Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium

Physiology and Behavior

Volumn 89, Issue 3, 2006, Pages 350-357

  Lyte, Mark ^a,b   Li, Wang ^a   Opitz, Noel ^b,c   Gaykema, Ronald P A ^d   Goehler, Lisa E ^d  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b MINNEAPOLIS MEDICAL RESEARCH FOUNDATION   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Behavior; Citrobacter rodentium; Infection; Inflammatory bowel disease

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; PROTEIN C FOS; SODIUM CHLORIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; AVOIDANCE BEHAVIOR; BACTERIAL INFECTION; BEHAVIORAL SCIENCE; BLOOD SAMPLING; CITROBACTER RODENTIUM; COLON; COLON DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENTERITIS; EXCISION; EXPERIMENTAL INFECTION; HISTOLOGY; HISTOPATHOLOGY; HYPERPLASIA; IMMUNOASSAY; MALE; MEASUREMENT; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; RISK ASSESSMENT; SENSORY GANGLION; STATISTICAL SIGNIFICANCE; TISSUE SECTION; VAGUS NERVE;

EID: 33748947870     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2006.06.019     Document Type: Article

References (59)

1. Addolorato G., Stefanini G.F., Capristo E., Caputo F., Gasbarrini A., and Gasbarrini G. Anxiety and depression in adult untreated celiac subjects and in patients affected by inflammatory bowel disease: a personality "trait" or a reactive illness?. Hepatogastroenterology 43 (1996) 1513-1517
2. Anisman H., and Merali Z. Anhedonic and anxiogenic effects of cytokine exposure. Adv Exp Med Biol 461 (1999) 199-233
3. Bauhofer A., Schwarting R.K., Koster M., Schmitt A., Lorenz W., and Pawlak C.R. Sickness behavior of rats with abdominal sepsis can be improved by antibiotic and G-CSF prophylaxis in clinic modeling randomized trials. Inflamm Res 53 (2004) 697-705
4. Berntson G.G., Sarter M., and Cacioppo J.T. Ascending visceral regulation of cortical affective information processing. Eur J Neurosci 18 (2003) 2103-2109
5. Blanchard E.B., Scharff L., Schwarz S.P., Suls J.M., and Barlow D.H. The role of anxiety and depression in the irritable bowel syndrome. Behav Res Ther 28 (1990) 401-405
6. Bluthe R.M., Bristow A., Lestage J., Imbs C., and Dantzer R. Central injection of interleukin-13 potentiates LPS-induced sickness behavior in rats. NeuroReport 12 (2001) 3979-3983
7. Bluthe R.M., Dantzer R., and Kelley K.W. Effects of interleukin-1 receptor antagonist on the behavioral effects of lipopolysaccharide in rat. Brain Res 573 (1992) 318-320
8. Casati J., and Toner B.B. Psychosocial aspects of inflammatory bowel disease. Biomed Pharmacother 54 (2000) 388-393
9. Crane C., and Martin M. Social learning, affective state and passive coping in irritable bowel syndrome and inflammatory bowel disease. Gen Hosp Psychiatry 26 (2004) 50-58
10. Dahan S., Wiles S., La Ragione R.M., Best A., Woodward M.J., Stevens M.P., et al. EspJ is a prophage-carried type III effector protein of attaching and effacing pathogens that modulates infection dynamics. Infect Immun 73 (2005) 679-686
11. Dantzer R. Cytokine-induced sickness behavior: mechanisms and implications. Ann N Y Acad Sci 933 (2001) 222-234
12. Dantzer R. Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur J Pharmacol 500 (2004) 399-411
13. Drossman D.A. Irritable bowel syndrome. Gastroenterologist 2 (1994) 315-326
14. Dunlop S.P., Jenkins D., Neal K.R., and Spiller R.C. Relative importance of enterochromaffin cell hyperplasia, anxiety, and depression in postinfectious IBS. Gastroenterology 125 (2003) 1651-1659
15. Ek M., Kurosawa M., Lundeberg T., and Ericsson A. Activation of vagal afferents after intravenous injection of interleukin-1beta: role of endogenous prostaglandins. J Neurosci 18 (1998) 9471-9479
16. Fiore M., Moroni R., Alleva E., and Aloe L. Schistosoma mansoni: influence of infection on mouse behavior. Exp Parasitol 83 (1996) 46-54
