Altered inflammatory responsiveness in serotonin transporter mutant rats

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Macchi, Flavia ^a,b   Homberg, Judith R ^c   Calabrese, Francesca ^a   Zecchillo, Claudia ^a   Racagni, Giorgio ^a   Riva, Marco A ^a   Molteni, Raffaella ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

^c RADBOUD UNIVERSITY   (Netherlands)

Author keywords

Animal model; Cytokines; Inflammation; Lipopolysaccharide (LPS); Microglia

Indexed keywords

BIOLOGICAL MARKER; CD11B ANTIGEN; CD47 ANTIGEN; CYTOKINE; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; FRACTALKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CINC 3 GENE; CONTROLLED STUDY; DEPRESSION; DISEASE PREDISPOSITION; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC CODE; GENETIC MODEL; HETEROZYGOTE; HOMOZYGOTE; IL 6 GENE; IL1 BETAGENE; IMMUNE DYSREGULATION; INFLAMMATION; MALE; MICROGLIA; NONHUMAN; PROTEIN EXPRESSION; RAT; SERT GENE; TNF ALPHA GENE; TNF BETA GENE;

ANIMALS; CYTOKINES; DEPRESSION; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; INFLAMMATION; LIPOPOLYSACCHARIDES; NEUROIMMUNOMODULATION; RATS; RATS, MUTANT STRAINS; REAL-TIME POLYMERASE CHAIN REACTION; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84884317961     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-116     Document Type: Article

References (54)

