Interleukin-6-mediated functional upregulation of TRPV1 receptors in dorsal root ganglion neurons through the activation of JAK/PI3K signaling pathway: Roles in the development of bone cancer pain in a rat model

Pain

Volumn 156, Issue 6, 2015, Pages 1124-1144

  Fang, Dong ^a,b   Kong, Ling Yu ^a,b   Cai, Jie ^a,b   Li, Song ^a,b   Liu, Xiao Dan ^a,b   Han, Ji Sheng ^a,b,c   Xing, Guo Gang ^a,b,c  

^a PEKING UNIVERSITY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

Bone cancer pain; Dorsal root ganglion; Hyperexcitability; Interleukin 6; Janus kinase; Phosphatidylinositol 3 kinase; TRPV1

Indexed keywords

INTERLEUKIN 6; JANUS KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; VANILLOID RECEPTOR 1; ENZYME INHIBITOR; INTERLEUKIN 6 RECEPTOR; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE CANCER; CANCER PAIN; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; INTRACELLULAR SIGNALING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT; RAT MODEL; SENSORY NERVE CELL; UPREGULATION; ACTION POTENTIAL; ANIMAL; BONE TUMOR; CELL CULTURE; COMPLICATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENETICS; HYPERALGESIA; METABOLISM; MOTOR ACTIVITY; NERVE CELL; PAIN; PAIN THRESHOLD; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPINAL GANGLION; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; BONE NEOPLASMS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FEMALE; GANGLIA, SPINAL; HYPERALGESIA; INTERLEUKIN-6; JANUS KINASES; MOTOR ACTIVITY; NEURONS; PAIN; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, INTERLEUKIN-6; SIGNAL TRANSDUCTION; TRPV CATION CHANNELS; UP-REGULATION;

EID: 84957402169     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000158     Document Type: Article

References (85)

