Transient receptor potential vanilloid 1: A potential therapeutic target for the treatment of osteoarthritis and rheumatoid arthritis

Zhidong Liao, Muhammad Umar, Xingyun Huang, Ling Qin, Guozhi Xiao, Yan Chen, Liping Tong, Di Chen

PDF
Cell Proliferation ›› 2024, Vol. 57 ›› Issue (3) : e13569. DOI: 10.1111/cpr.13569
REVIEW

Transient receptor potential vanilloid 1: A potential therapeutic target for the treatment of osteoarthritis and rheumatoid arthritis

Author information +
History +

Abstract

This study aims to determine the molecular mechanisms and analgesic effects of transient receptor potential vanilloid 1 (TRPV1) in the treatments of osteoarthritis (OA) and rheumatoid arthritis (RA). We summarize and analyse current studies regarding the biological functions and mechanisms of TRPV1 in arthritis. We search and analyse the related literature in Google Scholar, Web of Science and PubMed databases from inception to September 2023 through the multi-combination of keywords like ‘TRPV1’, ‘ion channel’, ‘osteoarthritis’, ‘rheumatoid arthritis’ and ‘pain’. TRPV1 plays a crucial role in regulating downstream gene expression and maintaining cellular function and homeostasis, especially in chondrocytes, synovial fibroblasts, macrophages and osteoclasts. In addition, TRPV1 is located in sensory nerve endings and plays an important role in nerve sensitization, defunctionalization or central sensitization. TRPV1 is a non-selective cation channel protein. Extensive evidence in recent years has established the significant involvement of TRPV1 in the development of arthritis pain and inflammation, positioning it as a promising therapeutic target for arthritis. TRPV1 likely represents a feasible therapeutic target for the treatment of OA and RA.

Cite this article

Download citation ▾
Zhidong Liao, Muhammad Umar, Xingyun Huang, Ling Qin, Guozhi Xiao, Yan Chen, Liping Tong, Di Chen. Transient receptor potential vanilloid 1: A potential therapeutic target for the treatment of osteoarthritis and rheumatoid arthritis. Cell Proliferation, 2024, 57(3): e13569 https://doi.org/10.1111/cpr.13569

