EphrinB-EphB receptor signaling contributes to bone cancer pain via Toll-like receptor and proinflammatory cytokines in rat spinal cord

Pain

Volumn 154, Issue 12, 2013, Pages 2823-2835

  Liu, Su ^a,b   Liu, Yue Peng ^a,b   Song, William B ^b   Song, Xue Jun ^a,b  

^a PEKING UNIVERSITY   (China)

^b Parker University Research Institute   (United States)

Author keywords

Bone cancer; EphB1; IL 1 ; TLR4; TNF

Indexed keywords

EPHRIN RECEPTOR; EPHRIN RECEPTOR B1; EPHRIN RECEPTOR B2; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BONE CANCER; CANCER PAIN; CELL ACTIVATION; FEMALE; GLIA CELL; HYPERALGESIA; HYPERSENSITIVITY; IMMUNOFLUORESCENCE; MICROGLIA; MOUSE; NONHUMAN; PAIN ASSESSMENT; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; TIBIA; TUMOR CELL; TUMOR XENOGRAFT;

BONE CANCER; EPHB1; IL-1Β; TLR4; TNF-Α;

ANIMALS; BONE NEOPLASMS; EPHRIN-B2; FEMALE; INFLAMMATION MEDIATORS; INJECTIONS, SPINAL; MICE; MICE, INBRED C57BL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPHB1; SIGNAL TRANSDUCTION; SPINAL CORD; TOLL-LIKE RECEPTOR 4;

EID: 84889081868     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2013.08.017     Document Type: Article

References (63)

