Effects of In utero environment and maternal behavior on neuroendocrine and behavioral alterations in a mouse model of prenatal trauma

Developmental Neurobiology

Volumn 76, Issue 11, 2016, Pages 1254-1265

  Golub, Y ^a,b   Canneva, F ^c   Funke, R ^a   Frey, S ^a   Distler, J ^a   von Horsten S ^c   Freitag, C M ^b   Kratz, O ^a   Moll, G H ^a   Solati, J ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

corticosterone; maternal behavior; prenatal trauma; prolactin; PTBS

Indexed keywords

CORTICOSTERONE; OXYTOCIN; PROLACTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR DISORDER; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ENVIRONMENTAL FACTOR; FEMALE; GESTATIONAL AGE; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; MOUSE; NEUROENDOCRINE DISEASE; NONHUMAN; OXYTOCIN BLOOD LEVEL; PERINATAL PERIOD; POSTTRAUMATIC STRESS DISORDER; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROLACTIN BLOOD LEVEL;

EID: 84991212082     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22387     Document Type: Article

References (44)

1. Barker DJ, Eriksson JG, Forsen T, Osmond C. 2002. Fetal origins of adult disease: Strength of effects and biological basis. Int J Epidemiol 31:1235–1239.
2. Barker DJ, Osmond C, Forsén TJ, Kajantie E, Eriksson JG. 2005. Trajectories of growth among children who have coronary events as adults. N Engl J Med 353:1802–1809.
3. Champagne F, Diorio J, Sharma S, Meaney MJ. 2001. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci U S A 98:12736–12741.
4. Chemtob CM, Nomura Y, Rajendran K, Yehuda R, Schwartz D, Abramovitz R. 2010. Impact of maternal posttraumatic stress disorder and depression following exposure to the September 11 attacks on preschool children's behavior. Child Dev 81:1129–1141.
5. Chokchaloemwong D, Rozenboim I, El Halawani ME, Chaiseha Y. 2015. Dopamine and prolactin involvement in the maternal care of chicks in the native Thai hen (Gallus domesticus). Gen Comp Endocrinol 212:131–144.
6. De Boo HA, Harding JE. 2006. The developmental origins of adult disease (Barker) hypothesis. Aust N Z J Obstet Gynaecol 46:4–14.
7. Eriksson J, Forsen T, Tuomilehto J, Osmond C, Barker D. 2001. Size at birth, childhood growth and obesity in adult life. Int J Obesity Relat Metab Disord 25:735–740.
8. Field T. 2011. Prenatal depression effects on early development: A review. Infant Behav Dev 34:1–14.
9. Fish EW, Shahrokh D, Bagot R, Caldji C, Bredy T, Szyf M, Meaney MJ. 2004. Epigenetic programming of stress responses through variations in maternal care. Ann N Y Acad Sci 1036:167–180.
10. Francis D, Diorio J, Liu D, Meaney MJ. 1999. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158.
11. Gluckman P, Hanson M. 2005. The Fetal Matrix: Evolution, Development and Disease. J R Soc Med 98(3):130–131.
12. Golub Y, Kaltwasser SF, Mauch CP, Herrmann L, Schmidt U, Holsboer F, Czisch M, Wotjak CT. 2011. Reduced hippocampus volume in the mouse model of posttraumatic stress disorder. J Psychiatr Res 45:650–659.
13. Golub Y, Mauch CP, Dahlhoff M, Wotjak CT. 2009. Consequences of extinction training on associative and non-associative fear in a mouse model of Posttraumatic Stress Disorder (PTSD). Behav Brain Res 205:544–549.
14. Harris A, Seckl J. 2011. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav 59:279–289.
15. Harville EW, Xiong X, Buekens P, Pridjian G, Elkind-Hirsch K. 2010. Resilience after Hurricane Katrina among pregnant and postpartum women. Womens Health Issues 20:20–27.
16. Lehrner A, Bierer LM, Passarelli V, Pratchett LC, Flory JD, Bader HN, Harris IR, Bedi A, Daskalakis NP, Makotkine I. 2014. Maternal PTSD associates with greater glucocorticoid sensitivity in offspring of Holocaust survivors. Psychoneuroendocrinology 40:213–220.
17. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena A, Cinque C, Van Reeth O. 2003. Prenatal stress and long-term consequences: Implications of glucocorticoid hormones. Neurosci Biobehav Rev 27:119–127.
18. Marco EM, Macrì S, Laviola G. 2011. Critical age windows for neurodevelopmental psychiatric disorders: Evidence from animal models. Neurotox Res 19:286–307.
19. Mcmillen IC, Robinson JS. 2005. Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Physiol Rev 85:571–633.
