Pain in Rheumatoid Arthritis: Models and Mechanisms

References

• Heiberg T , FinsetA , UhligT , KvienTK . Seven year changes in health status and priorities for improvement of health in patients with rheumatoid arthritis . Ann. Rheum. Dis.64 ( 2 ), 191 – 195 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Klooster ten PM , VeehofMM , TaalE , van RielPLCM , van de LaarMAFJ . Changes in priorities for improvement in patients with rheumatoid arthritis during 1 year of anti-tumour necrosis factor treatment . Ann. Rheum. Dis.66 ( 11 ), 1485 – 1490 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Rantapää-Dahlqvist S , de JongBAW , BerglinEet al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis . Arthritis Rheum.48 ( 10 ), 2741 – 2749 ( 2003 ).
   PubMedGoogle Scholar
• Nielen MM , van SchaardenburgD , ReesinkHWet al. Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors . Arthritis Rheum.50 ( 2 ), 380 – 386 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Bos WH , WolbinkGJ , BoersMet al. Arthritis development in patients with arthralgia is strongly associated with anti-citrullinated protein antibody status: a prospective cohort study . Ann. Rheum. Dis.69 ( 3 ), 490 – 494 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• van de Stadt LA , de KoningMHMT , van de StadtRJet al. Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis . Arthritis Rheum.63 ( 11 ), 3226 – 3233 ( 2011 ).
   PubMedGoogle Scholar
• Roche PA , KlestovAC , HeimHM . Description of stable pain in rheumatoid arthritis: a 6 year study . J. Rheumatol.30 ( 8 ), 1733 – 1738 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Koop SM , Klooster tenPM , VonkemanHE , SteunebrinkLMM , van de LaarMAFJ . Neuropathic-like pain features and cross-sectional associations in rheumatoid arthritis . Arthritis Res. Ther.17 ( 1 ), 237 ( 2015 ).
   PubMedGoogle Scholar
• Welsing PM , FransenJ , van RielPL . Is the disease course of rheumatoid arthritis becoming milder? Time trends since 1985 in an inception cohort of early rheumatoid arthritis . Arthritis Rheum.52 ( 9 ), 2616 – 2624 ( 2005 ).
   PubMedGoogle Scholar
• Lee YC , FritsML , IannacconeCKet al. Subgrouping of patients with rheumatoid arthritis based on pain, fatigue, inflammation, and psychosocial factors . Arthritis Rheumatol.66 ( 8 ), 2006 – 2014 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Taylor P , MangerB , Alvaro-GraciaJet al. Patient perceptions concerning pain management in the treatment of rheumatoid arthritis . J. Int. Med. Res.38 ( 4 ), 1213 – 1224 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Lee YC , CuiJ , LuBet al. Pain persists in DAS28 rheumatoid arthritis remission but not in ACR/EULAR remission: a longitudinal observational study . Arthritis Res. Ther.13 ( 3 ), R83 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Schipper LG , van HulstLTC , GrolR , van RielPLCM , HulscherMEJL , FransenJ . Meta-analysis of tight control strategies in rheumatoid arthritis: protocolized treatment has additional value with respect to the clinical outcome . Rheumatology (Oxford)49 ( 11 ), 2154 – 2164 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Durham CO , FowlerT , DonatoA , SmithW , JensenE . Pain management in patients with rheumatoid arthritis . Nurse Pract.40 ( 5 ), 38 – 45 ( 2015 ).
   PubMedGoogle Scholar
• Ahlqvist E , HultqvistM , HolmdahlR . The value of animal models in predicting genetic susceptibility to complex diseases such as rheumatoid arthritis . Arthritis Res. Ther.11 ( 3 ), 226 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Hu Y , ChengW , CaiW , YueY , LiJ , ZhangP . Advances in research on animal models of rheumatoid arthritis . Clin. Rheumatol.32 ( 2 ), 161 – 165 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Inglis JJ , NotleyCA , EssexDet al. Collagen-induced arthritis as a model of hyperalgesia: functional and cellular analysis of the analgesic actions of tumor necrosis factor blockade . Arthritis Rheum.56 ( 12 ), 4015 – 4023 ( 2007 ).
   PubMedGoogle Scholar
• Marinova-Mutafchieva L , WilliamsRO , MasonLJ , MauriC , FeldmannM , MainiRN . Dynamics of proinflammatory cytokine expression in the joints of mice with collagen-induced arthritis (CIA) . Clin. Exp. Immunol.107 ( 3 ), 507 – 512 ( 1997 ).
