The effects of postnatal maternal separation on stress responsivity and experimentally induced colitis in adult rats

Physiology and Behavior

Volumn 81, Issue 1, 2004, Pages 71-84

  Milde, Anne Marita ^a   Enger, Øystein ^a   Murison, Robert ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

Maternal separation; Stress responsivity; Ulcerative colitis

Indexed keywords

CORTICOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DISEASE ACTIVITY; FEMALE; INFLAMMATION; INTESTINE ULCER; MATERNAL DEPRIVATION; NONHUMAN; PRIORITY JOURNAL; RAT; RECTUM ULCER; STRESS;

EID: 1842575609     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2004.01.002     Document Type: Article

References (78)

1. McEwen B.S., Stellar E. Stress and the individual. Mechanisms leading to disease. Arch. Intern. Med. 153:1993;2093-2101.
2. Francis D.D., Meaney M.J. Maternal care and the development of stress responses. Curr. Opin. Neurobiol. 9:1999;128-134.
3. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry. 49:2001;1023-1039.
4. Kalinichev M., Easterling K.W., Holtzman S.G. Early neonatal experience of Long-Evans rats results in long-lasting changes in reactivity to a novel environment and morphine-induced sensitization and tolerance. Neuropsychopharmacology. 27:2002;518-533.
5. Heim C., Newport D.J., Wagner D., Wilcox M.M., Miller A.H., Nemeroff C.B. The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: a multiple regression analysis. Depress. Anxiety. 15:2002;117-125.
6. Wang S., Bartolome J.V., Schanberg S.M. Neonatal deprivation of maternal touch may suppress ornithine decarboxylase via downregulation of the proto-oncogenes c-myc and max. J. Neurosci. 16:1996;836-842.
7. Hofer M.A., Brunelli S.A., Masmela J., Shair H.N. Maternal interactions prior to separation potentiate isolation-induced calling in rat pups. Behav. Neurosci. 110:1996;1158-1167.
8. Wiener S.G., Bayart F., Faull K.F., Levine S. Behavioral and physiological responses to maternal separation in squirrel monkeys (Saimiri sciureus). Behav. Neurosci. 104:1990;108-115.
9. Stern J.M. Offspring-induced nurturance: animal-human parallels. Dev. Psychobiol. 31:1997;19-37.
10. Meerlo P., Horvath K.M., Nagy G.M., Bohus B., Koolhaas J.M. The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. J. Neuroendocrinol. 11:1999;925-933.
11. Meaney M.J., Mitchell J.B., Aitken D.H., Bhatnagar S., Bodnoff S.R., Iny L.J.et al. The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits in later life. Psychoneuroendocrinology. 16:1991;85-103.
12. Levine S. Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science. 156:1967;258-260.
13. Jans J.E., Woodside B.E. Nest temperature: effects on maternal behavior, pup development, and interactions with handling. Dev. Psychobiol. 23:1990;519-534.
14. Suchecki D., Rosenfeld P., Levine S. Maternal regulation of the hypothalamic-pituitary-adrenal axis in the infant rat: the roles of feeding and stroking. Brain Res. Dev. Brain Res. 75:1993;185-192.
15. Suchecki D., Nelson D.Y., Van Oers H., Levine S. Activation and inhibition of the hypothalamic-pituitary-adrenal axis of the neonatal rat: effects of maternal deprivation. Psychoneuroendocrinology. 20:1995;169-182.
16. Sapolsky R.M., Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 396:1986;64-76.
17. Emde R.N., Polak P.R., Spitz R.A. Anaclitic depression in an infant raised in an institution. J. Am. Acad. Child Psych. 4:1965;545-553.
