Brief maternal separation affects brain α1-adrenoceptors and apoptotic signaling in adult mice

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 48, Issue , 2014, Pages 161-169

  Coccurello, Roberto ^a   Bielawski, Adam ^b   Zelek Molik, Agnieszka ^b   Vetulani, Jerzy ^b   Kowalska, Marta ^b   D'Amato, Francesca R ^a   Nalepa, Irena ^b  

^a CNR   (Italy)

^b POLISH ACADEMY OF SCIENCES   (Poland)

Author keywords

Anhedonia; Bcl 2 proteins; Early life adversity; Heat shock proteins; Olfactory learning

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; ALPHA 1A ADRENERGIC RECEPTOR; ALPHA 1B ADRENERGIC RECEPTOR; ALPHA 1D ADRENERGIC RECEPTOR; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL;

AMYGDALOID NUCLEUS; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING SITE; BRAIN REGION; CINGULATE GYRUS; CONTROLLED STUDY; DEPRESSION; EARLY LIFE STRESS; FEMALE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LIMBIC CORTEX; LONG TERM EXPOSURE; MATERNAL DEPRIVATION; MESENCEPHALON; MOUSE; NEWBORN; NONHUMAN; OLFACTORY DISCRIMINATION; PROTEIN EXPRESSION; REWARD; SIGNAL TRANSDUCTION; THALAMUS;

AMY; AMYGDALOID NUCLEUS; ANHEDONIA; BCL-2 PROTEINS; CB; CEL; CEM; CENTRAL LATERAL; CENTRAL MEDIAL; CINGULATE CORTEX; CL; CLEAN BEDDING; CM; CTXCG; CTXM1 AND CTXM2; CTXPIR; CTXS2; EARLY LIFE ADVERSITY; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEINS; HSP; IMD; INTERMEDIODORSAL; LC; LOCUS COERULEUS; MDC; MDL; MDM; MEDIAL CENTRAL; MEDIAL LATERAL; MEDIODORSAL; NA; NAERGIC; NORADRENALINE; NORADRENERGIC; NUCLEUS ACB; NUCLEUS ACCUMBENS; OLFACTORY LEARNING; PARACENTRAL; PC; PIRIFORM CORTEX; PRIMARY AND SECONDARY MOTOR CORTICES; SACCHARINE PREFERENCE TEST; SECONDARY SOMATOSENSORY CORTEX; SPT; THAL; THALAMIC NUCLEUS; Α(1)-ADRENOCEPTORS;

ADRENERGIC ALPHA-1 RECEPTOR ANTAGONISTS; AGING; ANIMALS; APOPTOSIS; BRAIN; CYCLIN D1; DIOXANES; FEMALE; FOOD PREFERENCES; HEAT-SHOCK PROTEINS; HIPPOCAMPUS; MALE; MATERNAL DEPRIVATION; MICE; PRAZOSIN; RECEPTORS, ADRENERGIC, ALPHA-1; SACCHARIN; SIGNAL TRANSDUCTION; SWEETENING AGENTS; TIME FACTORS;

EID: 84886674068     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2013.10.004     Document Type: Article

References (80)

