Neuromodulation of experimental Shigella infection reduces damage to the gut mucosa

Microbes and Infection

Volumn 6, Issue 3, 2004, Pages 256-264

  Svensson, Lena ^a   Bergquist, Jonas ^b   Wennerås, Christine ^a  

^a SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Intestine; Neuromodulation; Neuropeptides; Rabbits; Shigella

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; GALANIN; MOTILIN; NEUROPEPTIDE; NEUROTENSIN; PEPTIDE YY; SODIUM CHLORIDE; SOMATOSTATIN; SUBSTANCE P; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FEMALE; GASTROINTESTINAL TRACT; INFLAMMATION; INTESTINE BIOPSY; INTESTINE MUCOSA; LEUKOCYTE; MALE; NERVE ENDING; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RABBIT; RADIOIMMUNOASSAY; SECRETION; SHIGELLA FLEXNERI; SHIGELLOSIS;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; DYSENTERY, BACILLARY; GALANIN; HEXAMETHONIUM; INFLAMMATION; INTESTINAL MUCOSA; INTESTINE, SMALL; MOTILIN; NEUROPEPTIDES; NEUROTENSIN; NICOTINIC ANTAGONISTS; PEPTIDE YY; RABBITS; SHIGELLA FLEXNERI; SOMATOSTATIN; SUBSTANCE P; VASOACTIVE INTESTINAL PEPTIDE;

BACTERIA (MICROORGANISMS); ORYCTOLAGUS CUNICULUS; SHIGELLA; SHIGELLA FLEXNERI;

EID: 1542268336     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micinf.2003.12.003     Document Type: Article

References (51)