17. Folks D.G. The interface of psychiatry and irritable bowel syndrome. Curr Psychiatry Rep 6 (2004) 210-215
18. Gibertini M. Cytokines and cognitive behavior. Neuroimmunomodulation 5 (1998) 160-165
19. Gibertini M., Newton C., Friedman H., and Klein T.W. Spatial learning impairment in mice infected with Legionella pneumophila or administered exogenous interleukin-1-beta. Brain Behav Immun 9 (1995) 113-128
20. Goehler L.E., Gaykema R.P., Hammack S.E., Maier S.F., and Watkins L.R. Interleukin-1 induces c-Fos immunoreactivity in primary afferent neurons of the vagus nerve. Brain Res 804 (1998) 306-310
21. Goehler L.E., Gaykema R.P., Opitz N., Reddaway R., Badr N., and Lyte M. Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni. Brain Behav Immun 19 (2005) 334-344
22. Harro J., Pold M., and Vasar E. Anxiogenic-like action of caerulein, a CCK-8 receptor agonist, in the mouse: influence of acute and subchronic diazepam treatment. Naunyn Schmiedebergs Arch Pharmacol 341 (1990) 62-67
23. Hermann G.E., Holmes G.M., and Rogers R.C. TNF(alpha) modulation of visceral and spinal sensory processing. Curr Pharm Des 11 (2005) 1391-1409
24. Higgins L.M., Frankel G., Connerton I., Goncalves N.S., Dougan G., and MacDonald T.T. Role of bacterial intimin in colonic hyperplasia and inflammation. Science 285 (1999) 588-591
25. 1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect Immun 67 (1999) 3031-3039
26. Hotchin J., and Seegal R. Alterations in behavior resulting from persistent lymphocytic choriomeningitis virus infection. Birth Defects Orig Artic Ser 14 (1978) 171-178
27. Husain A., and Triadafilopoulos G. Communicating with patients with inflammatory bowel disease. Inflamm Bowel Dis 10 (2004) 444-450 [discussion 451]
28. Iimura M., Gallo R.L., Hase K., Miyamoto Y., Eckmann L., and Kagnoff M.F. Cathelicidin mediates innate intestinal defense against colonization with epithelial adherent bacterial pathogens. J Immunol 174 (2005) 4901-4907
29. Irvine E.J. Review article: patients' fears and unmet needs in inflammatory bowel disease. Aliment Pharmacol Ther 20 Suppl 4 (2004) 54-59
30. Johnson R.W., Curtis S.E., Dantzer R., Bahr J.M., and Kelley KW. Sickness behavior in birds caused by peripheral or central injection of endotoxin. Physiol Behav 53 (1993) 343-348
31. Kelley K.W., Bluthe R.M., Dantzer R., Zhou J.H., Shen W.H., Johnson R.W., et al. Cytokine-induced sickness behavior. Brain Behav Immun 17 Suppl 1 (2003) S112-S118
32. Klapproth J.M., Sasaki M., Sherman M., Babbin B., Donnenberg M.S., Fernandes P.J., et al. Citrobacter rodentium lifA/efa1 is essential for colonic colonization and crypt cell hyperplasia in vivo. Infect Immun 73 (2005) 1441-1451
33. Konsman J.P., Parnet P., and Dantzer R. Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci 25 (2002) 154-159
34. Kusnecov A.W., and Goldfarb Y. Neural and behavioral responses to systemic immunologic stimuli: a consideration of bacterial T cell superantigens. Curr Pharm Des 11 (2005) 1039-1046
35. Langhans W. Bacterial products and the control of ingestive behavior: clinical implications. Nutrition 12 (1996) 303-315
36. Linthorst A.C., Flachskamm C., Muller-Preuss P., Holsboer F., and Reul J.M. Effect of bacterial endotoxin and interleukin-1 beta on hippocampal serotonergic neurotransmission, behavioral activity, and free corticosterone levels: an in vivo microdialysis study. J Neurosci 15 (1995) 2920-2934
37. Luperchio S.A., Newman J.V., Dangler C.A., Schrenzel M.D., Brenner D.J., Steigerwalt A.G., et al. Citrobacter rodentium, the causative agent of transmissible murine colonic hyperplasia, exhibits clonality: synonymy of C. rodentium and mouse-pathogenic Escherichia coli. J Clin Microbiol 38 (2000) 4343-4350
