Lipopolysaccharide administration induces sex-dependent behavioural and serotonergic neurochemical signatures in mice

Pharmacology Biochemistry and Behavior

Volumn 153, Issue , 2017, Pages 168-181

  Sens, Jonathon ^a   Schneider, Eric ^a   Mauch, Joseph ^a   Schaffstein, Anna ^a   Mohamed, Sara ^a   Fasoli, Kathryn ^a   Saurine, Joseph ^a   Britzolaki, Aikaterini ^a   Thelen, Connor ^a   Pitychoutis, Pothitos M ^a  

^a UNIVERSITY OF DAYTON   (United States)

Author keywords

Cytokines; Depression; Dopamine; Females; Forced swim test; Gender; Hippocampus; Immune; Prefrontal cortex; Serotonin; Sickness; Splash test; Stress

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; DIHYDROXYPHENYLACETIC ACID; DOPAMINE; HOMOVANILLIC ACID; LIPOPOLYSACCHARIDE; MONOAMINE; SEROTONIN; SUCROSE;

ADULT; AMYGDALA; ANHEDONIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANOREXIA; ARTICLE; BEHAVIOR CHANGE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC ACTIVITY; FEMALE; FOOD INTAKE; FORCED SWIM TEST; GROOMING; HIPPOCAMPUS; HYPERACTIVITY; HYPOTHALAMUS; LOCOMOTION; MAJOR DEPRESSION; MALE; MENTAL PERFORMANCE; MOUSE; NEUROCHEMISTRY; NONHUMAN; OPEN FIELD TEST; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PREVALENCE; PRIORITY JOURNAL; SCREENING TEST; SEROTONINERGIC SYSTEM; SEX DIFFERENCE; SPLASH TEST; SUCROSE PREFERENCE TEST; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECTS; EATING; METABOLISM; MOTOR ACTIVITY; SEXUAL DEVELOPMENT;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; EATING; FEMALE; GROOMING; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; SEROTONIN; SEX CHARACTERISTICS; SUCROSE;

EID: 85008657181     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2016.12.016     Document Type: Article

References (58)