   PubMed Web of Science ®Google Scholar
• Gao XH , GaoR , TianYZet al. A store-operated calcium channel inhibitor attenuates collagen-induced arthritis . Br. J. Pharmacol.172 ( 12 ), 2991 – 3002 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Boettger MK , HensellekS , RichterFet al. Antinociceptive effects of tumor necrosis factor alpha neutralization in a rat model of antigen-induced arthritis: evidence of a neuronal target . Arthritis Rheum.58 ( 8 ), 2368 – 2378 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Ebbinghaus M , UhligB , RichterFet al. The role of interleukin-1β in arthritic pain: main involvement in thermal, but not mechanical, hyperalgesia in rat antigen-induced arthritis . Arthritis Rheum.64 ( 12 ), 3897 – 3907 ( 2012 ).
   PubMedGoogle Scholar
• Cunha TM , VerriWA , ValérioDAet al. Role of cytokines in mediating mechanical hypernociception in a model of delayed-type hypersensitivity in mice . Eur. J. Pain12 ( 8 ), 1059 – 1068 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Pinto LG , CunhaTM , VieiraSMet al. IL-17 mediates articular hypernociception in antigen-induced arthritis in mice . Pain148 ( 2 ), 247 – 256 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Verri WA , GuerreroATG , FukadaSYet al. IL-33 mediates antigen-induced cutaneous and articular hypernociception in mice . Proc. Natl Acad. Sci. USA105 ( 7 ), 2723 – 2728 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Richter F , NaturaG , EbbinghausMet al. Interleukin-17 sensitizes joint nociceptors to mechanical stimuli and contributes to arthritic pain through neuronal interleukin-17 receptors in rodents . Arthritis Rheum.64 ( 12 ), 4125 – 4134 ( 2012 ).
   PubMedGoogle Scholar
• Sachs D , CoelhoFM , CostaVVet al. Cooperative role of tumour necrosis factor-α, interleukin-1β and neutrophils in a novel behavioural model that concomitantly demonstrates articular inflammation and hypernociception in mice . Br. J. Pharmacol.162 ( 1 ), 72 – 83 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Banchet von GS , PetrowPK , BräuerR , SchaibleHG . Monoarticular antigen-induced arthritis leads to pronounced bilateral upregulation of the expression of neurokinin 1 and bradykinin 2 receptors in dorsal root ganglion neurons of rats . Arthritis Res.2 ( 5 ), 424 – 427 ( 2000 ).
   PubMedGoogle Scholar
• Khodorova A , MontmayeurJP , StrichartzG . Endothelin receptors and pain . J. Pain10 ( 1 ), 4 – 28 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Massier J , EitnerA , Segond von BanchetG , SchaibleH-G . Effects of differently activated rodent macrophages on sensory neurons: implications for arthritis pain . Arthritis Rheumatol.67 ( 8 ), 2263 – 2272 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Segond von Banchet G , BoettgerMK , FischerN , GajdaM , BräuerR , SchaibleH-G . Experimental arthritis causes tumor necrosis factor-alpha-dependent infiltration of macrophages into rat dorsal root ganglia which correlates with pain-related behavior . Pain145 ( 1 ), 151 – 159 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Su J , GaoT , ShiTet al. Phenotypic changes in dorsal root ganglion and spinal cord in the collagen antibody-induced arthritis mouse model . J. Comp. Neurol.523 ( 10 ), 1505 – 1528 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Makino A , SakaiA , ItoH , SuzukiH . Involvement of tachykinins and NK1 receptor in the joint inflammation with collagen type II-specific monoclonal antibody-induced arthritis in mice . J. Nippon. Med. Sch.79 ( 2 ), 129 – 138 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Sluka KA , RasmussenLA , EdgarMMet al. Acid-sensing ion channel 3 deficiency increases inflammation but decreases pain behavior in murine arthritis . Arthritis Rheum.65 ( 5 ), 1194 – 1202 ( 2013 ).