1. Abdel Meguid MH, Hamad YH, Swilam RS, Barakat MS. Relation of interleukin-6 in rheumatoid arthritis patients to systemic bone loss and structural bone damage. Rheumatol Int 2013;33:697-703.
2. Andratsch M, Mair N, Constantin CE, Scherbakov N, Benetti C, Quarta S, Vogl C, Sailer CA, Uceyler N, Brockhaus J,Martini R, Sommer C, ZeilhoferHU, Muller W, Kuner R, Davis JB, Rose-John S, Kress M. A key role for gp130 expressed on peripheral sensory nerves in pathological pain. J Neurosci 2009; 29:13473-83.
3. Arruda JL, Sweitzer S, Rutkowski MD, DeLeo JA. Intrathecal anti-IL-6 antibody and IgG attenuates peripheral nerve injury-induced mechanical allodynia in the rat: possible immune modulation in neuropathic pain. Brain Res 2000;879:216-25.
4. Bevan S, Quallo T, Andersson DA. TRPV1. Handb Exp Pharmacol 2014; 222:207-45.
5. Binshtok AM, Wang H, Zimmermann K, Amaya F, Vardeh D, Shi L, Brenner GJ, Ji RR, Bean BP, Woolf CJ, Samad TA. Nociceptors are interleukin-1beta sensors. J Neurosci 2008;28:14062-73.
6. Boillat A, Alijevic O, Kellenberger S. Calcium entry via TRPV1 but not ASICs induces neuropeptide release from sensory neurons. Mol Cell Neurosci 2014;61:13-22.
7. Brenn D, Richter F, Schaible HG. Sensitization of unmyelinated sensory fibers of the joint nerve to mechanical stimuli by interleukin-6 in the rat: an inflammatory mechanism of joint pain. Arthritis Rheum 2007;56:351-9.
8. Brito R, Sheth S, Mukherjea D, Rybak LP, Ramkumar V. TRPV1: a potential drug target for treating various diseases. Cells 2014;3:517-45.
9. Busch-Dienstfertig M, Gonzalez-Rodriguez S. IL-4, JAK-STAT signaling, and pain. JAKSTAT 2013;2:e27638.
10. Campbell IL, Erta M, Lim SL, Frausto R, May U, Rose-John S, Scheller J, Hidalgo J. Trans-signaling is a dominant mechanism for the pathogenic actions of interleukin-6 in the brain. J Neurosci 2014;34:2503-13.
11. Chahine M, O'Leary ME. Regulation/modulation of sensory neuron sodium channels. Handb Exp Pharmacol 2014;221:111-35.
12. Chalaris A, Garbers C, Rabe B, Rose-John S, Scheller J. The soluble interleukin 6 receptor: generation and role in inflammation and cancer. Eur J Cell Biol 2011;90:484-94.
13. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994; 53:55-63.
14. Chung MK, Guler AD, Caterina MJ. TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 2008;11:555-64.
15. Constantin CE, Mair N, Sailer CA, Andratsch M, Xu ZZ, Blumer MJ, Scherbakov N, Davis JB, Bluethmann H, Ji RR, Kress M. Endogenous tumor necrosis factor alpha (TNFalpha) requires TNF receptor type 2 to generate heat hyperalgesia in a mouse cancer model. J Neurosci 2008; 28:5072-81.
16. Ding X, Cai J, Li S, Liu XD, Wan Y, Xing GG. BDNF contributes to the development of neuropathic pain by induction of spinal long-term potentiation via SHP2 associated GluN2B-containing NMDA receptors activation in rats with spinal nerve ligation.NeurobiolDis 2014;73C:428-51.
17. Dixon WJ. Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 1980;20:441-62.
18. Dominguez E, Rivat C, Pommier B, Mauborgne A, Pohl M. JAK/STAT3 pathway is activated in spinal cord microglia after peripheral nerve injury and contributes to neuropathic pain development in rat. J Neurochem 2008;107:50-60.
19. Dong Y, Mao-Ying QL, Chen JW, Yang CJ, Wang YQ, Tan ZM. Involvement of EphB1 receptor/ephrinB1 ligand in bone cancer pain. Neurosci Lett 2011;496:163-7.
20. Eulenfeld R, Dittrich A, Khouri C, Muller PJ, Mutze B, Wolf A, Schaper F. Interleukin-6 signalling: more than Jaks and STATs. Eur J Cell Biol 2012; 91:486-95.
21. Fang XX, Jiang XL, Han XH, Peng YP, Qiu YH. Neuroprotection of interleukin-6 against NMDA-induced neurotoxicity is mediated by JAK/ STAT3, MAPK/ERK, and PI3K/AKT signaling pathways. Cell Mol Neurobiol 2013;33:241-51.
