Role of enteric nerves in immune-mediated changes in protease-activated receptor 2 effects on gut function

Neurogastroenterology and Motility

Volumn 22, Issue 10, 2010, Pages

  Shea Donohue, T ^a   Notari, L ^a   Stiltz, J ^a   Sun, R ^a   Madden, K B ^b   Urban, J F ^c   Zhao, A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

epithelial cell; IL 13; IL 4; nematode infection; PAR2; smooth muscle

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; INTERLEUKIN 13; INTERLEUKIN 4; MESSENGER RNA; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 2 AGONIST; STAT6 PROTEIN; TETRODOTOXIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; HELIGMOSOMOIDES POLYGYRUS; IMMUNITY; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; INTESTINE CONTRACTION; INTESTINE FUNCTION; INTESTINE INNERVATION; INTESTINE MUSCLE; LAMINA PROPRIA; MOUSE; NEMATODIASIS; NERVE BLOCK; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; SMOOTH MUSCLE FIBER; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; ENTERIC NERVOUS SYSTEM; FLUORESCENT ANTIBODY TECHNIQUE; GASTROINTESTINAL TRACT; GENE EXPRESSION; IMMUNITY, CELLULAR; INFECTION; INTESTINAL MUCOSA; MICE; MICE, INBRED BALB C; MUSCLE CONTRACTION; MUSCLE, SMOOTH; NEMATODE INFECTIONS; NIPPOSTRONGYLUS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RECEPTOR, PAR-2; RNA; STAT6 TRANSCRIPTION FACTOR; TETRODOTOXIN; TH2 CELLS;

EID: 77956305516     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2010.01557.x     Document Type: Article

References (53)