   PubMedGoogle Scholar
• Christianson CA , CorrM , FiresteinGS , MobarghaA , YakshTL , SvenssonCI . Characterization of the acute and persistent pain state present in K/BxN serum transfer arthritis . Pain151 ( 2 ), 394 – 403 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Borbély É , BotzB , BölcskeiKet al. Capsaicin-sensitive sensory nerves exert complex regulatory functions in the serum-transfer mouse model of autoimmune arthritis . Brain Behav. Immun.45 , 50 – 59 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Botz B , BölcskeiK , KereskaiLet al. Differential regulatory role of pituitary adenylate cyclase-activating polypeptide in the serum-transfer arthritis model . Arthritis Rheumatol.66 ( 10 ), 2739 – 2750 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Clark AK , GristJ , Al-KashiA , PerrettiM , MalcangioM . Spinal cathepsin S and fractalkine contribute to chronic pain in the collagen-induced arthritis model . Arthritis Rheum.64 ( 6 ), 2038 – 2047 ( 2012 ).
   PubMedGoogle Scholar
• Nieto FR , ClarkAK , GristJ , ChapmanV , MalcangioM . Calcitonin gene-related peptide expressing sensory neurons and spinal microglial reactivity contribute to pain states in collagen-induced arthritis . Arthritis Rheumatol.67 ( 6 ), 1668 – 1677 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• König C , ZharskyM , MöllerC , SchaibleH-G , EbersbergerA . Involvement of peripheral and spinal tumor necrosis factor α in spinal cord hyperexcitability during knee joint inflammation in rats . Arthritis Rheumatol.66 ( 3 ), 599 – 609 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Boettger MK , WeberK , GrossmannDet al. Spinal tumor necrosis factor alpha neutralization reduces peripheral inflammation and hyperalgesia and suppresses autonomic responses in experimental arthritis: a role for spinal tumor necrosis factor alpha during induction and maintenance of peripheral inflammation . Arthritis Rheum.62 ( 5 ), 1308 – 1318 ( 2010 ).
   PubMedGoogle Scholar
• Bas DB , SuJ , SandorKet al. Collagen antibody-induced arthritis evokes persistent pain with spinal glial involvement and transient prostaglandin dependency . Arthritis Rheum.64 ( 12 ), 3886 – 3896 ( 2012 ).
   PubMedGoogle Scholar
• Agalave NM , SvenssonCI . Extracellular high-mobility group box 1 protein (HMGB1) as a mediator of persistent pain . Mol. Med.20 , 569 – 578 ( 2014 ).
   Web of Science ®Google Scholar
• Christianson CA , DumlaoDS , StokesJAet al. Spinal TLR4 mediates the transition to a persistent mechanical hypersensitivity after the resolution of inflammation in serum-transferred arthritis . Pain152 ( 12 ), 2881 – 2891 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Kinsey SG , NaiduPS , CravattBF , DudleyDT , LichtmanAH . Fatty acid amide hydrolase blockade attenuates the development of collagen-induced arthritis and related thermal hyperalgesia in mice . Pharmacol. Biochem. Behav.99 ( 4 ), 718 – 725 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Obreja O , BiasioW , AndratschMet al. Fast modulation of heat-activated ionic current by proinflammatory interleukin 6 in rat sensory neurons . Brain128 ( Pt 7 ), 1634 – 1641 ( 2005 ).
   PubMedGoogle Scholar
• Boettger MK , LeuchtweisJ , KümmelD , GajdaM , BräuerR , SchaibleH-G . Differential effects of locally and systemically administered soluble glycoprotein 130 on pain and inflammation in experimental arthritis . Arthritis Res. Ther.12 ( 4 ), R140 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Boettger MK , WeberK , GajdaM , BräuerR , SchaibleHG . Spinally applied ketamine or morphine attenuate peripheral inflammation and hyperalgesia in acute and chronic phases of experimental arthritis . Brain. Behav. Immun.24 ( 3 ), 474 – 485 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Trentham DE , TownesAS , KangAH . Autoimmunity to type II collagen an experimental model of arthritis . J. Exp. Med.146 ( 3 ), 857 – 868 ( 1977 ).
   PubMed Web of Science ®Google Scholar
• Courtenay JS , DallmanMJ , DayanAD , MartinA , MosedaleB . Immunisation against heterologous type II collagen induces arthritis in mice . Nature283 ( 5748 ), 666 – 668 ( 1980 ).
   PubMed Web of Science ®Google Scholar
• Wooley PH , LuthraHS , StuartJM , DavidCS . Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates . J. Exp. Med.154 ( 3 ), 688 – 700 ( 1981 ).
