Maternal genetic mutations as gestational and early life influences in producing psychiatric disease-like phenotypes in mice

Frontiers in Psychiatry

Volumn 2, Issue MAY, 2011, Pages

  Gleason, Georgia ^a   Zupan, Bojana ^a   Toth, Miklos ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Anxiety; Epigenetic; Fragile X; Maternal; Transgenerational

Indexed keywords

CYTOKINE; FRAGILE X MENTAL RETARDATION PROTEIN; POLYINOSINIC POLYCYTIDYLIC ACID; SEROTONIN 1A RECEPTOR;

ANXIETY; ATTENTION DEFICIT DISORDER; CHILD BEHAVIOR; CYTOKINE RESPONSE; DEPRESSION; DISEASE MODEL; EARLY LIFE STRESS; EXPERIMENTAL ANIMAL; EXTRACHROMOSOMAL INHERITANCE; FMR1 GENE; GENE INACTIVATION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; GESTATIONAL AGE; HYPERACTIVITY; MATERNAL BEHAVIOR; MATERNAL CARE; MENTAL DISEASE; MUTATOR GENE; NONHUMAN; PHENOTYPE; PROGENY; REVIEW;

EID: 84866752013     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2011.00025     Document Type: Review

References (101)

1. Abazyan, B., Nomura, J., Kannan, G., Ishizuka, K., Tamashiro, K. L., Nucifora, F., Pogorelov, V., Ladenheim, B., Yang, C., Krasnova, I. N., Cadet, J. L., Pardo, C., Mori, S., Kamiya, A., Vogel, M. W., Sawa, A., Ross, C. A., and Pletnikov, M. V. (2010). Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology. Biol. Psychiatry 68, 1172-1181.
2. Arango, V., Underwood, M. D., Boldrini, M., Tamir, H., Kassir, S. A., Hsiung, S., Chen, J. J., and Mann, J. J. (2001). Serotonin 1A receptors, serotonin transporter binding and serotonin transporter mRNA expression in the brainstem of depressed suicide vic-tims. Neuropsychopharmacology 25, 892-903.
3. Ashwood, P., Nguyen, D. V., Hessl, D., Hagerman, R. J., and Tassone, F. (2011). Plasma cytokine profiles in Fragile X subjects: is there a role for cytokines in the pathogenesis? Brain Behav. Immun. 24, 898-902.
4. Atladottir, H. O., Thorsen, P., Schendel, D. E., Ostergaard, L., Lemcke, S., and Parner, E. T. (2010). Association of hospitalization for infection in childhood with diagnosis of autism spectrum disorders: a Danish cohort study. Arch. Pediatr. Adolesc. Med. 164, 470-477.
5. Bannerman, D. M., Grubb, M., Deacon, R. M., Yee, B. K., Feldon, J., and Rawlins, J. N. (2003). Ventral hippocampal lesions affect anxiety but not spa-tial learning. Behav. Brain Res. 139, 197-213.
6. Blackwood, D. H., Fordyce, A., Walker, M. T., St Clair, D. M., Porteous, D. J., and Muir, W. J. (2001). Schizophrenia and affective disorders - cosegregation with a translocation at chromosome 1q42 that directly disrupts brain- expressed genes: clinical and P300 findings in a family. Am. J. Hum. Genet. 69, 428-433.
7. Boehme, S. A., Lio, F. M., Sikora, L., Pandit, T. S., Lavrador, K., Rao, S. P., and Sriramarao, P. (2004). Cutting edge: serotonin is a chemotactic fac-tor for eosinophils and functions additively with eotaxin. J. Immunol. 173, 3599-3603.
8. Boksa, P. (2010). Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 24, 881-897.
9. Bosch, O. J., and Neumann, I. D. (2008). Brain vasopressin is an important regulator of maternal behavior independent of dams' trait anxi-ety. Proc. Natl. Acad. Sci. U.S.A. 105, 17139-17144.
10. Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M., Babulas, V. P., and Susser, E. S. (2004a). Serologic evidence of pre-natal influenza in the etiology of schizophrenia. Arch. Gen. Psychiatry 61, 774-780.