18. Albers L.H., Johnson D.E., Hostetter M.K., Iverson S., Miller L.C. Health of children adopted from the former Soviet Union and eastern Europe. Comparison with preadoptive medical records. JAMA. 278:1997;922-924.
19. Lewis M.H., Gluck J.P., Petitto J.M., Hensley L.L., Ozer H. Early social deprivation in nonhuman primates: long-term effects on survival and cell-mediated immunity. Biol. Psychiatry. 47:2000;119-126.
20. Gutman D.A., Nemeroff C.B. Neurobiology of early life stress: rodent studies. Semin. Clin. Neuropsychiatry. 7:2002;89-95.
21. Zhang L.X., Levine S., Dent G., Zhan Y., Xing G., Okimoto D.et al. Maternal deprivation increases cell death in the infant rat brain. Brain Res. Dev. Brain Res. 133:2002;1-11.
22. Pihoker C., Owens M.J., Kuhn C.M., Schanberg S.M., Nemeroff C.B. Maternal separation in neonatal rats elicits activation of the hypothalamic-pituitary-adrenocortical axis: a putative role for corticotropin-releasing factor. Psychoneuroendocrinology. 18:1993;485-493.
23. van Oers H.J., de Kloet E.R., Whelan T., Levine S. Maternal deprivation effect on the infant's neural stress markers is reversed by tactile stimulation and feeding but not by suppressing corticosterone. J. Neurosci. 18:1998;10171-10179.
24. van Oers H.J., de Kloet E.R., Levine S. Persistent effects of maternal deprivation on HPA regulation can be reversed by feeding and stroking, but not by dexamethasone. J. Neuroendocrinol. 11:1999;581-588.
25. Plotsky P., Meaney M.J. Effects of early rearing environment on hypothalamic corticotrophin-releasing factor mRNA, synthesis, and stress-induced release. Mol. Brain Res. 18:1993;195-200.
26. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of behavioral fearfulness in adulthood in the rat. Proc. Natl. Acad. Sci. 95:1998;5335-5340.
27. Meaney M.J., Diorio J., Widdowson J., Laplante P., Caldji C., Seckl J.R.et al. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev. Neurosci. 18:1996;49-72.
28. Levine S. Enduring effects of early experience on adult behavior. Pfaff D.W., Rubin R.T., Arnold A.P., Etgen A.M., Fahrbach S.E. Hormones, brain and behavior. vol. 4:2002;535-542 Academic Press, San Diego.
29. Liu D.J., Diorio J., Tannenbaum B., Caldji C., Francis D., Freeman A.et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science. 277:1997;1659-1662.
30. Caldji C., Diorio J., Meaney M.J. Variations in maternal care in infancy regulate the development of stress reactivity. Biol. Psychiatry. 48:2000;1164-1174.
31. Lehmann J., Russig H., Feldon J., Pryce C.R. Effects of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats. Pharmacol. Biochem. Behav. 73:2002;141-145.
32. Kalinichev M., Easterling K.W., Plotsky P.M., Holtzman S.G. Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviours as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol. Biochem. Behav. 73:2002;131-140.
33. Coutinho S.V., Plotsky P.M., Sablad M., Miller J.C., Zhou H., Bayati A.I.et al. Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am. J. Physiol.: Gastrointest. Liver Physiol. 282:2002;307-316.
34. van Dijken H.H., Mos J., van der Heyden J.A., Tilders F.J. Characterization of stress-induced long-term behavioural changes in rats: evidence in favor of anxiety. Physiol. Behav. 52:1992;945-951.
35. van Dijken H.H., de Goeij D.C., Sutanto W., Mos J., de Kloet E.R., Tilders F.J. Short inescapable stress produces long-lasting changes in the brain-pituitary-adrenal axis of adult male rats. Neuroendocrinology. 58:1993;57-64.
