Congenitally learned helpless rats show abnormalities in intracellular signaling

Biological Psychiatry

Volumn 53, Issue 6, 2003, Pages 520-529

  Kohen, Ruth ^a,b   Neumaier, John F ^a,c   Hamblin, Mark W ^a,b   Edwards, Emmeline ^d,e  

^a UNIVERSITY OF WASHINGTON   (United States)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^e NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Animal models; Depression; Gene expression; Learned helplessness; Mood disorders; Second messengers

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE KINASE 3BETA; MESSENGER RNA; PROTEIN BCL 2; PROTEIN KINASE C EPSILON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENZYME ACTIVE SITE; FRONTAL CORTEX; GENE EXPRESSION; GENETIC MODEL; HELPLESSNESS; HIPPOCAMPUS; MALE; MOOD DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECOND MESSENGER; SIGNAL TRANSDUCTION; SPECIES COMPARISON;

EID: 0037443949     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3223(02)01503-2     Document Type: Article

References (77)

1. Diagnostic and Statistical Manual of Mental Disorder. 4th ed:1994;American Psychiatric Press, Washington, DC.
2. Avissar S., Nechamkin Y., Roitman G., Schreiber G. Reduced G protein functions and immunoreactive levels in mononuclear leukocytes of patients with depression. Am J Psychiatry. 154:1997;211-217.
3. Avissar S., Nechamkin Y., Roitman G., Schreiber G. Dynamics of ECT normalization of low G protein function and immunoreactivity in mononuclear leukocytes of patients with major depression. Am J Psychiatry. 155:1998;666-671.
4. Avissar S., Schreiber G., Nechamkin Y., Neuhaus I., Lam G.K., Schwartz P., et al. The effects of seasons and light therapy on G protein levels in mononuclear leukocytes of patients with seasonal affective disorder. Arch Gen Psychiatry. 56:1999;178-183.
5. Baumann B., Bogerts B. Neuroanatomical studies on bipolar disorder. Br J Psychiatry. 41:(suppl):2001;S142-S147.
6. Berrettini W.H. Linkage studies in bipolar syndromes. Young L.T., Joffe R.T. Bipolar Disorder - Biological Models and Their Clinical Application. 1st ed:1997;219-233 Marcel Dekker, New York.
7. Bowers B.J., Wehner J.M. Ethanol consumption and behavioral impulsivity are increased in protein kinase Cgamma null mutant mice. J Neurosci. 21:2001;RC180.
8. Bremner J.D., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. Am J Psychiatry. 157:2000;115-118.
9. Chen A.C., Shirayama Y., Shin K.-H., Neve R.L., Duman R.S. Expression of the cAMP response element binding protein (CREB) in hippocampus produces an antidepressant effect. Biol Psychiatry. 49:2001;753-762.
10. Chen G., Huang L.D., Jiang Y.M., Manji H.K. The mood-stabilizing agent valproate inhibits the activity of glycogen synthase kinase-3. J Neurochem. 72:1999;1327-1330.
11. Chen G., Zeng W.Z., Yuan P.X., Huang L.D., Jiang Y.M., Zhao Z.H., et al. The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. J Neurochem. 72:1999;879-882.
12. Cohen P., Frame S. The renaissance of GSK3. Nat Rev Mol Cell Biol. 2:2001;769-776.
13. Cowburn R.F., Marcusson J.O., Eriksson A., Wiehager B., O'Neill C. Adenylyl cyclase activity and G-protein subunit levels in postmortem frontal cortex of suicide victims. Brain Res. 633:1994;297-304.
14. DeVries A.C., Joh H.-D., Bernard O., Hattori K., Hurn P.D., Traystman R.J., et al. Social stress exacerbates stroke outcome by suppressing Bcl-2 expression. Proc Natl Acad Sci U S A. 98:2001;11824-11828.
15. Dowlatshahi D., MacQueen G.M., Wang J.F., Reiach J.S., Young L.T. G Protein-coupled cyclic AMP signaling in postmortem brain of subjects with mood disorders Effects of diagnosis, suicide, and treatment at the time of death . J Neurochem. 73:1999;1121-1126.
