Parents' adulthood stress induces behavioral and hormonal alterations in male rat offspring

Behavioural Brain Research

Volumn 252, Issue , 2013, Pages 136-143

  Niknazar, Somayeh ^a   Nahavandi, Arezo ^a   Najafi, Rezvan ^a   Danialy, Samira ^a   Zare Mehrjerdi, Fatemeh ^a   Karimi, Mohsen ^b  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b PASTEUR INSTITUTE OF IRAN   (Iran)

Author keywords

Elevated plus maze; Hypothalamo pituitary adrenal axis; Maternal behavior; Offspring; Parental stress; Repeated swim stress

Indexed keywords

CORTICOSTERONE;

ADULTHOOD; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR; BEHAVIOR CHANGE; CHRONIC STRESS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HORMONE RESPONSE; MALE; MATERNAL BEHAVIOR; MAZE TEST; NONHUMAN; PARENTAL STRESS; PRIORITY JOURNAL; PROGENY; RAT;

ELEVATED PLUS MAZE; HYPOTHALAMO-PITUITARY-ADRENAL AXIS; MATERNAL BEHAVIOR; OFFSPRING; PARENTAL STRESS; REPEATED SWIM STRESS;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BIRTH WEIGHT; CORTICOSTERONE; DISEASE MODELS, ANIMAL; FEMALE; GROOMING; LINEAR MODELS; MALE; MATERNAL BEHAVIOR; MAZE LEARNING; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SEX FACTORS; STRESS, PSYCHOLOGICAL;

EID: 84879726911     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.05.026     Document Type: Article

References (58)