1. I. Bettoni, F. Comelli, C. Rossini, F. Granucci, G. Giagnoni, F. Peri, and B. Costa Glial TLR4 receptor as new target to treat neuropathic pain: efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice Glia 56 2008 1312 1319
2. E. Borysiewicz, D. Fil, and G.W. Konat Rho proteins are negative regulators of TLR2, TLR3, and TLR4 signaling in astrocytes J Neurosci Res 87 2009 1565 1572
3. G. Christofori New signals from the invasive front Nature 441 2006 444 450
4. R.E. Coleman Clinical features of metastatic bone disease and risk of skeletal morbidity Clin Cancer Res 12 2006 6243s 6249s
5. M.B. Dalva, M.A. Takasu, M.Z. Lin, S.M. Shamah, L. Hu, N.W. Gale, and M.E. Greenberg EphB receptors interact with NMDA receptors and regulate excitatory synapse formation Cell 103 2000 945 956
6. A. Diogenes, C.C. Ferraz, A.N. Akopian, M.A. Henry, and K.M. Hargreaves LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons J Dent Res 90 2011 759 764
7. A.M. Dolga, I. Granic, T. Blank, H.G. Knaus, J. Spiess, P.G. Luiten, U.L. Eisel, and I.M. Nijholt TNF-alpha-mediates neuroprotection against glutamate-induced excitotoxicity via NF-kappaB-dependent up-regulation of K2.2 channels J Neurochem 107 2008 1158 1167
8. S. Fernandez-Lizarbe, M. Pascual, and C. Guerri Critical role of TLR4 response in the activation of microglia induced by ethanol J Immunol 183 2009 4733 4744
9. J.G. Flanagan, and P. Vanderhaeghen The ephrins and Eph receptors in neural development Annu Rev Neurosci 21 1998 309 345
10. P. Friedl, and K. Wolf Tumour-cell invasion and migration: diversity and escape mechanisms Nat Rev Cancer 3 2003 362 374
11. J.R. Ghilardi, H. Rohrich, T.H. Lindsay, M.A. Sevcik, M.J. Schwei, K. Kubota, K.G. Halvorson, J. Poblete, S.R. Chaplan, A.E. Dubin, N.I. Carruthers, D. Swanson, M. Kuskowski, C.M. Flores, D. Julius, and P.W. Mantyh Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain J Neurosci 25 2005 3126 3131
12. M.J. Goblirsch, P. Zwolak, and D.R. Clohisy Advances in understanding bone cancer pain J Cell Biochem 96 2005 682 688
13. R. Gorina, M. Font-Nieves, L. Marquez-Kisinousky, T. Santalucia, and A.M. Planas Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling, MAPK, and Jak1/Stat1 pathways Glia 59 2011 242 255
14. R.D. Gosselin, M.R. Suter, R.R. Ji, and I. Decosterd Glial cells and chronic pain Neuroscientist 16 2010 519 531
15. R. Griffin, R. Nally, Y. Nolan, Y. McCartney, J. Linden, and M.A. Lynch The age-related attenuation in long-term potentiation is associated with microglial activation J Neurochem 99 2006 1263 1272
16. A. Hald, S. Nedergaard, R.R. Hansen, M. Ding, and A.M. Heegaard Differential activation of spinal cord glial cells in murine models of neuropathic and cancer pain Eur J Pain 13 2009 138 145
17. Y. Han, X.S. Song, W.T. Liu, M. Henkemeyer, and X.J. Song Targeted mutation of EphB1 receptor prevents development of neuropathic hyperalgesia and physical dependence on morphine in mice Mol Pain 4 2008 60
18. M. Heroult, F. Schaffner, and H.G. Augustin Eph receptor and ephrin ligand-mediated interactions during angiogenesis and tumor progression Exp Cell Res 312 2006 642 650
19. M.R. Hutchinson, Y. Zhang, M. Shridhar, J.H. Evans, M.M. Buchanan, T.X. Zhao, P.F. Slivka, B.D. Coats, N. Rezvani, J. Wieseler, T.S. Hughes, K.E. Landgraf, S. Chan, S. Fong, S. Phipps, J.J. Falke, L.A. Leinwand, S.F. Maier, H. Yin, K.C. Rice, and L.R. Watkins Evidence that opioids may have toll-like receptor 4 and MD-2 effects Brain Behav Immun 24 2010 83 95
20. A. Kato, K. Minami, H. Ito, T. Tomii, M. Matsumoto, S. Orita, T. Kihara, M. Narita, and T. Suzuki Oxycodone-induced analgesic effects in a bone cancer pain model in mice Oncology 74 2008 55 60
21. Y. Kawasaki, L. Zhang, J.K. Cheng, and R.R. Ji 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 28 2008 5189 5194