References

[1]
Palazzo C, Nguyen C, Lefevre-Colau MM, et al. Risk factors and burden of osteoarthritis. Ann Phys Rehabil Med. 2016;59:134-138.
[2]
Huang WH, Ong TY, Fu SC, Yung SH. Prevalence of patellofemoral joint osteoarthritis after anterior cruciate ligament injury and associated risk factors: a systematic review. J Orthop Transl. 2020;22:14-25.
[3]
Sharma L. Osteoarthritis of the knee. N Engl J Med. 2021;384:51-59.
[4]
Smolen JS, Aletaha D, Barton A, et al. Rheumatoid arthritis. Nat Rev Dis Primers. 2018;4:18001.
[5]
Pelletier JP, Martel-Pelletier J, Rannou F, Cooper C. Efficacy and safety of oral NSAIDs and analgesics in the management of osteoarthritis: evidence from real-life setting trials and surveys. Semin Arthritis Rheum. 2016;45:S22-S27.
[6]
Zeng C, Wei J, Persson MSM, et al. Relative efficacy and safety of topical non-steroidal anti-inflammatory drugs for osteoarthritis: a systematic review and network meta-analysis of randomised controlled trials and observational studies. Br J Sports Med. 2018;52:642-650.
[7]
Salsitz EA. Chronic pain, chronic opioid addiction: a complex nexus. J Med Toxicol. 2016;12:54-57.
[8]
Ben Mrid R, Bouchmaa N, Ainani H, et al. Anti-rheumatoid drugs advancements: new insights into the molecular treatment of rheumatoid arthritis. Biomed Pharmacother. 2022;151:113126.
[9]
Wei M, Duan DM. Efficacy and safety of monoclonal antibodies targeting interleukin-17 pathway for inflammatory arthritis: a meta-analysis of randomized controlled clinical trials. Drug Des Dev Ther. 2016;10:2771-2777.
[10]
Yuan N, Yu GM, Liv D, et al. An emerging role of interleukin-23 in rheumatoid arthritis. Immunopharm Immunot. 2019;41:185-191.
[11]
Thakur S, Riyaz B, Patil A, et al. Novel drug delivery systems for NSAIDs in management of rheumatoid arthritis: an overview. Biomed Pharmacother. 2018;106:1011-1023.
[12]
Montell C, Rubin GM. Molecular characterization of the drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron. 1989;2:1313-1323.
[13]
Clapham DE. TRP channels as cellular sensors. Nature. 2003;426:517-524.
[14]
Venkatachalam K, Montell C. TRP channels. Annu Rev Biochem. 2007;76:387-417.
[15]
Caterina MJ, Schumacher MA, Tominaga M, et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997;389:816-824.
[16]
Premkumar LS, Sikand P. TRPV1: a target for next generation analgesics. Curr Neuropharmacol. 2008;6:151-163.
[17]
Helyes Z, Szabo A, Nemeth J, et al. Antiinflammatory and analgesic effects of somatostatin released from capsaicin-sensitive sensory nerve terminals in a Freund's adjuvant-induced chronic arthritis model in the rat. Arthritis Rheum. 2004;50:1677-1685.
[18]
Pan YZ, Pan HL. Primary afferent stimulation differentially potentiates excitatory and inhibitory inputs to spinal lamina II outer and inner neurons. J Neurophysiol. 2004;91:2413-2421.
[19]
Mizumura K, Sugiura T, Katanosaka K, et al. Excitation and sensitization of nociceptors by bradykinin: what do we know? Exp Brain Res. 2009;196:53-65.
[20]
Takeba Y, Suzuki N, Takeno M, et al. Modulation of synovial cell function by somatostatin in patients with rheumatoid arthritis. Arthritis Rheum. 1997;40:2128-2138.
[21]
Gavenis K, Schumacher C, Schneider U, et al. Expression of ion channels of the TRP family in articular chondrocytes from osteoarthritic patients: changes between native and in vitro propagated chondrocytes. Mol Cell Biochem. 2009;321:135-143.
[22]
Engler A, Aeschlimann A, Simmen BR, et al. Expression of transient receptor potential vanilloid 1 (TRPV1) in synovial fibroblasts from patients with osteoarthritis and rheumatoid arthritis. Biochem Biophys Res Commun. 2007;359:884-888.
[23]
Kelly S, Chapman RJ, Woodhams S, et al. Increased function of pronociceptive TRPV1 at the level of the joint in a rat model of osteoarthritis pain. Ann Rheum Dis. 2015;74:252-259.
[24]
Lv Z, Xu X, Sun Z, et al. TRPV1 alleviates osteoarthritis by inhibiting M1 macrophage polarization via Ca(2+)/CaMKII/Nrf2 signaling pathway. Cell Death Dis. 2021;12:504.
[25]
Menigoz A, Boudes M. The expression pattern of TRPV1 in brain. J Neurosci. 2011;31:13025-13027.
[26]
Rossi F, Siniscalco D, Luongo L, et al. The endovanilloid/endocannabinoid system in human osteoclasts: possible involvement in bone formation and resorption. Bone. 2009;44:476-484.
[27]
Idris AI, Landao-Bassonga E, Ralston SH. The TRPV1 ion channel antagonist capsazepine inhibits osteoclast and osteoblast differentiation in vitro and ovariectomy induced bone loss in vivo. Bone. 2010;46:1089-1099.
[28]
Honore P, Wismer CT, Mikusa J, et al. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel transient receptor potential type V1 receptor antagonist, relieves pathophysiological pain associated with inflammation and tissue injury in rats. J Pharmacol Exp Ther. 2005;314:410-421.
[29]
Deal CL, Schnitzer TJ, Lipstein E, et al. Treatment of arthritis with topical capsaicin: a double-blind trial. Clin Ther. 1991;13:383-395.
[30]
Anand P, Bley K. Topical capsaicin for pain management: therapeutic potential and mechanisms of action of the new high-concentration capsaicin 8% patch. Br J Anaesth. 2011;107:490-502.
[31]