   PubMed Web of Science ®Google Scholar
• Holmdahl R , JanssonL , LarssonA , JonssonR . Arthritis in DBA/1 mice induced with passively transferred type II collagen immune serum. Immunohistopathology and serum levels of anti-type II collagen auto-antibodies . Scand. J. Immunol.31 ( 2 ), 147 – 157 ( 1990 ).
   PubMed Web of Science ®Google Scholar
• Terato K , HastyKA , ReifeRA , CremerMA , KangAH , StuartJM . Induction of arthritis with monoclonal antibodies to collagen . J. Immunol.148 ( 7 ), 2103 – 2108 ( 1992 ).
   PubMed Web of Science ®Google Scholar
• Svensson L , JirholtJ , HolmdahlR , JanssonL . B cell-deficient mice do not develop type II collagen-induced arthritis (CIA) . Clin. Exp. Immunol.111 ( 3 ), 521 – 526 ( 1998 ).
   PubMed Web of Science ®Google Scholar
• Holmdahl R , JanssonL , AnderssonM , JonssonR . Genetic, hormonal and behavioural influence on spontaneously developing arthritis in normal mice . Clin. Exp. Immunol.88 ( 3 ), 467 – 472 ( 1992 ).
   PubMed Web of Science ®Google Scholar
• Baek YH , ChoiDY , YangHI , ParkDS . Analgesic effect of electroacupuncture on inflammatory pain in the rat model of collagen-induced arthritis: mediation by cholinergic and serotonergic receptors . Brain Res.1057 ( 1 ), 181 – 185 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Broom DC , MatsonDJ , BradshawEet al. Characterization of N-(adamantan-1-ylmethyl)-5-[(3R-amino-pyrrolidin-1-yl)methyl]-2-chloro-benzamide, a P2X7 antagonist in animal models of pain and inflammation . J. Pharmacol. Exp. Ther.327 ( 3 ), 620 – 633 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Patro N , SharmaA , KariayaK , PatroI . Spirulina platensis protects neurons via suppression of glial activation and peripheral sensitization leading to restoration of motor function in collagen-induced arthritic rats . Indian J. Exp. Biol.49 ( 10 ), 739 – 748 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Brackertz D , MitchellGF , VadasMA , MackayIR . Studies on antigen-induced arthritis in mice. III. Cell and serum transfer experiments . J. Immunol.118 ( 5 ), 1645 – 1648 ( 1977 ).
   PubMed Web of Science ®Google Scholar
• van den Berg WB , van de PutteLB , ZwartsWA , JoostenLA . Electrical charge of the antigen determines intraarticular antigen handling and chronicity of arthritis in mice . J. Clin. Invest.74 ( 5 ), 1850 – 1859 ( 1984 ).
   PubMed Web of Science ®Google Scholar
• van den Berg WB , van de PutteLB . Electrical charge of the antigen determines its localization in the mouse knee joint. Deep penetration of cationic BSA in hyaline articular cartilage . Am. J. Pathol.121 ( 2 ), 224 – 234 ( 1985 ).
   PubMed Web of Science ®Google Scholar
• Schaible HG , EbersbergerA , Banchet vonGS . Mechanisms of pain in arthritis . Ann. NY Acad. Sci.966 , 343 – 354 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Verri WA , CunhaTM , ParadaCAet al. Antigen-induced inflammatory mechanical hypernociception in mice is mediated by IL-18 . Brain Behav. Immun.21 ( 5 ), 535 – 543 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Leuchtweis J , ImhofAK , MontechiaroF , SchaibleHG , BoettgerMK . Validation of the digital pressure application measurement (PAM) device for detection of primary mechanical hyperalgesia in rat and mouse antigen-induced knee joint arthritis . Methods Find. Exp. Clin. Pharmacol.32 ( 8 ), 575 – 583 ( 2010 ).
   PubMedGoogle Scholar
• Stuart JM , DixonFJ . Serum transfer of collagen-induced arthritis in mice . J. Exp. Med.158 ( 2 ), 378 – 392 ( 1983 ).
   PubMed Web of Science ®Google Scholar
• Nandakumar KS , SvenssonL , HolmdahlR . Collagen type II-specific monoclonal antibody-induced arthritis in mice: description of the disease and the influence of age, sex, and genes . Am. J. Pathol.163 ( 5 ), 1827 – 1837 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Nandakumar KS , HolmdahlR . Collagen antibody induced arthritis . Methods Mol. Med.136 , 215 – 223 ( 2007 ).
