β2- and β3-adrenergic receptors drive COMT-dependent pain by increasing production of nitric oxide and cytokines

Pain

Volumn 155, Issue 7, 2014, Pages 1346-1355

  Hartung, Jane E ^a   Ciszek, Brittney P ^a   Nackley, Andrea G ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Allodynia; Catecholamines; Chemokine (C C motif) ligand 2 (CCL2); Epinephrine; Hyperalgesia; Inflammation; Interleukin 1 beta (IL 1 ); Interleukin 6 (IL 6); Monocyte chemotactic protein 1 (MCP 1); Nitrate; Nitrite; Norepinephrine; Tumor necrosis factor alpha (TNF )

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; BETA 3 ADRENERGIC RECEPTOR; BETA 3 ADRENERGIC RECEPTOR BLOCKING AGENT; CATECHOL METHYLTRANSFERASE; CATECHOL METHYLTRANSFERASE INHIBITOR; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; N(G) NITROARGININE METHYL ESTER; NEUTRALIZING ANTIBODY; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR ALPHA; CCL2 PROTEIN, RAT; IL1B PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; INNATE IMMUNITY; MALE; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; HYPERALGESIA; METABOLISM; SPRAGUE DAWLEY RAT;

ADRENERGIC BETA-2 RECEPTOR ANTAGONISTS; ADRENERGIC BETA-3 RECEPTOR ANTAGONISTS; ANIMALS; CATECHOL O-METHYLTRANSFERASE; CATECHOL O-METHYLTRANSFERASE INHIBITORS; CHEMOKINE CCL2; CYTOKINES; HYPERALGESIA; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA-2; RECEPTORS, ADRENERGIC, BETA-3; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84902333751     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.04.011     Document Type: Article

References (84)

1. Y. Akimoto, T. Horinouchi, M. Shibano, M. Matsushita, Y. Yamashita, T. Okamoto, F. Yamaki, Y. Tanaka, and K. Koike Nitric oxide (NO) primarily accounts for endothelium dependent component of B-adrenoceptor-activated smooth muscle relaxation of mouse aorta in response to isoprenaline J Smooth Muscle Res 38 2002 87 99
2. K.O. Aley, A. Martin, T. McMahon, J. Mok, J.D. Levine, and R.O. Messing Nociceptor sensitization by extracellular signal-regulated kinases J Neurosci 21 2001 6933 6939
3. K.O. Aley, G. McCarter, and J.D. Levine Nitric oxide signaling in pain and nociceptor sensitization in the rat J Neurosci 18 1998 7008 7014
4. A.M. Binshtok, H. Wang, K. Zimmermann, F. Amaya, D. Vardeh, L. Shi, G.J. Brenner, R.R. Ji, B.P. Bean, C.J. Woolf, and T.A. Samad Nociceptors are interleukin-1β sensors J Neurosci 28 2008 14062 14073
5. D. Boehning, and S.H. Snyder Novel neural modulators Annu Rev Neurosci 26 2003 105 131
6. M.E. Bote, J.J. Garcia, M.D. Hinchado, and E. Ortega Inflammatory/stress feedback dysregulation in women with fibromyalgia Neuroimmunomodulation 19 2012 343 351
7. N.K. Canova, D. Lincova, E. Kmonickova, L. Kamenikova, and H. Farghali Nitric oxide production from rat adipocytes is modulated by β3-adrenergic receptor agonists and is involved in a cyclic AMP-dependent lipolysis in adipocytes Nitric oxide 14 2006 200 211
8. D. Chatterjea, L. Paredes, T. Martinov, E. Balsells, J. Allen, A. Sykes, and A. Ashbaugh TNF-alpha neutralizing antibody blocks thermal sensitivity induced by compound 48:80-provoked mast cell degranulation F1000 Res 2 2013 1 13
