A role for BDNF/TrkB signaling in behavioral and physiological consequences of social defeat stress

Genes, Brain and Behavior

Volumn 10, Issue 4, 2011, Pages 424-433

  Razzoli, M ^a   Domenici, E ^a,c   Carboni, L ^a   Rantamaki, T ^b   Lindholm, J ^b   Castren E ^b   Arban, R ^a  

^a GSK   (Italy)

^b UNIVERSITY OF HELSINKI   (Finland)

^c F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

BDNF; Behavior; Immune; Metabolism; Social defeat; Stress; TrkB

Indexed keywords

BIOLOGICAL MARKER; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GHRELIN; INTERLEUKIN 1ALPHA; RANTES;

ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR; BODY WEIGHT; CONTROLLED STUDY; EMBRYO; ENDOCRINE SYSTEM; ENDOPHENOTYPE; FEEDING BEHAVIOR; FEMALE; FOOD INTAKE; GENE EXPRESSION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; HORMONE BLOOD LEVEL; IMMUNE RESPONSE; LONGITUDINAL STUDY; LYMPHOID ORGAN; MALE; METABOLIC PARAMETERS; MOUSE; NEUROPHYSIOLOGY; NONHUMAN; ORGAN WEIGHT; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SOCIAL DEFEAT STRESS; SOCIAL INTERACTION; SOCIAL STRESS; T LYMPHOCYTE; WILD TYPE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHEMOKINES; CYTOKINES; DOMINANCE-SUBORDINATION; HIPPOCAMPUS; MICE; MICE, TRANSGENIC; RECEPTOR, TRKB; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

MUS;

EID: 79958040992     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2011.00681.x     Document Type: Article

References (65)

