Proteinase-activated receptor-4 (PAR4) activation leads to sensitization of rat joint primary afferents via a bradykinin B2 receptor-dependent mechanism

Journal of Neurophysiology

Volumn 103, Issue 1, 2010, Pages 155-163

  Russell, Fiona A ^a   Veldhoen, Victoria E ^a   Tchitchkan, Dmitri ^a   McDougall, Jason J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYKININ B2 RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 4;

ANIMAL TISSUE; ARTHRITIS; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; JOINT; KNEE; MALE; NERVE CONDUCTION; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION; SPINAL GANGLION;

ACTION POTENTIALS; ADRENERGIC BETA-ANTAGONISTS; ANILIDES; ANIMALS; BRADYKININ; CINNAMATES; GANGLIA, SPINAL; KNEE JOINT; MALE; MOVEMENT; NEURONS, AFFERENT; OLIGOPEPTIDES; PAIN; RATS; RATS, WISTAR; RECEPTOR, BRADYKININ B2; RECEPTORS, THROMBIN; ROTATION; SENSORY RECEPTOR CELLS; TRPV CATION CHANNELS;

EID: 74049135647     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00486.2009     Document Type: Article

References (41)

1. Amadesi S, Cottrell GS, Divino L, Chapman K, Grady EF, Bautista F, Karanjia R, Barajas-Lopez C, Vanner S, Vergnolle N, Bunnett NW. Protease-activated receptor 2 sensitizes TRPV1 by protein kinase C-epsilon-and A-dependent mechanisms in rats and mice. J Physiol 575: 555-571, 2006.
2. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M, Manni C, Geppetti P, McRoberts JA, Ennes H, Davis JB, Mayer EA, Bunnett NW. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 24: 4300-4312, 2004.
3. 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 135: 1101-1106, 2002.
4. Asfaha S, Cenac N, Houle S, Altier C, Papez MD, Nguyen C, Steinhoff M, Chapman K, Zamponi GW, Vergnolle N. Protease-activated receptor-4: a novel mechanism of inflammatory pain modulation. BrJPharmacol 150: 176-185, 2007.
5. Auge C, Balz-Hara D, Steinhoff M, Vergnolle N, and Cenac N. Protease-activated receptor-4 (PAR(4)): a role as inhibitor of visceral pain and hypersensitivity. Neurogastroenterol Motil 2009. Epub ahead of print.
6. Cocks TM, Moffatt JD. Protease-activated receptors: sentries for inflammation? Trends Pharmacol Sci 21: 103-108, 2000.
7. Cottrell GS, Amadesi S, Grady EF, Bunnett NW. Trypsin IV, a novel agonist of protease-activated receptors 2 and 4. J Biol Chem 279: 13532-13539, 2004.
8. 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 162: 907-923, 2003.
9. Dai Y, Moriyama T, Higashi T, Togashi K, Kobayashi K, Yamanaka H, Tominaga M, Noguchi K. Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 24: 4293-4299, 2004.
10. Dai Y, Wang S, Tominaga M, Yamamoto S, Fukuoka T, Higashi T, Kobayashi K, Obata K, Yamanaka H, Noguchi K. Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin-Invest 117: 1979-1987, 2007.
11. 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 275: 19728-19734, 2000.
12. Grant AD, Cottrell GS, Amadesi S, Trevisani M, Nicoletti P, Materazzi S, Altier C, Cenac N, Zamponi GW, Bautista-Cruz F, Lopez CB, Joseph EK, Levine JD, Liedtke W, Vanner S, Vergnolle N, Geppetti P, Bunnett NW. Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol 578: 715-733, 2007.
13. Han JS, Bird GC, Li W, Jones J, Neugebauer V. Computerized analysis of audible and ultrasonic vocalizations of rats as a standardized measure of pain-related behavior. J Neurosci Methods 141: 261-269, 2005.
14. Hollenberg MD and Compton SJ. International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev 54: 203-217, 2002.
15. 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 143: 443-454, 2004.
16. 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 146: 670-678, 2005.
17. Ivanavicius SP, Blake DR, Chessell IP, Mapp PI. Isolectin B4 binding neurons are not present in the rat knee joint. Neuroscience 128: 555-560, 2004.
18. Just S, Pawlak M, Heppelmann B. Responses of fine primary afferent nerve fibres innervating the rat knee joint to defined torque. J Neurosci Methods 103: 157-162, 2000.
