Cancer-induced bone pain: Mechanisms and models

Neuroscience Letters

Volumn 557, Issue , 2013, Pages 52-59

  Lozano Ondoua, A N ^a   Symons Liguori, A M ^a   Vanderah, T W ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

ASIC; Cytokines; Glutamate; NGF; Oxidative Stress; Syngenic tumor model

Indexed keywords

ACID SENSING ION CHANNEL; ANTIPORTER; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CAPSAZEPINE; GLUTAMIC ACID; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; PROTEIN TYROSINE KINASE A; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VANILLOID RECEPTOR 1;

ALLODYNIA; BONE METASTASIS; BONE PAIN; CANCER INDUCED BONE PAIN; CANCER PAIN; CANCER PATIENT; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; HUMAN; NERVE SPROUTING; NEUROCHEMISTRY; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OXIDATIVE STRESS; PAIN RECEPTOR; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SENSORY NERVE; TUMOR MICROENVIRONMENT; UPREGULATION;

ASIC; CYTOKINES; GLUTAMATE; NGF; OXIDATIVE STRESS; SYNGENIC TUMOR MODEL;

ACID SENSING ION CHANNELS; ANIMALS; BONE NEOPLASMS; CYTOKINES; DISEASE MODELS, ANIMAL; HUMANS; MICE; NERVE GROWTH FACTORS; OXIDATIVE STRESS; PAIN; RATS;

EID: 84890250635     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2013.08.003     Document Type: Review

References (107)

