Nociceptor Sensory Neuron–Immune Interactions in Pain and Inflammation

Trends in Immunology

Volumn 38, Issue 1, 2017, Pages 5-19

  Pinho Ribeiro, Felipe A ^a,b   Verri, Waldiceu A ^b   Chiu, Isaac M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b STATE UNIVERSITY OF LONDRINA   (Brazil)

Author keywords

inflammation; neuroimmunology; nociceptor; pain; sensory neuron

Indexed keywords

CYTOKINE; GROWTH FACTOR; ION CHANNEL; LIPID; NEUROTRANSMITTER; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; NEUROPEPTIDE;

CHRONIC PAIN; HOST PATHOGEN INTERACTION; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFLAMMATION; LYMPH VESSEL; MICROGLIA; NOCICEPTION; PAIN RECEPTOR; PERIPHERAL NERVOUS SYSTEM; REVIEW; SENSITIZATION; SENSORY NERVE CELL; VASCULARIZATION; ADAPTIVE IMMUNITY; ANIMAL; HUMAN; IMMUNE SYSTEM; IMMUNOLOGY; IMMUNOMODULATION; INNATE IMMUNITY; METABOLISM; PAIN;

ADAPTIVE IMMUNITY; ANIMALS; HUMANS; IMMUNE SYSTEM; IMMUNITY, INNATE; INFLAMMATION; NEUROIMMUNOMODULATION; NEUROPEPTIDES; NEUROTRANSMITTER AGENTS; NOCICEPTORS; PAIN; SENSORY RECEPTOR CELLS;

EID: 85006043792     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2016.10.001     Document Type: Review

References (115)

