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6. Cytokines, Sickness Behavior, and Depression

Author

DANTZER, ROBERT, primary, BLUTHÉ, ROSE-MARIE, additional, CASTANON, NATHALIE, additional, KELLEY, KEITH W., additional, KONSMAN, JAN-PIETER, additional, LAYE, SOPHIE, additional, LESTAGE, JACQUES, additional, and PARNET, PATRICIA, additional

Published
2007
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13. Induction of IDO by Bacille Calmette-Guérin Is Responsible for Development of Murine Depressive-Like Behavior1

Author

O'Connor, Jason C., Lawson, Marcus A., André, Caroline, Briley, Eileen M., Szegedi, Sandra S., Lestage, Jacques, Castanon, Nathalie, Herkenham, Miles, Dantzer, Robert, and Kelley, Keith W.

Subjects
Inflammation, Male, Mice, Knockout, Transcriptional Activation, Mice, Inbred ICR, Depression, Mice, Transgenic, Motor Activity, Article, Up-Regulation, Mice, Inbred C57BL, Mice, Enzyme Induction, Chronic Disease, BCG Vaccine, Animals, Indoleamine-Pyrrole 2,3,-Dioxygenase
Abstract

Chronic inflammation activates the tryptophan-degrading enzyme IDO, which is well known to impair T cell proliferation. We have previously established that bacille Calmette-Guérin (BCG), an attenuated form of Mycobacterium bovis, is associated with persistent activation of IDO in the brain and chronic depressive-like behavior, but a causative role has not been established. In these experiments we used both pharmacologic and genetic approaches to test the hypothesis that IDO activation is responsible for the development of chronic depression that follows BCG infection. BCG induced TNF-alpha, IFN-gamma, and IDO mRNA steady-state transcripts in the brain as well as the enzyme 3-hydroxyanthranilic acid oxygenase (3-HAO) that lies downstream of IDO and generates the neuroactive metabolite, quinolinic acid. Behaviors characteristic of depression were apparent 1 wk after BCG infection. Pretreatment with the competitive IDO inhibitor 1-methyltryptophan fully blocked BCG-induced depressive-like behaviors. Importantly, IDO-deficient mice were completely resistant to BCG-induced depressive-like behavior but responded normally to BCG induction of proinflammatory cytokines. These results are the first to prove that the BCG-induced persistent activation of IDO is accompanied by the induction of 3-hydroxyanthranilic acid oxygenase and that IDO is required as an initial step for the subsequent development of chronic depressive-like behavior.

Published
2009

14. Role of inflammation and hypothalamic-pituitary-adrenal (HPA) axis activation in mood disorders associated with obesity

Author

Castanon, Nathalie, Dinel, Anne-Laure, Andre, Caroline, Lestage, Jacques, Psychoneuroimmunologie, nutrition et génétique, and Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS)

Subjects
[SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

International audience

Published
2008

15. Implication of inflammation in cognitive and mood disorders associated with obesity

Author

Castanon, Nathalie, Dinel, Anne-Laure, Andre, Caroline, Lestage, Jacques, Dantzer, Robert, Psychoneuroimmunologie, nutrition et génétique, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), and University of Illinois System

Subjects
[SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2007

16. Central localization of cytokines induced indoleamine 2,3-dioxygenase(IDO) activation following peripheral immune system stimulation in mice

Author

Andre, Caroline, O'Connor, Jason, Moreau, Maite, Lestage, Jacques, KELLEY, K.W., Dantzer, Robert, Castanon, Nathalie, Psychoneuroimmunologie, nutrition et génétique, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), University of Illinois System, and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2007

17. Inflammation and depression: the usefulness of animal models

Author

Castanon, Nathalie, Moreau, M., Andre, Caroline, O'Connor, J.C., KELLEY, K.W., Dantzer, Robert, Lestage, Jacques, Psychoneuroimmunologie, nutrition et génétique, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Nutrition et Neurobiologie intégrée (NutriNeuro), Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Université Sciences et Technologies - Bordeaux 1-Institut Polytechnique de Bordeaux-Ecole nationale supérieure de chimie, biologie et physique, and University of Illinois System

Subjects
[SDV.GEN]Life Sciences [q-bio]/Genetics, [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics, [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2007

18. Bases biologiques des troubles de l’humeur : la piste des cytokines

Author

Castanon, Nathalie, Andre, Caroline, Moreau, Maite, KELLEY, K.W., Dantzer, Robert, Lestage, Jacques, Psychoneuroimmunologie, nutrition et génétique, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), University of Illinois System, and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV.GEN]Life Sciences [q-bio]/Genetics, [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics, [SDV]Life Sciences [q-bio], [SDV.GEN] Life Sciences [q-bio]/Genetics, [SDV.GEN.GA] Life Sciences [q-bio]/Genetics/Animal genetics, ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2007