Webster LR, Peppin JF, Murphy FT, et al. Efficacy, safety, and tolerability of NGX-4010, capsaicin 8% patch, in an open-label study of patients with peripheral neuropathic pain. Diabetes Res Clin Pract. 2011;93:187-197.
[32]
Ghilardi JR, Rohrich H, Lindsay TH, et al. Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain. J Neurosci. 2005;25:3126-3131.
[33]
Keeble J, Russell F, Curtis B, et al. Involvement of transient receptor potential vanilloid 1 in the vascular and hyperalgesic components of joint inflammation. Arthritis Rheum. 2005;52:3248-3256.
[34]
Lv Z, Han J, Li J, et al. Single cell RNA-seq analysis identifies ferroptotic chondrocyte cluster and reveals TRPV1 as an anti-ferroptotic target in osteoarthritis. EBioMedicine. 2022;84:104258.
[35]
Chen D. Osteoarthritis: A complicated joint disease requiring extensive studies with multiple approaches comment. J Orthop Transl. 2022;32:130.
[36]
Teunissen M, Meij BP, Snel L, et al. The catabolic-to-anabolic shift seen in the canine osteoarthritic cartilage treated with knee joint distraction occurs after the distraction period. J Orthop Transl. 2023;38:44-55.
[37]
Yan WQ, Maimaitimin M, Zhao FY, et al. The transplantation of particulated juvenile allograft cartilage and synovium for the repair of meniscal defect in a lapine model. J Orthop Transl. 2022;33:72-89.
[38]
Zhang Y, Jordan JM. Epidemiology of osteoarthritis. Clin Geriatr Med. 2010;26:355-369.
[39]
Martel-Pelletier J, Barr AJ, Cicuttini FM, et al. Osteoarthritis. Nat Rev Dis Primers. 2016;2:16072.
[40]
Sellam J, Berenbaum F. Is osteoarthritis a metabolic disease? Jt Bone Spine. 2013;80:568-573.
[41]
Huang Z, Chen J, Ma J, et al. Effectiveness of low-level laser therapy in patients with knee osteoarthritis: a systematic review and meta-analysis. Osteoarth Cartil. 2015;23:1437-1444.
[42]
Piscitelli P, Iolascon G, di Tanna G, et al. Socioeconomic burden of total joint arthroplasty for symptomatic hip and knee osteoarthritis in the Italian population: a 5-year analysis based on hospitalization records. Arthritis Care Res (Hoboken). 2012;64:1320-1327.
[43]
Huang Z, Ding C, Li T, Yu SP. Current status and future prospects for disease modification in osteoarthritis. Rheumatology (Oxford). 2018;57:iv108-iv123.
[44]
Bodden J, Joseph GB, Schiro S, et al. Opioid users show worse baseline knee osteoarthritis and faster progression of degenerative changes: a retrospective case-control study based on data from the osteoarthritis initiative (OAI). Arthritis Res Ther. 2021;23:146.
[45]
Nelson AE, Allen KD, Golightly YM, et al. A systematic review of recommendations and guidelines for the management of osteoarthritis: the chronic osteoarthritis management initiative of the U.S. bone and joint initiative. Semin Arthritis Rheum. 2014;43:701-712.
[46]
Liu SH, Dube CE, Eaton CB, et al. Longterm effectiveness of intraarticular injections on patient-reported symptoms in knee osteoarthritis. J Rheumatol. 2018;45:1316-1324.
[47]
Wernecke C, Braun HJ, Dragoo JL. The effect of intra-articular corticosteroids on articular cartilage: a systematic review. Orthop J Sports Med. 2015;3:2325967115581163.
[48]
Skou ST, Roos EM, Laursen MB, et al. A randomized, controlled trial of total knee replacement. N Engl J Med. 2015;373:1597-1606.
[49]
Fibel KH, Hillstrom HJ, Halpern BC. State-of-the-art management of knee osteoarthritis. World J Clin Cases. 2015;3:89-101.
[50]
Lundblad H, Kreicbergs A, Jansson KA. Prediction of persistent pain after total knee replacement for osteoarthritis. J Bone Joint Surg Br. 2008;90:166-171.
[51]
Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet. 2010;376:1094-1108.
[52]
McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2011;365:2205-2219.
[53]
Smolen JS, Aletaha D, Koeller M, et al. New therapies for treatment of rheumatoid arthritis. Lancet. 2007;370:1861-1874.
[54]
Weinblatt ME. Efficacy of methotrexate in rheumatoid arthritis. Br J Rheumatol. 1995;34(2):43-48.
[55]
Nishimoto N, Miyasaka N, Yamamoto K, et al. Study of active controlled tocilizumab monotherapy for rheumatoid arthritis patients with an inadequate response to methotrexate (SATORI): significant reduction in disease activity and serum vascular endothelial growth factor by IL-6 receptor inhibition therapy. Mod Rheumatol. 2009;19:12-19.
[56]
Smolen JS, Landewe R, Bijlsma J, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2016 update. Ann Rheum Dis. 2017;76:960-977.
[57]
Spivey CA, Griffith J, Kaplan C, et al. A retrospective analysis of corticosteroid utilization before initiation of biologic DMARDs among patients with rheumatoid arthritis in the United States. Rheumatol Ther. 2018;5:255-270.
[58]
Liou YS, Lin TK, Chen HY, Jong GP. Medications associated with fracture risk in patients with rheumatoid arthritis. Ann Rheum Dis. 2021;80:e140.
[59]
Wang Y, Zhao R, Gu Z, et al. Effects of glucocorticoids on osteoporosis in rheumatoid arthritis: a systematic review and meta-analysis. Osteoporos Int. 2020;31:1401-1409.
[60]
Dunbar RP, Alexiades MM. Decision making in rheumatoid arthritis. Determining surgical priorities. Rheum Dis Clin North Am. 1998;24:35-54.
[61]
Charlier E, Relic B, Deroyer C, et al. Insights on molecular mechanisms of chondrocytes death in osteoarthritis. Int J Mol Sci. 2016;17:2146.
[62]