11. Brown, A. S., Hooton, J., Schaefer, C. A., Zhang, H., Petkova, E., Babulas, V., Perrin, M., Gorman, J. M., and Susser, E. S. (2004b). Elevated maternal inter-leukin-8 levels and risk of schizophre-nia in adult offspring. Am. J. Psychiatry 161, 889-895.
12. Brown, J. R., Ye, H., Bronson, R. T., Dikkes, P., and Greenberg, M. E. (1996). A defect in nurturing in mice lacking the immediate early gene fosB. Cell 86, 297-309.
13. Brummelte, S., and Galea, L. A. (2010). Depression during pregnancy and postpartum: contribution of stress and ovarian hormones. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 766-776.
14. Byrne, M., Agerbo, E., Bennedsen, B., Eaton, W. W., and Mortensen, P. B. (2007). Obstetric conditions and risk of first admission with schizophrenia: a Danish national register based study. Schizophr. Res. 97, 51-59.
15. Carola, V., Frazzetto, G., Pascucci, T., Audero, E., Puglisi-Allegra, S., Cabib, S., Lesch, K. P., and Gross, C. (2008). Identifying molecular substrates in a mouse model of the serotonin transporter × environment risk fac-tor for anxiety and depression. Biol. Psychiatry 63, 840-846.
16. Champagne, F. A., Curley, J. P., Swaney, W. T., Hasen, N. S., and Keverne, E. B. (2009). Paternal influence on female behavior: the role of Peg3 in explora-tion, olfaction, and neuroendocrine regulation of maternal behavior of female mice. Behav. Neurosci. 123, 469-480.
17. Chen, L., and Toth, M. (2001). Fragile X mice develop sensory hyperreactivity to auditory stimuli. Neuroscience 103, 1043-1050.
18. Clapcote, S. J., Lipina, T. V., Millar, J. K., Mackie, S., Christie, S., Ogawa, F., Lerch, J. P., Trimble, K., Uchiyama, M., Sakuraba, Y., Kaneda, H., Shiroishi, T., Houslay, M. D., Henkelman, R. M., Sled, J. G., Gondo, Y., Porteous, D. J., and Roder, J. C. (2007). Behavioral phenotypes of Disc1 missense muta-tions in mice. Neuron 54, 387-402.
19. Consortium TD-BFX. (1994). Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 78, 23-33.
20. Cory-Slechta, D. A., Zuch, C. L., and Fox, R. A. (1996). Comparison of the stimulus properties of a pre- vs. a putative postsynaptic dose of quin-pirole. Pharmacol. Biochem. Behav. 55, 423-432.
21. Cunningham, C., Campion, S., Teeling, J., Felton, L., and Perry, V. H. (2007). The sickness behaviour and CNS inflam-matory mediator profile induced by systemic challenge of mice with synthetic double-stranded RNA (poly I:C). Brain Behav. Immun. 21, 490-502.
22. Curley, J. P., Barton, S., Surani, A., and Keverne, E. B. (2004). Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proc. Biol. Sci. 271, 1303-1309.
23. Curley, J. P., Champagne, F. A., Bateson, P., Keverne, E. B., and Curley, K. O. Jr. (2008). Transgenerational effects of impaired maternal care on behav-iour of offspring and grandoffspring. Anim. Behav. 75, 1551-1561.
24. Davis, J. D., and Tremont, G. (2007). Neuropsychiatric aspects of hypothy-roidism and treatment reversibility. Minerva Endocrinol. 32, 49-65.
25. D'Hooge, R., Nagels, G., Franck, F., Bakker, C. E., Reyniers, E., Storm, K., Kooy, R. F., Oostra, B. A., Willems, P. J., and De Deyn, P. P. (1997). Mildly impaired water maze performance in male Fmr1 knockout mice. Neuroscience 76, 367-376.
26. Doolin, M. T., Barbaux, S., McDonnell, M., Hoess, K., Whitehead, A. S., and Mitchell, L. E. (2002). Maternal genetic effects, exerted by genes involved in homocysteine remethylation, influ-ence the risk of spina bifida. Am. J. Hum. Genet. 71, 1222-1226.
