Effect of intestinal inflammation on capsaicin-sensitive afferents in the ileum of Schistosoma mansoni-infected mice

Histochemistry and Cell Biology

Volumn 119, Issue 6, 2003, Pages 477-484

  De Jonge, Frederik ^a   Van Nassauw, Luc ^a   Adriaensen, Dirk ^a   Van Meir, Frans ^a   Miller, Hugh R P ^b   Van Marck, Eric ^a   Timmermans, Jean Pierre ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

CGRP; Extrinsic sensory innervation; Mouse ileum; Neuroimmune interaction; Schistosomiasis

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; DRUG RECEPTOR; SUBSTANCE P; UNCLASSIFIED DRUG; VANILLOID RECEPTOR; VANILLOID RECEPTOR 1;

ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL PARASITOSIS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE MODEL; DRUG EFFECT; ENTERITIS; EXTRINSIC SENSORY INNERVATION; FLUORESCENT ANTIBODY TECHNIQUE; ILEUM; ILEUM DISEASE; IMMUNOCYTOCHEMISTRY; INNERVATION; INTESTINE INNERVATION; INTESTINE MUCOSA; INTESTINE VILLUS; LAMINA PROPRIA; MALE; MAST CELL; METABOLISM; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; NEUROCHEMISTRY; NODOSE GANGLION; NONHUMAN; PARASITOLOGY; PATHOLOGY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SENSORY NERVE; SENSORY NERVE CELL; SPINAL GANGLION; SUBCUTANEOUS DRUG ADMINISTRATION;

ANIMALS; ANIMALS, NEWBORN; CALCITONIN GENE-RELATED PEPTIDE; CAPSAICIN; DISEASE MODELS, ANIMAL; ENTERIC NERVOUS SYSTEM; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GANGLIA, SPINAL; ILEUM; INJECTIONS, SUBCUTANEOUS; INTESTINAL MUCOSA; MALE; MAST CELLS; MICE; NEURONS, AFFERENT; NODOSE GANGLION; PARASITIC DISEASES, ANIMAL; RECEPTORS, DRUG; SCHISTOSOMIASIS MANSONI; SUBSTANCE P;

ANIMALIA; MURINAE; SCHISTOSOMA; SCHISTOSOMA MANSONI;

EID: 0041665190     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-003-0532-5     Document Type: Article

References (45)