9. Y. Chen, M.K. Boettger, A. Reif, A. Schmitt, N. Uceyler, and C. Sommer Nitric oxide synthase modulates CFA-induced thermal hyperalgesia through cytokine regulation in mice Mol Pain 6 2010 13
10. B.P. Ciszek, and A.G. Nackley Chronic catechol-o-methyltransferase- dependent pain: a peripheral adrenergic contribution 2012 Society for Neuroscience New Orleans, LA
11. T.J. Coderre, A.I. Basbaum, M.F. Dallman, C. Helms, and J.D. Levine Epinephrine exacerbates arthritis by an action at presynaptic B2-adrenoceptors Neuroscience 34 1990 521 523
12. T.M. Cunha, W.A. Verri Jr, J.S. Silva, S. Poole, F.Q. Cunha, and S.H. Ferreira A cascade of cytokines mediates mechanical inflammatory hypernociception in mice Proc Natl Acad Sci U S A 102 2005 1755 1760
13. Y. Cury, G. Picolo, V.P. Gutierrez, and S.H. Ferreira Pain and analgesia: the dual effect of nitric oxide in the nociceptive system Nitric oxide 25 2011 243 254
14. J.C. Czeschik, T. Hagenacker, M. Schafers, and D. Busselberg TNF-alpha differentially modulates ion channels of nociceptive neurons Neurosci Lett 434 2008 293 298
15. M. Di Franco, C. Iannuccelli, and G. Valesini Neuroendocrine immunology of fibromyalgia Ann N Y Acad Sci 1193 2010 84 90
16. L. Diatchenko, G.D. Slade, A.G. Nackley, K. Bhalang, A. Sigurdsson, I. Belfer, D. Goldman, K. Xu, S.A. Shabalina, D. Shagin, M.B. Max, S.S. Makarov, and W. Maixner Genetic basis for individual variations in pain perception and the development of a chronic pain condition Hum Mol Genet 14 2005 135 143
17. C.A. Dinarello, M.J. Kluger, J.J. Oppenheim, and M.C. Powanda The physiological and pathological effects of cytokines 1990 Liss/John Wiley New York
18. R.A. Dixon, B.K. Kobilka, D.J. Strader, J.L. Benovic, H.G. Dohlman, T. Frielle, M.A. Bolanowski, C.D. Bennett, E. Rands, R.E. Diehl, R.A. Mumford, E.E. Slater, I.S. Sigal, M.S. Caron, R.J. Lefkowitz, and C.D. Strader Cloning of the gene and cDNA for mammalian beta-adrenergic receptor and homology with rhodopsin Nature 321 1986 75 79
19. D.S. Evaskus, and D.M. Laskin A biochemical measure of stress in patients with myofascial pain-dysfunction syndrome J Dent Res 51 1972 1464 1466
20. W. Fan, F. Huang, Z. Wu, X. Zhu, D. Li, and H. He The role of nitric oxide in orofacial pain Nitric oxide 26 2012 32 37
21. X.F. Figueroa, I. Poblete, R. Fernandez, C. Pedemonte, V. Cortes, and J.P. Huidobro-Toro NO production and eNOS phosphorylation induced by epinephrine through the activation of β-adrenoceptors Am J Physiol Heart Circ Physiol 297 2009 H134 H143
22. R.A. Frost, G.J. Nystrom, and C.H. Lang Epinephrine stimulates IL-6 expression in skeletal muscle and C2C12 myoblasts: role of c-Jun NH2-terminal kinase and histone deacetylase activity Am J Physiol Endocrinol Metab 2004 E809 E817
23. C. Furlan, L. Sterin-Borda, and E. Borda Activation of β3 adrenergic receptor decreases DNA synthesis in human skin fibroblasts via cyclic GMP/ nitric oxide pathway Cell Physiol Biochem 18 2005 175 182
24. Y.J. Gao, and R.R. Ji Chemokines, neuronal-glial interactions, and central processing of neuropathic pain Pharmacol Ther 126 2010 56 68