22. GengSJ, LiaoFF,DangWH, DingX, LiuXD, Cai J,HanJS,WanY,XingGG. Contribution of the spinal cordBDNF to the development of neuropathic pain by activation of the NR2B-containing NMDA receptors in rats with spinal nerve ligation. Exp Neurol 2010;222:256-66.
23. Ghilardi JR, Rohrich H, Lindsay TH, Sevcik MA, Schwei MJ, Kubota K, Halvorson KG, Poblete J, Chaplan SR,DubinAE,CarruthersNI, SwansonD, Kuskowski M, Flores CM, Julius D, Mantyh PW. Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain. J Neurosci 2005; 25:3126-31.
24. Han Y, Li Y, Xiao X, Liu J, Meng XL, Liu FY, Xing GG,Wan Y. Formaldehyde up-regulates TRPV1 through MAPK and PI3K signaling pathways in a rat model of bone cancer pain. Neurosci Bull 2012;28:165-72.
25. He XH, Zang Y, Chen X, Pang RP, Xu JT, Zhou X, Wei XH, Li YY, Xin WJ, Qin ZH, Liu XG. TNF-alpha contributes to up-regulation ofNav1.3 and Nav1.8 in DRG neurons following motor fiber injury. PAIN 2010;151:266-79.
26. Hensellek S, Brell P, Schaible HG, Brauer R, Segond von BG. The cytokine TNFalpha increases the proportion of DRG neurones expressing the TRPV1 receptor via the TNFR1 receptor and ERK activation. Mol Cell Neurosci 2007;36:381-91.
27. Jazayeri JA, Upadhyay A, Vernallis AB, Carroll GJ. Targeting the glycoprotein 130 receptor subunit to control pain and inflammation. J Interferon Cytokine Res 2010;30:865-73.
28. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 2002;36:57-68.
29. Jiang H, Fang D, Kong LY, Jin ZR, Cai J, Kang XJ, Wan Y, Xing GG. Sensitization of neurons in the central nucleus of the amygdala via the decreased GABAergic inhibition contributes to the development of neuropathic pain-related anxiety-like behaviors in rats. Mol Brain 2014;7: 72-93.
30. Jin X, Gereau RW. Acute p38-mediated modulation of tetrodotoxinresistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J Neurosci 2006;26:246-55.
31. Jostock T, Blinn G, Renne C, Kallen KJ, Rose-John S, Mullberg J. Immunoadhesins of interleukin-6 and the IL-6/soluble IL-6R fusion protein hyper-IL-6. J Immunol Methods 1999;223:171-83.
32. Jostock T, Mullberg J, Ozbek S, Atreya R, Blinn G, Voltz N, Fischer M, Neurath MF, Rose-John S. Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses. Eur J Biochem 2001;268:160-7.
33. Julius D. TRP channels and pain. Annu Rev Cell Dev Biol 2013;29: 355-84.
34. Kao DJ, Li AH, Chen JC, Luo RS, Chen YL, Lu JC, Wang HL. CC chemokine ligand 2 upregulates the current density and expression of TRPV1 channels and Nav1.8 sodium channels in dorsal root ganglion neurons. J Neuroinflammation 2012;9:189.
35. Kawamata T, Niiyama Y, Yamamoto J, Furuse S. Reduction of bone cancer pain by CB1 activation and TRPV1 inhibition. J Anesth 2010;24: 328-32.
36. Kawasaki Y, Zhang L, Cheng JK, Ji RR. Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J Neurosci 2008;28: 5189-94.
37. Kochukov MY, McNearney TA, Yin H, Zhang L, Ma F, Ponomareva L, Abshire S, Westlund KN. Tumor necrosis factor-alpha (TNF-alpha) enhances functional thermal and chemical responses of TRP cation channels in human synoviocytes. Mol Pain 2009;5:49.
38. Langeslag M, Constantin CE, Andratsch M, Quarta S, Mair N, Kress M. Oncostatin M induces heat hypersensitivity by gp130-dependent sensitization of TRPV1 in sensory neurons. Mol Pain 2011;7:102-7.
39. Larrucea C, Castro P, Sepulveda FJ, Wandersleben G, Roa J, Aguayo LG. Sustained increase of Ca12 oscillations after chronic TRPV1 receptor activation with capsaicin in cultured spinal neurons. Brain Res 2008;1218: 70-6.
40. Lee KM, Jeon SM, Cho HJ. Interleukin-6 induces microglial CX3CR1 expression in the spinal cord after peripheral nerve injury through the activation of p38 MAPK. Eur J Pain 2010;14:682.e1-12.
41. Lei Q, Malykhina AP. Colonic inflammation up-regulates voltage-gated sodium channels in bladder sensory neurons via activation of peripheral transient potential vanilloid 1 receptors. Neurogastroenterol Motil 2012; 24:575-85, e257.
