Maternal stress retards fetal development in mice with transcriptome-wide impact on gene expression profiles of the limb

References

• Allan GJ, Flint DJ, Patel K. 2001. Insulin-like growth factor axis during embryonic development. Reproduction. 122:31–39.
   PubMed Web of Science ®Google Scholar
• Arnott JA, Nuglozeh E, Rico MC, Arango-Hisijara MC, Odgren PR, Safadi FF, Popoff SN. 2007. Connective tissue growth factor (CTGF/CCN2) is a downstream mediator for TGF-1-induced extracellular matrix production in osteoblasts. J Cell Physiol. 210:843–852.
   PubMed Web of Science ®Google Scholar
• Barbazanges A, Vallée M, Mayo W, Day J, Simon H, Le Moal M, Maccari S. 1996. Early and later adoptions have different long-term effects on male rat offspring. J Neurosci. 16:7783–7790.
   PubMed Web of Science ®Google Scholar
• Chung S, Son GH, Park SH, Park E, Lee KH, Geum D, Kim K. 2005. Differential adaptive responses to chronic stress of maternally stressed male mice offspring. Endocrinology. 146:3202–3210.
   PubMedGoogle Scholar
• Cottrell EC, Seckl JR. 2009. Prenatal stress, glucocorticoids and the programming of adult disease. Front Behav Neurosci. 3:1–9.
   PubMedGoogle Scholar
• Crossley PH, Minowada G, MacArthur CA, Martin GR. 1996. Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell. 84:127–136.
   PubMed Web of Science ®Google Scholar
• Duester G. 2007. Retinoic acid regulation of the somitogenesis clock. Birth Defects Res C Embryo Today. 81:84–92.
   PubMedGoogle Scholar
• Kamradt MC, Chen F, Sam S, Cryns VL. 2002. The small heat shock protein B-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting Caspase-3 activation. J Biol Chem. 277:38731–38736.
   PubMedGoogle Scholar
• Kang SS, Son GH, Seong JY, Choi D, Kwon HB, Lee CC, Kim K. 1998. Noradrenergic neurotoxin suppresses gonadotropin-releasing hormone (GnRH) and GnRH receptor gene expression in ovariectomized and steroid-treated rats. J Neuroendocrinol. 10:911–918.
   PubMedGoogle Scholar
• Kaufman MH. 1998. The Atlas of mouse development. London: Academic press.
   Google Scholar
• Lewandoski M, Sun X, Martin GR. 2000. Fgf8 signaling from the AER is essential for normal limb development. Nat Genet. 26:460–463.
   PubMed Web of Science ®Google Scholar
• Luo Q, Kang Q, Si W, Jiang W, Park JK, Peng Y, Li X, Luu HH, Luo J, Montag AG, Haydon RC, He TC. 2004. Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J Biol Chem. 279:55958–55968.
   PubMed Web of Science ®Google Scholar
• Lupien SJ, McEwen BS, Gunnar MR, Heim C. 2009. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 10:434–445.
   PubMed Web of Science ®Google Scholar
• Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M. 1995. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci. 15:110–116.
   PubMed Web of Science ®Google Scholar
• Mackem S. 2006. Limb development. In: Unsicker K, Krieglstein K. editors. Cell signaling and growth factors in development. Weinheim: Wiley-vch. p 523–618.
   Google Scholar
• Mallo M. 2001. Formation of the middle ear: Recent progress on the developmental and molecular mechanisms. Dev Biol. 231:410–419.
   PubMedGoogle Scholar
• McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonté B, Szyf M, Turecki G, Meaney MJ. 2009. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 12:342–348.
   PubMed Web of Science ®Google Scholar
• Meaney MJ. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 24:1161–1192.
   PubMed Web of Science ®Google Scholar
• Minamizato T, Sakamoto K, Liu T, Kokubo H, Katsube K, Perba Bl, Nakamura S, Yamaguchi A. 2007. CCN3/NOV inhibits BMP-2-induced osteoblast differentiation by interacting with BMP and Notch signaling pathways. Biochem Biophys Res Commun. 354:567–573.
   PubMedGoogle Scholar
• Moon AM, Capecchi MR. 2000. Fgf8 is required for outgrowth and patterning of the limbs. Nat Genet. 26:455–459.