1. 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, 9:46-56. 10.1038/nrn2297, 2919277, 18073775.
2. Zunszain PA, Hepgul N, Pariante CM. Inflammation and depression. Curr Top Behav Neurosci 2013, 14:135-151.
3. Benton T, Staab J, Evans DL. Medical co-morbidity in depressive disorders. Ann Clin Psychiatry 2007, 19:289-303. 10.1080/10401230701653542, 18058286.
4. Anisman H, Merali Z, Hayley S. Neurotransmitter, peptide and cytokine processes in relation to depressive disorder: comorbidity between depression and neurodegenerative disorders. Prog Neurobiol 2008, 85:1-74. 10.1016/j.pneurobio.2008.01.004, 18346832.
5. Miller AH. Depression and immunity: a role for T cells?. Brain Behav Immun 2010, 24:1-8. 10.1016/j.bbi.2009.09.009, 2787959, 19818725.
6. Connor TJ, Leonard BE. Depression, stress and immunological activation: the role of cytokines in depressive disorders. Life Sci 1998, 62:583-606. 10.1016/S0024-3205(97)00990-9, 9472719.
7. Maes M. Major depression and activation of the inflammatory response system. Adv Exp Med Biol 1999, 461:25-46. 10.1007/978-0-585-37970-8_2, 10442165.
8. Hestad KA, Tonseth S, Stoen CD, Ueland T, Aukrust P. Raised plasma levels of tumor necrosis factor alpha in patients with depression: normalization during electroconvulsive therapy. J ECT 2003, 19:183-188. 10.1097/00124509-200312000-00002, 14657769.
9. Thomas AJ, Davis S, Morris C, Jackson E, Harrison R, O'Brien JT. Increase in interleukin-1beta in late-life depression. Am J Psychiatry 2005, 162:175-177. 10.1176/appi.ajp.162.1.175, 15625217.
10. Lindqvist D, Janelidze S, Hagell P, Erhardt S, Samuelsson M, Minthon L, Hansson O, Bjorkqvist M, Traskman-Bendz L, Brundin L. Interleukin-6 is elevated in the cerebrospinal fluid of suicide attempters and related to symptom severity. Biol Psychiatry 2009, 66:287-292. 10.1016/j.biopsych.2009.01.030, 19268915.
11. Chourbaji S, Urani A, Inta I, Sanchis-Segura C, Brandwein C, Zink M, Schwaninger M, Gass P. IL-6 knockout mice exhibit resistance to stress-induced development of depression-like behaviors. Neurobiol Dis 2006, 23:587-594. 10.1016/j.nbd.2006.05.001, 16843000.
12. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res 1996, 711:163-174. 10.1016/0006-8993(95)01415-2, 8680860.
13. Pucak ML, Kaplin AI. Unkind cytokines: current evidence for the potential role of cytokines in immune-mediated depression. Int Rev Psychiatry 2005, 17:477-483. 10.1080/02646830500381757, 16401546.
14. Frenois F, Moreau M, O'Connor J, Lawson M, Micon C, Lestage J, Kelley KW, Dantzer R, Castanon N. Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 2007, 32:516-531. 10.1016/j.psyneuen.2007.03.005, 1978247, 17482371.
15. Capuron L, Ravaud A, Dantzer R. Early depressive symptoms in cancer patients receiving interleukin 2 and/or interferon alfa-2b therapy. J Clin Oncol 2000, 18:2143-2151.
16. Blakely RD, De Felice LJ, Hartzell HC. Molecular physiology of norepinephrine and serotonin transporters. J Exp Biol 1994, 196:263-281.
17. Lesch KP, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, Benjamin J, Muller CR, Hamer DH, Murphy DL. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531. 10.1126/science.274.5292.1527, 8929413.
18. Bennett AJ, Lesch KP, Heils A, Long JC, Lorenz JG, Shoaf SE, Champoux M, Suomi SJ, Linnoila MV, Higley JD. Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol Psychiatry 2002, 7:118-122. 10.1038/sj.mp.4000949, 11803458.
19. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, McClay J, Mill J, Martin J, Braithwaite A, Poulton R. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389. 10.1126/science.1083968, 12869766.
20. Caspi A, Hariri AR, Holmes A, Uher R, Moffitt TE. Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am J Psychiatry 2010, 167:509-527. 10.1176/appi.ajp.2010.09101452, 2943341, 20231323.
21. Holmes A, Lit Q, Murphy DL, Gold E, Crawley JN. Abnormal anxiety-related behavior in serotonin transporter null mutant mice: the influence of genetic background. Genes Brain Behav 2003, 2:365-380. 10.1046/j.1601-1848.2003.00050.x, 14653308.
22. Lira A, Zhou M, Castanon N, Ansorge MS, Gordon JA, Francis JH, Bradley-Moore M, Lira J, Underwood MD, Arango V, et al. Altered depression-related behaviors and functional changes in the dorsal raphe nucleus of serotonin transporter-deficient mice. Biol Psychiatry 2003, 54:960-971. 10.1016/S0006-3223(03)00696-6, 14625138.
23. Urani A, Chourbaji S, Gass P. Mutant mouse models of depression: candidate genes and current mouse lines. Neurosci Biobehav Rev 2005, 29:805-828. 10.1016/j.neubiorev.2005.03.020, 15925701.
24. Olivier JD, Van Der Hart MG, Van Swelm RP, Dederen PJ, Homberg JR, Cremers T, Deen PM, Cuppen E, Cools AR, Ellenbroek BA. A study in male and female 5-HT transporter knockout rats: an animal model for anxiety and depression disorders. Neuroscience 2008, 152:573-584. 10.1016/j.neuroscience.2007.12.032, 18295409.
25. Calabrese F, Molteni R, Cattaneo A, Macchi F, Racagni G, Gennarelli M, Ellenbroek BA, Riva MA. Long-Term duloxetine treatment normalizes altered brain-derived neurotrophic factor expression in serotonin transporter knockout rats through the modulation of specific neurotrophin isoforms. Mol Pharmacol 2010, 77:846-853. 10.1124/mol.109.063081, 20159945.
26. Calabrese F, Luoni A, Guidotti G, Racagni G, Fumagalli F, Riva MA. Modulation of neuronal plasticity following chronic concomitant administration of the novel antipsychotic lurasidone with the mood stabilizer valproic acid. Psychopharmacology (Berl) 2013, 226:101-112.
27. Molteni R, Cattaneo A, Calabrese F, Macchi F, Olivier JD, Racagni G, Ellenbroek BA, Gennarelli M, Riva MA. Reduced function of the serotonin transporter is associated with decreased expression of BDNF in rodents as well as in humans. Neurobiol Dis 2010, 37:747-755. 10.1016/j.nbd.2009.12.014, 20034565.
