Brain indoleamine 2,3-dioxygenase contributes to the comorbidity of pain and depression

Journal of Clinical Investigation

Volumn 122, Issue 8, 2012, Pages 2940-2954

  Kim, Hyangin ^a   Chen, Lucy ^a   Lim, Grewo ^a   Sung, Backil ^a   Wang, Shuxing ^a   McCabe, Michael F ^a   Rusanescu, Gabriel ^a   Yang, Liling ^a   Tian, Yinghong ^a   Mao, Jianren ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 1; INTERLEUKIN 6; JANUS KINASE; PARACETAMOL; SEROTONIN; STAT PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ADULT; AMINO ACID METABOLISM; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMORBIDITY; CONTROLLED STUDY; DEPRESSION; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; ENZYME INHIBITION; FEMALE; HIPPOCAMPUS; HUMAN; IN VITRO STUDY; INFLAMMATORY PAIN; MALE; MONARTHRITIS; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SOCIAL STRESS; UPREGULATION;

ADOLESCENT; ADULT; AGED; ANIMALS; BRAIN; CHRONIC PAIN; COMORBIDITY; DEPRESSION; FEMALE; GENE KNOCKOUT TECHNIQUES; HIPPOCAMPUS; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; UP-REGULATION; YOUNG ADULT;

EID: 84864772397     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI61884     Document Type: Article

References (79)

