Skip to main content
Log in

Effect of Bacterial Chemotactic Peptides on Intestinal Inflammation in Animal Models of Acute and Chronic “Relapsed” Colitis

  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

It is known that bacterial chemotactic peptides such as formyl-methionyl-leucyl-phenylalanine (fMLP) exacerbate colitis during the acute phase, but the precise role of fMLP during chronic “relapse” is unknown. In this study we examined the effect of bacterial peptides in animal models of acute and chronic “relapsed” colitis. Different parameters were evaluated, such as tissue damage, myeloperoxidase activity, and mucosal function. In acute trinitrobenezene sulfonic acid colitis, fMLP had significant adverse effects on mucosal function and worsened several parameters. In contrast, in chronic “relapsed” colitis the ability of fMLP to exacerbate the inflammation was dependent on whether it was confined to the lumen of the colon. Bacterial peptides such as fMLP appear to play a different role in the acute phase of inflammation compared with the chronic phase, depending on the integrity of the mucosal barrier.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Munkholm P, Langholz E, Nielsen OH, Kreiner S, Binder V: Incidence and prevalence of Crohn’s disease in the county of Copenhagen 1962–87: a sixfold increase in incidence. Scand J Gastroenterol 27:609–614, 1992

    PubMed  Google Scholar 

  2. Schultz M, Sartor RB: Probiotics and inflammatory bowel diseases. Am J Gastroenterol 95 (Suppl):S19–S21, 2000

    Article  PubMed  Google Scholar 

  3. Warren JR, Marshall BJ: Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1273–1275, 1983

  4. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening-Baucke V, Ortner M, Weber J, Hoffman U, Schreiber S, Dietel M, Lochs H: Mucosal flora in inflammatory bowel disease. Gastroenterology 122:44–54, 2002

    PubMed  Google Scholar 

  5. Taurog JD, Richardson JA, Croft JT, Simmons WA, Zhou M, Fernandez-Sueiro JL, Balish E, Hammer RE: The germfree state prevents development of gut and joint inflammatory disease in HLA–B27 transgenic rats. J Exp Med 180(6):2359–2364, 1994

    Article  PubMed  Google Scholar 

  6. Macpherson A, Khoo UY, Forgacs I, Philpott–Howard J, Bjarnason I: Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria. Gut 38(3):365–375, 1996

    PubMed  Google Scholar 

  7. Schultsz C, Van Den Berg F, Ten Kate F, Tytgat GN, Dankert J: The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology 117:1089–1097, 1999

    PubMed  Google Scholar 

  8. Elson CO, Sartor RB, Tennyson GS, Riddell RH: Experimental models of inflammatory bowel disease. Gastroenterology 109:1344–1367, 1995

    PubMed  Google Scholar 

  9. Rath HC, Schultz M, Freitag R, Dieleman LA, Li F, Linde HJ, Scholmerich J, Sartor RB: Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats. Infect Immun 69(4):2277–2285, 2001

    Article  PubMed  Google Scholar 

  10. Hernández GA, Alvarez A, Appleyard CB: Quantification of bacterial load in two different models of colitis. FASEB J 15(5):A821, 2001

    Google Scholar 

  11. Hernández GA, Appleyard CB: Bacterial load in animal models of acute and chronic “reactivated” colitis. Digestion 67(3):161–169, 2003

    Article  PubMed  Google Scholar 

  12. Merlin D, Si–Tahar M, Sitaraman SV, Eastburn K, Williams I, Liu X, Hediger MA, Madara JL: Colonic epithelial hPepT1 expression occurs in inflammatory bowel disease: Transport of bacterial peptides influences expression of MHC class 1 molecules. Gastroenterology 120(7):1666–1679, 2001

    PubMed  Google Scholar 

  13. Keshavarzian A, Haydek JM, Jacyno M, Holmes EW, Hardford F: Modulatory effects of the colonic milieu on neutrophil oxidative burst: A possible pathogenic mechanism of ulcerative colitis. J Lab Clin Med 130(2):216–225, 1997

    Article  PubMed  Google Scholar 

  14. Garcia–Lafuente A, Antolin M, Guarner F, Vilaseca J, Malagelada JR: Bacterial peptides enhance inflammatory activity in a rat model of colitis. Digestion 57(5):368–373, 1996

    PubMed  Google Scholar 

  15. Schiffmann E, Showell HV, Corcoran BA, Ward PA, Smith E, Becker EL: The isolation and partial characterization of neutrophil chemotactic factors from Escherichia coli. J Immunol 114(6):1831–1837, 1975

