XThe epithelial cell-derived atopic dermatitis cytokine TSLP activates neurons to induce itch

Cell

Volumn 155, Issue 2, 2013, Pages 285-295

  Wilson, Sarah R ^a   Thé, Lydia ^a   Batia, Lyn M ^a   Beattie, Katherine ^a   Katibah, George E ^a   McClain, Shannan P ^a   Pellegrino, Maurizio ^a   Estandian, Daniel M ^a   Bautista, Diana M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 AMINOETHOXYDIPHENYLBORANE; CALCIUM; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; CHLOROQUINE; CYCLOSPORIN A; PERIPHERIN; PHOSPHOLIPASE C; SMALL INTERFERING RNA; STROMAL INTERACTION MOLECULE 1; THYMIC STROMAL LYMPHOPOIETIN; TRANSCRIPTION FACTOR NFAT; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRYPTASE;

ALLERGIC RHINITIS; ANIMAL EXPERIMENT; ARTICLE; ASTHMA; ATOPIC DERMATITIS; CALCIUM DEPLETION; CALCIUM SIGNALING; CELL INTERACTION; EPITHELIUM CELL; EVOKED RESPONSE; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PRURITUS; SCRATCHING; SENSORY NERVE CELL; WILD TYPE;

EID: 84885674640     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.08.057     Document Type: Article

References (65)