1. 1 Wood, J.N., et al. Voltage-gated sodium channels and pain pathways. J. Neurobiol. 61 (2004), 55–71.
2. 2 Cunha, T.M., et al. Crucial role of neutrophils in the development of mechanical inflammatory hypernociception. J. Leukoc. Biol. 83 (2008), 824–832.
3. 3 Kiguchi, N., et al. Epigenetic augmentation of the macrophage inflammatory protein 2/C-X-C chemokine receptor type 2 axis through histone H3 acetylation in injured peripheral nerves elicits neuropathic pain. J. Pharmacol. Exp. Ther. 340 (2012), 577–587.
4. 4 Ghasemlou, N., et al. CD11b + Ly6G- myeloid cells mediate mechanical inflammatory pain hypersensitivity. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), E6808–E6817.
5. 5 Aich, A., et al. Mast cell-mediated mechanisms of nociception. Int. J. Mol. Sci. 16 (2015), 29069–29092.
6. 6 Chatterjea, D., Martinov, T., Mast cells: versatile gatekeepers of pain. Mol. Immunol. 63 (2015), 38–44.
7. 7 Woolf, C.J., et al. Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor alpha. Br. J. Pharmacol. 121 (1997), 417–424.
8. 8 Oliveira, S.M., et al. Involvement of mast cells in a mouse model of postoperative pain. Eur. J. Pharmacol. 672 (2011), 88–95.
9. 9 Li, W-W., et al. Substance P signaling controls mast cell activation, degranulation, and nociceptive sensitization in a rat fracture model of complex regional pain syndrome. Anesthesiology 116 (2012), 882–895.
10. 10 Kobayashi, Y., et al. Macrophage-T cell interactions mediate neuropathic pain through the glucocorticoid-induced tumor necrosis factor ligand system. J. Biol. Chem. 290 (2015), 12603–12613.
11. 11 Schuh, C.D., et al. Prostacyclin mediates neuropathic pain through interleukin 1β-expressing resident macrophages. Pain 155 (2014), 545–555.
12. 12 Trevisan, G., et al. TRPA1 mediates trigeminal neuropathic pain in mice downstream of monocytes/macrophages and oxidative stress. Brain 139 (2016), 1361–1377.
13. 13 Old, E.A., et al. Monocytes expressing CX3CR1 orchestrate the development of vincristine-induced pain. J. Clin. Invest. 124 (2014), 2023–2036.
14. 14 Shutov, L.P., et al. The complement system component C5a produces thermal hyperalgesia via macrophage-to-nociceptor signaling that requires NGF and TRPV1. J. Neurosci. 36 (2016), 5055–5070.
15. 15 Kim, C.F., Moalem-Taylor, G., Interleukin-17 contributes to neuroinflammation and neuropathic pain following peripheral nerve injury in mice. J. Pain 12 (2011), 370–383.
16. 16 Liu, X-J., et al. Nociceptive neurons regulate innate and adaptive immunity and neuropathic pain through MyD88 adapter. Cell Res. 24 (2014), 1374–1377.
17. 17 Vicuña, L., et al. The serine protease inhibitor SerpinA3N attenuates neuropathic pain by inhibiting T cell-derived leukocyte elastase. Nat. Med. 21 (2015), 518–523.
18. 18 Vincent, L., et al. Mast cell activation contributes to sickle cell pathobiology and pain in mice. Blood 122 (2013), 1853–1862.
19. 19 Ferreira, S.H., Prostaglandins, aspirin-like drugs and analgesia. Nat. New Biol. 240 (1972), 200–203.
20. 20 Souza, G.R., et al. Involvement of nuclear factor kappa B in the maintenance of persistent inflammatory hypernociception. Pharmacol. Biochem. Behav. 134 (2015), 49–56.
21. 21 Nieto-Posadas, A., et al. Lysophosphatidic acid directly activates TRPV1 through a C-terminal binding site. Nat. Chem. Biol. 8 (2012), 78–85.
22. 22 Langeslag, M., et al. Sphingosine 1-phosphate to p38 signaling via S1P1 receptor and Gαi/o evokes augmentation of capsaicin-induced ionic currents in mouse sensory neurons. Mol. Pain, 10, 2014, 74.
23. 23 Bisgaard, H., Kristensen, J.K., Effects of synthetic leukotriene D-4 on the local regulation of blood flow in human subcutaneous tissue. Prostaglandins 29 (1985), 155–159.
24. 24 Martin, H.A., et al. Leukotriene and prostaglandin sensitization of cutaneous high-threshold C- and A-delta mechanonociceptors in the hairy skin of rat hindlimbs. Neuroscience 22 (1987), 651–659.
25. 25 Andoh, T., Kuraishi, Y., Expression of BLT1 leukotriene B4 receptor on the dorsal root ganglion neurons in mice. Mol. Brain Res. 137 (2005), 263–266.
26. 26 Verri, W.A., et al. Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development?. Pharmacol. Ther. 112 (2006), 116–138.
27. 27 Ferreira, S.H., et al. Interleukin-1 beta as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature 334 (1988), 698–700.
28. 28 Binshtok, A.M., et al. Nociceptors are interleukin-1beta sensors. J. Neurosci. 28 (2008), 14062–14073.
29. 29 Ebbinghaus, M., et al. The role of interleukin-1β in arthritic pain: main involvement in thermal, but not mechanical, hyperalgesia in rat antigen-induced arthritis. Arthritis Rheum. 64 (2012), 3897–3907.
