PAIN
Volume 149, Issue 2 , Pages 263-272 , May 2010

Serine proteases and protease-activated receptor 2-dependent allodynia: A novel cancer pain pathway

  • D.K. Lam
  • ,
  • B.L. Schmidt

      Affiliations

    • Corresponding Author InformationCorresponding author. Address: Department of Oral and Maxillofacial Surgery, C-522 University of California – San Francisco, San Francisco, CA 94143-0440, USA. Tel.: +1 415 502 3297; fax: +1 415 476 6305.

Received 22 July 2009 ,Revised 5 February 2010 ,Accepted 5 February 2010.

References 

  1. Amadesi S, Cottrell GS, Divino L, Chapman K, Grady EF, Bautista F, et al. Protease-activated receptor 2 sensitizes TRPV1 by protein kinase Cε- and A-dependent mechanisms in rats and mice. J Physiol. 2006;575:555–571
  2. Aromando RF, Pérez MA, Heber EM, Trivillin VA, Tomasi VH, Schwint AE, et al. Potential role of mast cells in hamster cheek pouch carcinogenesis. Oral Oncol. 2008;44:1080–1087
  3. Bjordal K, Ahlner-Elmqvist M, Hammerlid E, Boysen M, Evensen JF, Biörklund A, et al. A prospective study of quality of life in head and neck cancer patients. Part II: Longitudinal data. Laryngoscope. 2001;111:1440–1452
  4. Brasseur L. Review of current pharmacologic treatment of pain. Drugs. 1997;53:10–17
  5. Cenac N, Andrews CN, Holzhausen M, Chapman K, Cottrell G, Andrade-Gordon P, et al. Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest. 2007;117:636–647
  6. Chen X, Tanner K, Levine JD. Mechanical sensitization of cutaneous C-fiber nociceptors by prostaglandin E2 in the rat. Neurosci Lett. 1999;267:105–108
  7. Connelly ST, Schmidt BL. Evaluation of pain in patients with oral squamous cell carcinoma. J Pain. 2004;5:505–510
  8. Dai Y, Moriyama T, Higashi T, Togashi K, Kobayashi K, Yamanaka H, 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
  9. D’Andrea MR, Derian CK, Santulli RJ, Andrade-Gordon P. Differential expression of protease-activated receptors-1 and -2 in stromal fibroblasts of normal, benign, and malignant human tissues. Am J Pathol. 2001;158:2031–2041
  10. Darmoul D, Marie J-C, Devaud H, Gratio V, Laburthe M. Initiation of human colon cancer cell proliferation by trypsin acting at protease-activated receptor-2. Brit J Cancer. 2001;85:772–779
  11. Dattilio A, Vizzard MA. Up-regulation of protease activated receptors in bladder after cyclophosphamide induced cystitis and colocalization with capsaicin receptor (VR1) in bladder nerve fibers. J Urol. 2005;173:635–639
  12. Diener KM. Bisphosphonates for controlling pain from metastatic bone disease. Am J Health Syst Pharm. 1996;53:1917–1927
  13. Eisenstein TK, Hilburger ME. Opioid modulation of immune responses: effects on phagocyte and lymphoid cell populations. J Neuroimmunol. 1998;83:36–44
  14. Eisenstein TK, Rogers TJ, Meissler JJ, Adler MW, Hilburger ME. Morphine depresses macrophage numbers and function in mouse spleens. Adv Exp Med Biol. 1998;437:33–41
  15. Ferrell WR, Lockhart JC, Kelso EB, Dunning L, Plevin R, Meek SE, et al. Essential role for proteinase activated receptor-2 in arthritis. J Clin Invest. 2003;111:35–41
  16. Foley KM, Gelband H. Improving palliative care for cancer: Summary and recommendations. Washington (DC): National Academies Press; 2001;
  17. Fujii K, Imamura S. Cell surface proteolysis by serine proteinases enhances RGD-sensitive melanoma cell adhesion on fibrinogen and vitronectin. Exp. Cell Res. 1995;220:201–211
  18. Fujita T, Matsui M, Takaku K, Uetake H, Ichikawa W, Taketo MM, et al. Size- and invasion-dependent increase in cyclooxygenase 2 levels in human colorectal carcinomas. Cancer Res. 1998;58:4823–4826
  19. Grant AD, Cottrell GS, Amadesi S, Trevisani M, Nicoletti P, Materazzi 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
  20. Grobelny D, Poncz L, Galardy RE. Inhibition of human skin fibroblast collagenase, thermolysin, and Pseudomonas aeriginosa elastase by peptide hydroxamic acids. Biochemistry. 1992;31:7152–7154