19. Kanaka R, Schaible HG, Schmidt RF. Activation of fine articular afferent units by bradykinin. Brain Res 327: 81-90, 1985.
20. Kaplan AP, Joseph K, Silverberg M. Pathways for bradykinin formation and inflammatory disease. J Allergy Clin Immunol 109: 195-209, 2002.
21. Kataoka H, Hamilton JR, McKemy DD, Camerer E, Zheng YW, Cheng A, Griffin C, Coughlin SR. Protease-activated receptors 1 and 4 mediate thrombin signaling in endothelial cells. Blood 102: 3224-3231, 2003.
22. Kawabata A, Kawao N, Kuroda R, Tanaka A, Shimada C. The PAR-1-activating peptide attenuates carrageenan-induced hyperalgesia in rats. Peptides 23: 1181-1183, 2002.
23. Keeble J, Russell F, Curtis B, Starr A, Pinter E, Brain SD. Involvement of transient receptor potential vanilloid 1 in the vascular and hyperalgesic components of joint inflammation. Arthritis Rheum 52: 3248-3256, 2005.
24. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. Proteinase-activated receptors. Pharmacol Rev 53: 245-282, 2001.
25. Maggi CA, Meli A. Suitability of urethan anesthesia for physiopharmacological investigations in various systems. I. General considerations. Experientia 42: 109-114, 1986.
26. McDougall JJ. Arthritis and pain. Neurogenic origin of joint pain. Arthritis Res Therapy 8: 220, 2006.
27. McDougall JJ, Pawlak M, Hanesch U, Schmidt RF. Peripheral modulation of rat knee joint afferent mechanosensitivity by nociceptin/orphanin FQ. Neurosci Lett 288: 123-126, 2000.
28. McDougall JJ, Zhang C, Cellars L, Joubert E, Dixon CM, Vergnolle N. Triggering of proteinase-activated receptor 4 leads to joint pain and inflammation in mice. Arthritis Rheum 60: 728-737, 2009.
29. Neugebauer V, Schaible HG, Schmidt RF. Sensitization of articular afferents to mechanical stimuli by bradykinin. Pfluegers 415: 330-335, 1989.
30. Paszcuk AF, Quintao NL, Fernandes ES, Juliano L, Chapman K, Andrade-Gordon P, Campos MM, Vergnolle N, Calixto JB. Mechanisms underlying the nociceptive and inflammatory responses induced by trypsin in the mouse paw. Eur J Pharmacol 581: 204-215, 2008.
31. Russell FA, Fernandes ES, Courade JP, Keeble JE, Brain SD. Tumour necrosis factor alpha mediates transient receptor potential vanilloid 1-dependent bilateral thermal hyperalgesia with distinct peripheral roles of interleukin-1beta, protein kinase C and cyclooxygenase-2 signalling. Pain 142: 264-274, 2009.
32. Russell FA, McDougall JJ. Proteinase activated receptor (PAR) involvement in mediating arthritis pain and inflammation. Inflamm Res 58: 119-126, 2009.
33. Salo PT, Theriault E. Number, distribution and neuropeptide content of rat knee joint afferents. J Anat 190: 515-522, 1997.
34. Schmued LC, Fallon JH. Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377: 147-154, 1986.
35. Shpacovitch V, Feld M, Bunnett NW, Steinhoff M. Protease-activated receptors: novel PARtners in innate immunity. Trends Immunol 28: 541-550, 2007.
36. Steranka LR, Manning DC, DeHaas CJ, Ferkany JW, Borosky SA, Connor JR, Vavrek RJ, Stewart JM, Snyder SH. Bradykinin as a pain mediator: receptors are localized to sensory neurons and antagonists have analgesic actions. Proc Natl Acad Sci USA 85: 3245-3249, 1988.
37. Tominaga M, Caterina MJ. Thermosensation and pain. J Neurobiol 61: 3-12, 2004.
38. Varga A, Nemeth J, Szabo A, McDougall JJ, Zhang C, Elekes K, Pinter E, Szolcsanyi J, Helyes Z. Effects of the novel TRPV1 receptor antagonist SB366791 in vitro and in vivo in the rat. Neurosci Lett 385: 137-142, 2005.
39. 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 169: 1467-1473, 2002.
40. Wiedow O, Meyer-Hoffert U. Neutrophil serine proteases: potential key regulators of cell signalling during inflammation. J Intern Med 257: 319-328, 2005.
41. Zhu WJ, Yamanaka H, Obata K, Dai Y, Kobayashi K, Kozai T, Tokunaga A, Noguchi K. Expression of mRNA for four subtypes of the proteinase-activated receptor in rat dorsal root ganglia. Brain Res 1041: 205-211, 2005.