27. Drevets, W. C., Frank, E., Price, J. C., Kupfer, D. J., Holt, D., Greer, P. J., Huang, Y., Gautier, C., and Mathis, C. (1999). PET imaging of serotonin 1A receptor binding in depression. Biol. Psychiatry 46, 1375-1387.
28. Drevets, W. C., Thase, M. E., Moses-Kolko, E. L., Price, J., Frank, E., Kupfer, D. J., and Mathis, C. (2007). Serotonin-1A receptor imaging in recurrent depres-sion: replication and literature review. Nucl. Med. Biol. 34, 865-877.
29. Ehninger, D., Sano, Y., de Vries, P. J., Dies, K., Franz, D., Geschwind, D. H., Kaur, M., Lee, Y. S., Li, W., Lowe, J. K., Nakagawa, J. A., Sahin, M., Smith, K., Whittemore, V., and Silva, A. J. (2010). Gestational immune acti-vation and Tsc2 haploinsufficiency cooperate to disrupt fetal survival and may perturb social behavior in adult mice. Mol. Psychiatry, [Epub ahead of print].
30. Engberg, G., Kling-Petersen, T., and Nissbrandt, H. (1993). GABAB- receptor activation alters the firing pattern of dopamine neurons in the rat substantia nigra. Synapse 15, 229-238.
31. Fatemi, S. H., and Folsom, T. D. (2011). The role of fragile X mental retarda-tion protein in major mental disorders. Neuropharmacology 60, 1221-1226.
32. Fatemi, S. H., Kneeland, R. E., Liesch, S. B., and Folsom, T. D. (2010). Fragile X mental retardation protein levels are decreased in major psychiatric dis-orders. Schizophr. Res. 124, 246-247.
33. Figueiredo, B., and Costa, R. (2009). Mother's stress, mood and emo-tional involvement with the infant: 3 months before and 3 months after childbirth. Arch. Womens Ment. Health 12, 143-153.
34. Francis, D., Diorio, J., Liu, D., and Meaney, M. J. (1999). Nongenomic transmis-sion across generations of maternal behavior and stress responses in the rat. Science 286, 1155-1158.
35. Francis, D. D., Szegda, K., Campbell, G., Martin, W. D., and Insel, T. R. (2003). Epigenetic sources of behavioral differ-ences in mice. Nat. Neurosci. 6, 445-446. doi: 10.1186/1471-2202-8-17
36. Gammie, S. C., Bethea, E. D., and Stevenson, S. A. (2007). Altered maternal profiles in corticotropin- releasing factor receptor 1 deficient mice. BMC Neurosci. 8, 17.
37. Gleason, G., Liu, B., Bruening, S., Zupan, B., Auerbach, A., Mark, W., Oh, J. E., Gal-Toth, J., Lee, F., and Toth, M. (2010). The serotonin1A receptor gene as a genetic and prenatal mater-nal environmental factor in anxiety. Proc. Natl. Acad. Sci. U.S.A. 107, 7592-7597.
38. Grace, A. (2001). " Psychostimulant actions on dopamine and limbic sys-tem function: relevance to the patho-physiology and treatment of ADHD," in Stimulant Drugs and ADHD: Basic and Clinical Neuroscience, eds M. V. Solanto, A. F. T. Arnsten, and F. X. Castellanos (New York: Oxford University Press), 134-155.
39. Gross, C., Zhuang, X., Stark, K., Ramboz, S., Oosting, R., Kirby, L., Santarelli, L., Beck, S., and Hen, R. (2002). Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature 416, 396-400.
40. Halligan, S. L., Herbert, J., Goodyer, I., and Murray, L. (2007). Disturbances in morning cortisol secretion in associa-tion with maternal postnatal depres-sion predict subsequent depressive symptomatology in adolescents. Biol. Psychiatry 62, 40-46.
41. Halligan, S. L., Herbert, J., Goodyer, I. M., and Murray, L. (2004). Exposure to postnatal depression predicts elevated cortisol in adolescent offspring. Biol. Psychiatry 55, 376-381.
42. Halmoy, A., Johansson, S., Winge, I., McKinney, J. A., Knappskog, P. M., and Haavik, J. (2011). Attention-deficit/ hyperactivity disorder symptoms in offspring of mothers with impaired serotonin production. Arch. Gen. Psychiatry 67, 1033-1043.