  21. Guerrero AV, Quang P, Dekker N, Jordan RC, Schmidt BL. Peripheral cannabinoids attenuate carcinoma-induced nociception in mice. Neurosci Lett. 2008;433:77–81
  22. Hammerlid E, Bjordal K, Ahlner-Elmqvist M, Boysen M, Evensen JF, Biörklund A, et al. A prospective study of quality of life in head and neck cancer patients. Part I: at diagnosis. Laryngoscope. 2001;111:669–680
  23. He S, Aslam A, Gaça MD, He Y, Buckley MG, Hollenberg MD, et al. Inhibitors of tryptase as mast cell-stabilizing agents in the human airways: effects of tryptase and other agonists of proteinase-activated receptor 2 on histamine release. J Pharmacol Exp Ther. 2004;309:119–126
  24. Hoogerwerf WA, Zou L, Shenoy M, Sun D, Micci MA, Lee-Hellmich H, et al. The proteinase-activated receptor 2 is involved in nociception. J Neurosci. 2001;21:9036–9042
  25. Hoogerwerf WA, Shenoy M, Winston JH, Xiao SY, He Z, Pasricha PJ. Trypsin mediates nociception via the proteinase-activated receptor 2: a potentially novel role in pancreatic pain. Gastroenterology. 2004;127:883–891
  26. Ichikawa Y, Koshikawa N, Hasegawa S, Ishikawa T, Momiyama N, Kunizaki C, et al. Marked increase of trypsin(ogen) in serum of linitis plastica (gastric cancer, borrmann 4) patients. Clin Cancer Res. 2000;6:1385–1388
  27. Ishikura H, Nishimura S, Matsunami M, Tsujiuchi T, Ishiki T, Sekiguchi F, et al. The proteinase inhibitor camostat mesilate suppresses pancreatic pain in rodents. Life Sci. 2007;80:1999–2004
  28. Jin G, Hayashi T, Kawagoe J, Takizawa T, Nagata T, Nagano I, et al. Deficiency of PAR-2 gene increases acute focal ischemic brain injury. J Cereb Blood Flow Metab. 2005;25:302–313
  29. Jung TT, Berlinger NT, Juhn SK. Prostaglandins in squamous cell carcinoma of the head and neck: a preliminary study. Laryngoscope. 1985;95:307–312
  30. Kawabata A, Kawao N, Itoh H, Shimada C, Takebe K, Kuroda R, 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
  31. Kawabata A, Kuroda R, Minami T, Kataoka K, Taneda M. Increased vascular permeability by a specific agonist of protease-activated receptor-2 in rat hindpaw. Br J Pharmacol. 1998;125:419–422
  32. Kelso EB, Lockhart JC, Hembrough T, Dunning L, Plevin R, Hollenberg MD, et al. Therapeutic promise of proteinase-activated receptor-2 antagonism in joint inflammation. J Pharmacol Exp Ther. 2006;316:1017–1024
  33. Knight DA, Lim S, Scaffidi AK, Roche N, Chung KF, Stewar GA, et al. Protease-activated receptors in human airways: upregulation of PAR-2 in respiratory epithelium from patients with asthma. J Allergy Clin Immunol. 2001;108:797–803
  34. Kolokythas A, Connelly ST, Schmidt BL. Validation of the University of California San Francisco oral cancer pain questionnaire. J Pain. 2007;8:950–953
  35. Koshikawa N, Hasegawa S, Nagashima Y, Mitsuhashi K, Tsubota Y, Miyata S, et al. Expression of trypsin by epithelial cells of various tissues, leukocytes, and neurons in human and mouse. Am J Pathol. 1998;153:937–944
  36. Koshikawa N, Nagashima Y, Miyagi Y, Mizushima H, Yanoma S, Yasumitsu H, et al. Expression of trypsin in vascular endothelial cells. FEBS Lett. 1997;409:442–448
  37. List MA, Stracks J, Colangelo L, Butler P, Ganzenko N, Lundy D, et al. How do head and neck cancer patients prioritize treatment outcomes before initiating treatment?. J Clin Oncol. 2000;18:877–884
  38. MacFarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. Proteinase-activated receptor. Pharmacol Rev. 2001;53:245–282
  39. Mantyh PW, Clohisy DR, Koltzenburg M, Hunt SP. Molecular mechanisms of cancer pain. Nat Rev Cancer. 2002;2:201–209
  40. Mayrhofer G. Fixation and staining of granules in mucosal mast cells and intraepithelial lymphocytes in the rat jejunum with specimen reference to the relationship between the acid glycosaminoglycans in the two cell types. Histochem J. 1980;12:513–526
