Chronic variable stress alters inflammatory and cholinergic parameters in hippocampus of rats

Neurochemical Research

Volumn 36, Issue 3, 2011, Pages 487-493

  Tagliari, Bárbara ^a   Tagliari, Ana Paula ^a   Schmitz, Felipe ^a   Da Cunha, Aline A ^a   Dalmaz, Carla ^a   Wyse, Angela T S ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Acetylcholinesterase; Chronic variable stress; Depression; Neuroinflammation

Indexed keywords

ACETYLCHOLINESTERASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ADRENAL GLAND; ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHOLINERGIC SYSTEM; CHRONIC STRESS; CONTROLLED STUDY; ENZYME ACTIVITY; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMUNE SYSTEM; INFLAMMATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; RAT;

ACETYLCHOLINESTERASE; ADRENAL GLANDS; ANIMALS; BODY WEIGHT; CHEMOKINE CCL2; CYTOKINES; HIPPOCAMPUS; INFLAMMATION; MALE; ORGAN SIZE; RATS; RATS, WISTAR; STRESS, PSYCHOLOGICAL;

RATTUS; RATTUS NORVEGICUS;

EID: 79954420691     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-010-0367-0     Document Type: Article

References (70)

1. Skilbeck KJ, Johnston GA, Hinton T (2010) Stress and GABA receptors. J Neurochem 112(5):1115-1130.
2. Licinio J, Wong M (2005) Biology of depression, 1st edn. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
3. Chrousos GP (1995) The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med 332:1351-1362.
4. Munhoz CD, García-Bueno B, Madrigal JLM et al (2008) Stressinduced neuroinflammation: mechanisms and new pharmacological targets. Braz J Med Biol Res 41:1037-1046.
5. Sorrels SF, Sapolski RM (2008) An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 21(3): 259-272.
6. Alesci S, Martinez PE, Kelkar S et al (2005) Major depression is associated with significant diurnal elevations in plasma interleukin- 6 levels, a shift of its circadian rhythm, and loss of physiological complexity in its secretion: clinical implications. J Clin Endocrinol Metab 90:2522-2530. (Pubitemid 40686286)
7. Schlatter J, Ortuño F, Cervera-Enguix S (2004) Monocytic parameters in patients with dysthymia versus major depression. J Affect Disord 78:243-247. (Pubitemid 38167743)
8. Tiemeier H, Hofman A, van Tuijl HR et al (2003) Inflammatory proteins and depression in the elderly. Epidemiology 14:103-107. (Pubitemid 40416821)
9. Danner M, Kasl SV, Abramson JL et al (2003) Association between depression and elevated C-reactive protein. Psychosom Med 65:347-356. (Pubitemid 36628886)
10. Steptoe A, Kunz-Ebrecht SR, Owen N (2003) Lack of association between depressive symptoms and markers of immune and vascular inflammation in middle-aged men and women. Psychol Med 33:667-674. (Pubitemid 36626048)
11. Haack M, Hinze-Selch D, Fenzel T et al (1999) Plasma levels of cytokines and soluble cytokine receptors in psychiatric patients upon hospital admission: effects of confounding factors and diagnosis. J Psychiatr Res 33:407-418. (Pubitemid 29392689)
12. Owen BM, Eccleston D, Ferrier IN et al (2001) Raised levels of plasma interleukin-1beta in major and postviral depression. Acta Psychiatr Scand 103:226-228. (Pubitemid 32154355)
13. Darvesh S, Hopkins DA, Geula C (2003) Neurobiology of butyrylcholinesterase. Nat Rev Neurosci 17:131-138. (Pubitemid 37271383)
14. Nomenclature Committee of the International Union of Biochemistry and Molecular Biology (NC-IUBMB) (1992) Enzyme nomenclature. Academic Press, San Diego.
15. Borovikova LV, Ivanova S, Zhang M et al (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405:458-462. (Pubitemid 30367422)
16. Srikumar BN, Raju TR, Shankaranarayana Rao BS (2006) The involvement of cholinergic and noradrenergic systems in behavioral recovery following oxotremorine treatment to chronically stressed rats. Neuroscience 143:679-688. (Pubitemid 44781287)
17. Mizoguchi K, Yuzurihara M, Ishige A et al (2001) Effect of chronic stress on cholinergic transmission in rat hippocampus. Brain Res 915:108-111. (Pubitemid 32907499)
18. Sunanda GV, Shankaranarayana Rao BS, Raju TR (2000) Restraint stress-induced alterations in the levels of biogenic amines, amino acids, and AChE activity in the hippocampus. Neurochem Res 25:1547-1552. (Pubitemid 32052015)
19. Lorenzetti V, Allen NB, Fornito A et al (2009) Structural brain abnormalities in major depressive disorder: a selective review of recent MRI studies. J Affect Disord 117(1-2):1-17.
20. Wayne C, Drevets JL, Price M (2008) Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 213: 93-118.