19. Inflammation-associated depressive-like behavior in mice is mediated by indoleamine 2,3-dioxygenase: utility of the tail suspension test

Author

Castanon, Nathalie, O'Connor, J.C., Lawson, M.A., Andre, Caroline, Moreau, Maite, Godbout, J.P., Lestage, Jacques, Kelley, K.W., Dantzer, Robert, Psychoneuroimmunologie, nutrition et génétique, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), University of Illinois System, and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2007

20. Long-term dietary leucine and valine supplementation induces significant hypofunction of brain serotonergic function in mice

Author

Castanon, Nathalie, Lestage, Jacques, Moreau, Maite, Dantzer, Robert, ProdInra, Migration, Psychoneuroimmunologie, nutrition et génétique, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), and University of Illinois System

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2007

21. Chronic brain indoleamine 2,3-dioxygenase activation based on Bacille Calmette-Guerin infection affects central 5-HT neurotransmission: a murine model of depressive-like behavior

Author

Castanon, Nathalie, Moreau, Maite, Frenois, François, Dantzer, Robert, Lestage, Jacques, Unité mixte de recherche neurobiologie intégrative, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA), University of Illinois System, and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

International audience

Published
2006

22. Mechanisms of cytokine-induced activation of brain indoleamine 2,3-dioxygenase (IDO), a tryptophan-catabolizing enzyme, involved in behavioral and mood alterations observed in mice models of infection and obesity

Author

Castanon, Nathalie, Andre, Caroline, Dinel, Anne-Laure, Lestage, Jacques, Dantzer, Robert, Unité mixte de recherche neurobiologie intégrative, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA), and University of Illinois System

Subjects
[SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

International audience

Published
2006

23. Activation of brain indoleamine 2,3-dioxygenase (IDO) by cytokines: a model of depressive disorders?

Author

Castanon, Nathalie, Moreau, Maïté, Verrier, Danielle, Lestage, Jacques, Unité mixte de recherche neurobiologie intégrative, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA), Institut National de la Recherche Agronomique (INRA), and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2005

24. Le Bacille de Calmette et Guérin induit l’activation chronique de l’IDO centrale et périphérique : un modèle expérimental de dépression induite par les cytokines

Author

Castanon, Nathalie, Moreau, Maite, Lestage, Jacques, Verrier, Danielle, Mormede, Cécile, Kelley, K.W., Dantzer, Robert, ProdInra, Migration, Unité mixte de recherche neurobiologie intégrative, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA), University of Illinois System, Psychoneuroimmunologie, nutrition et génétique, and Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS)

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2005

25. Role of the indoleamine 2,3 dioxygenase (IDO), a tryptophan-catabolizing enzyme, in the behavioral and mood alterations induced by cytokines

Author

Castanon, Nathalie, Moreau, Maïté, Verrier, Danièle, Dantzer, Robert, Lestage, Jacques, Unité mixte de recherche neurobiologie intégrative, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA), University of Illinois System, and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

International audience

Published
2004

26. Effet de l’administration d’un antidépresseur sur l’expression et les actions des cytokines dans le cerveau

Author

Castanon, Nathalie, Medina, Chantal, Lestage, Jacques, Dantzer, Robert, Unité mixte de recherche neurobiologie intégrative, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA), Institut National de la Santé et de la Recherche Médicale (INSERM), and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2001

27. Un exemple d’interactions entre le système nerveux central et le système immunitaire au travers du métabolisme du tryptophane

Author

Castanon, Nathalie, Lestage, Jacques, Verrier, Danièle, Dantzer, Robert, Unité mixte de recherche neurobiologie intégrative, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA), Institut National de la Recherche Agronomique (INRA), and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2001

28. Apoptosis occurs independently of the release of interleukin-1 beta in the anterior pituitary of end-lactating rats

Author

Chauvet, N., Mouihate, A., Verrier, D., Lestage, Jacques, Unité mixte de recherche neurobiologie intégrative, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA), and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], RAT, ComputingMilieux_MISCELLANEOUS
Abstract

International audience

Published
1996

30. Interferon-γ and Tumor Necrosis Factor-α Mediate the Upregulation of Indoleamine 2,3-Dioxygenase and the Induction of Depressive-Like Behavior in Mice in Response to Bacillus Calmette-Guérin

Author

O'Connor, Jason C., primary, André, Caroline, additional, Wang, Yunxia, additional, Lawson, Marcus A., additional, Szegedi, Sandra S., additional, Lestage, Jacques, additional, Castanon, Nathalie, additional, Kelley, Keith W., additional, and Dantzer, Robert, additional

Published
2009
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41. Aging Exacerbates Depressive-like Behavior in Mice in Response to Activation of the Peripheral Innate Immune System.

