Abstract
The present study examined, in mice, whether regional patterns of brain monoamines concentrations (DA, 5-HT and their metabolites) and expression of c-Fos protein, that may represent a prolonged functional change in neurons, could be changed after a combined exposure to stress and the peripheral cholinesterase reversible inhibitor pyridostigmine (PYR). Animals were subjected every day to a random combination of mild unescapable electric footshocks and immobilization over a 12-day period, resulting in a significant increase of glucocorticoids levels and an activation of c-fos in hippocampus, thalamus and piriform cortex. This stress protocol induced a significant increase of 5-HT levels in striatum, hippocampus and ponto mesencephalic area (PMA) but failed to induce any DA activation. When PYR (0.2 mg/kg s.c. inducing 19–35% inhibition of the plasmatic ChE activity) was administered twice a day during the last 5 days of the stress session, 5-HIAA levels and expression of c-fos oncogene were significantly increased in the most of the brain areas studied. DA levels were also enhanced in striatum/hippocampus as a result of a possible activation of mesolimbic and nigrostriatal dopamine systems. Taken together, these results suggest that a combined exposure to certain stress conditions and PYR leads, in mice, to functional changes in neurons and may affect centrally controlled functions. The mechanisms underlying these modifications and their behavioral implications remain to be further investigated.
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References
A. Friedman D. Kaufer J. Shemer I. Hendler H. Soreq I. Tur-Kaspa (1996) ArticleTitlePyridostigmine brain penetration under stress enhances neuronal excitability and induces early immediate transcriptional response Nat. Med. 2 382–1385
A. Abdel-Rahman A.K. Shetty M.B. Abou-Donia (2002) ArticleTitleDisruption of the blood-brain barrier and the neuronal cell death in cingulate cortex, dentate gyrus, thalamus and hypothalamus in a rat model of Gul War Syndrome Neurobiol. Dis. 10 306–326 Occurrence Handle1:CAS:528:DC%2BD38XmvFaisLs%3D Occurrence Handle12270692
M.B. Abou Donia K.F. Jensen F.W. Oehme T.L. Kurt K.R. Wilmarth (1996) ArticleTitleNeurotoxicity resulting from coexposure to pyridostigmine bromide, DEET, and permethrin: implications of Gulf War chemical exposures J. Toxicol. Environ. Health 48 35–56 Occurrence Handle1:CAS:528:DyaK28XjtFajt78%3D Occurrence Handle8637057
G.J. Kant R.A. Bauman S.R. Feaster S.M. Anderson G.A. Saviolakis G.E. Garcia (2001) ArticleTitleThe combined effects of pyridostigmine and chronic stress on brain cortical and blood acetylcholinesterase, corticosterone, prolactin and alteration performance in rats Pharmacol. Biochem. Behav. 70 209–218 Occurrence Handle1:CAS:528:DC%2BD3MXotFWjtLw%3D Occurrence Handle11701190
B.A. Morrow W.A. Clark R.H. Roth (1993) ArticleTitleStress activation of mesocorticolimbic clop neurons effects of a glycine/NMDA receptor antagonist Eur. J. Pharmacol. 238 255–262 Occurrence Handle1:CAS:528:DyaK3sXlslClsb8%3D Occurrence Handle8405096
J.J. Kim K.S. Yoon (1998) ArticleTitleStress: metaplasic effects in the hippocampus TINS 21 505–509 Occurrence Handle1:CAS:528:DyaK1cXotVWquro%3D Occurrence Handle9881846
T. Inoue K. Tsuchiya T. Koyama (1994) ArticleTitleRegional changes in dopamine and serotonin activation with various intensity of physical and psychological stress in the rat brain Pharmacol. Biochem. Behav. 49 911–920 Occurrence Handle7886107