20. Meek LR, Dittel PL, Sheehan MC, Chan JY, Kjolhaug SR. 2001. Effects of stress during pregnancy on maternal behavior in mice. Physiol Behav 72:473–479.
21. Meaney MJ. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann Rev Neurosci 24:1161–1192.
22. Nagy G, Halász B. 1983. Time course of the litter removal-induced depletion in plasma prolactin levels of lactating rats. An immediate full blockade of the hormone release after separation. Neuroendocrinology 37:459–462.
23. Palosaari E, Punamäki R-L, Qouta S, Diab M. 2013. Intergenerational effects of war trauma among Palestinian families mediated via psychological maltreatment. Child Abuse Negl 37:955–968.
24. Pedersen CA, Ascher JA, Monroe YL, Prange AJ. 1982. Oxytocin induces maternal behavior in virgin female rats. Science 216:648–650.
25. Pedersen CA, Boccia ML. 2003. Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups. Physiol Behav 80:233–241.
26. Pedersen CA, Caldwell JD, McGuire M, Evans DL. 1991. Corticotronpin-releasing hormone inhibits maternal behavior and induces pup-killing. Life Sci 48:1537–1546.
27. Pedersen CA, Prange AJ. 1979. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci 76:6661–6665.
28. Pérez-Edgar K, Fox NA. 2005. Temperament and anxiety disorders. Child Adolesc Psychiatr Clin N Am 14:681–706.
29. Pike K, Hanson M, Godfrey K. 2008. Developmental mismatch: Consequences for later cardiorespiratory health. Bjog 115:149–157. Review article
30. Portfors CV, Perkel DJ. 2014. The role of ultrasonic vocalizations in mouse communication. Curr Opin Neurobiol 28:115–120.
31. Rilling JK, Young LJ. 2014. The biology of mammalian parenting and its effect on offspring social development. Science 345:771–776.
32. Shair HN, Brunelli SA, Masmela JR, Boone E, Hofer MA. 2003. Social, thermal, and temporal influences on isolation-induced and maternally potentiated ultrasonic vocalizations of rat pups. Dev Psychobiol 42:206–222.
33. Siegmund A, Wotjak CT. 2007. A mouse model of posttraumatic stress disorder that distinguishes between conditioned and sensitised fear. J Psychiatr Res 41:848–860.
34. Solati J, Kleehaupt E, Kratz O, Moll GH, Golub Y. 2015. Inverse effects of lipopolysaccharides on anxiety in pregnant mice and their offspring. Physiol Behav 139:369–374.
35. Solati J, Zarrindast MR, Salari AA. 2010. Dorsal hippocampal opioidergic system modulates anxiety-like behaviors in adult male Wistar rats. Psychiatry Clin Neurosci 64:634–641.
36. Vaughan OR, Sferruzzi-Perri AN, Fowden AL. 2012. Maternal corticosterone regulates nutrient allocation to fetal growth in mice. J Physiol 590:5529–5540.
37. Walf AA, Frye CA. 2012. Gestational or acute restraint in adulthood reduces levels of 5α-reduced testosterone metabolites in the hippocampus and produces behavioral inhibition of adult male rats. Front Cell Neurosci 6:137–166.
38. Weems CF, Scheeringa MS. 2013. Maternal depression and treatment gains following a cognitive behavioral intervention for posttraumatic stress in preschool children. J Anxiety Disord 27:140–146.
39. Yehuda R. 2006. Advances in understanding neuroendocrine alterations in PTSD and their therapeutic implications. Ann N Y Acad Sci 1071:137–166.
40. Yehuda R, Antelman SM. 1993. Criteria for rationally evaluating animal models of postraumatic stress disorder. Biol Psychiatry 33:479–486.
41. Yehuda R, Halligan SL, Grossman R. 2001. Childhood trauma and risk for PTSD: Relationship to intergenerational effects of trauma, parental PTSD, and cortisol excretion. Dev Psychopathol 13:733–753.
42. Yehuda R, Schmeidler J, Wainberg M, Binder-Brynes K, Duvdevani T. 2014. Vulnerability to posttraumatic stress disorder in adult offspring of Holocaust survivors. Am J Psychiatry 9:1163–1171.
43. Yehuda R, Teicher MH, Seckl JR, Grossman RA, Morris A, Bierer LM. 2007. Parental posttraumatic stress disorder as a vulnerability factor for low cortisol trait in offspring of holocaust survivors. Arch Gen Psychiatry 64:1040–1048.
44. Zerach G, Greene T, Ein-Dor T, Solomon Z. 2012. The relationship between posttraumatic stress disorder symptoms and paternal parenting of adult children among ex-prisoners of war: A longitudinal study. J Fam Psychol 26:274.