42. Li Y, Cai J, Han Y, Xiao X, Meng XL, Su L, Liu FY, Xing GG, Wan Y. Enhanced function of TRPV1 via up-regulation by insulin-like growth factor-1 in a rat model of bone cancer pain. Eur J Pain 2014;18:774-84.
43. Liang R, Liu X, Wei L, Wang W, Zheng P, Yan X, Zhao Y, Liu L, Cao X. The modulation of the excitability of primary sensory neurons by Ca(2)(1)-CaMCaMKII pathway. Neurol Sci 2012;33:1083-93.
44. Liu M, Yang H, Fang D, Yang JJ, Cai J, Wan Y, ChuiDH, Han JS, XingGG. Upregulation of P2X3 receptors by neuronal calcium sensor protein VILIP-1 in dorsal root ganglions contributes to the bone cancer pain in rats. PAIN 2013;154:1551-68.
45. Liu XD, Yang JJ, Fang D, Cai J,Wan Y, Xing GG. Functional upregulation of nav1.8 sodium channels on the membrane of dorsal root ganglia neurons contributes to the development of cancer-induced bone pain. PLoS One 2014;9:e114623.
46. Lozano-Ondoua AN, Symons-Liguori AM, Vanderah TW. Cancer-induced bone pain: mechanisms and models. Neurosci Lett 2013;557:52-9.
47. Manjavachi MN, Motta EM, Marotta DM, Leite DF, Calixto JB. Mechanisms involved in IL-6-induced muscular mechanical hyperalgesia in mice. PAIN 2010;151:345-55.
48. Mao-Ying QL, Wang XW, Yang CJ, Li X, Mi WL, Wu GC, Wang YQ. Robust spinal neuroinflammation mediates mechanical allodynia in Walker 256 induced bone cancer rats. Mol Brain 2012;5:16-5.
49. Matsutomi T, Nakamoto C, Zheng T, Kakimura J, Ogata N. Multiple types of Na(1) currents mediate action potential electrogenesis in small neurons of mouse dorsal root ganglia. Pflugers Arch 2006;453:83-96.
50. Melemedjian OK, Asiedu MN, Tillu DV, Peebles KA, Yan J, Ertz N, Dussor GO, Price TJ. IL-6-and NGF-induced rapid control of protein synthesis and nociceptive plasticity via convergent signaling to the eIF4F complex. J Neurosci 2010;30:15113-23.
51. Miranda-Morales M, Ochoa-Cortes F, Stern E, Lomax AE, Vanner S. Axon reflexes evoked by transient receptor potential vanilloid 1 activation are mediated by tetrodotoxin-resistant voltage-gated Na1 channels in intestinal afferent nerves. J Pharmacol Exp Ther 2010;334:566-75.
52. MurakamiM,HibiM,NakagawaN,Nakagawa T, Yasukawa K, Yamanishi K, Taga T, Kishimoto T. IL-6-induced homodimerization of gp130 and associated activation of a tyrosine kinase. Science 1993;260:1808-10.
53. Natura G, von Banchet GS, Schaible HG. Calcitonin gene-related peptide enhances TTX-resistant sodium currents in cultured dorsal root ganglion neurons from adult rats. PAIN 2005;116:194-204.
54. Neelands TR, Jarvis MF, Faltynek CR, Surowy CS. Elevated temperatures alter TRPV1 agonist-evoked excitability of dorsal root ganglion neurons. Inflamm Res 2008;57:404-9.
55. Nicol GD, Lopshire JC, Pafford CM. Tumor necrosis factor enhances the capsaicin sensitivity of rat sensory neurons. J Neurosci 1997;17:975-82.
56. Niiyama Y, Kawamata T, Yamamoto J, Furuse S, Namiki A. SB366791, a TRPV1 antagonist, potentiates analgesic effects of systemic morphine in a murine model of bone cancer pain. Br J Anaesth 2009;102:251-8.
57. Niiyama Y, Kawamata T, Yamamoto J, Omote K, Namiki A. Bone cancer increases transient receptor potential vanilloid subfamily 1 expression within distinct subpopulations of dorsal root ganglion neurons. Neuroscience 2007;148:560-72.
58. Obreja O, Biasio W, Andratsch M, Lips KS, Rathee PK, Ludwig A, Rose-John S, Kress M. Fast modulation of heat-activated ionic current by proinflammatory interleukin 6 in rat sensory neurons. Brain 2005;128: 1634-41.
59. Opree A, Kress M. 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 2000;20:6289-93.
60. 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;6:85-6.
61. Peters CM, Ghilardi JR, Keyser CP, Kubota K, Lindsay TH, Luger NM, Mach DB, Schwei MJ, Sevcik MA, Mantyh PW. Tumor-induced injury of primary afferent sensory nerve fibers in bone cancer pain. Exp Neurol 2005;193:85-100.