Author

Godbout, Jonathan P., Moreau, Maïté, Lestage, Jacques, Chen, Jing, Sparkman, Nathan L., O'Connor, Jason, Castanon, Nathalie, Kelley, Keith W., Dantzer, Robert, and Johnson, Rodney W.

Subjects
DISEASES in older people, ETIOLOGY of diseases, AGE factors in disease, NEURAL stimulation, DEPRESSION in old age, REWARD (Psychology), MENTAL depression
Abstract

Exposure to peripheral infections may be permissive to cognitive and behavioral complications in the elderly. We have reported that peripheral stimulation of the innate immune system with lipopolysaccharide (LPS) causes an exaggerated neuroinflammatory response and prolonged sickness behavior in aged BALB/c mice. Because LPS also causes depressive behavior, the purpose of this study was to determine whether aging is associated with an exacerbated depressive-like response. We confirmed that LPS (0.33 mg/kg intraperitoneal) induced a protracted sickness response in aged mice with reductions in locomotor and feeding activities 24 and 48 h postinjection, when young adults had fully recovered. When submitted to the forced swim test 24 h post-LPS, both young adult and aged mice exhibited an increased duration of immobility. However, when submitted to either the forced swim test or the tail suspension test 72 h post-LPS, an increased duration of immobility was evident only in aged mice. This prolonged depressive-like behavior in aged LPS-treated mice was associated with a more pronounced induction of peripheral and brain indoleamine 2,3-dioxygenase and a markedly higher turnover rate of brain serotonin (as measured by the ratio of 5-hydroxy-indoleacetic acid over 5-hydroxyt-tryptamine) compared to young adult mice at 24 post-LPS injection. These results provide the first evidence that age-associated reactivity of the brain cytokine system could play a pathophysiological role in the increased prevalence of depression observed in the elderly.Neuropsychopharmacology (2008) 33, 2341–2351; doi:10.1038/sj.npp.1301649; published online 12 December 2007 [ABSTRACT FROM AUTHOR]

Published
2008
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43. Bacille Calmette-Guérin Inoculation Induces Chronic Activation of Peripheral and Brain Indoleamine 2,3-Dioxygenase in Mice.

Author

Maïté Moreau, Lestage, Jacques, Verrier, Danièle, Mormède, Cécile, Kelley, Keith W., Dantzer, Robert, and Castanon, Nathalie

Subjects
*ENZYMES, *CYTOKINES, *MENTAL depression, *INTERFERONS, *BCG vaccines, *LABORATORY mice
Abstract

Background. Activation of the indoleamine 2,3-dioxygenase (IDO) enzyme and the resulting decrease in plasma tryptophan (TRP) levels appears to be a crucial link in the relationship between cytokines and depression. We aimed to develop an experimental model of chronic IDO activation based on bacille Calmette-Guérin (BCG) infection that elicits a robust increase in levels of interferon (IFN)-γ, a key cytokine in the activation of IDO. Methods. Mice were inoculated intraperitoneally with BCG (107 cfu/mouse). Lung and brain IDO activity was measured over time, together with plasma levels of TRP and IFN-γ. Results. BCG induced, over the course of several weeks, a chronic increase in serum IFN-γ levels that was associated with a sustained enhancement of lung and brain IDO activity and with decreases in peripheral (serum and lungs) and brain concentrations of TRP, with different time courses between tissues. Conclusions. The model of BCG-induced IDO activation will be useful for the study of the consequences of peripheral immune activation in the brain and the role of TRP metabolism in cytokine-induced mood alteration. [ABSTRACT FROM AUTHOR]

Published
2005
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45. Apoptosis occurs independently of the release of interleukin1β in the anterior pituitary of endlactating rats

Author

Chauvet, Nathalie, Mouihate, Abdeslam, Verrier, Dany, and Lestage, Jacques

Abstract

THE mechanism of Interleukin-1β (IL-1β) release remains unknown. Because of the absence of typical peptide signal on the precursor, IL-1β is not secreted through the classical pathway. The aim of this study was to determine whether IL-1β is released during apoptosis, as has been reported for activated macrophages. We chose anterior pituitary cells of end-lactating rats because of their capacity to produce IL-1β spontaneously and because this organ undergoes cellular degeneration. The combination of two techniques, reverse haemolytic plaque assay (RHPA) and terminal transferase dUTP nick end labelling (TUNEL), allowed us to observe simultaneously the release of IL-1β and apoptosis. Our results show that in these conditions apoptosis is not the mechanism of IL-1β release.