1. McEwen B.S. Stress, adaptation, and disease: allostasis and allostatic load. Annals of the New York Academy of Sciences 1998, 840:33-44.
2. Dietz D.M., LaPlant Q., Watts E.L., Hodes G.E., Russo S.J., Feng J., et al. Paternal transmission of stress-induced pathologies. Biological Psychiatry 2011, 70:408-414.
3. Ulrich-Lai Y.M., Figueiredo H.F., Ostrander M.M., Choi D.C., Engeland W.C., Herman J.P. Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. American Journal of Physiology - Endocrinology and Metabolism 2006, 291:E73-E965.
4. Gao L., Zou L., Zhang Z., Yuan C. Chronic administration of CRF makes depression like changes in rats. Fen zi xi bao sheng wu xue bao 2009, 42:95-100.
5. Gregus A., Wintink A.J., Davis A.C., Kalynchuk L.E. Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behavioural Brain Research 2005, 156:105-114.
6. Nishikawa H., Hata T., Itoh E., Funakami Y. A role for corticotropin-releasing factor in repeated cold stress-induced anxiety-like behavior during forced swimming and elevated plus-maze tests in mice. Biological and Pharmaceutical Bulletin 2004, 27:352-356.
7. Conrad C.D., McLaughlin K.J., Harman J.S., Foltz C., Wieczorek L., Lightner E., et al. Chronic glucocorticoids increase hippocampal vulnerability to neurotoxicity under conditions that produce CA3 dendritic retraction but fail to impair spatial recognition memory. The Journal of Neuroscience 2007, 27:8278-8285.
8. Wright R.L., Lightner E.N., Harman J.S., Meijer O.C., Conrad C.D. Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. European Journal of Neuroscience 2006, 24:595-605.
9. Hu Y., Gursoy E., Cardounel A., Kalimi M. Biological effects of single and repeated swimming stress in male rats. Endocrine 2000, 13:123-129.
10. Bosch O.J., Müsch W., Bredewold R., Slattery D.A., Neumann I.D. Prenatal stress increases HPA axis activity and impairs maternal care in lactating female offspring: implications for postpartum mood disorder. Psychoneuroendocrinology 2007, 32:267-278.
11. Lordi B., Patin V., Protais P., Mellier D., Caston J. Chronic stress in pregnant rats: effects on growth rate, anxiety and memory capabilities of the offspring. International Journal of Psychophysiology 2000, 37:195-205.
12. Götz A.A., Stefanski V. Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behaviour in adult male rat offspring. Physiology & Behavior 2007, 90:108-115.
13. George E.D., Bordner K.A., Elwafi H.M., Simen A.A. Maternal separation with early weaning: a novel mouse model of early life neglect. BMC Neuroscience 2010, 11:123.
14. Estanislau C., Morato S. Prenatal stress produces more behavioral alterations than maternal separation in the elevated plus-maze and in the elevated T-maze. Behavioural Brain Research 2005, 163:70-77.
15. Vallée M., Mayo W., Dellu F., Le Moal M., Simon H., Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. The Journal of Neuroscience 1997, 17:2626-2636.
16. Woodruff-Borden J., Morrow C., Bourland S., Cambron S. The behavior of anxious parents: examining mechanisms of transmission of anxiety from parent to child. Journal of Clinical Child and Adolescent Psychology 2002, 31:364-374.
17. Chiu Y.-H.M., Coull B.A., Cohen S., Wooley A., Wright R.J. Prenatal and postnatal maternal stress and wheeze in urban children effect of maternal sensitization. American Journal of Respiratory and Critical Care Medicine 2012, 186:147-154.
18. Rice F., Harold G., Boivin J., Van den Bree M., Hay D., Thapar A. The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences. Psychological Medicine 2010, 40:335-345.
19. Bögels S.M., Perotti E.C. Does father know best? A formal model of the paternal influence on childhood social anxiety. Journal of Child and Family Studies 2011, 20:171-181.
20. Shi S.-S., Shao S.-h., Yuan B.-p., Pan F., Li Z.-L. Acute stress and chronic stress change brain-derived neurotrophic factor (BDNF) and tyrosine kinase-coupled receptor (TrkB) expression in both young and aged rat hippocampus. Yonsei Medical Journal 2010, 51:661-671.
21. Myers M.M., Brunelli S.A., Squire J.M., Shindeldecker R.D., Hofer M.A. Maternal behavior of SHR rats and its relationship to offspring blood pressures. Developmental Psychobiology 1989, 22:29-53.
22. Ivy A.S., Brunson K.L., Sandman C., Baram T.Z. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 2008, 154:1132-1142.
23. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 1987, 92:180-185.
24. Pellow S., Chopin P., File S.E., Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. Journal of Neuroscience Methods 1985, 14:149-167.
25. Treit D., Menard J., Royan C. Anxiogenic stimuli in the elevated plus-maze. Pharmacology Biochemistry and Behavior 1993, 44:463-469.
26. Fernandes C., File S.E. The influence of open arm ledges and maze experience in the elevated plus-maze. Pharmacology Biochemistry and Behavior 1996, 54:31-40.
27. Adamec R., Shallow T. Effects of baseline anxiety on response to kindling of the right medial amygdala. Physiology & Behavior 2000, 70:67-80.
28. Adamec R., Shallow T., Burton P. Anxiolytic and anxiogenic effects of kindling-role of baseline anxiety and anatomical location of the kindling electrode in response to kindling of the right and left basolateral amygdala. Behavioural Brain Research 2005, 159:73-88.
