Behavioural and biochemical changes in maternally separated Sprague–Dawley rats exposed to restraint stress

Metabolic Brain Disease

Volumn 31, Issue 1, 2016, Pages 121-133

  van Zyl, P J ^a   Dimatelis, J J ^a   Russell, V A ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Behaviour; Depression; Maternal separation; Proteomics; Restraint stress

Indexed keywords

ACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR; MITOCHONDRIAL PROTEIN;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BEHAVIOR CHANGE; BIOCHEMISTRY; CONTROLLED STUDY; DEPRESSION; ENERGY METABOLISM; FEMALE; FORCED SWIM TEST; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMOBILITY; IMMOBILIZATION STRESS; MALE; MAZE TEST; MITOCHONDRION; NONHUMAN; OPEN FIELD TEST; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PROTEOMICS; RAT; ANIMAL; ANIMAL BEHAVIOR; EXERCISE; MATERNAL DEPRIVATION; MENTAL STRESS; METABOLISM; PSYCHOLOGY; SEPARATION ANXIETY; SPRAGUE DAWLEY RAT;

ACTINS; ANIMALS; ANXIETY, SEPARATION; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; ENERGY METABOLISM; FEMALE; MALE; MATERNAL DEPRIVATION; MITOCHONDRIA; PREFRONTAL CORTEX; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL;

EID: 84946763808     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-015-9757-y     Document Type: Article

References (92)

