Alterations in anxiety-like behavior following knockout of the uncoupling protein 2 (ucp2) gene in mice

Life Sciences

Volumn 89, Issue 19-20, 2011, Pages 677-684

  Gimsa, Ulrike ^a   Kanitz, Ellen ^a   Otten, Winfried ^a   Aheng, Caroline ^b   Tuchscherer, Margret ^a   Ricquier, Daniel ^b   Miroux, Bruno ^b   Ibrahim, Saleh M ^c  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Dopamine; HPA reactivity; Mitochondria; Psychosocial stress; Serotonin; Social defeat; Transgenic mice

Indexed keywords

CD4 ANTIGEN; CD69 ANTIGEN; CD71 ANTIGEN; CORTICOSTERONE; INTERLEUKIN 2 RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCOUPLING PROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CD25+ T LYMPHOCYTE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CYTOKINE PRODUCTION; DISEASE EXACERBATION; DOPAMINERGIC TRANSMISSION; DOWN REGULATION; HELPER CELL; IMMUNE RESPONSE; IMMUNITY; IN VITRO STUDY; MALE; MENTAL STRESS; MOUSE; NEUROENDOCRINE SYSTEM; NEUROLOGIC EXAMINATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEROTONINERGIC SYSTEM; SPLEEN CELL; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANXIETY; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORTICOSTERONE; DISEASE MODELS, ANIMAL; DOPAMINE; GENE EXPRESSION REGULATION; ION CHANNELS; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, INBRED NZB; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; SEROTONIN; SPLEEN; STRESS, PSYCHOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA;

MUS; MUS MUSCULUS;

EID: 80054975968     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2011.08.009     Document Type: Article

References (51)

