Abstract
Toxin A from Clostridium difficile mediates acute inflammatory enterocolitis in experimental animals, while cholera toxin causes noninflammatory secretory diarrhea. The purpose of this study was to investigate whether an antagonist to the peptide substance P, a constituent of primary sensory neurons known to participate in inflammatory responses, would inhibit toxin A-mediated enteritis in the rat ileum. Pretreatment of rats with CP-96,345 (2.5 mg per kg of body weight), a substance P antagonist, dramatically inhibited fluid secretion (P < 0.01) and mannitol permeability (P < 0.01) in ileal loops exposed to toxin A. The protective effects, which were dose dependent, caused a significant reduction of inflammation in the lamina propria, reduction of the necrosis of intestinal epithelial cells, and complete inhibition of toxin A-mediated release of rat mast cell protease II, a specific product of rat mucosal mast cells. An inactive enantiomer of the substance P antagonist, CP-96,344, had no effect. In contrast, pretreatment with CP-96,345 had no inhibitory effect on the intestinal effects caused by administration of cholera toxin into the ileal loops. From these data, we conclude that the peptide substance P is involved in the secretory and inflammatory effects of toxin A but not of cholera toxin.
MeSH Terms
Animals
Bacterial Toxins/antagonists & inhibitors,toxicity
Biphenyl Compounds/pharmacology
Cholera Toxin/toxicity
Clostridioides difficile
Diarrhea/etiology,prevention & control
Enterocolitis/etiology,prevention & control
Enterotoxins/antagonists & inhibitors,toxicity
Ileum/drug effects,pathology,physiopathology
Male
Mast Cells/drug effects,metabolism
Rats
Rats, Wistar
Substance P/antagonists & inhibitors
Chemicals
Bacterial Toxins
Biphenyl Compounds
Enterotoxins
tcdA protein, Clostridium difficile
Substance P
Cholera Toxin
CP 96345
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Pothoulakis C
Section of Gastroenterology, University Hospital, Boston University School of Medicine, MA 02118.
Castagliuolo I
LaMont J T
Jaffer A
O'Keane J C
Snider R M
Leeman S E
References (33)
33 references, click to expand
-
Molecular characterization of the Clostridium difficile toxin A gene.
Infect Immun. 1990 Feb;58(2):480-8
PMID: 2105276
-
Mast cell heterogeneity: effects of neuroenteric peptides on histamine release.
J Immunol. 1985 Aug;135(2):1331-7
PMID: 2409146
-
Effect of CP-96,345, a nonpeptide substance P receptor antagonist, on salivation in rats.
Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10042-4
PMID: 1719543
-
Increased levels of substance P in the myenteric plexus of Trichinella-infected rats.
Gastroenterology. 1992 Jun;102(6):1913-9
PMID: 1375178
-
Modulation of the mRNAs encoding substance P and its receptor in rat macrophages by LPS.
Reg Immunol. 1992 Mar-Apr;4(2):105-12
PMID: 1380279
-
Diminished Clostridium difficile toxin A sensitivity in newborn rabbit ileum is associated with decreased toxin A receptor.
J Clin Invest. 1992 Sep;90(3):822-9
PMID: 1325998
-
Localization of targets for anti-ulcer drugs in cells of the immune system.
Science. 1992 Dec 4;258(5088):1662-5
PMID: 1333642
-
Effect of toxin A and B of Clostridium difficile on rabbit ileum and colon.
Gut. 1986 Jan;27(1):78-85
PMID: 3949240
-
Clostridium difficile cytotoxin inhibits protein synthesis in fibroblasts and intestinal mucosa.
Gastroenterology. 1986 Nov;91(5):1147-53
PMID: 3758606
-
The neuropharmacology of capsaicin: review of some recent observations.
Pharmacol Rev. 1986 Sep;38(3):179-226
PMID: 3534898
-
Gallbladder prostaglandins and lysophospholipids as mediators of mucin secretion during cholelithiasis.
Am J Physiol. 1986 Nov;251(5 Pt 1):G701-9
PMID: 3777174
-
Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves.
