Neurophysiology of arthritis pain

Current Pain and Headache Reports

Volumn 16, Issue 6, 2012, Pages 485-491

  McDougall, Jason J ^a   Linton, Patrick ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Arthritis; Cannabinoids; Cytokines; Joint inflammation; Neurophysiology; Osteoarthritis; Pain; Peripheral nervous system; Proteinase activated receptors; Sodium channel blockers; Therapeutics; Transient receptor potential receptors

Indexed keywords

A 803467; A 889425; CALCITONIN GENE RELATED PEPTIDE; CANNABIDIOL DERIVATIVE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; CYTOKINE; ENDOCANNABINOID; FATTY ACID AMIDASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; O 1602; PROTEINASE ACTIVATED RECEPTOR; SODIUM CHANNEL; SODIUM CHANNEL BLOCKING AGENT; SUBSTANCE P; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1 ANTAGONIST; VOLTAGE GATED SODIUM CHANNEL;

AMNESIA; ANALGESIA; ANALGESIC ACTIVITY; ARTHRALGIA; ARTHRITIS; ARTICLE; BINDING AFFINITY; DEPENDENT PERSONALITY DISORDER; DIZZINESS; DRUG EFFICACY; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG SAFETY; DYSPHORIA; HUMAN; MOTOR DYSFUNCTION; NEUROPATHIC PAIN; NEUROPHYSIOLOGY; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; OSTEOARTHRITIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ARTHRITIS; CYTOKINES; ENDOCANNABINOIDS; HUMANS; NEUROPHYSIOLOGY; PAIN; PERIPHERAL NERVOUS SYSTEM DISEASES; RECEPTORS, PROTEINASE-ACTIVATED; SODIUM CHANNELS; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84870488866     PISSN: 15313433     EISSN: 15343081     Source Type: Journal    
DOI: 10.1007/s11916-012-0300-0     Document Type: Article

References (62)