28. Gardier AM. Mutant mouse models and antidepressant drug research: focus on serotonin and brain-derived neurotrophic factor. Behav Pharmacol 2009, 20:18-32. 10.1097/FBP.0b013e3283243fcd, 19179848.
29. Lotrich FE. Major depression during interferon-alpha treatment: vulnerability and prevention. Dialogues Clin Neurosci 2009, 11:417-425. 3181938, 20135899.
30. Karg K, Burmeister M, Shedden K, Sen S. The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch Gen Psychiatry 2011, 68:444-454. 10.1001/archgenpsychiatry.2010.189, 3740203, 21199959.
31. Kalueff AV, Ren-Patterson RF, Murphy DL. The developing use of heterozygous mutant mouse models in brain monoamine transporter research. Trends Pharmacol Sci 2007, 28:122-127. 10.1016/j.tips.2007.01.002, 17275930.
32. Homberg JR, van den Hove DL. The serotonin transporter gene and functional and pathological adaptation to environmental variation across the life span. Prog Neurobiol 2012, 99:117-127. 10.1016/j.pneurobio.2012.08.003, 22954594.
33. Carola V, Frazzetto G, Pascucci T, Audero E, Puglisi-Allegra S, Cabib S, Lesch KP, Gross C. Identifying molecular substrates in a mouse model of the serotonin transporter x environment risk factor for anxiety and depression. Biol Psychiatry 2008, 63:840-846. 10.1016/j.biopsych.2007.08.013, 17949690.
34. Smits BM, Mudde JB, van de-Belt J, Verheul M, Olivier J, Homberg J, Guryev V, Cools AR, Ellenbroek BA, Plasterk RH, Cuppen E. Generation of gene knockouts and mutant models in the laboratory rat by ENU-driven target-selected mutagenesis. Pharmacogenet Genomics 2006, 16:159-169.
35. Molteni R, Macchi F, Zecchillo C, Dell'agli M, Colombo E, Calabrese F, Guidotti G, Racagni G, Riva MA. Modulation of the inflammatory response in rats chronically treated with the antidepressant agomelatine. Eur Neuropsychopharmacol 2013, Epub ahead of print.
36. Chourbaji S, Gass P. Glucocorticoid receptor transgenic mice as models for depression. Brain Res Rev 2008, 57:554-560. 10.1016/j.brainresrev.2007.04.008, 17524489.
37. Chourbaji S, Hortnagl H, Molteni R, Riva MA, Gass P, Hellweg R. The impact of environmental enrichment on sex-specific neurochemical circuitries - effects on brain-derived neurotrophic factor and the serotonergic system. Neuroscience 2012, 220:267-276.
38. Fumagalli F, Caffino L, Vogt MA, Frasca A, Racagni G, Sprengel R, Gass P, Riva MA. AMPA GluR-A receptor subunit mediates hippocampal responsiveness in mice exposed to stress. Hippocampus 2011, 21:1028-1035.
39. Fanselow MS, Dong HW. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19. 10.1016/j.neuron.2009.11.031, 2822727, 20152109.
40. Saijo K, Glass CK. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol 2011, 11:775-787. 10.1038/nri3086, 22025055.
41. Perego C, Fumagalli S, De Simoni MG. Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation 2011, 8:174. 10.1186/1742-2094-8-174, 3251548, 22152337.
42. Biber K, Neumann H, Inoue K, Boddeke HW. Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci 2007, 30:596-602. 10.1016/j.tins.2007.08.007, 17950926.
43. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, McNamara RK, Streit WJ, Salafranca MN, Adhikari S, Thompson DA, et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A 1998, 95:10896-10901. 10.1073/pnas.95.18.10896, 27992, 9724801.
44. Lotrich FE, El-Gabalawy H, Guenther LC, Ware CF. The role of inflammation in the pathophysiology of depression: different treatments and their effects. J Rheumatol Suppl 2011, 88:48-54. 10.3899/jrheum.110903, 22045979.
45. Raedler TJ. Inflammatory mechanisms in major depressive disorder. Curr Opin Psychiatry 2011, 24:519-525.
46. Su S, Zhao J, Bremner JD, Miller AH, Tang W, Bouzyk M, Snieder H, Novik O, Afzal N, Goldberg J, Vaccarino V. Serotonin transporter gene, depressive symptoms, and interleukin-6. Circ Cardiovasc Genet 2009, 2:614-620. 10.1161/CIRCGENETICS.109.870386, 2802220, 20031642.
47. Fredericks CA, Drabant EM, Edge MD, Tillie JM, Hallmayer J, Ramel W, Kuo JR, Mackey S, Gross JJ, Dhabhar FS. Healthy young women with serotonin transporter SS polymorphism show a pro-inflammatory bias under resting and stress conditions. Brain Behav Immun 2010, 24:350-357. 10.1016/j.bbi.2009.10.014, 2826575, 19883751.
48. Felice D, O'Leary OF, Pizzo RC, Cryan JF. Blockade of the GABA(B) receptor increases neurogenesis in the ventral but not dorsal adult hippocampus: Relevance to antidepressant action. Neuropharmacology 2012, 63:1380-1388. 10.1016/j.neuropharm.2012.06.066, 22884610.
49. Janssen DG, Caniato RN, Verster JC, Baune BT. A psychoneuroimmunological review on cytokines involved in antidepressant treatment response. Hum Psychopharmacol 2010, 25:201-215. 10.1002/hup.1103, 20373471.
50. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007, 10:1387-1394. 10.1038/nn1997, 17965659.
51. Neher JJ, Neniskyte U, Brown GC. Primary phagocytosis of neurons by inflamed microglia: potential roles in neurodegeneration. Front Pharmacol 2012, 3:27. 3288722, 22403545.
52. Garate I, Garcia-Bueno B, Madrigal JL, Bravo L, Berrocoso E, Caso JR, Mico JA, Leza JC. Origin and consequences of brain Toll-like receptor 4 pathway stimulation in an experimental model of depression. J Neuroinflammation 2011, 8:151. 10.1186/1742-2094-8-151, 3219571, 22053929.
53. Serretti A, Kato M, De-Ronchi D, Kinoshita T. Meta-analysis of serotonin transporter gene promoter polymorphism (5-HTTLPR) association with selective serotonin reuptake inhibitor efficacy in depressed patients. Mol Psychiatry 2007, 12:247-257.
54. Yoshimura R, Hori H, Ikenouchi-Sugita A, Umene-Nakano W, Ueda N, Nakamura J. Higher plasma interleukin-6 (IL-6) level is associated with SSRI- or SNRI-refractory depression. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:722-726. 10.1016/j.pnpbp.2009.03.020, 19332097.