1. Arborelius L., Eklund M.B. Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience 2007, 145:738-750.
2. Asea A., Kraeft S.K., Kurt-Jones E.A., Stevenson M.A., Chen L.B., Finberg R.W., et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 2000, 6:435-442.
3. Bennett M.R. The prefrontal-limbic network in depression: a core pathology of synaptic regression. Prog Neurobiol 2011, 93:457-467.
4. Bock J., Gruss M., Becker S., Braun K. Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb Cortex 2005, 15:802-808.
5. Brown I.R. Heat shock proteins and protection of the nervous system. Ann N Y Acad Sci 2007, 1113:147-158.
6. Cabib S., Puglisi-Allegra S., D'Amato F.R. Effects of postnatal stress on dopamine mesolimbic system responses to aversive experiences in adult life. Brain Res 1993, 604:232-239.
7. Campisi J., Fleshner M. Role of extracellular HSP72 in acute stress-induced potentiation of innate immunity in active rats. J Appl Physiol 2003, 94:43-52.
8. Cheslock S.J., Varlinskaya E.I., Petrov E.S., Spear N.E. Rapid and robust olfactory conditioning with milk before suckling experience: promotion of nipple attachment in the newborn rat. Behav Neurosci 2000, 114:484-495.
9. Coccurello R., D'Amato F.R., Moles A. Chronic social stress, hedonism and vulnerability to obesity: lessons from rodents. Neurosci Biobehav Rev 2009, 33:537-550.
10. Colman I., Ataullahjan A. Life course perspectives on the epidemiology of depression. Can J Psychiatry 2010, 55:622-632.
11. D'Amato F.R., Cabib S. Chronic exposure to a novel odor increases pups' vocalizations, maternal care, and alters dopaminergic functioning in developing mice. Behav Neural Biol 1987, 48:197-205.
12. D'Amato F.R., Mazzacane E., Capone F., Pavone F. Effects of postnatal manipulation on nociception and morphine sensitivity in adult mice. Brain Res Dev Brain Res 1999, 117:15-20.
13. 1D adrenergic receptor mRNA by corticosterone in adrenalectomized rats. Brain Res 2008, 1218:132-140.
14. 1-adrenoceptor. Cell Mol Life Sci 2010, 67:405-417.
15. Fleshner M., Campisi J., Amiri L., Diamond D.M. Cat exposure induces both intra- and extracellular Hsp72: the role of adrenal hormones. Psychoneuroendocrinology 2004, 29:1142-1152.
16. 1 adrenergic receptor antagonist prazosin reduces heroin self-administration in rats with extended access to heroin administration. Pharmacol Biochem Behav 2009, 91:295-302.
17. 1-noradrenergic receptors in the human brain postmortem. Arch Gen Psychiatry 1990, 47:1049-1053.
18. Haenisch B., Bönisch H. Depression and antidepressants: insights from knockout of dopamine, serotonin or noradrenaline re-uptake transporters. Pharmacol Ther 2011, 129:352-368.
19. 1-adrenoceptor activation initiates early odor preference learning in rat pups: support for the mitral cell/cAMP model of odor preference learning. Learn Mem 2006, 13:8-13.
20. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 2001, 49:1023-1039.
21. Hunsberger J.G., Machado-Vieira R., Austin D.R., Zarate C., Chuang D.M., Chen G., et al. Bax inhibitor 1, a modulator of calcium homeostasis, confers affective resilience. Brain Res 2011, 1403:19-27.
22. Jasmin L., Narasaiah M., Tien D. Noradrenaline is necessary for the hedonic properties of addictive drugs. Vascul Pharmacol 2006, 45:243-250.
23. Johnson J.D., Campisi J., Sharkey C.M., Kennedy S.L., Nickerson M., Fleshner M. Adrenergic receptors mediate stress-induced elevations in extracellular Hsp72. J Appl Physiol 2005, 99:1789-1795.
24. Kiang J.G., Tsokos G.C. Heat shock protein 70kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 1998, 80:183-201.
25. Kim H.P., Morse D., Choi A.M. Heat-shock proteins: new keys to the development of cytoprotective therapies. Expert Opin Ther Targets 2006, 10:759-769.
26. Kosten T.A., Galloway M.P., Duman R.S., Russell D.S., D'Sa C. Repeated unpredictable stress and antidepressants differentially regulate expression of the Bcl-2 family of apoptotic genes in rat cortical, hippocampal, and limbic brain structures. Neuropsychopharmacology 2008, 33:1545-1558.
27. Kovacs J.J., Murphy P.J., Gaillard S., Zhao X., Wu J.T., Nicchitta C.V., et al. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 2005, 18:601-607.
28. 1-adrenoceptor subtypes after antidepressant treatment. Pharmacol Rep 2011, 63:1349-1358.