1. Balemba OB, Mbassa GK, Assey RJ, Kahawa CKB, Makundi AE, Hay-Schmidt A, Dantzer V, Semuguruka WD (2000) Lesions of the enteric nervous system and the possible role of mast cells in the pathogenic mechanisms of migration of schistosome eggs in the small intestine of cattle during S. bovis infection. Vet Parasitol 90:57-71
2. Balemba OB, Semuguruka WD, Hay-Schmidt A, Johansen MV, Dantzer V (2001) Vasoactive intestinal peptide and substance P-like immunoreactivities in the enteric nervous system of the pig correlate with the severity of pathological changes induced by Schistosoma japonicum. Int J Parasitol 31:1503-1514
3. Bienenstock J, Tomioka M, Matsuda H, Stead RH, Quinonez G, Simon GT, Coughlin MD, Denburg JA (1987) The role of mast cells in inflammatory processes: evidence for nerve/mast cell interactions. Int Arch Allergy Immunol 82:238-243
4. Bienenstock J, Blennerhassett MG, Kakuta Y, Macqueen G, Marshall JS, Perdue MH, Siegel S, Tsuda T, Denburg JA, Stead RH (1989a) Evidence for central and peripheral nervous system interaction with mast cells. In: Galli SJ, Austen KF (eds) Mast cell and basophil differentiation and function in health and disease. Raven, New York, pp 275-284
5. Bienenstock J, Blennerhassett MG, Tomioka M, Marshall JS, Perdue MH, Stead RH (1989b) Evidence for mast cell-nerve interactions. In: Goetzl E (ed) Neuroimmune networks: physiology and disease. Liss, New York, pp 149-154
6. Bienenstock J, Macqueen G, Sestini P, Marshall JS, Stead RH, Perdue MH (2001) Mast cell/nerve interaction in vitro and in vivo. Am Rev Respir Dis 143:S55-S58
7. Blennerhassett MG, Bienenstock J (1997) Sympathetic nerve contact causes maturation of mast cells in vitro. J Neurobiol 35:173-182
8. Blennerhassett MG, Tomioka M, Bienenstock J (1991) Formation of contacts between mast cells and sympathetic neurons in vitro. Cell Tissue Res 265:121-128
9. Bogers J, Moreels T, De Man J, Vrolix G, Jacobs W, Pelckmans P, Van Marck E (2000) Schistosoma mansoni infection causing diffuse enteric inflammation and damage of the enteric nervous system in the mouse small intestine. Neurogastroenterol Motil 12:431-440
10. De Jonge F, Van Nassauw L, Van Meir F, Miller HRP, Van Marck E, Timmermans J-P (2002) Temporal distribution of distinct mast cell phenotypes during intestinal schistosomiasis in mice. Parasite Immunol 24:225-231
11. Domingo EO, Warren KS (1969) Pathology and pathophysiology of the small intestine in murine schistosomiasis mansoni, including a review of the literature. Gastroenterology 56:231-240
12. Domoto T, Yang H, Bishop AE, Polak JM, Oki M (1992) Distribution and origin of extrinsic nerve fibers containing calcitonin-gene related peptide, substance P and galanin in the rat upper rectum. Neurosci Res 15:64-73
13. El-Garem AA (1998) Schistosomiasis. Digestion 59:589-605
14. Foster EA, Mandak B, Kromer E, Rot A (1992) Calcitonin gene-related peptide is chemotactic for human T lymphocytes. Ann N Y Acad Sci 657:397-404
15. Gamse R (1982) Capsaicin and nociception in the rat and mouse. Naunyn Schmiedebergs Arch Pharmacol 320:205-216
16. Gay J, Fioramonti J, Garcia-Villar R, Bueno L (2000) Development and sequels of intestinal inflammation in nematode-infected rats: role of mast cells and capsaicin-sensitive afferents. Neuroimmunomodulation 8:171-178
17. Gottwald T, Lhotak S, Stead RH (1997) Effect of truncal vagotomy and capsaicin on mast cells and IgA-positive plasma cells in rat jejunal mucosa. Neurogastroenterol Motil 9:25-32
18. Gryseels B (1992) Morbidity due to infection with Schistosoma mansoni: an update. Trop Geog Med 44:189-200
19. Harti G, Sharkey KA, Pierau F-K (1989) Effects of capsaicin in rat and pigeon on peripheral nerves containing substance P and calcitonin gene-related peptide. Cell Tissue Res 256:465-474
20. Holzer P, Lippe ITh, Amann R (1992) Participation of capsaicin-sensitive afferent neurons in gastric motor inhibition caused by laparotomy and intraperitoneal acid. Neuroscience 48:715-722
21. Kar S, Gibson J, Polak JM (1988) Primary sensory neurones immunoreactive for calcitonin gene-related peptide (CGRP), galanin and substance P and CGRP-immunoreactive motoneurones constitute the major afferent and efferent peptidergic input to the genitofemoral nerve. J Pathol 154:A70