1. Abdelmagid S.A., Rickard J.A., McDonald W.J., Thomas L.N., Too C.K. CAT-1-mediated arginine uptake and regulation of nitric oxide synthases for the survival of human breast cancer cell lines. J. Cell. Biochem. 2011, 112:1084-1092.
2. Alsina M., Boyce B., Devlin R.D., Anderson J.L., Craig F., Mundy G.R., Roodman G.D. Development of an in vivo model of human multiple myeloma bone disease. Blood 1996, 87:1495-1501.
3. Ambs S., Glynn S.A. Candidate pathways linking inducible nitric oxide synthase to a basal-like transcription pattern and tumor progression in human breast cancer. Cell Cycle 2011, 10:619-624.
4. Arai K.I., Lee F., Miyajima A., Miyatake S., Arai N., Yokota T. Cytokines: coordinators of immune and inflammatory responses. Ann. Rev. Biochem. 1990, 59:783-836.
5. Asai H., Ozaki N., Shinoda M., Nagamine K., Tohnai I., Ueda M., Sugiura Y. Heat and mechanical hyperalgesia in mice model of cancer pain. Pain 2005, 117:19-29.
6. Baamonde A., Curto-Reyes V., Juarez L., Meana A., Hidalgo A., Menendez L. Antihyperalgesic effects induced by the IL-1 receptor antagonist anakinra and increased IL-1beta levels in inflamed and osteosarcoma-bearing mice. Life Sci. 2007, 81:673-682.
7. Balendiran G.K., Dabur R., Fraser D. The role of glutathione in cancer. Cell Biochem. Funct. 2004, 22:343-352.
8. Bevan S., Geppetti P. Protons: small stimulants of capsaicin-sensitive sensory nerves. Trends Neurosci. 1994, 17:509-512.
9. Black J.A., Nikolajsen L., Kroner K., Jensen T.S., Waxman S.G. Multiple sodium channel isoforms and mitogen-activated protein kinases are present in painful human neuromas. Ann. Neurol. 2008, 64:644-653.
10. Bleakman D., Alt A., Nisenbaum E.S. Glutamate receptors and pain. Semin. Cell Dev. Biol. 2006, 17:592-604.
11. Bloom A.P., Jimenez-Andrade J.M., Taylor R.N., Castaneda-Corral G., Kaczmarska M.J., Freeman K.T., Coughlin K.A., Ghilardi J.R., Kuskowski M.A., Mantyh P.W. Breast cancer-induced bone remodeling, skeletal pain, and sprouting of sensory nerve fibers. J. Pain 2011, 12:698-711.
12. Boucharaba A., Serre C.M., Gres S., Saulnier-Blache J.S., Bordet J.C., Guglielmi J., Clezardin P., Peyruchaud O. Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer. J. Clin. Invest. 2004, 114:1714-1725.
13. Boyle W.J., Simonet W.S., Lacey D.L. Osteoclast differentiation and activation. Nature 2003, 423:337-342.
14. Brahimi-Horn M.C., Chiche J., Pouyssegur J. Hypoxia and cancer. J. Mol. Med. (Berl) 2007, 85:1301-1307.
15. Brahimi-Horn M.C., Chiche J., Pouyssegur J. Hypoxia signalling controls metabolic demand. Curr. Opin. Cell Biol. 2007, 19:223-229.
16. Brahimi-Horn M.C., Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett. 2007, 581:3582-3591.
17. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
18. Ceyhan G.O., Bergmann F., Kadihasanoglu M., Altintas B., Demir I.E., Hinz U., Muller M.W., Giese T., Buchler M.W., Giese N.A., Friess H. Pancreatic neuropathy and neuropathic pain - a comprehensive pathomorphological study of 546 cases. Gastroenterology 2009, 136:177-186. e171.
19. Chiechio S., Nicoletti F. Metabotropic glutamate receptors and the control of chronic pain. Curr. Opin. Pharmacol. 2012, 12:28-34.
20. Coleman R.E., Purohit O.P. Osteoclast inhibition for the treatment of bone metastases. Cancer Treat. Rev. 1993, 19:79-103.
21. Constantin C.E., Mair N., Sailer C.A., Andratsch M., Xu Z.Z., Blumer M.J., Scherbakov N., Davis J.B., Bluethmann H., Ji R.R., 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, 28:5072-5081.
22. Cowan R.W., Seidlitz E.P., Singh G. Glutamate signaling in healthy and diseased bone. Front. Endocrinol. 2012, 3:89.
23. Deval E., Gasull X., Noel J., Salinas M., Baron A., Diochot S., Lingueglia E. Acid-sensing ion channels (ASICs): pharmacology and implication in pain. Pharmacol. Ther. 2010, 128:549-558.
24. Doyle T., Chen Z., Muscoli C., Bryant L., Esposito E., Cuzzocrea S., Dagostino C., Ryerse J., Rausaria S., Kamadulski A., Neumann W.L., Salvemini D. Targeting the overproduction of peroxynitrite for the prevention and reversal of paclitaxel-induced neuropathic pain. J. Neurosci. 2012, 32:6149-6160.