G. Lallement A. Foquin D. Baubichon M-F. Burckart P. Carpentier F. Canini (1998) ArticleTitleHeat stress, even stress, does not induce penetration of pyridostigmine into the brain of guinea pigs Neurotoxicology 19 759–766 Occurrence Handle9863765
E. Grauer D. Alkalai J. Kapon G. Cohen L. Raveh (2000) ArticleTitleStress does not enable pyridostigmine to inhibit brain cholinesterase after parental administration Toxicol. Appl. Pharmacol. 164 301. Occurrence Handle10799340
H. Shimizu S. Take T. Hori Y. Oomura (1992) ArticleTitleIn vivo measurement of hypothalamic serotonin release by intracerebral microdialysis: significant enhancement by immobilization stress Brain Res. Bull. 28 727–734 Occurrence Handle1:CAS:528:DyaK38XkvVemtrY%3D Occurrence Handle1377587
J.F. Reinhard M.J. Bannon R.H. Roth (1982) ArticleTitleAcceleration by stress of dopamine synthetis and metabolism in prefrontal cortex: antagonism by diazepam Naunyn-Schmiedeberg’s Arch. Pharmacol. 318 374–377 Occurrence Handle1:CAS:528:DyaL38XitFSrtLs%3D
S.P. Hunt A. Pini G. Evan (1987) ArticleTitleInduction of c-fos-like protein in spinal cord neurons following sensory stimulation Nature 328 632–634 Occurrence Handle10.1038/328632a0 Occurrence Handle1:CAS:528:DyaL2sXlsFWqtrY%3D Occurrence Handle3112583
D. Menetrey A. Gannon J.D. Levine A.I. Basbaum (1989) ArticleTitleExpression of c-fos protein in interneurons and projection neurons of the rat spinal cord in response to noxious somatic articular and visceral stimulation J. Comp. Neurol. 285 177–195 Occurrence Handle1:STN:280:BiaA2c7gtVM%3D Occurrence Handle2503547
E. Bullitt (1990) ArticleTitleExpression of c-fos like protein as a marker for neuronal activity following noxious stimulation in the rat J. Comp. Neurol. 196 517–530
M. Fitzgerald (1990) ArticleTitleC-fos and the changing face pain Trends Neurosci. 13 439–440 Occurrence Handle1:STN:280:By6D2srlsVY%3D Occurrence Handle1701574
G.L. Ellman K.D. Courney V. Andres R.H. Feathertone (1961) ArticleTitleA next and rapid colorimetric determination of acetylcholinesterase activities Biochem. Pharmacol. 7 88–95 Occurrence Handle1:CAS:528:DyaF3MXht1Gns7o%3D Occurrence Handle13726518
M. Bielavska J. Kassa (2000) ArticleTitleSimultaneous determination of dopamine, serotonin and their metabolites in the rat brain by HPLC method with colourometric detection Collect. Czech. Chem. Commun. 65 1677–1682 Occurrence Handle1:CAS:528:DC%2BD3cXosl2jtrs%3D
A.J. Dunn (1988) ArticleTitleStress-related activation of cerebral dopaminergic systems Ann NY. Acad. Sci. 537 188–205 Occurrence Handle1:CAS:528:DyaL1MXovFWktg%3D%3D Occurrence Handle3202543
H. Kawahara M. Yoshida H. Yokoo M. Nishi M. Tanaka (1993) ArticleTitlePsychological stress increases serotonin release in the rat amygdala and prefrontal cortex assessed by in vivo microdialysis Neurosci. Lett. 162 81–84 Occurrence Handle1:CAS:528:DyaK2cXmvF2rsw%3D%3D Occurrence Handle8121642
H. Miura M. Naoi D. Nakamura T. Ohta T. Nagatsu (1993) ArticleTitleChanges in monoamines levels in mouse brain elicited by forced swimming stress and the protective effect of a new monoamine oxidase inhibitor J. Neural. Trans. 94 175–189 Occurrence Handle1:CAS:528:DyaK2cXjtFGlsL4%3D
A. Adell R. Trullas E. Gelpi (1988) ArticleTitleTime course in serotonin and noradrenaline in rat brain after predictable or unpredictable shock Brain Res. 459 54–59 Occurrence Handle1:CAS:528:DyaL1cXlsVeis70%3D Occurrence Handle2458804
J.S. Soblosky J.B. Thurmond (1986) ArticleTitleBiochemical and behavioral correlates of chronic stress: effects of tricyclic antidepressants Pharmac. Biochem. Behav. 24 1361–1368 Occurrence Handle1:CAS:528:DyaL28XktlGms7Y%3D