   PubMedGoogle Scholar
• Agalave NM , LarssonM , AbdelmoatySet al. Spinal HMGB1 induces TLR4-mediated long-lasting hypersensitivity and glial activation and regulates pain-like behavior in experimental arthritis . Pain155 ( 9 ), 1802 – 1813 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Wigerblad G , SandorK , NandakumarKS , HolmdahlR , SvenssonC . Collagen antibodies induce pain-like behavior in mice without signs of inflammation . Arthritis Rheum.65 , S528 – S529 ( 2013 ).
   Google Scholar
• Kouskoff V , KorganowAS , DuchatelleV , DegottC , BenoistC , MathisD . Organ-specific disease provoked by systemic autoimmunity . Cell87 ( 5 ), 811 – 822 ( 1996 ).
   PubMed Web of Science ®Google Scholar
• Ji H , GauguierD , OhmuraKet al. Genetic influences on the end-stage effector phase of arthritis . J. Exp. Med.194 ( 3 ), 321 – 330 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Matsumoto I , StaubA , BenoistC , MathisD . Arthritis provoked by linked T and B cell recognition of a glycolytic enzyme . Science286 ( 5445 ), 1732 – 1735 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Ji H , PettitA , OhmuraKet al. Critical roles for interleukin 1 and tumor necrosis factor alpha in antibody-induced arthritis . J. Exp. Med.196 ( 1 ), 77 – 85 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Maccioni M , Zeder-LutzG , HuangHet al. Arthritogenic monoclonal antibodies from K/BxN mice . J. Exp. Med.195 ( 8 ), 1071 – 1077 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Korganow AS , JiH , MangialaioSet al. From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins . Immunity10 ( 4 ), 451 – 461 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Christianson CA , CorrM , YakshTL , SvenssonCI . K/BxN serum transfer arthritis as a model of inflammatory joint pain . Methods Mol. Biol.851 , 249 – 260 ( 2012 ).
   PubMedGoogle Scholar
• Suhail MS , ChristiansonC , KoehrnFet al. Effects of long term polyarthritis and subsequent NSAID treatment on activity with disassociation of tactile allodynia in the mouse . Neurocomputing84 , 47 – 52 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Siebert S , TsoukasA , RobertsonJ , McInnesI . Cytokines as therapeutic targets in rheumatoid arthritis and other inflammatory diseases . Pharmacol. Rev.67 ( 2 ), 280 – 309 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Schaible HG . Nociceptive neurons detect cytokines in arthritis . Arthritis Res. Ther.16 ( 5 ), 470 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Hess A , AxmannR , RechJet al. Blockade of TNF-α rapidly inhibits pain responses in the central nervous system . Proc. Natl Acad. Sci. USA108 ( 9 ), 3731 – 3736 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Tonussi CR , FerreiraSH . Tumour necrosis factor-alpha mediates carrageenin-induced knee-joint incapacitation and also triggers overt nociception in previously inflamed rat knee-joints . Pain82 ( 1 ), 81 – 87 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Miller RJ , JungH , BhangooSK , WhiteFA . Cytokine and chemokine regulation of sensory neuron function . Handb. Exp. Pharmacol. ( 194 ), 417 – 449 ( 2009 ).
   PubMedGoogle Scholar
• Shubayev VI , MyersRR . Axonal transport of TNF-alpha in painful neuropathy: distribution of ligand tracer and TNF receptors . J. Neuroimmunol.114 ( 1 ), 48 – 56 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Li Y , JiA , WeiheE , SchäferMK-H . Cell-specific expression and lipopolysaccharide-induced regulation of tumor necrosis factor alpha (TNFalpha) and TNF receptors in rat dorsal root ganglion . J. Neurosci.24 ( 43 ), 9623 – 9631 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Schäfers M , SorkinLS , GeisC , ShubayevVI . Spinal nerve ligation induces transient upregulation of tumor necrosis factor receptors 1 and 2 in injured and adjacent uninjured dorsal root ganglia in the rat . Neurosci. Lett.347 ( 3 ), 179 – 182 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Inglis JJ , NissimA , LeesDM , HuntSP , ChernajovskyY , KiddBL . The differential contribution of tumour necrosis factor to thermal and mechanical hyperalgesia during chronic inflammation . Arthritis. Res. Ther.7 ( 4 ), R807 – 16 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Nicol GD , VaskoMR . Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks?Mol. Interv.7 ( 1 ), 26 – 41 ( 2007 ).