1. Blaveri E, Kelly F, Mallei A, Harris K, Taylor A, Reid J, Razzoli M, Carboni L, Piubelli C, Musazzi L, Racagni G, Mathé A, Popoli M, Domenici E, Bates S (2010) Expression profiling of a genetic animal model of depression reveals novel molecular pathways underlying depressive-like behaviours. PLoS ONE 5:1–10.
2. Brotto LA, Gorzalka BB, Barr AM (2001) Paradoxical effects of chronic corticosterone on forced swim behaviours in aged male and female rats. Eur J Pharmacol 424:203–209.
3. Calabrese V, Scapagnini G, Giuffrida Stella AM, Bates TE, Clark JB (2001) Mitochondrial involvement in brain function and dysfunction: relevance to aging, neurodegenerative disorders and longevity. Neurochem Res 26:739–764.
4. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95:5335–5340.
5. Cancela LM, Rossi S, Molina VA (1991) Effect of different restraint schedules on the immobility in the forced swim test: modulation by an opiate mechanism. Brain Res Bull 26:671–675.
6. Carboni L, Becchi S, Piubelli C, Mallei A, Giambelli R, Razzoli M, Mathé AA, Popoli M, Domenici E (2010) Early-life stress and antidepressants modulate peripheral biomarkers in a gene–environment rat model of depression. Prog Neuro-Psychopharmacol Biol Psychiatry 34:1037–1048.
7. Castrén E, Rantamäki T (2010) Role of brain-derived neurotrophic factor in the aetiology of depression. CNS Drugs 24:1–7.
8. Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H (2012) Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brainderived neurotrophic factor in the prefrontal cortex. Prog Neuro- Psychopharmacol Biol Psychiatry 39:112–119.
9. Chourbaji S, Vogt MA, Fumagalli F, Sohr R, Frasca A, Brandwein C, Hörtnagl H, Riva MA, Sprengel R, Gass P (2008) AMPA receptor subunit 1 (GluR-A) knockout mice model the glutamate hypothesis of depression. FASEB J Off Publ Fed Am Soc Exp Biol 22: 3129–3134.
10. Clemens MJ, Bushell M, Morley SJ (1998) Degradation of eukaryotic polypeptide chain initiation factor (eIF) 4G in response to induction of apoptosis in human lymphoma cell lines. Oncogene 17: 2921–2931.
11. Clemens MJ, Bushell M, Jeffrey IW, Pain VM, Morley SJ (2000) Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death Differ 7:603–615.
12. Cryan JF, Markou A, Lucki I (2002) Assessing antidepressant activity in rodents: recent developments and future needs. TRENDS Pharmacol Sci 23:238–245.
13. Daniels WMU, Pietersen CY, Carstens ME, Stein DJ (2004) Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab Brain Dis 19:3–14.
14. Daniels WMU, Marais L, Stein DJ, Russell VA (2012) Exercise normalizes altered expression of proteins in the ventral hippocampus of rats subjected to maternal separation. Exp Physiol 97:239–247.
15. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG (2010) Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 170:1179–1188.
16. Dimatelis JJ, Russell VA, Stein DJ, Daniels WM (2012a) Effects of maternal separation andmethamphetamine exposure on protein expression in the nucleus accumbens shell and core. Metab Brain Dis 27: 363–375.
17. Dimatelis JJ, Stein DJ, Russell VA (2012b) Behavioral changes after maternal separation are reversed by chronic constant light treatment. Brain Res 1480:61–71.
18. Dimatel JJ, Russel l VA, Stein DJ, Daniels WM (2014) Methamphetamine reversed maternal separation-induced decrease in nerve growth factor in the ventral hippocampus. Metab Brain Dis 29:433–439.
19. Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitaryadrenal responses to stress. J Neurosci 13:3839–3847.
20. Eiland L, McEwen BS (2012) Early life stress followed by subsequent adult chronic stress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus 22:82–91.
21. Francis DD, Meaney MJ (1999) Maternal care and the development of stress responses. Curr Opin Neurobiol 9:128–134.
22. Gale M Jr., Tan SL, Katze MG (2000) Translational control of viral gene expression in eukaryotes. Microbiol Mol Biol Rev: MMBR 64:239–280.
23. Gass P, Riva MA (2007) CREB, neurogenesis and depression. Bioessays: News Rev Mol Cell Dev Biol 29:957–961.
24. Greisen MH, Altar CA, Bolwig TG, Whitehead R, Wörtwein G (2005) Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis inmaternal separation rats. J Neurosci Res 79:772–778.
25. Han X, Shao W, Liu Z, Fan S, Yu J, Chen J, Qiao R, Zhou J, Xie P (2015) iTRAQ-based quantitative analysis of hippocampal postsynaptic density-associated proteins in a rat chronic mild stress model of depression. Neuroscience 298:220–292.