21. Gamaro GD, Manoli LP, Torres ILS et al (2003) Effects of chronic variate stress on feeding behavior and on monoamine levels in different rat brain structures. Neurochem Int 42:107-114. (Pubitemid 35284779)
22. Marin MT, Cruz FC, Planeta CS (2007) Chronic restraint or variable stresses differently affect the behavior, corticosterone secretion and body weight in rats. Physiol Behav 90(1):29-35. (Pubitemid 44918003)
23. Porsolt RD, Bertin A, Jalfre M (1997) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229:327-336.
24. Harro J, Tõnissaar M, Eller M et al (2001) Chronic variable stress and partial 5-HT denervation by parachloroamphetamine treatment in the rat: effects on behavior and monoamine neurochemistry. Brain Res 899(1-2):227-239. (Pubitemid 32324164)
25. Konarska M, Stewart RE, McCarty R (1990) Predictability of chronic intermittent stress: effects on sympathetic-adrenal medullary responses of laboratory rats. Behav Neural Biol 53:231-243. (Pubitemid 20249737)
26. Froger N, Palazzo E, Boni C (2004) Neurochemical and behavioral alterations in glucocorticoid receptor-impaired transgenic mice after chronic mild stress. J Neurosci 24(11):2787-2796. (Pubitemid 38380956)
27. Ellman GL, Courtney KD, Andres V Jr (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88-95.
28. Bradford MM (1976) A rapid and sensitive method for the quantification of micrograms quantities of protein utilizing the principle of protein-diebinding. Anal Biochem 72:248-254.
29. Lowry OH, Rosebrough NJ, Farr AL et al (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-267.
30. Kessler RC, McGonagle KA, Zhao S et al (1994) Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch Gen Psychiatry 51:8-19. (Pubitemid 24028993)
31. Willner P (2005) Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52:90-110. (Pubitemid 41160326)
32. Elizalde N, Pastor PM, Garcia-García AL et al (2010) Regulation of markers of synaptic function in mouse models of depression: chronic mild stress and decreased expression of VGLUT1. J Neurochem 114(5):1302-1314.
33. Mao QQ, Xian YF, Xian YF, Ip SP et al (2010) Long-term treatment with peony glycosides reverses chronic unpredictable mild stress-induced depressive-like behavior via increasing expression of neurotrophins in rat brain. Behav Brain Res 210(2):171-177.
34. Rezin GT, Gonçalves C, Daufenbach JF et al (2009) Acute administration of ketamine reverses the inhibition of mitochondrial respiratory chain induced by chronic mild stress. Brain Res Bull 79:418-421.
35. Willner P (1997) The chronic mild stress model of depression: valid, reasonably reliable, and useful. Psychopharmacology 134: 371-377.
36. Grippo AJ, Sullivan NR, Damjanoska KJ et al (2005) Chronic mild stress induces behavioural and physiological changes, and may alter serotonin 1A receptor function in male and cycling female rats. Psychopharmacology 179:769-780. (Pubitemid 40774824)
37. Benelli A, Filaferro M, Bertonili A et al (1999) Influence of S-adenosyl-L-carnitine on chronic mild stress-induced anhedonia in castrated rats. Braz J Pharmacol 127:645-654. (Pubitemid 29276649)
38. Nielsen CK, Arnt J, Sanchez C (2000) Intracranial self-stimulation and sucrose intake differ as hedonic measures following chronic mild stress: interstrain and inter-individual differences. Behav Brain Res 107:21-33.
39. Moreau JL, Scherschlict R, Jenck F et al (1995) Chronic mild stress-induced anhedonia model of depression: sleep abnormalities and curative effects of electroshock treatment. Behav Pharmacol 6:682-687.
40. Gronli J, Murison R, Fiske E et al (2003) Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol Behav 84:571-577. (Pubitemid 40487476)
41. Brotto LA, Gorzalka BB, LaMarre AK (2001) Melatonin protects against the effects of chronic stress on sexual behaviour in male rats. Neuroreport 12:3465-3469. (Pubitemid 33065479)
42. Tagliari B, dos Santos TM, Cunha AA et al (2010) Chronic variable stress induces oxidative stress and decrease butyrylcholineterase activity in blood of rats. Neural Transm 117(9):1067-1076.
43. Bielajew C, Konkle AT, Mentne AC et al (2003) Strain and gender specific effects in the forced swim tests: effects of previous stress exposure. Stress 6:269-280. (Pubitemid 38101486)
44. Fujisaki C, Utsuyama M, Kuroda Y (2002) An immunosuppressive drug, cyclosporine-A acts like anti-depressant for rats under unpredictable chronic stress. J Med Dent Sci 50:93-100. (Pubitemid 41124461)