   PubMedGoogle Scholar
• Woolf CJ , AllchorneA , Safieh-GarabedianB , PooleS . Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor alpha . Br. J. Pharmacol.121 ( 3 ), 417 – 424 ( 1997 ).
   PubMed Web of Science ®Google Scholar
• Queiroz-Junior CM , BessoniRLC , CostaVV , SouzaDG , TeixeiraMM , SilvaTA . Preventive and therapeutic anti-TNF-α therapy with pentoxifylline decreases arthritis and the associated periodontal co-morbidity in mice . Life. Sci.93 ( 9 ), 423 – 428 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• McInnes IB , SchettG . The pathogenesis of rheumatoid arthritis . N. Engl. J. Med.365 ( 23 ), 2205 – 2219 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Marchand F , PerrettiM , McMahonSB . Role of the immune system in chronic pain . Nat. Rev. Neurosci.6 ( 7 ), 521 – 532 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Copray JC , MantinghI , BrouwerNet al. Expression of interleukin-1 beta in rat dorsal root ganglia . J. Neuroimmunol.118 ( 2 ), 203 – 211 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Binshtok AM , WangH , ZimmermannKet al. Nociceptors are interleukin-1beta sensors . J. Neurosci.28 ( 52 ), 14062 – 14073 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Fukuoka H , KawataniM , HisamitsuT , TakeshigeC . Cutaneous hyperalgesia induced by peripheral injection of interleukin-1 beta in the rat . Brain Res.657 ( 1 ), 133 – 140 ( 1994 ).
   PubMed Web of Science ®Google Scholar
• Hirano T , MatsudaT , TurnerMet al. Excessive production of interleukin 6/B cell stimulatory factor-2 in rheumatoid arthritis . Eur. J. Immunol.18 ( 11 ), 1797 – 1801 ( 1988 ).
   PubMed Web of Science ®Google Scholar
• Navarro-Millán I , SinghJA , CurtisJR . Systematic review of tocilizumab for rheumatoid arthritis: a new biologic agent targeting the interleukin-6 receptor . Clin. Ther.34 ( 4 ), 788 – 802 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Vazquez E , KahlenbachJ , Segond von BanchetG , KönigC , SchaibleHG , EbersbergerA . Spinal interleukin-6 is an amplifier of arthritic pain in the rat . Arthritis Rheum.64 ( 7 ), 2233 – 2242 ( 2012 ).
   PubMedGoogle Scholar
• Gardiner NJ , CaffertyWBJ , SlackSE , ThompsonSWN . Expression of gp130 and leukaemia inhibitory factor receptor subunits in adult rat sensory neurones: regulation by nerve injury . J. Neurochem.83 ( 1 ), 100 – 109 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Dubový P , KlusákováI , SvízenskáI , BrázdaV . Satellite glial cells express IL-6 and corresponding signal-transducing receptors in the dorsal root ganglia of rat neuropathic pain model . Neuron Glia Biol.6 ( 1 ), 73 – 83 ( 2010 ).
   PubMedGoogle Scholar
• Oprée A , KressM . Involvement of the proinflammatory cytokines tumor necrosis factor-alpha, IL-1 beta, and IL-6 but not IL-8 in the development of heat hyperalgesia: effects on heat-evoked calcitonin gene-related peptide release from rat skin . J. Neurosci.20 ( 16 ), 6289 – 6293 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Banchet von GS , KiehlM , SchaibleHG . Acute and long-term effects of IL-6 on cultured dorsal root ganglion neurones from adult rat . J. Neurochem.94 ( 1 ), 238 – 248 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Gaffen SL . Structure and signalling in the IL-17 receptor family . Nat. Rev. Immunol.9 ( 8 ), 556 – 567 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Segond von Banchet G , BoettgerMK , KönigC , IwakuraY , BräuerR , SchaibleH-G . Neuronal IL-17 receptor upregulates TRPV4 but not TRPV1 receptors in DRG neurons and mediates mechanical but not thermal hyperalgesia . Mol. Cell. Neurosci.52 , 152 – 160 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Fattahi MJ , MirshafieyA . Prostaglandins and rheumatoid arthritis . Arthritis2012 ( 5 ), 239310 – 239317 ( 2012 ).
   PubMedGoogle Scholar
• Park HJ , SandorK , McQueenJet al. The effect of gabapentin and ketorolac on allodynia and conditioned place preference in antibody-induced inflammation . Eur. J. Pain doi:10.1002/ejp.816 ( 2015 ) ( Epub ahead of print ).
