Early life stress increases anxiety-like behavior in Balbc mice despite a compensatory increase in levels of postnatal maternal care

Hormones and Behavior

Volumn 57, Issue 4-5, 2010, Pages 396-404

  Wei, Lan ^a   David, Aisha ^a   Duman, Ron S ^a   Anisman, Hymie ^b   Kaffman, Arie ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CARLETON UNIVERSITY   (Canada)

Author keywords

Anxiety; Early life stress; Handling; Hippocampus; Maternal care; Mice; Neurodevelopment

Indexed keywords

CORTICOSTERONE; DNA; RNA;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BAGG ALBINO MOUSE; BEHAVIOR; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; EARLY LIFE STRESS; ENVIRONMENTAL EXPOSURE; FEMALE; GROWTH ACCELERATION; HIPPOCAMPUS; MALE; MATERNAL CARE; MATERNAL DEPRIVATION; MENTAL DISEASE; MOUSE; NONHUMAN; PERINATAL PERIOD; POSTNATAL CARE; PRIORITY JOURNAL; PROGENY; REARING; RODENT;

ANIMALS; ANIMALS, NEWBORN; ANXIETY; ANXIETY, SEPARATION; CORTICOSTERONE; DNA; FEMALE; GROOMING; HIPPOCAMPUS; MALE; MATERNAL BEHAVIOR; MATERNAL DEPRIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOTOR ACTIVITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; STRESS, PSYCHOLOGICAL; TRIIODOTHYRONINE;

EID: 77950945886     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2010.01.007     Document Type: Article

References (61)

