Robust spinal neuroinflammation mediates mechanical allodynia in Walker 256 induced bone cancer rats

Molecular Brain

Volumn 5, Issue 1, 2012, Pages

  Mao Ying, Qi Liang ^a   Wang, Xiao Wei ^a   Yang, Chang Jiang ^a   Li, Xiu ^a   Mi, Wen Li ^a   Wu, Gen Cheng ^a   Wang, Yan Qing ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Cancer induced pain; Glial activation; Neuroinflammation; Rat; Toll like receptor 4

Indexed keywords

FLUOROCITRIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MINOCYCLINE; NALOXONE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BONE CANCER; CANCER PAIN; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD; WALKER CARCINOMA;

ANIMALS; ANTIGENS, CD11B; ASTROCYTES; BEHAVIOR, ANIMAL; BONE NEOPLASMS; CARCINOMA 256, WALKER; CYTOKINES; FEMALE; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HYPERALGESIA; HYPERTROPHY; INFLAMMATION; MICROGLIA; NEOPLASM TRANSPLANTATION; PAIN; PAIN THRESHOLD; POSTERIOR HORN CELLS; RATS; RATS, WISTAR; RNA, MESSENGER; SPINAL CORD; TIBIA; TIME FACTORS; TOLL-LIKE RECEPTOR 4;

RATTUS;

EID: 84861133515     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-5-16     Document Type: Article

References (53)

1. Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. Schwei MJ, Honore P, Rogers SD, Salak-Johnson JL, Finke MP, Ramnaraine ML, Clohisy DR, Mantyh PW, J Neurosci 1999 19 10886 10897 10594070 (Pubitemid 30235733)
2. A rat model of bone cancer pain. Medhurst SJ, Walker K, Bowes M, Kidd BL, Glatt M, Muller M, Hattenberger M, Vaxelaire J, O'Reilly T, Wotherspoon G, et al. Pain 2002 96 129 140 10.1016/S0304-3959(01)00437-7 11932069 (Pubitemid 34270635)
3. Morphine analgesia suppresses tumor growth and metastasis in a mouse model of cancer pain produced by orthotopic tumor inoculation. Sasamura T, Nakamura S, Iida Y, Fujii H, Murata J, Saiki I, Nojima H, Kuraishi Y, Eur J Pharmacol 2002 441 185 191 10.1016/S0014-2999(02)01450-4 12063091 (Pubitemid 34626170)
4. Different tumors in bone each give rise to a distinct pattern of skeletal destruction, bone cancer-related pain behaviors and neurochemical changes in the central nervous system. Sabino MA, Luger NM, Mach DB, Rogers SD, Schwei MJ, Mantyh PW, Int J Cancer 2003 104 550 558 10.1002/ijc.10999 12594809 (Pubitemid 36337254)
5. Spinal glial activation in a new rat model of bone cancer pain produced by prostate cancer cell inoculation of the tibia. Zhang RX, Liu B, Wang L, Ren K, Qiao JT, Berman BM, Lao L, Pain 2005 118 125 136 10.1016/j.pain.2005.08.001 16154703 (Pubitemid 41566591)
6. Glial activation: a driving force for pathological pain. Watkins LR, Milligan ED, Maier SF, Trends Neurosci 2001 24 450 455 10.1016/S0166-2236(00) 01854-3 11476884 (Pubitemid 32695356)
7. A rat model of bone cancer pain induced by intra-tibia inoculation of Walker 256 mammary gland carcinoma cells. Mao-Ying QL, Zhao J, Dong ZQ, Wang J, Yu J, Yan MF, Zhang YQ, Wu GC, Wang YQ, Biochem Biophys Res Commun 2006 345 1292 1298 10.1016/j.bbrc.2006.04.186 16725112 (Pubitemid 43817875)
8. "Listening" and "talking" to neurons: implications of immune activation for pain control and increasing the efficacy of opioids. Watkins LR, Hutchinson MR, Milligan ED, Maier SF, Brain Res Rev 2007 56 148 169 10.1016/j.brainresrev.2007.06.006 17706291 (Pubitemid 350100866)
9. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Tanga FY, Nutile-McMenemy N, DeLeo JA, Proc Natl Acad Sci U S A 2005 102 5856 5861 10.1073/pnas.0501634102 15809417 (Pubitemid 40559649)
10. Neuroimmune activation and neuroinflammation in chronic pain and opioid tolerance/hyperalgesia. DeLeo JA, Tanga FY, Tawfik VL, Neuroscientist 2004 10 40 52 10.1177/1073858403259950 14987447 (Pubitemid 38112699)
11. Toll-like receptor 3 contributes to spinal glial activation and tactile allodynia after nerve injury. Obata K, Katsura H, Miyoshi K, Kondo T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Akira S, Noguchi K, J Neurochem 2008 105 2249 2259 10.1111/j.1471-4159.2008.05353.x 18363823 (Pubitemid 351782279)
12. The role of TLR2 in nerve injury-induced neuropathic pain is essentially mediated through macrophages in peripheral inflammatory response. Shi XQ, Zekki H, Zhang J, Glia 2011 59 231 241 10.1002/glia.21093 21125644
13. 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. Bettoni I, Comelli F, Rossini C, Granucci F, Giagnoni G, Peri F, Costa B, Glia 2008 56 1312 1319 10.1002/glia.20699 18615568
14. The "toll" of opioid-induced glial activation: improving the clinical efficacy of opioids by targeting glia. Watkins LR, Hutchinson MR, Rice KC, Maier SF, Trends Pharmacol Sci 2009 30 581 591 10.1016/j.tips.2009.08.002 19762094
15. Naloxone-precipitated morphine withdrawal behavior and brain IL-1beta expression: comparison of different mouse strains. Liu L, Coller JK, Watkins LR, Somogyi AA, Hutchinson MR, Brain Behav Immun 2011 25 1223 1232 10.1016/j.bbi.2011.03.016 21447380
16. Toll-like receptors in the induction of the innate immune response. Aderem A, Ulevitch RJ, Nature 2000 406 782 787 10.1038/35021228 10963608
17. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells. Re F, Strominger JL, J Biol Chem 2001 276 37692 37699 10.1074/jbc.M105927200 11477091