1. W.I. Al-Daraji, K.R. Grant, K. Ryan, A. Saxton, and N.J. Reynolds Localization of calcineurin/NFAT in human skin and psoriasis and inhibition of calcineurin/NFAT activation in human keratinocytes by cyclosporin A J. Invest. Dermatol. 118 2002 779 788
2. W. Almers, and E. Neher The Ca signal from fura-2 loaded mast cells depends strongly on the method of dye-loading FEBS Lett. 192 1985 13 18
3. T. Andoh, N. Katsube, M. Maruyama, and Y. Kuraishi Involvement of leukotriene B(4) in substance P-induced itch-associated response in mice J. Invest. Dermatol. 117 2001 1621 1626
4. A.I. Basbaum, D.M. Bautista, G. Scherrer, and D. Julius Cellular and molecular mechanisms of pain Cell 139 2009 267 284
5. D.M. Bautista, M. Pellegrino, and M. Tsunozaki TRPA1: A gatekeeper for inflammation Annu. Rev. Physiol. 75 2013 181 200
6. S.I. Bogiatzi, M. Guillot-Delost, A. Cappuccio, J.C. Bichet, O. Chouchane-Mlik, M.H. Donnadieu, E. Barillot, P. Hupe, K. Chlichlia, and E.I. Efremidou Multiple-checkpoint inhibition of thymic stromal lymphopoietin-induced TH2 response by TH17-related cytokines J. Allergy Clin. Immunol. 130 2012 233 240
7. A. Briot, C. Deraison, M. Lacroix, C. Bonnart, A. Robin, C. Besson, P. Dubus, and A. Hovnanian Kallikrein 5 induces atopic dermatitis-like lesions through PAR2-mediated thymic stromal lymphopoietin expression in Netherton syndrome J. Exp. Med. 206 2009 1135 1147
8. A. Briot, M. Lacroix, A. Robin, M. Steinhoff, C. Deraison, and A. Hovnanian Par2 inactivation inhibits early production of TSLP, but not cutaneous inflammation, in Netherton syndrome adult mouse model J. Invest. Dermatol. 130 2010 2736 2742
9. M.D. Cahalan STIMulating store-operated Ca(2+) entry Nat. Cell Biol. 11 2009 669 677
10. F. Cevikbas, A. Steinhoff, B. Homey, and M. Steinhoff Neuroimmune interactions in allergic skin diseases Curr. Opin. Allergy Clin. Immunol. 7 2007 365 373
11. W.C. Chang, C.H. Lee, T. Hirota, L.F. Wang, S. Doi, A. Miyatake, T. Enomoto, K. Tomita, M. Sakashita, and T. Yamada ORAI1 genetic polymorphisms associated with the susceptibility of atopic dermatitis in Japanese and Taiwanese populations PLoS ONE 7 2012 e29387
12. Y. Dai, S. Wang, M. Tominaga, S. Yamamoto, T. Fukuoka, T. Higashi, K. Kobayashi, K. Obata, H. Yamanaka, and K. Noguchi Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain J. Clin. Invest. 117 2007 1979 1987
13. W.I. DeHaven, J.T. Smyth, R.R. Boyles, G.S. Bird, and J.W. Putney Jr. Complex actions of 2-aminoethyldiphenyl borate on store-operated calcium entry J. Biol. Chem. 283 2008 19265 19273
14. S. Feske CRAC channelopathies Pflugers Arch. 460 2010 417 435
15. S. Feske, Y. Gwack, M. Prakriya, S. Srikanth, S.H. Puppel, B. Tanasa, P.G. Hogan, R.S. Lewis, M. Daly, and A. Rao A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function Nature 441 2006 179 185
16. C. Fitzsimons, N. Engel, H. Durán, L. Policastro, G. Cricco, G. Martín, B. Molinari, and E. Rivera Histamine production in mouse epidermal keratinocytes is regulated during cellular differentiation Inflamm. Res. 50 Suppl 2 2001 S100 S101
17. K.A. Gerhold, M. Pellegrino, M. Tsunozaki, T. Morita, D.B. Leitch, P.R. Tsuruda, R.B. Brem, K.C. Catania, and D.M. Bautista The star-nosed mole reveals clues to the molecular basis of mammalian touch PLoS ONE 8 2013 e55001
18. G.A. Gusarova, H.E. Trejo, L.A. Dada, A. Briva, L.C. Welch, R.B. Hamanaka, G.M. Mutlu, N.S. Chandel, M. Prakriya, and J.I. Sznajder Hypoxia leads to Na,K-ATPase downregulation via Ca(2+) release-activated Ca(2+) channels and AMPK activation Mol. Cell. Biol. 31 2011 3546 3556
19. Y. Gwack, S. Feske, S. Srikanth, P.G. Hogan, and A. Rao Signalling to transcription: store-operated Ca2+ entry and NFAT activation in lymphocytes Cell Calcium 42 2007 145 156
20. U.M. Halfter, Z.E. Derbyshire, and R.R. Vaillancourt Interferon-gamma- dependent tyrosine phosphorylation of MEKK4 via Pyk2 is regulated by annexin II and SHP2 in keratinocytes Biochem. J. 388 2005 17 28
21. R. He, and R.S. Geha Thymic stromal lymphopoietin Ann. N Y Acad. Sci. 1183 2010 13 24
22. S.T. Holgate The epithelium takes centre stage in asthma and atopic dermatitis Trends Immunol. 28 2007 248 251
