Sensory TRP channels contribute differentially to skin inflammation and persistent itch

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Feng, Jing ^a   Yang, Pu ^a   Mack, Madison R ^a   Dryn, Dariia ^a,b   Luo, Jialie ^a   Gong, Xuan ^a,c   Liu, Shenbin ^a   Oetjen, Landon K ^a   Zholos, Alexander V ^b   Mei, Zhinan ^c   Yin, Shijin ^c   Kim, Brian S ^a   Hu, Hongzhen ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TARAS SHEVCHENKO NATIONAL UNIVERSITY OF KYIV   (Ukraine)

^c SOUTH CENTRAL UNIVERSITY FOR NATIONALITIES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; SQUARIC ACID DIBUTYL ESTER; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TUMOR NECROSIS FACTOR; VANILLOID RECEPTOR 1; TRPA1 PROTEIN, MOUSE; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ALLERGY; CELLS AND CELL COMPONENTS; ESTER; GENE; GENETIC ANALYSIS; IDENTIFICATION METHOD; MOLECULAR ANALYSIS; SKIN DISORDER;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HEK293 CELL LINE; LYMPHOCYTE; MACROPHAGE; MEMBRANE DEPOLARIZATION; MOUSE; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PRURITUS; SCRATCHING; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SKIN ALLERGY; ANIMAL; C57BL MOUSE; DISEASE MODEL; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; MALE; SKIN;

ANIMALS; DERMATITIS, ALLERGIC CONTACT; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; PRURITUS; SKIN; TRPA1 CATION CHANNEL; TRPV CATION CHANNELS;

EID: 85032494733     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-01056-8     Document Type: Article

References (58)