29. Boyce-Rustay J.M., Cameron H.A., Holmes A. Chronic swim stress alters sensitivity to acute behavioral effects of ethanol in mice. Physiology & Behavior 2007, 91:77-86.
30. Makino S., Smith M., Gold P. Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology 1995, 136:3299-3309.
31. Zelena D., Mergl Z., Földes A., Kovacs K., Toth Z., Makara G. Role of hypothalamic inputs in maintaining pituitary-adrenal responsiveness in repeated restraint. American Journal of Physiology - Endocrinology and Metabolism 2003, 285:E7-E1110.
32. Gamallo A., Villanua A., Trancho G., Fraile A. Stress adaptation and adrenal activity in isolated and crowded rats. Physiology & Behavior 1986, 36:217-221.
33. Hata T., Nishikawa H., Itoh E., Funakami Y. Anxiety-like behavior in elevated plus-maze tests in repeatedly cold-stressed mice. The Japanese Journal of Pharmacology 2001, 85:189-196.
34. Albonetti M., Farabollini F. Behavioural responses to single and repeated restraint in male and female rats. Behavioural Processes 1992, 28:97-109.
35. Avital A., Richter-Levin G., Leschiner S., Spanier I., Veenman L., Weizman A., et al. Acute and repeated swim stress effects on peripheral benzodiazepine receptors in the rat hippocampus, adrenal, and kidney. Neuropsychopharmacology 2001, 25:669-678.
36. Rosenblatt J.S. Outline of the evolution of behavioral and nonbehavioral patterns of parental care among the vertebrates: critical characteristics of mammalian and avian parental behavior. Scandinavian Journal of Psychology 2003, 44:265-271.
37. Del Cerro M., Perez-Laso C., Ortega E., Martín J., Gomez F., Perez-Izquierdo M., et al. Maternal care counteracts behavioral effects of prenatal environmental stress in female rats. Behavioural Brain Research 2010, 208:593-602.
38. Smith J., Seckl J., Evans A., Costall B., Smythe J. Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 2004, 29:227-244.
39. Pérez-Laso C., Segovia S., Martín J.L.R., Ortega E., Gómez F., Del Cerro M.C.R. Environmental prenatal stress alters sexual dimorphism of maternal behavior in rats. Behavioural Brain Research 2008, 187:284-288.
40. Meek L.R., Dittel P.L., Sheehan M.C., Chan J.Y., Kjolhaug S.R. Effects of stress during pregnancy on maternal behavior in mice. Physiology & Behavior 2001, 72:473-479.
41. Champagne F.A., Meaney M.J. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biological Psychiatry 2006, 59:1227-1235.
42. Gonzalez A., Lovic V., Ward G.R., Wainwright P.E., Fleming A.S. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Developmental Psychobiology 2001, 38:11-32.
43. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 2001, 24:1161-1192.
44. Curley J.P., Mashoodh R., Champagne F.A. Epigenetics and the origins of paternal effects. Hormones and Behavior 2011, 59:306-314.
45. Mashoodh R., Franks B., Curley J.P., Champagne F.A. Paternal social enrichment effects on maternal behavior and offspring growth. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:17232-17238.
46. Cordero M.I., Poirier G., Marquez C., Veenit V., Fontana X., Salehi B., et al. Evidence for biological roots in the transgenerational transmission of intimate partner violence. Translational Psychiatry 2012, 2:e106. 10.1038/tp.2012.32.
47. Cameron N.M. Maternal programming of reproductive function and behavior in the female rat. Frontiers in Evolutionary Neuroscience 2011, 3. 10.3389/fnevo.2011.00010.
48. Takahashi L.K., Kalin N.H. Early developmental and temporal characteristics of stress-induced secretion of pituitary-adrenal hormones in prenatally stressed rat pups. Brain Research 1991, 558:75-78.
49. Mulder E., Robles de Medina P., Huizink A., Van den Bergh B., Buitelaar J., Visser G. Prenatal maternal stress: effects on pregnancy and the (unborn) child. Early Human Development 2002, 70:3-14.
50. Fish E.W., Shahrokh D., Bagot R., Caldji C., Bredy T., Szyf M., et al. Epigenetic programming of stress responses through variations in maternal care. Annals of the New York Academy of Sciences 2004, 1036:167-180.
51. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
52. Francis D.D., Caldji C., Champagne F., Plotsky P.M., Meaney M.J. The role of corticotropin-releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biological Psychiatry 1999, 46:1153-1166.
53. Francis D.D., Diorio J., Plotsky P.M., Meaney M.J. Environmental enrichment reverses the effects of maternal separation on stress reactivity. The Journal of Neuroscience 2002, 22:7840-7843.
54. Francis D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999, 286:1155-1158.
55. Tu M.T., Lupien S.J., Walker C.-D. Measuring stress responses in postpartum mothers: perspectives from studies in human and animal populations. Stress: The International Journal on the Biology of Stress 2005, 8:19-34.
56. Levine S. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 2005, 30:939-946.
57. Champagne F.A., Curley J.P., Keverne E.B., Bateson P.P. Natural variations in postpartum maternal care in inbred and outbred mice. Physiology & Behavior 2007, 91:325-334.
58. Franklin T.B., Russig H., Weiss I.C., Gräff J., Linder N., Michalon A., et al. Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry 2010, 68:408-415.