Kobayashi M, Squires GR, Mousa A, et al. Role of interleukin-1 and tumor necrosis factor alpha in matrix degradation of human osteoarthritic cartilage. Arthritis Rheum. 2005;52:128-135.
[63]
Lefebvre V, Peeters-Joris C, Vaes G. Modulation by interleukin 1 and tumor necrosis factor alpha of production of collagenase, tissue inhibitor of metalloproteinases and collagen types in differentiated and dedifferentiated articular chondrocytes. Biochim Biophys Acta. 1990;1052:366-378.
[64]
Valdes AM, De Wilde G, Doherty SA, et al. The Ile585Val TRPV1 variant is involved in risk of painful knee osteoarthritis. Ann Rheum Dis. 2011;70:1556-1561.
[65]
Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149:1060-1072.
[66]
Yao X, Sun K, Yu S, et al. Chondrocyte ferroptosis contribute to the progression of osteoarthritis. J Orthop Translat. 2021;27:33-43.
[67]
Miao Y, Chen Y, Xue F, et al. Contribution of ferroptosis and GPX4's dual functions to osteoarthritis progression. EBioMedicine. 2022;76:103847.
[68]
Argote PF, Kaplan JT, Poon A, et al. Chondrocyte viability is lost during high-rate impact loading by transfer of amplified strain, but not stress, to pericellular and cellular regions. Osteoarth Cartil. 2019;27:1822-1830.
[69]
Stove J, Huch K, Gunther KP, Scharf HP. Interleukin-1beta induces different gene expression of stromelysin, aggrecan and tumor-necrosis-factor-stimulated gene 6 in human osteoarthritic chondrocytes in vitro. Pathobiology. 2000;68:144-149.
[70]
Hsueh YH, Buddhakosai W, Le PN, et al. Therapeutic effect of induced pluripotent stem cell-derived extracellular vesicles in an in vitro and in vivo osteoarthritis model. J Orthop Translat. 2023;38:141-155.
[71]
Ohtsuki T, Shinaoka A, Kumagishi-Shinaoka K, et al. Mechanical strain attenuates cytokine-induced ADAMTS9 expression via transient receptor potential vanilloid type 1. Exp Cell Res. 2019;383:111556.
[72]
Waning J, Vriens J, Owsianik G, et al. A novel function of capsaicin-sensitive TRPV1 channels: involvement in cell migration. Cell Calcium. 2007;42:17-25.
[73]
Somogyi CS, Matta C, Foldvari Z, et al. Polymodal transient receptor potential Vanilloid (TRPV) ion channels in chondrogenic cells. Int J Mol Sci. 2015;16:18412-18438.
[74]
Philp AM, Davis ET, Jones SW. Developing anti-inflammatory therapeutics for patients with osteoarthritis. Rheumatology (Oxford). 2017;56:869-881.
[75]
Motta F, Barone E, Sica A, Selmi C. Inflammaging and osteoarthritis. Clin Rev Allergy Immunol. 2023;64:222-238.
[76]
MacDonald IJ, Liu SC, Su CM, et al. Implications of angiogenesis involvement in arthritis. Int J Mol Sci. 2018;19:2012.
[77]
Sanchez-Lopez E, Coras R, Torres A, et al. Synovial inflammation in osteoarthritis progression. Nat Rev Rheumatol. 2022;18:258-275.
[78]
Guccione AA, Felson DT, Anderson JJ, et al. The effects of specific medical conditions on the functional limitations of elders in the Framingham study. Am J Public Health. 1994;84:351-358.
[79]
Ayral X, Pickering EH, Woodworth TG, et al. Synovitis: a potential predictive factor of structural progression of medial tibiofemoral knee osteoarthritis—results of a 1 year longitudinal arthroscopic study in 422 patients. Osteoarthritis Cartilage. 2005;13:361-367.
[80]
Ritchlin C. Fibroblast biology. Effector signals released by the synovial fibroblast in arthritis. Arthritis Res. 2000;2:356-360.
[81]
Szabo A, Helyes Z, Sandor K, et al. Role of transient receptor potential vanilloid 1 receptors in adjuvant-induced chronic arthritis: in vivo study using gene-deficient mice. J Pharmacol Exp Ther. 2005;314:111-119.
[82]
Hsieh WS, Kung CC, Huang SL, et al. TDAG8, TRPV1, and ASIC3 involved in establishing hyperalgesic priming in experimental rheumatoid arthritis. Sci Rep. 2017;7:8870.
[83]
Westlund KN, Kochukov MY, Lu Y, McNearney TA. Impact of central and peripheral TRPV1 and ROS levels on proinflammatory mediators and nociceptive behavior. Mol Pain. 2010;6:46.
[84]
Terenzi R, Romano E, Manetti M, et al. Neuropeptides activate TRPV1 in rheumatoid arthritis fibroblast-like synoviocytes and foster IL-6 and IL-8 production. Ann Rheum Dis. 2013;72:1107-1109.
[85]
Hu F, Sun WW, Zhao XT, et al. TRPV1 mediates cell death in rat synovial fibroblasts through calcium entry-dependent ROS production and mitochondrial depolarization. Biochem Biophys Res Commun. 2008;369:989-993.
[86]
Logashina YA, Palikova YA, Palikov VA, et al. Anti-inflammatory and analgesic effects of TRPV1 polypeptide modulator APHC3 in models of osteo- and rheumatoid arthritis. Mar Drugs. 2021;19:39.
[87]
Daghestani HN, Pieper CF, Kraus VB. Soluble macrophage biomarkers indicate inflammatory phenotypes in patients with knee osteoarthritis. Arthritis Rheumatol. 2015;67:956-965.
[88]
Caires R, Luis E, Taberner FJ, et al. Hyaluronan modulates TRPV1 channel opening, reducing peripheral nociceptor activity and pain. Nat Commun. 2015;6:8095.
[89]
Gomis A, Pawlak M, Balazs EA, et al. Effects of different molecular weight elastoviscous hyaluronan solutions on articular nociceptive afferents. Arthritis Rheum. 2004;50:314-326.
[90]
Evanko SP, Tammi MI, Tammi RH, Wight TN. Hyaluronan-dependent pericellular matrix. Adv Drug Deliv Rev. 2007;59:1351-1365.
[91]
Balazs EA, Denlinger JL. Clinical uses of hyaluronan. Ciba Found Symp. 1989;143:265-275. discussion 275–280, 281–265.