1. Xu, H., Diiulio, N. A. & Fairchild, R. L. T cell populations primed by hapten sensitization in contact sensitivity are distinguished by polarized patterns of cytokine production: interferon gamma-producing (Tc1) effector CD8+ T cells and interleukin (Il) 4/Il-10-producing (Th2) negative regulatory CD4+ T cells. J. Exp. Med. 183, 1001-1012 (1996).
2. Askenase, P. W. Yes T cells, but three different T cells (alphabeta, gammadelta and NK T cells), and also B-1 cells mediate contact sensitivity. Clin. Exp. Immunol. 125, 345-350 (2001).
3. Wang, B., Feliciani, C., Freed, I., Cai, Q. & Sauder, D. N. Insights into molecular mechanisms of contact hypersensitivity gained from gene knockout studies. J. Leukoc. Biol. 70, 185-191 (2001).
4. Mastrolonardo, M., Lopalco, P. L. & Diaferio, A. Topical immunotherapy with contact sensitizers: a model to study the natural history of delayed hypersensitivity. Contact Dermatitis 47, 210-214 (2002).
5. Zoller, M. et al. Chronic delayed-type hypersensitivity reaction as a means to treat alopecia areata. Clin. Exp. Immunol. 135, 398-408 (2004).
6. Qu, L. et al. Enhanced excitability of MRGPRA3-and MRGPRD-positive nociceptors in a model of inflammatory itch and pain. Brain 137, 1039-1050 (2014).
7. Luo, J., Feng, J., Liu, S., Walters, E. T. & Hu, H. Molecular and cellular mechanisms that initiate pain and itch. Cell Mol. Life. Sci. 72, 3201-3223 (2015).
8. Caterina, M. J. et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306-313 (2000).
9. Jordt, S. E. et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260-265 (2004).
10. Bautista, D. M. et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124, 1269-1282 (2006).
11. Liu, S. et al. Eact, a small molecule activator of TMEM16A, activates TRPV1 and elicits pain-and itch-related behaviours. Br. J. Pharmacol. 173, 1208-1218 (2016).
12. Imamachi, N. et al. TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms. Proc. Natl Acad. Sci. USA 106, 11330-11335 (2009).
13. Shim, W. S. et al. TRPV1 mediates histamine-induced itching via the activation of phospholipase A2 and 12-lipoxygenase. J. Neurosci. 27, 2331-2337 (2007).
14. Wilson, S. R. et al. TRPA1 is required for histamine-independent, Mas-related G protein-coupled receptor-mediated itch. Nat. Neurosci. 14, 595-602 (2011).
15. Qu, L., Fu, K., Yang, J., Shimada, S. G. & LaMotte, R. H. CXCR3 chemokine receptor signaling mediates itch in experimental allergic contact dermatitis. Pain. 156, 1737-1746 (2015).
16. Sun, S. & Dong, X. Trp channels and itch. Semin. Immunopathol. 38, 293-307 (2016).
17. Liu, B. et al. TRPA1 controls inflammation and pruritogen responses in allergic contact dermatitis. FASEB J. 27, 3549-3563 (2013).
18. Banvolgyi, A. et al. Evidence for a novel protective role of the vanilloid TRPV1 receptor in a cutaneous contact allergic dermatitis model. J. Neuroimmunol. 169, 86-96 (2005).
19. Christensen, A. D. & Haase, C. Immunological mechanisms of contact hypersensitivity in mice. APMIS 120, 1-27 (2012).
20. Nosbaum, A., Vocanson, M., Rozieres, A., Hennino, A. & Nicolas, J. F. Allergic and irritant contact dermatitis. Eur. J. Dermatol. 19, 325-332 (2009).
21. Mombaerts, P. et al. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68, 869-877 (1992).
22. Zhi, L. et al. FTY720 blocks egress of T cells in part by abrogation of their adhesion on the lymph node sinus. J. Immunol. 187, 2244-2251 (2011).
23. O'Leary, J. G., Goodarzi, M., Drayton, D. L. & von Andrian, U. H. T cell-and B cell-independent adaptive immunity mediated by natural killer cells. Nat. Immunol. 7, 507-516 (2006).
24. Akiyama, T. & Carstens, E. Neural processing of itch. Neuroscience 250, 697-714 (2013).
25. Bautista, D. M. et al. Pungent products from garlic activate the sensory ion channel TRPA1. Proc. Natl Acad. Sci. USA 102, 12248-12252 (2005).
26. Story, G. M. et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112, 819-829 (2003).
27. Ringkamp, M. et al. A role for nociceptive, myelinated nerve fibers in itch sensation. J. Neurosci. 31, 14841-14849 (2011).
28. Riol-Blanco, L. et al. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature 510, 157-161 (2014).
29. Mollanazar, N. K., Smith, P. K. & Yosipovitch, G. Mediators of chronic pruritus in atopic dermatitis: getting the itch out? Clin. Rev. Allergy Immunol. 51, 263-292 (2015).
