Sleep Medicine
Volume 10, Issue 6 , Pages 597-603 , June 2009

Sleep deprivation worsens inflammation and delays recovery in a mouse model of colitis

  • Yueming Tang

      Affiliations

    • Department of Internal Medicine, Division of Digestive Disease and Nutrition, Rush University Medical Center, 1725 W. Harrison, Suite 206, Chicago, IL 60612, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 312 942 8927; fax: +1 312 942 5664.
    • These authors contributed equally to this work.
  • ,
  • Fabian Preuss

      Affiliations

    • Department of Internal Medicine, Division of Digestive Disease and Nutrition, Rush University Medical Center, 1725 W. Harrison, Suite 206, Chicago, IL 60612, USA
    • Center for Sleep & Circadian Biology, Department of Neurobiology & Physiology, Northwestern University, Evanston, IL 60208, USA
    • These authors contributed equally to this work.
  • ,
  • Fred W. Turek

      Affiliations

    • Center for Sleep & Circadian Biology, Department of Neurobiology & Physiology, Northwestern University, Evanston, IL 60208, USA
  • ,
  • Shriram Jakate

      Affiliations

    • Department of Pathology, Rush University Medical Center, Chicago, IL 60612, USA
  • ,
  • Ali Keshavarzian

      Affiliations

    • Department of Internal Medicine, Division of Digestive Disease and Nutrition, Rush University Medical Center, 1725 W. Harrison, Suite 206, Chicago, IL 60612, USA
    • Department of Pharmacology and Molecular Biophysics & Physiology, Rush University Medical Center, Chicago, IL 60612, USA

Received 15 August 2008 ,Revised 7 December 2008 ,Accepted 11 December 2008.

