Fecal proteases from diarrheic-IBS and ulcerative colitis patients exert opposite effect on visceral sensitivity in mice

Pain

Volumn 144, Issue 1-2, 2009, Pages 209-217

  Annaházi, Anita ^a,b   Gecse, Krisztina ^b   Dabek, Marta ^a   Ait Belgnaoui, Afifa ^a   Rosztóczy, András ^b   Róka, Richárd ^b   Molnár, Tamás ^b   Theodorou, Vassilia ^a   Wittmann, Tibor ^b   Bueno, Lionel ^a   Eutamene, Helene ^a  

^a CNRS   (France)

^b UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Cathepsin G; Irritable bowel syndrome; Proteinase activated receptor; Ulcerative colitis; Visceral pain

Indexed keywords

CATHEPSIN G; PEPDUCIN; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 4; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DIARRHEA; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; INTESTINE DISTENSION; IRRITABLE COLON; MALE; MOUSE; NEWBORN; NOCICEPTION; NONHUMAN; PAIN ASSESSMENT; PRIORITY JOURNAL; ULCERATIVE COLITIS; VISCERAL PAIN;

ADULT; ANALYSIS OF VARIANCE; ANIMALS; COLITIS, ULCERATIVE; ENZYME INHIBITORS; FECES; FEMALE; HUMANS; IRRITABLE BOWEL SYNDROME; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; PERCEPTION; RECEPTORS, PROTEINASE-ACTIVATED; SENSORY THRESHOLDS; SERINE ENDOPEPTIDASES; VISCERA;

EID: 66049093837     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2009.04.017     Document Type: Article

References (37)