26. Hansson AC, Rimondini R, Heilig M, Mathé AA, Sommer WH (2011) Dissociation of antidepressant-like activity of escitalopram and nortriptyline on behaviour and hippocampal BDNF expression in female rats. J Psychopharmacol 25:1378–1387.
27. Harkness KL, Bruce AE, Lumley MN (2006) The role of childhood abuse and neglect in the sensitization to stressful life events in adolescent depression. J Abnorm Psychol 115:730–741.
28. Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78–84.
29. Hong IS, Lee HY, Kim HP (2014) Anti-oxidative effects of rooibos tea (Aspalathus linearis) on immobilization-induced oxidative stress in rat brain. PLoS ONE 9:1–9.
30. Husum H, Wörtwein G, Andersson W, Bolwig TG, Mathé AA (2008) Gene-environment interaction affects substance P and neurokinin A in the entorhinal cortex and periaqueductal grey in a genetic animal model of depression: implications for the pathophysiology of depression. Int J Neuropsychopharmacol 11:93–101.
31. Kendler KS, Karkowski LM, Prescott CA (1998) Stressful life events and major depression: risk period, long-term contextual threat, and diagnostic specificity. J Nerv Mental Dis 186:661–669.
32. Kendler KS, Karkowski LM, Prescott CA (1999) Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 156:837–841.
33. Kuroda Y, McEwen BS (1998) Effect of chronic restraint stress and tianeptine on growth factors, growth-associated protein-43 and microtubule-associated protein 2 mRNA expression in the rat hippocampus. Brain Res Mol Brain Res 59:35–39.
34. Lambás-Señas L, Mnie-Filali O, Certin V, Faure C, Lemoine L, Zimmer L, Haddjeri N (2009) Functional correlates for 5-HT1A receptors in maternally deprived rats displaying anxiety and depression-like behaviors. Prog Neuro-Psychopharmacol Biol Psychiatry 33:262–268.
35. Larsen MH, Mikkelsen JD, Hay-Schmidt A, Sandi C (2010) Regulation of brain-derived neurotrophic factor (BDNF) in the chronic unpredictable stress rat model and the effects of chronic antidepressant treatment. J Psychiatr Res 44:808–816.
36. Lee B, Sur B, Park J, Kim SH, Kwon S, Yeom M, Shim I, Lee H, Hahm DH (2013) Chronic administration of baicalein decreases depression-like behavior induced by repeated restraint stress in rats. Korean J Physiol Pharmacol 17:393–403.
37. Lees-Miller JP, Goodwin LO, Helfman DM (1990) Three novel brain tropomyosin isoforms are expressed from the rat alphatropomyosin gene through the use of alternative promoters and alternative RNA processing. Mol Cell Biol 10:1729–1742.
38. Li X, Tizzano JP, Griffey K, Clay M, Lindstrom T, Skolnick P (2001) Antidepressant-like actions of an AMPA receptor potentiator (LY392098). Neuropharmacology 40:1028–1033.
39. Lindvall O, Kokaia Z, Bengzon J, Elmér E, Kokaia M (1994) Neurotrophins and brain insults. Trends Neurosci 17:490–496.
40. Liu SJ, Zukin RS (2007) Ca2+−permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 30:126–134.
41. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamicpituitary- adrenal responses to stress. Science (New York, NY) 277:1659–1662.
42. Madrigal JL, Olivenza R, Moro MA, Lizasoain I, Lorenzo P, Rodrigo J, Leza JC (2001) Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 24:420–429.
43. Mallei A, Giambelli R, Gass P, Racagni G, Mathé AA, Vollmayr B, Popoli M (2011) Synaptoproteomics of learned helpless rats involve energy metabolism and cellular remodeling pathways in depressivelike behavior and antidepressant response. Neuropharmacology 60: 1243–1253.
44. Marais L, van Rensburg SJ, van Zyl JM, Stein DJ, Daniels WMU (2008) Maternal separation of rat pups increases the risk of developing depressive-like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus. Neurosci Res 61:106–112.
45. Martinez-Turrillas R, Frechilla D, Del Río J (2002) Chronic antidepressant treatment increases the membrane expression of AMPA receptors in rat hippocampus. Neuropharmacology 43:1230–1237.
46. Martínez-Turrillas R, Del Río J, Frechilla D (2007) Neuronal proteins involved in synaptic targeting of AMPA receptors in rat hippocampus by antidepressant drugs. Biochem Biophys Res Commun 353: 750–755.
47. Mathé AA, Husum H, Khoury AE, Jiménez-Vasquez P, Gruber SHM, Wörtwein G, Nikisch G, Baumann P, Ågren H, Andersson W, Södergren Å, Angelucci F (2007) Search for biological correlates of depression and mechanisms of action of antidepressant treatment modalities. Do neuropeptides play a role. Physiol Behav 92: 226–231.
48. McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295–318.
49. McEwen BS (2000) The neurobiology of stress: from serendipity to clinical relevance. Brain Res 886:172–189.
50. McEwen BS (2008) Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 583:174–185.
51. Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann Rev Neurosci 24:1161–1192.
52. Mochida S (1995) Role of myosin in neurotransmitter release: functional studies at synapses formed in culture. J Physiol, Paris 89:83–94.
53. Mu J, Xie P, Yang ZS, Yang DL, Lv FJ, Luo TY, Li Y (2007) Neurogenesis and major depression: implications from proteomic analyses of hippocampal proteins in a rat depression model. Neurosci Lett 416:252–256.
54. Naert G, Ixart G, Maurice T, Tapia-Arancibia L, Givalois L (2011) Brainderived neurotrophic factor and hypothalamic-pituitary-adrenal axis adaptation processes in a depressive-like state induced by chronic restraint stress. MCN: Mol Cell Neurosci 46:55–66.
55. O’Connor TM, O’Halloran DJ, Shanahan F (2000) The stress response and the hypothalamic-pituitary-adrenal axis: from molecule to melancholia. QJM: Mon J Assoc Phys 93:323–333.
56. Paxinos G, Watson C (1986) The rat brain on stereotaxic co-ordinates, 2nd edn. Academic, San Diego
57. Pickering C, Gustafsson L, Cebere A, Nylander I, Liljequist S (2006) Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res 1099:101–108.
58. Pigino G, Kirkpatrick LL, Brady ST (2006) The cytoskeleton of neurons and glia. In: Siegel G, Albers RW, Brady S, Price D (eds) Basic neurochemistry: molecular, cellular, and medical aspects. Elsevier Academic Press, USA, pp 123–137.
59. Piubelli C, Vighini M, Mathé AA, Domenici E, Carboni L (2011) Escitalopram modulates neuron-remodelling proteins in a rat geneenvironment interaction model of depression as revealed by proteomics. Part I: genetic background. Int J Neuropsychopharmacol 14: 796–833.
60. Platt JE, Stone EA (1982) Chronic restraint stress elicits a positive antidepressant response on the forced swim test. Eur J Pharmacol 82: 179–181.
61. Popoli M, Mori S, Brunello N, Perez J, Gennarelli M, Racagni G (2001) Serine/threonine kinases as molecular targets of antidepressants: implications for pharmacological treatment and pathophysiology of affective disorders. Pharmacol Ther 89:149–170.
62. Raison CL, Miller AH (2003) When not enough is too much: the role of insufficient glucocorticoid signaling in the pathophysiology of stress-related disorders. Am J Psychiatry 160:1554–1565.
63. Rasmusson AM, Shi L, Duman R (2002) Downregulation of BDNF mRNA in the hippocampal dentate gyrus after re-exposure to cues previously associated with footshock. Neuropsychopharmacology 27:133–142.
64. Ray B, Gaskins DL, Sajdyk TJ, Spence JP, Fitz SD, Shekhar A, Lahiri DK (2011) Restraint stress and repeated corticotrophin-releasing factor receptor activation in the amygdala both increase amyloid-b precursor protein and amyloid-b peptide but have divergent effects on brain-derived neurotrophic factor and pre-synaptic proteins in the prefrontal cortex of rats. Neuroscience 184:139–150.
65. Reagan LP, Hendry RM, Reznikov LR, Piroli GG, Wood GE, McEwen BS, Grillo CA (2007) Tianeptine increases brain-derived neurotrophic factor expression in the rat amygdala. Eur J Pharmacol 565:68–75.
66. Réus GZ, Abelaira HM, Maciel AL, dos Santos MA, Carlessi AS, Steckert AV, Ferreira GK, De Prá SD, Streck EL, Macêdo DS, Quevedo J (2014) Minocycline protects against oxidative damage and alters energy metabolism parameters in the brain of rats subjected to chronic mild stress. Metab Brain Dis 30:545–553.
67. Roceri M, Cirulli F, Pessina C, Peretto P, Racagni G, Riva MA (2004) Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol Psychiatry 55:708–714.
68. Rosenbrock H, Koros E, Bloching A, Podhorna J, Borsini F (2005) Effect of chronic intermittent restraint stress on hippocampal expression of marker proteins for synaptic plasticity and progenitor cell proliferation in rats. Brain Res 1040:55–63.
69. Rüedi-Bettschen D, Pedersen EM, Feldon J, Pryce CR (2005) Early deprivation under specific conditions leads to reduced interest in reward in adulthood in Wistar rats. Behav Brain Res 156:297–310.
70. Rutter M (2007) Psychopathological development across adolescence. J Youth Adolesc 36:101–110.
71. Rutter M (2010) Gene–environment interplay. Depress Anxiety 27:1–4.
