An Early Postnatal Oxytocin Treatment Prevents Social and Learning Deficits in Adult Mice Deficient for Magel2, a Gene Involved in Prader-Willi Syndrome and Autism

Biological Psychiatry

Volumn 78, Issue 2, 2015, Pages 85-94

  Meziane, Hamid ^c   Schaller, Fabienne ^a,b   Bauer, Sylvian ^a,b   Villard, Claude ^d   Matarazzo, Valery ^a,b   Riet, Fabrice ^c   Guillon, Gilles ^e   Lafitte, Daniel ^d   Desarmenien, Michel G ^e   Tauber, Maithé ^f   Muscatelli, Françoise ^a,b  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c INSTITUT CLINIQUE DE LA SOURIS   (France)

^d Plateforme Protéomique et Innovation Technologique Timone   (France)

^e UNIV MONTPELLIER   (France)

^f HÔPITAL DES ENFANTS   (France)

Author keywords

Autism spectrum disorder; MAGEL2; Neurodevelopment; Oxytocin; Prader Willi syndrome; Therapy

Indexed keywords

MAGEL2 PROTEIN; MELANOMA ANTIGEN; OXYTOCIN; UNCLASSIFIED DRUG; MAGEL2 PROTEIN, MOUSE; PROTEIN; TUMOR ANTIGEN;

ADULT; ADULTHOOD; ANIMAL BEHAVIOR; ANIMAL MODEL; ARTICLE; AUTISM; BIRTH; BRAIN; CLINICAL ASSESSMENT; COGNITION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; FEMALE; GENE EXPRESSION; GENE MUTATION; LEARNING; LEARNING DISORDER; LONG TERM CARE; MALE; MOUSE; MUTANT MOUSE STRAIN; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRADER WILLI SYNDROME; PRIORITY JOURNAL; RECOGNITION; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SPATIAL LEARNING; WILD TYPE; ANIMAL; AUTISTIC DISORDER; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY; PRADER-WILLI SYNDROME; PSYCHOLOGY;

ANIMALS; ANTIGENS, NEOPLASM; AUTISTIC DISORDER; BRAIN; COGNITION; DISEASE MODELS, ANIMAL; FEMALE; MALE; MICE; MICE, INBRED C57BL; OXYTOCIN; PRADER-WILLI SYNDROME; PROTEINS; RECOGNITION (PSYCHOLOGY); SOCIAL BEHAVIOR; SPATIAL LEARNING;

EID: 84937600004     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.11.010     Document Type: Article

References (51)

