Mice deficient for wild-type p53-induced phosphatase 1 display elevated anxiety- and depression-like behaviors

Neuroscience

Volumn 293, Issue , 2015, Pages 12-22

  Ruan, C S ^a,b   Zhou, F H ^b,d   He, Z Y ^a,f   Wang, S F ^a   Yang, C R ^a,g   Shen, Y J ^a   Guo, Y ^a   Zhao, H B ^a   Chen, L ^a   Liu, D ^d,e   Liu, J ^b   Baune, B T ^d   Xiao, Z C ^a,c   Zhou, X F ^a,b  

^a KUNMING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF ADELAIDE   (Australia)

^e DEPARTMENT OF HEALTH   (Australia)

^f SOUTH CHINA NORMAL UNIVERSITY   (China)

^g SECOND HOSPITAL OF TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Anxiety like behavior; CUMS; Depression like behavior; Exploratory behavior; Fluoxetine; Wip1

Indexed keywords

FLUOXETINE; MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE; UNCLASSIFIED DRUG; WILD TYPE P53 INDUCED PHOSPHATASE 1; ANTIDEPRESSANT AGENT; PROTEIN PHOSPHATASE 2C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CHRONIC DRUG ADMINISTRATION; CHRONIC STRESS; CONTROLLED STUDY; DEPRESSION; DOWN REGULATION; ELEVATED ZERO MAZE TEST; ENVIRONMENTAL STRESS; EXPLORATORY BEHAVIOR; FORCED SWIM TEST; HIPPOCAMPUS; MOUSE; NEOCORTEX; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; TAIL SUSPENSION TEST; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; MALE; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; ANXIETY; DEPRESSION; EXPLORATORY BEHAVIOR; FLUOXETINE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHOPROTEIN PHOSPHATASES; RNA, MESSENGER; STRESS, PSYCHOLOGICAL;

EID: 84924778578     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.02.037     Document Type: Article

References (75)