25. P.S. Grabowski, H. Macpherson, and S.H. Ralston Nitric oxide production in cells derived from the human joint Br J Rhuematol 35 1996 207 212
26. S. Gursoy, E. Erdal, H. Herken, E. Madenci, B. Alasehirli, and N. Erdal Significance of catechol-O-methyltransferase gene polymorphism in fibromyalgia syndrome Rheumatol Int 23 2003 104 107
27. K. Hargreaves, R. Dubner, F. Brown, C. Flores, and J. Joris A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia PAIN® 32 1988 77 88
28. G.J. Hodges, W.A. Kosiba, K. Zhao, and J.M. Johnson The involvement of norepinephrine, neuropeptide Y, and nitric oxide in the cutaneous vasodilator response to local heating in humans J Appl Physiol 105 2008 233 240
29. A. Holguin, K.A. O'Connor, J. Biedenkapp, J. Campisi, J. Wieseler-Frank, E.D. Milligan, M.K. Hansen, L. Spataro, E. Maksimova, C. Bravmann, D. Martin, M. Fleshner, S.F. Maier, and L.R. Watkins HIV-1 gp120 stimulates proinflammatory cytokine-mediated pain facilitation via activation of nitric oxide synthase-I (nNOS) PAIN® 110 2004 517 530
30. J.D. Johnson, V. Cortez, S.L. Kennedy, T.E. Foley, H. Hanson, and M. Fleshner Role of central beta-adrenergic receptors in regulating proinflammatory cytokine responses to a peripheral bacterial challenge Brain Behav Immun 22 2008 1078 1086
31. J.D. Johnson, Z.R. Zimomra, and L.T. Stewart Beta-adrenergic receptor activation primes microglia cytokine production J Neuroimmunol 254 2013 161 164
32. C. Jongeneel Transcriptional regulation of the tumor necrosis factor alpha gene Immunobiology 193 1995 210 216
33. H. Jung, P.T. Toth, F.A. White, and R.J. Miller Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons J Neurochem 104 2008 254 263
34. O. Kambur, R. Talka, O.B. Ansah, V.K. Kontinen, A. Pertovaara, E. Kalso, and P.T. Mannisto Inhibitors of catechol-O-methyltransferase sensitize mice to pain Br J Pharmacol 161 2010 1553 1565
35. T. Kanno, T. Yaguchi, and T. Nishizaki Noradrenaline stimulates ATP release from DRG neurons by targeting beta(3) adrenoceptors as a factor of neuropathic pain J Cell Physiol 224 2010 345 351
36. S.G. Khasar, Y.-H. Lin, A. Martin, J. Dadgar, T. McMahon, D. Wang, G. McCarter, P.G. Green, C.W. Hodge, J.D. Levine, and R.O. Messing A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice Neuron 24 1999 253 260
37. S.G. Khasar, G. McCarter, and J.D. Levine Epinephrine produces a B-Adrenergic receptor induced hyperalgesia and in vitro nociceptor sensitization J Neurophysiol 8 1999 1104 1112
38. B.K. Kobilka, R.A. Dixon, T. Frielle, H.G. Dohlman, M.A. Bolanowski, I.S. Sigal, T.L. Yang-Feng, U. Francke, M.G. Caron, and R.J. Lefkowitz CDNA for the human beta 2-adrenergic receptor: a protein with multiple membrane-spanning domains and encoded by a gene whose chromosomal location is shared with that of the receptor for platelet-derived growth factor Proc Natl Acad Sci U S A 84 1987 46 50
39. E. Kubota, T. Kubota, J. Matsumoto, T. Shibata, and K.I. Murakami Synovial fluid cytokines and proteinases as markers of temporomandibular joint disease J Oral Maxillofac Surg 56 1998 192 198