References 

  1. Keighley MR, Stockbrugger RW. Inflammatory bowel disease. Aliment Pharmacol Ther. 2003;18(Suppl. 3):66–70
  2. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347:417–429
  3. Hart A, Kamm MA. Review article: mechanisms of initiation and perpetuation of gut inflammation by stress. Aliment Pharmacol Ther. 2002;16:2017–2028
  4. Mawdsley JE, Rampton DS. Psychological stress in IBD: new insights into pathogenic and therapeutic implications. Gut. 2005;54:1481–1491
  5. Mawdsley JE, Rampton DS. The role of psychological stress in inflammatory bowel disease. Neuroimmunomodulation. 2006;13:327–336
  6. Mawdsley JE, Macey MG, Feakins RM, Langmead L, Rampton DS. The effect of acute psychologic stress on systemic and rectal mucosal measures of inflammation in ulcerative colitis. Gastroenterology. 2006;131:410–419
  7. Ranjbaran Z, Keefer L, Farhadi A, Stepanski E, Sedghi S, Keshavarzian A. Impact of sleep disturbances in inflammatory bowel disease. J Gastroenterol Hepatol. 2007;22:1748–1753
  8. Ranjbaran Z, Keefer L, Stepanski E, Farhadi A, Keshavarzian A. The relevance of sleep abnormalities to chronic inflammatory conditions. Inflamm Res. 2007;56:51–57
  9. Keefer L, Stepanski EJ, Ranjbaran Z, Benson LM, Keshavarzian A. An initial report of sleep disturbance in inactive inflammatory bowel disease. J Clin Sleep Med. 2006;2:409–416
  10. North CS, Alpers DH, Helzer JE, Spitznagel EL, Clouse RE. Do life events or depression exacerbate inflammatory bowel disease? A prospective study. Ann Intern Med. 1991;114:381–386
  11. Levenstein S, Prantera C, Varvo V, Scribano ML, Andreoli A, Luzi C, et al. Stress and exacerbation in ulcerative colitis: a prospective study of patients enrolled in remission. Am J Gastroenterol. 2000;95:1213–1220
  12. Zisapel N. Sleep and sleep disturbances: biological basis and clinical implications. Cell Mol Life Sci. 2007;64:1174–1186
  13. Bryant PA, Trinder J, Curtis N. Sick and tired: does sleep have a vital role in the immune system?. Nat Rev Immunol. 2004;4:457–467
  14. Orr WC, Chen CL. Sleep and the gastrointestinal tract. Neurol Clin. 2005;23:1007–1024
  15. Zimmerman J. Extraintestinal symptoms in irritable bowel syndrome and inflammatory bowel diseases: nature, severity, and relationship to gastrointestinal symptoms. Dig Dis Sci. 2003;48:743–749
  16. Kim Y, Laposky AD, Bergmann BM, Turek FW. Repeated sleep restriction in rats leads to homeostatic and allostatic responses during recovery sleep. Proc Natl Acad Sci USA. 2007;104:10697–10702
  17. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98:694–702
  18. Abdelbaqi M, Chidlow JH, Matthews KM, Pavlick KP, Barlow SC, Linscott AJ, et al. Regulation of dextran sodium sulfate induced colitis by leukocyte beta 2 integrins. Lab Invest. 2006;86:380–390
  19. Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131:117–129
  20. Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE, Balish E, et al. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Invest. 1996;98:945–953
  21. Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol. 1982;78:206–209
  22. Strober W, Fuss IJ, Blumberg RS. The immunology of mucosal models of inflammation. Annu Rev Immunol. 2002;20:495–549
  23. Pizarro TT, Arseneau KO, Bamias G, Cominelli F. Mouse models for the study of Crohn’s disease. Trends Mol Med. 2003;9:218–222
  24. Elson CO, Sartor RB, Tennyson GS, Riddell RH. Experimental models of inflammatory bowel disease. Gastroenterology. 1995;109:1344–1367
  25. Costa F, Mumolo MG, Ceccarelli L, Bellini M, Romano MR, Sterpi C. Calprotectin is a stronger predictive marker of relapse in ulcerative colitis than in Crohn’s disease. Gut. 2005;54:364–368
  26. Bernstein CN, Walker JR, Graff LA. On studying the connection between stress and IBD. Am J Gastroenterol. 2006;101:782–785
  27. Sperber AD, Tarasiuk A. Disrupted sleep in patients with IBS–a wake-up call for further research?. Nat Clin Pract Gastroenterol Hepatol. 2007;4:412–413
  28. van Dieren JM, Kuipers EJ, Samsom JN, Nieuwenhuis EE, van der Woude CJ. Revisiting the immunomodulators tacrolimus, methotrexate, and mycophenolate mofetil: their mechanisms of action and role in the treatment of IBD. Inflamm Bowel Dis. 2006;12:311–327
  29. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427–434
  30. Vgontzas AN, Bixler EO, Lin HM, Prolo P, Trakada G, Chrousos GP. IL-6 and its circadian secretion in humans. Neuroimmunomodulation. 2005;12:131–140
  31. Opp MR. Cytokines and sleep. Sleep Med Rev. 2005;9:355–364
  32. Uthgenannt D, Schoolmann D, Pietrowsky R, Fehm HL, Born J. Effects of sleep on the production of cytokines in humans. Psychosom Med. 1995;57:97–104
  33. Irwin M, Clark C, Kennedy B, Christian Gillin J, Ziegler M. Nocturnal catecholamines and immune function in insomniacs, depressed patients, and control subjects. Brain Behav Immun. 2003;17:365–372
  34. Savard J, Laroche L, Simard S, Ivers H, Morin CM, et al. Chronic insomnia and immune functioning. Psychosom Med. 2003;65:211–221
  35. Sakami S, Ishikawa T, Kawakami N, Haratani T, Fukui A, Kobayashi F, et al. Coemergence of insomnia and a shift in the Th1/Th2 balance toward Th2 dominance. Neuroimmunomodulation. 2002;10:337–343

PII: S1389-9457(09)00052-5

doi: 10.1016/j.sleep.2008.12.009

Sleep Medicine
Volume 10, Issue 6 , Pages 597-603 , June 2009