1. World Health Organization. The burden of musculoskeletal conditions at the start of the new millennium. World Health Organ Tech Rep Ser. 2003;919:1-218.
2. McDougall JJ. Arthritis and pain. Neurogenic origin of joint pain. Arthritis Res Ther. 2006;8:220-9.
3. Hannan MT, Felson DT, Pincus T. Analysis of the discordance between radiographic changes and knee pain in osteoarthritis of the knee. J Rheumatol. 2000;27:1513-17.
4. Lethbridge-Cejku M, Scott Jr WW, Reichle R, Ettinger WH, Zonderman A, Costa P, Plato CC, Tobin JD, Hochberg MC. Association of radiographic features of osteoarthritis of the knee with knee pain: data from the Baltimore Longitudinal Study of Aging. Arthritis Care Res. 1995;8:182-8.
5. McDougall JJ, Andruski B, Schuelert N, Hallgrimsson B, Matyas Jr. Unravelling the relationship between age, nociception and joint destruction in naturally occurring osteoarthritis of Dunkin Hartley guinea pigs. Pain. 2009;141:222-32. This study showed for the first time a lack of correlation between joint degeneration and nociception in an animal model of spontaneous OA.
6. Schuelert N, McDougall JJ. Cannabinoid-mediated antinociception is enhanced in rat osteoarthritic knees. Arthritis and Rheum. 2008;58:145-53.
7. Devane WA, Dysarz 3rd FA, Johnson MR, Melvin LS, Howlett AC. Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol. 1988;34:605-13.
8. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature. 1990;346:561-4.
9. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature. 1993;365:61-5.
10. Baker CL, McDougall JJ. The cannabinomimetic arachidonyl-2- chloroethylamide (ACEA) acts on capsaicin-sensitive TRPV1 receptors but not cannabinoid receptors in rat joints. Br J Pharmacol. 2004;142:1361-7.
11. McDougall JJ, Yu V, Thomson J. In vivo effects of CB2 receptorselective cannabinoids on the vasculature of normal and arthritic rat knee joints. Br J Pharmacol. 2008;153:358-66.
12. Schuelert N, Zhang C,Mogg AJ, Broad LM, Hepburn DL, Nisenbaum ES, Johnson MP, McDougall JJ. Paradoxical effects of the cannabinoid CB2 receptor agonist GW405833 on rat osteoarthritic knee joint pain. Osteoarthr Cartil. 2010;18:1536-43.
13. Carlini EA. The good and the bad effects of (-) trans-delta-9- tetrahydrocannabinol (Delta 9-THC) on humans. Toxicon. 2004;44:461-7.
14. Degenhardt L, Hall WD. The adverse effects of cannabinoids: implications for use of medical marijuana. CMAJ. 2008;178: 1685-6.
15. Leweke FM, Koethe D. Cannabis and psychiatric disorders: it is not only addiction. Addict Biol. 2008;13:264-75.
16. Wang T, Collet JP, Shapiro S, Ware MA. Adverse effects of medical cannabinoids: a systematic review. CMAJ. 2008;178: 1669-78.
17. Di Marzo V. Endocannabinoids: synthesis and degradation. Rev Physiol Biochem Pharmacol. 2008;160:1-24.
18. Deutsch DG, Ueda N, Yamamoto S. The fatty acid amide hydrolase (FAAH). Prostaglandins Leukot Essent Fatty Acids. 2002;66:201-10.
19. Schuelert N, Johnson MP, Oskins JL, Jassal K, Chambers MG, McDougall JJ. Local application of the endocannabinoid hydrolysis inhibitor URB597 reduces nociception in spontaneous and chemically induced models of osteoarthritis. Pain. 2011;152:975-77. This study gave the first indication that endocannabinoids could be promoted in osteoarthritic joints leading to analgesia.
20. Pertwee RG. GPR55: a new member of the cannabinoid receptor clan? Br J Pharmacol. 2007;152:984-6.
21. Lauckner JE, Jensen JB, Chen HY, Lu HC, Hille B, Mackie K. GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits M current. Proc Natl Acad Sci U S A. 2008;105: 2699-704.
22. Staton PC, Hatcher JP, Walker DJ, Morrison AD, Shapland EM, Hughes JP, Chong E, Mander PK, Green PJ, Billinton A, Fulleylove M, Lancaster HC, Smith JC, Bailey LT,Wise A, Brown AJ, Richardson JC, Chessell IP. The putative cannabinoid receptor GPR55 plays a role in mechanical hyperalgesia associated with inflammatory and neuropathic pain. Pain. 2008;139:225-36.
23. Ryberg E, Larsson N, Sjogren S, Hjorth S, Hermansson NO, Leonova J, Elebring T, Nilsson K, Drmota T, Greasley PJ. The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol. 2007;152:1092-101.