40. K. Kuboyama, M. Tsuda, M. Tsutsui, Y. Toyohara, H. Tozaki-Saitoh, H. Shimokawa, N. Yanagihara, and K. Inoue Reduced spinal microglial activation and neuropathic pain after nerve injury in mice lacking all three nitric oxide synthases Mol Pain 7 2011 50
41. S. Lamas, T. Michel, B.M. Brenner, and P.A. Marsden Nitric oxide synthesis in endothelial cells- evidence for a pathway inducible by TNF-a Am J Physiol Cell Physiol 261 1991 C634 C641
42. R. Landmann Beta-adrenergic receptors in human leukocyte subpopulations Eur J Clin Invest 22 1992 30 36
43. A.A. Larson, S.L. Giovengo, I.J. Russell, and J.E. Michalek Changes in the concentrations of amino acids in the cerebrospinal fluid that correlate with pain in patients with fibromyalgia- implications for nitric oxide pathways PAIN® 87 2000 201 211
44. W. Li, X. Shi, L. Wang, T. Guo, T. Wei, K. Cheng, K.C. Rice, W.S. Kingery, and J.D. Clark Epidermal adrenergic signaling contributes to inflammation and pain sensitization in a rat model of complex regional pain syndrome PAIN® 154 2013 1224 1236
45. K.C. Light, E.E. Bragdon, K.M. Grewen, K.A. Brownley, S.S. Girdler, and W. Maixner Adrenergic dysregulation and pain with and without acute beta-blockade in women with fibromyalgia and temporomandibular disorder J Pain 10 2009 542 552
46. T. Lindenlaub, P. Teuteberg, T. Hartung, and C. Sommer Effects of neutralizing antibodies to TNF-alpha on pain related behavior and nerve regeneration in mice with chronic constriction injury Brain Res 806 2000 15 22
47. C.J. Lowenstein, E.W. Alley, P. Raval, A.M. Snowman, S.H. Snyder, S.W. Russell, and W.J. Murphy Macrophage nitric oxide synthase gene - two upstream regions mediate induction by interferon y and lipopolysaccharide Proc Natl Acad Sci U S A 90 1993 9730 9734
48. D. Maimone, C. Cioni, S. Rosa, G. Macchia, F. Aloisi, and P. Annunziata Norepinephrine and vasoactive intestinal peptide induce IL-6 secretion by astrocytes: synergism with IL-1 beta and TNF alpha J Neuroimmunol 47 1993 73 81
49. P.T. Mannisto, and S. Kaakkola Catchechol-O-methyltransferase (COMT): biochemistry, molecular biology, pharmacology, and clinical efficacy of the new selective COMT inhibitors ASPET 51 1999 593 628
50. F. Marchand, M. Perretti, and S.B. McMahon Role of the immune system in chronic pain Nat Rev Neurosci 6 2005 521 532
51. S.B. McMahon, W.B. Cafferty, and F. Marchand Immune and glial cell factors as pain mediators and modulators Exp Neurol 192 2005 444 462
52. A.G. Nackley, K.S. Tan, K. Fecho, P. Flood, L. Diatchenko, and W. Maixner Catechol-O-methyltransferase inhibition increases pain sensitivity through activation of both β2- and β3-adrenergic receptors PAIN® 128 2007 199 208
53. D.M. Nance, and V.M. Sanders Autonomic innervation and regulation of the immune system (1987-2007) Brain Behav Immun 21 2007 736 745
54. A.P. Nicholas, T. Hokfelt, and V.A. Pieribone The distribution and significance of CNS adrenoceptors examined with in situ hybridization Trends Pharmacol Sci 17 1996 245 255
55. R. Nicholson, A.K. Dixon, D. Spanswick, and K. Lee Noradrenergic receptor mRNA expression in adult rat superficial dorsal horn and dorsal root ganglion neurons Neurosci Lett 380 2005 316 321