1. M.C. Alves-Guerra, S. Rousset, C. Pecqueur, Z. Mallat, J. Blanc, A. Tedgui, F. Bouillaud, A.M. Cassard-Doulcier, D. Ricquier, and B. Miroux Bone marrow transplantation reveals the in vivo expression of the mitochondrial uncoupling protein 2 in immune and nonimmune cells during inflammation J Biol Chem 278 2003 42307 42312
2. Z.B. Andrews, A. Rivera, J.D. Elsworth, R.H. Roth, L. Agnati, B. Gago, A. Abizaid, M. Schwartz, K. Fuxe, and T.L. Horvath Uncoupling protein-2 promotes nigrostriatal dopamine neuronal function Eur J Neurosci 24 2006 32 36
3. D. Arsenijevic, H. Onuma, C. Pecqueur, S. Raimbault, B.S. Manning, B. Miroux, E. Couplan, M.C. Alves-Guerra, M. Goubern, R. Surwit, F. Bouillaud, D. Richard, S. Collins, and D. Ricquier Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production Nat Genet 26 2000 435 439
4. R. Avitsur, D.A. Padgett, F.S. Dhabhar, J.L. Stark, K.A. Kramer, H. Engler, and J.F. Sheridan Expression of glucocorticoid resistance following social stress requires a second signal J Leukoc Biol 74 2003 507 513
5. M.T. Bailey, H. Engler, N.D. Powell, D.A. Padgett, and J.F. Sheridan Repeated social defeat increases the bactericidal activity of splenic macrophages through a Toll-like receptor-dependent pathway Am J Physiol Regul Integr Comp Physiol 293 2007 R1180 R1190
6. M.T. Bailey, S.G. Kinsey, D.A. Padgett, J.F. Sheridan, and B. Leblebicioglu Social stress enhances IL-1beta and TNF-alpha production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b + cells Physiol Behav 98 2009 351 358
7. T.L. Bale, A. Contarino, G.W. Smith, R. Chan, L.H. Gold, P.E. Sawchenko, G.F. Koob, W.W. Vale, and K.F. Lee Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress Nat Genet 24 2000 410 414
8. T.L. Bale, R. Picetti, A. Contarino, G.F. Koob, W.W. Vale, and K.F. Lee Mice deficient for both corticotropin-releasing factor receptor 1 (CRFR1) and CRFR2 have an impaired stress response and display sexually dichotomous anxiety-like behavior J Neurosci 22 2002 193 199
9. C. Belzung, and G. Griebel Measuring normal and pathological anxiety-like behaviour in mice: a review Behav Brain Res 125 2001 141 149
10. J. Bouayed, H. Rammal, and R. Soulimani Oxidative stress and anxiety. Relationship and cellular pathways Oxid Med Cell Longev 2 2009 63 67
11. P.D. Butler, J.M. Weiss, J.C. Stout, and C.B. Nemeroff Corticotropin-releasing factor produces fear-enhancing and behavioral activating effects following infusion into the locus coeruleus J Neurosci 10 1990 176 183
12. D.S. Charney Psychobiological mechanisms of resilience and vulnerability: implications for successful adaptation to extreme stress Am J Psychiatry 161 2004 195 216
13. P.L. Dobkin, P.R. Fortin, L. Joseph, J.M. Esdaile, D.S. Danoff, and A.E. Clarke Psychosocial contributors to mental and physical health in patients with systemic lupus erythematosus Arthritis Care Res 11 1998 23 31
14. Y. Emre, C. Hurtaud, T. Nubel, F. Criscuolo, D. Ricquier, and A.M. Cassard-Doulcier Mitochondria contribute to LPS-induced MAPK activation via uncoupling protein UCP2 in macrophages Biochem J 402 2007 271 278
15. M. Fleshner, K.T. Nguyen, C.S. Cotter, L.R. Watkins, and S.F. Maier Acute stressor exposure both suppresses acquired immunity and potentiates innate immunity Am J Physiol Regul Integr Comp Physiol 275 1998 R870 R878
16. K. Fuxe, A. Rivera, K.X. Jacobsen, M. Hoistad, G. Leo, T.L. Horvath, W. Staines, A. De la Calle, and L.F. Agnati Dynamics of volume transmission in the brain. Focus on catecholamine and opioid peptide communication and the role of uncoupling protein 2 J Neural Transm 112 2005 65 76
17. U. Gimsa, E. Kanitz, W. Otten, and S.M. Ibrahim Behavior and stress reactivity in mouse strains with mitochondrial DNA variations Ann N Y Acad Sci 1153 2009 131 138
18. I. Hovatta, R.S. Tennant, R. Helton, R.A. Marr, O. Singer, J.M. Redwine, J.A. Ellison, E.E. Schadt, I.M. Verma, D.J. Lockhart, and C. Barlow Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice Nature 438 2005 662 666
19. C. Hurtaud, C. Gelly, Z. Chen, C. Levi-Meyrueis, and F. Bouillaud Glutamine stimulates translation of uncoupling protein 2mRNA Cell Mol Life Sci 64 2007 1853 1860
20. S.G. Kinsey, M.T. Bailey, J.F. Sheridan, D.A. Padgett, and R. Avitsur Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice Brain Behav Immun 21 2007 458 466
21. T. Kizaki, K. Suzuki, Y. Hitomi, N. Taniguchi, D. Saitoh, K. Watanabe, K. Onoe, N.K. Day, R.A. Good, and H. Ohno Uncoupling protein 2 plays an important role in nitric oxide production of lipopolysaccharide-stimulated macrophages Proc Natl Acad Sci USA 99 2002 9392 9397
22. M. Komada, K. Takao, and T. Miyakawa Elevated plus maze for mice JoVE 2008 e1088
23. S.A. Kromer, M.S. Kessler, D. Milfay, I.N. Birg, M. Bunck, L. Czibere, M. Panhuysen, B. Putz, J.M. Deussing, F. Holsboer, R. Landgraf, and C.W. Turck Identification of glyoxalase-I as a protein marker in a mouse model of extremes in trait anxiety J Neurosci 25 2005 4375 4384
24. H.V. Lad, L. Liu, J.L. Paya-Cano, M.J. Parsons, R. Kember, C. Fernandes, and L.C. Schalkwyk Behavioural battery testing: evaluation and behavioural outcomes in 8 inbred mouse strains Physiol Behav 99 2010 301 316