[92]
Lieben L, Carmeliet G. The involvement of TRP channels in bone homeostasis. Front Endocrinol (Lausanne). 2012;3:99.
[93]
Henriksen K, Neutzsky-Wulff AV, Bonewald LF, Karsdal MA. Local communication on and within bone controls bone remodeling. Bone. 2009;44:1026-1033.
[94]
Plotkin LI, Gortazar AR, Davis HM, et al. Inhibition of osteocyte apoptosis prevents the increase in osteocytic receptor activator of nuclear factor kappaB ligand (RANKL) but does not stop bone resorption or the loss of bone induced by unloading. J Biol Chem. 2015;290:18934-18942.
[95]
Burr DB. Anatomy and physiology of the mineralized tissues: role in the pathogenesis of osteoarthrosis. Osteoarth Cartil. 2004;12:S20-S30.
[96]
Kovacs B, Vajda E, Nagy EE. Regulatory effects and interactions of the Wnt and OPG-RANKL-RANK signaling at the bone-cartilage interface in osteoarthritis. Int J Mol Sci. 2019;20:4653.
[97]
Takeuchi T, Tanaka Y, Soen S, et al. Effects of the anti-RANKL antibody denosumab on joint structural damage in patients with rheumatoid arthritis treated with conventional synthetic disease-modifying antirheumatic drugs (DESIRABLE study): a randomised, double-blind, placebo-controlled phase 3 trial. Ann Rheum Dis. 2019;78:899-907.
[98]
Lu K, Ma F, Yi D, et al. Molecular signaling in temporomandibular joint osteoarthritis. J Orthop Transl. 2022;32:21-27.
[99]
Rossi F, Bellini G, Torella M, et al. The genetic ablation or pharmacological inhibition of TRPV1 signalling is beneficial for the restoration of quiescent osteoclast activity in ovariectomized mice. Br J Pharmacol. 2014;171:2621-2630.
[100]
He LH, Liu M, He Y, et al. TRPV1 deletion impaired fracture healing and inhibited osteoclast and osteoblast differentiation. Sci Rep. 2017;7:42385.
[101]
Kuroda Y, Hisatsune C, Nakamura T, et al. Osteoblasts induce Ca2+ oscillation-independent NFATc1 activation during osteoclastogenesis. Proc Natl Acad Sci U S A. 2008;105:8643-8648.
[102]
Kun J, Helyes Z, Perkecz A, et al. Effect of surgical and chemical sensory denervation on non-neural expression of the transient receptor potential vanilloid 1 (TRPV1) receptors in the rat. J Mol Neurosci. 2012;48:795-803.
[103]
Kalff KM, El Mouedden M, van Egmond J, et al. Pre-treatment with capsaicin in a rat osteoarthritis model reduces the symptoms of pain and bone damage induced by monosodium iodoacetate. Eur J Pharmacol. 2010;641:108-113.
[104]
Borbely E, Kiss T, Szabadfi K, et al. Complex role of capsaicin-sensitive afferents in the collagen antibody-induced autoimmune arthritis of the mouse. Sci Rep. 2018;8:15916.
[105]
Farr M, Garvey K, Bold AM, et al. Significance of the hydrogen ion concentration in synovial fluid in rheumatoid arthritis. Clin Exp Rheumatol. 1985;3:99-104.
[106]
Zu SQ, Feng YB, Zhu CJ, et al. Acid-sensing ion channel 1a mediates acid-induced pyroptosis through calpain-2/calcineurin pathway in rat articular chondrocytes. Cell Biol Int. 2020;44:2140-2152.
[107]
Tominaga M, Tominaga T. Structure and function of TRPV1. Pflugers Arch. 2005;451:143-150.
[108]
Hu F, Yang S, Zhao D, et al. Moderate extracellular acidification inhibits capsaicin-induced cell death through regulating calcium mobilization, NF-kappaB translocation and ROS production in synoviocytes. Biochem Biophys Res Commun. 2012;424:196-200.
[109]
Reni C, Mangialardi G, Meloni M, Madeddu P. Diabetes stimulates osteoclastogenesis by acidosis-induced activation of transient receptor potential cation channels. Sci Rep. 2016;6:30639.
[110]
Rossi F, Bellini G, Luongo L, et al. The endovanilloid/endocannabinoid system: a new potential target for osteoporosis therapy. Bone. 2011;48:997-1007.
[111]
Caterina MJ, Leffler A, Malmberg AB, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 2000;288:306-313.
[112]
Davis JB, Gray J, Gunthorpe MJ, et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature. 2000;405:183-187.
[113]
Barton NJ, McQueen DS, Thomson D, et al. Attenuation of experimental arthritis in TRPV1R knockout mice. Exp Mol Pathol. 2006;81:166-170.
[114]
Cui M, Honore P, Zhong C, et al. TRPV1 receptors in the CNS play a key role in broad-spectrum analgesia of TRPV1 antagonists. J Neurosci. 2006;26:9385-9393.
[115]
Tominaga M, Caterina MJ, Malmberg AB, et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 1998;21:531-543.
[116]
Morgan M, Nencini S, Thai J, Ivanusic JJ. TRPV1 activation alters the function of Adelta and C fiber sensory neurons that innervate bone. Bone. 2019;123:168-175.
[117]
Cho WG, Valtschanoff JG. Vanilloid receptor TRPV1-positive sensory afferents in the mouse ankle and knee joints. Brain Res. 2008;1219:59-65.
[118]
Ioi H, Kido MA, Zhang JQ, et al. Capsaicin receptor expression in the rat temporomandibular joint. Cell Tissue Res. 2006;325:47-54.
[119]
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.
[120]
Lotz M, Vaughan JH, Carson DA. Effect of neuropeptides on production of inflammatory cytokines by human monocytes. Science. 1988;241:1218-1221.
[121]
McDougall JJ, Karimian SM, Ferrell WR. Prolonged alteration of vasoconstrictor and vasodilator responses in rat knee joints by adjuvant monoarthritis. Exp Physiol. 1995;80:349-357.
[122]