22. Kobayashi H, Yamataka A, Fujimoto T, Lane GJ, Miyano T (1999) Mast cells and gut nerve development: implications for Hirschsprung's disease and intestinal neuronal dysplasia. J Pediatr Surg 34:543-548
23. Llewellyn-Smith IJ, Costa M, Fumess JB (1985) Light and electron microscope immunohistochemistry of the same nerves from whole mount preparation. J Histochem Cytochem 33:857-866
24. Mazelin L, Theodorou V, More J, Fioramonti J, Bueno L (1998) Protective role of vagal afferents in experimentally-induced colitis in rats. J Auton Nerv Syst 73:38-43
25. Mazelin L, Theodorou V, Fioramonti J, Bueno L (1999) Vagally dependent protective action of calcitonin gene-related peptide on colitis. Peptides 20:1367-1374
26. Miller HRP, Newlands GFJ, McKellar A, Inglis L, Coulson PS, Wilson RA (1994) Hepatic recruitment of mast cells occurs in rats but not mice infected with Schistosoma mansoni. Parasite Immunol 16:145-155
27. Orozco OE, Walus L, Sah DWY, Pepinsky RB, Sanicola M (2001) GFRalpha3 is expressed predominantly in nociceptive sensory neurons. Eur J Neurosci 13:2177-2182
28. Reinshagen M, Patel A, Sottili M, Nast C, Davis W, Mueller K, Eysselein VE (1994) Protective function of extrinsic sensory neurons in acute rabbit experimental colitis. Gastroenterology 106:1208-1214
29. Reinshagen M, Flämig G, Ernst S, Geerling I, Wong H, Walsh JH, Eysselein VE, Adler G (1998) Calcitonin gene-related peptide mediates the protective effect of sensory nerves in a model of colonic injury. J Pharmacol Exp Ther 286:657-661
30. Sang Q, Young HM (1996) Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res 284:39-53
31. Sang Q, Young HM (1998) The identification and chemical coding of cholinergic neurons in the small and large intestine of the mouse. Anat Rec 251:185-199
32. Sang Q, Williamson S, Young HM (1997) Projections of chemically identified myenteric neurons of the small and large intestine of the mouse. J Anat 190:209-222
33. Smithers SR, Terry RJ (1965) The infection of laboratory hosts with cercariae of S. mansoni and the recovery of the adult worms. Parasitology 55:695-700
34. Stead RH (1992) Innervation of mucosal immune cells in the gastrointestinal tract. Reg Immunol 4:91-99
35. Stead RH, Tomioka M, Quinonez G, Simon GT, Felten SY, Bienenstock J (1987) 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 84:2975-2979
36. Stead RH, Perdue MH, Blennerhassett MG, Kakuta Y, Sestini P, Bienenstock J (1990) The innervation of mast cells. In: Freier S (ed) The neuroendocrine-immune network. CRC Press, Boca Raton, pp 9-37
37. Stead RH, Bienenstock J, Stanisz A (2001) Neuropeptide regulation of mucosal immunity. Immunol Rev 100:333-359
38. Timmermans J-P, Scheuermann DW, Barbiers M, Adriaensen D, Stach W, Van Hee R, De Groodt-Lasseel MHA (1992) Calcitonin gene related peptide-like immunoreactivity in the human small intestine. Acta Anat 143:48-53
39. Timmermans J-P, Adriaensen D, Cornelissen W, Scheuermann DW (1997) Structural organization and neuropeptide distribution in the mammalian enteric nervous system, with special attention to those components involved in mucosal reflexes. Comp Biochem Physiol 118:331-340
40. Van Nassauw L, Hens J, Bogers J, Van Marck E, Timmermans J-P (2000) Retrograde DiI tracing of enteric neurons projecting to the mucosa in the murine small intestine. Falk symposium. In: Singer MV, Krammer H-J (eds) Neurogastroenterology: from the basics to the clinics. Kluwer Academic, Dordrecht, pp 92-95
41. Van Nassauw L, Bogers J, Van Marck E, Timmermans J-P (2001) Role of reactive nitrogen species in neuronal cell damage during intestinal schistosomiasis. Cell Tissue Res 303:329-336
42. Varilek GW, Weinstock JV, Williams TH, Jew J (1991) Alterations of the intestinal innervation in mice infected with S. mansoni. J Parasitol 77:472-478
43. Williams RM, Bienenstock J, Stead RH (1995) Mast cells: the neuroimmune connection. In: Marone G (ed) Human basophils and mast cells: biological aspects. Karger, Basel, pp 208-235
44. Williams RM, Berthoud H-R, Stead RH (1997) Vagal afferent nerve fibers contact mast cells in rat small intestinal mucosa. Neuroimmunomodulation 4:266-270
45. Wood JD, Alpers DH, Andrews PR (1999) Fundamentals of neurogastroenterology. Gut 45:6-16