25. G. Mattiasson, M. Shamloo, G. Gido, K. Mathi, G. Tomasevic, S. Yi, C.H. Warden, R.F. Castilho, T. Melcher, M. Gonzalez-Zulueta, K. Nikolich, and T. Wieloch Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma Nat Med 9 2003 1062 1068
26. S.L. Mehta, and P.A. Li Neuroprotective role of mitochondrial uncoupling protein 2 in cerebral stroke J Cereb Blood Flow Metab 29 2009 1069 1078
27. E. Merlot, E. Moze, R. Dantzer, and P.J. Neveu Cytokine production by spleen cells after social defeat in mice: activation of T cells and reduced inhibition by glucocorticoids Stress 7 2004 55 61
28. D.C. Mohr, S.L. Hart, L. Julian, D. Cox, and D. Pelletier Association between stressful life events and exacerbation in multiple sclerosis: a meta-analysis BMJ 328 2004 731 735
29. D.A. Morilak, and A. Frazer Antidepressants and brain monoaminergic systems: a dimensional approach to understanding their behavioural effects in depression and anxiety disorders Int J Neuropsychopharmacol 7 2004 193 218
30. W. Otten, E. Kanitz, D. Couret, I. Veissier, A. Prunier, and E. Merlot Maternal social stress during late pregnancy affects hypothalamic-pituitary- adrenal function and brain neurotransmitter systems in pig offspring Domest Anim Endocrinol 38 2010 146 155
31. C. Pecqueur, M.C. Alves-Guerra, C. Gelly, C. Levi-Meyrueis, E. Couplan, S. Collins, D. Ricquier, F. Bouillaud, and B. Miroux Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation J Biol Chem 276 2001 8705 8712
32. H. Rammal, J. Bouayed, J. Falla, N. Boujedaini, and R. Soulimani The impact of high anxiety level on cellular and humoral immunity in mice Neuroimmunomodulation 17 2010 1 8
33. H. Rammal, J. Bouayed, C. Younos, and R. Soulimani Evidence that oxidative stress is linked to anxiety-related behaviour in mice Brain Behav Immun 22 2008 1156 1159
34. H. Rammal, J. Bouayed, C. Younos, and R. Soulimani The impact of high anxiety level on the oxidative status of mouse peripheral blood lymphocytes, granulocytes and monocytes Eur J Pharmacol 589 2008 173 175
35. B.A. Reyes, R.J. Valentino, G. Xu, and E.J. Van Bockstaele Hypothalamic projections to locus coeruleus neurons in rat brain Eur J Neurosci 22 2005 93 106
36. D. Richard, S. Clavel, Q. Huang, D. Sanchis, and D. Ricquier Uncoupling protein 2 in the brain: distribution and function Biochem Soc Trans 29 2001 812 817
37. D. Richard, R. Rivest, Q. Huang, F. Bouillaud, D. Sanchis, O. Champigny, and D. Ricquier Distribution of the uncoupling protein 2 mRNA in the mouse brain J Comp Neurol 397 1998 549 560
38. A. Rivera, L.F. Agnati, T.L. Horvath, J.J. Valderrama, A. De la Calle, and K. Fuxe Uncoupling protein 2/3 immunoreactivity and the ascending dopaminergic and noradrenergic neuronal systems: relevance for volume transmission Neuroscience 137 2006 1447 1461
39. R.J. Rodgers, and A. Dalvi Anxiety, defence and the elevated plus-maze Neurosci Biobehav Rev 21 1997 801 810
40. H.G. Ruhe, N.S. Mason, and A.H. Schene Mood is indirectly related to serotonin, norepinephrine and dopamine levels in humans: a meta-analysis of monoamine depletion studies Mol Psychiatry 12 2007 331 359
41. U. Schmitt, and C. Hiemke Strain differences in open-field and elevated plus-maze behavior of rats without and with pretest handling Pharmacol Biochem Behav 59 1998 807 811
42. V. Stefanski Social stress in loser rats: opposite immunological effects in submissive and subdominant males Physiol Behav 63 1998 605 613
43. M. Tagen, A. Elorza, D. Kempuraj, W. Boucher, C.L. Kepley, O.S. Shirihai, and T.C. Theoharides Mitochondrial uncoupling protein 2 inhibits mast cell activation and reduces histamine content J Immunol 183 2009 6313 6319
44. B.T. Thomason, P.J. Brantley, G.N. Jones, H.R. Dyer, and J.L. Morris The relation between stress and disease activity in rheumatoid arthritis J Behav Med 15 1992 215 220
45. S. Vogler, R. Goedde, B. Miterski, R. Gold, A. Kroner, D. Koczan, U.K. Zettl, P. Rieckmann, J.T. Epplen, and S.M. Ibrahim Association of a common polymorphism in the promoter of UCP2 with susceptibility to multiple sclerosis J Mol Med 83 2005 806 811
46. S. Vogler, J. Pahnke, S. Rousset, D. Ricquier, H. Moch, B. Miroux, and S.M. Ibrahim Uncoupling protein 2 has protective function during experimental autoimmune encephalomyelitis Am J Pathol 168 2006 1570 1575
47. A.A. Walf, and C.A. Frye The use of the elevated plus maze as an assay of anxiety-related behavior in rodents Nat Protoc 2 2007 322 328
48. M.J. Watt, A.R. Burke, K.J. Renner, and G.L. Forster Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults Behav Neurosci 123 2009 564 576
49. X. Yu, L. Wester-Rosenlöf, U. Gimsa, S.A. Holzhueter, A. Marques, L. Jonas, K. Bauer, M. Kunz, H. Nizze, M. Tiedge, R. Holmdahl, and S.M. Ibrahim The mtDNA nt7778 G/T polymorphism affects autoimmune diseases and reproductive performance in the mouse Hum Mol Genet 18 2009 4689 4698
50. X. Yu, S. Wieczorek, A. Franke, H. Yin, M. Pierer, C. Sina, T.H. Karlsen, K.M. Boberg, A. Bergquist, M. Kunz, T. Witte, W.L. Gross, J.T. Epplen, M.E. Alarcon-Riquelme, S. Schreiber, and S.M. Ibrahim Association of UCP2-866 G/A polymorphism with chronic inflammatory diseases Genes Immun 10 2009 601 605
51. A. Zafir, and N. Banu Modulation of in vivo oxidative status by exogenous corticosterone and restraint stress in rats Stress 12 2009 167 177