22. C.E. Krull, R. Lansford, N.W. Gale, A. Collazo, C. Marcelle, G.D. Yancopoulos, S.E. Fraser, and M. Bronner-Fraser Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration Curr Biol 7 1997 571 580
23. K. Kullander, and R. Klein Mechanisms and functions of Eph and ephrin signalling Nat Rev Mol Cell Biol 3 2002 475 486
24. L.S. Lan, Y.J. Ping, W.L. Na, J. Miao, Q.Q. Cheng, M.Z. Ni, L. Lei, L.C. Fang, R.C. Guang, Z. Jin, and L. Wei Down-regulation of Toll-like receptor 4 gene expression by short interfering RNA attenuates bone cancer pain in a rat model Mol Pain 6 2010 2
25. S. Lehnardt, C. Lachance, S. Patrizi, S. Lefebvre, P.L. Follett, F.E. Jensen, P.A. Rosenberg, J.J. Volpe, and T. Vartanian The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS J Neurosci 22 2002 2478 2486
26. S. Lehnardt, L. Massillon, P. Follett, F.E. Jensen, R. Ratan, P.A. Rosenberg, J.J. Volpe, and T. Vartanian Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway Proc Natl Acad Sci U S A 100 2003 8514 8519
27. S. Liu, and T. Kielian Microglial activation by Citrobacter koseri is mediated by TLR4- and MyD88-dependent pathways J Immunol 183 2009 5537 5547
28. S. Liu, W.T. Liu, Y.P. Liu, H.L. Dong, M. Henkemeyer, L.Z. Xiong, and X.J. Song Blocking EphB1 receptor forward signaling in spinal cord relieves bone cancer pain and rescues analgesic effect of morphine treatment in rodents Cancer Res 71 2011 4392 4402
29. W.T. Liu, Y. Han, Y.P. Liu, A.A. Song, B. Barnes, and X.J. Song Spinal matrix metalloproteinase-9 contributes to physical dependence on morphine in mice J Neurosci 30 2010 7613 7623
30. W.T. Liu, H.C. Li, X.S. Song, Z.J. Huang, and X.J. Song EphB receptor signaling in mouse spinal cord contributes to physical dependence on morphine FASEB J 23 2009 90 98
31. M. Maroso, S. Balosso, T. Ravizza, J. Liu, E. Aronica, A.M. Iyer, C. Rossetti, M. Molteni, M. Casalgrandi, A.A. Manfredi, M.E. Bianchi, and A. Vezzani Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures Nat Med 16 2010 413 419
32. S.J. Medhurst, K. Walker, M. Bowes, B.L. Kidd, M. Glatt, M. Muller, M. Hattenberger, J. Vaxelaire, T. O'Reilly, G. Wotherspoon, J. Winter, J. Green, and L. Urban A rat model of bone cancer pain PAIN® 96 2002 129 140
33. R. Medzhitov, and C. Janeway Jr. Innate immune recognition: mechanisms and pathways Immunol Rev 173 2000 89 97
34. E.D. Milligan, and L.R. Watkins Pathological and protective roles of glia in chronic pain Nat Rev Neurosci 10 2009 23 36
35. T. Nakagawa, and S. Kaneko Spinal astrocytes as therapeutic targets for pathological pain J Pharmacol Sci 114 2010 347 353
36. M. Nakamoto, and A.D. Bergemann Diverse roles for the Eph family of receptor tyrosine kinases in carcinogenesis Microsc Res Tech 59 2002 58 67
37. E.J. Nestler Molecular basis of long-term plasticity underlying addiction Nat Rev Neurosci 2 2001 119 128
38. P. Pasinelli, M.E. Belford, N. Lennon, B.J. Bacskai, B.T. Hyman, D. Trotti, and R.H. Brown Jr. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria Neuron 43 2004 19 30
39. E.B. Pasquale Eph receptor signalling casts a wide net on cell behaviour Nat Rev Mol Cell Biol 6 2005 462 475
40. B.X. Ren, X.P. Gu, Y.G. Zheng, C.L. Liu, D. Wang, Y.E. Sun, and Z.L. Ma Intrathecal injection of metabotropic glutamate receptor subtype 3 and 5 agonist/antagonist attenuates bone cancer pain by inhibition of spinal astrocyte activation in a mouse model Anesthesiology 116 2012 122 132
41. K. Riazi, M.A. Galic, J.B. Kuzmiski, W. Ho, K.A. Sharkey, and Q.J. Pittman Microglial activation and TNFalpha production mediate altered CNS excitability following peripheral inflammation Proc Natl Acad Sci U S A 105 2008 17151 17156
42. A. Romero-Sandoval, N. Chai, N. Nutile-McMenemy, and J.A. Deleo A comparison of spinal Iba1 and GFAP expression in rodent models of acute and chronic pain Brain Res 1219 2008 116 126