25. Dunn L.K., Mohammad K.S., Fournier P.G., McKenna C.R., Davis H.W., Niewolna M., Peng X.H., Chirgwin J.M., Guise T.A. Hypoxia and TGF-beta drive breast cancer bone metastases through parallel signaling pathways in tumor cells and the bone microenvironment. PLoS One 2009, 4:e6896.
26. Eder A.M., Sasagawa T., Mao M., Aoki J., Mills G.B. Constitutive and lysophosphatidic acid (LPA)-induced LPA production: role of phospholipase D and phospholipase A2. Clin. Cancer Res. 2000, 6:2482-2491.
27. Fang X., Schummer M., Mao M., Yu S., Tabassam F.H., Swaby R., Hasegawa Y., Tanyi J.L., LaPushin R., Eder A., Jaffe R., Erickson J., Mills G.B. Lysophosphatidic acid is a bioactive mediator in ovarian cancer. Biochim. Biophys. Acta 2002, 1582:257-264.
28. Fundytus M.E. Glutamate receptors and nociception: implications for the drug treatment of pain. CNS Drugs 2001, 15:29-58.
29. Geis C., Graulich M., Wissmann A., Hagenacker T., Thomale J., Sommer C., Schafers M. Evoked pain behavior and spinal glia activation is dependent on tumor necrosis factor receptor 1 and 2 in a mouse model of bone cancer pain. Neuroscience 2010, 169:463-474.
30. Ghilardi J.R., Freeman K.T., Jimenez-Andrade J.M., Mantyh W.G., Bloom A.P., Kuskowski M.A., Mantyh P.W. Administration of a tropomyosin receptor kinase inhibitor attenuates sarcoma-induced nerve sprouting, neuroma formation and bone cancer pain. Mol. Pain 2010, 6:87.
31. Ghilardi J.R., Rohrich H., Lindsay T.H., Sevcik M.A., Schwei M.J., Kubota K., Halvorson K.G., Poblete J., Chaplan S.R., Dubin A.E., Carruthers N.I., Swanson D., Kuskowski M., Flores C.M., Julius D., Mantyh P.W. Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain. J. Neurosci. 2005, 25:3126-3131.
32. Gu X., Zheng Y., Ren B., Zhang R., Mei F., Zhang J., Ma Z. Intraperitoneal injection of thalidomide attenuates bone cancer pain and decreases spinal tumor necrosis factor-alpha expression in a mouse model. Mol. Pain 2010, 6:64.
33. Guo C.H., Hsia S., Chen P.C. Distribution of selenium and oxidative stress in breast tumor-bearing mice. Nutrients 2013, 5:594-607.
34. Hacimuftuoglu A., Handy C.R., Goettl V.M., Lin C.G., Dane S., Stephens R.L. Antioxidants attenuate multiple phases of formalin-induced nociceptive response in mice. Behav. Brain Res. 2006, 173:211-216.
35. Halvorson K.G., Kubota K., Sevcik M.A., Lindsay T.H., Sotillo J.E., Ghilardi J.R., Rosol T.J., Boustany L., Shelton D.L., Mantyh P.W. A blocking antibody to nerve growth factor attenuates skeletal pain induced by prostate tumor cells growing in bone. Cancer Res. 2005, 65:9426-9435.
36. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
37. Hasan H.R., Mathkor T.H., Al-Habal M.H. Superoxide dismutase isoenzyme activities in plasma and tissues of Iraqi patients with breast cancer. Asian Pac. J. Cancer Prev. 2012, 13:2571-2576.
38. Hongo J.S., Laramee G.R., Urfer R., Shelton D.L., Restivo T., Sadick M., Galloway A., Chu H., Winslow J.W. Antibody binding regions on human nerve growth factor identified by homolog- and alanine-scanning mutagenesis. Hybridoma 2000, 19:215-227.
39. Honore P., Rogers S.D., Schwei M.J., Salak-Johnson J.L., Luger N.M., Sabino M.C., Clohisy D.R., Mantyh P.W. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 2000, 98:585-598.
40. Hu J.H., Yang J.P., Liu L., Li C.F., Wang L.N., Ji F.H., Cheng H. Involvement of CX3CR1 in bone cancer pain through the activation of microglia p38 MAPK pathway in the spinal cord. Brain Res. 2012, 1465:1-9.
41. Hu J.H., Zheng X.Y., Yang J.P., Wang L.N., Ji F.H. Involvement of spinal monocyte chemoattractant protein-1 (MCP-1) in cancer-induced bone pain in rats. Neurosci. Lett. 2012, 517:60-63.
42. Idris A.I., Landao-Bassonga E., Ralston S.H. 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.
43. Ishii T., Sugita Y., Bannai S. Regulation of glutathione levels in mouse spleen lymphocytes by transport of cysteine. J. Cell. Physiol. 1987, 133:330-336.