43. Heisler, L. K., Chu, H. M., Brennan, T. J., Danao, J. A., Bajwa, P., Parsons, L. H., and Tecott, L. H. (1998). Elevated anxi-ety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc. Natl. Acad. Sci. U.S.A. 95, 15049-15054.
44. Hikida, T., Jaaro-Peled, H., Seshadri, S., Oishi, K., Hookway, C., Kong, S., Wu, D., Xue, R., Andrade, M., Tankou, S., Mori, S., Gallagher, M., Ishizuka, K., Pletnikov, M., Kida, S., and Sawa, A. (2007). Dominant-negative DISC1 transgenic mice display schizophre-nia-associated phenotypes detected by measures translatable to humans. Proc. Natl. Acad. Sci. U.S.A. 104, 14501-14506.
45. Jin, D., Liu, H. X., Hirai, H., Torashima, T., Nagai, T., Lopatina, O., Shnayder, N. A., Yamada, K., Noda, M., Seike, T., Fujita, K., Takasawa, S., Yokoyama, S., Koizumi, K., Shiraishi, Y., Tanaka, S., Hashii, M., Yoshihara, T., Higashida, K., Islam, M. S., Yamada, N., Hayashi, K., Noguchi, N., Kato, I., Okamoto, H., Matsushima, A., Salmina, A., Munesue, T., Shimizu, N., Mochida, S., Asano, M., and Higashida, H. (2007). CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446, 41-45.
46. Jin, S. H., Blendy, J. A., and Thomas, S. A. (2005). Cyclic AMP response ele-ment-binding protein is required for normal maternal nurturing behavior. Neuroscience 133, 647-655.
47. Johnson, W. G. (2003). Teratogenic alle-les and neurodevelopmental disorders. Bioessays 25, 464-477.
48. Kao, D. I., Aldridge, G. M., Weiler, I. J., and Greenough, W. T. (2010). Altered mRNA transport, docking, and pro-tein translation in neurons lacking fragile X mental retardation protein. Proc. Natl. Acad. Sci. U.S.A. 107, 15601-15606.
49. Kessler, M. S., Bosch, O. J., Bunck, M., Landgraf, R., and Neumann, I. D. (2011). Maternal care differs in mice bred for high vs. low trait anxiety: impact of brain vasopressin and cross- fostering. Soc. Neurosci. 6, 156-168.
50. Kilpinen, H., Ylisaukko-Oja, T., Hennah, W., Palo, O. M., Varilo, T., Vanhala, R., Nieminen-von Wendt, T., von Wendt, L., Paunio, T., and Peltonen, L. (2008). Association of DISC1 with autism and Asperger syndrome. Mol. Psychiatry 13, 187-196.
51. Kong, A., Steinthorsdottir, V., Masson, G., Thorleifsson, G., Sulem, P., Besenbacher, S., Jonasdottir, A., Sigurdsson, A., Kristinsson, K. T., Jonasdottir, A., Frigge, M. L., Gylfason, A., Olason, P. I., Gudjonsson, S. A., Sverrisson, S., Stacey, S. N., Sigurgeirsson, B., Benediktsdottir, K. R., Sigurdsson, H., Jonsson, T., Benediktsson, R., Olafsson, J. H., Johannsson, O. T., Hreidarsson, A. B., Sigurdsson, G., Ferguson-Smith, A. C., Gudbjartsson, D. F., Thorsteinsdottir, U., and Stefansson, K. (2009). Parental origin of sequence variants associated with complex diseases. Nature 462, 868-874.
52. Koob, G. F., and Swerdlow, N. R. (1988). The functional output of the mesolim-bic dopamine system. Ann. N. Y. Acad. Sci. 537, 216-227.
53. Kuroda, K. O., Meaney, M. J., Uetani, N., and Kato, T. (2008). Neurobehavioral basis of the impaired nurturing in mice lacking the immediate early gene FosB. Brain Res. 1211, 57-71.
54. Kushnir-Sukhov, N. M., Gilfillan, A. M., Coleman, J. W., Brown, J. M., Bruening, S., Toth, M., and Metcalfe, D. D. (2006). 5-hydroxytryptamine induces mast cell adhesion and migra-tion. J. Immunol. 177, 6422-6432.