1. Sullivan MJ, Reesor K, Mikail S, Fisher R. The treatment of depression in chronic low back pain: review and recommendations. Pain. 1992;50(1):5-13.
2. Von KM, Simon G. The relationship between pain and depression. Br J Psychiatry Suppl. 1996; (30):101-108. (Pubitemid 26179810)
3. Mao J, Gold MS, Backonja MM. Combination drug therapy for chronic pain: a call for more clinical studies. J Pain. 2011;12(2):157-166.
4. Ganong AH, Cotman CW. Kynurenic acid and quinolinic acid act at N-methyl-D-aspartate receptors in the rat hippocampus. J Pharmacol Exp Ther. 1986;236(1):293-299. (Pubitemid 16186161)
5. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9(1):46-56. (Pubitemid 350295688)
6. Popov A, et al. Indoleamine 2,3-dioxygenase-expressing dendritic cells form suppurative granulomas following Listeria monocytogenes infection. J Clin Invest. 2006;116(12):3160-3170. (Pubitemid 44878630)
7. Heyes MP, et al. Quinolinic acid and kynurenine pathway metabolism in inflammatory and non-inflammatory neurological disease. Brain. 1992;115(pt 5):1249-1273.
8. Heyes MP, Lackner A. Increased cerebrospinal fluid quinolinic acid, kynurenic acid, and L-kynurenine in acute septicemia. J Neurochem. 1990;55(1):338-341.
9. Yoshida R, Urade Y, Tokuda M, Hayaishi O. Induction of indoleamine 2,3-dioxygenase in mouse lung during virus infection. Proc Natl Acad Sci U S A. 1979;76(8):4084-4086. (Pubitemid 9249028)
10. O'Connor JC, et al. 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. J Neurosci. 2009;29(13):4200-4209.
11. De Jongh RF, Vissers KC, Meert TF, Booij LH, De Deyne CS, Heylen RJ. The role of interleukin-6 in nociception and pain. Anesth Analg. 2003; 96(4):1096-1103. (Pubitemid 36359050)
12. Maes M, Verkerk R, Bonaccorso S, Ombelet W, Bosmans E, Scharpe S. Depressive and anxiety symptoms in the early puerperium are related to increased degradation of tryptophan into kynurenine, a phenomenon which is related to immune activation. Life Sci. 2002;71(16):1837-1848. (Pubitemid 34880232)
13. Butler SH, Godefroy F, Besson JM, Weil-Fugazza J. A limited arthritic model for chronic pain studies in the rat. Pain. 1992;48(1):73-81.
14. Porsolt RD, Le PM, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature. 1977;266(5604):730-732. (Pubitemid 8073804)
15. Hall CS. Emotional behavior in rat. J Comp Physiol Psychol. 1934;18(3):385-403.
16. Pare WP. Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiol Behav. 1994;55(3):433-439. (Pubitemid 24088009)
17. Guillemin GJ, Smythe G, Takikawa O, Brew BJ. Expression of indoleamine 2,3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia. 2005;49(1):15-23. (Pubitemid 40023649)
18. Roy EJ, Takikawa O, Kranz DM, Brown AR, Thomas DL. Neuronal localization of indoleamine 2,3-dioxygenase in mice. Neurosci Lett. 2005;387(2):95-99. (Pubitemid 41134205)
19. O'Connor JC, et al. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol Psychiatry. 2009;14(5):511-522.
20. Hama AT, Sagen J. Cannabinoid receptor-mediated antinociception with acetaminophen drug combinations in rats with neuropathic spinal cord injury pain. Neuropharmacology. 2010;58(4-5):758-766.
21. Mitchell D, Gelgor L, Weber J, Kamerman PR. Antihypernociceptive synergy between ibuprofen, paracetamol and codeine in rats. Eur J Pharmacol. 2010;642(1-3):86-92.
22. Wang S, Lim G, Mao J, Sung B, Mao J. Regulation of the trigeminal NR1 subunit expression induced by inflammation of the temporomandibular joint region in rats. Pain. 2009;141(1-2):97-103.
23. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J. 1998;334(pt 2):297-314. (Pubitemid 28448572)
24. Legendre F, Dudhia J, Pujol JP, Bogdanowicz P. JAK/STAT but not ERK1/ERK2 pathway mediates interleukin (IL)-6/soluble IL-6R down-regulation of Type II collagen, aggrecan core, and link protein transcription in articular chondrocytes. Association with a down-regulation of SOX9 expression. J Biol Chem. 2003;278(5):2903-2912. (Pubitemid 36801195)
25. Wallenius K, Wallenius V, Sunter D, Dickson SL, Jansson JO. Intracerebroventricular interleukin-6 treatment decreases body fat in rats. Biochem Biophys Res Commun. 2002;293(1):560-565. (Pubitemid 34694245)
26. Dominguez E, Rivat C, Pommier B, Mauborgne A, Pohl M. JAK/STAT3 pathway is activated in spinal cord microglia after peripheral nerve injury and contributes to neuropathic pain development in rat. J Neurochem. 2008;107(1):50-60.
27. Dworkin RH, Gitlin MJ. Clinical aspects of depression in chronic pain patients. Clin J Pain. 1991;7(2):79-94.
