Proteinase activated receptor (PAR) involvement in mediating arthritis pain and inflammation

Inflammation Research

Volumn 58, Issue 3, 2009, Pages 119-126

  Russell, F A ^a   McDougall, J J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; ENMD 1068; HIRUDIN; INTERLEUKIN 1BETA; N 3 METHYLBUTYRYL N 6 AMINOHEXANOYL PIPERAZINE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; RANTES; SERINE PROTEINASE; THROMBIN; THROMBIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTHRALGIA; ARTHRITIS; CYTOKINE RELEASE; DRUG INHIBITION; FIBRIN FORMATION; FIBROBLAST; HUMAN; KNOCKOUT MOUSE; MACROPHAGE; MAST CELL; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NOCICEPTION; NONHUMAN; OSTEOARTHRITIS; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; RHEUMATOID ARTHRITIS;

ANIMALS; ARTHRITIS; HUMANS; INFLAMMATION; PAIN; PEPTIDE HYDROLASES; PROTEIN ISOFORMS; RECEPTORS, PROTEINASE-ACTIVATED; SIGNAL TRANSDUCTION;

EID: 60849134552     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-009-8087-0     Document Type: Review

References (82)

1. Hollenberg MD, Compton SJ. International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev 2002; 54: 203-217.
2. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. Proteinase-activated receptors. Pharmacol Rev 2001; 53: 245-282.
3. Vu TK, Hung DT, Wheaton VI, Coughlin SR. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 1991; 64: 1057-1068.
4. Ossovskaya VS, Bunnett NW. Protease-activated receptors: contribution to physiology and disease. Physiol Rev 2004; 84: 579-621.
5. Shapiro MJ, Weiss EJ, Faruqi TR, Coughlin SR. Protease-activated receptors 1 and 4 are shut off with distinct kinetics after activation by thrombin. J Biol Chem 2000; 275: 25216-25221.
6. Camerer E, Kataoka H, Kahn M, Lease K, Coughlin SR. Genetic evidence that protease-activated receptors mediate factor Xa signaling in endothelial cells. J Biol Chem 2002; 277: 16081-16087.
7. Connolly AJ, Ishihara H, Kahn ML, Farese RV, Jr., Coughlin SR. Role of the thrombin receptor in development and evidence for a second receptor. Nature 1996; 381: 516-519.
8. Ishihara H, Connolly AJ, Zeng D et al. Protease-activated receptor 3 is a second thrombin receptor in humans. Nature 1997; 386: 502-506.
9. Hansen KK, Saifeddine M, Hollenberg MD. Tethered ligand-derived peptides of proteinase-activated receptor 3 (PAR3) activate PAR1 and PAR2 in Jurkat T cells. Immunology 2004; 112: 183-190.
10. Kahn ML, Zheng YW, Huang W et al. A dual thrombin receptor system for platelet activation. Nature 1998; 394: 690-694.
11. Nakanishi-Matsui M, Zheng YW, Sulciner DJ, Weiss EJ, Ludeman MJ, Coughlin SR. PAR3 is a cofactor for PAR4 activation by thrombin. Nature 2000; 404: 609-613.
12. Owen WG. PAR-3 is a low-affinity substrate, high affinity effector of thrombin. Biochem Biophys Res Commun 2003; 305: 166-168.
13. Schmidt VA, Nierman WC, Maglott DR et al. The human proteinase-activated receptor-3 (PAR-3) gene. Identification within a Par gene cluster and characterization in vascular endothelial cells and platelets. J Biol Chem 1998; 273: 15061-15068.
14. McLaughlin JN, Patterson MM, Malik AB. Protease-activated receptor-3 (PAR3) regulates PAR1 signaling by receptor dimerization. Proc Natl Acad Sci U S A 2007; 104: 5662-5667.
15. Bretschneider E, Spanbroek R, Lotzer K, Habenicht AJ, Schror K. Evidence for functionally active protease-activated receptor-3 (PAR-3) in human vascular smooth muscle cells. Thromb Haemost 2003; 90: 704-709.
16. Xu WF, Andersen H, Whitmore TE et al. Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci U S A 1998; 95: 6642-6646.
17. Sambrano GR, Huang W, Faruqi T, Mahrus S, Craik C, Coughlin SR. Cathepsin G activates protease-activated receptor-4 in human platelets. J Biol Chem 2000; 275: 6819-6823.
18. Cottrell GS, Amadesi S, Grady EF, Bunnett NW. Trypsin IV, a novel agonist of protease-activated receptors 2 and 4. J Biol Chem 2004; 279: 13532-13539.
