Prereproductive stress to female rats alters corticotropin releasing factor type 1 expression in ova and behavior and brain corticotropin releasing factor type 1 expression in offspring

Biological Psychiatry

Volumn 74, Issue 9, 2013, Pages 680-687

  Zaidan, Hiba ^a,b   Leshem, Micah ^a   Gaisler Salomon, Inna ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Behavior CRF1 oocyte rat stress transgenerational

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR TYPE 1; MESSENGER RNA; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR; BRAIN REGION; CLIMBING; CONTROLLED STUDY; FEAR; FEMALE; FRONTAL CORTEX; MALE; MATERNAL STRESS; MAZE TEST; NEWBORN; NONHUMAN; OOCYTE; OPEN FIELD TEST; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; STARTLE REFLEX;

BEHAVIOR; CRF1; OOCYTE; RAT; STRESS; TRANSGENERATIONAL;

ANIMALS; ANIMALS, NEWBORN; ANXIETY; BEHAVIOR, ANIMAL; BRAIN; FEMALE; MALE; MOTHERS; OOCYTES; RATS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RESTRAINT, PHYSICAL; RNA, MESSENGER; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 84885435415     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.04.014     Document Type: Article

References (53)

1. L. Baider, T. Peretz, P.E. Hadani, S. Perry, R. Avramov, and A.K. De-Nour Transmission of response to trauma? Second-generation Holocaust survivors' reaction to cancer Am J Psychiatry 157 2000 904 910
2. R. Yehuda, and L.M. Bierer Transgenerational transmission of cortisol and PTSD risk Prog Brain Res 167 2008 121 135
3. D.K. Nagata The Japanese American internment: Exploring the transgenerational consequences of traumatic stress J Trauma Stress 3 1990 47 69
4. D. Kupelian, A.S. Kalayjian, and A. Kassabian The Turkish Genocide of the Armenians: Continuing Effects on Survivors and their Families Eight Decades After Massive Trauma 1998 Plenum Press New York
5. M.H. van-IJzendoorn, M.J. Bakermans-Kranenburg, and A. Sagi-Schwartz Are children of Holocaust survivors less well-adapted? A meta-analytic investigation of secondary traumatization J Trauma Stress 16 2003 459 469
6. A. Sagi-Schwartz, M.H. van IJzendoorn, and M.J. Bakermans-Kranenburg Does intergenerational transmission of trauma skip a generation? No meta-analytic evidence for tertiary traumatization with third generation of Holocaust survivors Attach Hum Dev 10 2008 105 121
7. T.B. Franklin, N. Linder, H. Russig, B. Thony, and I.M. Mansuy Influence of early stress on social abilities and serotonergic functions across generations in mice PLoS One 6 2011 e21842
8. I.C. Weiss, T.B. Franklin, S. Vizi, and I.M. Mansuy Inheritable effect of unpredictable maternal separation on behavioral responses in mice Front Behav Neurosci 5 2011 3 doi:10.3389/fnbeh.2011.00003
9. F.A. Champagne Epigenetic mechanisms and the transgenerational effects of maternal care Front Neuroendocrinol 29 2008 386 397
10. F.A. Champagne, and M.J. Meaney Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty Behav Neurosci 121 2007 1353 1363
11. T.L. Roth, F.D. Lubin, A.J. Funk, and J.D. Sweatt Lasting epigenetic influence of early-life adversity on the BDNF gene Biol Psychiatry 65 2009 760 769
12. M. Weinstock The long-term behavioural consequences of prenatal stress Neurosci Biobehav Rev 32 2008 1073 1086
13. M. Leshem, and J. Schulkin Transgenerational effects of infantile adversity and enrichment in male and female rats Dev Psychobiol 54 2012 169 186
14. A. Shachar-Dadon, J. Schulkin, and M. Leshem Adversity before conception will affect adult progeny in rats Dev Psychol 45 2009 9 16