1. Hollenberg MD, Saifeddine M, Al Ani B, Kawabata A. Proteinase-activated receptors: structural requirements for activity, receptor cross-reactivity, and receptor selectivity of receptor-activating peptides. Can J Physiol Pharmacol 1997 75 : 832 841.
2. Amadesi S, Bunnett N. Protease-activated receptors: protease signaling in the gastrointestinal tract. Curr Opin Pharmacol 2004 4 : 551 556.
3. Vergnolle N. Review article: proteinase-activated receptors - novel signals for gastrointestinal pathophysiology. Aliment Pharmacol Ther 2000 14 : 257 266.
4. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. Proteinase-activated receptors. Pharmacol Rev 2001 53 : 245 282.
5. Cocks TM, Sozzi V, Moffatt JD, Selemidis S. Protease-activated recep-tors mediate apamin-sensitive relaxation of mouse and guinea pig gastrointestinal smooth muscle. Gastroenterology 1999 116 : 586 592.
6. Corvera CU, Dery O, McConalogue K et al. Mast cell tryptase regulates rat colonic myocytes through proteinase-activated receptor 2. J Clin Invest 1997 100 : 1383 1393.
7. Gao C, Liu S, Hu HZ et al. Serine proteases excite myenteric neurons through protease-activated receptors in guinea pig small intestine. Gastroenterology 2002 123 : 1554 1564.
8. Kong W, McConalogue K, Khitin LM et al. Luminal trypsin may regulate enterocytes through proteinase-activated receptor 2. Proc Natl Acad Sci USA 1997 94 : 8884 8889.
9. Colognato R, Slupsky JR, Jendrach M, Burysek L, Syrovets T, Simmet T. Differential expression and regulation of protease-activated receptors in human peripheral monocytes and monocyte-derived antigen-presenting cells. Blood 2003 102 : 2645 2652.
10. Jacob C, Yang PC, Darmoul D et al. Mast cell tryptase controls paracellular permeability of the intestine: role of protease-activated receptor 2 and beta-arrestins. J Biol Chem 2005 280 : 31936 31948.
11. Li X, Syrovets T, Paskas S, Laumonnier Y, Simmet T. Mature dendritic cells express functional thrombin receptors triggering chemotaxis and CCL18/pulmonary and activation-regulated chemokine induction. J Immunol 2008 181 : 1215 1223.
12. Mari B, Guerin S, Far DF et al. Thrombin and trypsin-induced Ca(2+) mobilization in human T cell lines through interaction with different protease-activated receptors. FASEB J 1996 10 : 309 316.
13. Bueno L, Fioramonti J. Protease-activated receptor 2 and gut permeability: a review. Neurogastroenterol Motil 2008 20 : 580 587.
14. Cenac N, Chin AC, Garcia-Villar R et al. PAR2 activation alters colonic paracellular permeability in mice via IFN-gamma-dependent and -independent pathways. J Physiol (Lond) 2004 558 : 913 925.
15. Vergnolle N, MacNaughton WK, Al-Ani B, Saifeddine M, Wallace JL, Hollenberg MD. Proteinase-activated receptor 2 (PAR2)-activating peptides: identification of a receptor distinct from PAR2 that regulates intestinal transport. Proc Natl Acad Sci USA 1998 95 : 7766 7771.
16. Zhao A, Shea-Donohue T. PAR-2 agonists induce contraction of murine small intestine through neurokinin receptors. Am J Physiol Gastrointest Liver Physiol 2003 285 : G696 703.
17. Coughlin SR, Camerer E. PARticipation in inflammation. J Clin Invest 2003 111 : 25 7.
18. Fiorucci S, Mencarelli A, Palazzetti B et al. Proteinase-activated receptor 2 is an anti-inflammatory signal for colonic lamina propria lymphocytes in a mouse model of colitis. Proc Natl Acad Sci USA 2001 98 : 13936 13941.
19. Hansen KK, Sherman PM, Cellars L et al. A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc Natl Acad Sci USA 2005 102 : 8363 8368.
20. Vergnolle N, Cellars L, Mencarelli A et al. A role for proteinase-activated receptor-1 in inflammatory bowel diseases. J Clin Invest 2006 116 : 2056.
21. Vergnolle N. Protease-activated recep-tors as drug targets in inflammation and pain. Pharmacol Ther 2009 123 : 292 309.
22. Urban JF Jr., Schopf L, Morris SC et al. Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. J Immunol 2000 164 : 2046 2052.
23. Akiho H, Blennerhassett P, Deng Y, Collins SM. Role of IL-4, IL-13, and STAT6 in inflammation-induced hypercontractility of murine smooth muscle cells 3. Am J Physiol Gastrointest Liver Physiol 2002 282 : G226 32.
24. Khan WI, Vallance BA, Blennerhassett PA et al. Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infect Immun 2001 69 : 838 844.
25. Zhao A, McDermott J, Urban JF Jr. et al. Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. J Immunol 2003 171 : 948 954.
26. Devlin M, Gasser R, Cocks T. Initial support for the hypothesis that PAR2 is involved in the immune response to Nippostrongylus brasiliensis in mice. Parasitol Res 2007 101 : 105 109.
