Repetitive behaviors in the Shank1 knockout mouse model for autism spectrum disorder: Developmental aspects and effects of social context

Journal of Neuroscience Methods

Volumn 234, Issue , 2014, Pages 92-100

  Sungur, A Özge ^a   Vörckel, Karl J ^a   Schwarting, Rainer K W ^a   Wöhr, Markus ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Animal model; Marble burying; Neurodevelopmental disorders; Postsynaptic density; Repetitive behavior; Self grooming

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; COMPULSION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; GENE; GENE DELETION; GENOTYPE; GROOMING; HETEROZYGOTE; JUVENILE; KNOCKOUT MOUSE; LOCOMOTION; MARBLE BURYING TEST; MOUSE; MUTANT; NONHUMAN; ODOR; PRIORITY JOURNAL; REARING; SHANK1 GENE; SOCIAL ENVIRONMENT; WILD TYPE; AGE; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; GENETICS; NEWBORN; PATHOPHYSIOLOGY; PHYSIOLOGY; SOCIAL BEHAVIOR; STEREOTYPY; TIME; TRANSGENIC MOUSE;

NERVE PROTEIN; SHANK1 PROTEIN, MOUSE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CHILD DEVELOPMENT DISORDERS, PERVASIVE; DISEASE MODELS, ANIMAL; GENOTYPE; GROOMING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; SOCIAL BEHAVIOR; STEREOTYPED BEHAVIOR; TIME FACTORS;

EID: 84905381699     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2014.05.003     Document Type: Article

References (70)