1. Ahn W.K., Proctor C.C., Flanagan E.H. Mental health clinicians' beliefs about the biological, psychological, and environmental bases of mental disorders. Cognit Sci 2009, 33:147-182.
2. Asnis G.M., McGinn L.K., Sanderson W.C. Atypical depression: clinical aspects and noradrenergic function. Am J Psychiatry 1995, 152:31-36.
3. Bachis A., Cruz M.I., Nosheny R.L., Mocchetti I. Chronic unpredictable stress promotes neuronal apoptosis in the cerebral cortex. Neurosci Lett 2008, 442:104-108.
4. Brown A., Gershon S. Dopamine and depression. J Neural Transm/Gen Sect JNT 1993, 91:75-109.
5. Bruchas M.R., Land B.B., Aita M., Xu M., Barot S.K., Li S., Chavkin C. Stress-induced p38 mitogen-activated protein kinase activation mediates kappa-opioid-dependent dysphoria. J Neurosci 2007, 27:11614-11623.
6. Bruchas M.R., Schindler A.G., Shankar H., Messinger D.I., Miyatake M., Land B.B., Lemos J.C., Hagan C.E., Neumaier J.F., Quintana A. Selective p38α MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 2011, 71:498-511.
7. Brunello N., Blier P., Judd L.L., Mendlewicz J., Nelson C.J., Souery D., Zohar J., Racagni G. Noradrenaline in mood and anxiety disorders: basic and clinical studies. Int Clin Psychopharmacol 2003, 18:191-202.
8. Cassano P., Fava M. Depression and public health: an overview. J Psychosom Res 2002, 53:849-857.
9. Castagné V, Moser P, Roux S, Porsolt RD (2011) Rodent models of depression: forced swim and tail suspension behavioral despair tests in rats and mice. Curr Protoc Neurosci 8:8.10 A.
10. Chew J., Biswas S., Shreeram S., Humaidi M., Wong E.T., Dhillion M.K., Teo H., Hazra A., Fang C.C., Lopez-Collazo E., Bulavin D.V., Tergaonkar V. WIP1 phosphatase is a negative regulator of NF-kappaB signalling. Nat Cell Biol 2009, 11:659-666.
11. Choi J., Nannenga B., Demidov O.N., Bulavin D.V., Cooney A., Brayton C., Zhang Y., Mbawuike I.N., Bradley A., Appella E., Donehower L.A. Mice deficient for the wild-type p53-induced phosphatase gene (Wip1) exhibit defects in reproductive organs, immune function, and cell cycle control. Mol Cell Biol 2002, 22:1094-1105.
12. Chouinard G. A double-blind controlled clinical trial of fluoxetine and amitriptyline in the treatment of outpatients with major depressive disorder. J Clin Psychiatry 1985, 46:32-37.
13. Corman C.D., Shafer J.N. Open-field activity and exploratory behavior. Psychonomic Sci 1968, 13:55-56.
14. Corsi M, Faiferman I, Pich EM, Ratti E, Wren PB (2011) Use of a p38 kinase inhibitor for treating psychiatric disorders. U.S. Patent No. 7,989,479.
15. Dayaram T., Lemoine F.J., Donehower L.A., Marriott S.J. Activation of WIP1 phosphatase by HTLV-1 Tax mitigates the cellular response to DNA damage. PLoS One 2013, 8:e55989.
16. Demidov O., Kek C., Shreeram S., Timofeev O., Fornace A., Appella E., Bulavin D. The role of the MKK6/p38 MAPK pathway in Wip1-dependent regulation of ErbB2-driven mammary gland tumorigenesis. Oncogene 2006, 26:2502-2506.
17. Demidov O.N., Timofeev O., Lwin H.N., Kek C., Appella E., Bulavin D.V. Wip1 phosphatase regulates p53-dependent apoptosis of stem cells and tumorigenesis in the mouse intestine. Cell Stem Cell 2007, 1:180-190.
18. Demirtaş T., Utkan T., Karson A., Yazir Y., Bayramgürler D., Gacar N. The link between unpredictable chronic mild stress model for depression and vascular inflammation?. Inflammation 2014, 37(5):1432-1438.
19. Diehl D.J., Gershon S. The role of dopamine in mood disorders. Compr Psychiatry 1992, 33:115-120.
20. Duffy K.J., Ford R.M. Turn angle and run time distributions characterize swimming behavior for Pseudomonas putida. J Bacteriol 1997, 179:1428-1430.