30. Macpherson, L. J. et al. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445, 541-545 (2007).
31. Trevisani, M. et al. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc. Natl Acad. Sci. USA 104, 13519-13524 (2007).
32. Jordt, S. E. & Julius, D. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108, 421-430 (2002).
33. Shimada, S. G. & LaMotte, R. H. Behavioral differentiation between itch and pain in mouse. Pain 139, 681-687 (2008).
34. Undem, B. J. & Taylor-Clark, T. Mechanisms underlying the neuronal-based symptoms of allergy. J. Allergy Clin. Immunol. 133, 1521-1534 (2014).
35. McDonald, D. M., Bowden, J. J., Baluk, P. & Bunnett, N. W. Neurogenic inflammation. A model for studying efferent actions of sensory nerves. Adv. Exp. Med. Biol. 410, 453-462 (1996).
36. Chen, J. et al. Selective blockade of TRPA1 channel attenuates pathological pain without altering noxious cold sensation or body temperature regulation. Pain 152, 1165-1172 (2011).
37. Suzuki, K., Meguro, K., Nakagomi, D. & Nakajima, H. Roles of alternatively activated M2 macrophages in allergic contact dermatitis. Allergol. Int. 66, 392-397 (2017).
38. Arango Duque, G. & Descoteaux, A. Macrophage cytokines: involvement in immunity and infectious diseases. Front. Immunol. 5, 491 (2014).
39. Simon, D. & Bieber, T. Systemic therapy for atopic dermatitis. Allergy 69, 46-55 (2014).
40. Panahi, Y., Davoudi, S. M., Madanchi, N. & Abolhasani, E. Recombinant human interferon gamma (Gamma Immunex) in treatment of atopic dermatitis. Clin. Exp. Med. 12, 241-245 (2012).
41. Hamilton, J. D., Ungar, B. & Guttman-Yassky, E. Drug evaluation review: dupilumab in atopic dermatitis. Immunotherapy 7, 1043-1058 (2015).
42. Cassano, N., Tessari, G., Vena, G. A. & Girolomoni, G. Chronic pruritus in the absence of specific skin disease: an update on pathophysiology, diagnosis, and therapy. Am. J. Clin. Dermatol. 11, 399-411 (2010).
43. Xu, A. Z., Tripathi, S. V., Kau, A. L., Schaffer, A. & Kim, B. S. Immune dysregulation underlies a subset of patients with chronic idiopathic pruritus. J. Am. Acad. Dermatol. 74, 1017-1020 (2016).
44. Werfel, T. et al. Cellular and molecular immunologic mechanisms in patients with atopic dermatitis. J. Allergy Clin. Immunol. 138, 336-349 (2016).
45. Simpson, E. L. et al. Two phase 3 trials of dupilumab versus Placebo in atopic dermatitis. N. Engl. J. Med. 375, 2335-2348 (2016).
46. Valenzuela, F. et al. Tofacitinib versus etanercept or placebo in patients with moderate to severe chronic plaque psoriasis: patient-reported outcomes from a Phase 3 study. J. Eur. Acad. Dermatol. Venereol. 30, 1753-1759 (2016).
47. Beresford, L., Orange, O., Bell, E. B. & Miyan, J. A. Nerve fibres are required to evoke a contact sensitivity response in mice. Immunology 111, 118-125 (2004).
48. Han, L. et al. A subpopulation of nociceptors specifically linked to itch. Nat. Neurosci. 16, 174-182 (2013).
49. Zylka, M. J., Rice, F. L. & Anderson, D. J. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 45, 17-25 (2005).
50. Cavanaugh, D. J. et al. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc. Natl Acad. Sci. USA 106, 9075-9080 (2009).
51. Liu, Q. et al. Mechanisms of itch evoked by beta-alanine. J. Neurosci. 32, 14532-14537 (2012).
52. Kashem, S. W. et al. Nociceptive sensory fibers drive interleukin-23 production from CD301b+ dermal dendritic cells and drive protective cutaneous immunity. Immunity 43, 515-526 (2015).
53. Maruyama, K. et al. Nociceptors boost the resolution of fungal osteoinflammation via the TRP channel-CGRP-Jdp2 Axis. Cell Rep. 19, 2730-2742 (2017).
54. de Jong, P. R. et al. TRPM8 on mucosal sensory nerves regulates colitogenic responses by innate immune cells via CGRP. Mucosal Immunol. 8, 491-504 (2015).
55. Nong, Y. H., Titus, R. G., Ribeiro, J. M. & Remold, H. G. Peptides encoded by the calcitonin gene inhibit macrophage function. J. Immunol. 143, 45-49 (1989).
56. Liu, J., Chen, M. & Wang, X. Calcitonin gene-related peptide inhibits lipopolysaccharide-induced interleukin-12 release from mouse peritoneal macrophages, mediated by the cAMP pathway. Immunology 101, 61-67 (2000).
57. Cruz-Orengo, L. et al. Cutaneous nociception evoked by 15-delta PGJ2 via activation of ion channel TRPA1. Mol. Pain 4, 30 (2008).
58. Yin, S. et al. Retinoids activate the irritant receptor TRPV1 and produce sensory hypersensitivity. J. Clin. Invest. 123, 3941-3951 (2013).