   PubMed Web of Science ®Google Scholar
• Hökfelt T , Wiesenfeld-HallinZ , VillarM , MelanderT . Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy . Neurosci. Lett.83 ( 3 ), 217 – 220 ( 1987 ).
   PubMed Web of Science ®Google Scholar
• Bileviciute I , LundebergT , EkblomA , TheodorssonE . Bilateral changes of substance P-, neurokinin A-, calcitonin gene-related peptide- and neuropeptide Y-like immunoreactivity in rat knee joint synovial fluid during acute monoarthritis . Neurosci. Lett.153 ( 1 ), 37 – 40 ( 1993 ).
   PubMed Web of Science ®Google Scholar
• Donnerer J , SchuligoiR , SteinC , AmannR . Upregulation, release and axonal transport of substance P and calcitonin gene-related peptide in adjuvant inflammation and regulatory function of nerve growth factor . Regul. Pept.46 ( 1 ), 150 – 154 ( 1993 ).
   PubMedGoogle Scholar
• Calzà L , PozzaM , ZanniM , ManziniCU , ManziniE , HökfeltT . Peptide plasticity in primary sensory neurons and spinal cord during adjuvant-induced arthritis in the rat: an immunocytochemical and in situ hybridization study . Neuroscience82 ( 2 ), 575 – 589 ( 1998 ).
   PubMed Web of Science ®Google Scholar
• Ji RR , ZhangX , Wiesenfeld-HallinZ , HökfeltT . Expression of neuropeptide Y and neuropeptide Y (Y1) receptor mRNA in rat spinal cord and dorsal root ganglia following peripheral tissue inflammation . J. Neurosci.14 ( 11 Pt 1 ), 6423 – 6434 ( 1994 ).
   PubMed Web of Science ®Google Scholar
• Patel YC . Somatostatin and its receptor family . Front. Neuroendocrinol.20 ( 3 ), 157 – 198 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Barajon I , BersaniM , QuartuMet al. Neuropeptides and morphological changes in cisplatin-induced dorsal root ganglion neuronopathy . Exp. Neurol.138 ( 1 ), 93 – 104 ( 1996 ).
   PubMed Web of Science ®Google Scholar
• Imhof AK , GlückL , GajdaMet al. Differential antiinflammatory and antinociceptive effects of the somatostatin analogs octreotide and pasireotide in a mouse model of immune-mediated arthritis . Arthritis Rheum.63 ( 8 ), 2352 – 2362 ( 2011 ).
   PubMedGoogle Scholar
• Vaudry D , Falluel-MorelA , BourgaultSet al. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery . Pharmacol. Rev.61 ( 3 ), 283 – 357 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Stösser S , AgarwalN , Tappe-TheodorA , YanagisawaM , KunerR . Dissecting the functional significance of endothelin A receptors in peripheral nociceptors in vivo via conditional gene deletion . Pain148 ( 2 ), 206 – 214 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Werner MFP , TrevisaniM , CampiB , AndréE , GeppettiP , RaeGA . Contribution of peripheral endothelin ETA and ETB receptors in neuropathic pain induced by spinal nerve ligation in rats . Eur. J. Pain14 ( 9 ), 911 – 917 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Pomonis JD , RogersSD , PetersCM , GhilardiJR , MantyhPW . Expression and localization of endothelin receptors: implications for the involvement of peripheral glia in nociception . J. Neurosci.21 ( 3 ), 999 – 1006 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Imhof AK , GlückL , GajdaM , BräuerR , SchaibleHG , SchulzS . Potent anti-inflammatory and antinociceptive activity of the endothelin receptor antagonist bosentan in monoarthritic mice . Arthritis Res. Ther.13 ( 3 ), R97 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Rahman W , DickensonAH . Voltage gated sodium and calcium channel blockers for the treatment of chronic inflammatory pain . Neurosci. Lett.557 ( Pt A ), 19 – 26 ( 2013 ).