18. Toll-like receptors in peripheral nerve injury and neuropathic pain. Kim D, Lee S, Lee SJ, Curr Top Microbiol Immunol 2009 336 169 186 10.1007/978-3-642-00549-7-10 19688334
19. Immune cell activation by bacterial CpG-DNA through myeloid differentiation marker 88 and tumor necrosis factor receptor-associated factor (TRAF)6. Hacker H, Vabulas RM, Takeuchi O, Hoshino K, Akira S, Wagner H, J Exp Med 2000 192 595 600 10.1084/jem.192.4.595 10952730 (Pubitemid 30666261)
20. Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. Vabulas RM, Ahmad-Nejad P, da Costa C, Miethke T, Kirschning CJ, Hacker H, Wagner H, J Biol Chem 2001 276 31332 31339 10.1074/jbc.M103217200 11402040 (Pubitemid 37385004)
21. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. Ohashi K, Burkart V, Flohe S, Kolb H, J Immunol 2000 164 558 561 10623794 (Pubitemid 30043672)
22. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. Smiley ST, King JA, Hancock WW, J Immunol 2001 167 2887 2894 11509636 (Pubitemid 32768923)
23. Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Midwood K, Sacre S, Piccinini AM, Inglis J, Trebaul A, Chan E, Drexler S, Sofat N, Kashiwagi M, Orend G, et al. Nat Med 2009 15 774 780 10.1038/nm.1987 19561617
24. Evidence that intrathecal morphine-3-glucuronide may cause pain enhancement via toll-like receptor 4/MD-2 and interleukin-1beta. Lewis SS, Hutchinson MR, Rezvani N, Loram LC, Zhang Y, Maier SF, Rice KC, Watkins LR, Neuroscience 2010 165 569 583 10.1016/j.neuroscience.2009.10.011 19833175
25. Naloxone ameliorates retinal lesions in Ccl2/Cx3cr1 double-deficient mice via modulation of microglia. Shen D, Cao X, Zhao L, Tuo J, Wong WT, Chan CC, Invest Ophthalmol Vis Sci 2011 52 2897 2904 10.1167/iovs.10-6114 21245403
26. Malignant bone pain: pathophysiology and treatment. Mercadante S, Pain 1997 69 1 18 10.1016/S0304-3959(96)03267-8 9060007 (Pubitemid 27081402)
27. Malignant bone pain: pathophysiology and treatments. Ripamonti C, Fulfaro F, Curr Rev Pain 2000 4 187 196 10.1007/s11916-000-0078-3 10998732
28. Differential activation of spinal cord glial cells in murine models of neuropathic and cancer pain. Hald A, Nedergaard S, Hansen RR, Ding M, Heegaard AM, Eur J Pain 2009 13 138 145 10.1016/j.ejpain.2008.03.014 18499488
29. Implications of immune-to-brain communication for sickness and pain. Watkins LR, Maier SF, Proc Natl Acad Sci U S A 1999 96 7710 7713 10.1073/pnas.96.14.7710 10393885 (Pubitemid 29328345)
30. Evidence for glutamate-mediated activation of hippocampal neurons by glial calcium waves. Hassinger TD, Atkinson PB, Strecker GJ, Whalen LR, Dudek FE, Kossel AH, Kater SB, J Neurobiol 1995 28 159 170 10.1002/neu.480280204 8537822
31. Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Parri HR, Gould TM, Crunelli V, Nat Neurosci 2001 4 803 812 10.1038/90507 11477426 (Pubitemid 32702512)
32. Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. Milligan ED, Twining C, Chacur M, Biedenkapp J, O'Connor K, Poole S, Tracey K, Martin D, Maier SF, Watkins LR, J Neurosci 2003 23 1026 1040 12574433 (Pubitemid 36206195)
33. Could chronic pain and spread of pain sensation be induced and maintained by glial activation? Hansson E, Acta Physiol (Oxf) 2006 187 321 327 10.1111/j.1748-1716.2006.01568.x (Pubitemid 43828790)
34. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. Olson JK, Miller SD, J Immunol 2004 173 3916 3924 15356140 (Pubitemid 39280755)
35. Toll-like receptor 4: the missing link of the cerebral innate immune response triggered by circulating gram-negative bacterial cell wall components. Laflamme N, Rivest S, FASEB J 2001 15 155 163 10.1096/fj.00-0339com 11149903 (Pubitemid 32061666)
36. Non-stereoselective reversal of neuropathic pain by naloxone and naltrexone: involvement of toll-like receptor 4 (TLR4). Hutchinson MR, Zhang Y, Brown K, Coats BD, Shridhar M, Sholar PW, Patel SJ, Crysdale NY, Harrison JA, Maier SF, et al. Eur J Neurosci 2008 28 20 29 10.1111/j.1460-9568.2008.06321.x 18662331