30. 30 Cunha, F.Q., et al. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br. J. Pharmacol. 107 (1992), 660–664.
31. 31 Malsch, P., et al. Deletion of interleukin-6 signal transducer gp130 in small sensory neurons attenuates mechanonociception and down-regulates TRPA1 expression. J. Neurosci. 34 (2014), 9845–9856.
32. 32 Fang, D., et al. 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 156 (2015), 1124–1144.
33. 33 Jin, X., Gereau, R.W., Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J. Neurosci. 26 (2006), 246–255.
34. 34 Fernandes, E.S., et al. A distinct role for transient receptor potential ankyrin 1, in addition to transient receptor potential vanilloid 1, in tumor necrosis factor alpha-induced inflammatory hyperalgesia and Freund's complete adjuvant-induced monarthritis. Arthritis Rheum. 63 (2011), 819–829.
35. 35 Nicol, G.D., et al. Tumor necrosis factor enhances the capsaicin sensitivity of rat sensory neurons. J. Neurosci. 17 (1997), 975–982.
36. 36 Cunha, T.M., et al. A cascade of cytokines mediates mechanical inflammatory hypernociception in mice. Proc. Natl. Acad. Sci. U.S.A. 102 (2005), 1755–1760.
37. 37 Gudes, S., et al. The role of slow and persistent TTX-resistant sodium currents in acute tumor necrosis factor-α-mediated increase in nociceptors excitability. J. Neurophysiol. 113 (2015), 601–619.
38. 38 Sorkin, L.S., Doom, C.M., Epineurial application of TNF elicits an acute mechanical hyperalgesia in the awake rat. J. Peripher. Nerv. Syst. 5 (2000), 96–100.
39. 39 Constantin, C.E., et al. Endogenous tumor necrosis factor α (TNFα) requires TNF receptor type 2 to generate heat hyperalgesia in a mouse cancer model. J. Neurosci. 28 (2008), 5072–5081.
40. 40 Richter, F., et al. Interleukin-17 sensitizes joint nociceptors to mechanical stimuli and contributes to arthritic pain through neuronal interleukin-17 receptors in rodents. Arthritis Rheum. 64 (2012), 4125–4134.
41. 41 Pinto, L.G., et al. IL-17 mediates articular hypernociception in antigen-induced arthritis in mice. Pain 148 (2010), 247–256.
42. 42 Talbot, S., et al. Silencing nociceptor neurons reduces allergic airway inflammation. Neuron 87 (2015), 341–354.
43. 43 Eskander, M.A., et al. Persistent nociception triggered by nerve growth factor (NGF) Is mediated by TRPV1 and oxidative mechanisms. J. Neurosci. 35 (2015), 8593–8603.
44. 44 Zhang, X., et al. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J. 24 (2005), 4211–4223.
45. 45 Ji, R.R., et al. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002), 57–68.
46. 46 Ro, L.S., et al. Effect of NGF and anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain 79 (1999), 265–274.
47. 47 Tang, X-Q., et al. Semaphorin3A inhibits nerve growth factor-induced sprouting of nociceptive afferents in adult rat spinal cord. J. Neurosci. 24 (2004), 819–827.
48. 48 Yue, J-X., et al. Histamine upregulates Nav1.8 expression in primary afferent neurons via H2 receptors: involvement in neuropathic pain. CNS Neurosci. Ther. 20 (2014), 883–892.
49. 49 Perin-Martins, A., et al. Mechanisms underlying transient receptor potential ankyrin 1 (TRPA1)-mediated hyperalgesia and edema. J. Peripher. Nerv. Syst. 18 (2013), 62–74.
50. 50 Massaad, C.A., et al. Involvement of substance P, CGRP and histamine in the hyperalgesia and cytokine upregulation induced by intraplantar injection of capsaicin in rats. J. Neuroimmunol. 153 (2004), 171–182.
51. 51 Parada, C.A., et al. The major role of peripheral release of histamine and 5-hydroxytryptamine in formalin-induced nociception. Neuroscience 102 (2001), 937–944.
52. 2 receptors in rat dorsal root ganglion neurons. Neuropharmacology 63 (2012), 494–500.
53. 53 Foster, E., et al. Targeted ablation, silencing, and activation establish glycinergic dorsal horn neurons as key components of a spinal gate for pain and itch. Neuron 85 (2015), 1289–1304.
54. 54 Daou, I., et al. Optogenetic silencing of Nav1.8-positive afferents alleviates inflammatory and neuropathic pain. eNeuro 3 (2016), 1–12.
55. 55 Shubayev, V.I., Myers, R.R., Axonal transport of TNF-alpha in painful neuropathy: distribution of ligand tracer and TNF receptors. J. Neuroimmunol. 114 (2001), 48–56.
56. 56 Guan, Z., et al. Injured sensory neuron–derived CSF1 induces microglial proliferation and DAP12-dependent pain. Nat. Neurosci. 19 (2015), 1–10.
57. 57 Berta, T., et al. Extracellular caspase-6 drives murine inflammatory pain via microglial TNF-α secretion. J. Clin. Invest. 124 (2014), 1173–1186.