1. Aigner, L., Arber, S., Kapfhammer, J.P., Laux, T., Schneider, C., Botteri, F., Brenner, H.-R. & Caroni, P. (1995) Overexpression of neural growth-associated protein GAP-43 induces nerve sprouti in the adult nervous system of transgenic mice. Cell 83, 269-278.
2. Ariyasu, H., Takaya, K., Tagami, T., Ogawa, Y., Hosoda, K., Akamizu, T., Suda, M., Koh, T., Natsui, K., Toyooka, S., Shirakami, G., Usui, T., Shimatsu, A., Doi, K., Hosoda, H., Kojima, M., Kangawa, K. & Nakao, K. (2001) Stomach is a major source of circulating ghrelin, and feeding state determines plasma ghrelin-like immunoreactivity levels in humans. J Clin Endocrinol Metab 86, 4753-4758.
3. Bartolomucci, A., Carola, V., Pascucci, T., Puglisi-Allegra, S., Cabib, S., Lesch, K.P., Parmigiani, S., Palanza, P. & Gross, C. (2010) Increased vulnerability to psychosocial stress in heterozygous serotonin transporter knockout mice. Dis Model Mech 3, 459-470.
4. Berton, O., McClung, C.A., DiLeone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., Monteggia, L.M., Self, D.W. & Nestler, E.J. (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868.
5. Beydoun, M.A. & Wang, Y. (2009) Pathways linking socioeconomic status to obesity through depression and lifestyle factors among young US adults. J Affect Disord 123, 52-63.
6. Caspi, A., Sugden, K., Moffitt, T.E., Taylor, A., Craig, I.W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A. & Poulton, R. (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389.
7. Chen, G. & Manji, H.K. (2006) The extracellular signal-regulated kinase pathway: an emerging promising target for mood stabilizers. Curr Opin Psychiatry 19, 313-323.
8. Chen, B., Dowlatshahi, D., MacQueen, G.M., Wang, J.F. & Young, LT. (2001) Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication. Biol Psychiatry 50, 260-265.
9. Chuang, J.C., Krishnanm, V., Yu, H.G., Mason, B., Cui, H., Wilkinson, M.B., Zigman, J.M., Elmquist, J.K., Nestler, E.J. & Lutter, M. (2010) A beta3-adrenergic-leptin-melanocortin circuit regulates behavioral and metabolic changes induced by chronic stress. Biol Psychiatry 67, 1075-1082.
10. Connor, T.J., Harkin, A., Kelly, J.P. & Leonard, B.E. (2000) Olfactory bulbectomy provokes a suppression of interleukin-1beta and tumour necrosis factor-alpha production in response to an in vivo challenge with lipopolysaccharide: effect of chronic desipramine treatment. Neuroimmunomodulation 7, 27-35.
11. Derijk, R.H. (2009) Single nucleotide polymorphisms related to HPA axis reactivity. Neuroimmunomodulation 16, 340-352.
12. Diano, S., Farr, S.A., Benoit, S.C., McNay, E.C., da Silva, I., Horvath, B., Gaskin, F.S., Nonaka, N., Jaeger, L.B., Banks, W.A., Morley, J.E., Pinto, S., Sherwin, R.S., Xu, L., Yamada, K.A., Sleeman, M.W., Tschop, M.H. & Horvath, T.L. (2006) Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci 9, 381-388.
13. Dwivedi, Y., Rizavi, H.S., Conley, R.R., Roberts, R.C., Tamminga, C.A. & Pandey, G.N. (2003) Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects. Arch Gen Psychiatry 60, 804-815.
14. Egan, M.F., Kojima, M., Callicott, J.H., Goldberg, T.E., Kolachana, B.S., Bertolino, A., Zaitsev, E., Gold, B., Goldman, D., Dean, M., Lu, B. & Weinberger, D.R. (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112, 257-269.
15. Ferrer, I., Marín, C., Rey, M.J., Ribalta, T., Goutan, E., Blanco, R., Tolosa, E., Martí, E. (1999) BDNF and full-length and truncated TrkB expression in Alzheimer disease. Implications in therapeutic strategies. J Neuropathol Exp Neurol 58, 729-739.
16. Fox, E.A. & Byerly, M.S. (2004) A mechanism underlying mature-onset obesity: evidence from the hyperphagic phenotype of brain-derived neurotrophic factor mutants. Am J Physiol Regul Integr Comp Physiol 286, R994-R1004.
17. Gatt, J.M., Nemeroff, C.B., Dobson-Stone, C., Paul, R.H., Bryant, R.A., Schofield, P.R., Gordon, E., Kemp, A.H. & Williams L.M. (2009) Interactions between BDNF Val66Met polymorphism and early life stress predict brain and arousal pathways to syndromal depression and anxiety. Mol Psychiatry, 14, 681-695.
18. Goldbacher, E.M., Bromberger, J. & Matthews, K.A. (2009) Lifetime history of major depression predicts the development of the metabolic syndrome in middle-aged women. Psychosom Med 71, 266-272.
19. Golden, S.H., Lazo, M., Carnethon, M., Bertoni, A.G., Schreiner, P.J., Diez Roux, A.V., Lee, H.B. & Lyketsos, C. (2008) Examining a bidirectional association between depressive symptoms and diabetes. JAMA 299, 2751-2759.
20. Gomez-Pinilla, F., Vaynman, S. & Ying, Z. (2008) Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. Eur J Neurosci 28, 2278-2287.