72. Ryan B, Musazzi L, Mallei A, Tardito D, Gruber SHM, El Khoury A, Anwyl R, Racagni G, Mathé AA, Rowan MJ, Popoli M (2009) Remodelling by early-life stress of NMDA receptor-dependent synaptic plasticity in a gene-environment rat model of depression. Int J Neuropsychopharmacol 12:553–559.
73. Serang O, Cansizoglu AE, Käll L, Steen H, Steen JA (2013) Nonparametric Bayesian evaluation of differential protein quantification. J Proteome Res 12:4556–4565.
74. Sheikh MS, Fornace AJ (1999) Regulation of translation initiation following stress. Oncogene 18:6121–6128.
75. Suvrathan A, Tomar A, Chattarji S (2010) Effects of chronic and acute stress on rat behaviour in the forced-swim test. Stress: Int J Biol Stress 13:533–540.
76. Swiergiel AH, Zhou Y, Dunn AJ (2007) Effects of chronic footshock, restraint and corticotropin-releasing factor on freezing, ultrasonic vocalization and forced swim behavior in rats. Behav Brain Res 183:178–187.
77. Tabassum I, Siddiqui ZN, Rizvi SJ (2010) Effects of Ocimum sanctum and Camellia sinensis on stress-induced anxiety and depression in male albino Rattus norvegicus. Indian J Pharm 42:283–288.
78. Tamburella A, Micale V, Leggio GM, Drago F (2010) The beta3 adrenoceptor agonist, amibegron (SR58611A) counteracts stressinduced behavioral and neurochemical changes. Eur Neuropsychopharmacol: J Eur Coll Neuropsychopharmacol 20: 704–713.
79. Tobe EH (2013) Mitochondrial dysfunction, oxidative stress, and major depressive disorder. Neuropsychiatr Dis Treat 9:567–573.
80. Uchida S, Hara K, Kobayashi A, Funato H, Hobara T, Otsuki K, Yamagata H, McEwen BS, Watanabe Y (2010) Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. J Neurosci 30:15007–15018.
81. Ulloa JL, Castañeda P, Berríos C, Díaz-Veliz G, Mora S, Bravo JA, Araneda K, Menares C, Morales P, Fiedler JL (2010) Comparison of the antidepressant sertraline on differential depression-like behaviors elicited by restraint stress and repeated corticosterone administration. Pharmacol Biochem Behav 97:213–221.
82. Uys JDK, Hattingh S, Stein DJ, Daniels WMU (2008) Large scale hippocampal cellular distress may explain the behavioral consequences of repetitive traumatic experiences: a proteomic approach. Neurochem Res 33:1724–1734
83. van Heerden JH, Russell V, Korff A, Stein DJ, Illing N (2010) Evaluating the behavioural consequences of early maternal separation in adult C57BL/6 mice; the importance of time. Behav Brain Res 207:332–342
84. van Veen T, Wardenaar KJ, Carlier IVE, Spinhoven P, Penninx BWJH, Zitman FG (2013) Are childhood and adult life adversities differentially associated with specific symptom dimensions of depression and anxiety? Testing the tripartite model. J Affect Disord 146:238–245.
85. Wang F, Qiao M, Xue L, Wei S (2015) Possible involvement of μ opioid receptor in the antidepressant-like effect of Shuyu formula in restraint stress-induced depression-like rats. Evid-based Complement Alternat Med (eCAM) 2015:1–11.
86. Wörtwein G, Husum H, Andersson W, Bolwig TG, Mathé AA (2006) Effects ofmaternal separation on neuropetide Yand calcitonin generelated peptide in ‘depressed’ Flinders sensitive line rats: a study of gene-environment interactions. Prog Neuro-Psychopharmacol Biol Psychiatry 30:684–693.
87. Wu WW, Wang G, Baek SJ, Shen RF (2006) Comparative study of three proteomic quantitative methods, DIGE, cICAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF. J Proteome Res 5:651–658.
88. Xu H, Luo C, Richardson JS, Li XM (2004) Recovery of hippocampal cell proliferation and BDNF levels, both of which are reduced by repeated restraint stress, is accelerated by chronic venlafaxine. Pharmacogenomics J 4:322–331.
89. Xu H, Chen Z, He J, Haimanot S, Li X, Dyck L, Li XM (2006) Synergetic effects of quetiapine and venlafaxine in preventing the chronic restraint stress-induced decrease in cell proliferation and BDNF expression in rat hippocampus. Hippocampus 16:551–559.
90. Yan Q, Rosenfeld RD, Matheson CR, Hawkins N, Lopez OT, Bennett L, Welcher AA (1997) Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience 78: 431–448.
91. Yoo SB, Kim BT, Kim JY, Ryu V, Kang DW, Lee JH, Jahng JW (2013) Adolescence fluoxetine increases serotonergic activity in the raphehippocampus axis and improves depression-like behaviors in female rats that experienced neonatal maternal separation. Psychoneuroendocrinology 38:777–788.
92. Zimmerberg B, Sageser KA (2011) Comparison of two rodent models of maternal separation on juvenile social behavior. Front Psychiatry 2:39–49