1. Adachi, M., Barrot, M., Autry, A.E., Theobald, D., Monteggia, L.M., Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol. Psychiatry 63 (2008), 642–649.
2. Adzic, M., Djordjevic, J., Mitic, M., Brkic, Z., Lukic, I., Radojcic, M., The contribution of hypothalamic neuroendocrine, neuroplastic and neuroinflammatory processes to lipopolysaccharide-induced depressive-like behaviour in female and male rats: involvement of glucocorticoid receptor and C/EBP-beta. Behav. Brain Res. 291 (2015), 130–139.
3. Asarian, L., Langhans, W., A new look on brain mechanisms of acute illness anorexia. Physiol. Behav. 100 (2010), 464–471.
4. Autry, A.E., Adachi, M., Nosyreva, E., Na, E.S., Los, M.F., Cheng, P.F., Kavalali, E.T., Monteggia, L.M., NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475 (2011), 91–95.
5. Avitsur, R., Yirmiya, R., The immunobiology of sexual behavior: gender differences in the suppression of sexual activity during illness. Pharmacol. Biochem. Behav. 64 (1999), 787–796.
6. Avitsur, R., Donchin, O., Barak, O., Cohen, E., Yirmiya, R., Behavioral effects of interleukin-1 beta: modulation by gender, estrus cycle, and progesterone. Brain Behav. Immun. 9 (1995), 234–241.
7. Avitsur, R., Cohen, E., Yirmiya, R., Effects of interleukin-1 on sexual attractivity in a model of sickness behavior. Physiol. Behav. 63 (1997), 25–30.
8. Berton, O., Nestler, E.J., New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7 (2006), 137–151.
9. Bouman, A., Heineman, M.J., Faas, M.M., Sex hormones and the immune response in humans. Hum. Reprod. Update 11 (2005), 411–423.
10. Brachman, R.A., McGowan, J.C., Perusini, J.N., Lim, S.C., Pham, T.H., Faye, C., Gardier, A.M., Mendez-David, I., David, D.J., Hen, R., Denny, C.A., Ketamine as a prophylactic against stress-induced depressive-like behavior. Biol. Psychiatry 79 (2016), 776–786.
11. Can, A., Dao, D.T., Arad, M., Terrillion, C.E., Piantadosi, S.C., Gould, T.D., The mouse forced swim test. J. Vis. Exp., 2012, e3638.
12. Collins, P.Y., Patel, V., Joestl, S.S., March, D., Insel, T.R., Daar, A.S., Anderson, W., Dhansay, M.A., Phillips, A., Shurin, S., Walport, M., Ewart, W., Savill, S.J., Bordin, I.A., Costello, E.J., Durkin, M., Fairburn, C., Glass, R.I., Hall, W., Huang, Y., Hyman, S.E., Jamison, K., Kaaya, S., Kapur, S., Kleinman, A., Ogunniyi, A., Otero-Ojeda, A., Poo, M.M., Ravindranath, V., Sahakian, B.J., Saxena, S., Singer, P.A., Stein, D.J., Grand challenges in global mental health. Nature 475 (2011), 27–30.
13. Commissiong, J.W., Monoamine metabolites: their relationship and lack of relationship to monoaminergic neuronal activity. Biochem. Pharmacol. 34 (1985), 1127–1131.
14. Dalla, C., Pitychoutis, P.M., Kokras, N., Papadopoulou-Daifoti, Z., Sex differences in animal models of depression and antidepressant response. Basic Clin. Pharmacol. Toxicol. 106 (2010), 226–233.
15. Dalla, C., Pitychoutis, P.M., Kokras, N., Papadopoulou-Daifoti, Z., Sex differences in response to stress and expression of depressive-like behaviours in the rat. Curr. Top. Behav. Neurosci. 8 (2011), 97–118.
16. Dantzer, R., O'Connor, J.C., Freund, G.G., Johnson, R.W., Kelley, K.W., From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9 (2008), 46–56.
17. Darnall, B.D., Suarez, E.C., Sex and gender in psychoneuroimmunology research: past, present and future. Brain Behav. Immun. 23 (2009), 595–604.
18. Dunn, A.J., Endotoxin-induced activation of cerebral catecholamine and serotonin metabolism: comparison with interleukin-1. J. Pharmacol. Exp. Ther. 261 (1992), 964–969.
19. Dunn, A.J., Swiergiel, A.H., de Beaurepaire, R., Cytokines as mediators of depression: what can we learn from animal studies?. Neurosci. Biobehav. Rev. 29 (2005), 891–909.
20. Elenkov, I.J., Neurohormonal-cytokine interactions: implications for inflammation, common human diseases and well-being. Neurochem. Int. 52 (2008), 40–51.
