosis. Eur J Neurosci. 2006;23:686-692. https://doi.org/10.1111/j.1460-9568.2006.04594.x
  75. Nie D, Di Nardo A, Han JM, Baharanyi H, Kramvis I, Huynh T, Dabora S, Codeluppi S, Pandolfi PP, Pasquale EB, Sahin M. Tsc2-Rheb signaling regulates EphA-mediated axon guidance. Nat Neurosci. 2010;13:163-172. https://doi.org/10.1038/nn.2477
  76. Auerbach BD, Osterweil EK, Bear MF. Mutations causing syndromic autism define an axis of synaptic pathophysiology. Nature. 2011;480:63-68. https://doi.org/10.1038/nature10658
  77. Bateup HS, Takasaki KT, Saulnier JL, Denefrio CL, Sabatini BL. Loss of Tsc1 in vivo impairs hippocampal mGluR-LTD and increases excitatory synaptic function. J Neurosci. 2011; 31:8862-8869. https://doi.org/10.1523/JNEUROSCI.1617-11.2011
  78. Zeng LH, Ouyang Y, Gazit V, Cirrito JR, Jansen LA, Ess KC, Yamada KA, Wozniak DF, Holtzman DM, Gutmann DH, Wong M. Abnormal glutamate homeostasis and impaired synaptic plasticity and learning in a mouse model of tuberous sclerosis complex. Neurobiol Dis. 2007;28:184-196. https://doi.org/10.1016/j.nbd.2007.07.015
  79. Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, Steinberg J, Crawley JN, Regehr WG, Sahin M. Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature. 2012;488:647-651. https://doi.org/10.1038/nature11310
  80. Chévere-Torres I, Maki JM, Santini E, Klann E. Impaired social interactions and motor learning skills in tuberous sclerosis complex model mice expressing a dominant/negative form of tuberin. Neurobiol Dis. 2012;45:156-164. https://doi.org/10.1016/j.nbd.2011.07.018
  81. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet. 1999;23:185-188. https://doi.org/10.1038/13810
  82. Chahrour M, Zoghbi HY. The story of Rett syndrome: from clinic to neurobiology. Neuron. 2007;56:422-437. https://doi.org/10.1016/j.neuron.2007.10.001
  83. Smeets EE, Pelc K, Dan B. Rett Syndrome. Mol Syndromol. 2012;2:113-127.
  84. Nan X, Campoy FJ, Bird A. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell. 1997;88:471-481. https://doi.org/10.1016/S0092-8674(00)81887-5
  85. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science. 2008;320:1224- 1229. https://doi.org/10.1126/science.1153252
  86. Chen RZ, 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. 2001;27:327-331. https://doi.org/10.1038/85906
  87. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J, Armstrong D, Paylor R, Zoghbi H. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron. 2002;35: 243-254. https://doi.org/10.1016/S0896-6273(02)00768-7
  88. Na ES, Nelson ED, Kavalali ET, Monteggia LM. The Impact of MeCP2 Loss- or Gain-of-Function on Synaptic Plasticity. Neuropsychopharmacology. 2012. [Epub ahead of print]
  89. Collins AL, Levenson JM, Vilaythong AP, Richman R, Armstrong DL, Noebels JL, David Sweatt J, Zoghbi HY. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum Mol Genet. 2004;13:2679-2689. https://doi.org/10.1093/hmg/ddh282
  90. Na ES, Nelson ED, Adachi M, Autry AE, Mahgoub MA, Kavalali ET, Monteggia LM. A mouse model for MeCP2 duplication syndrome: MeCP2 overexpression impairs learning and memory and synaptic transmission. J Neurosci. 2012;32: 3109-3117. https://doi.org/10.1523/JNEUROSCI.6000-11.2012
  91. Moretti P, Bouwknecht JA, Teague R, Paylor R, Zoghbi HY. Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Hum Mol Genet. 2005; 14:205-220.