1. Wennerås C., Sansonetti P.J. Cary J.W., Linz J.E., Bhatnagar D. Microbial Foodborne Diseases; Mechanisms of Pathogenesis and Toxin Synthesis. 2000;51-85 Technomic Publishing Company, Inc, Lancaster.
2. Kotloff K.L., Winickoff J.P., Ivanoff B., Clemens J.D., Swerdlow D.L., Sansonetti P.J., Adak G.K., Levine M.M. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull. World Health Organ. 77:1999;651-666.
3. Lima A.A., Lima N.L., Pinho M.C., Barros E.A. Jr, Teixeira M.J., Martins M.C., Guerrant R.L. High frequency of strains multiply resistant to ampicillin, trimethoprim-sulfamethoxazole, streptomycin, chloramphenicol, and tetracycline isolated from patients with shigellosis in northeastern Brazil during the period 1988-1993. Antimicrob. Agents Chemother. 39:1995;256-259.
4. Sack R.B., Rahman M., Yunus M., Khan E.H. Antimicrobial resistance in organisms causing diarrheal disease. Clin. Infect. Dis. 24:(Suppl. 1):1997;S102-S105.
5. Butler T., Islam M.R., Azad M.A., Jones P.K. Risk factors for development of hemolytic uremic syndrome during shigellosis. J. Pediatr. 110:1987;894-897.
6. Mathan M.M., Mathan V.I. Morphology of rectal mucosa of patients with shigellosis. Rev. Infect. Dis. 13:(Suppl. 4):1991;S314-S318.
7. Mathan M.M., Mathan V.I. Ultrastructural pathology of the rectal mucosa in Shigella dysentery. Am. J. Pathol. 123:1986;25-38.
8. Raqib R., Lindberg A.A., Wretlind B., Bardhan P.K., Andersson U., Andersson J. Persistence of local cytokine production in shigellosis in acute and convalescent stages. Infect. Immun. 63:1995;289-296.
9. Perdomo J.J., Gounon P., Sansonetti P.J. Polymorphonuclear leukocyte transmigration promotes invasion of colonic epithelial monolayer by Shigella flexneri. J. Clin. Invest. 93:1994;633-643.
10. Perdomo O.J., Cavaillon J.M., Huerre M., Ohayon H., Gounon P., Sansonetti P.J. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J. Exp. Med. 180:1994;1307-1319.
11. Sansonetti P.J., Arondel J., Cavaillon J.M., Huerre M. Role of interleukin-1 in the pathogenesis of experimental shigellosis. J. Clin. Invest. 96:1995;884-892.
12. D'Hauteville H., Khan S., Maskell D.J., Kussak A., Weintraub A., Mathison J., Ulevitch R.J., Wuscher N., Parsot C., Sansonetti P.J. Two msbB genes encoding maximal acylation of lipid A are required for invasive Shigella flexneri to mediate inflammatory rupture and destruction of the intestinal epithelium. J. Immunol. 168:2002;5240-5251.
13. Wenneras C., Ave P., Huerre M., Arondel J., Ulevitch R.J., Mathison J.C., Sansonetti P. Blockade of CD14 increases Shigella-mediated invasion and tissue destruction. J. Immunol. 164:2000;3214-3221.
14. J.B. Furness, M. Costa, in: J.B. Furness, M. Costa (Eds.), The Enteric Nervous System, Bell and Bain Ltd., Glasgow, 1987, pp. 1-5.
15. Cutz E., Chan W., Track N.S., Goth A., Said S.I. Release of vasoactive intestinal polypeptide in mast cells by histamine liberators. Nature. 275:1978;661-662.
16. O'Dorisio M.S., O'Dorisio T. M., Cataland S., Balcerzak S.P. Vasoactive intestinal polypeptide as a biochemical marker for polymorphonuclear leukocytes. J. Lab. Clin. Med. 96:1980;666-672.
17. Weinstock J.V., Blum A., Walder J., Walder R. Eosinophils from granulomas in murine Schistosomiasis mansoni produce substance P. J. Immunol. 141:1988;961-966.
18. Pascual D.W., Bost K.L. Substance P production by P388D1 macrophages: a possible autocrine function for this neuropeptide. Immunology. 71:1990;52-56.
19. Bergquist J., Tarkowski A., Ekman R., Ewing A. Discovery of endogenous catecholamines in lymphocytes and evidence for catecholamine regulation of lymphocyte function via an autocrine loop. Proc. Natl. Acad. Sci. USA. 91:1994;12912-12916.
20. Arizono N., Matsuda S., Hattori T., Kojima Y., Maeda T., Galli S.J. Anatomical variation in mast cell nerve associations in the rat small intestine, heart, lung, and skin. Similarities of distances between neural processes and mast cells, eosinophils, or plasma cells in the jejunal lamina propria. Lab. Invest. 62:1990;626-634.
21. McKay D.M., Bienenstock J. The interaction between mast cells and nerves in the gastrointestinal tract. Immunol. Today. 15:1994;533-538.
22. Perdue M.H., McKay D.M. Integrative immunophysiology in the intestinal mucosa. Am. J. Physiol. 267:1994;G151-G165.
23. Cassuto J., Fahrenkrug J., Jodal M., Tuttle R., Lundgren O. Release of vasoactive intestinal polypeptide from the cat small intestine exposed to cholera toxin. Gut. 22:1981;958-963.
24. Castagliuolo I., Keates A.C., Qiu B., Kelly C.P., Nikulasson S., Leeman S.E., Pothoulakis C. Increased substance P responses in dorsal root ganglia and intestinal macrophages during Clostridium difficile toxin A enteritis in rats. Proc. Natl. Acad. Sci. USA. 94:1997;4788-4793.
25. Brunsson I. Enteric nerves mediate the fluid secretory response due to Salmonella typhimurium R5 infection in the rat small intestine. Acta Physiol. Scand. 131:1987;609-617.