Zhang L, Hoff AO, Wimalawansa SJ, et al. Arthritic calcitonin/alpha calcitonin gene-related peptide knockout mice have reduced nociceptive hypersensitivity. Pain. 2001;89:265-273.
[123]
Schaible HG, Ebersberger A, von Banchet GS. Mechanisms of pain in arthritis. Ann N Y Acad Sci. 2002;966:343-354.
[124]
Holzer P. Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience. 1988;24:739-768.
[125]
Meng J, Ovsepian SV, Wang J, et al. Activation of TRPV1 mediates calcitonin gene-related peptide release, which excites trigeminal sensory neurons and is attenuated by a retargeted botulinum toxin with anti-nociceptive potential. J Neurosci. 2009;29:4981-4992.
[126]
Kim Y, Kim EH, Lee KS, et al. The effects of intra-articular resiniferatoxin on monosodium iodoacetate-induced osteoarthritic pain in rats. Korean J Physiol Pharmacol. 2016;20:129-136.
[127]
Puttfarcken PS, Han P, Joshi SK, et al. A-995662 [(R)-8-(4-methyl-5-(4-(trifluoromethyl)phenyl)oxazol-2-ylamino)-1,2,3,4-tetrahydronaphthalen-2-ol], a novel, selective TRPV1 receptor antagonist, reduces spinal release of glutamate and CGRP in a rat knee joint pain model. Pain. 2010;150:319-326.
[128]
Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain. 2009;10:895-926.
[129]
David-Pereira A, Puga S, Goncalves S, et al. Metabotropic glutamate 5 receptor in the infralimbic cortex contributes to descending pain facilitation in healthy and arthritic animals. Neuroscience. 2016;312:108-119.
[130]
David-Pereira A, Sagalajev B, Wei H, et al. The medullary dorsal reticular nucleus as a relay for descending pronociception induced by the mGluR5 in the rat infralimbic cortex. Neuroscience. 2017;349:341-354.
[131]
Firner M, Greffrath W, Treede RD. Phosphorylation of extracellular signal-related protein kinase is required for rapid facilitation of heat-induced currents in rat dorsal root ganglion neurons. Neuroscience. 2006;143:253-263.
[132]
Cruz CD, Neto FL, Castro-Lopes J, et al. Inhibition of ERK phosphorylation decreases nociceptive behaviour in monoarthritic rats. Pain. 2005;116:411-419.
[133]
Chen Y, Willcockson HH, Valtschanoff JG. Vanilloid receptor TRPV1-mediated phosphorylation of ERK in murine adjuvant arthritis. Osteoarth Cartil. 2009;17:244-251.
[134]
Pan HL, Zhang YQ, Zhao ZQ. Involvement of lysophosphatidic acid in bone cancer pain by potentiation of TRPV1 via PKCepsilon pathway in dorsal root ganglion neurons. Mol Pain. 2010;6:85.
[135]
Lee SY, Lee JH, Kang KK, et al. Sensitization of vanilloid receptor involves an increase in the phosphorylated form of the channel. Arch Pharm Res. 2005;28:405-412.
[136]
Premkumar LS, Ahern GP. Induction of vanilloid receptor channel activity by protein kinase C. Nature. 2000;408:985-990.
[137]
Mandadi S, Tominaga T, Numazaki M, et al. Increased sensitivity of desensitized TRPV1 by PMA occurs through PKCepsilon-mediated phosphorylation at S800. Pain. 2006;123:106-116.
[138]
Koda K, Hyakkoku K, Ogawa K, et al. Sensitization of TRPV1 by protein kinase C in rats with mono-iodoacetate-induced joint pain. Osteoarthr Cartil. 2016;24:1254-1262.
[139]
Lewin GR, Ritter AM, Mendell LM. Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J Neurosci. 1993;13:2136-2148.
[140]
Huang J, Zhang X, McNaughton PA. Inflammatory pain: the cellular basis of heat hyperalgesia. Curr Neuropharmacol. 2006;4:197-206.
[141]
Szolcsanyi J, Sandor Z. Multisteric TRPV1 nocisensor: a target for analgesics. Trends Pharmacol Sci. 2012;33:646-655.
[142]
Kissin EY, Freitas CF, Kissin I. The effects of intraarticular resiniferatoxin in experimental knee-joint arthritis. Anesth Analg. 2005;101:1433-1439.
[143]
Honore P, Chandran P, Hernandez G, et al. Repeated dosing of ABT-102, a potent and selective TRPV1 antagonist, enhances TRPV1-mediated analgesic activity in rodents, but attenuates antagonist-induced hyperthermia. Pain. 2009;142:27-35.
[144]
Chu KL, Chandran P, Joshi SK, et al. TRPV1-related modulation of spinal neuronal activity and behavior in a rat model of osteoarthritic pain. Brain Res. 2011;1369:158-166.
[145]
Okun A, Liu P, Davis P, et al. Afferent drive elicits ongoing pain in a model of advanced osteoarthritis. Pain. 2012;153:924-933.
[146]
Abdullah M, Mahowald ML, Frizelle SP, et al. The effect of intra-articular vanilloid receptor agonists on pain behavior measures in a murine model of acute monoarthritis. J Pain Res. 2016;9:563-570.
[147]
Iadarola MJ, Sapio MR, Raithel SJ, et al. Long-term pain relief in canine osteoarthritis by a single intra-articular injection of resiniferatoxin, a potent TRPV1 agonist. Pain. 2018;159:2105-2114.
[148]
Hwang HS, Park IY, Hong JI, et al. Comparison of joint degeneration and pain in male and female mice in DMM model of osteoarthritis. Osteoarth Cartil. 2021;29:728-738.
[149]
Campbell JN, Stevens R, Hanson P, et al. Injectable capsaicin for the management of pain due to osteoarthritis. Molecules. 2021;26:778.
[150]
Colpaert FC, Donnerer J, Lembeck F. Effects of capsaicin on inflammation and on the substance P content of nervous tissues in rats with adjuvant arthritis. Life Sci. 1983;32:1827-1834.
[151]
Jancso G, Santha P. The foundation of sensory pharmacology: Nicholas (Miklos) Jancso and the Szeged contribution. Temperature (Austin). 2015;2:152-157.
[152]
Szolcsanyi J, Pinter E. Transient receptor potential vanilloid 1 as a therapeutic target in analgesia. Expert Opin Ther Targets. 2013;17:641-657.