16. Dowlatshahi D., MacQueen G.M., Wang J.F., Young L.T. Increased temporal cortex CREB concentrations and antidepressant treatment in major depression. Lancet. 352:1998;1754-1755.
17. Drevets W.C. Neuroimaging studies of mood disorders. Biol Psychiatry. 48:2000;813-829.
18. Duman R.S., Malberg J., Nakagawa S., D'Sa C. Neuronal plasticity and survival in mood disorders. Biol Psychiatry. 48:2000;732-739.
19. Edwards E., Johnson J., Anderson D., Turano P., Henn F.A. Neurochemical and behavioral consequences of mild, uncontrollable shock Effects of PCPA . Pharmacol Biochem Behav. 25:1986;415-421.
20. Edwards E., King J.A., Fray J. Hypertension and insulin resistant models have divergent propensities to learned helpless behavior in rodents. Am J Hypertens. 13:2000;659-665.
21. Edwards E., King J.A., Fray J.C. Increased basal activity of the HPA axis and renin-angiotensin system in congenital learned helpless rats exposed to stress early in development. Int J Dev Neurosci. 17:1999;805-812.
22. Fields A., Li P.P., Kish S.J., Warsh J.J. Increased cyclic AMP-dependent protein kinase activity in postmortem brain from patients with bipolar affective disorder. J Neurochem. 73:1999;1704-1710.
23. Fiol C.J., Williams J.S., Chou C.H., Wang Q.M., Roach P.J., Andrisani O.M. A secondary phosphorylation of CREB341 at Ser129 is required for the cAMP-mediated control of gene expression. A role for glycogen synthase kinase-3 in the control of gene expression. J Biol Chem. 269:1994;32187-32193.
24. Friedman E., Hoau Y.W., Levinson D., Connell T.A., Singh H. Altered platelet protein kinase C activity in bipolar affective disorder, manic episode. Biol Psychiatry. 33:1993;520-525.
25. Henn F.A., Edwards E. Animal models in the study of genetic factors in human psychopathology. Papolos D.F., Lachman H.M. Genetic Studies in Affective Disorders Overview of Basic Methods, Current Directions, and Critical Research Issues . 1994;177-192 John Wiley & Sons, New York.
26. Hetman M., Cavanaugh J.E., Kimelman D., Xia Z. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J Neurosci. 20:2000;2567-2574.
27. Kendler K.S., Kessler R.C., Walters E.E., MacLean C., Neale M.C., Heath A.C., et al. Stressful life events, genetic liability, and onset of an episode of major depression in women. Am J Psychiatry. 152:1995;833-842.
28. Kessler R.C., McGonagle K.A., Zhao S., Nelson C.B., Hughes M., Eshleman S., et al. Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch Gen Psychiatry. 51:1994;8-19.
29. King J.A., Abend S., Edwards E. Genetic predisposition and the development of posttraumatic stress disorder in an animal model. Biol Psychiatry. 50:2001;231-237.
30. King J.A., Campbell D., Edwards E. Differential development of the stress response in congenital learned helplessness. Int J Dev Neurosci. 11:1993;435-442.
31. King J.A., Edwards E. Early stress and genetic influences on hypothalamic-pituitary-adrenal axis functioning in adulthood. Horm Behav. 36:1999;79-85.
32. Klein P.S., Melton D.A. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A. 93:1996;8455-8459.
33. Lachman H.M., Papolos D.F., Boyle A., Sheftel G., Juthani M., Edwards E., et al. Alterations in glucocorticoid inducible RNAs in the limbic system of learned helpless rats. Brain Res. 609:1993;110-116.
34. Lesort M., Greendorfer A., Stockmeier C., Johnson G.V., Jope R.S. Glycogen synthase kinase-3beta, beta-catenin, and tau in postmortem bipolar brain. J Neural Transm. 106:1999;1217-1222.
35. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci. 20:2000;9104-9110.