56. O. Obreja, W. Biasio, M. Andratsch, K.S. Lips, P.K. Rathee, A. Ludwig, S. Rose-John, and M. Kress Fast modulation of heat-activated ionic current by proinflammatory interleukin 6 in rat sensory neurons Brain 128 2005 1634 1641
57. O. Obreja, P.K. Rathee, K.S. Lips, C. Distler, and M. Kress IL-1B potentiates heat-activated currents in rat sensory neurons: involvement of IL-1RI, tyrosine kinase, and protein kinase C FASEB J 16 2002 1497 1503
58. K. Omote, K. Hazama, T. Kawamata, M. Kawamata, Y. Nakayaka, M. Toriyabe, and A. Namiki Peripheral nitric oxide in carrageenan-induced inflammation Brain Res 2001 171 175
59. D. Pflucke, D. Hackel, S.A. Mousa, A. Partheil, A. Neumann, A. Brack, and H.L. Rittner The molecular link between C-C-chemokine ligand 2-induced leukocyte recruitment and hyperalgesia J Pain 14 2013 897 910
60. T.C. Rainbow, B. Parsons, and B.B. Wolfe Quantitative autoradiography of beta 1- and beta 2-adrenergic receptors in rat brain Proc Natl Acad Sci U S A 81 1984 1585 1589
61. R. Ramachandran, K.B. Ploug, A. Hay-Schmidt, J. Olesen, I. Jansen-Olesen, and S. Gupta Nitric oxide synthase (NOS) in the trigeminal vascular system and other brain structures related to pain in rats Neurosci Lett 484 2010 192 196
62. R.J. Roth Flach, A. Matevossian, T.E. Akie, K.A. Negrin, M.T. Paul, and M.P. Czech beta3-Adrenergic receptor stimulation induces E-selectin-mediated adipose tissue inflammation J Biol Chem 288 2013 2882 2892
63. A.K. Salm, and K.D. McCarthy The evidence for astrocytes as a target for central noradrenergic activity: expression of adrenergic receptors Brain Res Bull 29 1992 265 275
64. P. Sarchielli, A. Alberti, A. Baldi, F. Coppola, C. Rossi, L. Pierguidi, A. Floridi, and P. Calabresi Proinflammatory cytokines, adhesion molecules, and lymphocyte integrin expression in the internal jugular blood of migraine patients without aura assessed ictally Headache 46 2006 200 207
65. A. Schmidtko, I. Tegeder, and G. Geisslinger No NO, no pain? The role of nitric oxide and cGMP in spinal pain processing Trends Neurosci 32 2009 339 346
66. D. Shafer, L. Assael, L.B. White, and E.F. Rossomando Tumor necrosis factor-a as a biochemical marker of pain and outcome in temporomandibular joints with internal derangements J Oral Maxillofac Surg 52 1994 786 791
67. G.D. Slade, M.S. Conrad, L. Diatchenko, N.U. Rashid, S. Zhong, S. Smith, J. Rhodes, A. Medvedev, S. Makarov, W. Maixner, and A.G. Nackley Cytokine biomarkers and chronic pain: association of genes, transcription, and circulating proteins with temporomandibular disorders and widespread palpation tenderness PAIN® 152 2011 2802 2812
68. C. Sommer, T. Lindenlaub, P. Teuteberg, M. Schafers, T. Hartung, and K.V. Toyka Anti-TNF neutralizing antibodies reduce pain-related behavior in two different mouse models of painful mononeuropathy Brain Res 913 2001 86 89
69. R. Staud Fibromyalgia pain: do we know the source? Curr Opin Rheumatol 16 2004 157 163
70. E.A. Stone, and M.A. Ariano Are glial cells targets of the central noradrenergic system? A review of the evidence Brain Res Rev 14 1989 297 309
71. A.D. Strosberg Structure and function of the β3-adrenergic receptor Annu Rev Pharmacol Toxicol 37 1997 421 450