21. Gratacòs, M., González, J.R., Mercader, J.M., de Cid, R., Urretavizcaya, M., Estivill, X. (2007) Brain-derived neurotrophic factor Val66Met and psychiatric disorders: meta-analysis of case-control studies confirm association to substance-related disorders, eating disorders, and schizophrenia. Biol Psychiatry 61, 911-922.
22. Guan, X.M., Yu, H., Palyha, O.C., McKee, K.K., Feighner, S.D., Sirinathsinghji, D.J., Smith, R.G., Van der Ploeg, L.H. & Howard, A.D. (1997) Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Brain Res Mol Brain Res 48, 23-29.
23. Haapasalo, A., Saarelainen, T., Moshnyakov, M., Arumae, U., Kiema, T.R., Saarma, M., Wong, G. & Castren, E. (1999) Expression of the naturally occurring truncated TrkB neurotrophin receptor induces outgrowth of filopodia and processes in neuroblastoma cells. Oncogene 18, 1285-1296.
24. Ingraham, H.A. & Evans, G.A. (1986) Characterization of two atypical promoters and alternate mRNA processing in the mouse Thy-1.2 glycoprotein gene. Mol Cell Biol 6, 2923-2931.
25. Jeanneteau, F., Garabedian, M.J. & Chao, M.V. (2008) Activation of Trk neurotrophin receptors by glucocorticoids provides a neuroprotective effect. Proc Natl Acad Sci U S A 105, 4862-4867.
26. Karpova, N.N., Rantamäki, T., Di Lieto, A., Lindemann, L., Hoener, M.C., Castrén, E. (2010) Darkness reduces BDNF expression in the visual cortex and induces repressive chromatin remodeling at the BDNF gene in both hippocampus and visual cortex. Cell Mol Neurobiol 30, 1117-11123.
27. Kernie, S.G., Liebl, D.J. & Parada, L.F. (2000) BDNF regulates eating behavior and locomotor activity in mice. EMBO J 19, 1290-1300.
28. Kojima, M., Hosoda, H., Date, Y., Nakazato, M., Matsuo, H. & Kangawa, K. (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402, 656-660.
29. Komori, T., Yamamoto, M., Matsumoto, T., Zhang, K. & Okazaki, Y. (2002) Effects of imipramine on T cell subsets in olfactory bulbectomized mice. Neuropsychobiology 46, 194-196.
30. Krishnan, V., Han, M.H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., Laplant, Q., Graham, A., Lutter, M., Lagace, D.C., Ghose, S., Reister, R., Tannous, P., Green, T.A., Neve, R.L., Chakravarty, S., Kumar, A., Eisch, A.J., Self, D.W., Lee, F.S., Tamminga, C.A., Cooper, D.C., Gershenfeld, H.K. & Nestler, E.J. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404.
31. Li, Y., Luikart, B.W., Birnbaum, S., Chen, J., Kwon, C.-H., Kernie, S.G., Bassel-Duby, R. & Parada, L.F. (2008) TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59, 399-412.
32. Lyons, W.E., Mamounas, L.A., Ricaurte, G.A., Coppola, V., Reid, S.W., Bora, S.H., Wihler, C., Koliatsos, V.E. & Tessarollo, L. (1999) Brain-derived neurotrophic factor deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc Natl Acad Sci USA 96, 15239-15244.
33. Ma, J. & Xiao, L. (2009) Obesity and depression in US women: results from the 2005-2006 National Health and Nutritional Examination Survey. Obesity (Silver Spring) 18, 347-353.
34. MacQueen, G.M., Ramakrishnan, K., Croll, S.D., Siuciak, J.A., Yu, G., Young, L.T. & Fahnestock, M. (2001) Performance of heterozygous brain-derived neurotrophic factor knockout mice on behavioral analogues of anxiety, nociception, and depression. Behav Neurosci 115, 1145-1153.
35. Monteggia, L.M., Barrot, M., Powell, C.M., Berton, O., Galanis, V., Gemelli, T., Meuth, S., Nagy, A., Greene, R.W. & Nestler, E.J. (2004) Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc Natl Acad Sci USA 101, 10827-10832.
36. Nibuya, M., Morinobu, S. & Duman, R.S. (1995) Regulation of BDNF and TrkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 15, 7539-7547.
37. Nibuya, M., Nestler, E.J. & Duman, R.S. (1996) Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci 16, 2365-2372.
38. Picchini, A.L., Manji, H.K. & Gould, T.D. (2004) GSK-3 and neurotrophic signalling: novel targets underlying the pathophysiology and treatment of mood disorders? Drug Disc Today 1, 419-428.
39. Pliakas, A.M., Carlson, R.R., Neve, R.L., Konradi, C., Nestler, E.J. & Carlezon, W.A. Jr. (2001) 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, 7397-7403.
40. Raab, A., Seixinger, B.R. & Herz, A. (1985) Continuous social defeat induces an increase of endogenous opioids in discrete brain areas of the Mongolian Gerbil. Peptides 6, 387-391.
41. Rantamäki, T., Hendolin, P., Kankaanpää, A., Mijatovic, J., Piepponen, P., Domenici, E., Chao, M.V., Männistö, P.T. & Castrén, E. (2007) Pharmacologically diverse antidepressants rapidly activate brain-derived neurotrophic factor receptor TrkB and induce phospholipase-Cgamma signaling pathways in mouse brain. Neuropsychopharmacology 10, 2152-2162.