1. Anisman H., Hayley S., Kelly O., Borowski T., Merali Z. Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: mouse strain-dependent outcomes. Behav. Neurosci. 2001, 115:443-454.
2. Bebbington P.E., Bhugra D., Brugha T., Singleton N., Farrell M., Jenkins R., Lewis G., Meltzer H. Psychosis, victimisation and childhood disadvantage: evidence from the second British National Survey of Psychiatric Morbidity. Br. J. Psychiatry 2004, 185:220-226.
3. Berrebi A.S., Fitch R.H., Ralphe D.L., Denenberg J.O., Friedrich V.L., Denenberg V.H. Corpus callosum: region-specific effects of sex, early experience and age. Brain Res. 1988, 438:216-224.
4. Bohn M.C. Granule cell genesis in the hippocampus of rats treated neonatally with hydrocortisone. Neuroscience 1980, 5:2003-2012.
5. Bryer J.B., Nelson B.A., Miller J.B., Krol P.A. Childhood sexual and physical abuse as factors in adult psychiatric illness. Am. J. Psychiatry 1987, 144:1426-1430.
6. Caldji C., Diorio J., Anisman H., Meaney M.J. Maternal behavior regulates benzodiazepine/GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice. Neuropsychopharmacology 2004, 29:1344-1352.
7. Carola V., D'Olimpio F., Brunamonti E., Bevilacqua A., Renzi P., Mangia F. Anxiety-related behaviour in C57BL/6<->BALB/c chimeric mice. Behav. Brain Res. 2004, 150:25-32.
8. Carola V., Frazzetto G., Pascucci T., Audero E., Puglisi-Allegra S., Cabib S., Lesch K.P., Gross C. Identifying molecular substrates in a mouse model of the serotonin transporter x environment risk factor for anxiety and depression. Biol. Psychiatry 2007.
9. Casolini P., Domenici M.R., Cinque C., Alema G.S., Chiodi V., Galluzzo M., Musumeci M., Mairesse J., Zuena A.R., Matteucci P., Marano G., Maccari S., Nicoletti F., Catalani A. Maternal exposure to low levels of corticosterone during lactation protects the adult offspring against ischemic brain damage. J. Neurosci. 2007, 27:7041-7046.
10. Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 2003, 79:359-371.
11. D'Amato F.R., Cabib S., Ventura R., Orsini C. Long-term effects of postnatal manipulation on emotionality are prevented by maternal anxiolytic treatment in mice. Dev. Psychobiol. 1998, 32:225-234.
12. Denenberg V.H., Rosen G.D., Hofmann M., Gall J., Stockler J., Yutzey D.A. Neonatal postural asymmetry and sex differences in the rat. Brain Res. 1981, 254:417-419.
13. Faulkner R.L., Low L.K., Cheng H.J. Axon pruning in the developing vertebrate hippocampus. Dev. Neurosci. 2007, 29:6-13.
14. Francis D.D., Szegda K., Campbell G., Martin W.D., Insel T.R. Epigenetic sources of behavioral differences in mice. Nat. Neurosci. 2003, 6:445-446.
15. Gilbert R., Widom C.S., Browne K., Fergusson D., Webb E., Janson S. Burden and consequences of child maltreatment in high-income countries. Lancet 2009, 373:68-81.
16. Habibi L., Ebtekar M., Jameie S.B. Immune and nervous systems share molecular and functional similarities: memory storage mechanism. Scand. J. Immunol. 2009, 69:291-301.
17. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry. 2001, 49:1023-1039.
18. Hensch T.K., Fagiolini M. Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog. Brain Res. 2005, 147:115-124.
19. Hess J., Denenberg V.H., Zarrow M.X., Pfeifer D. Modification of the corticosterone response curve as a function of handling in infancy. Physiol. Behav. 1969, 4:109-111.
20. Hofer M.A. Hidden regulators in attachment, separation, and loss. Monogr. Soc. Res. Child. Dev. 1994, 59:192-207.
21. Howard E. Reductions in size and total DNA of cerebrum and cerebellum in adult mice after corticosterone treatment in infancy. Exp. Neurol. 1968, 22:191-208.
22. Howard E., Granoff D.M. Increased voluntary running and decreased motor coordination in mice after neonatal corticosterone implantation. Exp. Neurol. 1968, 22:661-673.
23. Hua J.Y., Smith S.J. Neural activity and the dynamics of central nervous system development. Nat. Neurosci. 2004, 7:327-332.
24. Kaffman A. The silent epidemic of neurodevelopmental injuries. Biol. Psychiatry 2009, 66:624-626.
25. Kaffman A., Meaney M. Neurodevelopmental Sequelae of Postnatal Maternal Care in Rodents: Clinical and Research Implications of Molecular Insights. J. Child. Psychol. Psychiatry 2007, 48:224-244.
26. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
27. Kaufman J., Charney D. Effects of early stress on brain structure and function: implications for understanding the relationship between child maltreatment and depression. Dev. Psychopathol. 2001, 13:451-471.
28. Kikusui T., Nakamura K., Kakuma Y., Mori Y. Early weaning augments neuroendocrine stress responses in mice. Behav. Brain Res. 2006, 175:96-103.
29. Lalli E., Ohe K., Latorre E., Bianchi M.E., Sassone-Corsi P. Sexy splicing: regulatory interplays governing sex determination from Drosophila to mammals. J. Cell. Sci. 2003, 116:441-445.
30. Lee M.H.S., Williams D.I. Changes in licking behavior in the rat mother following handling of young. Anim. Behav. 1974, 679-681.
31. Levine S. Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat. Physiol. Behav. 2001, 73:255-260.
32. Levine S., Alpert M., Lewis G.W. Infantile experience and the maturation of the pituitary adrenal axis. Science 1957, 126:1347.