24. Schuelert N, McDougall JJ. The abnormal cannabidiol analogue O-1602 reduces nociception in a rat model of acute arthritis via the putative cannabinoid receptorGPR55.Neurosci Lett. 2011;500:72-6.
25. Jones SA, Richards PJ, Scheller J, Rose-John S. IL-6 transsignaling: the in vivo consequences. J Interferon Cytokine Res. 2005;25: 241-53.
26. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. The proand anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta. 2011;1813:878-88.
27. Arvidson NG, Gudbjornsson B, Elfman L, Ryden AC, Totterman TH, Hallgren R. Circadian rhythm of serum interleukin-6 in rheumatoid arthritis. Ann Rheum Dis. 1994;53:521-4.
28. De Benedetti F, Massa M, Pignatti P, Albani S, Novick D, Martini A. Serum soluble interleukin 6 (IL-6) receptor and IL-6/soluble IL-6 receptor complex in systemic juvenile rheumatoid arthritis. J Clin Invest. 1994;93:2114-19.
29. Desgeorges A, Gabay C, Silacci P, Novick D, Roux-Lombard P, Grau G, Dayer JM, Vischer T, Guerne PA. Concentrations and origins of soluble interleukin 6 receptor-alpha in serum and synovial fluid. J Rheumatol. 1997;24:1510-16.
30. Vazquez E, Kahlenbach J, von Segond Banchet G, Konig C, Schaible HG, Ebersberger A. Spinal interleukin-6 is an amplifier of arthritic pain in the rat. Arthritis Rheum. 2012;64:2233-42.
31. 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. 2005;52:3248-56.
32. Eid SR, Crown ED, Moore EL, Liang HA, Choong KC, Dima S, Henze DA, Kane SA, Urban MO. HC-030031, a TRPA1 selective antagonist, attenuates inflammatory-and neuropathy-induced mechanical hypersensitivity. Mol Pain. 2008;4:48.
33. Petrus M, Peier AM, Bandell M, Hwang SW, Huynh T, Olney N, Jegla T, Patapoutian A. A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol Pain. 2007;3:40.
34. Fernihough J, Gentry C, Bevan S, Winter J. Regulation of calcitonin gene-related peptide and TRPV1 in a rat model of osteoarthritis. Neurosci Lett. 2005;388:75-80.
35. Chu KL, Chandran P, Joshi SK, Jarvis MF, Kym PR, McGaraughty S. TRPV1-related modulation of spinal neuronal activity and behavior in a rat model of osteoarthritic pain. Brain Res. 2011;1369: 158-66.
36. Kim H, Neubert JK, San Miguel A, Xu K, Krishnaraju RK, Iadarola MJ, Goldman D, Dionne RA. Genetic influence on variability in human acute experimental pain sensitivity associated with gender, ethnicity and psychological temperament. Pain. 2004;109:488-96.
37. Valdes AM, De Wilde G, Doherty SA, Lories RJ, Vaughn FL, Laslett LL, Maciewicz RA, Soni A, Hart DJ, Zhang W, Muir KR, Dennison EM, Wheeler M, Leaverton P, Cooper C, Spector TD, Cicuttini FM, Chapman V, Jones G, Arden NK, Doherty M. The Ile585Val TRPV1 variant is involved in risk of painful knee osteoarthritis. Ann Rheum Dis. 2011;70:1556-61.
38. Fernandes ES, Russell FA, Spina D, McDougall JJ, Graepel R, Gentry C, Staniland AA, Mountford DM, Keeble JE, Malcangio M, Bevan S, Brain SD. A distinct role for transient receptor potential ankyrin 1, in addition to transient receptor potential vanilloid 1, in tumor necrosis factor alpha-induced inflammatory hyperalgesia and Freund's complete adjuvant-induced monarthritis. Arthritis Rheum. 2011;63:819-29.
39. Russell FA, McDougall JJ. Proteinase activated receptor (PAR) involvement in mediating arthritis pain and inflammation. Inflamm Res. 2009;58(3):119-26.
40. Russell FA, Schuelert N, Veldhoen VE, Hollenberg MD, McDougall JJ. Proteinase-activated receptor-2 (PAR(2)) activation sensitises primary afferents and causes leukocyte rolling and adherence in the rat knee joint. Br J Pharmacol. doi:10.1111/j.1476-5381.2012.02120.x.
41. Russell FA, Veldhoen VE, Tchitchkan D, McDougall JJ. Proteinase-activated receptor-4 (PAR4) activation leads to sensitization of rat joint primary afferents via a bradykinin B2 receptordependent mechanism. J Neurophysiol. 2010;103:155-63.
42. 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;17:161-70.
43. McDougall JJ, Schuelert N, Bowyer J. Cathepsin K inhibition reduces CTXII levels and joint pain in the guinea pig model of spontaneous osteoarthritis. Osteoarthr Cartil. 2010;18:1355-7.