36. Milde A.M., Sundberg H., Røseth A.G., Murison R. Proactive sensitizing effects of acute stress on acoustic startle responses and experimentally induced colitis in rats: relationship to corticosterone. Stress. 6:2003;49-57.
37. Weiner H. Psychobiology and human disease. 1977;Elsevier North-Holland, New York, USA. chapter 6.
38. Anton P.A. Stress and mind-body impact on the course of inflammatory bowel diseases. Semin. Gastrointest. Dis. 10:1999;14-19.
39. Levenstein S., Prantera C., Varvo V., Scribano M.L., Berto E., Andreoli A.et al. Psychological stress and disease activity in ulcerative colitis: a multidimensional cross-sectional study. Am. J. Gastroenterol. 89:1994;1219-1225.
40. North C.S., Alpers D.H., Helzer J.E., Spitznagel E.L., Clouse R.E. Do life events or depression exacerbate inflammatory bowel disease? A prospective study. Ann. Intern. Med. 114:1991;381-386.
41. Gué M., Bonbonne C., Fioramonti J., Moré J., Rio-Lechèze C.D., Coméra C.et al. Stress-induced enhancement of colitis in rats: CRF and arginine vasopressin are not involved. Am. J. Physiol. 272:1997;84-91.
42. Qiu B.S., Vallance B.A., Blennerhassett P.A., Collins S.M. The role of CD4+ lymphocytes in the susceptibility of mice to stress-induced reactivation of experimental colitis. Nat. Med. 5:1999;1178-1182.
43. Venkatraman A., Ramakrishna B.S., Pulimood A.B., Patra S., Murthy S. Increased permeability in dextran sulphate colitis in rats: time course of development and effect of butyrate. Scand. J. Gastroenterol. 35:2000;1053-1059.
44. Arslan G., Atasever T., Cindoruk M., Yildirim I.S. (51)CrEDTA colonic permeability and therapy response in patients with ulcerative colitis. Nucl. Med. Commun. 22:2001;997-1001.
45. Gaudio E., Taddei G., Vetuschi A., Sferra R., Frieri G., Ricciardi G.et al. Dextran sulphate sodium (DSS) colitis in rats. Clinical, structural and ultrastructural aspects. Dig. Dis. Sci. 44:1999;1458-1475.
46. Million M., Taché Y., Anton P. Susceptibility of Lewis and Fischer rats to stress-induced worsening of TNB-colitis: protective role of brain CRF. Am. J. Physiol. 276:1999;1027-1036.
47. Milde A.M., Murison R. A study of the effects of restraint stress on colitis induced by dextran sulphate sodium in singly housed rats. Integr. Physiol. Behav. Sci. 37:2002;140-150.
48. Söderholm J.D., Yates D.A., Gareau M.G., Yang P.-C., MacQuenn G., Perdue M.H. Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am. J. Physiol.: Gastrointest. Liver Physiol. 283:2002;1257-1263.
49. Aadland E., Fagerhol M.K. Faecal calprotectin: a marker of inflammation throughout the intestinal tract. Eur. J. Gastroenterol. Hepatol. 14:2002;823-825.
50. Røseth A.G., Aadland E., Jahnsen J., Raknerud N. Assessment of disease activity in ulcerative colitis by fecal calprotectin, a novel granulocyte marker protein. Digestion. 58:1997;176-180.
51. Kuhn C.M., Pauk J., Schanberg S.M. Endocrine responses to mother-infant separation in developing rats. Dev. Psychobiol. 23:1990;395-410.
52. Lehmann J., Pryce C.R., Bettschen D., Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol. Biochem. Behav. 64:1999;705-715.
53. Mahmud T., Somasundaram S., Sigthorsson G., Simpson R.J., Rafi S., Foster R.et al. Enantiomers of flurbiprofen can distinguish key pathophysiological steps of NSAID enteropathy in the rat. Gut. 43:1998;775-782.
54. Plotsky P.M., Meaney M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol. Brain Res. 18:1993;195-200.
55. Rots N.Y., de Jong D., Workel J.O., Levine S., Cools A.R., De Kloet A.R. Neonatal, maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J. Neuroendocrinol. 8:1996;501-506.