29. Kubera M., Obuchowicz E., Goehler L., Brzeszcz J., Maes M. In animal models, psychosocial stress-induced (neuro)inflammation, apoptosis and reduced neurogenesis are associated to the onset of depression. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:744-759.
30. Lee H.J., Kim J.W., Yim S.V., Kim M.J., Kim S.A., Kim Y.J., et al. Fluoxetine enhances cell proliferation and prevents apoptosis in dentate gyrus of maternally separated rats. Mol Psychiatry 2001, 6:725-728.
31. Li Z., Jo J., Jia J.M., Lo S.C., Whitcomb D.J., Jiao S., et al. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 2010, 141:859-871.
32. Maes M., Yirmyia R., Noraberg J., Brene S., Hibbeln J., Perini G., et al. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab Brain Dis 2009, 24:27-53.
33. Maes M., Kubera M., Obuchowiczwa E., Goehler L., Brzeszcz J. Depression's multiple comorbidities explained by (neuro)inflammatory and oxidative & nitrosative stress pathways. Neuro Endocrinol Lett 2011, 32:7-24.
34. Martínez-Téllez R.I., Hernández-Torres E., Gamboa C., Flores G. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse 2009, 63:794-804.
35. McDonald A.J. Cortical pathways to the mammalian amygdala. Prog Neurobiol 1998, 55:257-332.
36. McEwen B.S. Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev 2003, 9:149-154.
37. McEwen B.S. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 2005, 54:20-33.
38. McLaughlin B. The kinder side of killer proteases: caspase activation contributes to neuroprotection and CNS remodeling. Apoptosis 2004, 9:111-121.
39. Miyamichi K., Amat F., Moussavi F., Wang C., Wickersham I., Wall N.R., et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 2011, 472:191-196.
40. Monroy E., Hernández-Torres E., Flores G. Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. J Chem Neuroanat 2010, 40:93-101.
41. Moretti M., Budni J., Dos Santos D.B., Antunes A., Daufenbach J.F., Manosso L.M., et al. Protective effects of ascorbic acid on behavior and oxidative status of restraint-stressed mice. J Mol Neurosci 2013, 49:68-69.
42. Morgane P.J., Galler J.R., Mokler D.J. A review of systems and networks of the limbic forebrain/limbic midbrain. Prog Neurobiol 2005, 75:143-160.
43. Morilak D.A., Barrera G., Echevarria D.J., Garcia A.S., Hernandez A., Ma S., et al. Role of brain norepinephrine in the behavioral response to stress. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:1214-1224.
44. Murmu M., Salomon S., Biala Y., Weinstock M., Braun K., Bock J. Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 2006, 24:1477-1487.
45. Murphy P.J., Morishima Y., Kovacs J.J., Yao T.P., Pratt W.B. Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/deacetylation of the chaperone. J Biol Chem 2005, 280:33792-33799.
46. Nakamura S., Sakaguchi T. Development and plasticity of the locus coeruleus: a review of recent physiological and pharmacological experimentation. Prog Neurobiol 1990, 34:505-526.
47. Nakamura S., Kimura F., Sakaguchi T. Postnatal development of electrical activity in the locus coeruleus. J Neurophysiol 1987, 58:510-524.
48. Nalepa I., Sulser F. New hypotheses to guide future antidepressant drug development. Handbook of Experimental Pharmacology 2004, vol. 157:519-563. Springer-Verlag, London. S.H. Preskorn, C. Stanga, J.P. Feighner, R. Ross (Eds.).
49. 1A-adrenoceptor mRNA level in rat prefrontal cortex. Eur J Pharmacol 2002, 444:151-159.
50. 1-adrenoceptors in specific regions of the mouse brain and spinal cord. J Neural Transm 2005, 112:1309-1319.
51. 1-adrenoceptors in brain regions of the rat: an autoradiographic study. Pharmacol Rep 2006, 58:827-835.
52. O'Sullivan J.B., Ryan K.M., Curtin N.M., Harkin A., Connor T.J. Noradrenaline reuptake inhibitors limit neuroinflammation in rat cortex following a systemic inflammatory challenge: implications for depression and neurodegeneration. Int J Neuropsychopharmacol 2009, 12:687-699.
53. Pae C.U., Mandelli L., Serretti A., Patkar A.A., Kim J.J., Lee C.U., et al. Heat-shock protein-70 genes and response to antidepressants in major depression. Prog Neuropsychopharmacol Biol Psychiatry 2007, 31:1006-1011.
54. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2001, Academic Press, San Diego. 2nd ed.
