Chronic stress-induced changes in the rat brain: Role of sex differences and effects of long-term tianeptine treatment

Neuropharmacology

Volumn 75, Issue , 2013, Pages 426-436

  Kuipers, Sjoukje D ^a,c   Trentani, Andrea ^a,b,c   Van Der Zee, Eddy A ^b   Den Boer, Johan A ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF BERGEN   (Norway)

Author keywords

BrdU; Chronic stress; CREB phosphorylation; FOS expression; Sex differences; Tianeptine

Indexed keywords

BROXURIDINE; CORTICOSTERONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; TIANEPTINE;

ADAPTATION; AMYGDALOID NUCLEUS; ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHRONIC STRESS; DRUG EFFICACY; DRUG MECHANISM; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; FEMALE; FOOTSHOCK; HIPPOCAMPUS; HYPOPHYSIS ADRENAL SYSTEM; MALE; MOOD DISORDER; NERVE CELL PLASTICITY; NEUROBIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SEX DIFFERENCE;

BRDU; CHRONIC STRESS; CREB PHOSPHORYLATION; FOS EXPRESSION; SEX DIFFERENCES; TIANEPTINE;

ADRENAL GLANDS; ANIMALS; ANTIDEPRESSIVE AGENTS, TRICYCLIC; BODY WEIGHT; BROMODEOXYURIDINE; CORTICOSTERONE; CREB-BINDING PROTEIN; ELECTROSHOCK; FEMALE; HIPPOCAMPUS; MALE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SEX FACTORS; STRESS, PSYCHOLOGICAL; THIAZEPINES; THYMUS GLAND; TIME FACTORS;

EID: 84884336401     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.08.018     Document Type: Article

References (72)