44. Jahr H., van Driel M., van Osch G.J., Weinans H., van Leeuwen J.P. Identification of acid-sensing ion channels in bone. Biochem. Biophys. Res. Commun. 2005, 337:349-354.
45. Jimenez-Andrade J.M., Bloom A.P., Stake J.I., Mantyh W.G., Taylor R.N., Freeman K.T., Ghilardi J.R., Kuskowski M.A., Mantyh P.W. Pathological sprouting of adult nociceptors in chronic prostate cancer-induced bone pain. J. Neurosci. 2010, 30:14649-14656.
46. Jimenez-Andrade J.M., Ghilardi J.R., Castaneda-Corral G., Kuskowski M.A., Mantyh P.W. Preventive or late administration of anti-NGF therapy attenuates tumor-induced nerve sprouting, neuroma formation, and cancer pain. Pain 2011, 152:2564-2574.
47. Jimenez-Andrade J.M., Mantyh P.W. Sensory and sympathetic nerve fibers undergo sprouting and neuroma formation in the painful arthritic joint of geriatric mice. Arthritis Res. Ther. 2012, 14:R101.
48. Kallenborn-Gerhardt W., Schroder K., Geisslinger G., Schmidtko A. NOXious signaling in pain processing. Pharmacol Ther. 2013, 137:309-317.
49. Kerba M., Wu J.S., Duan Q., Hagen N.A., Bennett M.I. Neuropathic pain features in patients with bone metastases referred for palliative radiotherapy. J. Clin. Oncol. 2010, 28:4892-4897.
50. Khattab M.M. TEMPOL, a membrane-permeable radical scavenger, attenuates peroxynitrite- and superoxide anion-enhanced carrageenan-induced paw edema and hyperalgesia: a key role for superoxide anion. Eur. J. Pharmacol. 2006, 548:167-173.
51. Kim S.H., Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50:355-363.
52. Krieger N.S., Sessler N.E., Bushinsky D.A. Acidosis inhibits osteoblastic and stimulates osteoclastic activity in vitro. Am. J. Physiol. 1992, 262:F442-F448.
53. Krishtal O.A., Pidoplichko V.I. A receptor for protons in the nerve cell membrane. Neuroscience 1980, 5:2325-2327.
54. Kroemer G., Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008, 13:472-482.
55. Lautner M.A., Ruparel S.B., Patil M.J., Hargreaves K.M. In vitro sarcoma cells release a lipophilic substance that activates the pain transduction system via TRPV1. Ann. Surg. Oncol. 2011, 18:866-871.
56. Lindqvist A., Rivero-Melian C., Turan I., Fried K. Neuropeptide- and tyrosine hydroxylase-immunoreactive nerve fibers in painful Morton's neuromas. Muscle Nerve 2000, 23:1214-1218.
57. Little J.W., Chen Z., Doyle T., Porreca F., Ghaffari M., Bryant L., Neumann W.L., Salvemini D. Supraspinal peroxynitrite modulates pain signaling by suppressing the endogenous opioid pathway. J. Neurosci. 2012, 32:10797-10808.
58. Little J.W., Doyle T., Salvemini D. Reactive nitroxidative species and nociceptive processing: determining the roles for nitric oxide, superoxide, and peroxynitrite in pain. Amino Acids 2012, 42:75-94.
59. Liu X., Bu H., Liu C., Gao F., Yang H., Tian X., Xu A., Chen Z., Cao F., Tian Y. Inhibition of glial activation in rostral ventromedial medulla attenuates mechanical allodynia in a rat model of cancer-induced bone pain. J. Huazhong Univ. Sci. Technol. Med. Sci. 2012, 32:291-298.
60. Lo M., Wang Y.Z., Gout P.W. The x(c)- cystine/glutamate antiporter: a potential target for therapy of cancer and other diseases. J. Cell. Physiol. 2008, 215:593-602.
61. Lozano-Ondoua A.N., Hanlon K.E., Symons-Liguori A.M., Largent-Milnes T.M., Havelin J.J., Ferland H.L., Chandramouli A., Owusu-Ankomah M., Nikolich-Zugich T., Bloom A.P., Jimenez-Andrade J.M., King T., Porreca F., Nelson M.A., Mantyh P.W., Vanderah T.W. Disease modification of breast cancer-induced bone remodeling by cannabinoid 2 receptor agonists. J. Bone Miner. Res. 2013, 28:92-107.
62. Mach D.B., Rogers S.D., Sabino M.C., Luger N.M., Schwei M.J., Pomonis J.D., Keyser C.P., Clohisy D.R., Adams D.J., O'Leary P., Mantyh P.W. Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience 2002, 113:155-166.
63. Mamet J., Baron A., Lazdunski M., Voilley N. Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J. Neurosci. 2002, 22:10662-10670.