15. H.H. Li, L. Zhang, Z.M. Fang, L.Y. Lin, C.R. Wu, and Q.J. Huang Behavioral and neurobiological studies on the male progeny of maternal rats exposed to chronic unpredictable stress before pregnancy Neurosci Lett 469 2010 278 282
16. D.M. Dietz, Q. Laplant, E.L. Watts, G.E. Hodes, S.J. Russo, and J. Feng Paternal transmission of stress-induced pathologies Biol Psychiatry 70 2011 408 414
17. R. Yehuda, S.M. Engel, S.R. Brand, J. Seckl, S.M. Marcus, and G.S. Berkowitz Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy J Clin Endocrinol Metab 90 2005 4115 4118
18. T.B. Franklin, H. Russig, I.C. Weiss, J. Graff, N. Linder, and A. Michalon Epigenetic transmission of the impact of early stress across generations Biol Psychiatry 68 2010 408 415
19. M. Larauche, G. Gourcerol, L.X. Wang, K. Pambukchian, S. Brunnhuber, and D.W. Adelson Cortagine, a CRF1 agonist, induces stresslike alterations of colonic function and visceral hypersensitivity in rodents primarily through peripheral pathways Am J Physiol Gastrointest Liver Physiol 297 2009 G215 G227
20. M. Ising, U.S. Zimmermann, H.E. Kunzel, M. Uhr, A.C. Foster, and S.M. Learned-Coughlin High-affinity CRF1 receptor antagonist NBI-34041: Preclinical and clinical data suggest safety and efficacy in attenuating elevated stress response Neuropsychopharmacology 32 2007 1941 1949
21. G. Aguilera, M. Nikodemova, P.C. Wynn, and K.J. Catt Corticotropin releasing hormone receptors: Two decades later Peptides 25 2004 319 329
22. G. Wypior, U. Jeschke, M. Kurpisz, and J. Szekeres-Bartho Expression of CRH, CRH-related peptide and CRH receptor in the ovary and potential CRH signalling pathways J Reprod Immunol 90 2011 67 73
23. R.E. Nappi, and S. Rivest Stress-induced genetic expression of a selective corticotropin-releasing factor-receptor subtype within the rat ovaries: An effect dependent on the ovulatory cycle Biol Reprod 53 1995 1417 1428
24. L. Regev, M. Tsoory, S. Gil, and A. Chen Site-specific genetic manipulation of amygdala corticotropin-releasing factor reveals its imperative role in mediating behavioral response to challenge Biol Psychiatry 71 2012 317 326
25. J. Bohacek, K. Gapp, B.J. Saab, and I.M. Mansuy Transgenerational epigenetic effects on brain functions Biol Psychiatry 73 2013 313 320
26. B. Tannenbaum, G.S. Tannenbaum, K. Sudom, and H. Anisman Neurochemical and behavioral alterations elicited by a chronic intermittent stressor regimen: Implications for allostatic load Brain Res 953 2002 82 92
27. I. Zohar, and M. Weinstock Differential effect of prenatal stress on the expression of corticotrophin-releasing hormone and its receptors in the hypothalamus and amygdala in male and female rats J Neuroendocrinol 23 2011 320 328
28. I. Gaisler-Salomon, Y. Wang, N. Chuhma, H. Zhang, Y.N. Golumbic, and A. Mihali Synaptic underpinnings of altered hippocampal function in glutaminase-deficient mice during maturation Hippocampus 22 2012 1027 1039
29. E. Choleris, A.W. Thomas, M. Kavaliers, and F.S. Prato A detailed ethological analysis of the mouse open field test: Effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field Neurosci Biobehav Rev 25 2001 235 260
30. S. Pellow, P. Chopin, S.E. File, and M. Briley Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat J Neurosci Methods 14 1985 149 167
31. M. Davis The mammalian startle response R.C. Eaton, Neural Mechanisms of Startle Behavior 1984 Plenum New York 287 351
32. S. Maren Neurobiology of Pavlovian fear conditioning Annu Rev Neurosci 24 2001 897 931