Published
1996

48. Characterization of one {alpha}2-macroglobulin with anticomplementary activity from pregnant women

Author

Lestage, Jacques, Bellott, Ricardo, Metivaud, Jacqueline, Bon, André, Giroud, Jean-Paul, Laulan, Aline, and Châteaureynaud, Pierrette

Abstract

In 15 pregnant women during the third term of pregnancy, the immunomodulatory property of α2-macroglobulin (α2M) was initially detected by measuring the inhibitory effect on immune complement-dependent haemolysis of serum α2M fractions obtained by gel filtration. By a two-step chromatography procedure consisting of gel filtration followed by anion-exchange chromatography, different sub-forms of α2M in serum were separated. Amongst them, it was shown that the inhibition of complement activity was almost exclusively linked to one particular subform. Additional studies revealed that the observed effect was not due to proteases bound to α2M during clotting since, by using protease-specific inhibitors, no change was observed in complement inhibition. This subform, though present at very low levels in control sera, appeared in strikingly increased amounts during the third trimester of pregnancy (35 mg/1) and comprised between 3 and 5% of the total α2M. Results show that the increase of α2M anticomplementary activity is linked to the increase in α2M levels in serum.

Published
1990

50. Interferon-gamma and tumor necrosis factor-alpha mediate the upregulation of indoleamine 2,3-dioxygenase and the induction of depressive-like behavior in mice in response to bacillus Calmette-Guerin.

Author

O'Connor JC, André C, Wang Y, Lawson MA, Szegedi SS, Lestage J, Castanon N, Kelley KW, and Dantzer R

Subjects
Animals, Animals, Newborn, Anti-Inflammatory Agents, Non-Steroidal therapeutic use, Brain drug effects, Brain enzymology, Cells, Cultured, Chromatography, High Pressure Liquid methods, Cytokines metabolism, Depression drug therapy, Depression microbiology, Depression pathology, Dose-Response Relationship, Immunologic, Drug Synergism, Etanercept, Hindlimb Suspension methods, Illness Behavior drug effects, Immobility Response, Tonic drug effects, Immobility Response, Tonic physiology, Immunoglobulin G therapeutic use, Indoleamine-Pyrrole 2,3,-Dioxygenase genetics, Interferon-gamma metabolism, Lung drug effects, Lung enzymology, Male, Mice, Mice, Inbred C57BL, Mice, Inbred ICR, Mice, Knockout, Motor Activity drug effects, Motor Activity physiology, Neuroglia, RNA, Messenger metabolism, Receptors, Interferon deficiency, Receptors, Tumor Necrosis Factor therapeutic use, Serotonin metabolism, Swimming, Tumor Necrosis Factor-alpha metabolism, Up-Regulation physiology, Interferon gamma Receptor, Depression etiology, Indoleamine-Pyrrole 2,3,-Dioxygenase metabolism, Interferon-gamma administration & dosage, Mycobacterium bovis immunology, Tumor Necrosis Factor-alpha administration & dosage, Up-Regulation drug effects
Abstract

Although the tryptophan-degrading enzyme, indoleamine 2,3-dioxygenase (IDO), is a pivotal mediator of inflammation-induced depression, its mechanism of regulation has not yet been investigated in this context. Here, we demonstrate an essential role for interferon (IFN)gamma and tumor necrosis factor (TNF)alpha in the induction of IDO and depressive-like behaviors in response to chronic immune activation. Wild-type (WT) control mice and IFNgammaR(-/-) mice were inoculated with an attenuated form of Mycobacterium bovis, bacille Calmette-Guérin (BCG). Infection with BCG induced an acute episode of sickness that was similar in WT and IFNgammaR(-/-) mice. Increased immobility during the forced swim and tail suspension tests occurred in WT mice 7 d after BCG inoculation but was entirely absent in IFNgammaR(-/-) mice. In WT mice, these indices of depressive-like behavior were associated with chronic upregulation of IFNgamma, interleukin(IL)-1beta, TNFalpha, and IDO. Proinflammatory cytokine expression was elevated in BCG-infected IFNgammaR(-/-) mice as well, but upregulation of lung and brain IDO mRNA was completely abolished. This was accompanied by an attenuation of BCG-induced TNFalpha mRNA and the lack of an increase in plasma kynurenine/tryptophan ratio in the BCG-inoculated IFNgammaR(-/-) mice compared with WT controls. Pretreatment of mice with the TNFalpha antagonist, etanercept, partially blunted BCG-induced IDO activation and depressive-like behavior. In accordance with these in vivo data, IFNgamma and TNFalpha synergized to induce IDO in primary microglia. Together, these data demonstrate that IFNgamma, with TNFalpha, is necessary for induction of IDO and depressive-like behavior in mice after BCG infection.

Published
2009
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