21. Elhwuegi, A.S., Central monoamines and their role in major depression. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 28 (2004), 435–451.
22. Engler, H., Benson, S., Wegner, A., Spreitzer, I., Schedlowski, M., Elsenbruch, S., Men and women differ in inflammatory and neuroendocrine responses to endotoxin but not in the severity of sickness symptoms. Brain Behav. Immun. 52 (2016), 18–26.
23. Franceschelli, A., Sens, J., Herchick, S., Thelen, C., Pitychoutis, P.M., Sex differences in the rapid and the sustained antidepressant-like effects of ketamine in stress-naive and “depressed” mice exposed to chronic mild stress. Neuroscience 290 (2015), 49–60.
24. Frederic, F., Oliver, C., Wollman, E., Delhaye-Bouchaud, N., Mariani, J., IL-1 and LPS induce a sexually dimorphic response of the hypothalamo-pituitary-adrenal axis in several mouse strains. Eur. Cytokine Netw. 4 (1993), 321–329.
25. Frenois, F., Moreau, M., O'Connor, J., Lawson, M., Micon, C., Lestage, J., Kelley, K.W., 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 32 (2007), 516–531.
26. Gaillard, R.C., Spinedi, E., Sex- and stress-steroids interactions and the immune system: evidence for a neuroendocrine-immunological sexual dimorphism. Domest. Anim. Endocrinol. 15 (1998), 345–352.
27. Geary, N., Asarian, L., Sheahan, J., Langhans, W., Estradiol-mediated increases in the anorexia induced by intraperitoneal injection of bacterial lipopolysaccharide in female rats. Physiol. Behav. 82 (2004), 251–261.
28. Grigoriadis, S., Robinson, G.E., Gender issues in depression. Ann. Clin. Psychiatry 19 (2007), 247–255.
29. Hartley, J.E., Montgomery, A.M., 8-OH-DPAT inhibits both prandial and waterspray-induced grooming. J. Psychopharmacol. 22 (2008), 746–752.
30. Hodes, G.E., Kana, V., Menard, C., Merad, M., Russo, S.J., Neuroimmune mechanisms of depression. Nat. Neurosci. 18 (2015), 1386–1393.
31. Holden, C., Sex and the suffering brain. Science, 308, 2005, 1574.
32. Leech, N.L., Barrett, K.C., Morgan, G.A., SPSS for Intermediate Statistics: Use and 5 Interpretation. 2005, Lawrence Erlbaum, Mahwah, N.J.
33. Linthorst, A.C., Reul, J.M., Brain neurotransmission during peripheral inflammation. Ann. N. Y. Acad. Sci. 840 (1998), 139–152.
34. Linthorst, A.C., Reul, J.M., Inflammation and brain function under basal conditions and during long-term elevation of brain corticotropin-releasing hormone levels. Adv. Exp. Med. Biol. 461 (1999), 129–152.
35. Linthorst, A.C., Flachskamm, C., Holsboer, F., Reul, J.M., Intraperitoneal administration of bacterial endotoxin enhances noradrenergic neurotransmission in the rat preoptic area: relationship with body temperature and hypothalamic–pituitary–adrenocortical axis activity. Eur. J. Neurosci. 7 (1995), 2418–2430.
36. Lu, Y.C., Yeh, W.C., Ohashi, P.S., LPS/TLR4 signal transduction pathway. Cytokine 42 (2008), 145–151.
37. Machado, D.G., Cunha, M.P., Neis, V.B., Balen, G.O., Colla, A., Grando, J., Brocardo, P.S., Bettio, L.E., Capra, J.C., Rodrigues, A.L., Fluoxetine reverses depressive-like behaviors and increases hippocampal acetylcholinesterase activity induced by olfactory bulbectomy. Pharmacol. Biochem. Behav. 103 (2012), 220–229.
38. Marcus, S.M., Young, E.A., Kerber, K.B., Kornstein, S., Farabaugh, A.H., Mitchell, J., Wisniewski, S.R., Balasubramani, G.K., Trivedi, M.H., Rush, A.J., Gender differences in depression: findings from the STAR*D study. J. Affect. Disord. 87 (2005), 141–150.
39. Marriott, I., Huet-Hudson, Y.M., Sexual dimorphism in innate immune responses to infectious organisms. Immunol. Res. 34 (2006), 177–192.
40. Martin-de-Saavedra, M.D., Budni, J., Cunha, M.P., Gomez-Rangel, V., Lorrio, S., Del Barrio, L., Lastres-Becker, I., Parada, E., Tordera, R.M., Rodrigues, A.L., Cuadrado, A., Lopez, M.G., Nrf2 participates in depressive disorders through an anti-inflammatory mechanism. Psychoneuroendocrinology 38 (2013), 2010–2022.