Proc Natl Acad Sci U S A. 1987 May;84(9):2975-9
PMID: 2437589
-
Distribution of substance P receptors on murine spleen and Peyer's patch T and B cells.
J Immunol. 1987 Aug 1;139(3):749-54
PMID: 2439591
-
Receptor binding sites for substance P, but not substance K or neuromedin K, are expressed in high concentrations by arterioles, venules, and lymph nodules in surgical specimens obtained from patients with ulcerative colitis and Crohn disease.
Proc Natl Acad Sci U S A. 1988 May;85(9):3235-9
PMID: 2834738
-
Effect of neuropeptides on production of inflammatory cytokines by human monocytes.
Science. 1988 Sep 2;241(4870):1218-21
PMID: 2457950
-
An electrophysiological and anatomical study of intestinal afferent fibres in the rat.
J Physiol. 1988 Jul;401:381-97
PMID: 3171991
-
Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers.
J Clin Invest. 1988 Nov;82(5):1516-24
PMID: 3141478
-
Pavlovian conditioning of rat mucosal mast cells to secrete rat mast cell protease II.
Science. 1989 Jan 6;243(4887):83-5
PMID: 2911721
-
Mast cells are closely apposed to nerves in the human gastrointestinal mucosa.
Gastroenterology. 1989 Sep;97(3):575-85
PMID: 2666250
-
Receptors for sensory neuropeptides in human inflammatory diseases: implications for the effector role of sensory neurons.
Peptides. 1989 May-Jun;10(3):627-45
PMID: 2550912
-
Comparative study of Clostridium difficile toxin A and cholera toxin in rabbit ileum.
Gastroenterology. 1989 Nov;97(5):1186-92
PMID: 2551764
-
Activation of human neutrophils by substance P: effect on FMLP-stimulated oxidative and arachidonic acid metabolism and on antibody-dependent cell-mediated cytotoxicity.
Immunology. 1989 Nov;68(3):359-64
PMID: 2480329
-
The role of substance P and calcitonin gene-related peptide in neurogenic plasma extravasation and vasodilatation in the rat.
Neuroscience. 1989;32(3):581-6
PMID: 2481241
-
Cholera toxin-sensitive neurons in guinea pig submucosal plexus.
Am J Physiol. 1993 Jan;264(1 Pt 1):G86-94
PMID: 8430809
-
Saccharomyces boulardii inhibits Clostridium difficile toxin A binding and enterotoxicity in rat ileum.
Gastroenterology. 1993 Apr;104(4):1108-15
PMID: 8462799
-
Ketotifen inhibits Clostridium difficile toxin A-induced enteritis in rat ileum.
Gastroenterology. 1993 Sep;105(3):701-7
PMID: 8395445
-
On the role of intramural nerves in the pathogenesis of cholera toxin-induced intestinal secretion.
Scand J Gastroenterol. 1981 Apr;16(3):377-84
PMID: 16435479
-
Isolation of a sialogogic peptide from bovine hypothalamic tissue and its characterization as substance P.
J Biol Chem. 1970 Sep 25;245(18):4784-90
PMID: 5456150
-
Effects of prostaglandins and cholera enterotoxin on intestinal mucosal cyclic AMP accumulation. Evidence against an essential role for prostaglandins in the action of toxin.
J Clin Invest. 1974 Mar;53(3):941-9
PMID: 4359941
-
Release of vasoactive intestinal polypeptide from the cat small intestine exposed to cholera toxin.
Gut. 1981 Nov;22(11):958-63
PMID: 7308850
-
Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker.
J Invest Dermatol. 1982 Mar;78(3):206-9
PMID: 6276474
-
Effects of Clostridium difficile toxins given intragastrically to animals.
Infect Immun. 1985 Feb;47(2):349-52
PMID: 3917975
-
Capsaicin-sensitive nerves in the gastrointestinal tract.
Arch Int Pharmacodyn Ther. 1990 Jan-Feb;303:157-66
PMID: 2196856