28. Delgado PL. Common pathways of depression and pain. J Clin Psychiatry. 2004;65(suppl 12):16-19.
29. Dohrenwend BP, Raphael KG, Marbach JJ, Gallagher RM. Why is depression comorbid with chronic myofascial face pain? A family study test of alternative hypotheses. Pain. 1999;83(2):183-192. (Pubitemid 29479276)
30. Blackburn-Munro G, Blackburn-Munro RE. Chronic pain, chronic stress and depression: coincidence or consequence? J Neuroendocrinol. 2001;13(12):1009- 1023. (Pubitemid 33100218)
31. Schatzberg AF. The relationship of chronic pain and depression. J Clin Psychiatry. 2004;65(suppl 12):3-4.
32. Jasmin L, Rabkin SD, Granato A, Boudah A, Ohara PT. Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature. 2003;424(6946):316-320. (Pubitemid 36899373)
33. Andre J, Zeau B, Pohl M, Cesselin F, Benoliel JJ, Becker C. Involvement of cholecystokininergic systems in anxiety-induced hyperalgesia in male rats: behavioral and biochemical studies. J Neurosci. 2005;25(35):7896-7904. (Pubitemid 41254392)
34. Gameiro GH, da Silva AA, Nouer DF, Ferraz de Arruda Veiga MC. How may stressful experiences contribute to the development of temporomandibular disorders? Clin Oral Investig. 2006;10(4):261-268.
35. Tsigos C, Chrousos GP. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res. 2002;53(4):865-871. (Pubitemid 35282615)
36. Max MB, et al. Amitriptyline relieves diabetic neuropathy pain in patients with normal or depressed mood. Neurology. 1987;37(4):589-596. (Pubitemid 17057933)
37. Sharav Y, Singer E, Schmidt E, Dionne RA, Dubner R. The analgesic effect of amitriptyline on chronic facial pain. Pain. 1987;31(2):199-209.
38. Atkinson JH, et al. A placebo-controlled randomized clinical trial of nortriptyline for chronic low back pain. Pain. 1998;76(3):287-296.
39. Zhang L, Zhang Y, Zhao ZQ. Anterior cingulate cortex contributes to the descending facilitatory modulation of pain via dorsal reticular nucleus. Eur J Neurosci. 2005;22(5):1141-1148. (Pubitemid 41395378)
40. Vogt BA. Pain and emotion interactions in sub-regions of the cingulate gyrus. Nat Rev Neurosci. 2005;6(7):533-544. (Pubitemid 40942820)
41. Derbyshire SW, Jones AK, Gyulai F, Clark S, Townsend D, Firestone LL. Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain. 1997; 73(3):431-445. (Pubitemid 28021849)
42. Ploghaus A, et al. Exacerbation of pain by anxiety is associated with activity in a hippocampal network. J Neurosci. 2001;21(24):9896-9903. (Pubitemid 34184074)
43. Miura H, Ozaki N, Sawada M, Isobe K, Ohta T, Nagatsu T. A link between stress and depression: shifts in the balance between the kynurenine and serotonin pathways of tryptophan metabolism and the etiology and pathophysiology of depression. Stress. 2008;11(3):198-209. (Pubitemid 351874183)
44. Myint AM, Kim YK. Cytokine-serotonin interaction through IDO: a neurodegeneration hypothesis of depression. Med Hypotheses. 2003;61(5-6):519- 525. (Pubitemid 37411894)
45. Mico JA, Gibert-Rahola J, Casas J, Rojas O, Serrano MI, Serrano JS. Implication of beta 1- and beta 2-adrenergic receptors in the antinociceptive effect of tricyclic antidepressants. Eur Neuropsychopharmacol. 1997;7(2):139-145. (Pubitemid 27240347)
46. Sawynok J, Esser MJ, Reid AR. Antidepressants as analgesics: an overview of central and peripheral mechanisms of action. J Psychiatry Neurosci. 2001;26(1):21-29. (Pubitemid 32185176)
47. Stone TW, Perkins MN. Quinolinic acid: a potent endogenous excitant at amino acid receptors in CNS. Eur J Pharmacol. 1981;72(4):411-412. (Pubitemid 11081065)
48. Kwidzinski E, et al. Indolamine 2,3-dioxygenase is expressed in the CNS and down-regulates autoimmune inf lammation. FASEB J. 2005; 19(10):1347-1349. (Pubitemid 41113745)
49. Yan Y, et al. IDO upregulates regulatory T cells via tryptophan catabolite and suppresses encephalitogenic T cell responses in experimental autoimmune encephalomyelitis. J Immunol. 2010; 185(10):5953-5961.
50. Hori T, Oka T, Hosoi M, Aou S. Pain modulatory actions of cytokines and prostaglandin E2 in the brain. Ann N Y Acad Sci. 1998;840:269-281. (Pubitemid 28302054)
51. Lenczowski MJ, et al. Central administration of rat IL-6 induces HPA activation and fever but not sickness behavior in rats. Am J Physiol. 1999; 276(3 pt 2):R652-R658. (Pubitemid 29157493)
52. Huang Y, Henry CJ, Dantzer R, Johnson RW, Godbout JP. Exaggerated sickness behavior and brain proinflammatory cytokine expression in aged mice in response to intracerebroventricular lipopolysaccharide. Neurobiol Aging. 2008;29(11):1744-1753.