21. Dulawa S.C., Holick K.A., Gundersen B., Hen R. Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 2004, 29:1321-1330.
22. Eilat E., Mendlovic S., Doron A., Zakuth V., Spirer Z. Increased apoptosis in patients with major depression: a preliminary study. J Immunol 1999, 163:533-534.
23. Fiscella M., Zhang H., Fan S., Sakaguchi K., Shen S., Mercer W.E., Vande Woude G.F., O'Connor P.M., Appella E. Wip1, a novel human protein phosphatase that is induced in response to ionizing radiation in a p53-dependent manner. Proc Natl Acad Sci U S A 1997, 94:6048-6053.
24. Fukunaga M., Miyata S., Liu B.F., Miyazaki H., Hirota Y., Higo S., Hamada Y., Ueyama S., Kasuga M. Methylglyoxal induces apoptosis through activation of p38 MAPK in rat Schwann cells. Biochem Biophys Res Commun 2004, 320:689-695.
25. Galeotti N., Ghelardini C. Regionally selective activation and differential regulation of ERK, JNK and p38 MAP kinase signalling pathway by protein kinase C in mood modulation. Int J Neuropsychopharmacol 2012, 15:781-793.
26. Gillespie C.F., Phifer J., Bradley B., Ressler K.J. Risk and resilience: genetic and environmental influences on development of the stress response. Depression Anxiety 2009, 26:984-992.
27. Gururajan A., Hill R., van den Buuse M. Long-term differential effects of chronic young-adult corticosterone exposure on anxiety and depression-like behaviour in BDNF heterozygous rats depend on the experimental paradigm used. Neurosci Lett 2014, 576:6-10.
28. Hastings R.S., Parsey R.V., Oquendo M.A., Arango V., Mann J.J. Volumetric analysis of the prefrontal cortex, amygdala, and hippocampus in major depression. Neuropsychopharmacology 2004, 29:952-959.
29. Herlaar E., Brown Z. P38 MAPK signalling cascades in inflammatory disease. Mol Med Today 1999, 5:439-447.
30. Huang G.J., Herbert J. Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol Psychiatry 2006, 59:619-624.
31. Kale A.Y., Paranjape S.A., Briski K.P. Site-specific habituation of insulin-induced hypoglycemic induction of fos immunoreactivity in glucocorticoid receptor: immunopositive neurons in the male rat brain. Exp Brain Res 2007, 176:260-266.
32. Krystal J., Sanacora G., Blumberg H., Anand A., Charney D., Marek G., Epperson C., Goddard A., Mason G. Glutamate and GABA systems as targets for novel antidepressant and mood-stabilizing treatments. Mol Psychiatry 2001, 7:S71-80.
33. Kulkarni S., Singh K., Bishnoi M. Elevated zero maze: a paradigm to evaluate antianxiety effects of drugs. Methods Find Exp Clin Pharmacol 2007, 29:343-348.
34. Lee H., Kim J., Yim S., Kim M., Kim S., Kim Y., Kim C., Chung J. Fluoxetine enhances cell proliferation and prevents apoptosis in dentate gyrus of maternally separated rats. Mol Psychiatry 2001, 6(610). 725-618.
35. Lowe J., Cha H., Lee M.O., Mazur S.J., Appella E., Fornace A.J. Regulation of the Wip1 phosphatase and its effects on the stress response. Front Biosci 2012, 17:1480.
36. Lu J., Xu Y., Hu W., Gao Y., Ni X., Sheng H., Liu Y. Exercise ameliorates depression-like behavior and increases hippocampal BDNF level in ovariectomized rats. Neurosci Lett 2014, 573:13-18.
37. Macurek L., Benada J., Müllers E., Halim V.A., Krejčíková K., Burdová K., Pecháčková S., Hodný Z., Lindqvist A., Medema R.H. Downregulation of Wip1 phosphatase modulates the cellular threshold of DNA damage signaling in mitosis. Cell Cycle 2012, 12:251-262.
38. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 2009, 65:732-741.
39. Oshima T., Sasaki M., Kataoka H., Miwa H., Takeuchi T., Joh T. Wip1 protects hydrogen peroxide-induced colonic epithelial barrier dysfunction. Cell Mol Life Sci: CMLS 2007, 64:3139-3147.