   PubMed Web of Science ®Google Scholar
• Mueller BR, Bale TL. 2008. Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci. 28:9055–9065.
   PubMed Web of Science ®Google Scholar
• Mulder EJ, Robles de Medina PG, Huizink AC, Van den Bergh BR, Buitelaar JK, Visser GH. 2002. Prenatal maternal stress: Effects on pregnancy and the (unborn) child. Early Hum Dev. 70:3–14.
   PubMed Web of Science ®Google Scholar
• O'Donnell K, O'Connor TG, Glover V. 2009. Prenatal stress and neurodevelopment of the child: Focus on the HPA axis and role of the placenta. Dev Neurosci. 31:285–292.
   PubMed Web of Science ®Google Scholar
• Rosenfeld MG, Briata P, Dasen J, Gleiberman AS, Kioussi C, Lin C, O'Connell SM, Ryan A, Szeto DP, Treier M. 2000. Multistep signaling and transcriptional requirements for pituitary organogenesis in vivo. Recent Prog Horm Res. 55:1–13.
   PubMedGoogle Scholar
• Roussa E, Krieglstein K. 2004. Induction and specification of midbrain dopaminergic cells: Focus on SHH, FGF8, and TGF-beta. Cell Tissue Res. 318:23–33.
   PubMedGoogle Scholar
• Seckl JR. 2004. Prenatal glucocorticoids and long-term programming. Eur Endocrinol. 151:U49–U62.
   PubMed Web of Science ®Google Scholar
• Seckl JR. 2008. Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction. Prog Brain Res. 167:17–34.
   PubMed Web of Science ®Google Scholar
• Song JJ, Aswad R, Kanaan RA, Rico MC, Owen TA, Barbe MF, Safadi FF, Popoff SN. 2007. Connective tissue growth factor (CTGF) acts as a downstream mediator of TGF-1 to induce mesenchymal cell condensation. J Cell Physiol. 210:398–410.
   PubMed Web of Science ®Google Scholar
• Son GH, Geum D, Chung S, Kim EJ, Jo JH, Kim CM, Lee KH, Kim H, Choi S, Kim HT, Lee CJ, Kim K. 2006. Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J Neurosci. 26:3309–3318.
   PubMed Web of Science ®Google Scholar
• Son GH, Chung S, Geum D, Kang SS, Choi WS, Kim K, Choi S. 2007. Hyperactivity and alteration of the midbrain dopaminergic system in maternally stressed male mice offspring. Biochem Biophys Res Commun. 352:823–829.
   PubMedGoogle Scholar
• Son GH, Chung S, Choe HK, Kim HD, Baik SM, Lee H, Lee HW, Choi S, Sun W, Kim H, Cho S, Lee KH, Kim K. 2008. Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc Natl Acad Sci USA. 105:20970–20975.
   PubMed Web of Science ®Google Scholar
• Sun W, Choi SH, Park SK, Kim SJ, Noh MR, Kim EH, Kim HJ, Kim H. 2007. Identification and characterization of novel activity-dependent transcription factors in rat cortical neurons. J Neurochem. 100:269–278.
   PubMedGoogle Scholar
• Vogel A, Rodriguez C, Izpisua-Belmonte JC. 1996. Involvement of FGF8 in initiation, outgrowth and patterning of the vertebrate limb. Development. 122:1737–1750.
   PubMed Web of Science ®Google Scholar
• Wan Y, Saghatelian A, Chong LW, Zhang CL, Cravatt BF, Evans RM. 2007. Maternal PPAR gamma protects nursing neonates by suppressing the production of inflammatory milk. Genes Dev. 21:1895–1908.
   PubMedGoogle Scholar
• Waterland RA, Michels KB. 2007. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 27:363–388.
   PubMed Web of Science ®Google Scholar
• Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nat Neurosci. 7:847–854.
   PubMed Web of Science ®Google Scholar
• Weinstock M. 2005. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun. 19:296–308.
   PubMed Web of Science ®Google Scholar
• Weinstock M. 2008. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev. 32:1073–1086.
   PubMed Web of Science ®Google Scholar
• Yashiro K, Zhao X, Uehara M, Yamashita K, Nishijima M, Nishino J, Saijoh Y, Sakai Y, Hamada H. 2004. Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev Cell. 6:411–422.
   PubMed Web of Science ®Google Scholar