Serine proteases and protease-activated receptor 2 mediate the proinflammatory and algesic actions of diverse stimulants

British Journal of Pharmacology

Volumn 171, Issue 16, 2014, Pages 3814-3826

  Cattaruzza, F ^a   Amadesi, S ^b   Carlsson, J F ^c   Murphy, J E ^a   Lyo, V ^a   Kirkwood, K ^a   Cottrell, G S ^b   Bogyo, M ^d   Knecht, W ^c   Bunnett, N W ^e,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF READING   (United Kingdom)

^c ASTRAZENECA R AND D   (Sweden)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MONASH UNIVERSITY   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYKININ; CAPSAICIN; FORMALDEHYDE; MELAGATRAN; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 4; SERINE PROTEINASE; SOYBEAN TRYPSIN INHIBITOR; TRYPSIN; TRYPSIN 4; UNCLASSIFIED DRUG; 2-FUROYL-LIGRLO-AMIDE; AZETIDINE DERIVATIVE; BENZYLAMINE DERIVATIVE; OLIGOPEPTIDE; SERINE PROTEINASE INHIBITOR; TRY4 PROTEIN, MOUSE;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HYPERALGESIA; INFLAMMATION; INFLAMMATORY PAIN; INTRAPLANTAR DRUG ADMINISTRATION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PAIN; PAIN THRESHOLD; PAW EDEMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; AGONISTS; ANIMAL; C57BL MOUSE; CELL LINE; CHEMICALLY INDUCED; DEFICIENCY; FOOT; GENETICS; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; AZETIDINES; BENZYLAMINES; BRADYKININ; CELL LINE; FEMALE; FOOT; FORMALDEHYDE; INFLAMMATION; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGOPEPTIDES; PAIN; RECEPTOR, PAR-2; SERINE PROTEASES; SERINE PROTEINASE INHIBITORS; TRYPSIN;

EID: 84903849154     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12738     Document Type: Article