56. Overmier J.B. On learned helplessness. Integr. Physiol. Behav. Sci. 37:2002;4-8.
57. Levine S., Madden J., Conner R.L., Moskal J.R., Anderson D.C. Physiological and behavioral effects of prior aversive stimulation (preshock) in the rat. Physiol. Behav. 10:1973;467-471.
58. Bruijnzeel A.W., Stam R., Compaan J.C., Croiset G., Akkermans L.M., Olivier B.et al. Long-term sensitization of Fos-responsivity in the rat central nervous system after a single stressful experience. Brain Res. 819:1999;15-22.
59. 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. 50:1989;597-604.
60. 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. 55:1992;204-213.
61. Morgan C.A. III, Grillon C., Lubin H., Southwick S.M. Startle reflex abnormalities in women with sexual assault-related posttraumatic stress disorder. Am. J. Psychiatry. 154:1997;1076-1080.
62. Garrick T., Morrow N., Eth S., Marciano D., Shalev A. Psychophysiologic parameters of traumatic stress disorder in rats. Ann. N.Y. Acad. Sci. 821:1997;533-537.
63. Koch M. The neurobiology of startle. Prog. Neurobiol. 59:1999;107-128.
64. Davis M., Walker D.L., Lee Y. Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. Philos. Trans. R. Soc. Lond., B Biol. Sci. 352:1997;1675-1687.
65. Walker D.L., Davis M. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J. Neurosci. 17:1997;9375-9383.
66. Richardson R. Shock sensitization of startle: learned or unlearned fear? Behav. Brain Res. 110:2000;109-117.
67. Schwartz B., Robbins S.J. Psychology of learning and behavior. 4th ed. 1995;W.W. Norton and Company, New York.
68. Aranowitz R.A., Spiro H.M. The rise and fall of ulcerative colitis as a psychosomatic disease. J. Clin. Gastroenterol. 10:1988;298-305.
69. Mayer E.M. The neurobiology of stress and gastrointestinal disease. Gut. 47:2000;861-869.
70. Wood J.D., Peck O.C., Tefend K.S., Stonerook M.J., Caniano D.A., Mutabagani K.H.et al. Evidence that colitis is initiated by environmental stress and sustained by fecal factors in the cotton-top tamarind (Saguinus oedipus). Dig. Dis. Sci. 45:2000;385-393.
71. Murison R., Overmier J.B. Some psychosomatic causal factors of restraint-in-water stress ulcers. Physiol. Behav. 53:1993;577-581.
72. Elson C.O., Sartor R.B., Tennyson G.S., Riddell R.H. Experimental models of inflammatory bowel disease. Gastroenterology. 109:1995;1344-1367.
73. Anisman H., Zaharia M.D., Meaney M.J., Merali Z. Do early-life events permanently alter behavioral and hormonal responses to stressors? Int. J. Dev. Neurosci. 16:1998;149-164.
74. Dancey C.P., Taghavi M., Fox R.J. The relationship between daily stress and symptoms of irritable syndrome: a time-series approach. J. Psychosom. Res. 44:1998;537-545.
75. Røseth A.G., Schmidt P.N., Fagerhol M.K. Correlation between faecal excretion of indium-111-labelled granulocytes and calprotectin, a granulocyte marker protein, in patients with inflammatory bowel disease. Scand. J. Gastroenterol. 34:1999;50-54.
76. Kristinsson J., Røseth A.G., Sundset K., Nygaard K., Løberg E.M., Paulsen J.E.et al. Granulocyte marker protein is increased in stools from rats with azoxymethane-induced colon cancer. Scand. J. Gastroenterol. 34:1999;1216-1223.
77. Berstad A., Arslan G., Folvik G. Relationship between intestinal permeability and calprotectin concentration in gut lavage fluid. Scand. J. Gastroenterol. 35:2000;64-69.
78. Engel G.L. The need for a new medical model: a challenge for biomedicine. Science. 196:1977;129-136.