Effects of advanced paternal age on trajectories of social behavior in offspring

Genes, Brain and Behavior

Volumn 14, Issue 6, 2015, Pages 443-453

  Janecka, M ^a   Manduca, A ^b   Servadio, M ^b   Trezza, V ^b   Smith, R ^a   Mill, J ^a,c   Schalkwyk, L C ^a,d   Reichenberg, A ^e,f   Fernandes, C ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b ROMA TRE UNIVERSITY   (Italy)

^c UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

^d UNIVERSITY OF ESSEX   (United Kingdom)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

De novo mutations; Environmental effects; Epidemiology; Mouse models; Neurodevelopment autism; Neuroligin; Paternal age effects; Psychiatry; Schizophrenia; Social behavior

Indexed keywords

ADULT; ADULTHOOD; ADVANCED PATERNAL AGE; AGED; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR ASSESSMENT; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NONHUMAN; PATERNAL AGE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROGENY; SEX DIFFERENCE; SOCIAL BEHAVIOR; VERY ELDERLY; YOUNG ADULT; ANIMAL; ANIMAL BEHAVIOR; ANIMAL MODEL; C57BL MOUSE; PARENT; PHYSIOLOGY; REPRODUCTION;

MUS; RODENTIA;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; MALE; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; PARENTS; PATERNAL AGE; REPRODUCTION; SOCIAL BEHAVIOR;

EID: 84937708935     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12227     Document Type: Article

References (39)