36. Manier D.H., Eiring A., Shelton R.C., Sulser F. Beta-adrenoceptor-linked protein kinase A (PKA) activity in human fibroblasts from normal subjects and from patients with major depression. Neuropsychopharmacology. 15:1996;555-561.
37. Manji H.K., Bebchuk J.M., Moore G.J., Glitz D., Hasanat K.A., Chen G. Modulation of CNS signal transduction pathways and gene expression by mood-stabilizing agents Therapeutic implications . J Clin Psychiatry. 60:(suppl 2):1999;27-39.
38. Manji H.K., Lenox R.H. Ziskind-Somerfeld Research Award. Protein kinase C signaling in the brain Molecular transduction of mood stabilization in the treatment of manic-depressive illness . Biol Psychiatry. 46:1999;1328-1351.
39. Manji H.K., Moore G.J., Rajkowska G., Chen G. Neuroplasticity and cellular resilience in mood disorders. Mol Psychiatry. 5:2000;578-593.
40. Moore G.J., Bebchuk J.M., Wilds I.B., Chen G., Manji H.K., Menji H.K. Lithium-induced increase in human brain grey matter. Lancet. 356:2000;1241-1242.
41. Neumaier JF, Edwards E, Plotsky PM (2002): 5-HT1B mRNA regulation in two animal models of altered stress reactivity. Biol Psychiatry 51:902-908.
42. Nibuya M., Morinobu S., Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci. 15:1995;7539-7547.
43. Nibuya M., Nestler E.J., Duman R.S. Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci. 16:1996;2365-2372.
44. Odagaki Y., Garcia-Sevilla J.A., Huguelet P., La Harpe R., Koyama T., Guimon J. Cyclic AMP-mediated signaling components are upregulated in the prefrontal cortex of depressed suicide victims. Brain Res. 898:2001;224-231.
45. Ozaki N., Chuang D.M. Lithium increases transcription factor binding to AP-1 and cyclic AMP-responsive element in cultured neurons and rat brain. J Neurochem. 69:1997;2336-2344.
46. Pacheco M.A., Stockmeier C., Meltzer H.Y., Overholser J.C., Dilley G.E., Jope R.S. Alterations in phosphoinositide signaling and G-protein levels in depressed suicide brain. Brain Res. 723:1996;37-45.
47. Pandey G.N., Dwivedi Y., Kumari R., Janicak P.G. Protein kinase C in platelets of depressed patients. Biol Psychiatry. 44:1998;909-911.
48. Pandey S.C., Mittal N., Lumeng L., Li T.K. Involvement of the cyclic AMP-responsive element binding protein gene transcription factor in genetic preference for alcohol drinking behavior. Alcohol Clin Exp Res. 23:1999;1425-1434.
49. Pandey S.C., Zhang D., Mittal N., Nayyar D. Potential role of the gene transcription factor cyclic AMP-responsive element binding protein in ethanol withdrawal-related anxiety. J Pharmacol Exp Ther. 288:1999;866-878.
50. Perez J., Tardito D. Implicatons of the cAMP signaling pathway in psychiatric disorders A systematic review of the evidence . CNS Spectrums. 6:2001;294-305.
51. Perez J., Tardito D., Mori S., Racagni G., Smeraldi E., Zanardi R. Abnormalities of cyclic adenosine monophosphate signaling in platelets from untreated patients with bipolar disorder. Arch Gen Psychiatry. 56:1999;248-253.
52. Perez J., Tardito D., Racagni G., Smeraldi E., Zanardi R. Protein kinase A and Rap1 levels in platelets of untreated patients with major depression. Mol Psychiatry. 6:2001;44-49.
53. Pliakas A.M., Carlson R.R., Neve R.L., Konradi C., Nestler E.J., Carlezon W.A.J. Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci. 21:2001;7397-7403.
54. Pugazhenthi S., Nesterova A., Sable C., Heidenreich K.A., Boxer L.M., Heasley L.E., et al. Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem. 275:2000;10761-10766.
55. Rajeevan M.S., Vernon S.D., Taysavang N., Unger E.R. Validation of array-based gene expression profiles by real-time (kinetic) RT-PCR. J Mol Diagn. 3:2001;26-31.