27. Urban JF Jr., Madden KB, Cheever AW, Trotta PP, Katona IM, Finkelman FD. IFN inhibits inflammatory responses and protective immunity in mice infected with the nematode parasite, Nippostrongylus brasiliensis. J Immunol 1993 151 : 7086 7094.
28. Finkelman FD, Shea-Donohue T, Morris SC et al. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol Rev 2004 201 : 139 155.
29. Zhao A, Morimoto M, Dawson H et al. Immune regulation of protease-activated receptor-1 expression in murine small intestine during Nippostrongylus brasiliensis infection. J Immunol 2005 175 : 2563 2569.
30. Linden DR, Manning BP, Bunnett NW, Mawe GM. Agonists of proteinase-activated receptor 2 excite guinea pig ileal myenteric neurons. Eur J Pharmacol 2001 431 : 311 314.
31. Vergnolle N, Bunnett NW, Sharkey KA et al. Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway. Nat Med 2001 7 : 821 826.
32. Grant AD, Cottrell GS, Amadesi S et al. Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol 2007 578 : 715 733.
33. Cenac N, Andrews CN, Holzhausen M et al. Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest 2007 117 : 636 647.
34. Cenac N, Coelho AM, Nguyen C et al. Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor-2. Am J Pathol 2002 161 : 1903 1915.
35. Zhao A, Urban JF Jr., Morimoto M et al. Contribution of 5-HT2A receptor in nematode infection-induced murine intestinal smooth muscle hypercontractility. Gastroenterology 2006 131 : 568 578.
36. Madden KB, Urban JF Jr., Ziltener HJ, Schrader JW, Finkelman FD, Katona IM. Antibodies to IL-3 and IL-4 suppress helminth-induced intestinal mastocytosis. J Immunol 1991 147 : 1387 1391.
37. Donaldson LE, Schmitt E, Huntley JF, Newlands GFJ, Grencis RK. A critical role for stem cell factor and c-kit in host protective immunity to an intestinal helminth. Int Immunol 1996 8 : 559 567.
38. Pennock JL, Grencis RK. The mast cell and gut nematodes: damage and defence. Chem Immunol Allergy 2006 90 : 128 140.
39. Knight PA, Wright SH, Lawrence CE, Paterson YY, Miller HR. Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cell-specific granule chymase, mouse mast cell protease-1. J Exp Med 2000 192 : 1849 1856.
40. Rosbottom A, Knight PA, McLachlan G et al. Chemokine and cytokine expression in murine intestinal epithelium following Nippostrongylus brasiliensis infection. Parasite Immunol 2002 24 : 67 75.
41. Barbara G, Wang B, Stanghellini V et al. Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 2007 132 : 26 37.
42. Kawabata A, Kuroda R, Nagata N et al. In vivo evidence that protease-activated receptors 1 and 2 modulate gastrointestinal transit in the mouse. Br J Pharmacol 2001 133 : 1213 1218.
43. Bunnett NW. Protease-activated receptors: how proteases signal to cells to cause inflammation and pain. Semin Thromb Hemost 2006 32 (Suppl. 1 39 48.
44. Cuffe JE, Bertog M, Velazquez-Rocha S, Dery O, Bunnett N, Korbmacher C. Basolateral PAR-2 receptors mediate KCl secretion and inhibition of Na+ absorption in the mouse distal colon. J Physiol 2002 539 : 209 222.
45. Van der Merwe JQ, Ohland CL, Hirota CL, MacNaughton WK. Prostaglandin E2 derived from cyclooxygenases 1 and 2 mediates intestinal epithelial ion transport stimulated by the activation of protease-activated receptor 2. J Pharmacol Exp Ther 2009 329 : 747 752.
46. Madden KB, Yeung KA, Zhao A et al. Enteric nematodes induce stereotypic STAT6-dependent alterations in intestinal epithelial cell function. J Immunol 2004 172 : 5616 5621.
47. Shea-Donohue T, Sullivan C, Finkelman FD et al. The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. J Immunol 2001 167 : 2234 2239.
48. Madden KB, Whitman L, Sullivan C et al. Role of STAT6 and mast cells in IL-4- and IL-13-induced alterations in murine intestinal epithelial cell function. J Immunol 2002 169 : 4417 4422.
49. Cottrell GS, Amadesi S, Pikios S et al. Protease-activated receptor 2, dipeptidyl peptidase I, and proteases mediate clostridium difficile toxin A enteritis. Gastroenterology 2007 132 : 2422 2437.
50. Rhoads ML, Fetterer RH, Hill DE, Urban J. Trichuris suis: a secretory chymotrypsin/elastase inhibitor with potential as an immunomodulator. Exp Parasitol 2000 95 : 36 44.
51. Toubarro D, Lucena-Robles M, Nascimento G et al. An apoptosis-inducing serine protease secreted by the entomopathogenic nematode Steinernema carpocapsae. Int J Parasitol 2009 39 : 1319 1330.
52. Trap C, Boireau P. Proteases in helminthic parasites. Vet Res 2000 31 : 461 471.
53. Trap C, Fu B, Le GF et al. Cloning and analysis of a cDNA encoding a putative serine protease comprising two trypsin-like domains of Trichinella spiralis. Parasitol Res 2006 98 : 288 294.