33. K.L. Brunson, D.E. Grigoriadis, M.T. Lorang, and T.Z. Baram Corticotropin-releasing hormone (CRH) downregulates the function of its receptor (CRF1) and induces CRF1 expression in hippocampal and cortical regions of the immature rat brain Exp Neurol 176 2002 75 86
34. S.N. Kalantaridou, A. Makrigiannakis, G. Mastorakos, and G.P. Chrousos Roles of reproductive corticotropin-releasing hormone Ann N Y Acad Sci 997 2003 129 135
35. E. Kiapekou, E. Zapanti, G. Mastorakos, and D. Loutradis Update on the role of ovarian corticotropin-releasing hormone Ann N Y Acad Sci 1205 2010 225 229
36. D. Govorko, R.A. Bekdash, C. Zhang, and D.K. Sarkar Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations Biol Psychiatry 72 2012 378 388
37. R. Jaenisch, and A. Bird Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals Nat Genet 33 2003 245 254
38. L. Sterrenburg, B. Gaszner, J. Boerrigter, L. Santbergen, M. Bramini, and E. Elliott Chronic stress induces sex-specific alterations in methylation and expression of corticotropin-releasing factor gene in the rat PLoS One 6 2011 e28128
39. J.P. Curley, and R. Mashoodh Parent-of-origin and trans-generational germline influences on behavioral development: The interacting roles of mothers, fathers, and grandparents Dev Psychobiol 52 2010 312 330
40. Y. Huang, H. Xu, H. Li, H. Yang, Y. Chen, and X. Shi Pre-gestational stress reduces the ratio of 5-HIAA to 5-HT and the expression of 5-HT1A receptor and serotonin transporter in the brain of foetal rat BMC Neurosci 13 2012 22
41. P.A. Dell, and F.D. Rose Transfer of effects from environmentally enriched and impoverished female rats to future offspring Physiol Behav 39 1987 187 190
42. A.V. Kalueff, C.L. Jensen, and D.L. Murphy Locomotory patterns, spatiotemporal organization of exploration and spatial memory in serotonin transporter knockout mice Brain Res 1169 2007 87 97
43. I. Lapin, R. Khaunina, and S. Mirzaev Vertical motor activity of mice is slowed by lower doses of psychotropic drugs than horizontal Bull Exp Biol Med 120 1995 385 387
44. E. Ericson, J. Samuelsson, and S. Ahlenius Photocell measurements of rat motor activity. A contribution to sensitivity and variation in behavioral observations J Pharmacol Methods 25 1991 111 122
45. L. Prut, and C. Belzung The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: A review Eur J Pharmacol 463 2003 3 33
46. G. Zhang, G. Shi, H. Tan, Y. Kang, and H. Cui Intranasal administration of testosterone increased immobile-sniffing, exploratory behavior, motor behavior and grooming behavior in rats Horm Behav 59 2011 477 483
47. M.D. Kendig, M.T. Bowen, A.H. Kemp, and I.S. McGregor Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience Behav Brain Res 225 2011 405 414
48. M.J. Meaney The development of individual differences in behavioral and endocrine responses to stress Annu Rev Neurosci 24 2001 1161 1192
49. A.A. Agrawal, C. Laforsch, and R. Tollrian Transgenerational induction of defences in animals and plants Nature 401 1999 60 63
50. T.G.G. Groothuis, W. Muller, N. von Engelhardt, C. Carere, and C. Eising Maternal hormones as a tool to adjust offspring phenotype in avian species Neurosci Biobehav Rev 29 2005 329 352
51. H. Cohen, and R. Yehuda Gender differences in animal models of posttraumatic stress disorder Dis Markers 30 2011 141 150
52. S. Jacobson-Pick, and G. Richter-Levin Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats Behav Brain Res 214 2010 268 276
53. T. Ricon, E. Toth, M. Leshem, K. Braun, and G. Richter-Levin Unpredictable chronic stress in juvenile or adult rats has opposite effects, respectively, promoting and impairing resilience Stress 15 2012 11 20