1. T.R. Insel, and R.D. Fernald How the brain processes social information: Searching for the social brain Annu Rev Neurosci 27 2004 697 722
2. Z.R. Donaldson, and L.J. Young Oxytocin, vasopressin, and the neurogenetics of sociality Science 322 2008 900 904
3. H. Higashida, O. Lopatina, T. Yoshihara, Y.A. Pichugina, A.A. Soumarokov, T. Munesue, and et al. Oxytocin signal and social behavior: Comparison among adult and infant oxytocin, oxytocin receptor and CD38 gene knockout mice J Neuroendocrinol 22 2010 373 379
4. H.J. Lee, H.K. Caldwell, A.H. Macbeth, and W.S. Young 3rd Behavioral studies using temporal and spatial inactivation of the oxytocin receptor Prog Brain Res 170 2008 73 77
5. M. Sala, D. Braida, D. Lentini, M. Busnelli, E. Bulgheroni, V. Capurro, and et al. Pharmacologic rescue of impaired cognitive flexibility, social deficits, increased aggression, and seizure susceptibility in oxytocin receptor null mice: A neurobehavioral model of autism Biol Psychiatry 69 2011 875 882
6. M.E. Modi, and L.J. Young The oxytocin system in drug discovery for autism: Animal models and novel therapeutic strategies Horm Behav 61 2012 340 350
7. H. Harony, and S. Wagner The contribution of oxytocin and vasopressin to mammalian social behavior: Potential role in autism spectrum disorder Neurosignals 18 2010 82 97
8. C.F. Zink, and A. Meyer-Lindenberg Human neuroimaging of oxytocin and vasopressin in social cognition Horm Behav 61 2012 400 409
9. R.P. Ebstein, A. Knafo, D. Mankuta, S.H. Chew, and P.S. Lai The contributions of oxytocin and vasopressin pathway genes to human behavior Horm Behav 61 2012 359 379
10. Y. Aoki, N. Yahata, T. Watanabe, Y. Takano, Y. Kawakubo, H. Kuwabara, and et al. Oxytocin improves behavioral and neural deficits in inferring others' social emotions in autism Brain 137 2014 3073 3086
11. G. Miller Neuroscience. The promise and perils of oxytocin Science 339 2013 267 269
12. A.P. Goldstone, A.J. Holland, B.P. Hauffa, A.C. Hokken-Koelega, and M. Tauber Recommendations for the diagnosis and management of Prader-Willi syndrome J Clin Endocrinol Metab 93 2008 4183 4197
13. S.B. Cassidy, S. Schwartz, J.L. Miller, and D.J. Driscoll Prader-Willi syndrome Genet Med 14 2012 10 26
14. M.G. Butler Prader-Willi Syndrome: Obesity due to genomic imprinting Curr Genomics 12 2011 204 215
15. C.J. McAllister, J.E. Whittington, and A.J. Holland Development of the eating behavior in Prader-Willi Syndrome: Advances in our understanding Int J Obes (Lond) 35 2011 188 197
16. E.M. Dykens, E. Lee, and E. Roof Prader-Willi syndrome and autism spectrum disorders: An evolving story J Neurodev Disord 3 2011 225 237
17. N. Bachere, G. Diene, V. Delagnes, C. Molinas, P. Moulin, and M. Tauber Early diagnosis and multidisciplinary care reduce the hospitalization time and duration of tube feeding and prevent early obesity in PWS infants Horm Res 69 2008 45 52
18. J.V. Butler, J.E. Whittington, A.J. Holland, C.J. McAllister, and A.P. Goldstone The transition between the phenotypes of Prader-Willi syndrome during infancy and early childhood Dev Med Child Neurol 52 2010 e88 e93
19. J.L. Miller, C.H. Lynn, D.C. Driscoll, A.P. Goldstone, J.A. Gold, V. Kimonis, and et al. Nutritional phases in Prader-Willi syndrome Am J Med Genet A 155A 2011 1040 1049
20. A.Y. Ho, and A. Dimitropoulos Clinical management of behavioral characteristics of Prader-Willi syndrome Neuropsychiatr Dis Treat 6 2010 107 118
21. A.J. Holland, J.E. Whittington, J. Butler, T. Webb, H. Boer, and D. Clarke Behavioral phenotypes associated with specific genetic disorders: Evidence from a population-based study of people with Prader-Willi syndrome Psychol Med 33 2003 141 153
22. N. Greaves, E. Prince, D.W. Evans, and T. Charman Repetitive and ritualistic behavior in children with Prader-Willi syndrome and children with autism J Intellect Disabil Res 50 2006 92 100
23. K. Koenig, A. Klin, and R. Schultz Deficits in social attribution ability in Prader-Willi syndrome J Autism Dev Disord 34 2004 573 582
24. A. Dimitropoulos, A. Ho, and B. Feldman Social responsiveness and competence in Prader-Willi Syndrome: Direct comparison to autism spectrum disorder J Autism Dev Disord 43 2013 103 113
25. C.P. Schaaf, M.L. Gonzalez-Garay, F. Xia, L. Potocki, K.W. Gripp, B. Zhang, and et al. Truncating mutations of MAGEL2 cause Prader-Willi phenotypes and autism Nat Genet 45 2013 1405 1408
26. D.F. Swaab Prader-Willi syndrome and the hypothalamus Acta Paediatr Suppl 423 1997 50 54
27. I. Boccaccio, H. Glatt-Deeley, F. Watrin, N. Roeckel, M. Lalande, and F. Muscatelli The human MAGEL2 gene and its mouse homologue are paternally expressed and mapped to the Prader-Willi region Hum Mol Genet 8 1999 2497 2505