64. Mantyh P.W., Koltzenburg M., Mendell L.M., Tive L., Shelton D.L. Antagonism of nerve growth factor-TrkA signaling and the relief of pain. Anesthesiology 2011, 115:189-204.
65. Mantyh W.G., Jimenez-Andrade J.M., Stake J.I., Bloom A.P., Kaczmarska M.J., Taylor R.N., Freeman K.T., Ghilardi J.R., Kuskowski M.A., Mantyh P.W. Blockade of nerve sprouting and neuroma formation markedly attenuates the development of late stage cancer pain. Neuroscience 2010, 171:588-598.
66. Mercadante S. Malignant bone pain: pathophysiology and treatment. Pain 1997, 69:1-18.
67. Mundy G.R. Pathophysiology of cancer-associated hypercalcemia. Semin. Oncol. 1990, 17:10-15.
68. Nagae M., Hiraga T., Yoneda T. Acidic microenvironment created by osteoclasts causes bone pain associated with tumor colonization. J. Bone Miner. Metab. 2007, 25:99-104.
69. O'Connell J.X., Nanthakumar S.S., Nielsen G.P., Rosenberg A.E. Osteoid osteoma: the uniquely innervated bone tumor. Mod. Pathol. 1998, 11:175-180.
70. Olson T.H., Riedl M.S., Vulchanova L., Ortiz-Gonzalez X.R., Elde R. An acid sensing ion channel (ASIC) localizes to small primary afferent neurons in rats. Neuroreport 1998, 9:1109-1113.
71. Omori M., Yokoyama M., Matsuoka Y., Kobayashi H., Mizobuchi S., Itano Y., Morita K., Ichikawa H. Effects of selective spinal nerve ligation on acetic acid-induced nociceptive responses and ASIC3 immunoreactivity in the rat dorsal root ganglion. Brain Res. 2008, 1219:26-31.
72. Osikowicz M., Mika J., Przewlocka B. The glutamatergic system as a target for neuropathic pain relief. Exp. Physiol. 2013, 98:372-384.
73. Palazzo E., Luongo L., de Novellis V., Rossi F., Marabese I., Maione S. Transient receptor potential vanilloid type 1 and pain development. Curr. Opin. Pharmacol. 2012, 12:9-17.
74. Pan H.L., Zhang Y.Q., Zhao Z.Q. 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.
75. Poirot O., Berta T., Decosterd I., Kellenberger S. Distinct ASIC currents are expressed in rat putative nociceptors and are modulated by nerve injury. J. Physiol. 2006, 576:215-234.
76. Portenoy R.K., Hagen N.A. Breakthrough pain: definition, prevalence and characteristics. Pain 1990, 41:273-281.
77. Portenoy R.K., Lesage P. Management of cancer pain. Lancet 1999, 353:1695-1700.
78. Price T.J., Louria M.D., Candelario-Soto D., Dussor G.O., Jeske N.A., Patwardhan A.M., Diogenes A., Trott A.A., Hargreaves K.M., Flores C.M. Treatment of trigeminal ganglion neurons in vitro with NGF, GDNF or BDNF: effects on neuronal survival, neurochemical properties and TRPV1-mediated neuropeptide secretion. BMC Neurosci. 2005, 6:4.
79. Rausaria S., Ghaffari M.M., Kamadulski A., Rodgers K., Bryant L., Chen Z., Doyle T., Shaw M.J., Salvemini D., Neumann W.L. Retooling manganese(III) porphyrin-based peroxynitrite decomposition catalysts for selectivity and oral activity: a potential new strategy for treating chronic pain. J. Med. Chem. 2011, 54:8658-8669.
80. Reeh P.W., Steen K.H. Tissue acidosis in nociception and pain. Prog. Brain Res. 1996, 113:143-151.
81. Ren B.X., Gu X.P., Zheng Y.G., Liu C.L., Wang D., Sun Y.E., Ma Z.L. 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 2012, 116:122-132.
82. Ryu C.S., Kwak H.C., Lee J.Y., Oh S.J., Phuong N.T., Kang K.W., Kim S.K. Elevation of cysteine consumption in tamoxifen-resistant MCF-7 cells. Biochem. Pharmacol. 2013, 85:197-206.
83. Salvemini D., Neumann W. Targeting peroxynitrite driven nitroxidative stress with synzymes: a novel therapeutic approach in chronic pain management. Life Sci. 2010, 86:604-614.
84. Scheid T., Bosco L.D., Guedes R.P., Pavanato M.A., Bello-Klein A., Partata W.A. Sciatic Nerve Transection Modulates Oxidative Parameters in Spinal and Supraspinal Regions 2013, Neurochem. Res.
85. Schiller K.R., Zillhardt M.R., Alley J., Borjesson D.L., Beitz A.J., Mauro L.J. Secretion of MCP-1 and other paracrine factors in a novel tumor-bone coculture model. BMC Cancer 2009, 9:45.
86. Schwei M.J., Honore P., Rogers S.D., Salak-Johnson J.L., Finke M.P., Ramnaraine M.L., Clohisy D.R., Mantyh P.W. Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. J. Neurosci. 1999, 19:10886-10897.