41. Merali, Z., Brennan, K., Brau, P., Anisman, H., Dissociating anorexia and anhedonia elicited by interleukin-1beta: antidepressant and gender effects on responding for “free chow” and “earned” sucrose intake. Psychopharmacology 165 (2003), 413–418.
42. MohanKumar, S.M., MohanKumar, P.S., Quadri, S.K., Lipopolysaccharide-induced changes in monoamines in specific areas of the brain: blockade by interleukin-1 receptor antagonist. Brain Res. 824 (1999), 232–237.
43. MohanKumar, S.M., MohanKumar, P.S., Quadri, S.K., Effects of bacterial lipopolysaccharide on central monoamines and fever in the rat: involvement of the vagus. Neurosci. Lett. 284 (2000), 159–162.
44. Moieni, M., Irwin, M.R., Jevtic, I., Olmstead, R., Breen, E.C., Eisenberger, N.I., Sex differences in depressive and socioemotional responses to an inflammatory challenge: implications for sex differences in depression. Neuropsychopharmacology 40 (2015), 1709–1716.
45. Nollet, M., Le Guisquet, A.M., Belzung, C., Models of depression: unpredictable chronic mild stress in mice. Curr. Protoc. Pharmacol., 65, 2013 (Chapter 5, Unit 5).
46. O'Connor, J.C., Lawson, M.A., Andre, C., Moreau, M., Lestage, J., Castanon, N., Kelley, K.W., Dantzer, R., Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol. Psychiatry 14 (2009), 511–522.
47. Pitychoutis, P.M., Papadopoulou-Daifoti, Z., Of depression and immunity: does sex matter?. Int. J. Neuropsychopharmacol. 13 (2010), 675–689.
48. Pitychoutis, P.M., Nakamura, K., Tsonis, P.A., Papadopoulou-Daifoti, Z., Neurochemical and behavioral alterations in an inflammatory model of depression: sex differences exposed. Neuroscience 159 (2009), 1216–1232.
49. Pitychoutis, P.M., Pallis, E.G., Mikail, H.G., Papadopoulou-Daifoti, Z., Individual differences in novelty-seeking predict differential responses to chronic antidepressant treatment through sex- and phenotype-dependent neurochemical signatures. Behav. Brain Res. 223 (2011), 154–168.
50. Pitychoutis, P.M., Dalla, C., Sideris, A.C., Tsonis, P.A., Papadopoulou-Daifoti, Z., 5-HT(1A), 5-HT(2A), and 5-HT(2C) receptor mRNA modulation by antidepressant treatment in the chronic mild stress model of depression: sex differences exposed. Neuroscience 210 (2012), 152–167.
51. Spinedi, E., Salas, M., Chisari, A., Perone, M., Carino, M., Gaillard, R.C., Sex differences in the hypothalamo-pituitary-adrenal axis response to inflammatory and neuroendocrine stressors. Evidence for a pituitary defect in the autoimmune disease-susceptible female Lewis rat. Neuroendocrinology 60 (1994), 609–617.
52. Spinedi, E., Gaillard, R.C., Chisari, A., Sexual dimorphism of neuroendocrine-immune interactions. Front. Horm. Res. 29 (2002), 91–107.
53. Stratinaki, M., Varidaki, A., Mitsi, V., Ghose, S., Magida, J., Dias, C., Russo, S.J., Vialou, V., Caldarone, B.J., Tamminga, C.A., Nestler, E.J., Zachariou, V., Regulator of G protein signaling 4 [corrected] is a crucial modulator of antidepressant drug action in depression and neuropathic pain models. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 8254–8259.
54. Tikhonova, M.A., Kulikov, V.A., Kulikov, A.V., Effects of LPS and serotonergic drugs on hygienic behavior in mice. Pharmacol. Biochem. Behav. 98 (2011), 392–397.
55. Tonelli, L.H., Holmes, A., Postolache, T.T., Intranasal immune challenge induces sex-dependent depressive-like behavior and cytokine expression in the brain. Neuropsychopharmacology 33 (2008), 1038–1048.
56. Walker, A.K., Budac, D.P., Bisulco, S., Lee, A.W., Smith, R.A., Beenders, B., Kelley, K.W., Dantzer, R., NMDA receptor blockade by ketamine abrogates lipopolysaccharide-induced depressive-like behavior in C57BL/6J mice. Neuropsychopharmacology 38 (2013), 1609–1616.
57. WHO, Global burden of mental disorders and the need for a comprehensive, coordinated response from health and social sectors at the country level. http://apps.who.int/gb/ebwha/pdf_files/EB130/B130_9-en.pdf, 2011 Accessed June 15, 2015.
58. Yirmiya, R., Endotoxin produces a depressive-like episode in rats. Brain Res. 711 (1996), 163–174.