40. Park J.Y., Song J.Y., Kim H.M., Han H.S., Seol H.S., Jang S.J., Choi J. P53-Independent expression of wild-type p53-induced phosphatase 1 (Wip1) in methylmethane sulfonate-treated cancer cell lines and human tumors. Int J Biochem Cell Biol 2012, 44:896-904.
41. Peng Z., Wang H., Zhang R., Chen Y., Xue F., Nie H., Chen Y., Wu D., Wang Y., Wang H., Tan Q. Gastrodin ameliorates anxiety-like behaviors and inhibits IL-1beta level and p38 MAPK phosphorylation of hippocampus in the rat model of posttraumatic stress disorder. Physiol Res 2013, 62(5):537-545.
42. Petty F. GABA and mood disorders: a brief review and hypothesis. J Affect Disord 1995, 34:275-281.
43. Pierce A., Williamson A., Jaworska E., Griffiths J.R., Taylor S., Walker M., O'Dea M.A., Spooncer E., Unwin R.D., Poolman T. Identification of nuclear protein targets for six leukemogenic tyrosine kinases governed by post-translational regulation. PLoS One 2012, 7:e38928.
44. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 2003, 463:3-33.
45. Raison C.L., Capuron L., Miller A.H. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 2006, 27:24-31.
46. Roumestan C., Michel A., Bichon F., Portet K., Detoc M., Henriquet C., Jaffuel D., Mathieu M. Anti-inflammatory properties of desipramine and fluoxetine. Respir Res 2007, 8:35.
47. Ruan C.S., Wang S.F., Shen Y.J., Guo Y., Yang C.R., Zhou F.H., Tan L.T., Zhou L., Liu J.J., Wang W.Y., Xiao Z.C., Zhou X.F. Deletion of TRIM32 protects mice from anxiety- and depression-like behaviors under mild stress. Eur J Neurosci 2014, 40:2680-2690.
48. Sablina A.A., Chen W., Arroyo J.D., Corral L., Hector M., Bulmer S.E., DeCaprio J.A., Hahn W.C. The tumor suppressor PP2A Abeta regulates the RalA GTPase. Cell 2007, 129:969-982.
49. Sheline Y.I. Neuroimaging studies of mood disorder effects on the brain. Biol Psychiatry 2003, 54:338-352.
50. Shepherd J.K., Grewal S.S., Fletcher A., Bill D.J., Dourish C.T. Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology 1994, 116:56-64.
51. Snyder J.S., Soumier A., Brewer M., Pickel J., Cameron H.A. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 2011, 476:458-461.
52. Spink A.J., Tegelenbosch R.A., Buma M.O., Noldus L.P. The EthoVision video tracking system-a tool for behavioral phenotyping of transgenic mice. Physiol Behav 2001, 73:731-744.
53. Stapley J., Keogh J.S. Exploratory and antipredator behaviours differ between territorial and nonterritorial male lizards. Anim Behav 2004, 68:841-846.
54. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology 1985, 85:367-370.
55. Sun Z.G., Huang Q.Z., Xu C.Y., Chen L.P. [Effects of shuyu ningxln recipe on the praxiology and the expressions of hippocampal BDNF and trkB of model rats with chronic stress-induced depression]. Zhongguo Zhong xi yi jie he za zhi Zhongguo Zhongxiyi jiehe zazhi = Chinese journal of integrated traditional and Western medicine / Zhongguo Zhong xi yi jie he xue hui. Zhongguo Zhong yi yan jiu yuan zhu ban 2013, 33:370-375.
56. Takekawa M., Adachi M., Nakahata A., Nakayama I., Itoh F., Tsukuda H., Taya Y., Imai K. P53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. EMBO J 2000, 19:6517-6526.
57. Treusch S., Hamamichi S., Goodman J.L., Matlack K.E., Chung C.Y., Baru V., Shulman J.M., Parrado A., Bevis B.J., Valastyan J.S., Han H., Lindhagen-Persson M., Reiman E.M., Evans D.A., Bennett D.A., Olofsson A., DeJager P.L., Tanzi R.E., Caldwell K.A., Caldwell G.A., Lindquist S. Functional links between Abeta toxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast. Science 2011, 334:1241-1245.
58. Trullas R., Jackson B., Skolnick P. Genetic differences in a tail suspension test for evaluating antidepressant activity. Psychopharmacology 1989, 99:287-288.