  92. Samaco RC, Mandel-Brehm C, McGraw CM, Shaw CA, McGill BE, Zoghbi HY. Crh and Oprm1 mediate anxiety-related behavior and social approach in a mouse model of MECP2 duplication syndrome. Nat Genet. 2012;44:206-211. https://doi.org/10.1038/ng.1066
  93. Gemelli T, Berton O, Nelson ED, Perrotti LI, Jaenisch R, Monteggia LM. Postnatal loss of methyl-CpG binding protein 2 in the forebrain is sufficient to mediate behavioral aspects of Rett syndrome in mice. Biol Psychiatry. 2006;59:468-476. https://doi.org/10.1016/j.biopsych.2005.07.025
  94. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, Neul JL, Gong S, Lu HC, Heintz N, Ekker M, Rubenstein JL, Noebels JL, Rosenmund C, Zoghbi HY. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature. 2010;468:263-269. https://doi.org/10.1038/nature09582
  95. Asaka Y, Jugloff DG, Zhang L, Eubanks JH, Fitzsimonds RM. Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis. 2006;21:217-227. https://doi.org/10.1016/j.nbd.2005.07.005
  96. Moretti P, Levenson JM, Battaglia F, Atkinson R, Teague R, Antalffy B, Armstrong D, Arancio O, Sweatt JD, Zoghbi HY. Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J Neurosci. 2006;26: 319-327. https://doi.org/10.1523/JNEUROSCI.2623-05.2006
  97. Weng SM, McLeod F, Bailey ME, Cobb SR. Synaptic plasticity deficits in an experimental model of rett syndrome: long-term potentiation saturation and its pharmacological reversal. Neuroscience. 2011;180:314-321.
  98. Grabrucker AM, Schmeisser MJ, Schoen M, Boeckers TM. Postsynaptic ProSAP/Shank scaffolds in the cross-hair of synaptopathies. Trends Cell Biol. 2011;21:594-603. https://doi.org/10.1016/j.tcb.2011.07.003
  99. Boeckers TM, Bockmann J, Kreutz MR, Gundelfinger ED. ProSAP/Shank proteins - a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J Neurochem. 2002;81:903-910. https://doi.org/10.1046/j.1471-4159.2002.00931.x
  100. Durand CM, Betancur C, Boeckers TM, Bockmann J, Chaste P, Fauchereau F, Nygren G, Rastam M, Gillberg IC, Anckarsater H, Sponheim E, Goubran-Botros H, Delorme R, Chabane N, Mouren-Simeoni MC, de Mas P, Bieth E, Roge B, Heron D, Burglen L, Gillberg C, Leboyer M, Bourgeron T. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat Genet. 2007;39:25-27. https://doi.org/10.1038/ng1933
  101. Berkel S, Marshall CR, Weiss B, Howe J, Roeth R, Moog U, Endris V, Roberts W, Szatmari P, Pinto D, Bonin M, Riess A, Engels H, Sprengel R, Scherer SW, Rappold GA. Mutations in the SHANK2 synaptic scaffolding gene in autism spectrum disorder and mental retardation. Nat Genet. 2010;42:489-491. https://doi.org/10.1038/ng.589
  102. Pinto D, Pagnamenta AT, Klei L, Anney R, Merico D, Regan R, Conroy J, Magalhaes TR, Correia C, Abrahams BS, Almeida J, Bacchelli E, Bader GD, Bailey AJ, Baird G, Battaglia A, Berney T, Bolshakova N, Bölte S, Bolton PF, Bourgeron T, Brennan S, Brian J, Bryson SE, Carson AR, Casallo G, Casey J, Chung BH, Cochrane L, Corsello C, Crawford EL, Crossett A, Cytrynbaum C, Dawson G, de Jonge M, Delorme R, Drmic I, Duketis E, Duque F, Estes A, Farrar P, Fernandez BA, Folstein