1. M. Aihara, I. Ida, N. Yuuki, A. Oshima, H. Kumano, K. Takahashi, M. Fukuda, N. Oriuchi, K. Endo, H. Matsuda, and M. Mikuni HPA axis dysfunction in unmedicated major depressive disorder and its normalization by pharmacotherapy correlates with alteration of neural activity in prefrontal cortex and limbic/paralimbic regions Psychiatry Res. 155 2007 245 256 (Pubitemid 47042359)
2. C.K. Barha, S. Brummelte, S.E. Lieblich, and L.A. Galea Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats Hippocampus 21 2011 1216 1227
3. C.B. Brink, B.H. Harvey, and L. Brand Tianeptine: a novel atypical antidepressant that may provide new insights into the biomolecular basis of depression Recent Pat. CNS. Drug Discov. 1 2006 29 41
4. T. Bschor, M. Ising, S. Erbe, P. Winkelmann, D. Ritter, M. Uhr, and U. Lewitzka Impact of citalopram on the HPA system. A study of the combined DEX/CRH test in 30 unipolar depressed patients J. Psychiatr. Res. 46 2012 111 117
5. A.M. Campbell, C.R. Park, P.R. Zoladz, C. Munoz, M. Fleshner, and D.M. Diamond Pre-training administration of tianeptine, but not propranolol, protects hippocampus-dependent memory from being impaired by predator stress Eur. Neuropsychopharmacol. 18 2008 87 98
6. W.A. Carlezon Jr., R.S. Duman, and E.J. Nestler The many faces of CREB Trends Neurosci. 28 2005 436 445 (Pubitemid 40982557)
7. N. Carrier, and M. Kabbaj Sex differences in the antidepressant-like effects of ketamine Neuropharmacology 70 2013 27 34
8. R.N. Carter, S.B. Pinnock, and J. Herbert Does the amygdala modulate adaptation to repeated stress? Neuroscience 126 2004 9 19 (Pubitemid 38609102)
9. B. Czeh, T. Michaelis, T. Watanabe, J. Frahm, G. de Biurrun, M. van Kampen, A. Bartolomucci, and E. Fuchs Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine Proc. Natl. Acad. Sci. U. S. A. 98 2001 12796 12801 (Pubitemid 33020024)
10. G. Dagyte, E.A. Van der Zee, F. Postema, P.G. Luiten, J.A. Den Boer, A. Trentani, and P. Meerlo Chronic but not acute foot-shock stress leads to temporary suppression of cell proliferation in rat hippocampus Neuroscience 162 2009 904 913
11. G. Dagyte, A. Trentani, F. Postema, P.G. Luiten, J.A. Den Boer, C. Gabriel, E. Mocaer, P. Meerlo, and E.A. Van der Zee The novel antidepressant agomelatine normalizes hippocampal neuronal activity and promotes neurogenesis in chronically stressed rats CNS. Neurosci. Ther. 16 2010 195 207
12. G. Dagyte, P.G. Luiten, T. De Jager, C. Gabriel, E. Mocaër, J.A. Den Boer, and E.A. Van der Zee Chronic stress and antidepressant agomelatine induce region-specific changes in synapsin I expression in the rat brain J. Neurosci. Res. 89 2011 1646 1657
13. K. Dedovic, A. Duchesne, J. Andrews, V. Engert, and J.C. Pruessner The brain and the stress axis: the neural correlates of cortisol regulation in response to stress Neuroimage 47 2009 864 871
14. C. Delbende, B.D. Tranchand, G. Tarozzo, M. Grino, C. Oliver, E. Mocaer, and H. Vaudry Effect of chronic treatment with the antidepressant tianeptine on the hypothalamo-pituitary-adrenal axis Eur. J. Pharmacol. 251 1994 245 251 (Pubitemid 24061100)
15. R.S. Duman, and L.M. Monteggia A neurotrophic model for stress-related mood disorders Biol. Psychiatry 59 2006 1116 1127
16. I. Elakovic, A. Djordjevic, M. Adzic, J. Djordjevic, M. Radojcic, and G. Matic Gender-specific response of brain corticosteroid receptors to stress and fluoxetine Brain Res. 1384 2011 61 68
17. J.N. Flak, M.B. Solomon, R. Jankord, E.G. Krause, and J.P. Herman Identification of chronic stress-activated regions reveals a potential recruited circuit in rat brain Eur. J. Neurosci. 36 2012 2547 2555
18. G. Guidotti, F. Calabrese, C. Anacker, G. Racagni, C.M. Pariante, and M.A. Riva Glucocorticoid receptor and FKBP5 expression is altered following exposure to chronic stress: modulation by antidepressant treatment Neuropsychopharmacology 38 2013 616 627
19. R.W. Guillery On counting and counting errors J. Comp. Neurol. 447 2002 1 7 (Pubitemid 34298840)
20. N.D. Hanson, M.J. Owens, K.A. Boss-Williams, J.M. Weiss, and C.B. Nemeroff Several stressors fail to reduce adult hippocampal neurogenesis Psychoneuroendocrinology 36 2011 1520 1529
21. K.M. Hillerer, I.D. Neumann, S. Couillard-Despres, L. Aigner, and D.A. Slattery Sex-dependent regulation of hippocampal neurogenesis under basal and chronic stress conditions in rats Hippocampus 2013 Mar 18 10.1002/hipo.22107 (Epub ahead of print)
22. G.E. Hodes, T.E. Hill-Smith, R.F. Suckow, T.B. Cooper, and I. Lucki Sex-specific effects of chronic fluoxetine treatment on neuroplasticity and pharmacokinetics in mice J. Pharmacol. Exp. Ther. 332 2010 266 273
23. P.E. Holtzheimer, and H.S. Mayberg Stuck in a rut: rethinking depression and its treatment Trends Neurosci. 34 2011 1 9