1. Croen, L., Najjar, D.V., Fireman, B. & Grether, J.K. (2007) Maternal and paternal age and risk of autism spectrum disorders. Arch Pediatr Adolesc Med 161, 334-340. DOI:10.1001/archpedi.161.4.334.
2. Dolores, M., Keller, A., Antonius, D., Perrin, M., Opler, M., Ahn, H., Kleinhaus, K., Messinger, J., Goetz, R. & Harlap, S. (2012) Advanced paternal age contributes to a specific subtype of schizophrenia. Schizophr Res 136, S3.
3. D'Onofrio, B.M., Rickert, M.E., Frans, E., Kuja-Halkola, R., Almqvist, C., Sjölander, A., Larsson, H. & Lichtenstein, P. (2014) Paternal age at childbearing and offspring psychiatric and academic morbidity. JAMA Psychiatry 71, 432-438. DOI:10.1001/jamapsychiatry.2013.4525.
4. Flatscher-Bader, T., Foldi, C.J., Chong, S., Whitelaw, E., Moser, R.J., Burne, T.H.J., Eyles, D.W. & McGrath, J.J. (2011) Increased de novo copy number variants in the offspring of older males. Transl Psychiatry 1, e34. DOI:10.1038/tp.2011.30.
5. Foldi, C.J., Eyles, D.W., McGrath, J.J. & Burne, T.H.J. (2010) Advanced paternal age is associated with alterations in discrete behavioural domains and cortical neuroanatomy of C57BL/6J mice. Eur J Neurosci 31, 556-564. DOI:10.1111/j.1460-9568.2010.07074.x.
6. Fournier, K., Hass, C.J., Naik, S.K., Lodha, N. & Cauraugh, J.H. (2010) Motor coordination in autism spectrum disorders: a synthesis and meta-analysis. J Autism Dev Disord 40, 1227-1240. DOI:10.1007/s10803-010-0981-3.
7. Frans, E.M., Sandin, S., Reichenberg, A., Lichtenstein, P., Långström, N. & Hultman, C.M. (2008) Advancing paternal age and bipolar disorder. Arch Gen Psychiatry 65, 1034-1040. DOI:10.1001/archpsyc.65.9.1034.
8. Gockley, J., Willsey, A.J., Dong, S., Dougherty, J.D., Constantino, J.N. & Sanders, S.J. (2015) The female protective effect in autism spectrum disorder is not mediated by a single genetic locus. Mol Autism 6, 1-10. DOI:10.1186/s13229-015-0014-3.
9. Jacquemont, S., Coe, B.P., Hersch, M., Duyzend, M.H., Krumm, N., Bergmann, S., Beckmann, J.S., Rosenfeld, J.A. & Eichler, E. (2014) A higher mutational burden in females supports a "female protective model" in neurodevelopmental disorders. Am J Hum Genet 94, 415-425. DOI:10.1016/j.ajhg.2014.02.001.
10. Jaffe, A.E., Gao, Y., & Tao, R. (2014) The methylome of the human frontal cortex across development. doi: 10.1101/005504
11. Kong, A., Frigge, M.L., Masson, G., Besenbacher, S., Sulem, P., Magnusson, G., Gudjonsson, S.A. et al. (2012) Rate of de novo mutations and the importance of father's age to disease risk. Nature 488, 471-475. DOI:10.1038/nature11396.
12. Lad, H.V., Liu, L., Paya-Cano, J.L., Parsons, M.J., Kember, R., Fernandes, C. & Schalkwyk, L.C. (2010) Behavioural battery testing: evaluation and behavioural outcomes in 8 inbred mouse strains. Physiol Behav 99, 301-316. DOI:10.1016/j.physbeh.2009.11.007.
13. Lai, M.-C., Lombardo, M.V., Pasco, G., Ruigrok, A.N.V., Wheelwright, S.J., Sadek, S.A., Chakrabarti, B. & Baron-Cohen, S. (2011) A behavioral comparison of male and female adults with high functioning autism spectrum conditions. PLoS One 6, e20835. DOI:10.1371/journal.pone.0020835.
14. Lai, M.-C., Baron-Cohen, S. & Buxbaum, J.D. (2015) Understanding autism in the light of sex/gender. Mol Autism 6, 1-5. DOI:10.1186/s13229-015-0021-4.
15. Life span as a biomarker. (2011). The Jackson Laboratory. URL http://research.jax.org/faculty/harrison/ger1vLifespan1.html#VD
16. Lord, C., Rutter, M.L., Goode, S., Heemsbergen, J., Jordan, H., Mawhood, L. & Schopler, E. (1989) Autism diagnostic observation schedule: a standardized observation of communicative and social behavior. J Autism Dev Disord 19, 185-212.
17. Lord, C., Rutter, M. & Le Couteur, A. (1994) Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24, 659-685.
18. Malaspina, D. (2001) Paternal factors and schizophrenia risk: de novo mutations and imprinting. Schizophr Bull 27, 379-393.
19. Markham, J. (2012) Sex steroids and schizophrenia. Rev Endocr Metab Disord 13, 187-207. DOI:10.1007/s11154-011-9184-2.
20. Matson, J.L. & Wilkins, J. (2007) A critical review of assessment targets and methods for social skills excesses and deficits for children with autism spectrum disorders. Res Autism Spect Disord 1, 28-37. DOI:10.1016/j.rasd.2006.07.003.