SE, Fombonne E, Freitag CM, Gilbert J, Gillberg C, Glessner JT, Goldberg J, Green A, Green J, Guter SJ, Hakonarson H, Heron EA, Hill M, Holt R, Howe JL, Hughes G, Hus V, Igliozzi R, Kim C, Klauck SM, Kolevzon A, Korvatska O, Kustanovich V, Lajonchere CM, Lamb JA, Laskawiec M, Leboyer M, Le Couteur A, Leventhal BL, Lionel AC, Liu XQ, Lord C, Lotspeich L, Lund SC, Maestrini E, Mahoney W, Mantoulan C, Marshall CR, McConachie H, McDougle CJ, McGrath J, McMahon WM, Merikangas A, Migita O, Minshew NJ, Mirza GK, Munson J, Nelson SF, Noakes C, Noor A, Nygren G, Oliveira G, Papanikolaou K, Parr JR, Parrini B, Paton T, Pickles A, Pilorge M, Piven J, Ponting CP, Posey DJ, Poustka A, Poustka F, Prasad A, Ragoussis J, Renshaw K, Rickaby J, Roberts W, Roeder K, Roge B, Rutter ML, Bierut LJ, Rice JP, Salt J, Sansom K, Sato D, Segurado R, Sequeira AF, Senman L, Shah N, Sheffield VC, Soorya L, Sousa I, Stein O, Sykes N, Stoppioni V, Strawbridge C, Tancredi R, Tansey K, Thiruvahindrapduram B, Thompson AP, Thomson S, Tryfon A, Tsiantis J, Van Engeland H, Vincent JB, Volkmar F, Wallace S, Wang K, Wang Z, Wassink TH, Webber C, Weksberg R, Wing K, Wittemeyer K, Wood S, Wu J, Yaspan BL, Zurawiecki D, Zwaigenbaum L, Buxbaum JD, Cantor RM, Cook EH, Coon H, Cuccaro ML, Devlin B, Ennis S, Gallagher L, Geschwind DH, Gill M, Haines JL, Hallmayer J, Miller J, Monaco AP, Nurnberger JI Jr, Paterson AD, Pericak-Vance MA, Schellenberg GD, Szatmari P, Vicente AM, Vieland VJ, Wijsman EM, Scherer SW, Sutcliffe JS, Betancur C. Functional impact of global rare copy number variation in autism spectrum disorders. Nature. 2010;466:368-372. https://doi.org/10.1038/nature09146
  103. Sato D, Lionel AC, Leblond CS, Prasad A, Pinto D, Walker S, O'Connor I, Russell C, Drmic IE, Hamdan FF, Michaud JL, Endris V, Roeth R, Delorme R, Huguet G, Leboyer M, Rastam M, Gillberg C, Lathrop M, Stavropoulos DJ, Anagnostou E, Weksberg R, Fombonne E, Zwaigenbaum L, Fernandez BA, Roberts W, Rappold GA, Marshall CR, Bourgeron T, Szatmari P, Scherer SW. SHANK1 Deletions in Males with Autism Spectrum Disorder. Am J Hum Genet. 2012;90:879-887. https://doi.org/10.1016/j.ajhg.2012.03.017
  104. Naisbitt S, Kim E, Tu JC, Xiao B, Sala C, Valtschanoff J, Weinberg RJ, Worley PF, Sheng M. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron. 1999; 23:569-582. https://doi.org/10.1016/S0896-6273(00)80809-0
  105. Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, Doan A, Aakalu VK, Lanahan AA, Sheng M, Worley PF. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron. 1999; 23:583-592. https://doi.org/10.1016/S0896-6273(00)80810-7
  106. Hung AY, Futai K, Sala C, Valtschanoff JG, Ryu J, Woodworth MA, Kidd FL, Sung CC, Miyakawa T, Bear MF, Weinberg RJ, Sheng M. Smaller dendritic spines, weaker synaptic transmission, but enhanced spatial learning in mice lacking Shank1. J Neurosci. 2008;28:1697-1708. https://doi.org/10.1523/JNEUROSCI.3032-07.2008