24. P. Hughes, P. Lawlor, and M. Dragunow Basal expression of Fos, Fos-related, Jun, and Krox 24 proteins in rat hippocampus Brain Res. Mol. Brain Res. 13 1992 355 357
25. E. Jazin, and L. Cahill Sex differences in molecular neuroscience: from fruit flies to humans Nat. Rev. Neurosci. 11 2010 9 17
26. R.C. Kessler, K.A. McGonagle, M. Swartz, D.G. Blazer, and C.B. Nelson Sex and depression in the National Comorbidity Survey. I: lifetime prevalence, chronicity and recurrence J. Affect. Disord. 29 1993 85 96 (Pubitemid 23334116)
27. M.H. Kole, L. Swan, and E. Fuchs The antidepressant tianeptine persistently modulates glutamate receptor currents of the hippocampal CA3 commissural associational synapse in chronically stressed rats Eur. J. Neurosci. 16 2002 807 816 (Pubitemid 35463572)
28. K.J. Kovacs Measurement of immediate-early gene activation- c-fos and beyond J. Neuroendocrinol 20 2008 665 672 (Pubitemid 351858715)
29. S.D. Kuipers, A. Trentani, J.A. den Boer, and G.J. ter Horst Molecular correlates of impaired prefrontal plasticity in response to chronic stress J. Neurochem. 85 2003 1312 1323 (Pubitemid 36613278)
30. S.D. Kuipers, A. Trentani, C. Westenbroek, C.R. Bramham, J. Korf, I.P. Kema, G.J. Ter Horst, and J.A. Den Boer Unique patterns of FOS, phospho-CREB and BrdU immunoreactivity in the female rat brain following chronic stress and citalopram treatment Neuropharmacology 50 2006 428 440 (Pubitemid 43209039)
31. S.D. Kuipers, A. Tiron, J. Soule, E. Messaoudi, A. Trentani, and C.R. Bramham Selective survival and maturation of adult-born dentate granule cells expressing the immediate early gene Arc/Arg3.1 PLoS One 4 2009 e4885
32. T. Lee, T. Jarome, S.J. Li, J.J. Kim, and F.J. Helmstetter Chronic stress selectively reduces hippocampal volume in rats: a longitudinal magnetic resonance imaging study Neuroreport 20 2009 1554 1558
33. E. Leibenluft Gender differences in major depressive disorder and bipolar disorder CNS. Spectr. 4 1999 25 33 (Pubitemid 29491607)
34. B. Leuner, and E. Gould Structural plasticity and hippocampal function Annu. Rev. Psychol. 61 2010 111 113
35. G. MacQueen, and T. Frodl The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research? Mol. Psychiatry 16 2011 252 264
36. A.M. Magarinos, J.M. Verdugo, and B.S. McEwen Chronic stress alters synaptic terminal structure in hippocampus Proc. Natl. Acad. Sci. U. S. A. 94 1997 14002 14008 (Pubitemid 28009699)
37. A.M. Magarinos, A. Deslandes, and B.S. McEwen Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress Eur. J. Pharmacol. 371 1999 113 122 (Pubitemid 29216993)
38. J.E. Malberg, A.J. Eisch, E.J. Nestler, and R.S. Duman Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus J. Neurosci. 20 2000 9104 9110 (Pubitemid 32042912)
39. M. Martinez, A. Calvo-Torrent, and J. Herbert Mapping brain response to social stress in rodents with c-fos expression: a review Stress 5 2002 3 13 (Pubitemid 34241889)
40. B.S. McEwen, C.D. Conrad, Y. Kuroda, M. Frankfurt, A.M. Magarinos, and C. McKittrick Prevention of stress-induced morphological and cognitive consequences Eur. Neuropsychopharmacol. 7 Suppl. 3 1997 S323 S328
41. B.S. McEwen, S. Chattarji, D.M. Diamond, T.M. Jay, L.P. Reagan, P. Svenningsson, and E. Fuchs The neurobiological properties of tianeptine (Stablon): from monoamine hypothesis to glutamatergic modulation Mol. Psychiatry 15 2010 237 249
42. K.J. McLaughlin, S.E. Baran, and C.D. Conrad Chronic stress- and sex-specific neuromorphological and functional changes in limbic structures Mol. Neurobiol. 40 2009 166 182
43. M. Nibuya, E.J. Nestler, and R.S. Duman Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus J. Neurosci. 16 1996 2365 2372 (Pubitemid 26154346)
44. C.A. Oomen, C.E. Girardi, R. Cahyadi, E.C. Verbeek, H. Krugers, M. Joels, and P.J. Lucassen Opposite effects of early maternal deprivation on neurogenesis in male versus female rats PLoS One 4 2009 e3675
45. P. Palanza Animal models of anxiety and depression: how are females different? Neurosci. Biobehav. Rev. 25 2001 19 33
46. E. Palazidou The neurobiology of depression Br. Med. Bull. 101 2012 127 145
47. G. Parker, and H. Brotchie Gender differences in depression Int. Rev. Psychiatry 22 2012 429 436
48. I.A. Paul, and P. Skolnick Glutamate and depression: clinical and preclinical studies Ann. N. Y. Acad. Sci. 1003 2003 250 272 (Pubitemid 38083061)
49. J.J. Pratt Steroid immunoassay in clinical chemistry Clin. Chem. 24 1978 1869 1890 (Pubitemid 9049054)
50. J.L. Price, and W.C. Drevets Neurocircuitry of mood disorders Neuropsychopharmacology 35 2010 192 216