58. 58 Gao, Y.J., Ji, R.R., Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol. Ther. 126 (2010), 56–68.
59. 59 Ji, R.R., et al. Glia and pain: is chronic pain a gliopathy?. Pain 154 (2013), S10–S28.
60. 60 Sorge, R.E., et al. Different immune cells mediate mechanical pain hypersensitivity in male and female mice. Nat. Neurosci. 18 (2015), 1–5.
61. 61 Taves, S., et al. Spinal inhibition of p38 MAP kinase reduces inflammatory and neuropathic pain in male but not female mice: Sex-dependent microglial signaling in the spinal cord. Brain. Behav. Immun. 55 (2016), 70–81.
62. 62 Xu, J., et al. NFκB-mediated CXCL1 production in spinal cord astrocytes contributes to the maintenance of bone cancer pain in mice. J. Neuroinflammation, 11, 2014, 38.
63. 63 Zarpelon, A.C., et al. Spinal cord oligodendrocyte-derived alarmin IL-33 mediates neuropathic pain. FASEB J. 30 (2016), 54–65.
64. 64 Andersson, U., Tracey, K.J., Reflex principles of immunological homeostasis. Annu. Rev. Immunol. 30 (2012), 313–335.
65. 65 Bruce, A.N., Vaso-dilator axon-reflexes. Quat. J. Exp. Physiol 6 (1913), 339–354.
66. 66 Jancsó, N., et al. Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br. J. Pharmacol. Chemother. 31 (1967), 138–151.
67. 67 Brain, S.D., Williams, T.J., Inflammatory oedema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability. Br. J. Pharmacol. 86 (1985), 855–860.
68. 68 Davis, M.J., et al. Modulation of lymphatic muscle contractility by the neuropeptide substance P. Am. J. Physiol. Heart Circ. Physiol. 295 (2008), H587–H597.
69. 69 Chakraborty, S., et al. Substance P activates both contractile and inflammatory pathways in lymphatics through the neurokinin receptors NK1R and NK3R. Microcirculation 18 (2011), 24–35.
70. 70 Hosaka, K., et al. Calcitonin gene-related peptide activates different signaling pathways in mesenteric lymphatics of guinea pigs. Am. J. Physiol. Heart Circ. Physiol. 290 (2006), H813–H822.
71. 71 Kurashige, C., et al. Roles of receptor activity-modifying protein 1 in angiogenesis and lymphangiogenesis during skin wound healing in mice. FASEB J. 28 (2014), 1237–1247.
72. 72 Liu, T., et al. Emerging role of Toll-like receptors in the control of pain and itch. Neurosci. Bull. 28 (2012), 131–144.
73. 73 Baral, P., et al. Pain and itch: beneficial or harmful to antimicrobial defense?. Cell Host Microbe 19 (2016), 755–759.
74. 74 Kashem, S.W., et al. Nociceptive sensory fibers drive interleukin-23 production from CD301b+ dermal dendritic cells and drive protective cutaneous immunity. Immunity 43 (2015), 515–526.
75. 75 Chiu, I.M., et al. Bacteria activate sensory neurons that modulate pain and inflammation. Nature 501 (2013), 52–57.
76. 76 Altmayr, F., et al. The neuropeptide calcitonin gene-related peptide causes repression of tumor necrosis factor-alpha transcription and suppression of ATF-2 promoter recruitment in Toll-like receptor-stimulated dendritic cells. J. Biol. Chem. 285 (2010), 3525–3531.
77. 77 Jusek, G., et al. Deficiency of the CGRP receptor component RAMP1 attenuates immunosuppression during the early phase of septic peritonitis. Immunobiology 217 (2012), 761–767.
78. 78 Baliu-Piqué, M., et al. Neuroimmunological communication via CGRP promotes the development of a regulatory phenotype in TLR4-stimulated macrophages. Eur. J. Immunol. 44 (2014), 3708–3716.
79. 79 Martinez, C., et al. Anti-inflammatory role in septic shock of pituitary adenylate cyclase-activating polypeptide receptor. Proc. Natl. Acad. Sci. U.S.A. 99 (2002), 1053–1058.
80. 80 Gomes, R.N., et al. Calcitonin gene-related peptide inhibits local acute inflammation and protects mice against lethal endotoxemia. Shock 24 (2005), 590–594.
81. 81 Fernandes, E.S., et al. TRPV1 deletion enhances local inflammation and accelerates the onset of systemic inflammatory response syndrome. J. Immunol. 188 (2012), 5741–5751.
82. 82 Calil, I.L., et al. Lipopolysaccharide induces inflammatory hyperalgesia triggering a TLR4/MyD88-dependent cytokine cascade in the mice paw. PLoS ONE, 9, 2014, e90013.
83. 83 Meseguer, V., et al. TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins. Nat. Commun., 5, 2014, 3125.
84. 84 Walters, N., et al. Enhanced immunoglobulin A response and protection against Salmonella enterica serovar typhimurium in the absence of the substance P receptor. Infect. Immun. 73 (2005), 317–324.
85. 85 Gabanyi, I., et al. Neuro-immune interactions drive tissue programming in intestinal macrophages. Cell 164 (2016), 378–391.
86. 86 Riol-Blanco, L., et al. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature 510 (2014), 157–161.