37. Down-regulation of Toll-like receptor 4 gene expression by short interfering RNA attenuates bone cancer pain in a rat model. Lan LS, Ping YJ, Na WL, Miao J, Cheng QQ, Ni MZ, Lei L, Fang LC, Guang RC, Jin Z, Wei L, Mol Pain 2010 6 2 10.1186/1744-8069-6-2 20089147
38. Tibia tumor-induced cancer pain involves spinal p38 mitogen-activated protein kinase activation via TLR4-dependent mechanisms. Liu S, Yang J, Wang L, Jiang M, Qiu Q, Ma Z, Liu L, Li C, Ren C, Zhou J, Li W, Brain Res 2010 1346 213 223 20478276
39. The innate immunity of the central nervous system in chronic pain: the role of Toll-like receptors. Guo LH, Schluesener HJ, Cell Mol Life Sci 2007 64 1128 1136 10.1007/s00018-007-6494-3 17440679 (Pubitemid 46684548)
40. A critical role of toll-like receptor 2 in nerve injury-induced spinal cord glial cell activation and pain hypersensitivity. Kim D, Kim MA, Cho IH, Kim MS, Lee S, Jo EK, Choi SY, Park K, Kim JS, Akira S, et al. J Biol Chem 2007 282 14975 14983 10.1074/jbc.M607277200 17355971 (Pubitemid 47093373)
41. Evidence for a role of heat shock protein-90 in toll like receptor 4 mediated pain enhancement in rats. Hutchinson MR, Ramos KM, Loram LC, Wieseler J, Sholar PW, Kearney JJ, Lewis MT, Crysdale NY, Zhang Y, Harrison JA, et al. Neuroscience 2009 164 1821 1832 10.1016/j.neuroscience.2009.09.046 19788917
42. Possible involvement of toll-like receptor 4/myeloid differentiation factor-2 activity of opioid inactive isomers causes spinal proinflammation and related behavioral consequences. Hutchinson MR, Lewis SS, Coats BD, Rezvani N, Zhang Y, Wieseler JL, Somogyi AA, Yin H, Maier SF, Rice KC, Watkins LR, Neuroscience 2010 167 880 893 10.1016/j.neuroscience.2010.02.011 20178837
43. Ethical guidelines for investigations of experimental pain in conscious animals. Zimmermann M, Pain 1983 16 109 110 10.1016/0304-3959(83)90201-4 6877845 (Pubitemid 13058546)
44. Blocking EphB1 receptor forward signaling in spinal cord relieves bone cancer pain and rescues analgesic effect of morphine treatment in rodents. Liu S, Liu WT, Liu YP, Dong HL, Henkemeyer M, Xiong LZ, Song XJ, Cancer Res 2011 71 4392 4402 10.1158/0008-5472.CAN-10-3870 21555368
45. Efficient analysis of experimental observations. Dixon WJ, Annu Rev Pharmacol Toxicol 1980 20 441 462 10.1146/annurev.pa.20.040180.002301 7387124
46. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Hargreaves K, Dubner R, Brown F, Flores C, Joris J, Pain 1988 32 77 88 10.1016/0304-3959(88)90026-7 3340425
47. Disruption of glial function enhances electroacupuncture analgesia in arthritic rats. Sun S, Chen WL, Wang PF, Zhao ZQ, Zhang YQ, Exp Neurol 2006 198 294 302 10.1016/j.expneurol.2005.11.011 16490194
48. Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maier SF, Watkins LR, Pain 2005 115 71 83 10.1016/j.pain.2005.02.009 15836971
49. Evidence that opioids may have toll-like receptor 4 and MD-2 effects. Hutchinson MR, Zhang Y, Shridhar M, Evans JH, Buchanan MM, Zhao TX, Slivka PF, Coats BD, Rezvani N, Wieseler J, et al. Brain Behav Immun 2010 24 83 95 10.1016/j.bbi.2009.08.004 19679181
50. Puncture of a lumbar intervertebral disc induces changes in spontaneous pain behavior: an experimental study in rats. Olmarker K, Spine (Phila Pa 1976) 2008 33 850 855 10.1097/BRS.0b013e31816b46ca (Pubitemid 351533852)
51. Spinal microglial expression and mechanical hypersensitivity in a postoperative pain model: comparison with a neuropathic pain model. Ito N, Obata H, Saito S, Anesthesiology 2009 111 640 648 10.1097/ALN.0b013e3181b05f42 19672178
52. Electroacupuncture downregulates TLR2/4 and pro-inflammatory cytokine expression after surgical trauma stress without adrenal glands involvement. Wang J, Zhao H, Mao-Ying QL, Cao XD, Wang YQ, Wu GC, Brain Res Bull 2009 80 89 94 10.1016/j.brainresbull.2009.04.020 19508885
53. Beta-adrenoceptor mediated surgery-induced production of pro-inflammatory cytokines in rat microglia cells. Wang J, Li J, Sheng X, Zhao H, Cao XD, Wang YQ, Wu GC, J Neuroimmunol 2010 223 77 83 10.1016/j.jneuroim.2010.04.006 20452680