23. A. Hovnanian Netherton syndrome: skin inflammation and allergy by loss of protease inhibition Cell Tissue Res. 351 2013 289 300
24. A. Ikoma, R. Rukwied, S. Ständer, M. Steinhoff, Y. Miyachi, and M. Schmelz Neuronal sensitization for histamine-induced itch in lesional skin of patients with atopic dermatitis Arch. Dermatol. 139 2003 1455 1458
25. A. Ikoma, M. Steinhoff, S. Ständer, G. Yosipovitch, and M. Schmelz The neurobiology of itch Nat. Rev. Neurosci. 7 2006 535 547
26. N. Imamachi, G.H. Park, H. Lee, D.J. Anderson, M.I. Simon, A.I. Basbaum, and S.K. Han TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms Proc. Natl. Acad. Sci. USA 106 2009 11330 11335
27. S.P. Jariwala, E. Abrams, A. Benson, J. Fodeman, and T. Zheng The role of thymic stromal lymphopoietin in the immunopathogenesis of atopic dermatitis Clin. Exp. Allergy 41 2011 1515 1520
28. H.K. Jessup, A.W. Brewer, M. Omori, E.A. Rickel, A.L. Budelsky, B.R. Yoon, S.F. Ziegler, and M.R. Comeau Intradermal administration of thymic stromal lymphopoietin induces a T cell- and eosinophil-dependent systemic Th2 inflammatory response J. Immunol. 181 2008 4311 4319
29. N. Kanda, S. Koike, and S. Watanabe Prostaglandin E2 enhances neurotrophin-4 production via EP3 receptor in human keratinocytes J. Pharmacol. Exp. Ther. 315 2005 796 804
30. H. Kouzaki, S.M. O'Grady, C.B. Lawrence, and H. Kita Proteases induce production of thymic stromal lymphopoietin by airway epithelial cells through protease-activated receptor-2 J. Immunol. 183 2009 1427 1434
31. C.H. Lee, and H.S. Yu Biomarkers for itch and disease severity in atopic dermatitis Curr. Probl. Dermatol. 41 2011 136 148
32. M. Li, N. Messaddeq, M. Teletin, J.L. Pasquali, D. Metzger, and P. Chambon Retinoid X receptor ablation in adult mouse keratinocytes generates an atopic dermatitis triggered by thymic stromal lymphopoietin Proc. Natl. Acad. Sci. USA 102 2005 14795 14800
33. A. Lis, C. Peinelt, A. Beck, S. Parvez, M. Monteilh-Zoller, A. Fleig, and R. Penner CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties Curr. Biol. 17 2007 794 800
34. Q. Liu, Z. Tang, L. Surdenikova, S. Kim, K.N. Patel, A. Kim, F. Ru, Y. Guan, H.J. Weng, and Y. Geng Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus Cell 139 2009 1353 1365
35. Q. Liu, H.J. Weng, K.N. Patel, Z. Tang, H. Bai, M. Steinhoff, and X. Dong The distinct roles of two GPCRs, MrgprC11 and PAR2, in itch and hyperalgesia Sci. Signal. 4 2011 ra45
36. B. Liu, J. Escalera, S. Balakrishna, L. Fan, A.I. Caceres, E. Robinson, A. Sui, M.C. McKay, M.A. McAlexander, C.A. Herrick, and S.E. Jordt TRPA1 controls inflammation and pruritogen responses in allergic contact dermatitis FASEB J. 27 2013 3549 3563
37. R.M. Locksley Asthma and allergic inflammation Cell 140 2010 777 783
38. V. Madan, and C.E. Griffiths Systemic ciclosporin and tacrolimus in dermatology Dermatol. Ther. 20 2007 239 250
39. E.S. McCoy, B. Taylor-Blake, and M.J. Zylka CGRPα-expressing sensory neurons respond to stimuli that evoke sensations of pain and itch PLoS ONE 7 2012 e36355
40. E.S. McCoy, B. Taylor-Blake, S.E. Street, A.L. Pribisko, J. Zheng, and M.J. Zylka Peptidergic CGRPα primary sensory neurons encode heat and itch and tonically suppress sensitivity to cold Neuron 78 2013 138 151
41. K. Mitchell, B.D. Bates, J.M. Keller, M. Lopez, L. Scholl, J. Navarro, N. Madian, G. Haspel, M.I. Nemenov, and M.J. Iadarola Ablation of rat TRPV1-expressing Adelta/C-fibers with resiniferatoxin: analysis of withdrawal behaviors, recovery of function and molecular correlates Mol. Pain 6 2010 94
42. C.S. Moniaga, S.K. Jeong, G. Egawa, S. Nakajima, M. Hara-Chikuma, J.E. Jeon, S.H. Lee, T. Hibino, Y. Miyachi, and K. Kabashima Protease activity enhances production of thymic stromal lymphopoietin and basophil accumulation in flaky tail mice Am. J. Pathol. 182 2013 841 851
43. G. Owsianik, K. Talavera, T. Voets, and B. Nilius Permeation and selectivity of TRP channels Annu. Rev. Physiol. 68 2006 685 717
44. A. Pandey, K. Ozaki, H. Baumann, S.D. Levin, A. Puel, A.G. Farr, S.F. Ziegler, W.J. Leonard, and H.F. Lodish Cloning of a receptor subunit required for signaling by thymic stromal lymphopoietin Nat. Immunol. 1 2000 59 64