  107. Bozdagi O, Sakurai T, Papapetrou D, Wang X, Dickstein DL, Takahashi N, Kajiwara Y, Yang M, Katz AM, Scattoni ML, Harris MJ, Saxena R, Silverman JL, Crawley JN, Zhou Q, Hof PR, Buxbaum JD. Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction, and social communication. Mol Autism. 2010;1:15. https://doi.org/10.1186/2040-2392-1-15
  108. Peca J, Feliciano C, Ting JT, Wang W, Wells MF, Venkatraman TN, Lascola CD, Fu Z, Feng G. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature. 2011;472:437-442. https://doi.org/10.1038/nature09965
  109. Bangash MA, Park JM, Melnikova T, Wang D, Jeon SK, Lee D, Syeda S, Kim J, Kouser M, Schwartz J, Cui Y, Zhao X, Speed HE, Kee SE, Tu JC, Hu JH, Petralia RS, Linden DJ, Powell CM, Savonenko A, Xiao B, Worley PF. Enhanced polyubiquitination of Shank3 and NMDA receptor in a mouse model of autism. Cell. 2011;145:758-772. https://doi.org/10.1016/j.cell.2011.03.052
  110. Wang X, McCoy PA, Rodriguiz RM, Pan Y, Je HS, Roberts AC, Kim CJ, Berrios J, Colvin JS, Bousquet-Moore D, Lorenzo I, Wu G, Weinberg RJ, Ehlers MD, Philpot BD, Beaudet AL, Wetsel WC, Jiang YH. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum Mol Genet. 2011;20:3093-3108. https://doi.org/10.1093/hmg/ddr212
  111. Won H, Lee HR, Gee HY, Mah W, Kim JI, Lee J, Ha S, Chung C, Jung ES, Cho YS, Park SG, Lee JS, Lee K, Kim D, Bae YC, Kaang BK, Lee MG, Kim E. Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function. Nature. 2012;486:261-265. https://doi.org/10.1038/nature11208
  112. Schmeisser MJ, Ey E, Wegener S, Bockmann J, Stempel AV, Kuebler A, Janssen AL, Udvardi PT, Shiban E, Spilker C, Balschun D, Skryabin BV, Dieck St, Smalla KH, Montag D, Leblond CS, Faure P, Torquet N, Le Sourd AM, Toro R, Grabrucker AM, Shoichet SA, Schmitz D, Kreutz MR, Bourgeron T, Gundelfinger ED, Boeckers TM. Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/ Shank2. Nature. 2012;486:256-260.
  113. Moessner R, Marshall CR, Sutcliffe JS, Skaug J, Pinto D, Vincent J, Zwaigenbaum L, Fernandez B, Roberts W, Szatmari P, Scherer SW. Contribution of SHANK3 mutations to autism spectrum disorder. Am J Hum Genet. 2007;81: 1289-1297. https://doi.org/10.1086/522590
  114. Uchino S, Wada H, Honda S, Nakamura Y, Ondo Y, Uchiyama T, Tsutsumi M, Suzuki E, Hirasawa T, Kohsaka S. Direct interaction of post-synaptic density-95/Dlg/ZO-1 domain-containing synaptic molecule Shank3 with GluR1 alpha-amino- 3-hydroxy-5-methyl-4-isoxazole propionic acid receptor. J Neurochem. 2006;97:1203-1214. https://doi.org/10.1111/j.1471-4159.2006.03831.x
  115. Cho KK, Bear MF. Promoting neurological recovery of function via metaplasticity. Future Neurol. 2010;5:21-26. https://doi.org/10.2217/fnl.09.62
  116. Belger A, Carpenter KL, Yucel GH, Cleary KM, Donkers FC. The neural circuitry of autism. Neurotox Res. 2011;20:201-214. https://doi.org/10.1007/s12640-010-9234-7
  117. Pare D, Duvarci S. Amygdala microcircuits mediating fear expression and extinction. Curr Opin Neurobiol. 2012;22:717-723. https://doi.org/10.1016/j.conb.2012.02.014
  118. Sotres-Bayon F, Quirk GJ. Prefrontal control of fear: more than just extinction. Curr Opin Neurobiol. 2010;20:231-235. https://doi.org/10.1016/j.conb.2010.02.005