  41. Mercadante S, Portenoy RK. Opioid poorly-responsive cancer pain. Part 3. Clinical strategies to improve opioid responsiveness. J Pain Symptom Manage. 2001;21:338–354
  42. Mercadante S. Malignant bone pain: pathophysiology and treatment. Pain. 1997;69:1–18
  43. Metcalfe DD, Baram D, Mekori YA. Mast cells. Physiol Rev. 1997;77:1033–1079
  44. Noorbakhsh F, Vergnolle N, Hollenberg MD, Power C. Proteinase-activated receptors in the nervous system. Nat Rev Neurosci. 2003;4:981–990
  45. Noorbakhsh F, Vergnolle N, McArthur JC, Silva C, Vodjgani M, Andrade-Gordon P, et al. Proteinase activated receptor-2 induction by neuroinflammation prevents neuronal death during HIV infection. J Immunol. 2005;174:7320–7329
  46. Nyberg P, Ylipalosaari M, Sorsa T, Salo T. Trypsins and their role in carcinoma growth. Exp Cell Res. 2006;312:1219–1228
  47. 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
  48. Ossovskaya VS, Bunnett NW. Protease-activated receptors: contribution to physiology and disease. Physiol Rev. 2004;84:579–621
  49. Pacharinsak C, Beitz A. Animal models of cancer pain. Comp Med. 2008;58:220–233
  50. Paszcuk AF, Quintão NL, Fernandes ES, Juliano L, Chapman K, Andrade-Gordon P, et al. Mechanisms underlying the nociceptive and inflammatory responses induced by trypsin in the mouse paw. Eur J Pharmacol. 2008;581:204–215
  51. Patwardhan AM, Diogenes A, Berg KA, Fehrenbacher JC, Clarke WP, Akopian AN, et al. PAR-2 agonists activate trigeminal nociceptors and induce functional competence in the delta opioid receptor. Pain. 2006;125:114–124
  52. Portenoy RK, Payne D, Jacobsen P. Breakthrough pain: characteristics and impact in patients with cancer pain. Pain. 1999;81:129–134
  53. Ritchie E, Saka M, Mackenzie C, Drummond R, Wheeler-Jones C, Kanke T, et al. Cytokine upregulation of proteinase-activated-receptors 2 and 4 expression mediated by p38 MAP kinase and inhibitory kappa B kinase beta in human endothelial cells. Br J Pharmacol. 2007;150:1044–1054
  54. Schmidlin F, Bunnett NW. Protease-activated receptors: how proteases signal to cells. Curr Opin Pharmacol. 2001;1:575–582
  55. Sorge J. The lesson from cancer pain. Eur J Pain. 2000;4:3–7
  56. Striggow F, Riek-Burchardt M, Kiesel A, Schmidt W, Henrich-Noack P, Breder J, et al. Four different types of protease-activated receptors are widely expressed in the brain and are upregulated in hippocampus by severe ischemia. Eur J Neurosci. 2001;14:595–608
  57. Sumitani K, Kamijo R, Toyoshima T, Nakanishi Y, Takizawa K, Hatori M, et al. Specific inhibition of cyclooxygenase-2 results in inhibition of proliferation of oral cancer cell lines via suppression of prostaglandin E2 production. J Oral Pathol Med. 2001;30:41–47
  58. Taiwo YO, Goetzl EJ, Levine JD. Hyperalgesia onset latency suggests a hierarchy of action. Brain Res. 1987;423:333–337
  59. Taiwo YO, Bjerknes LK, Goetzl EJ, Levine JD. Mediation of primary afferent peripheral hyperalgesia by the cAMP second messenger system. Neurosci. 1989;32:577–580
  60. Vergnolle N, Bunnett NW, Sharkey KA, Brussee V, Compton SJ, Grady EF, et al. Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway. Nat Med. 2001;7:821–826
  61. Yoshii M, Jikuhara A, Mori S, Iwagaki H, Takahashi HK, Nishibori M, et al. Mast cell tryptase stimulates DLD-1 carcinoma through prostaglandin and MAP kinase-dependent manners. J Pharmacol Sci. 2005;98:450–458
  62. Zhu WJ, Dai Y, Fukuoka T, Yamanaka H, Kobayashi K, Obata K, et al. Agonist of proteinase-activated receptor 2 increases painful behavior produced by alpha, beta-methylene adenosine 5′-triphosphate. Neuroreport. 2006;17:1257–1261
  63. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983;16:109–110

PII: S0304-3959(10)00085-0

doi: 10.1016/j.pain.2010.02.010

PAIN
Volume 149, Issue 2 , Pages 263-272 , May 2010