1. Abrahams B.S., Geschwind D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 2008, 9:341-355.
2. American Psychiatric Association Diagnostic and statistical manual of mental disorders 2013, American Psychiatric Publishing, Arlington, VA. 5th ed.
3. Arakawa H., Blanchard D.C., Arakawa K., Dunlap C., Blanchard R.J. Scent marking behavior as an odorant communication in mice. Neurosci Biobehav Rev 2008, 32:1236-1248.
4. Asendorpf J. Nichtreaktive Stressmessung Bewegungsstereotypien als Aktivierungsindikatoren. Z Exp Angew Psychol 1980, 27:44-58.
5. Baron-Cohen S. Do autistic children have obsessions and compulsions. Br J Clin Psychol 1989, 28:193-200.
6. Berkel S., Marshall C.R., Weiss B., Howe J., Roeth R., Moog U., et al. Mutations in the SHANK2 synaptic scaffolding gene in autism spectrum disorder and mental retardation. Nat Genet 2010, 42:489-491.
7. Bienvenu O.J., Wang Y., Shugart Y.Y., Welch J.M., Grados M.A., Fyer A.J., et al. Sapap3 and pathological grooming in humans: results from the OCD collaborative genetics study. Am J Med Genet B Neuropsychiatr Genet 2009, 150B:710-720.
8. Bishop S.L., Lahvis G.P. The autism diagnosis in translation: shared affect in children and mouse models of ASD. Autism Res 2011, 4:317-335.
9. Boccuto L., Lauri M., Sarasua S.M., Skinner C.D., Buccella D., Dwivedi A., et al. Prevalence of SHANK3 variants in patients with different subtypes of autism spectrum disorders. Eur J Hum Genet 2013, 21:310-316.
10. Carruthers P. Autism as mind-blindness: an elaboration and partial defence. Theories of theories of mind 1996, 257-273. Cambridge University Press, Cambridge. P. Carruthers, P.K. Smith (Eds.).
11. Dhar S.U., del Gaudio D., German J.R., Peters S.U., Ou Z., Bader P.I., et al. 22q13.3 deletion syndrome: clinical and molecular analysis using array CGH. Am J Med Genet A 2010, 152:573-581.
12. Dizinno G., Whitney G., Nyby J. Ultrasonic vocalizations by male mice (Mus musculus) to female sex pheromone: experimental determinants. Behav Biol 1978, 22:104-113.
13. Drapeau E., Dorr N.P., Elder G.A., Buxbaum J.D. Absence of strong strain effects in behavioral analyses of Shank3-deficient mice. Dis Model Mech 2014, [in press].
14. Durand C.M., Betancur C., Boeckers T.M., Bockmann J., Chaste P., Fauchereau F., et al. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat Genet 2007, 39:25-27.
15. Ebert D.H., Greenberg M.E. Activity-dependent neuronal signalling and autism spectrum disorder. Nature 2013, 493:327-337.
16. Ecker C., Spooren W., Murphy D.G. Translational approaches to the biology of autism: false dawn or a new era. Mol Psychiatry 2013, 18:435-442.
17. Folstein S., Rutter M. Genetic influences and infantile autism. Nature 1977, 265:726-728.
18. Gauthier J., Spiegelman D., Piton A., Lafrenière R.G., Laurent S., St-Onge J., et al. Novel de novo SHANK3 mutation in autistic patients. Am J Med Genet B Neuropsychiatr Genet 2009, 150:421-424.
19. Gauthier J., Champagne N., Lafrenière R.G., Xiong L., Spiegelman D., Brustein E., et al. De novo mutations in the gene encoding the synaptic scaffolding protein SHANK3 in patients ascertained for schizophrenia. Proc Natl Acad Sci USA 2010, 107:7863-7868. S2D Team.
20. Gong X., Jiang Y.W., Zhang X., An Y., Zhang J., Wu Y., et al. High proportion of 22q13 deletions and SHANK3 mutations in Chinese patients with intellectual disability. PLoS One 2012, 7:e34739.
21. Grabrucker A.M., Schmeisser M.J., Schoen M., Boeckers T.M. Postsynaptic ProSAP/Shank scaffolds in the cross-hair of synaptopathies. Trends Cell Biol 2011, 21:594-603.
22. Guilmatre A., Huguet G., Delorme R., Bourgeron T. The emerging role of SHANK genes in neuropsychiatric disorders. Dev Neurobiol 2014, 74:113-122.
23. Guo Z., Holy T.E. Sex selectivity of mouse ultrasonic songs. Chem Senses 2007, 23:463-473.
24. Hammerschmidt K., Radyushkin K., Ehrenreich H., Fischer J. Female mice respond to male ultrasonic 'songs' with approach behaviour. Biol Lett 2009, 5:589-592.
25. Han K., Holder J.L., Schaaf C.P., Lu H., Chen H., Kang H., et al. SHANK3 overexpression causes manic-like behaviour with unique pharmacogenetic properties. Nature 2013, 503:72-77.
26. Hung A.Y., Futai K., Sala C., Valtschanoff J.G., Ryu J., Woodworth M.A., et al. Smaller dendritic spines, weaker synaptic transmission, but enhanced spatial learning in mice lacking Shank1. J Neurosci 2008, 28:1697-1708.
27. Jiang Y.H., Ehlers M.D. Modeling autism by SHANK gene mutations in mice. Neuron 2013, 78:8-27.
28. Jones R.M., Lord C. Diagnosing autism in neurobiological research studies. Behav Brain Res 2013, 251:113-124.
29. Kim E., Sheng M. PDZ domain proteins of synapses. Nat Rev Neurosci 2004, 5:771-781.
30. Kreienkamp H.J. Scaffolding proteins at the postsynaptic density: shank as the architectural framework. Handb Exp Pharmacol 2008, 365-380.
31. Kouser M., Speed H.E., Dewey C.M., Reimers J.M., Widman A.J., Gupta N., et al. Loss of predominant shank3 isoforms results in hippocampus-dependent impairments in behavior and synaptic transmission. J Neurosci 2013, 33:18448-18468.
32. Leblond C.S., Heinrich J., Delorme R., Proepper C., Betancur C., Huguet G., et al. Genetic and functional analyses of SHANK2 mutations suggest a multiple hit model of autism spectrum disorders. PLoS Genet 2012, 8:e1002521.
33. Maggio J.C., Maggio J.H., Whitney G. Experience-based vocalization of male mice to female chemosignals. Physiol Behav 1983, 31:269-272.
34. Marshall C.R., Noor A., Vincent J.B., Lionel A.C., Feuk L., Skaug J., et al. Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet 2008, 82:477-488.
35. McFarlane H.G., Kusek G.K., Yang M., Phoenix J.L., Bolivar V.J., Crawley J.N. Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav 2008, 7:152-163.
36. Moessner R., Marshall C.R., Sutcliffe J.S., Skaug J., Pinto D., Vincent J., et al. Contribution of SHANK3 mutations to autism spectrum disorder. Am J Hum Genet 2007, 81:1289-1297.