21. Milekic, M.H., Xin, Y., O'Donnell, A., Kumar, K.K., Bradley-Moore, M., Malaspina, D., Moore, H., Brunner, D., Ge, Y., Edwards, J., Paul, S., Haghighi, F.G. & Gingrich, J.A. (2014) Age-related sperm DNA methylation changes are transmitted to offspring and associated with abnormal behavior and dysregulated gene expression. Mol Psychiatry January, 1-7. DOI:10.1038/mp.2014.84.
22. Miller, B., Suvisaari, J., Miettunen, J., Järvelin, M.-R., Haukka, J., Tanskanen, A., Lönnqvist, J., Isohanni, M. & Kirkpatrick, B. (2011) Advanced paternal age and parental history of schizophrenia. Schizophr Res 133, 125-132. DOI:10.1016/j.schres.2011.08.013.
23. Numata, S., Ye, T., Hyde, T.M., Guitart-Navarro, X., Tao, R., Wininger, M., Colantuoni, C., Weinberger, D.R., Kleinman, J.E. & Lipska, B.K. (2012) DNA methylation signatures in development and aging of the human prefrontal cortex. Am J Hum Genet 90, 260-272. DOI:10.1016/j.ajhg.2011.12.020.
24. Perrin, M.C., Brown, A.S. & Malaspina, D. (2007) Aberrant epigenetic regulation could explain the relationship of paternal age to schizophrenia. Schizophr Bull 33, 1270-1273. DOI:10.1093/schbul/sbm093.
25. Petersen, L., Mortensen, P.B. & Pedersen, C.B. (2011) Paternal age at birth of first child and risk of schizophrenia. Am J Psychiatry 168, 82-88. DOI:10.1176/appi.ajp.2010.10020252.
26. Rapoport, J.L., Giedd, J.N. & Gogtay, N. (2012) Neurodevelopmental model of schizophrenia: update 2012. Mol Psychiatry 17, 1228-1238. DOI:10.1038/mp.2012.23.
27. Reichenberg, A., Gross, R., Weiser, M., Bresnahan, M., Silverman, J., Harlap, S., Rabinowitz, J., Shulman, C., Malaspina, D., Lubin, G., Knobler, H., Davidson, M. & Susser, E. (2006) Advancing paternal age and autism. Arch Gen Psychiatry 63, 1026-1032. DOI:10.1001/archpsyc.63.9.1026.
28. Robinson, E.B., Lichtenstein, P., Anckarsäter, H., Happé, F. & Ronald, A. (2013) Examining and interpreting the female protective effect against autistic behavior. Proc Natl Acad Sci U S A 110, 5258-5262. DOI:10.1073/pnas.1211070110.
29. Rumsey, J., Rapoport, J. & Sceery, W. (1985) Autistic children as adults: psychiatric, social and behavioral outcomes. J Am Acad Child Psychiatry 24, 465-473.
30. Sampino, S., Juszczak, G.R., Zacchini, F., Swiergiel, A.H., Modlinski, J.A., Loi, P. & Ptak, G.E. (2014) Grand-paternal age and the development of autism-like symptoms in mice progeny. Transl Psychiatry 4, e386. DOI:10.1038/tp.2014.27.
31. Schneider, M. & Koch, M. (2005) Behavioral and morphological alterations following neonatal excitotoxic lesions of the medial prefrontal cortex in rats. Exp Neurol 195, 185-198. DOI:10.1016/j.expneurol.2005.04.014.
32. Schwartz, B.L., Rosse, R.B., Veazey, C. & Deutsch, S.I. (1996) Impaired motor skill learning in schizophrenia: Implications for corticostriatal dysfunction. Biol Psychiatry 39, 241-248. DOI:10.1016/0006-3223(95)00130-1.
33. Smith, R.G., Kember, R.L., Mill, J., Fernandes, C., Schalkwyk, L.C., Buxbaum, J.D. & Reichenberg, A. (2009) Advancing paternal age is associated with deficits in social and exploratory behaviors in the offspring: a mouse model. PLoS One 4, e8456. DOI:10.1371/journal.pone.0008456.
34. Smith, R.G., Reichenberg, A., Kember, R.L., Buxbaum, J.D., Schalkwyk, L.C., Fernandes, C. & Mill, J. (2012) Advanced paternal age is associated with altered DNA methylation at brain-expressed imprinted loci in inbred mice: implications for neuropsychiatric disease. Mol Psychiatry 18, 635-36.
35. Terranova, L. & Laviola, G. (2005) Scoring of social interactions and play in mice during adolescence. Current Protocols in Toxicology, Unit 13.10. DOI:10.1002/0471140856.tx1310s26.
36. Tsuchiya, K.J., Matsumoto, K., Miyachi, T., Tsujii, M., Nakamura, K., Takagai, S., Kawai, M., Yagi, A., Iwaki, K., Suda, S., Sugihara, G., Iwata, Y., Matsuzaki, H., Sekine, Y., Suzuki, K., Sugiyama, T., Mori, N. & Takei, N. (2008) Paternal age at birth and high-functioning autistic-spectrum disorder in offspring. Br J Psychiatry 193, 316-321. DOI:10.1192/bjp.bp.107.045120.
37. Werling, D.M. & Geschwind, D.H. (2013) Sex differences in autism spectrum disorders. Curr Opin Neurol 26, 146-153. DOI:10.1097/WCO.0b013e32835ee548.
38. Wing, L. (1981) Language, social and cognitive impairments in autism and severe mental retardation. J Autism Dev Disord 11, 31-44.
39. Winslow, J. T. (2003). Mouse social recognition and preference. Current Protocols in Neuroscience/Editorial Board, Jacqueline N. Crawley .. [et al.], Chapter 8, Unit 8.16. doi:10.1002/0471142301.ns0816s22