   PubMedGoogle Scholar
• Sousa-Valente J , AndreouAP , UrbanL , NagyI . Transient receptor potential ion channels in primary sensory neurons as targets for novel analgesics . Br. J. Pharmacol.171 ( 10 ), 2508 – 2527 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Ikeuchi M , KolkerSJ , BurnesLA , WalderRY , SlukaKA . Role of ASIC3 in the primary and secondary hyperalgesia produced by joint inflammation in mice . Pain137 ( 3 ), 662 – 669 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Ikeuchi M , KolkerSJ , SlukaKA . Acid-sensing ion channel 3 expression in mouse knee joint afferents and effects of carrageenan-induced arthritis . J. Pain10 ( 3 ), 336 – 342 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Loggia ML , ChondeDB , AkejuOet al. Evidence for brain glial activation in chronic pain patients . Brain138 ( Pt 3 ), 604 – 615 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Ji RR , BertaT , NedergaardM . Glia and pain: Is chronic pain a gliopathy?Pain154 ( Suppl. 1 ), 10 – 28 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Alfonso Romero-Sandoval E , SweitzerS . Nonneuronal central mechanisms of pain: glia and immune response . Prog. Mol. Biol. Transl. Sci.131 , 325 – 358 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Sorge RE , MapplebeckJCS , RosenSet al. Different immune cells mediate mechanical pain hypersensitivity in male and female mice . Nat. Neurosci.18 ( 8 ), 1081 – 1083 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Gao YJ , XuZZ , LiuYC , WenYR , DecosterdI , JiRR . The c-Jun N-terminal kinase 1 (JNK1) in spinal astrocytes is required for the maintenance of bilateral mechanical allodynia under a persistent inflammatory pain condition . Pain148 ( 2 ), 309 – 319 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Nishioku T , YamauchiA , TakataFet al. Disruption of the blood-brain barrier in collagen-induced arthritic mice . Neurosci. Lett.482 ( 3 ), 208 – 211 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Lampa J , WestmanM , KadetoffDet al. Peripheral inflammatory disease associated with centrally activated IL-1 system in humans and mice . Proc. Natl Acad. Sci. USA109 ( 31 ), 12728 – 12733 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Clark AK , MalcangioM . Fractalkine/CX3CR1 signaling during neuropathic pain . Front. Cell. Neurosci.8 , 121 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Kato J , SvenssonCI . Role of extracellular damage-associated molecular pattern molecules (DAMPs) as mediators of persistent pain . Prog. Mol. Biol. Transl. Sci.131 , 251 – 279 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Feldman P , DueMR , RipschMS , KhannaR , WhiteFA . The persistent release of HMGB1 contributes to tactile hyperalgesia in a rodent model of neuropathic pain . J. Neuroinflammation9 ( 1 ), 180 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Nakamura Y , MoriokaN , AbeHet al. Neuropathic pain in rats with a partial sciatic nerve ligation is alleviated by intravenous injection of monoclonal antibody to high mobility group box-1 . PLoS ONE8 ( 8 ), e73640 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Kim JB , Sig ChoiJ , YuYMet al. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain . J. Neurosci.26 ( 24 ), 6413 – 6421 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Pedrazzi M , PatroneM , PassalacquaMet al. Selective proinflammatory activation of astrocytes by high-mobility group box 1 protein signaling . J. Immunol.179 ( 12 ), 8525 – 8532 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Raghavendra V , TangaFY , DeLeoJA . Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS . Eur. J. Neurosci.20 ( 2 ), 467 – 473 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Sorge RE , LaCroix-FralishML , TuttleAHet al. Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice . J. Neurosci.31 ( 43 ), 15450 – 15454 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Tsan MF , GaoB . Endogenous ligands of Toll-like receptors . J. Leukoc. Biol.76 ( 3 ), 514 – 519 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Scher JU , PillingerMH . The anti-inflammatory effects of prostaglandins . J. Investig. Med.57 ( 6 ), 703 – 708 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Schug SA , GoddardC . Recent advances in the pharmacological management of acute and chronic pain . Ann. Palliat. Med.3 ( 4 ), 263 – 275 ( 2014 ).
   PubMedGoogle Scholar
• Persson J . Ketamine in pain management . CNS Neurosci. Ther.19 ( 6 ), 396 – 402 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• King T , PorrecaF . Preclinical assessment of pain: improving models in discovery research . Curr. Top. Behav. Neurosci.20 , 101 – 120 ( 2014 ).
   PubMedGoogle Scholar
• Fairbanks CA , Goracke-PostleCJ . Neurobiological studies of chronic pain and analgesia: rationale and refinements . Eur. J. Pharmacol.759 , 169 – 181 ( 2015 ).
   PubMed Web of Science ®Google Scholar