28. S. Lee, S. Kozlov, L. Hernandez, S.J. Chamberlain, C.I. Brannan, C.L. Stewart, and et al. Expression and imprinting of MAGEL2 suggest a role in Prader-Willi syndrome and the homologous murine imprinting phenotype Hum Mol Genet 9 2000 1813 1819
29. S. Lee, C.L. Walker, and R. Wevrick Prader-Willi syndrome transcripts are expressed in phenotypically significant regions of the developing mouse brain Gene Expr Patterns 3 2003 599 609
30. S.V. Kozlov, J.W. Bogenpohl, M.P. Howell, R. Wevrick, S. Panda, J.B. Hogenesch, and et al. The imprinted gene Magel2 regulates normal circadian output Nat Genet 39 2007 1266 1272
31. F. Schaller, F. Watrin, R. Sturny, A. Massacrier, P. Szepetowski, and F. Muscatelli A single postnatal injection of oxytocin rescues the lethal feeding behavior in mouse newborns deficient for the imprinted Magel2 gene Hum Mol Genet 19 2010 4895 4905
32. National Research Council Committee (2011): Guide for the Care and Use of Laboratory Animals, 8th ed. Washington, DC: The National Academic Press.
33. Y. Ben-Barak, J.T. Russell, M.H. Whitnall, K. Ozato, and H. Gainer Neurophysin in the hypothalamo-neurohypophysial system. I. Production and characterization of monoclonal antibodies J Neurosci 5 1985 81 97
34. M. Altstein, M.H. Whitnall, S. House, S. Key, and H. Gainer An immunochemical analysis of oxytocin and vasopressin prohormone processing in vivo Peptides 9 1988 87 105
35. M. Andres, A. Pena, S. Derick, D. Raufaste, J. Trojnar, K. Wisniewski, and et al. Comparative pharmacology of bovine, human and rat vasopressin receptor isoforms Eur J Pharmacol 501 2004 59 69
36. M. Sala, D. Braida, A. Donzelli, R. Martucci, M. Busnelli, E. Bulgheroni, and et al. Mice heterozygous for the oxytocin receptor gene (Oxtr(+/-)) show impaired social behavior but not increased aggression or cognitive inflexibility: Evidence of a selective haploinsufficiency gene effect J Neuroendocrinol 25 2013 107 118
37. H.S. Knobloch, A. Charlet, L.C. Hoffmann, M. Eliava, S. Khrulev, A.H. Cetin, and et al. Evoked axonal oxytocin release in the central amygdala attenuates fear response Neuron 73 2012 553 566
38. C.S. Carter Oxytocin pathways and the evolution of human behavior Annu Rev Psychol 65 2014 17 39
39. I.F. Bielsky, S.B. Hu, X. Ren, E.F. Terwilliger, and L.J. Young The V1a vasopressin receptor is necessary and sufficient for normal social recognition: A gene replacement study Neuron 47 2005 503 513
40. Y.F. Guzman, N.C. Tronson, V. Jovasevic, K. Sato, A.L. Guedea, H. Mizukami, and et al. Fear-enhancing effects of septal oxytocin receptors Nat Neurosci 16 2013 1185 1187
41. Y. Yamamoto, B.S. Cushing, K.M. Kramer, P.D. Epperson, G.E. Hoffman, and C.S. Carter Neonatal manipulations of oxytocin alter expression of oxytocin and vasopressin immunoreactive cells in the paraventricular nucleus of the hypothalamus in a gender-specific manner Neuroscience 125 2004 947 955
42. K.L. Bales, P.M. Plotsky, L.J. Young, M.M. Lim, N. Grotte, E. Ferrer, and C.S. Carter Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors Neuroscience 144 2007 38 45
43. Y. Takayanagi, M. Yoshida, I.F. Bielsky, H.E. Ross, M. Kawamata, T. Onaka, and et al. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice Proc Natl Acad Sci U S A 102 2005 16096 16101
44. J.N. Ferguson, L.J. Young, E.F. Hearn, M.M. Matzuk, T.R. Insel, and J.T. Winslow Social amnesia in mice lacking the oxytocin gene Nat Genet 25 2000 284 288
45. S. Jacob, C.W. Brune, C.S. Carter, B.L. Leventhal, C. Lord, and E.H. Cook Jr Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism Neurosci Lett 417 2007 6 9
46. J.L. Silverman, M. Yang, S.M. Turner, A.M. Katz, D.B. Bell, J.I. Koenig, and J.N. Crawley Low stress reactivity and neuroendocrine factors in the BTBR T+tf/J mouse model of autism Neuroscience 171 2010 1197 1208
47. S.M. Francis, A. Sagar, T. Levin-Decanini, W. Liu, C.S. Carter, and S. Jacob Oxytocin and vasopressin systems in genetic syndromes and neurodevelopmental disorders Brain Res 1580 2014 199 218
48. A. Martin, M. State, K. Koenig, R. Schultz, E.M. Dykens, S.B. Cassidy, and J.F. Leckman Prader-Willi syndrome [clinical conference] Am J Psychiatry 155 1998 1265 1273
49. R. Tyzio, R. Nardou, D.C. Ferrari, T. Tsintsadze, A. Shahrokhi, S. Eftekhari, and et al. Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring Science 343 2014 675 679
50. V. Chevaleyre, F.C. Moos, and M.G. Desarmenien Correlation between electrophysiological and morphological characteristics during maturation of rat supraoptic neurons Eur J Neurosci 13 2001 1136 1146
51. V. Chevaleyre, G. Dayanithi, F.C. Moos, and M.G. Desarmenien Developmental regulation of a local positive autocontrol of supraoptic neurons J Neurosci 20 2000 5813 5819