19. 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.
20. Faruqi TR, Weiss EJ, Shapiro MJ, Huang W, Coughlin SR. Structure-function analysis of protease-activated receptor 4 tethered ligand peptides. Determinants of specificity and utility in assays of receptor function. J Biol Chem 2000; 275: 19728-19734.
21. Mari B, Imbert V, Belhacene N et al. Thrombin and thrombin receptor agonist peptide induce early events of T cell activation and synergize with TCR cross-linking for CD69 expression and interleukin 2 production. J Biol Chem 1994; 269: 8517-8523.
22. Naldini A, Sower L, Bocci V, Meyers B, Carney DH. Thrombin receptor expression and responsiveness of human monocytic cells to thrombin is linked to interferon-induced cellular differentiation. J Cell Physiol 1998; 177: 76-84.
23. Cirino G, Cicala C, Bucci MR, Sorrentino L, Maraganore JM, Stone SR. Thrombin functions as an inflammatory mediator through activation of its receptor. J Exp Med 1996; 183: 821-827.
24. D'Andrea MR, Rogahn CJ, ndrade-Gordon P. Localization of protease-activated receptors-1 and -2 in human mast cells: indications for an amplified mast cell degranulation cascade. Biotech Histochem 2000; 75: 85-90.
25. de GL, Vergnolle N, Young SH et al. Agonists of proteinase-activated receptor 1 induce plasma extravasation by a neurogenic mechanism. Br J Pharmacol 2001; 133: 975-987.
26. Vergnolle N, Hollenberg MD, Wallace JL. Pro- and anti-inflammatory actions of thrombin: a distinct role for proteinase-activated receptor-1 (PAR1). Br J Pharmacol 1999; 126: 1262-1268.
27. Vergnolle N, Derian CK, D'Andrea MR, Steinhoff M, ndrade-Gordon P. Characterization of thrombin-induced leukocyte rolling and adherence: a potential proinflammatory role for proteinase-activated receptor-4. J Immunol 2002; 169: 1467-1473.
28. Knecht W, Cottrell GS, Amadesi S et al. Trypsin IV or mesotrypsin and p23 cleave protease-activated receptors 1 and 2 to induce inflammation and hyperalgesia. J Biol Chem 2007; 282: 26089-26100.
29. Vergnolle N, Cellars L, Mencarelli A et al. A role for proteinase-activated receptor-1 in inflammatory bowel diseases. J Clin Invest 2004; 114: 1444-1456.
30. Cenac N, Cellars L, Steinhoff M et al. Proteinase-activated receptor-1 is an anti-inflammatory signal for colitis mediated by a type 2 immune response. Inflamm Bowel Dis 2005; 11: 792-798.
31. Saban R, D'Andrea MR, ndrade-Gordon P et al. Mandatory role of proteinase-activated receptor 1 in experimental bladder inflammation. BMC Physiol 2007; 7: 4.
32. Renesto P, Si-Tahar M, Moniatte M et al. Specific inhibition of thrombin-induced cell activation by the neutrophil proteinases elastase, cathepsin G, and proteinase 3: evidence for distinct cleavage sites within the aminoterminal domain of the thrombin receptor. Blood 1997; 89: 1944-1953.
33. Uehara A, Sugawara S, Muramoto K, Takada H. Activation of human oral epithelial cells by neutrophil proteinase 3 through protease-activated receptor-2. J Immunol 2002; 169: 4594-4603.
34. Vergnolle N, Ferazzini M, D'Andrea MR, Buddenkotte J, Steinhoff M. Proteinase-activated receptors: novel signals for peripheral nerves. Trends Neurosci 2003; 26: 496-500.
35. Nystedt S, Ramakrishnan V, Sundelin J. The proteinase-activated receptor 2 is induced by inflammatory mediators in human endothelial cells. Comparison with the thrombin receptor. J Biol Chem 1996; 271: 14910-14915.
36. Vergnolle N, Hollenberg MD, Sharkey KA, Wallace JL. Characterization of the inflammatory response to proteinase-activated receptor-2 (PAR2)-activating peptides in the rat paw. Br J Pharmacol 1999; 127: 1083-1090.
37. Shpacovitch VM, Brzoska T, Buddenkotte J et al. Agonists of proteinase-activated receptor 2 induce cytokine release and activation of nuclear transcription factor kappaB in human dermal microvascular endothelial cells. J Invest Dermatol 2002; 118: 380-385.