62. Planells-Cases R, Valente P, Ferrer-Montiel A, Qin F, Szallasi A. Complex regulation of TRPV1 and related thermo-TRPs: implications for therapeutic intervention. Adv Exp Med Biol 2011;704:491-515.
63. Qu XX, Cai J, Li MJ, Chi YN, Liao FF, Liu FY, Wan Y, Han JS, Xing GG. Role of the spinal cord NR2B-containing NMDA receptors in the development of neuropathic pain. Exp Neurol 2009;215:298-307.
64. Rivlin AS, Tator CH. Objective clinical assessment of motor function after experimental spinal cord injury in the rat. J Neurosurg 1977;47:577-81.
65. Rose-John S, Scheller J, Elson G, Jones SA. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 2006;80:227-36.
66. Schaible HG, von Banchet GS, Boettger MK, Brauer R, Gajda M, Richter F, Hensellek S, Brenn D, Natura G. The role of proinflammatory cytokines in the generation and maintenance of joint pain. Ann N Y Acad Sci 2010;1193: 60-9.
67. Scheller J, Ohnesorge N, Rose-John S. Interleukin-6 trans-signalling in chronic inflammation and cancer. Scand J Immunol 2006;63:321-9.
68. Smith H, Brooks JR. Capsaicin-based therapies for pain control. Prog Drug Res 2014;68:129-46.
69. Spooren A, Kolmus K, Laureys G, Clinckers R, De KJ, Haegeman G, Gerlo S. Interleukin-6, amental cytokine. Brain Res Rev 2011;67:157-83.
70. Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE. Phosphoinositide 3-kinase binds to TRPV1 and mediates NGFstimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol 2006;128:509-22.
71. Tyrrell L, Renganathan M, Dib-Hajj SD, Waxman SG. Glycosylation alters steady-state inactivation of sodium channel Nav1.9/NaN in dorsal root ganglion neurons and is developmentally regulated. J Neurosci 2001;21: 9629-37.
72. Vallejo R, Tilley DM, Vogel L, Benyamin R. The role of glia and the immune system in the development and maintenance of neuropathic pain. Pain Pract 2010;10:167-84.
73. Vazquez E, Kahlenbach J, Segond von BG, Konig C, Schaible HG, Ebersberger A. Spinal interleukin-6 is an amplifier of arthritic pain in the rat. Arthritis Rheum 2012;64:2233-42.
74. von Banchet GS, Kiehl M, Schaible HG. Acute and long-term effects of IL-6 on cultured dorsal root ganglion neurones from adult rat. J Neurochem 2005;94:238-48.
75. Waxman SG. Channel, neuronal and clinical function in sodium channelopathies: from genotype to phenotype. NatNeurosci 2007;10:405-9.
76. Wei XH, Na XD, Liao GJ, Chen QY, Cui Y, Chen FY, Li YY, Zang Y, Liu XG. The up-regulation of IL-6 in DRG and spinal dorsal horn contributes to neuropathic pain following L5 ventral root transection. Exp Neurol 2013; 241:159-68.
77. Xu Q, Zhang XM, Duan KZ, Gu XY, Han M, Liu BL, Zhao ZQ, Zhang YQ. Peripheral TGF-beta1 signaling is a critical event in bone cancer-induced hyperalgesia in rodents. J Neurosci 2013;33:19099-111.
78. Yamada O, Ozaki K, Akiyama M, Kawauchi K. JAK-STAT and JAK-PI3KmTORC1 pathways regulate telomerase transcriptionally and posttranslationally in ATL cells. Mol Cancer Ther 2012;11:1112-21.
79. Yan J, Melemedjian OK, Price TJ, Dussor G. Sensitization of dural afferents underlies migraine-related behavior following meningeal application of interleukin-6 (IL-6). Mol Pain 2012;8:6-8.
80. Zhang X, Huang J, McNaughton PA. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBOJ 2005;24:4211-23.
81. Zheng Q, Fang D, Cai J, Wan Y, Han JS, Xing GG. Enhanced excitability of small dorsal root ganglion neurons in rats with bone cancer pain. Mol Pain 2012;8:24-8.
82. Zheng Q, Fang D, Liu M, Cai J, Wan Y, Han JS, Xing GG. Suppression of KCNQ/M (Kv7) potassium channels in dorsal root ganglion neurons contributes to the development of bone cancer pain in a rat model. PAIN 2013;154:434-48.
83. Zhuang ZY, Xu H, Clapham DE, Ji RR. Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 2004;24:8300-9.
84. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. PAIN 1983;16:109-10.
85. Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol 2001;429:23-37.