1. Asfaha S., Brussee V., Chapman K., Zochodne D.W., and Vergnolle N. Proteinase-activated receptor-1 agonists attenuate nociception in response to noxious stimuli. Br J Pharmacol 135 (2002) 1101-1106
2. Asfaha S., Cenac N., Houle S., Altier C., Papez M.D., Nguyen C., Steinhoff M., Chapman K., Zamponi G.W., and Vergnolle N. Protease-activated receptor-4: a novel mechanism of inflammatory pain modulation. Br J Pharmacol 150 (2007) 176-185
3. Barbara G., Stanghellini V., De Giorgio R., Cremon C., Cottrell G.S., Santini D., Pasquinelli G., Morselli-Labate A.M., Grady E.F., Bunnett N.W., Collins S.M., and Corinaldesi R. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126 (2004) 693-702
4. Bernstein C.N., Niazi N., Robert M., Mertz H., Kodner A., Munakata J., Naliboff B., and Mayer E.A. Rectal afferent function in patients with inflammatory and functional intestinal disorders. Pain 66 (1996) 151-161
5. Beyak M.J., and Vanner S. Inflammation-induced hyperexcitability of nociceptive gastrointestinal DRG neurones: the role of voltage-gated ion channels. Neurogastroenterol Motil 17 (2005) 175-186
6. Bradette M., Delvaux M., Staumont G., Fioramonti J., Bueno L., and Frexinos J. Evaluation of colonic sensory thresholds in IBS patients using a barostat. Definition of optimal conditions and comparison with healthy subjects. Dig Dis Sci 39 (1994) 449-457
7. Cervero F., and Laird J.M. Understanding the signaling and transmission of visceral nociceptive events. J Neurobiol 61 (2004) 45-54
8. Chadwick V.S., Chen W., Shu D., Paulus B., Bethwaite P., Tie A., and Wilson I. Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology 122 (2002) 1778-1783
9. Chang L., Munakata J., Mayer E.A., Schmulson M.J., Johnson T.D., Bernstein C.N., Saba L., Naliboff B., Anton P.A., and Matin K. Perceptual responses in patients with inflammatory and functional bowel disease. Gut 47 (2000) 497-505
10. Coelho A.M., Vergnolle N., Guiard B., Fioramonti J., and Bueno L. Proteinases and proteinase-activated receptor 2: a possible role to promote visceral hyperalgesia in rats. Gastroenterology 122 (2002) 1035-1047
11. Compton S.J., Renaux B., Wijesuriya S.J., and Hollenberg M.D. Glycosylation and the activation of proteinase-activated receptor 2 (PAR(2)) by human mast cell tryptase. Br J Pharmacol 134 (2001) 705-718
12. Compton S.J., Sandhu S., Wijesuriya S.J., and Hollenberg M.D. Glycosylation of human proteinase-activated receptor-2 (hPAR2): role in cell surface expression and signalling. Biochem J 368 (2002) 495-505
13. Dabek M., Ferrier L., Chaumaz G., Salvador-Cartier C., Gecse K., Moreau J., Buscail L., Escourrou J., Fioramonti J., Theodorou V., and Bueno L. High fecal serine-protease activity in IBD patients triggers alterations of paracellular permeability in mice colon through PAR 4 receptor activation. Gastroenterology 134 Suppl. (2008) A-356
14. Dulon S., Cande C., Bunnett N.W., Hollenberg M.D., Chignard M., and Pidard D. Proteinase-activated receptor-2 and human lung epithelial cells: disarming by neutrophil serine proteinases. Am J Respir Cell Mol Biol 28 (2003) 339-346
15. Dunlop S.P., Jenkins D., Neal K.R., and Spiller R.C. Relative importance of enterochromaffin cell hyperplasia, anxiety, and depression in postinfectious IBS. Gastroenterology 125 (2003) 1651-1659
16. Gecse K., Roka R., Ferrier L., Leveque M., Eutamene H., Cartier C., Ait-Belgnaoui A., Rosztoczy A., Izbeki F., Fioramonti J., Wittmann T., and Bueno L. Increased faecal serine protease activity in diarrhoeic IBS patients: a colonic lumenal factor impairing colonic permeability and sensitivity. Gut 57 (2008) 591-599
17. Gwee K.A., Leong Y.L., Graham C., McKendrick M.W., Collins S.M., Walters S.J., Underwood J.E., and Read N.W. The role of psychological and biological factors in postinfective gut dysfunction. Gut 44 (1999) 400-406
18. Hollenberg M.D., and Compton S.J. International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev 54 (2002) 203-217
19. Hoogerwerf W.A., Hellmich H.L., Micci M.A., Winston J.H., Zou L., and Pasricha P.J. Molecular cloning of the rat proteinase-activated receptor 4 (PAR4). BMC Mol Biol 3 (2002) 2
20. Houle S., Papez M.D., Ferazzini M., Hollenberg M.D., and Vergnolle N. Neutrophils and the kallikrein-kinin system in proteinase-activated receptor 4-mediated inflammation in rodents. Br J Pharmacol 146 (2005) 670-678
21. Kawabata A., Matsunami M., and Sekiguchi F. Gastrointestinal roles for proteinase-activated receptors in health and disease. Br J Pharmacol 153 Suppl. 1 (2008) S230-240
22. La J.H., Kim T.W., Sung T.S., Kim H.J., Kim J.Y., and Yang I.S. Role of mucosal mast cells in visceral hypersensitivity in a rat model of irritable bowel syndrome. J Vet Sci 5 (2004) 319-324
23. Larsson M.H., Rapp L., and Lindstrom E. Effect of DSS-induced colitis on visceral sensitivity to colorectal distension in mice. Neurogastroenterol Motil 18 (2006) 144-152
24. Mayer E.A., Berman S., Suyenobu B., Labus J., Mandelkern M.A., Naliboff B.D., and Chang L. Differences in brain responses to visceral pain between patients with irritable bowel syndrome and ulcerative colitis. Pain 115 (2005) 398-409
25. Mertz H., Naliboff B., Munakata J., Niazi N., and Mayer E.A. Altered rectal perception is a biological marker of patients with irritable bowel syndrome. Gastroenterology 109 (1995) 40-52
26. Pham C.T. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 6 (2006) 541-550
27. Rachmilewitz D. Coated mesalazine (5-aminosalicylic acid) versus sulphasalazine in the treatment of active ulcerative colitis: a randomised trial. BMJ 298 (1989) 82-86
28. Ritchie J. Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14 (1973) 125-132
29. Roka R., Rosztoczy A., Leveque M., Izbeki F., Nagy F., Molnar T., Lonovics J., Garcia-Villar R., Fioramonti J., Wittmann T., and Bueno L. A pilot study of fecal serine-protease activity: a pathophysiologic factor in diarrhea-predominant irritable bowel syndrome. Clin Gastroenterol Hepatol 5 (2007) 550-555
30. Sabri A., Alcott S.G., Elouardighi H., Pak E., Derian C., Andrade-Gordon P., Kinnally K., and Steinberg S.F. Neutrophil cathepsin G promotes detachment-induced cardiomyocyte apoptosis via a protease-activated receptor-independent mechanism. J Biol Chem 278 (2003) 23944-23954
31. Saverymuttu S.H., Chadwick V.S., and Hodgson H.J. Granulocyte migration in ulcerative colitis. Eur J Clin Invest 15 (1985) 60-63
32. Sharkey K.A. Visceral sensation and colitis: inflammation and hypersensitivity do not always go hand in hand. Neurogastroenterol Motil 18 (2006) 87-90
33. Shimoda N., Fukazawa N., Nonomura K., and Fairchild R.L. Cathepsin g is required for sustained inflammation and tissue injury after reperfusion of ischemic kidneys. Am J Pathol 170 (2007) 930-940
34. Shpacovitch V., Feld M., Bunnett N.W., and Steinhoff M. Protease-activated receptors: novel PARtners in innate immunity. Trends Immunol 28 (2007) 541-550
35. Uehara A., Muramoto K., Takada H., and Sugawara S. Neutrophil serine proteinases activate human nonepithelial cells to produce inflammatory cytokines through protease-activated receptor 2. J Immunol 170 (2003) 5690-5696
36. Xu W.F., Andersen H., Whitmore T.E., Presnell S.R., Yee D.P., Ching A., Gilbert T., Davie E.W., and Foster D.C. Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci USA 95 (1998) 6642-6646
37. Zar S., Benson M.J., and Kumar D. Rectal afferent hypersensitivity and compliance in irritable bowel syndrome: differences between diarrhoea-predominant and constipation-predominant subgroups. Eur J Gastroenterol Hepatol 18 (2006) 151-158