    PubMed  Google Scholar 

  16. Marasco WA, Phan SH, Krutzsch H: Purification and identification of formyl-methionyl-leucyl-phenylalanine as the major peptide neutrophil chemotactic factor produced by Escherichia coli. J Biol Chem 259:5430–5439, 1984

    PubMed  Google Scholar 

  17. Broom MF, Sherriff RM, Ferry DM, Chadwick VS: Formyl-methiony-leucyl-phenylalanine and the SOS operon in Escherichia coli: A model of host–bacterial interactions. Biochem J 291(3):895–900, 1996

    Google Scholar 

  18. Mackay DM: Intestinal inflammation and the gut microflora. Can J Gastroenterol 13:509–516, 1999

    PubMed  Google Scholar 

  19. Morris GP, Beck PL Herridge MS, Depew WT, Szewczuk MR, Wallace JL: Hapten induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96:795–803, 1989

    PubMed  Google Scholar 

  20. Appleyard CB, Wallace JL: Reactivation of hapten–induced colitis and its prevention by anti–inflammatory drugs. Am J Physiol 269:G119–G125, 1995

    PubMed  Google Scholar 

  21. Percy WH: The use of in vitro techniques for the study of gastrointestinal motility. In: Gaginella TS (ed) Handbook of methods in gastrointestinal pharmacology. Boca Raton, FL CRC Press, 1995, pp 189–223

    Google Scholar 

  22. Percy WH, Burton MB, Rose K, Donovan V, Burakoff R: In vitro changes in the properties of rabbit colonic muscularis mucosae in colitis. Gastroenterology 104:369–376, 1993

    PubMed  Google Scholar 

  23. Ledesma de Paolo MI, Celener Gravelle P, De Paula JA, Panzita MT, Bandi JC, Bustos Fernandez L: Stimulation of inflammatory mediators secretion by chemotactic peptides in rat colitis model. Acta Gastroenterol Latinoamer 26:23–30, 1996

    Google Scholar 

  24. Chester JF, Ross JS, Malt RA, Weitzman SA: Acute colitis produced by chemotactic peptides in rats and mice. Am J Pathol 121:284–290, 1985

    PubMed  Google Scholar 

  25. Anton P, O’Connell J, O’Connell D, Whitaker L, O’ Sullivan GC, Collins JK, Shanahan F: Mucosal subepithelial binding sites for the bacterial chemotactic peptide, formyl-methionyl-leucyl-phenylalanine (FMLP). Gut 42:374–379, 1998

    PubMed  Google Scholar 

  26. Nast CC, LeDuc LE: Chemotactic peptides. Mechanisms, functions and possible role in inflammatory bowel disease. Dig Dis Sci 33:50S–57S, 1988

    Article  PubMed  Google Scholar 

  27. Pacha J, Popp M, Capek K: Effects of deoxycorticosterone acetate on the electrical properties of rat large intestine: segmented differences. Physiol Bohemoslov 36(2):141–147, 1987

    PubMed  Google Scholar 

  28. von Engelhardt W, Rosel E, Rechkemmer G: Comparative views of electrophysiological parameters of large intestinal segments in pig, sheep, pony, guinea pig and rat. Dtsch Tierarztl Wochenschr 102(4):157–159, 1995

    PubMed  Google Scholar 

  29. Lobo AJ, Burke DA, Sobala GM, Axon AT: Oral tobramycin in ulcerative colitis: effect on maintenance of remission. Aliment Pharmacol Ther 7:155–158, 1993

    PubMed  Google Scholar 

  30. Mantzaris GJ, Archavlis E, Christoforidis P, Kourtessas D, Amberiadis P, Florakis N, Petraki K, Spiliadi C, Triantafyllou G: A prospective randomized controlled trial of oral ciprofloxacin in acute ulcerative colitis. Am J Gastroenterol 92:454–456, 1997

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Caroline B. Appleyard PhD.

Additional information

The experiments reported herein were performed in accordance with the principles described in the “Guide for the Care and Use of Laboratory Animals,” Publication No. DHHS (NIH) 86-23.

This work was supported by National Institutes of Health grants including National Research Service Award F31DK60245 from the NIDDK (G.A.H.), S06-GM08239 (C.B.A.), and G12-RR03050 (C.B.A.).

Rights and permissions

Reprints and permissions

About this article

Cite this article

HernÁndez, G.A., ValentÍn, M.R. & Appleyard, C.B. Effect of Bacterial Chemotactic Peptides on Intestinal Inflammation in Animal Models of Acute and Chronic “Relapsed” Colitis. Dig Dis Sci 50, 1444–1453 (2005). https://doi.org/10.1007/s10620-005-2859-3

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-005-2859-3

Key Words

Navigation