55. Kvajo, M., McKellar, H., Arguello, P. A., Drew, L. J., Moore, H., MacDermott, A. B., Karayiorgou, M., and Gogos, J. A. (2008). A mutation in mouse Disc1 that models a schizophrenia risk allele leads to specific alterations in neuronal architecture and cognition. Proc. Natl. Acad. Sci. U.S.A. 105, 7076-7081.
56. Labouebe, G., Lomazzi, M., Cruz, H. G., Creton, C., Lujan, R., Li, M., Yanagawa, Y., Obata, K., Watanabe, M., Wickman, K., Boyer, S. B., Slesinger, P. A., and Luscher, C. (2007). RGS2 modulates coupling between GABAB receptors and GIRK channels in dopamine neu-rons of the ventral tegmental area. Nat. Neurosci. 10, 1559-1568.
57. Lefebvre, L., Viville, S., Barton, S. C., Ishino, F., Keverne, E. B., and Surani, M. A. (1998). Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat. Genet. 20, 163-169.
58. Lemonde, S., Turecki, G., Bakish, D., Du, L., Hrdina, P. D., Bown, C. D., Sequeira, A., Kushwaha, N., Morris, S. J., Basak, A., Ou, X. M., and Albert, P. R. (2003). Impaired repression at a 5-hydroxytryptamine 1A recep-tor gene polymorphism associated with major depression and suicide. J. Neurosci. 23, 8788-8799.
59. Lerch-Haner, J. K., Frierson, D., Crawford, L. K., Beck, S. G., and Deneris, E. S. (2008). Serotonergic transcriptional programming determines maternal behavior and offspring survival. Nat. Neurosci. 11, 1001-1003.
60. Lesch, K. P., Wiesmann, M., Hoh, A., Muller, T., Disselkamp-Tietze, J., Osterheider, M., and Schulte, H. M. (1992). 5-HT1A receptor-effector system responsivity in panic disor-der. Psychopharmacology (Berl.) 106, 111-117.
61. Li, L., Keverne, E. B., Aparicio, S. A., Ishino, F., Barton, S. C., and Surani, M. A. (1999). Regulation of maternal behav-ior and offspring growth by paternally expressed Peg3. Science 284, 330-333.
62. Liebsch, G., Montkowski, A., Holsboer, F., and Landgraf, R. (1998). Behavioural profiles of two Wistar rat lines selec-tively bred for high or low anxiety- related behaviour. Behav. Brain Res. 94, 301-310.
63. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., and Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoid recep-tors, and hypothalamic-pituitary- adrenal responses to stress. Science 277, 1659-1662.
64. Lopez, J. F., Chalmers, D. T., Little, K. Y., and Watson, S. J. (1998). A.E. Bennett Research Award. Regulation of serot-onin1A, glucocorticoid, and mineralo-corticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol. Psychiatry 43, 547-573.
65. Lucas, B. K., Ormandy, C. J., Binart, N., Bridges, R. S., and Kelly, P. A. (1998). Null mutation of the prolactin recep-tor gene produces a defect in mater-nal behavior. Endocrinology 139, 4102-4107.
66. Madden, T. E., and Johnson, S. W. (1998). Gamma-hydroxybutyrate is a GABAB receptor agonist that increases a potassium conductance in rat ven-tral tegmental dopamine neurons. J. Pharmacol. Exp. Ther. 287, 261-265.
67. Mann, J. J. (1999). Role of the seroton-ergic system in the pathogenesis of major depression and suicidal behav-ior. Neuropsychopharmacology 21, 99S-105S.
68. Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., McCarthy, M. I., Ramos, E. M., Cardon, L. R., Chakravarti, A., Cho, J. H., Guttmacher, A. E., Kong, A., Kruglyak, L., Mardis, E., Rotimi, C. N., Slatkin, M., Valle, D., Whittemore, A. S., Boehnke, M., Clark, A. G., Eichler, E. E., Gibson, G., Haines, J. L., Mackay, T. F., McCarroll, S. A., and Visscher, P. M. (2009). Finding the missing her-itability of complex diseases. Nature 461, 747-753.
69. Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reac-tivity across generations. Annu. Rev. Neurosci. 24, 1161-1192.
70. Millar, J. K., Christie, S., Anderson, S., Lawson, D., Hsiao-Wei Loh, D., Devon, R. S., Arveiler, B., Muir, W. J., Blackwood, D. H., and Porteous, D. J. (2001). Genomic structure and localisation within a linkage hotspot of disrupted in Schizophrenia 1, a gene disrupted by a translocation segregating with schizophrenia. Mol. Psychiatry 6, 173-178.
71. Millar, J. K., Wilson-Annan, J. C., Anderson, S., Christie, S., Taylor, M. S., Semple, C. A., Devon, R. S., St Clair, D. M., Muir, W. J., Blackwood, D. H., and Porteous, D. J. (2000). Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet. 9, 1415-1423.
72. Moses-Kolko, E. L., Wisner, K. L., Price, J. C., Berga, S. L., Drevets, W. C., Hanusa, B. H., Loucks, T. L., and Meltzer, C. C. (2008). Serotonin 1A receptor reduc-tions in postpartum depression: a positron emission tomography study. Fertil. Steril. 89, 685-692.
73. Murray, C., and Johnston, C. (2006). Parenting in mothers with and with-out attention-deficit/hyperactivity disorder. J. Abnorm. Psychol. 115, 52-61.
74. Murray, L., Halligan, S. L., Goodyer, I., and Herbert, J. (2010). Disturbances in early parenting of depressed moth-ers and cortisol secretion in offspring: a preliminary study. J. Affect. Disord. 122, 218-223.
75. Neumeister, A., Bain, E., Nugent, A. C., Carson, R. E., Bonne, O., Luckenbaugh, D. A., Eckelman, W., Herscovitch, P., Charney, D. S., and Drevets, W. C. (2004). Reduced serotonin type 1A receptor binding in panic disorder. J. Neurosci. 24, 589-591.
76. Parks, C. L., Robinson, P. S., Sibille, E., Shenk, T., and Toth, M. (1998). Increased anxiety of mice lacking the serotonin1A receptor. Proc. Natl. Acad. Sci. U.S.A. 95, 10734-10739.
77. Patterson, P. H. (2009). Immune involve-ment in schizophrenia and autism: eti-ology, pathology and animal models. Behav. Brain Res. 204, 313-321.
78. Peier, A. M., McIlwain, K. L., Kenneson, A., Warren, S. T., Paylor, R., and Nelson, D. L. (2000). (Over)correction of FMR1 deficiency with YAC transgenics: behavioral and physical features. Hum. Mol. Genet. 9, 1145-1159.
79. Pletnikov, M. V., Ayhan, Y., Nikolskaia, O., Xu, Y., Ovanesov, M. V., Huang, H., Mori, S., Moran, T. H., and Ross, C. A. (2008). Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizo-phrenia. Mol. Psychiatry 13, 173-186.
80. Ramboz, S., Oosting, R., Amara, D. A., Kung, H. F., Blier, P., Mendelsohn, M., Mann, J. J., Brunner, D., and Hen, R. (1998). Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc. Natl. Acad. Sci. U.S.A. 95, 14476-14481.
81. Rouse, B., and Azen, C. (2004). Effect of high maternal blood phenylalanine on offspring congenital anomalies and developmental outcome at ages 4 and 6 years: the importance of strict dietary control preconception and throughout pregnancy. J. Pediatr. 144, 235-239.
82. Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S. L., Chatzi, C., He, S., Mackie, I., Brandon, N. J., Marquis, K. L., Day, M., Hurko, O., McCaig, C. D., Riedel, G., and St Clair, D. (2008). Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J. Neurosci. 28, 10893-10904.
83. Smith, S. E., Li, J., Garbett, K., Mirnics, K., and Patterson, P. H. (2007). Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 27, 10695-10702.
84. Smolders, I., De Klippel, N., Sarre, S., Ebinger, G., and Michotte, Y. (1995). Tonic GABA-ergic modulation of striatal dopamine release studied by in vivo microdialysis in the freely mov-ing rat. Eur. J. Pharmacol. 284, 83-91.