56. Rozen S., Skaletsky H.J. Primer3 on the WWW for general users and for biologist programmers. Krawetz S., Misener S. Bioinformatics Methods and Protocols: Methods in Molecular Biology. 2002;365-386 Humana Press, Totowa, NJ.
57. Seligman M.E., Maier S.F. Failure to escape traumatic shock. J Exp Psychol. 74:1967;1-9.
58. Seligman M.E., Rosellini R.A., Kozak M.J. Learned helplessness in the rat Time course, immunization, and reversibility . J Comp Physiol Psychol. 88:1975;542-547.
59. Sheline Y.I., Sanghavi M., Mintun M.A., Gado M.H. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci. 19:1999;5034-5043.
60. Sheline Y.I., Wang P.W., Gado M.H., Csernansky J.G., Vannier M.W. Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci U S A. 93:1996;3908-3913.
61. Shelton R.C., Mainer D.H., Sulser F. CAMP-dependent protein kinase activity in major depression. Am J Psychiatry. 153:1996;1037-1042.
62. Shumake J., Edwards E., Gonzalez-Lima F. Hypermetabolism of paraventricular hypothalamus in the congenitally helpless rat. Neurosci Lett. 311:2001;45-48.
63. Shumake J., Poremba A., Edwards E., Gonzalez-Lima F. Congenital helpless rats as a genetic model for cortex metabolism in depression. Neuroreport. 11:2000;3793-3798.
64. Silva A.J., Kogan J.H., Frankland P.W., Kida S. CREB and memory. Ann Rev Neurosci. 21:1998;127-148.
65. Siuciak J.A., Lewis D.R., Wiegand S.J., Lindsay R.M. Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol Biochem Behav. 56:1997;131-137.
66. Soares J.C., Chen G., Dippold C.S., Wells K.F., Frank E., Kupfer D.J., et al. Concurrent measures of protein kinase C and phosphoinositides in lithium-treated bipolar patients and healthy individuals A preliminary study . Psychiatry Res. 95:2000;109-118.
67. Spleiss O., van Calker D., Scharer L., Adamovic K., Berger M., Gebicke-Haerter P.J. Abnormal G protein alpha(s) - and alpha(i2)-subunit mRNA expression in bipolar affective disorder. Mol Psychiatry. 3:1998;512-520.
68. Sullivan P., Neale M., Kendler K. Genetic epidemiology of major depression Review and meta-analysis . Am J Psychiatry. 157:2000;1552-1562.
69. Thome J., Sakai N., Shin K., Steffen C., Zhang Y.J., Impey S., et al. CAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment. J Neurosci. 20:2000;4030-4036.
70. Vollmayr B., Faust H., Lewicka S., Henn F.A. Brain-derived neurotrophic factor (BDNF) stress response in rats bred for learned helplessness. Mol Psychiatry. 6:2001;471-474.
71. Wang H.Y., Friedman E. Enhanced protein kinase C activity and translocation in bipolar affective disorder brains. Biol Psychiatry. 40:1996;568-575.
72. Wang H.Y., Markowitz P., Levinson D., Undie A.S., Friedman E. Increased membrane-associated protein kinase C activity and translocation in blood platelets from bipolar affective disorder patients. J Psychiatr Res. 33:1999;171-179.
73. Wang J.-F., Young L.T., Li P.P., Warsh J.J. Signal transduction abnormalities in bipolar disorder. Young L.T., Joffe R.T. Bipolar Disorder - Biological Models and Their Clinical Application, 1st ed. 1997;41-79 Marcel Dekker, New York.
74. Weeber E.J., Atkins C.M., Selcher J.C., Varga A.W., Mirnikjoo B., Paylor R., et al. A role for the beta isoform of protein kinase C in fear conditioning. J Neurosci. 20:2000;5906-5914.
75. Willner P. Animal models of depression Validity and applications . Adv Biochem Psychopharmacol. 49:1995;19-41.
76. Young L.T., Li P.P., Kish S.J., Siu K.P., Kamble A., Hornykiewicz O., Warsh J.J. Cerebral cortex Gs alpha protein levels and forskolin-stimulated cyclic AMP formation are increased in bipolar affective disorder. J Neurochem. 61:1993;890-898.
77. Zhang K.Z., Westberg J.A., Holtta E., Andersson L.C. BCL2 regulates neural differentiation. Proc Natl Acad Sci U S A. 93:1996;4504-4508.