26. Sansonetti P.J., Kopecko D.J., Formal S.B. Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect. Immun. 35:1982;852-860.
27. Snider R.M., Constantine J.W., Lowe J.A. III, Longo K.P., Lebel W.S., Woody H.A., Drozda S.E., Desai M.C., Vinick F.J., Spencer R.W., et al. A potent nonpeptide antagonist of the substance P (NK1) receptor. Science. 251:1991;435-437.
28. Lange S. A rat model for an in vivo assay of enterotoxic diarrhea. FEMS Micobiol. Lett. 15:1982;239-242.
29. Hunter W.M., Greenwood F.C. Preparation of Iodine-131 labelled human growth hormone of high specific activity. Nature. 194:1962;595-596.
30. Sun Y., Fihn B.M., Jodal M., Sjovall H. Effects of neural blocking agents on motor activity and secretion in the proximal and distal rat colon: evidence of marked segmental differences in nicotinic receptor activity. Scand. J. Gastroenterol. 35:2000;380-388.
31. Berggreen P., Grondahl M.L., Ersboll A.K., Maltbaek J.S., Thorboll J.E., Skadhauge E., Hansen M.B. Regional differences in neurogenic signal transduction pathway of cholera toxin-induced fluid, electrolyte and serotonin accumulation in the porcine jejunum. Pharmacol. Toxicol. 86:2000;270-275.
32. Sakai T., Satoh M., Koyama H., Iesaki K., Umahara M., Fujikura K., Itoh Z. Localization of motilin-immunopositive cells in the rat intestine by light microscopic immunocytochemistry. Peptides. 15:1994;987-991.
33. Satoh M., Sakai T., Koyama H., Shiba Y., Itoh Z. Immunocytochemical localization of motilin-containing cells in the rabbit gastrointestinal tract. Peptides. 16:1995;883-887.
34. Castagliuolo I., Riegler M., Pasha A., Nikulasson S., Lu B., Gerard C., Gerard N.P., Pothoulakis C. Neurokinin-1 (NK-1) receptor is required in Clostridium difficile-induced enteritis. J. Clin. Invest. 101:1998;1547-1550.
35. Aliakbari J., Sreedharan S.P., Turck C.W., Goetzl E.J. Selective localization of vasoactive intestinal peptide and substance P in human eosinophils. Biochem. Biophys. Res. Commun. 148:1987;1440-1445.
36. Metwali A., Blum A.M., Ferraris L., Klein J.S., Fiocchi C., Weinstock J.V. Eosinophils within the healthy or inflamed human intestine produce substance P and vasoactive intestinal peptide. J. Neuroimmunol. 52:1994;69-78.
37. Bernstein C.N., Robert M.E., Eysselein V.E. Rectal substance P concentrations are increased in ulcerative colitis but not in Crohn's disease. Am. J. Gastroenterol. 88:1993;908-913.
38. Goldin E., Karmeli F., Selinger Z., Rachmilewitz D. Colonic substance P levels are increased in ulcerative colitis and decreased in chronic severe constipation. Dig. Dis. Sci. 34:1989;754-757.
39. Sharkey K.A. Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Ann. N.Y. Acad. Sci. 664:1992;425-442.
40. Kowalska K., Carr D.B., Lipkowski A.W. Direct antimicrobial properties of substance P. Life Sci. 71:2002;747-750.
41. Ottaway C.A. In vitro alteration of receptors for vasoactive intestinal peptide changes the in vivo localization of mouse T cells. J. Exp. Med. 160:1984;1054-1069.
42. Wiik P. Vasoactive intestinal peptide inhibits the respiratory burst in human monocytes by a cyclic AMP-mediated mechanism. Regul. Pept. 25:1989;187-197.
43. Lundberg J.M., Tatemoto K., Terenius L., Hellstrom P.M., Mutt V., Hokfelt T., Hamberger B. Localization of peptide YY (PYY) in gastrointestinal endocrine cells and effects on intestinal blood flow and motility. Proc. Natl. Acad. Sci. USA. 79:1982;4471-4475.
44. Chariot J., Tsocas A., Souli A., Presset O., Roze C. Neural mechanism of the antisecretory effect of peptide YY in the rat colon in vivo. Peptides. 21:2000;59-63.
45. De la Fuente M., Bernaez I., Del Rio M., Hernanz A. Stimulation of murine peritoneal macrophage functions by neuropeptide Y and peptide YY. Involvement of protein kinase C. Immunology. 80:1993;259-265.
46. Vouldoukis I., Shai Y., Nicolas P., Mor A. Broad spectrum antibiotic activity of the skin-PYY. FEBS Lett. 380:1996;237-240.
47. El-Salhy M., Suhr O., Danielsson A. Peptide YY in gastrointestinal disorders. Peptides. 23:2002;397-402.
48. Lundgren O., Peregrin A.T., Persson K., Kordasti S., Uhnoo I., Svensson L. Role of the enteric nervous system in the fluid and electrolyte secretion of rotavirus diarrhea. Science. 287:2000;491-495.
49. Cassuto J., Jodal M., Lundgren O. The effect of nicotinic and muscarinic receptor blockade on cholera toxin induced intestinal secretion in rats and cats. Acta Physiol. Scand. 114:1982;573-577.
50. Sorensson J., Jodal M., Lundgren O. Involvement of nerves and calcium channels in the intestinal response to Clostridium difficile toxin A: an experimental study in rats in vivo. Gut. 49:2001;56-65.
51. Fontaine A., Arondel J., Sansonetti P.J. Role of Shiga toxin in the pathogenesis of bacillary dysentery, studied by using a Tox- mutant of Shigella dysenteriae 1. Infect. Immun. 56:1988;3099-3109.