33. Levine S., Haltmeyer G., Karas G., Denenberg V.H. Physiological and behavioral effects of infantile stimulation. Physiol. Behav. 1967, 2:55-59.
34. Lippmann M., Bress A., Nemeroff C.B., Plotsky P.M., Monteggia L.M. Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur. J. Neurosci. 2007, 25:3091-3098.
35. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
36. Lund A.H., van Lohuizen M. Epigenetics and cancer. Genes Dev. 2004, 18:2315-2335.
37. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., Turecki G., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 2009, 12:342-348.
38. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24:1161-1192.
39. Meaney M.J., Aitken D.H., Sapolsky R.M. Thyroid hormones influence the development of hippocampal glucocorticoid receptors in the rat: a mechanism for the effects of postnatal handling on the development of the adrenocortical stress response. Neuroendocrinology 1987, 45:278-283.
40. Meaney M.J., Aitken D.H., Viau V., Sharma S., Sarrieau A. Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 1989, 50:597-604.
41. Meaney M.J., Aitken D.H., Sharma S., Viau V. Basal ACTH, corticosterone and corticosterone-binding globulin levels over the diurnal cycle, and age-related changes in hippocampal type I and type II corticosteroid receptor binding capacity in young and aged, handled and nonhandled rats. Neuroendocrinology 1992, 55:204-213.
42. Meaney M.J., Diorio J., Francis D., Weaver S., Yau J., Chapman K., Seckl J.R. Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin. J. Neurosci. 2000, 20:3926-3935.
43. Miller C.A., Campbell S.L., Sweatt J.D. DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiol. Learn. Mem. 2008, 89:599-603.
44. Millstein R.A., Holmes A. Effects of repeated maternal separation on anxiety-and depression-related phenotypes in different mouse strains. Neurosci. Biobehav. Rev. 2007, 31:3-17.
45. Millstein R.A., Ralph R.J., Yang R.J., Holmes A. Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes Brain Behav. 2006, 5:346-354.
46. Moles A., Sarli C., Bartolomucci A., D'Amato F.R. Interaction with stressed mothers affects corticosterone levels in pups after reunion and impairs the response to dexamethasone in adult mice. Psychoneuroendocrinology 2008, 33:462-470.
47. Muenzenmaier K., Meyer I., Struening E., Ferber J. Childhood abuse and neglect among women outpatients with chronic mental illness. Hosp. Commun. Psychiatry 1993, 44:666-670.
48. Mullen P.E., Martin J.L., Anderson J.C., Romans S.E., Herbison G.P. The long-term impact of the physical, emotional, and sexual abuse of children: a community study. Child. Abuse Negl. 1996, 20:7-21.
49. Nemeroff C.B., Heim C.M., Thase M.E., Klein D.N., Rush A.J., Schatzberg A.F., Ninan P.T., McCullough J.P., Weiss P.M., Dunner D.L., Rothbaum B.O., Kornstein S., Keitner G., Keller M.B. Differential responses to psychotherapy versus pharmacotherapy in patients with chronic forms of major depression and childhood trauma. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:14293-14296.
50. Novikova S.I., He F., Bai J., Cutrufello N.J., Lidow M.S., Undieh A.S. Maternal cocaine administration in mice alters DNA methylation and gene expression in hippocampal neurons of neonatal and prepubertal offspring. PLoS ONE. 2008, e1919:3.
51. Parfitt D.B., Levin J.K., Saltstein K.P., Klayman A.S., Greer L.M., Helmreich D.L. Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Res. 2004, 1016:111-118.
52. Payer B., Lee J.T. X chromosome dosage compensation: how mammals keep the balance. Annu. Rev. Genet. 2008, 42:733-772.
53. Priebe K., Romeo R.D., Francis D.D., Sisti H.M., Mueller A., McEwen B.S., Brake W.G. Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/cJ mice: a cross-fostering study. Dev. Psychobiol. 2005, 47:398-407.
54. Qureshi I.A., Mehler M.F. Regulation of non-coding RNA networks in the nervous system-what's the REST of the story?. Neurosci. Lett. 2009.
55. Rakic P., Bourgeois J.P., Eckenhoff M.F., Zecevic N., Goldman-Rakic P.S. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 1986, 232:232-235.
56. Ren-Patterson R.F., Cochran L.W., Holmes A., Lesch K.P., Lu B., Murphy D.L. Gender-dependent modulation of brain monoamines and anxiety-like behaviors in mice with genetic serotonin transporter and BDNF deficiencies. Cell. Mol. Neurobiol. 2006, 26:755-780.
57. Shanks N., Griffiths J., Zalcman S., Zacharko R.M., Anisman H. Mouse strain differences in plasma corticosterone following uncontrollable footshock. Pharmacol. Biochem. Behav. 1990, 36:515-519.
58. Szyf M., Weaver I.C., Champagne F.A., Diorio J., Meaney M.J. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front. Neuroendocrinol. 2005, 26:139-162.
59. Tan B.Z., Huang H., Lam R., Soong T.W. Dynamic regulation of RNA editing of ion channels and receptors in the mammalian nervous system. Mol. Brain 2009, 2:13.
60. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
61. Zaharia M.D., Kulczycki J., Shanks N., Meaney M.J., Anisman H. The effects of early postnatal stimulation on Morris water-maze acquisition in adult mice: genetic and maternal factors. Psychopharmacology. (Berl) 1996, 128:227-239.