37. Moy S.S., Riddick N.V., Nikolova V.D., Teng B.L., Agster K.L., Nonneman R.J., et al. Repetitive behavior profile and supersensitivity to amphetamine in the C58/J mouse model of autism. Behav Brain Res 2014, 259:200-214.
38. Muehlmann A.M., Edington G., Mihalik A.C., Buchwald Z., Koppuzha D., Korah M., et al. Further characterization of repetitive behavior in C58 mice: developmental trajectory and effects of environmental enrichment. Behav Brain Res 2012, 235:143-149.
39. Murphy D., Spooren W. EU-AIMS: a boost to autism research. Nat Rev Drug Discov 2012, 11:815-816.
40. Nyby J., Bigelow J., Kerchner M., Barbehenn F. Male mouse (Mus musculus) ultrasonic vocalizations to female urine: why is heterosexual experience necessary. Behav Neural Biol 1983, 38:32-46.
41. Peça J., Feliciano C., Ting J.T., Wang W., Wells M.F., Venkatraman T.N., et al. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 2011, 472:437-442.
42. Phelan M.C. Deletion 22q13.3 syndrome. Orphanet J Rare Dis 2008, 3:14.
43. Pinto D., Pagnamenta A.T., Klei L., Anney R., Merico D., Regan R., et al. Functional impact of global rare copy number variation in autism spectrum disorders. Nature 2010, 466:368-372.
44. Pomerantz S.M., Nunez A.A., Bean N.J. Female behavior is affected by male ultrasonic vocalizations in house mice. Physiol Behav 1983, 31:91-96.
45. Posthuma D., Polderman T.J. What have we learned from recent twin studies about the etiology of neurodevelopmental disorders. Curr Opin Neurol 2013, 26:111-121.
46. Roullet F.I., Wöhr M., Crawley J.N. Female urine-induced male mice ultrasonic vocalizations, but not scent-marking, is modulated by social experience. Behav Brain Res 2011, 216:19-28.
47. Ryan B.C., Young N.B., Crawley J.N., Bodfish J.W., Moy S.S. Social deficits, stereotypy and early emergence of repetitive behavior in the C58/J inbred mouse strain. Behav Brain Res 2010, 208:178-188.
48. Sato D., Lionel A.C., Leblond C.S., Prasad A., Pinto D., Walker S., et al. SHANK1 deletions in males with autism spectrum disorder. Am J Hum Genet 2012, 90:879-887.
49. Schaaf C.P., Sabo A., Sakai Y., Crosby J., Muzny D., Hawes A., et al. Oligogenic heterozygosity in individuals with high-functioning autism spectrum disorders. Hum Mol Genet 2011, 20:3366-3375.
50. Schmeisser M.J., Ey E., Wegener S., Bockmann J., Stempel A.V., Kuebler A., et al. Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature 2012, 486:256-260.
51. Sheng M., Kim E. The Shank family of scaffold proteins. J Cell Sci 2000, 113:1851-1856.
52. Silverman J.L., Turner S.M., Barkan C.L., Tolu S.S., Saxena R., Hung A.Y., et al. Sociability and motor functions in Shank1 mutant mice. Brain Res 2011, 1380:120-137.
53. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 2010, 11:490-502.
54. Sipos M.L., Kerchner M., Nyby J.G. An ephemeral sex pheromone in the urine of female house mice (Mus domesticus). Behav Neural Biol 1992, 58:138-143.
55. Sipos M.L., Wysocki C.J., Nyby J.G., Wysocki L., Nemura T.A. An ephemeral pheromone of female house mice: perception via the main and accessory olfactory systems. Physiol Behav 1995, 58:529-534.
56. State M.W. The genetics of child psychiatric disorders: focus on autism and Tourette syndrome. Neuron 2010, 68:254-269.
57. Thomas A., Burant A., Bui N., Graham D., Yuva-Paylor L.A., Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl) 2009, 204:361-373.
58. Ting J.T., Peça J., Feng G. Functional consequences of mutations in postsynaptic scaffolding proteins and relevance to psychiatric disorders. Annu Rev Neurosci 2012, 35:49-71.
59. Toro R., Konyukh M., Delorme R., Leblond C., Chaste P., Fauchereau F., et al. Key role for gene dosage and synaptic homeostasis in autism spectrum disorders. Trends Genet 2010, 26:363-372.
60. Turner M. Annotation: repetitive behavior in autism: a review of psychological research. J Child Psychol Psychiatry 1999, 40:839-849.
61. Waga C., Okamoto N., Ondo Y., Fukumura-Kato R., Goto Y., Kohsaka S., et al. Novel variants of the SHANK3 gene in Japanese autistic patients with severe delayed speech development. Psychiatr Genet 2011, 21:208-211.
62. Wang X., McCoy P.A., Rodriguiz R.M., Pan Y., Je H.S., Roberts A.C., et al. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum Mol Genet 2011, 20:3093-3108.
63. Welch J.M., Lu J., Rodriguiz R.M., Trotta N.C., Peca J., Ding J.D., et al. Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice. Nature 2007, 448:894-900.
64. Wilson H.L., Wong A.C., Shaw S.R., Tse W.Y., Stapleton G.A., Phelan M.C., et al. Molecular characterisation of the 22q13 deletion syndrome supports the role of haploinsufficiency of SHANK3/PROSAP2 in the major neurological symptoms. J Med Genet 2003, 40:575-584.
65. Wöhr M. Ultrasonic vocalizations in Shank mouse models for autism spectrum disorders: detailed spectrographic analyses and developmental profiles. Neurosci Biobehav Rev 2014, 43:199-212.
66. Wöhr M., Roullet F.I., Hung A.Y., Sheng M., Crawley J.N. Communication impairments in mice lacking Shank1: reduced levels of ultrasonic vocalizations and scent marking behavior. PLoS One 2011, 6:e20631.
67. Wöhr M., Scattoni M.L. Behavioural methods used in rodent models of autism spectrum disorders: current standards and new developments. Behav Brain Res 2013, 251:5-17.
68. Won H., Lee H.R., Gee H.Y., Mah W., Kim J.I., Lee J., et al. Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function. Nature 2012, 486:261-265.
69. Yang M., Bozdagi O., Scattoni M.L., Wöhr M., Roullet F.I., Katz A.M., et al. Reduced excitatory neurotransmission and mild autism-relevant phenotypes in adolescent Shank3 null mutant mice. J Neurosci 2012, 32:6525-6541.
70. Yoo J., Bakes J., Bradley C., Collingridge G.L., Kaang B.K. Shank mutant mice as an animal model of autism. Philos Trans R Soc Lond B Biol Sci 2013, 369:20130143.