[153]
Holzer P. Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol Rev. 1991;43:143-201.
[154]
Jeffry JA, Yu SQ, Sikand P, et al. Selective targeting of TRPV1 expressing sensory nerve terminals in the spinal cord for long lasting analgesia. PLoS One. 2009;4:e7021.
[155]
Yaksh TL, Farb DH, Leeman SE, Jessell TM. Intrathecal capsaicin depletes substance P in the rat spinal cord and produces prolonged thermal analgesia. Science. 1979;206:481-483.
[156]
Brown DC, Iadarola MJ, Perkowski SZ, et al. Physiologic and antinociceptive effects of intrathecal resiniferatoxin in a canine bone cancer model. Anesthesiology. 2005;103:1052-1059.
[157]
Arora V, Campbell JN, Chung MK. Fight fire with fire: neurobiology of capsaicin-induced analgesia for chronic pain. Pharmacol Ther. 2021;220:107743.
[158]
Chung MK, Campbell JN. Use of capsaicin to treat pain: mechanistic and therapeutic considerations. Pharmaceuticals (Basel). 2016;9:66.
[159]
Jancso G, Kiraly E, Joo F, et al. Selective degeneration by capsaicin of a subpopulation of primary sensory neurons in the adult rat. Neurosci Lett. 1985;59:209-214.
[160]
Szolcsanyi J, Jancso-Gabor A, Joo F. Functional and fine structural characteristics of the sensory neuron blocking effect of capsaicin. Naunyn Schmiedebergs Arch Pharmacol. 1975;287:157-169.
[161]
Docherty RJ, Yeats JC, Piper AS. Capsazepine block of voltage-activated calcium channels in adult rat dorsal root ganglion neurones in culture. Br J Pharmacol. 1997;121:1461-1467.
[162]
Liu L, Simon SA. Capsazepine, a vanilloid receptor antagonist, inhibits nicotinic acetylcholine receptors in rat trigeminal ganglia. Neuroscience Letters. 1997;228:29-32.
[163]
Nocerino E, Izzo AA, Borrelli F, et al. Relaxant effect of capsazepine in the isolated rat ileum. N-S Arch Pharmacol. 2002;365:187-192.
[164]
Ahmed M, Bjurholm A, Srinivasan GR, et al. Capsaicin effects on substance P and CGRP in rat adjuvant arthritis. Regul Pept. 1995;55:85-102.
[165]
Miller F, Bjornsson M, Svensson O, Karlsten R. Experiences with an adaptive design for a dose-finding study in patients with osteoarthritis. Contemp Clin Trials. 2014;37:189-199.
[166]
Angeby Moller K, Berge OG, Finn A, et al. Using gait analysis to assess weight bearing in rats with Freund's complete adjuvant-induced monoarthritis to improve predictivity: interfering with the cyclooxygenase and nerve growth factor pathways. Eur J Pharmacol. 2015;756:75-84.
[167]
Malek N, Mrugala M, Makuch W, et al. A multi-target approach for pain treatment: dual inhibition of fatty acid amide hydrolase and TRPV1 in a rat model of osteoarthritis. Pain. 2015;156:890-903.
[168]
Gavva NR, Treanor JJ, Garami A, et al. Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain. 2008;136:202-210.
[169]
Cathcart CJ, Johnston SA, Reynolds LR, et al. Efficacy of ABT-116, an antagonist of transient receptor potential vanilloid type 1, in providing analgesia for dogs with chemically induced synovitis. Am J Vet Res. 2012;73:19-26.
[170]
Round P, Priestley A, Robinson J. An investigation of the safety and pharmacokinetics of the novel TRPV1 antagonist XEN-D0501 in healthy subjects. Br J Clin Pharmacol. 2011;72:921-931.
[171]
Steiner AA, Turek VF, Almeida MC, et al. Nonthermal activation of transient receptor potential vanilloid-1 channels in abdominal viscera tonically inhibits autonomic cold-defense effectors. J Neurosci. 2007;27:7459-7468.
[172]
Iida T, Shimizu I, Nealen ML, et al. Attenuated fever response in mice lacking TRPV1. Neurosci Lett. 2005;378:28-33.
[173]
Zhang WY, Po ALW. The effectiveness of topically applied capsaicin. A meta-analysis. Eur J Clin Pharmacol. 1994;46:517-522.
[174]
Lu M, Chen C, Lan Y, et al. Capsaicin-the major bioactive ingredient of chili peppers: bio-efficacy and delivery systems. Food Funct. 2020;11:2848-2860.
[175]
Iftinca M, Defaye M, Altier C. TRPV1-targeted drugs in development for human pain conditions. Drugs. 2021;81:7-27.
[176]
Chen CC, Chang C, Hsu YH, et al. fMRI indicates cortical activation through TRPV1 modulation during acute gouty attacks. Sci Rep. 2019;9:12348.
[177]
Xu XJ, Farkas-Szallasi T, Lundberg JM, et al. Effects of the capsaicin analogue resiniferatoxin on spinal nociceptive mechanisms in the rat: behavioral, electrophysiological and in situ hybridization studies. Brain Res. 1997;752:52-60.
[178]
Jensen MT, Petersen KL. Gender differences in pain and secondary hyperalgesia after heat/capsaicin sensitization in healthy volunteers. J Pain. 2006;7:211-217.
[179]
Loyd DR, Sun XX, Locke EE, et al. Sex differences in serotonin enhancement of capsaicin-evoked calcitonin gene-related peptide release from human dental pulp. Pain. 2012;153:2061-2067.
[180]
Gazerani P, Andersen OK, Arendt-Nielsen L. Site-specific, dose-dependent, and sex-related responses to the experimental pain model induced by intradermal injection of capsaicin to the foreheads and forearms of healthy humans. J Orofac Pain. 2007;21:289-302.
[181]
Bai X, Zhang X, Zhou Q. Effect of testosterone on TRPV1 expression in a model of orofacial myositis pain in the rat. J Mol Neurosci. 2018;64:93-101.
[182]