53. Zeng Q, et al. Exacerbated mechanical allodynia in rats with depression-like behavior. Brain Res. 2008;1200:27-38.
54. Norman GJ, Karelina K, Zhang N, Walton JC, Morris JS, Devries AC. Stress and IL-1beta contribute to the development of depressive-like behavior following peripheral nerve injury. Mol Psychiatry. 2010;15(4):404-414.
55. Yalcin I, et al. A time-dependent history of mood disorders in a murine model of neuropathic pain. Biol Psychiatry. 2011;70(10):946-953.
56. Pallotta MT, et al. Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat Immunol. 2011;12(9):870-878.
57. Kiefer R, Kieseier BC, Stoll G, Hartung HP. The role of macrophages in immune-mediated damage to the peripheral nervous system. Prog Neurobiol. 2001;64(2):109-127. (Pubitemid 32195409)
58. Smith PC, Hobisch A, Lin DL, Culig Z, Keller ET. Interleukin-6 and prostate cancer progression. Cytokine Growth Factor Rev. 2001;12(1):33-40. (Pubitemid 32294585)
59. Connor TJ, Leonard BE. Depression, stress and immunological activation: the role of cytokines in depressive disorders. Life Sci. 1998;62(7):583-606. (Pubitemid 28045567)
60. Thomas AJ, Davis S, Morris C, Jackson E, Harrison R, O'Brien JT. Increase in interleukin-1beta in latelife depression. Am J Psychiatry. 2005;162(1):175-177.
61. Hou DY, et al. Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res. 2007;67(2):792-801.
62. Okamoto A, et al. Indoleamine 2,3-dioxygenase serves as a marker of poor prognosis in gene expression profiles of serous ovarian cancer cells. Clin Cancer Res. 2005;11(16):6030-6039. (Pubitemid 41170335)
63. Metz R, Duhadaway JB, Kamasani U, Laury- Kleintop L, Muller AJ, Prendergast GC. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2,3-dioxygenase inhibitory compound D-1-methyl- tryptophan. Cancer Res. 2007;67(15):7082-7087. (Pubitemid 47206533)
64. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York, New York, USA: Academic Press; 1998.
65. Krsiak M. Timid singly-housed mice: their value in prediction of psychotropic activity of drugs. Br J Pharmacol. 1975;55(1):141-150.
66. Strekalova T, Spanagel R, Bartsch D, Henn FA, Gass P. Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology. 2004;29(11):2007-2017. (Pubitemid 39486552)
67. Rygula R, Abumaria N, Flugge G, Fuchs E, Ruther E, Havemann-Reinecke U. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res. 2005;162(1):127-134. (Pubitemid 40731540)
68. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 1988;32(1):77-88.
69. Tal M, Bennett GJ. Extra-territorial pain in rats with a peripheral mononeuropathy: mechano-hyperalgesia and mechano-allodynia in the territory of an uninjured nerve. Pain. 1994;57(3):375-382. (Pubitemid 24197338)
70. Steru L, Chermat R, Thierry B, Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl). 1985;85(3):367-370. (Pubitemid 15123115)
71. Denenberg VH. Open-field beavior in the rat: what does it mean? Ann N Y Acad Sci. 1969;159(3):852-859.
72. 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 (Berl). 1987;93(3):358-364. (Pubitemid 17160661)
73. Sigwalt AR, et al. Molecular aspects involved in swimming exercise training reducing anhedonia in a rat model of depression. Neuroscience. 2011; 192:661-674.
74. Zorina Y, Iyengar R, Bromberg KD. Cannabinoid 1 receptor and interleukin-6 receptor together induce integration of protein kinase and transcription factor signaling to trigger neurite outgrowth. J Biol Chem. 2010;285(2):1358-1370.
75. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991;37(2):173-182.
76. Fu X, Zunich SM, O'Connor JC, Kavelaars A, Dantzer R, Kelley KW. Central administration of lipopolysaccharide induces depressive-like behavior in vivo and activates brain indoleamine 2,3 dioxygenase in murine organotypic hippocampal slice cultures. J Neuroinflammation. 2010;7:43.
77. Hakkoum D, Stoppini L, Muller D. Interleukin-6 promotes sprouting and functional recovery in lesioned organotypic hippocampal slice cultures. J Neurochem. 2007;100(3):747-757. (Pubitemid 46095624)
78. Widner B, Werner ER, Schennach H, Wachter H, Fuchs D. Simultaneous measurement of serum tryptophan and kynurenine by HPLC. Clin Chem. 1997;43(12):2424-2426. (Pubitemid 28022985)
79. Laich A, Neurauter G, Widner B, Fuchs D. More rapid method for simultaneous measurement of tryptophan and kynurenine by HPLC. Clin Chem. 2002;48(3):579-581. (Pubitemid 34174597)