A.Y. Deutch R.H. Roth (1991) ArticleTitleThe determinants of stress-induced activation of the prefrontal cortical dopamine system Prog. Brain Res. 85 367–385
M. Denoyer G. Lallement A. Collet I. Pernot-Marino D. Séréno G. Blanchet (1992) ArticleTitleInfluence of medial septal cholinoceptive cells on c-Fos-like proteins induced by soman Brain Res. 592 157–162 Occurrence Handle1:CAS:528:DyaK38Xmt1yjtrw%3D Occurrence Handle1450906
S.M. Sagar F.R. Sharp (1990) ArticleTitleLight induces a Fos-like nuclear antigen in retinal neurons Ml Brain. Res. 7 17–21 25 Occurrence Handle1:CAS:528:DyaK3cXps1Wqtg%3D%3D
J.I. Morgan D.R. Cohen J.L. Hempstead T. Curran (1987) ArticleTitleMapping patterns of c-fos expression in the central nervous system after seizure Science 237 192–197 Occurrence Handle1:CAS:528:DyaL2sXkslajs7k%3D Occurrence Handle3037702
A. D’Costa R.B. Breese L.B. Rhonda M.B. Rosemarie E. Sonnatg (1991) ArticleTitleAttenuation of Fos-like immunoreactivity induced by a single retroconvulsive shock in brains of aging mice Brain Res. 567 204 Occurrence Handle1:STN:280:By2B1cfnt1Q%3D Occurrence Handle1687805
F.R. Sharp S.H. Sagar K. Hicks D. Lowenstein F. Hisanaga (1991) ArticleTitlec.fos mRNA, Fos and Fos related antigen induction by hypertonic saline and stress J. Neurosci. 11 2321–2331 Occurrence Handle1:CAS:528:DyaK3MXmslKlurk%3D Occurrence Handle1908006
S. Ceccatelli M.J. Villar M. Goldstein T. Hokfelt (1989) ArticleTitleExpression of c-Fos immunoreactivity in transmitter-characterized neurons after stress Proc. Natl. Acad. Sci. 86 9569–9573 Occurrence Handle1:CAS:528:DyaK3cXlt12ktA%3D%3D Occurrence Handle2512584
A. Adell J.M. Casanovas F. Artigas (1997) ArticleTitleComparative study in the rat of the activiy of different types of stress on the release of 5-HT in the raphe nuclei and forebrain areas Neuropharmacology 36 735–741 Occurrence Handle1:CAS:528:DyaK2sXktlajsLc%3D Occurrence Handle9225300
B.L. Jacobs C.A. Fornal (1991) ArticleTitleActivity of brain serotoninergic neurons in the behaving animals Pharmacol. Rev. 43 563–578 Occurrence Handle1:CAS:528:DyaK38XhsVeqtbc%3D Occurrence Handle1775508
T.J. Sajdy J.S. Katner A. Shekhar (1997) ArticleTitleMonoamines in the dorsomedial hypothalamus of rats following exposure to different tests of anxiety Prog. Neuro. Psychopharm. Biol. Psychiatr. 21 193–209
X. Song H. Tian J. Bressler S. Pruett C. Pope (2002) ArticleTitleAcute and repeated restraint stress have little effect on pyridostigmine toxicity or brain regional cholinesterase inhibition in rats Toxicol. Sci. 69 157–164 Occurrence Handle1:CAS:528:DC%2BD38XmvVGjsrg%3D Occurrence Handle12215670
K.D. Beck F.X. Brennan R.L. Moldow J.E. Ottenweller G. Zhu R.J. Servatius (2003) ArticleTitleStress interacts with peripheral cholinesterase inhibitors to cause central nervous system effects Life Sci. 73 41–51 Occurrence Handle1:CAS:528:DC%2BD3sXjt1KgsbY%3D Occurrence Handle12726885
G.J. Kant R.A. Bauman S.R. Feaster S.M. Anderson G.A. Garcia Saviolakis G.E. (2001) ArticleTitleThe combined effects of pyridostigmine and chronic stress on brain cortical and blood acetylcholinesterase, corticosterone, prolactin and alteration performance in rats Pharmacol. Biochem. Behav. 70 209–218 Occurrence Handle1:CAS:528:DC%2BD3MXotFWjtLw%3D Occurrence Handle11701190
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Taysse, L., Christin, D., Delamanche, S. et al. Peripheral ChE Inhibition Modulates Brain Monoamines Levels and c-fos Oncogene in Mice Subjected to a Stress Situation. Neurochem Res 30, 391–402 (2005). https://doi.org/10.1007/s11064-005-2614-3
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DOI: https://doi.org/10.1007/s11064-005-2614-3