59. Van Laethem A., Van Kelst S., Lippens S., Declercq W., Vandenabeele P., Janssens S., Vandenheede J.R., Garmyn M., Agostinis P. Activation of p38 MAPK is required for Bax translocation to mitochondria, cytochrome c release and apoptosis induced by UVB irradiation in human keratinocytes. FASEB J 2004, 18:1946-1948.
60. Vaswani M., Linda F.K., Ramesh S. Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review. Prog Neuropsychopharmacol Biol Psychiatry 2003, 27:85-102.
61. Vaz B., Ramadan K. Wip1 downregulation conserves truncated DNA damage response (DDR) in mitosis. Cell Cycle 2013, 12:391.
62. Velazquez-Moctezuma J., Diaz Ruiz O. Neonatal treatment with clomipramine increased immobility in the forced swim test: an attribute of animal models of depression. Pharmacol Biochem Behav 1992, 42:737-739.
63. Venkitaramani D.V., Moura P.J., Picciotto M.R., Lombroso P.J. Striatal-enriched protein tyrosine phosphatase (STEP) knockout mice have enhanced hippocampal memory. Eur J Neurosci 2011, 33:2288-2298.
64. Vollmer L.E., Ghosal S., Rush J.A., Sallee F.R., Herman J.P., Weinert M., Sah R. Attenuated stress-evoked anxiety, increased sucrose preference and delayed spatial learning in glucocorticoid-induced receptor-deficient mice. Genes Brain Behav 2013, 12:241-249.
65. Willner P., Towell A., Sampson D., Sophokleous S., Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 1987, 93:358-364.
66. Wong D.T., Horng J.S., Bymaster F.P., Hauser K.L., Molloy B.B. A selective inhibitor of serotonin uptake: Lilly 110140, 3-(p-trifluoromethylphenoxy)-N-methyl-3-phenylpropylamine. Life Sci 1974, 15:471-479.
67. Yang C.R., Zhang Z.G., Bai Y.Y., Zhou H.F., Zhou L., Ruan C.S., Li F., Li C.Q., Zheng H.Y., Shen L.J., Zhou X.F. Foraging activity is reduced in a mouse model of depression. Neurotox Res 2014, 25:235-247.
68. Yang J.M., Rui B.B., Chen C., Chen H., Xu T.J., Xu W.P., Wei W. Acetylsalicylic acid enhances the anti-inflammatory effect of fluoxetine through inhibition of NF-kappaB, p38-MAPK and ERK1/2 activation in lipopolysaccharide-induced BV-2 microglia cells. Neuroscience 2014, 275:296-304.
69. Yao Z., DuBois D.C., Almon R.R., Jusko W.J. Modeling circadian rhythms of glucocorticoid receptor and glutamine synthetase expression in rat skeletal muscle. Pharm Res 2006, 23:670-679.
70. Young L.T., Warsh J.J., Kish S.J., Shannak K., Hornykeiwicz O. Reduced brain 5-HT and elevated NE turnover and metabolites in bipolar affective disorder. Biol Psychiatry 1994, 35:121-127.
71. Young S.N., Leyton M. The role of serotonin in human mood and social interaction: insight from altered tryptophan levels. Pharmacol Biochem Behav 2002, 71:857-865.
72. Yu E., Ahn Y.S., Jang S.J., Kim M.J., Yoon H.S., Gong G., Choi J. Overexpression of the wip1 gene abrogates the p38 MAPK/p53/Wip1 pathway and silences p16 expression in human breast cancers. Breast Cancer Res Treat 2007, 101:269-278.
73. Zhou H., Wang J., Jiang J., Stavrovskaya I.G., Li M., Li W., Wu Q., Zhang X., Luo C., Zhou S., Sirianni A.C., Sarkar S., Kristal B.S., Friedlander R.M., Wang X. N-acetyl-serotonin offers neuroprotection through inhibiting mitochondrial death pathways and autophagic activation in experimental models of ischemic injury. J Neurosci 2014, 34:2967-2978.
74. Zhu Y.H., Zhang C.W., Lu L., Demidov O.N., Sun L., Yang L., Bulavin D.V., Xiao Z.C. Wip1 regulates the generation of new neural cells in the adult olfactory bulb through p53-dependent cell cycle control. Stem cells 2009, 27:1433-1442.
75. Zwerina J., Hayer S., Redlich K., Bobacz K., Kollias G., Smolen J.S., Schett G. Activation of p38 MAPK is a key step in tumor necrosis factor-mediated inflammatory bone destruction. Arthritis Rheum 2006, 54:463-472.