45. M. Prakriya, S. Feske, Y. Gwack, S. Srikanth, A. Rao, and P.G. Hogan Orai1 is an essential pore subunit of the CRAC channel Nature 443 2006 230 233
46. J. Rae, K. Cooper, P. Gates, and M. Watsky Low access resistance perforated patch recordings using amphotericin B J. Neurosci. Methods 37 1991 15 26
47. I.S. Ramsey, M. Delling, and D.E. Clapham An introduction to TRP channels Annu. Rev. Physiol. 68 2006 619 647
48. A. Rao, C. Luo, and P.G. Hogan Transcription factors of the NFAT family: regulation and function Annu. Rev. Immunol. 15 1997 707 747
49. S.E. Ross Pain and itch: insights into the neural circuits of aversive somatosensation in health and disease Curr. Opin. Neurobiol. 21 2011 880 887
50. R.J. Santulli, C.K. Derian, A.L. Darrow, K.A. Tomko, A.J. Eckardt, M. Seiberg, R.M. Scarborough, and P. Andrade-Gordon Evidence for the presence of a protease-activated receptor distinct from the thrombin receptor in human keratinocytes Proc. Natl. Acad. Sci. USA 92 1995 9151 9155
51. N.M. Schechter, L.F. Brass, R.M. Lavker, and P.J. Jensen Reaction of mast cell proteases tryptase and chymase with protease activated receptors (PARs) on keratinocytes and fibroblasts J. Cell. Physiol. 176 1998 365 373
52. S.G. Shimada, and R.H. LaMotte Behavioral differentiation between itch and pain in mouse Pain 139 2008 681 687
53. J.M. Spergel, and A.S. Paller Atopic dermatitis and the atopic march J. Allergy Clin. Immunol. 112 6, Suppl 2003 S118 S127
54. M. Steinhoff, U. Neisius, A. Ikoma, M. Fartasch, G. Heyer, P.S. Skov, T.A. Luger, and M. Schmelz Proteinase-activated receptor-2 mediates itch: a novel pathway for pruritus in human skin J. Neurosci. 23 2003 6176 6180
55. D. Tobin, G. Nabarro, H. Baart de la Faille, W.A. van Vloten, S.C. van der Putte, and H.J. Schuurman Increased number of immunoreactive nerve fibers in atopic dermatitis J. Allergy Clin. Immunol. 90 1992 613 622
56. M. Tominaga, S. Tengara, A. Kamo, H. Ogawa, and K. Takamori Psoralen-ultraviolet A therapy alters epidermal Sema3A and NGF levels and modulates epidermal innervation in atopic dermatitis J. Dermatol. Sci. 55 2009 40 46
57. H. Ui, T. Andoh, J.B. Lee, H. Nojima, and Y. Kuraishi Potent pruritogenic action of tryptase mediated by PAR-2 receptor and its involvement in anti-pruritic effect of nafamostat mesilate in mice Eur. J. Pharmacol. 530 2006 172 178
58. S.R. Wilson, K.A. Gerhold, A. Bifolck-Fisher, Q. Liu, K.N. Patel, X. Dong, and D.M. Bautista TRPA1 is required for histamine-independent, Mas-related G protein-coupled receptor-mediated itch Nat. Neurosci. 14 2011 595 602
59. S.R. Wilson, A.M. Nelson, L. Batia, T. Morita, D. Estandian, D.M. Owens, E.A. Lumpkin, and D.M. Bautista The ion channel TRPA1 is required for chronic itch J. Neurosci. 33 2013 9283 9294
60. A.V. Yeromin, S.L. Zhang, W. Jiang, Y. Yu, O. Safrina, and M.D. Cahalan Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai Nature 443 2006 226 229
61. S. Ying, B. O'Connor, J. Ratoff, Q. Meng, K. Mallett, D. Cousins, D. Robinson, G. Zhang, J. Zhao, T.H. Lee, and C. Corrigan Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity J. Immunol. 174 2005 8183 8190
62. J. Yoo, M. Omori, D. Gyarmati, B. Zhou, T. Aye, A. Brewer, M.R. Comeau, D.J. Campbell, and S.F. Ziegler Spontaneous atopic dermatitis in mice expressing an inducible thymic stromal lymphopoietin transgene specifically in the skin J. Exp. Med. 202 2005 541 549
63. S.L. Zhang, J.A. Kozak, W. Jiang, A.V. Yeromin, J. Chen, Y. Yu, A. Penna, W. Shen, V. Chi, and M.D. Cahalan Store-dependent and -independent modes regulating Ca2+ release-activated Ca2+ channel activity of human Orai1 and Orai3 J. Biol. Chem. 283 2008 17662 17671
64. Y. Zhu, X.R. Wang, C. Peng, J.G. Xu, Y.X. Liu, L. Wu, Q.G. Zhu, J.Y. Liu, F.Q. Li, and Y.H. Pan Induction of leukotriene B(4) and prostaglandin E(2) release from keratinocytes by protease-activated receptor-2-activating peptide in ICR mice Int. Immunopharmacol. 9 2009 1332 1336
65. S.F. Ziegler, F. Roan, B.D. Bell, T.A. Stoklasek, M. Kitajima, and H. Han The biology of thymic stromal lymphopoietin (TSLP) Adv. Pharmacol. 66 2013 129 155