43. E. Sahai Mechanisms of cancer cell invasion Curr Opin Genet Dev 15 2005 87 96
44. D. Schomberg, and J.K. Olson Immune responses of microglia in the spinal cord: contribution to pain states Exp Neurol 234 2012 262 270
45. A.L. Shiau, S.Y. Chen, M.Y. Chang, C.H. Su, S.Y. Chung, Y.T. Yo, C.R. Wang, and C.L. Wu Prothymosin alpha lacking the nuclear localization signal as an effective gene therapeutic strategy in collagen-induced arthritis J Immunol 178 2007 4688 4694
46. H.S. Smith Activated microglia in nociception Pain Phys 13 2010 295 304
47. X.J. Song, J.L. Cao, H.C. Li, J.H. Zheng, X.S. Song, and L.Z. Xiong Upregulation and redistribution of ephrinB and EphB receptor in dorsal root ganglion and spinal dorsal horn neurons after peripheral nerve injury and dorsal rhizotomy Eur J Pain 12 2008 1031 1039
48. X.J. Song, Z.B. Wang, Q. Gan, and E.T. Walters CAMP and cGMP contribute to sensory neuron hyperexcitability and hyperalgesia in rats with dorsal root ganglia compression J Neurophysiol 95 2006 479 492
49. X.J. Song, J.H. Zheng, J.L. Cao, W.T. Liu, X.S. Song, and Z.J. Huang EphrinB-EphB receptor signaling contributes to neuropathic pain by regulating neural excitability and spinal synaptic plasticity in rats PAIN® 139 2008 168 180
50. H. Surawska, P.C. Ma, and R. Salgia The role of ephrins and Eph receptors in cancer Cytokine Growth Factor Rev 15 2004 419 433
51. M.A. Takasu, M.B. Dalva, R.E. Zigmond, and M.E. Greenberg Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors Science 295 2002 491 495
52. F.Y. Tanga, N. Nutile-McMenemy, and J.A. DeLeo The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy Proc Natl Acad Sci U S A 102 2005 5856 5861
53. F.Y. Tanga, V. Raghavendra, and J.A. DeLeo Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain Neurochem Int 45 2004 397 407
54. M.H. van den Beuken-van Everdingen, J.M. de Rijke, A.G. Kessels, H.C. Schouten, M. van Kleef, and J. Patijn Prevalence of pain in patients with cancer: a systematic review of the past 40 years Ann Oncol 18 2007 1437 1449
55. B. Viviani, S. Bartesaghi, F. Gardoni, A. Vezzani, M.M. Behrens, T. Bartfai, M. Binaglia, E. Corsini, M. Di Luca, C.L. Galli, and M. Marinovich Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases J Neurosci 23 2003 8692 8700
56. H.U. Wang, and D.J. Anderson Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth Neuron 18 1997 383 396
57. L.N. Wang, J.P. Yang, Y. Zhan, F.H. Ji, X.Y. Wang, J.L. Zuo, and Q.N. Xu Minocycline-induced reduction of brain-derived neurotrophic factor expression in relation to cancer-induced bone pain in rats J Neurosci Res 90 2012 672 681
58. L.N. Wang, M. Yao, J.P. Yang, J. Peng, Y. Peng, C.F. Li, Y.B. Zhang, F.H. Ji, H. Cheng, Q.N. Xu, X.Y. Wang, and J.L. Zuo Cancer-induced bone pain sequentially activates the ERK/MAPK pathway in different cell types in the rat spinal cord Mol Pain 7 2011 48
59. Z.B. Wang, Q. Gan, R.L. Rupert, Y.M. Zeng, and X.J. Song Thiamine, pyridoxine, cyanocobalamin and their combination inhibit thermal, but not mechanical hyperalgesia in rats with primary sensory neuron injury PAIN® 114 2005 266 277
60. D.G. Wilkinson Eph receptors and ephrins: regulators of guidance and assembly Int Rev Cytol 196 2000 177 244
61. D.G. Wilkinson Multiple roles of EPH receptors and ephrins in neural development Nat Rev Neurosci 2 2001 155 164
62. M. Yao, X.Y. Chang, Y.X. Chu, J.P. Yang, L.N. Wang, H.Q. Cao, M.J. Liu, and Q.N. Xu Antiallodynic effects of propentofylline elicited by interrupting spinal glial function in a rat model of bone cancer pain J Neurosci Res 89 2011 1877 1886
63. R.X. Zhang, B. Liu, L. Wang, K. Ren, J.T. Qiao, B.M. Berman, and L. Lao Spinal glial activation in a new rat model of bone cancer pain produced by prostate cancer cell inoculation of the tibia PAIN® 118 2005 125 136