  119. Langen M, Durston S, Kas MJ, van Engeland H, Staal WG. The neurobiology of repetitive behavior: …and men. Neurosci Biobehav Rev. 2011;35:356-365. https://doi.org/10.1016/j.neubiorev.2010.02.005
  120. Langen M, Kas MJ, Staal WG, van Engeland H, Durston S. The neurobiology of repetitive behavior: of mice…. Neurosci Biobehav Rev. 2011;35:345-355. https://doi.org/10.1016/j.neubiorev.2010.02.004
  121. Kreitzer AC, Malenka RC. Striatal plasticity and basal ganglia circuit function. Neuron. 2008;60:543-554. https://doi.org/10.1016/j.neuron.2008.11.005
  122. Luscher C, Huber KM. Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron. 2010;65:445-459. https://doi.org/10.1016/j.neuron.2010.01.016
  123. Scattoni ML. Special interest section on mouse ultrasonic vocalizations. Genes Brain Behav. 2011;10:1-3. https://doi.org/10.1111/j.1601-183X.2010.00653.x
  124. Fischer J, Hammerschmidt K. Ultrasonic vocalizations in mouse models for speech and socio-cognitive disorders: insights into the evolution of vocal communication. Genes Brain Behav. 2011;10:17-27. https://doi.org/10.1111/j.1601-183X.2010.00610.x
  125. Rotschafer SE, Trujillo MS, Dansie LE, Ethell IM, Razak KA. Minocycline treatment reverses ultrasonic vocalization production deficit in a mouse model of Fragile X Syndrome. Brain Res. 2012;1439:7-14.
  126. Young DM, Schenk AK, Yang SB, Jan YN, Jan LY. Altered ultrasonic vocalizations in a tuberous sclerosis mouse model of autism. Proc Natl Acad Sci USA. 2010;107:11074-11079. https://doi.org/10.1073/pnas.1005620107
  127. De Filippis B, Ricceri L, Laviola G. Early postnatal behavioral changes in the Mecp2-308 truncation mouse model of Rett syndrome. Genes Brain Behav. 2010;9:213-223. https://doi.org/10.1111/j.1601-183X.2009.00551.x
  128. Wohr M, Roullet FI, Hung AY, Sheng M, Crawley JN. Communication impairments in mice lacking Shank1: reduced levels of ultrasonic vocalizations and scent marking behavior. PLoS One. 2011;6:e20631. https://doi.org/10.1371/journal.pone.0020631
  129. Van Daele DJ, Cassell MD. Multiple forebrain systems converge on motor neurons innervating the thyroarytenoid muscle. Neuroscience. 2009;162:501-524. https://doi.org/10.1016/j.neuroscience.2009.05.005
  130. Van Daele DJ, Fazan VP, Agassandian K, Cassell MD. Amygdala connections with jaw, tongue and laryngo-pharyngeal premotor neurons. Neuroscience. 2011;177:93-113.

Cited by

  1. Overview of Mouse Models of Autism Spectrum Disorders vol.66, pp.1, 2012, https://doi.org/10.1002/0471141755.ph0566s66
  2. Mutation of the CH1 Domain in the Histone Acetyltransferase CREBBP Results in Autism-Relevant Behaviors in Mice vol.11, pp.1, 2012, https://doi.org/10.1371/journal.pone.0146366
  3. Oxytocin as a Modulator of Synaptic Plasticity: Implications for Neurodevelopmental Disorders vol.10, pp.None, 2012, https://doi.org/10.3389/fnsyn.2018.00017
  4. Impact of Auditory Integration Therapy (AIT) on the Plasma Levels of Human Glial Cell Line-Derived Neurotrophic Factor (GDNF) in Autism Spectrum Disorder vol.68, pp.4, 2012, https://doi.org/10.1007/s12031-019-01332-w