87. 87 Liu, B., et al. TRPA1 controls inflammation and pruritogen responses in allergic contact dermatitis. FASEB J. 27 (2013), 3549–3563.
88. 88 Mikami, N., et al. Calcitonin gene-related peptide is an important regulator of cutaneous immunity: effect on dendritic cell and T cell functions. J. Immunol. 186 (2011), 6886–6893.
89. 89 Mikami, N., et al. Calcitonin gene-related peptide regulates type IV hypersensitivity through dendritic cell functions. PLoS ONE, 9, 2014, e86367.
90. 90 Stangenberg, L., et al. Denervation protects limbs from inflammatory arthritis via an impact on the microvasculature. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 11419–11424.
91. 91 Ding, W., et al. Calcitonin gene-related peptide-exposed endothelial cells bias antigen presentation to CD4+ T cells toward a Th17 response. J. Immunol. 196 (2016), 2181–2194.
92. 92 Ebbinghaus, M., et al. Interleukin-6-dependent influence of nociceptive sensory neurons on antigen-induced arthritis. Arthritis Res. Ther., 17, 2015, 334.
93. 93 Borbély, É., et al. Capsaicin-sensitive sensory nerves exert complex regulatory functions in the serum-transfer mouse model of autoimmune arthritis. Brain. Behav. Immun. 45 (2015), 50–59.
94. 94 Caceres, A.I., et al. A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 9099–9104.
95. 95 Tränkner, D., et al. Population of sensory neurons essential for asthmatic hyperreactivity of inflamed airways. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 11515–11520.
96. 96 Kim, J.H., et al. CGRP, a neurotransmitter of enteric sensory neurons, contributes to the development of food allergy due to the augmentation of microtubule reorganization in mucosal mast cells. Biomed. Res. 35 (2014), 285–293.
97. 97 Engel, M.A., et al. TRPA1 and substance P mediate colitis in mice. Gastroenterology 141 (2011), 1346–1358.
98. 98 Ramachandran, R., et al. TRPM8 activation attenuates inflammatory responses in mouse models of colitis. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 7476–7481.
99. 99 de Jong, P.R., et al. TRPM8 on mucosal sensory nerves regulates colitogenic responses by innate immune cells via CGRP. Mucosal Immunol. 8 (2015), 491–504.
100. 100 Shi, X., et al. Keratinocytes express cytokines and nerve growth factor in response to neuropeptide activation of the ERK1/2 and JNK MAPK transcription pathways. Regul. Pept. 186 (2013), 92–103.
101. 101 Shi, X., et al. Neuropeptides contribute to peripheral nociceptive sensitization by regulating interleukin-1β production in keratinocytes. Anesth. Analg. 113 (2011), 175–183.
102. 102 Branchfield, K., et al. Pulmonary neuroendocrine cells function as airway sensors to control lung immune response. Science 351 (2016), 707–710.
103. 103 Basbaum, A.I., et al. Cellular and molecular mechanisms of pain. Cell 139 (2009), 267–284.
104. 104 Dib-Hajj, S.D., Waxman, S.G., Translational pain research: lessons from genetics and genomics. Sci. Transl. Med., 6, 2014, 249sr4.
105. 105 Von Hehn, C.A., et al. Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 73 (2012), 638–652.
106. 106 Julius, D., TRP channels and pain. Annu. Rev. Cell. Dev. Biol. 29 (2013), 355–384.
107. 107 Ranade, S.S., et al. Mechanically activated ion channels. Neuron 87 (2015), 1162–1179.
108. 108 Napimoga, M.H., et al. 15d-prostaglandin J2 inhibits inflammatory hypernociception: involvement of peripheral opioid receptor. J. Pharmacol. Exp. Ther. 324 (2008), 313–321.
109. 109 Ji, R.R., et al. Emerging roles of resolvins in the resolution of inflammation and pain. Trends Neurosci. 34 (2011), 599–609.
110. 110 Serhan, C.N., Pro-resolving lipid mediators are leads for resolution physiology. Nature 510 (2014), 92–101.
111. 111 Park, C-K., et al. Resolvin D2 is a potent endogenous inhibitor for transient receptor potential subtype V1/A1, inflammatory pain, and spinal cord synaptic plasticity in mice: distinct roles of resolvin D1, D2, and E1. J. Neurosci. 31 (2011), 18433–18438.
112. 112 Wang, H., Zylka, M., Mrgprd-expressing polymodal nociceptive neurons innervate most known classes of substantia gelatinosa neurons. J. Neuroscience 29 (2009), 13202–13209.
113. 113 Russo, A.F., CGRP as a neuropeptide in migraine: lessons from mice. Br. J. Clin. Pharmacol. 80 (2015), 403–414.
114. 114 Bigal, M.E., et al. Therapeutic antibodies against CGRP or its receptor. Br. J. Clin. Pharmacol. 79 (2015), 886–895.
115. 115 Russell, F.A., et al. Calcitonin gene-related peptide: physiology and pathophysiology. Physiol. Rev. 94 (2014), 1099–1142.