Rage M, Van Acker N, Facer P, et al. The time course of CO2 laser-evoked responses and of skin nerve fibre markers after topical capsaicin in human volunteers. Clin Neurophysiol. 2010;121:1256-1266.
[183]
Salas MM, Hargreaves KM, Akopian AN. TRPA1-mediated responses in trigeminal sensory neurons: interaction between TRPA1 and TRPV1. Eur J Neurosci. 2009;29:1568-1578.
[184]
Bautista DM, Movahed P, Hinman A, et al. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci U S A. 2005;102:12248-12252.
[185]
McCleane G. The analgesic efficacy of topical capsaicin is enhanced by glyceryl trinitrate in painful osteoarthritis: a randomized, double blind, placebo controlled study. Eur J Pain. 2000;4:355-360.
[186]
Schnitzer TJ, Pelletier JP, Haselwood DM, et al. Civamide cream 0.075% in patients with osteoarthritis of the knee: a 12-week randomized controlled clinical trial with a longterm extension. J Rheumatol. 2012;39:610-620.
[187]
Mayorga AJ, Flores CM, Trudeau JJ, et al. A randomized study to evaluate the analgesic efficacy of a single dose of the TRPV1 antagonist mavatrep in patients with osteoarthritis. Scand J Pain. 2017;17:134-143.
[188]
Manitpisitkul P, Flores CM, Moyer JA, et al. A multiple-dose double-blind randomized study to evaluate the safety, pharmacokinetics, pharmacodynamics and analgesic efficacy of the TRPV1 antagonist JNJ-39439335 (mavatrep). Scand J Pain. 2018;18:151-164.
[189]
Arsenault P, Chiche D, Brown W, et al. NEO6860, modality-selective TRPV1 antagonist: a randomized, controlled, proof-of-concept trial in patients with osteoarthritis knee pain. Pain Rep. 2018;3:e696.
[190]
Stevens RM, Ervin J, Nezzer J, et al. Randomized, double-blind, placebo-controlled trial of intraarticular trans-capsaicin for pain associated with osteoarthritis of the knee. Arthritis Rheumatol. 2019;71:1524-1533.
[191]
McCarthy GM, McCarty DJ. Effect of topical capsaicin in the therapy of painful osteoarthritis of the hands. J Rheumatol. 1992;19:604-607.
[192]
Persson MSM, Stocks J, Walsh DA, et al. The relative efficacy of topical non-steroidal anti-inflammatory drugs and capsaicin in osteoarthritis: a network meta-analysis of randomised controlled trials. Osteoarthr Cartil. 2018;26:1575-1582.
[193]
Garami A, Shimansky YP, Pakai E, et al. Contributions of different modes of TRPV1 activation to TRPV1 antagonist-induced hyperthermia. J Neurosci. 2010;30:1435-1440.
[194]
Reilly RM, McDonald HA, Puttfarcken PS, et al. Pharmacology of modality-specific transient receptor potential vanilloid-1 antagonists that do not alter body temperature. J Pharmacol Exp Ther. 2012;342:416-428.
[195]
Trevisan G, Hoffmeister C, Rossato MF, et al. Transient receptor potential ankyrin 1 receptor stimulation by hydrogen peroxide is critical to trigger pain during monosodium urate-induced inflammation in rodents. Arthritis Rheum. 2013;65:2984-2995.
[196]
Su KH, Lin SJ, Wei J, et al. The essential role of transient receptor potential vanilloid 1 in simvastatin-induced activation of endothelial nitric oxide synthase and angiogenesis. Acta Physiol (Oxf). 2014;212:191-204.
[197]
Yu YB, Su KH, Kou YR, et al. Role of transient receptor potential vanilloid 1 in regulating erythropoietin-induced activation of endothelial nitric oxide synthase. Acta Physiol (Oxf). 2017;219:465-477.
[198]
Nakanishi M, Morita Y, Hata K, Muragaki Y. Acidic microenvironments induce lymphangiogenesis and IL-8 production via TRPV1 activation in human lymphatic endothelial cells. Exp Cell Res. 2016;345:180-189.
[199]
Ruan GF, Xu JH, Wang K, et al. Associations between serum IL-8 and knee symptoms, joint structures, and cartilage or bone biomarkers in patients with knee osteoarthritis. Clin Rheumatol. 2019;38:3609-3617.
[200]
Solari E, Marcozzi C, Negrini D, Moriondo A. Fluid osmolarity modulates the rate of spontaneous contraction of lymphatic vessels and lymph flow by means of a cooperation between TRPV and VRAC channels. Biology-Basel. 2023;12:1039.
[201]
Li Z, Zhou Y, Li Z. NFKB1 signalling activation contributes to TRPV1 over-expression via repressing MiR-375 and MiR-455: a study on neuropathic low back pain. Folia Biol (Praha). 2022;68:105-111.
[202]
Mottaghitalab F, Rastegari A, Farokhi M, et al. Prospects of siRNA applications in regenerative medicine. Int J Pharm. 2017;524:312-329.
[203]
Benitez-Del-Castillo JM, Moreno-Montanes J, Jimenez-Alfaro I, et al. Safety and efficacy clinical trials for SYL1001, a novel short interfering RNA for the treatment of dry eye disease. Invest Ophthalmol Vis Sci. 2016;57:6447-6454.
[204]
Kasama S, Kawakubo M, Suzuki T, et al. RNA interference-mediated knock-down of transient receptor potential vanilloid 1 prevents forepaw inflammatory hyperalgesia in rat. Eur J Neurosci. 2007;25:2956-2963.
[205]
Zhang S, Zhao J, Meng Q. AAV-mediated siRNA against TRPV1 reduces nociception in a rat model of bone cancer pain. Neurol Res. 2019;41:972-979.
[206]
Akhilesh , Uniyal A, Gadepalli A, et al. Unlocking the potential of TRPV1 based siRNA therapeutics for the treatment of chemotherapy-induced neuropathic pain. Life Sci. 2022;288:120187.

RIGHTS & PERMISSIONS

2023 2023 The Authors. Cell Proliferation published by Beijing Institute for Stem Cell and Regenerative Medicine and John Wiley & Sons Ltd.
PDF

Accesses

Citations

Detail

Sections
Recommended

/