42. Razzoli, M., Carboni, L., Andreoli, M., Ballottari, A. & Arban, R. (2010) Different susceptibility to social defeat stress of BalbC and C57BL/6J mice. Behav Brain Res 216, 100-108.
43. Renn, C.L., Leitch, C.C. & Dorsey, S.G. (2009) In vivo evidence that truncated TrkB.T1 participates in nociception. Mol Pain 5, 61. DOI: 10.1186/1744-8069-5-61.
44. Richardson, L.P., Davis, R., Poulton, R., McCauley, E., Moffitt, T.E., Caspi, A. & Connell F. (2003) A longitudinal evaluation of adolescent depression and adult obesity. Arch Pediatr Adolesc Med 157, 739-745.
45. Rios, M., Fan, G., Fekete, C., Kelly, J., Bates, B., Kuehn, R., Lechan, R.M. & Jaenisch, R. (2001) Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol Endocrinol 15, 1748-1757.
46. Saarelainen, T., Pussinen, R., Koponen, E., Alhonen, L., Wong, G., Sirviö, J. & Castrén, E. (2000) Transgenic mice over-expressing truncated TrkB neurotrophin receptors in neurons have impaired long-term spatial memory but normal hippocampal LTP. Synapse 38, 102-104.
47. Saarelainen, T., Hendolin, P., Lucas, G., Koponen, E., Sairanen, M., MacDonald, E., Agerman, K., Haapasalo, A., Nawa, H., Aloyz, R., Ernfors, P. & Castrén, E. (2003) Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J Neurosci 23, 349-357.
48. Schinder, A.F. & Poo, M. (2000) The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23, 639-645.
49. Schüle, C., Zill, P., Baghai, T.C., Eser, D., Zwanzger, P., Wenig, N., Rupprecht, R. & Bondy, B. (2006) Brain-derived neurotrophic factor Val66Met polymorphism and dexamethasone/CRH test results in depressed patients. Psychoneuroendocrinology 31, 1019-1025.
50. Selye, H. (1950) Stress. Acta, Montreal.
51. Shaltiel, G., Chen, G. & Manji, H.K. (2007) Neurotrophic signaling cascades in the pathophysiology and treatment of bipolar disorder. Curr Opin Pharmacol 7, 22-26.
52. Shirayama, Y., Chen, A.C., Nakagawa, S., Russell, D.S. & Duman, R.S. (2002) Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 22, 3251-3261.
53. Siuciak, J.A., Lewis, D.R., Wiegand, S.J. & Lindsay, R.M. (1997) Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol Biochem Behav 56, 131-137.
54. Tsankova, N.M., Berton, O., Renthal, W., Kumar, A., Neve, R.L. & Nestler, E.J. (2006) Sustained hippocampal chromatin regulation in a mouse model o fdepression and antidepressant action. Nat Neurosci 9, 520-525.
55. Tsankova, N.M., Renthal, W., Kumar, A. & Nestler, E.J. (2007) Epigenetic regulation of psychiatric disorders. Nat Rev Neurosci 8, 355-367.
56. Tsao, D., Thomsen, H.K., Chou, J., Stratton, J., Hagen, M., Loo, C., Garcia, C., Sloane, D.L., Rosenthal, A. & Lin, J.C. (2008) TrkB agonists ameliorate obesity and associated metabolic conditions in mice. Endocrinology 149, 1038-1048.
57. Unger, T.J., Calderon, G.A., Bradley, L.C., Sena-Esteves, M. & Rios, M. (2007) Selective deletion of Bdnf in the ventromedial and dorsomedial hypothalamus of adult mice results in hyperphagic behavior and obesity. J Neurosci 27, 14265-14274.
58. Van Kampen, M., Kramer, M., Hiemke, C., Flugge, G. & Fuchs, E. (2002) The chronic psychosocial stress paradigm in male tree shrews: evaluation of a novel animal model for depressive disorders. Stress 5, 37-46.
59. Vieweg, W.V., Julius, D.A., Benesek, J., Satterwhite, L., Fernandez, A., Feuer, S.J. & Pandurangi, A.K. (2006) Posttraumatic stress disorder and body mass index in military veterans. Preliminary findings. Prog Neuropsychopharmacol Biol Psychiatry 30, 1150-1154.
60. Wang, J.W., Dranovsky, A. & Hen, R. (2008) The when and where of BDNF and the antidepressant response. Biol Psychiatry 63, 640-641.
61. Weisse, C.S. (1992) Depression and immunocompetence: a review of the literature.Psychol Bull 111, 475-489.
62. Wisse, B.E. & Schwartz, M.W. (2003) The skinny on neurotrophins. Nat Neurosci 6, 655-656.
63. Xu, B., Goulding, E.H., Zang, K., Cepoi, D., Cone, R.D., Jones, K.R., Tecott, L.H. & Reichardt, L.F. (2003) Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor. Nat Neurosci 6, 736-742.
64. Yan, H.C., Qu, H.D., Sun, L.R., Li, S.J., Cao, X., Fang, Y.Y., Jie, W., Bean, J.C., Wu, W.K., Zhu, X.H. & Gao, T.M. (2010) Fuzi polysaccharide-1 produces antidepressant-like effects in mice. Int J Neuropsychopharmacol 13, 623-633.
65. Yeo, G.S., Connie Hung, C.C., Rochford, J., Keogh, J., Gray, J., Sivaramakrishnan, S., O'Rahilly, S. & Farooqi, I.S. (2004) A de novo mutation affecting human TrkB associated with severe obesity and developmental delay. Nat Neurosci 7, 1187-1189.