44. Helyes Z, Sandor K, Borbely E, Tekus V, Pinter E, Elekes K, Toth DM, Szolcsanyi J, McDougall JJ. Involvement of transient receptor potential vanilloid 1 receptors in protease-activated receptor-2-induced joint inflammation and nociception. Eur J Pain. 2010;14: 351-8.
45. 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. 2009;60:728-37.
46. Russell FA, Zhan S, Dumas A, Lagarde S, Pouliot M, McDougall JJ. The pronociceptive effect of proteinase-activated receptor-4 stimulation in rat knee joints is dependent on mast cell activation. Pain. 2011;152:354-60.
47. Amir R, Argoff CE, Bennett GJ, Cummins TR, Durieux ME, Gerner P, Gold MS, Porreca F, Strichartz GR. The role of sodium channels in chronic inflammatory and neuropathic pain. J Pain. 2006;7(5 Suppl 3):S1-29.
48. Akopian AN, Sivilotti L, Wood JN. A tetrodotoxin-resistant voltage-gated sodiumchannel expressed by sensory neurons. Nature. 1996;379:257-62.
49. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, Smith A, Kerr BJ, McMahon SB, Boyce S, Hill R, Stanfa LC, Dickenson AH, Wood JN. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci. 1999;2:541-8.
50. Strickland IT, Martindale JC, Woodhams PL, Reeve AJ, Chessell IP, McQueen DS. Changes in the expression of NaV1.7, NaV1.8 and NaV1.9 in a distinct population of dorsal root ganglia innervating the rat knee joint in a model of chronic inflammatory joint pain. Eur J Pain. 2008;12:564-72.
51. Karaman Y, Kayali C, Ozturk H, Kaya A, Bor C. A comparison of analgesic effect of intra-articular levobupivacaine with bupivacaine following knee arthroscopy. SaudiMed J. 2009;30:629-32.
52. Araujo MC, Sinnott CJ, Strichartz GR. Multiple phases of relief from experimental mechanical allodynia by systemic lidocaine: responses to early and late infusions. Pain. 2003;103:21-9.
53. Kastrup J, Petersen P, Dejgard A, Angelo HR, Hilsted J. Intravenous lidocaine infusion-A new treatment of chronic painful diabetic neuropathy? Pain. 1987;28:69-75.
54. Kinloch RA, Cox PJ. New targets for neuropathic pain therapeutics. Expert Opin Ther Targets. 2005;9:685-98.
55. Schuelert N, McDougall JJ. Involvement of Nav 1.8 sodium ion channels in the transduction of mechanical pain in a rodent model of osteoarthritis. Arthritis Res Ther. 2012;14:R5.
56. Jarvis MF, Honore P, Shieh CC, Chapman M, Joshi S, Zhang XF, Kort M, Carroll W, Marron B, Atkinson R, Thomas J, Liu D, Krambis M, Liu Y, McGaraughty S, Chu K, Roeloffs R, Zhong C, Mikusa JP, Hernandez G, Gauvin D, Wade C, Zhu C, Pai M, ScanioM, Shi L, Drizin I, Gregg R,MatulenkoM, Hakeem A, Gross M, Johnson M, Marsh K, Wagoner PK, Sullivan JP, Faltynek CR, Krafte DS. A-803467, a potent and selective Nav1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat. Proc Natl Acad Sci U S A. 2007;104:8520-5.
57. Coggeshall RE, Tate S, Carlton SM. Differential expression of tetrodotoxin-resistant sodium channels Nav1.8 and Nav1.9 in normal and inflamed rats. Neurosci Lett. 2004;355:45-8.
58. McDougall JJ, Bray RC, Sharkey KA. A morphological and immunohistochemical examination of nerves in normal and injured collateral ligaments of rat, rabbit and human knee joints. Anat Rec. 1997;248:29-39.
59. McDougall JJ, Yeung G, Leonard CA, Bray RC. A rôle for calcitonin gene-related peptide in rabbit knee joint ligament healing. Can J Physiol Pharmacol. 2000;78:535-40.
60. Grönblad M, Konntinen YT, Korkala O, Liesi P, Hukkanen M, Polak JM. Neuropeptides in the synovium of patients with rheumatoid arthritis and osteoarthritis. J Rheumatol. 1988;15: 1807-10.
61. Hanesch U, McDougall JJ, Pawlak M. Inhibitory effects of gabapentin on rat articular afferent mechanosensitivity. Regul Pept. 2000;89:63.
62. Orita S, Ishikawa T, Miyagi M, Ochiai N, Inoue G, Eguchi Y, Kamoda H, Arai G, Toyone T, Aoki Y, Kubo T, Takahashi K, Ohtori S. Pain-related sensory innervation in monoiodoacetateinduced osteoarthritis in rat knees that gradually develops neuronal injury in addition to inflammatory pain. BMC Musculoskelet Disord. 2011;12:134.