85. Spencer, C. M., Alekseyenko, O., Hamilton, S. M., Thomas, A. M., Serysheva, E., Yuva-Paylor, L. A., and Paylor, R. (2011). Modifying behavioral pheno-types in Fmr1KO mice: genetic back-ground differences reveal autistic-like responses. Autism Res. 4, 40-56.
86. Spencer, C. M., Alekseyenko, O., Serysheva, E., Yuva-Paylor, L. A., and Paylor, R. (2005). Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav. 4, 420-430.
87. Spinelli, S., Chefer, S., Carson, R. E., Jagoda, E., Lang, L., Heilig, M., Barr, C. S., Suomi, S. J., Higley, J. D., and Stein, E. A. (2010). Effects of early-life stress on serotonin(1A) receptors in juvenile Rhesus monkeys measured by positron emission tomography. Biol. Psychiatry 67, 1146-1153.
88. Starke, K., Gothert, M., and Kilbinger, H. (1989). Modulation of neurotransmitter release by presynaptic autoreceptors. Physiol. Rev. 69, 864-989.
89. Strobel, A., Gutknecht, L., Rothe, C., Reif, A., Mossner, R., Zeng, Y., Brocke, B., and Lesch, K. P. (2003). Allelic vari-ation in 5-HT1A receptor expres-sion is associated with anxiety- and depression-related personality traits. J. Neural Transm. 110, 1445-1453.
90. Szczypka, M. S., Kwok, K., Brot, M. D., Marck, B. T., Matsumoto, A. M., Donahue, B. A., and Palmiter, R. D. (2001). Dopamine production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron 30, 819-828.
91. Takayanagi, Y., Yoshida, M., Bielsky, I. F., Ross, H. E., Kawamata, M., Onaka, T., Yanagisawa, T., Kimura, T., Matzuk, M. M., Young, L. J., and Nishimori, K. (2005). Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 102, 16096-16101.
92. Usiello, A., Baik, J. H., Rouge-Pont, F., Picetti, R., Dierich, A., LeMeur, M., Piazza, P. V., and Borrelli, E. (2000). Distinct functions of the two isoforms of dopamine D2 receptors. Nature 408, 199-203.
93. Van den Bergh, B. R., Van Calster, B., Smits, T., Van Huffel, S., and Lagae, L. (2008). Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symp-toms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 33, 536-545.
94. Van den Hove, D. L., Lauder, J. M., Scheepens, A., Prickaerts, J., Blanco, C. E., and Steinbusch, H. W. (2006). Prenatal stress in the rat alters 5-HT1A receptor binding in the ventral hip-pocampus. Brain Res. 1090, 29-34.
95. Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., and Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854.
96. Weller, A., Leguisamo, A. C., Towns, L., Ramboz, S., Bagiella, E., Hofer, M., Hen, R., and Brunner, D. (2003). Maternal effects in infant and adult phenotypes of 5HT1A and 5HT1B receptor knockout mice. Dev. Psychobiol. 42, 194-205.
97. Williams, T. A., Mars, A. E., Buyske, S. G., Stenroos, E. S., Wang, R., Factura- Santiago, M. F., Lambert, G. H., and Johnson, W. G. (2007). Risk of autistic disorder in affected offspring of moth-ers with a glutathione S-transferase P1 haplotype. Arch. Pediatr. Adolesc. Med. 161, 356-361.
98. Yehuda, R., Bell, A., Bierer, L. M., and Schmeidler, J. (2008). Maternal, not paternal, PTSD is related to increased risk for PTSD in offspring of Holocaust survivors. J. Psychiatr. Res. 42, 1104-1111.
99. Yun, S. W., Platholi, J., Flaherty, M. S., Fu, W., Kottmann, A. H., and Toth, M. (2006). Fmrp is required for the estab-lishment of the startle response during the critical period of auditory develop-ment. Brain Res. 1110, 159-165.
100. Zupan, B., and Toth, M. (2008a). Wild-type male offspring of fmr-1(+/-) mothers exhibit characteristics of the fragile X phenotype. Neuropsychopharmacology 33, 2667-2675.
101. Zupan, B., and Toth, M. (2008b). Inactivation of the maternal fragile X gene results in sensitization of GABAB receptor function in the offspring. J. Pharmacol. Exp. Ther. 327, 820-826.