45. Cheeta S, Ruigt G, van Proosdij J et al (1997) Changes in sleep architecture following chronic mild stress. Biol Psychiatry 41: 419-427. (Pubitemid 27087325)
46. O'Connor KA, Johnson JD, Hansen MK et al (2003) Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res 991(1-2):123-132. (Pubitemid 37297941)
47. Mormède C, Castanon N, Médina C et al (2003) Chronic mild stress in mice decreases peripheral cytokine and increases central cytokine expression independently of IL-10 regulation of the cytokine network. Neuroimmunomodulation 10(6):359-366. (Pubitemid 36980746)
48. Nguyen KT, Deak T, Owens SM et al (1998) Exposure to acute stress induces brain interleukin-1b protein in the rat. J Neurosci 19:2799-2805.
49. Hanisch UK (2002) Microglia as a source and target of cytokines. Glia 40:140-155.
50. Breder CA, Tsujimoto M, Terano Y et al (1993) Distribution and characterization of tumor necrosis factor-alpha-like immunoreactivity in the murine and central nervous system. J Comp Neurol 337:543-567. (Pubitemid 23323643)
51. Miyahara S, Komori T, Fujiwara R et al (2000) Effects of repeated stress on expression of interleukin-6 (IL-6) and IL-6 receptor mRNAs in rat hypothalamus and midbrain. Life Sci 66:PL93- PL98.
52. Lee M, Cho T, Jantaratnotai N, Wang YT et al (2010) Depletion of GSH in glial cells induces neurotoxicity: relevance to aging and degenerative neurological diseases. FASEB J 24(7):2533-2545.
53. Innamorato NG, Lastres-Becker I, Cuadrado A (2009) Role of microglial redox balance in modulation of neuroinflammation. Curr Opin Neurol 22(3):308-314.
54. Hensley K, Mhatre M, Mou S et al (2006) On the relation of oxidative stress to neuroinflammation: lessons learned from the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. Antioxid Redox Signal 8(11-12):2075-2087. (Pubitemid 46489632)
55. De A, Krueger JM, Simasko SM (2005) Glutamate induces the expression and release of tumor necrosis factor-alpha in cultured hypothalamic cells. Brain Res 1053(1-2):54-61. (Pubitemid 41116790)
56. Rogove AD, Tsirka SE (1998) Neurotoxic responses by microglia elicited by excitotoxic injury in the mouse hippocampus. Curr Biol 8(1):19-25. (Pubitemid 28056250)
57. Nair A, Bonneau RH (2006) Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol 171:72-85. (Pubitemid 41832279)
58. Frank MG, Baratta MV, Sprunger DB et al (2006) Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 21:47-59. (Pubitemid 44854445)
59. Lucca G, Comim CM, Valvassori SS et al (2009) Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int 54:358-362.
60. Vasconcellos APS, Nieto FB, Crema LM et al (2006) Chronic lithium treatment has antioxidant properties but does not prevent oxidative damage induced by chronic variate stress. Neurochem Res 31:1141-1151. (Pubitemid 44379675)
61. Madrigal JL, Garcia-Bueno B, Hinojosa AE et al (2010) Regulation of MCP-1 production in brain by stress and noradrenalinemodulating drugs. J Neurochem 113:543-551.
62. McEwen BS (2001) Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 933:265-277. (Pubitemid 32390122)
63. Sapolsky RM (2000) The possibility of neurotoxicity in the hippocampus in major depression: a primer on neuron death. Biol Psychiatry 48:755-765.
64. Moghaddam B (1993) Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 60: 1650-1657. (Pubitemid 23127567)
65. Luo L, Tan RX (2001) Fluoxetine inhibits dendrite atrophy of hippocampal neurons by decreasing nitric oxide synthase expression in rat depression model. Acta Pharmacol Sin 22:865-870. (Pubitemid 32928974)
66. Madrigal JLM, Olivenza R, Moro MA et al (2001) Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology 24(4):420-429. (Pubitemid 32157558)
67. Little AR, Sriram K, O'Callaghan JP (2006) Corticosterone regulates expression of CCL2 in the intact and chemically injured hippocampus. Neurosci Lett 399:162-166.
68. Rada P, Colasante C, Skirzewski M et al (2006) Behavioral depression in the swim test causes a biphasic, long-lasting change in accumbens acetylcholine release, with partial compensation by acetylcholinesterase and muscarinic-1 receptors. Neuroscience 141:67-76.
69. Müller TC, Rocha JBC, Morsch VM et al (2002) Antidepressants inhibit human acetylcholinesterase and butyrylcholinesterase activity. Biochim Biophys Acta 1587:92-98. (Pubitemid 34493839)
70. Barcellos CK, Schetinger MRC, Dias RD et al (1998) In vitro effect of central nervous system active drugs on the ATPase- ADPase activity and acetylcholinesterase activity from cerebral cortex of adult rats. Gen Pharmacol 31:563-567. (Pubitemid 28458924)