72. J.H. Sun, B. Yang, D.F. Donnelly, C. Ma, and R.H. LaMotte MCP-1 enhances excitability of nociceptive neurons in chronically compressed dorsal root ganglia J Neurophysiol 96 2006 2189 2199
73. C.S. Sung, Z.H. Wen, W.K. Chang, K.H. Chan, S.T. Ho, S.K. Tsai, Y.C. Chang, and C.S. Wong Inhibition of p38 mitogen-activated protein kinase attenuates interleukin-1β-induced thermal hyperalgesia and inducible nitric oxide synthase expression in the spinal cord J Neurochem 94 2005 742 752
74. K.S. Tan, A.G. Nackley, K. Satterfield, W. Maixner, L. Diatchenko, and P.M. Flood β2 adrenergic receptor activation stimulates proinflammatory cytokine production in macrophages via PKA- and NF-kappaB-independent mechanisms Cell Signal 19 2007 251 260
75. I.E. Tchivileva, P.F. Lim, S.B. Smith, G.D. Slade, L. Diatchenko, S.A. McLean, and W. Maixner Effect of catechol-O-methyltransferase polymorphism on response to propranolol therapy in chronic musculoskeletal pain: a randomized, double-blind, placebo-controlled, crossover pilot study Pharmacogenet Genomics 20 2010 239 248
76. I.E. Tchivileva, K.S. Tan, M. Gambarian, A.G. Nackley, A.V. Medvedev, S. Romanov, P.M. Flood, W. Maixner, S.S. Makarov, and L. Diatchenko Signaling pathways mediating β3-adrenergic receptor-induced production of interleukin-6 in adipocytes Mol Immunol 46 2009 2256 2266
77. M.M. Teixeira, T.J. Williams, and P.G. Hellewell Role of prostaglandins and nitric oxide in acute inflammatory reactions in guinea-pig skin Br J Pharmacol 110 1993 1515 1521
78. D.J. Torpy, D.A. Papanicolaou, A.J. Lotsikas, R.L. Wilder, G.P. Chrousos, and S.R. Pillemer Responses of the sympathetic nervous system and the hypothalamic-pituitary-adrenal axis to interleukin-6 Arthritis Rheum 43 2000 872 880
79. E. Uzar, O. Evliyaoglu, Y. Yucel, M. Ugur Cevik, A. Acar, I. Guzel, Y. Islamoglu, L. Colpan, and N. Tasdemir Serum cytokine and pro-brain natriuretic peptide (BNP) levels in patients with migraine Eur Rev Med Pharmacol Sci 10 2011 1111 1116
80. G. Vargas-Alarcon, J.M. Fragoso, D. Cruz-Robles, A. Vargas, A. Vargas, J.I. Lao-Villadoniga, F. Garcia-Fructuoso, M. Ramos-Kuri, F. Hernandez, R. Springall, R. Bojalil, M. Vallejo, and M. Martinez-Lavin Catechol-O- methyltransferase gene haplotypes in Mexican and Spanish patients with fibromyalgia Arthritis Res Ther 9 2007 R110
81. J. Wang, J. Li, X. Sheng, H. Zhao, X.D. Cao, Y.Q. Wang, and G.C. Wu β-adrenoceptor mediated surgery-induced production of proinflammatory cytokines in rat microglia cells J Neuroimmunol 223 2010 77 83
82. L.R. Watkins, M.K. Hansen, K.T. Ngyuen, J.E. Lee, and S.F. Maier Dynamic regulation of the proinflammatory cytokine, interleukin-1B: molecular biology for non-molecular biologists Life Sci 65 1999 449 481
83. E.S. Wohleb, M.L. Hanke, A.W. Corona, N.D. Powell, L.M. Stiner, M.T. Bailey, R.J. Nelson, J.P. Godbout, and J.F. Sheridan β-adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat J Neurosci 31 2011 6277 6288
84. P.B. Wood, A.S. Kablinger, and G.S. Caldito Open trial of pindolol in the treatment of fibromyalgia Ann Pharmacother 39 2005 1812 1816