38. Luperchio S.A., and Schauer D.B. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect 3 (2001) 333-340
39. Lydiard R.B. Irritable bowel syndrome, anxiety, and depression: what are the links?. J Clin Psychiatry 62 Suppl 8 (2001) 38-45 [discussion 46-37]
40. Lyte M., Arulanandam B.P., and Frank C.D. Production of Shiga-like toxins by Escherichia coli O157:H7 can be influenced by the neuroendocrine hormone norepinephrine. J Lab Clin Med 128 (1996) 392-398
41. Lyte M., Erickson A.K., Arulanandam B.P., Frank C.D., Crawford M.A., and Francis D.H. Norepinephrine-induced expression of the K99 pilus adhesin of enterotoxigenic Escherichia coli. Biochem Biophys Res Commun 232 (1997) 682-686
42. Lyte M., Varcoe J.J., and Bailey M.T. Anxiogenic effect of subclinical bacterial infection in mice in the absence of overt immune activation. Physiol Behav 65 (1998) 63-68
43. Maaser C., Housley M.P., Iimura M., Smith J.R., Vallance B.A., Finlay B.B., et al. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect Immun 72 (2004) 3315-3324
44. MacDonald T.T., Frankel G., Dougan G., Goncalves N.S., and Simmons C. Host defences to Citrobacter rodentium. Int J Med Microbiol 293 (2003) 87-93
45. Mahida Y.R., and Rolfe V.E. Host-bacterial interactions in inflammatory bowel disease. Clin Sci (Lond) 107 (2004) 331-341
46. + currents involves activation of both EP2 and EP4 receptors in neonatal rat nodose ganglion neurones. Br J Pharmacol 145 (2005) 503-513
47. Mayer E.A., Naliboff B.D., Chang L., and Coutinho S.V. Stress and irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 280 (2001) G519-G524
48. Miller V., Hopkins L., and Whorwell P.J. Suicidal ideation in patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 2 (2004) 1064-1068
49. Mundy R., Petrovska L., Smollett K., Simpson N., Wilson R.K., Yu J., et al. Identification of a novel Citrobacter rodentium type III secreted protein, EspI, and roles of this and other secreted proteins in infection. Infect Immun 72 (2004) 2288-2302
50. Nakamura K., Kaneko T., Yamashita Y., Hasegawa H., Katoh H., and Negishi M. Immunohistochemical localization of prostaglandin EP3 receptor in the rat nervous system. J Comp Neurol 421 (2000) 543-569
51. Nataro J.P., and Kaper J.B. Diarrheagenic Escherichia coli. Clin Microbiol Rev 11 (1998) 142-201
52. Porcelli P., Leoci C., and Guerra V. A prospective study of the relationship between disease activity and psychologic distress in patients with inflammatory bowel disease. Scand J Gastroenterol 31 (1996) 792-796
53. Reichenberg A., Yirmiya R., Schuld A., Kraus T., Haack M., Morag A., et al. Cytokine-associated emotional and cognitive disturbances in humans. Arch Gen Psychiatry 58 (2001) 445-452
54. Sperandio V., Torres A.G., Jarvis B., Nataro J.P., and Kaper J.B. Bacteria-host communication: the language of hormones. Proc Natl Acad Sci U S A 100 (2003) 8951-8956
55. Sykes M.A., Blanchard E.B., Lackner J., Keefer L., and Krasner S. Psychopathology in irritable bowel syndrome: support for a psychophysiological model. J Behav Med 26 (2003) 361-372
56. Vallance B.A., Deng W., De Grado M., Chan C., Jacobson K., and Finlay B.B. Modulation of inducible nitric oxide synthase expression by the attaching and effacing bacterial pathogen Citrobacter rodentium in infected mice. Infect Immun 70 (2002) 6424-6435
57. Walker E.A., Gelfand M.D., Gelfand A.N., Creed F., and Katon W.J. The relationship of current psychiatric disorder to functional disability and distress in patients with inflammatory bowel disease. Gen Hosp Psychiatry 18 (1996) 220-229
58. Watkins L.R., Maier S.F., and Goehler L.E. Cytokine-to-brain communication: a review and analysis of alternative mechanisms. Life Sci 57 (1995) 1011-1026
59. Wiles S., Clare S., Harker J., Huett A., Young D., Dougan G., et al. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol 6 (2004) 963-972