87. Seidlitz E.P., Sharma M.K., Singh G. Extracellular glutamate alters mature osteoclast and osteoblast functions. Can. J. Physiol. Pharmacol. 2010, 88:929-936.
88. Sevcik M.A., Ghilardi J.R., Peters C.M., Lindsay T.H., Halvorson K.G., Jonas B.M., Kubota K., Kuskowski M.A., Boustany L., Shelton D.L., Mantyh P.W. Anti-NGF therapy profoundly reduces bone cancer pain and the accompanying increase in markers of peripheral and central sensitization. Pain 2005, 115:128-141.
89. Sharma M.K., Seidlitz E.P., Singh G. Cancer cells release glutamate via the cystine/glutamate antiporter. Biochem. Biophys. Res. Commun. 2010, 391:91-95.
90. Shinoda M., Ogino A., Ozaki N., Urano H., Hironaka K., Yasui M., Sugiura Y. Involvement of TRPV1 in nociceptive behavior in a rat model of cancer pain. J. Pain 2008, 9:687-699.
91. Skaper S.D. The neurotrophin family of neurotrophic factors: an overview. Methods Mol. Biol. 2012, 846:1-12.
92. Stucky C.L., Lewin G.R. Isolectin B(4)-positive and -negative nociceptors are functionally distinct. J. Neurosci. 1999, 19:6497-6505.
93. Swanson D.M., Dubin A.E., Shah C., Nasser N., Chang L., Dax S.L., Jetter M., Breitenbucher J.G., Liu C., Mazur C., Lord B., Gonzales L., Hoey K., Rizzolio M., Bogenstaetter M., Codd E.E., Lee D.H., Zhang S.P., Chaplan S.R., Carruthers N.I. Identification and biological evaluation of 4-(3-trifluoromethylpyridin-2-yl)piperazine-1-carboxylic acid (5-trifluoromethylpyridin-2-yl)amide, a high affinity TRPV1 (VR1) vanilloid receptor antagonist. J. Med. Chem. 2005, 48:1857-1872.
94. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998, 21:531-543.
95. Trotti D., Rossi D., Gjesdal O., Levy L.M., Racagni G., Danbolt N.C., Volterra A. Peroxynitrite inhibits glutamate transporter subtypes. J. Biol. Chem. 1996, 271:5976-5979.
96. Ungard R.G., Seidlitz E.P., Singh G. Oxidative stress and cancer pain. Can. J. Physiol. Pharmacol. 2013, 91:31-37.
97. Verri W.A., Cunha T.M., Parada C.A., Poole S., Cunha F.Q., Ferreira S.H. Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development?. Pharmacol. Ther. 2006, 112:116-138.
98. Waldmann R., Champigny G., Bassilana F., Heurteaux C., Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature 1997, 386:173-177.
99. Wang L.N., Yang J.P., Ji F.H., Zhan Y., Jin X.H., Xu Q.N., Wang X.Y., Zuo J.L. Brain-derived neurotrophic factor modulates N-methyl-d-aspartate receptor activation in a rat model of cancer-induced bone pain. J. Neurosci. Res. 2012, 90:1249-1260.
100. Wang Z.Q., Porreca F., Cuzzocrea S., Galen K., Lightfoot R., Masini E., Muscoli C., Mollace V., Ndengele M., Ischiropoulos H., Salvemini D. A newly identified role for superoxide in inflammatory pain. J. Pharmacol. Exp. Ther. 2004, 309:869-878.
101. Warburg O., Wind F., Negelein E. The metabolism of tumors in the body. J. Gen. Physiol. 1927, 8:519-530.
102. Watkins L.R., Wiertelak E.P., Goehler L.E., Smith K.P., Martin D., Maier S.F. Characterization of cytokine-induced hyperalgesia. Brain Res. 1994, 654:15-26.
103. Yeo J.F., Ling S.F., Tang N., Ong W.Y. Antinociceptive effect of CNS peroxynitrite scavenger in a mouse model of orofacial pain. Exp. Brain Res. 2008, 184:435-438.
104. Yin Q., Cheng W., Cheng M.Y., Fan S.Z., Shen W. Intrathecal injection of anti-CX3CR1 neutralizing antibody delayed and attenuated pain facilitation in rat tibial bone cancer pain model. Behav. Pharmacol. 2010, 21:595-601.
105. Zanelli S.A., Ashraf Q.M., Delivoria-Papadopoulos M., Mishra O.P. Peroxynitrite-induced modification of the N-methyl-d-aspartate receptor in the cerebral cortex of the guinea pig fetus at term. Neurosci. Lett. 2000, 296:5-8.
106. Zanelli S.A., Ashraf Q.M., Mishra O.P. Nitration is a mechanism of regulation of the NMDA receptor function during hypoxia. Neuroscience 2002, 112:869-877.
107. Zelenka M., Schafers M., Sommer C. Intraneural injection of interleukin-1beta and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 2005, 116:257-263.