51. L.P. Reagan, D.R. Rosell, G.E. Wood, M. Spedding, C. Munoz, J. Rothstein, and B.S. McEwen Chronic restraint stress up-regulates GLT-1 mRNA and protein expression in the rat hippocampus: reversal by tianeptine Proc. Natl. Acad. Sci. U. S. A. 101 2004 2179 2184 (Pubitemid 38229035)
52. P.H. Roseboom, S.A. Nanda, V.P. Bakshi, A. Trentani, S.M. Newman, and N.H. Kalin Predator threat induces behavioral inhibition, pituitary-adrenal activation and changes in amygdala CRF-binding protein gene expression Psychoneuroendocrinology 32 2007 44 55 (Pubitemid 44959459)
53. L. Santarelli, M. Saxe, C. Gross, A. Surget, F. Battaglia, S. Dulawa, N. Weisstaub, J. Lee, R. Duman, O. Arancio, C. Belzung, and R. Hen Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants Science 301 2003 805 809 (Pubitemid 36962615)
54. T.J. Shors, J. Mathew, H.M. Sisti, C. Edgecomb, S. Beckoff, and C. Dalla Neurogenesis and helplessness are mediated by controllability in males but not in females Biol. Psychiatry 62 2007 487 495 (Pubitemid 47284029)
55. J.S. Snyder, A. Soumier, M. Brewer, J. Pickel, and H.A. Cameron Adult hippocampal neurogenesis buffers stress responses and depressive behaviour Nature 476 2011 458 461
56. M.B. Solomon, and J.P. Herman Sex differences in psychopathology: of gonads, adrenals and mental illness Physiol. Behav. 97 2009 250 258
57. J.J. Sramek, and N.R. Cutler The impact of gender on antidepressants Curr. Top. Behav. Neurosci. 8 2011 231 249
58. J. Stamp, and J. Herbert Corticosterone modulates autonomic responses and adaptation of central immediate-early gene expression to repeated restraint stress Neuroscience 107 2001 465 479 (Pubitemid 33079122)
59. R.M. Sullivan, and A. Gratton Lateralized effects of medial prefrontal cortex lesions on neuroendocrine and autonomic stress responses in rats J. Neurosci. 19 1999 2834 2840 (Pubitemid 29162429)
60. A. Surget, A. Tanti, E.D. Leonardo, A. Laugeray, Q. Rainer, C. Touma, R. Palme, G. Griebel, Y. Ibarguen-Vargas, R. Hen, and C. Belzung Antidepressants recruit new neurons to improve stress response regulation Mol. Psychiatry 16 2011 1177 1188
61. M. Szymanska, B. Budziszewska, L. Jaworska-Feil, A. Basta-Kaim, M. Kubera, M. Leskiewicz, M. Regulska, and W. Lason The effect of antidepressant drugs on the HPA axis activity, glucocorticoid receptor level and FKBP51 concentration in prenatally stressed rats Psychoneuroendocrinology 34 2009 822 832
62. P. Tanapat, N.B. Hastings, A.J. Reeves, and E. Gould Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat J. Neurosci. 19 1999 5792 5801 (Pubitemid 29327916)
63. J. Thome, N. Sakai, K. Shin, C. Steffen, Y.J. Zhang, S. Impey, D. Storm, and R.S. Duman cAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment J. Neurosci. 20 2000 4030 4036 (Pubitemid 30365673)
64. A. Trentani, S.D. Kuipers, G.J. Ter Horst, and J.A. Den Boer Selective chronic stress-induced in vivo ERK1/2 hyperphosphorylation in medial prefrontocortical dendrites: implications for stress-related cortical pathology? Eur. J. Neurosci. 15 2002 1681 1691 (Pubitemid 35471924)
65. A. Trentani, S.D. Kuipers, G.J. te Meerman, J. Beekman, G.J. ter Horst, and J.A. den Boer Immunohistochemical changes induced by repeated footshock stress: revelations of gender-based differences Neurobiol. Dis. 14 2003 602 618 (Pubitemid 37543537)
66. J.G. Veening, L.M. Coolen, W.J. Spooren, H. Joosten, R. van Oorschot, J. Mos, E. Ronken, and B. Olivier Patterns of c-fos expression induced by fluvoxamine are different after acute vs. chronic oral administration Eur. Neuropsychopharmacol. 8 1998 213 226 (Pubitemid 28334183)
67. C. Westenbroek, G.J. Ter Horst, M.H. Roos, S.D. Kuipers, A. Trentani, and J.A. Den Boer Gender-specific effects of social housing in rats after chronic mild stress exposure Prog. Neuropsychopharmacol. Biol. Psychiatry 27 2003 21 30 (Pubitemid 36126643)
68. C. Westenbroek, J.A. Den Boer, M. Veenhuis, and G.J. Ter Horst Chronic stress and social housing differentially affect neurogenesis in male and female rats Brain Res. Bull. 64 2004 303 308 (Pubitemid 39550765)
69. F.R. Westwood The female rat reproductive cycle: a practical histological guide to staging Toxicol. Pathol. 36 2008 375 384
70. G.Y. Wu, K. Deisseroth, and R.W. Tsien Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway Proc. Natl. Acad. Sci. U. S. A. 98 2001 2808 2813 (Pubitemid 32209565)
71. C.A. Zarate Jr., J. Du, J. Quiroz, N.A. Gray, K.D. Denicoff, J. Singh, D.S. Charney, and H.K. Manji Regulation of cellular plasticity cascades in the pathophysiology and treatment of mood disorders: role of the glutamatergic system Ann. N. Y. Acad. Sci. 1003 2003 273 291 (Pubitemid 38083062)
72. P.R. Zoladz, C.R. Park, C. Muñoz, M. Fleshner, and D.M. Diamond Tianeptine: an antidepressant with memory-protective properties Curr. Neuropharmacol 6 2008 311 321