55. Piazza P.V., Rouge-Pont F., Deroche V., Maccari S., Simon H., Le Moal M. Glucocorticoids have state-dependent stimulant effects on the mesencephalic dopaminergic transmission. Proc Natl Acad Sci U S A 1996, 93:8716-8720.
56. Poeggel G., Helmeke C., Abraham A., Schwabe T., Friedrich P., Braun K. Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc Natl Acad Sci U S A 2003, 100:16137-16142.
57. Roth T.L., Sullivan R.M. Memory of early maltreatment: neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biol Psychiatry 2005, 57:823-831.
58. Rothman R.B., Baumann M.H., Dersch C.M., Romero D.V., Rice K.C., Carroll F.I., et al. Amphetamine-type central nervous system stimulants release norepinephrine more potently than they release dopamine and serotonin. Synapse 2001, 39:32-41.
59. Samali A., Orrenius S. Heat shock proteins: regulators of stress response and apoptosis. Cell Stress Chaperones 1998, 3:228-236.
60. Sapolsky R.M. Is impaired neurogenesis relevant to the affective symptoms of depression?. Biol Psychiatry 2004, 56:137-139.
61. Schmidt M.V., Wang X.D., Meijer O.C. Early life stress paradigms in rodents: potential animal models of depression?. Psychopharmacology (Berl) 2011, 214:131-140.
62. Shipley M.T., Ennis M. Functional organization of olfactory system. J Neurobiol 1996, 30:123-176.
63. Shishkina G.T., Kalinina T.S., Berezova I.V., Bulygina V.V., Dygalo N.N. Resistance to the development of stress-induced behavioral despair in the forced swim test associated with elevated hippocampal Bcl-xL expression. Behav Brain Res 2010, 213:218-224.
64. Stone E.A., Platt J.E., Herrera A.S., Kirk K.L. The effect of repeated restraintstress, desmethylimipramine or adrenocorticotropin on the α and β-adrenergic components of the cyclic AMP response to norepinephrinein rat brain slices. J Pharmacol Exp Ther 1986, 230:702-707.
65. Stone E., Lin Y., Rosengarten H., Kramer H., Quartermain D. Emerging evidence for a central epinephrine-innervated α1-adrenergic system that regulates behavioral activation and is impaired in depression. Neuropsychopharmacology 2003, 28:1387-1399.
66. Swanson L.W., Petrovich G.D. What is the amygdala?. Trends Neurosci 1998, 21:323-331.
67. Underwood M.D., Mann J.J., Arango V. Serotonergic and noradrenergic neurobiology of alcoholic suicide. Alcohol Clin Exp Res 2004, 28:57S-69S.
68. Vanderwolf C.H. The hippocampus as an olfacto-motor mechanism: were the classical anatomists right after all?. Behav Brain Res 2001, 127:25-47.
69. Ventura R., Cabib S., Alcaro A., Orsini C., Puglisi-Allegra S. Norepinephrine in the prefrontal cortex is critical for amphetamine-induced reward and mesoaccumbens dopamine release. J Neurosci 2003, 23:1879-1885.
70. Ventura R., Coccurello R., Andolina D., Latagliata E.C., Zanettini C., Lampis V., et al. Postnatal aversive experience impairs sensitivity to natural rewards and increases susceptibility to negative events in adult life. Cereb Cortex 2013, 23:1606-1617.
71. Vetulani J. Early maternal separation: a rodent model of depression and a prevailing human condition. Pharmacol Rep 2013, 65. [in press].
72. Vetulani J., Nalepa I. Antidepressants: past, presence and future. Eur J Pharmacol 2000, 405:351-363.
73. Wager-Smith K., Markou A. Depression: a repair response to stress-induced neuronal microdamage that can grade into a chronic neuroinflammatory condition?. Neurosci Biobehav Rev 2011, 35:742-764.
74. 1-Noradrenergic system role in increased motivation for cocaine intake in rats with prolonged access. Eur Neuropsychopharmacol 2008, 18:303-311.
75. Weinshenker D., Schroeder J.P. There and back again: a tale of norepinephrine and drug addiction. Neuropsychopharmacology 2007, 32:1433-1451.
76. 1-adrenergic receptors in rat cerebral cortex: modulation by GABA-mimetic drugs. Pharmacol Rep 2008, 60:980-984.
77. 1-adrenoceptor subtypes. Naunyn Schmiedebergs Arch Pharmacol 1999, 359:439-446.
78. Yao S., Peng M., Zhu X., Cheng M., Qi X. Heat shock protein72 protects hippocampal neurons from apoptosis induced by chronic psychological stress. Int J Neurosci 2007, 117:1551-1564.
79. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res 1996, 711:163-174.
80. Zhang X.Y., Kosten T.A. Prazosin, an α-1 adrenergic antagonist, reduces cocaine-induced reinstatement of drug-seeking. Biol Psychiatry 2005, 57:1202-1204.