38. Lindner JR, Kahn ML, Coughlin SR et al. Delayed onset of inflammation in protease-activated receptor-2-deficient mice. J Immunol 2000; 165: 6504-6510.
39. Steinhoff M, Vergnolle N, Young SH et al. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 2000; 6: 151-158.
40. Palmer HS, Kelso EB, Lockhart JC et al. Protease-activated receptor 2 mediates the proinflammatory effects of synovial mast cells. Arthritis Rheum 2007; 56: 3532-3540.
41. Kong W, McConalogue K, Khitin LM et al. Luminal trypsin may regulate enterocytes through proteinase-activated receptor 2. Proc Natl Acad Sci U S A 1997; 94: 8884-8889.
42. Oikonomopoulou K, Hansen KK, Saifeddine M et al. Proteinase-activated receptors, targets for kallikrein signaling. J Biol Chem 2006; 281: 32095-32112.
43. D'Andrea MR, Saban MR, Nguyen NB, ndrade-Gordon P, Saban R. Expression of protease-activated receptor-1, -2, -3, and -4 in control and experimentally inflamed mouse bladder. Am J Pathol 2003; 162: 907-923.
44. Hollenberg MD, Saifeddine M, Sandhu S, Houle S, Vergnolle N. Proteinase-activated receptor-4: evaluation of tethered ligand-derived peptides as probes for receptor function and as inflammatory agonists in vivo. Br J Pharmacol 2004; 143: 443-454.
45. Houle S, Papez MD, Ferazzini M, Hollenberg MD, Vergnolle N. Neutrophils and the kallikrein-kinin system in proteinase-activated receptor 4-mediated inflammation in rodents. Br J Pharmacol 2005; 146: 670-678.
46. Slofstra SH, Bijlsma MF, Groot AP et al. Protease-activated receptor-4 inhibition protects from multiorgan failure in a murine model of systemic inflammation. Blood 2007; 110: 3176-3182.
47. Asokananthan N, Graham PT, Fink J et al. Activation of protease-activated receptor (PAR)-1, PAR-2, and PAR-4 stimulates IL-6, IL-8, and prostaglandin E2 release from human respiratory epithelial cells. J Immunol 2002; 168: 3577-3585.
48. Asfaha S, Brussee V, Chapman K, Zochodne DW, Vergnolle N. Proteinase-activated receptor-1 agonists attenuate nociception in response to noxious stimuli. Br J Pharmacol 2002; 135: 1101-1106.
49. Kawabata A, Kawao N, Kuroda R, Tanaka A, Shimada C. The PAR-1-activating peptide attenuates carrageenan-induced hyperalgesia in rats. Peptides 2002; 23: 1181-1183.
50. Vergnolle N, Bunnett NW, Sharkey KA et al. Proteinase-activated receptor-2 and hyperalgesia: A novel pain pathway. Nat Med 2001; 7: 821-826.
51. Kawabata A, Kawao N, Kuroda R, Tanaka A, Itoh H, Nishikawa H. Peripheral PAR-2 triggers thermal hyperalgesia and nociceptive responses in rats. Neuroreport 2001; 12: 715-719.
52. Kawabata A, Kawao N, Itoh H et al. Role of N-methyl-D-aspartate receptors and the nitric oxide pathway in nociception/hyperalgesia elicited by protease-activated receptor-2 activation in mice and rats. Neurosci Lett 2002; 329: 349-353.
53. Amadesi S, Nie J, Vergnolle N et al. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 2004; 24: 4300-4312.
54. Amadesi S, Cottrell GS, Divino L et al. Protease-activated receptor 2 sensitizes TRPV1 by protein kinase Cepsilon- and A-dependent mechanisms in rats and mice. J Physiol 2006; 575: 555-571.
55. Dai Y, Moriyama T, Higashi T et al. Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 2004; 24: 4293-4299.
56. Alier KA, Endicott JA, Stemkowski PL et al. Intrathecal Administration of Proteinase-Activated Receptor-2 Agonists Produces Hyperalgesia by Exciting the Cell Bodies of Primary Sensory Neurons. J Pharmacol Exp Ther 2007.
57. 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.
58. Dai Y, Wang S, Tominaga M et al. Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 2007; 117: 1979-1987.
59. Coelho AM, Vergnolle N, Guiard B, Fioramonti J, Bueno L. Proteinases and proteinase-activated receptor 2: a possible role to promote visceral hyperalgesia in rats. Gastroenterology 2002; 122: 1035-1047.