References (54)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et-al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G Protein-Coupled Receptors. Br J Pharmacol 170: 1459-1581.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Catterall WA, et-al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Ion Channels. Br J Pharmacol 170: 1607-1651.
3. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M, et-al. (2004). Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 24: 4300-4312.
4. Amadesi S, Cottrell GS, Divino L, Chapman K, Grady EF, Bautista F, et-al. (2006). Protease-activated receptor 2 sensitizes TRPV1 by protein kinase Cepsilon- and A-dependent mechanisms in rats and mice. J Physiol 575: 555-571.
5. Bohm SK, Kong W, Bromme D, Smeekens SP, Anderson DC, Connolly A, et-al. (1996). Molecular cloning, expression and potential functions of the human proteinase-activated receptor-2. Biochem J 314 (Pt 3): 1009-1016.
6. Camerer E, Huang W, Coughlin SR, (2000). Tissue factor- and factor X-dependent activation of protease-activated receptor 2 by factor VIIa. Proc Natl Acad Sci U S A 97: 5255-5260.
7. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D, (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824.
8. Cattaruzza F, Lyo V, Jones E, Pham D, Hawkins J, Kirkwood K, et-al. (2011). Cathepsin S is activated during colitis and causes visceral hyperalgesia by a PAR2-dependent mechanism in mice. Gastroenterology 141: 1864-1874.
9. Cenac N, Coelho AM, Nguyen C, Compton S, Andrade-Gordon P, MacNaughton WK, et-al. (2002). Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor-2. Am J Pathol 161: 1903-1915.
10. Cenac N, Garcia-Villar R, Ferrier L, Larauche M, Vergnolle N, Bunnett NW, et-al. (2003). Proteinase-activated receptor-2-induced colonic inflammation in mice: possible involvement of afferent neurons, nitric oxide, and paracellular permeability. J Immunol 170: 4296-4300.
11. Cenac N, Andrews CN, Holzhausen M, Chapman K, Cottrell G, Andrade-Gordon P, et-al. (2007). Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest 117: 636-647.
12. Ceppa EP, Lyo V, Grady EF, Knecht W, Grahn S, Peterson A, et-al. (2011). Serine proteases mediate inflammatory pain in acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 300: G1033-G1042.
13. Corvera CU, Dery O, McConalogue K, Bohm SK, Khitin LM, Caughey GH, et-al. (1997). Mast cell tryptase regulates rat colonic myocytes through proteinase-activated receptor 2. J Clin Invest 100: 1383-1393.
14. Cottrell GS, Amadesi S, Grady EF, Bunnett NW, (2004). Trypsin IV, a novel agonist of protease-activated receptors 2 and 4. J Biol Chem 279: 13532-13539.
15. Dai Y, Wang S, Tominaga M, Yamamoto S, Fukuoka T, Higashi T, et-al. (2007). Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 117: 1979-1987.
16. Diederichs S, Bulk E, Steffen B, Ji P, Tickenbrock L, Lang K, et-al. (2004). S100 family members and trypsinogens are predictors of distant metastasis and survival in early-stage non-small cell lung cancer. Cancer Res 64: 5564-5569.
17. Eilers H, Cattaruzza F, Nassini R, Materazzi S, Andre E, Chu C, et-al. (2010). Pungent general anesthetics activate transient receptor potential-A1 to produce hyperalgesia and neurogenic bronchoconstriction. Anesthesiology 112: 1452-1463.
18. Emi M, Nakamura Y, Ogawa M, Yamamoto T, Nishide T, Mori T, et-al. (1986). Cloning, characterization and nucleotide sequences of two cDNAs encoding human pancreatic trypsinogens. Gene 41: 305-310.
19. Ferrell WR, Lockhart JC, Kelso EB, Dunning L, Plevin R, Meek SE, et-al. (2003). Essential role for proteinase-activated receptor-2 in arthritis. J Clin Invest 111: 35-41.
20. Gallatz K, Medveczky P, Nemeth P, Szilagyi L, Graf L, Palkovits M, (2007). Human trypsin(ogen) 4-like immunoreactivity in the white matter of the cerebral cortex and the spinal cord. Ideggyogy Sz 60: 118-123.
21. Grant AD, Cottrell GS, Amadesi S, Trevisani M, Nicoletti P, Materazzi S, et-al. (2007). Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol 578: 715-733.
22. Grishina Z, Ostrowska E, Halangk W, Sahin-Toth M, Reiser G, (2005). Activity of recombinant trypsin isoforms on human proteinase-activated receptors (PAR): mesotrypsin cannot activate epithelial PAR-1, -2, but weakly activates brain PAR-1. Br J Pharmacol 146: 990-999.
23. Gustafsson D, Antonsson T, Bylund R, Eriksson U, Gyzander E, Nilsson I, et-al. (1998). Effects of melagatran, a new low-molecular-weight thrombin inhibitor, on thrombin and fibrinolytic enzymes. Thromb Haemost 79: 110-118.
24. Hansen KK, Sherman PM, Cellars L, Andrade-Gordon P, Pan Z, Baruch A, et-al. (2005). A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc Natl Acad Sci U S A 102: 8363-8368.
25. Hoogerwerf WA, Shenoy M, Winston JH, Xiao SY, He Z, Pasricha PJ, (2004). Trypsin mediates nociception via the proteinase-activated receptor 2: a potentially novel role in pancreatic pain. Gastroenterology 127: 883-891.
26. Jacob C, Cottrell GS, Gehringer D, Schmidlin F, Grady EF, Bunnett NW, (2005). c-Cbl mediates ubiquitination, degradation, and down-regulation of human protease-activated receptor 2. J Biol Chem 280: 16076-16087.
27. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
28. Knecht W, Cottrell GS, Amadesi S, Mohlin J, Skaregarde A, Gedda K, et-al. (2007). Trypsin IV or mesotrypsin and p23 cleave protease-activated receptors 1 and 2 to induce inflammation and hyperalgesia. J Biol Chem 282: 26089-26100.
29. Koistinen H, Koistinen R, Zhang WM, Valmu L, Stenman UH, (2009). Nexin-1 inhibits the activity of human brain trypsin. Neuroscience 160: 97-102.
30. Lam DK, Schmidt BL, (2010). Serine proteases and protease-activated receptor 2-dependent allodynia: a novel cancer pain pathway. Pain 149: 263-272.
31. Li L, Fan X, Warner M, Xu XJ, Gustafsson JA, Wiesenfeld-Hallin Z, (2009). Ablation of estrogen receptor alpha or beta eliminates sex differences in mechanical pain threshold in normal and inflamed mice. Pain 143: 37-40.
32. Lindner JR, Kahn ML, Coughlin SR, Sambrano GR, Schauble E, Bernstein D, et-al. (2000). Delayed onset of inflammation in protease-activated receptor-2-deficient mice. J Immunol 165: 6504-6510.
33. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
34. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, et-al. (2007). TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci U S A 104: 13525-13530.
35. Medveczky P, Antal J, Patthy A, Kekesi K, Juhasz G, Szilagyi L, et-al. (2006). Myelin basic protein, an autoantigen in multiple sclerosis, is selectively processed by human trypsin 4. FEBS Lett 580: 545-552.
36. Minn A, Schubert M, Neiss WF, Muller-Hill B, (1998). Enhanced GFAP expression in astrocytes of transgenic mice expressing the human brain-specific trypsinogen IV. Glia 22: 338-347.
37. Nguyen C, Coelho AM, Grady E, Compton SJ, Wallace JL, Hollenberg MD, et-al. (2003). Colitis induced by proteinase-activated receptor-2 agonists is mediated by a neurogenic mechanism. Can J Physiol Pharmacol 81: 920-927.
38. Nyaruhucha CN, Kito M, Fukuoka SI, (1997). Identification and expression of the cDNA-encoding human mesotrypsin(ogen), an isoform of trypsin with inhibitor resistance. J Biol Chem 272: 10573-10578.
39. Nystedt S, Emilsson K, Wahlestedt C, Sundelin J, (1994). Molecular cloning of a potential proteinase activated receptor. Proc Natl Acad Sci U S A 91: 9208-9212.
40. Oikonomopoulou K, Hansen KK, Saifeddine M, Tea I, Blaber M, Blaber SI, et-al. (2006). Proteinase-activated receptors, targets for kallikrein signaling. J Biol Chem 281: 32095-32112.
41. Ossovskaya VS, Bunnett NW, (2004). Protease-activated receptors: contribution to physiology and disease. Physiol Rev 84: 579-621.
42. Poole DP, Amadesi S, Veldhuis NA, Abogadie FC, Lieu T, Darby W, et-al. (2013). Protease-activated receptor 2 (PAR2) protein and transient receptor potential vanilloid 4 (TRPV4) protein coupling is required for sustained inflammatory signaling. J Biol Chem 288: 5790-5802.
43. Ramachandran R, Noorbakhsh F, Defea K, Hollenberg MD, (2012). Targeting proteinase-activated receptors: therapeutic potential and challenges. Nat Rev Drug Discov 11: 69-86.
44. Sahin-Toth M, (2005). Human mesotrypsin defies natural trypsin inhibitors: from passive resistance to active destruction. Protein Pept Lett 12: 457-464.
45. Schick J, Kern H, Scheele G, (1984). Hormonal stimulation in the exocrine pancreas results in coordinate and anticoordinate regulation of protein synthesis. J Cell Biol 99: 1569-1574.
46. Steinhoff M, Corvera CU, Thoma MS, Kong W, McAlpine BE, Caughey GH, et-al. (1999). Proteinase-activated receptor-2 in human skin: tissue distribution and activation of keratinocytes by mast cell tryptase. Exp Dermatol 8: 282-294.
47. Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, Ennes HS, et-al. (2000). Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 6: 151-158.
48. Szmola R, Kukor Z, Sahin-Toth M, (2003). Human mesotrypsin is a unique digestive protease specialized for the degradation of trypsin inhibitors. J Biol Chem 278: 48580-48589.
49. Toth J, Siklodi E, Medveczky P, Gallatz K, Nemeth P, Szilagyi L, et-al. (2007). Regional distribution of human trypsinogen 4 in human brain at mRNA and protein level. Neurochem Res 32: 1423-1433.
50. Vergnolle N, Bunnett NW, Sharkey KA, Brussee V, Compton SJ, Grady EF, et-al. (2001). Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway. Nat Med 7: 821-826.
51. Vergnolle N, Cenac N, Altier C, Cellars L, Chapman K, Zamponi GW, et-al. (2010). A role for transient receptor potential vanilloid 4 in tonicity-induced neurogenic inflammation. Br J Pharmacol 159: 1161-1173.
52. Wang Y, Luo W, Wartmann T, Halangk W, Sahin-Toth M, Reiser G, (2006). Mesotrypsin, a brain trypsin, activates selectively proteinase-activated receptor-1, but not proteinase-activated receptor-2, in rat astrocytes. J Neurochem 99: 759-769.
53. Wiegand U, Corbach S, Minn A, Kang J, Muller-Hill B, (1993). Cloning of the cDNA encoding human brain trypsinogen and characterization of its product. Gene 136: 167-175.
54. Wiesenfeld-Hallin Z, (2005). Sex differences in pain perception. Gender Med 2: 137-145.