60. 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.
61. Zhu WJ, Yamanaka H, Obata K et al. Expression of mRNA for four subtypes of the proteinase-activated receptor in rat dorsal root ganglia. Brain Res 2005; 1041: 205-211.
62. Asfaha S, Cenac N, Houle S et al. Protease-activated receptor-4: a novel mechanism of inflammatory pain modulation. Br J Pharmacol 2007; 150: 176-185.
63. McDougall JJ. Arthritis and pain. Neurogenic origin of joint pain. Arthritis Res Ther 2006;8: 220.
64. Pelletier JP, Martel-Pelletier J, Abramson SB. Osteoarthritis, an inflammatory disease: potential implication for the selection of new therapeutic targets. Arthritis Rheum 2001; 44: 1237-1247.
65. Lavery JP, Lisse JR. Preliminary study of the tryptase levels in the synovial fluid of patients with inflammatory arthritis. Ann Allergy 1994; 72: 425-427.
66. Nakano S, Ikata T, Kinoshita I, Kanematsu J, Yasuoka S. Characteristics of the protease activity in synovial fluid from patients with rheumatoid arthritis and osteoarthritis. Clin Exp Rheumatol 1999; 17: 161-170.
67. Marty I, Peclat V, Kirdaite G, Salvi R, So A, Busso N. Amelioration of collagen-induced arthritis by thrombin inhibition. J Clin Invest 2001; 107: 631-640.
68. Varisco PA, Peclat V, van NK, Bischof-Delaloye A, So A, Busso N. Effect of thrombin inhibition on synovial inflammation in antigen induced arthritis. Ann Rheum Dis 2000; 59: 781-787.
69. Morris R, Winyard PG, Brass LF, Blake DR, Morris CJ. Thrombin receptor expression in rheumatoid and osteoarthritic synovial tissue. Ann Rheum Dis 1996; 55: 841-843.
70. Hirano F, Kobayashi A, Hirano Y, Nomura Y, Fukawa E, Makino I. Thrombin-induced expression of RANTES mRNA through protease activated receptor-1 in human synovial fibroblasts. Ann Rheum Dis 2002; 61: 834-837.
71. Yang YH, Hall P, Little CB et al. Reduction of arthritis severity in protease-activated receptor-deficient mice. Arthritis Rheum 2005; 52: 1325-1332.
72. Ferrell WR, Lockhart JC, Kelso EB et al. Essential role for proteinase-activated receptor-2 in arthritis. J Clin Invest 2003; 111:35-41.
73. Xiang Y, Masuko-Hongo K, Sekine T et al. Expression of proteinase-activated receptors (PAR)-2 in articular chondrocytes is modulated by IL-1beta, TNF-alpha and TGF-beta. Osteoarthritis Cartilage 2006; 14: 1163-1173.
74. Busso N, Frasnelli M, Feifel R et al. Evaluation of protease-activated receptor 2 in murine models of arthritis. Arthritis Rheum 2007; 56: 101-107.
75. Nakano S, Mishiro T, Takahara S et al. Distinct expression of mast cell tryptase and protease activated receptor-2 in synovia of rheumatoid arthritis and osteoarthritis. Clin Rheumatol 2007; 26: 1284-1292.
76. Kelso EB, Lockhart JC, Hembrough T et al. Therapeutic promise of proteinase-activated receptor-2 antagonism in joint inflammation. J Pharmacol Exp Ther 2006; 316: 1017-1024.
77. Kelso EB, Ferrell WR, Lockhart JC et al. Expression and proinflammatory role of proteinase-activated receptor 2 in rheumatoid synovium: ex vivo studies using a novel proteinase-activated receptor 2 antagonist. Arthritis Rheum 2007; 56: 765-771.
78. Breedveld FC, Kalden JR. Appropriate and effective management of rheumatoid arthritis. Ann Rheum Dis 2004; 63: 627-633.
79. Mc Dougall, J.J. Involvement of proteinase-activated receptor-4 in inflammatory joint disease. Inflammation Research 2007; 56: S354.
80. th Annual Meeting of the European Neuropeptide Club, Santorini, Greece 2007.
81. Busso N, Chobaz-Peclat V, Hamilton J, Spee P, Wagtmann N, So A. Essential role of platelet activation via PAR-4 in tissue factor-initiated inflammation. Arthritis Res Ther. 2008 Apr 15; 10: R42.
82. Busso N, Peclat V, Van Ness K, Kolodziesczyk E, Degen J, Bugge T, et al. Exacerbation of antigen-induced arthritis in urokinase-deficient mice. J Clin Invest. 1998 Jul 1; 102: 41-50.