Signaling through purinergic receptors for ATP induces human cutaneous innate and adaptive Th17 responses: Implications in the pathogenesis of psoriasis

Journal of Immunology

Volumn 190, Issue 8, 2013, Pages 4324-4336

  Killeen, Meaghan E ^a   Ferris, Laura ^a   Kupetsky, Erine A ^a   Falo, Louis ^a   Mathers, Alicia R ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; INTERLEUKIN 23; INTERLEUKIN 6; MICRORNA 21; PURINERGIC P2X7 RECEPTOR; VASCULOTROPIN;

ADAPTIVE IMMUNITY; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DENDRITIC CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPATHOGENESIS; INFLAMMATION; INNATE IMMUNITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSORIASIS; SIGNAL TRANSDUCTION; TH17 CELL;

EID: 84875988735     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202045     Document Type: Article

References (76)

1. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
2. Igyártó, B. Z., K. Haley, D. Ortner, A. Bobr, M. Gerami-Nejad, B. T. Edelson, S. M. Zurawski, B. Malissen, G. Zurawski, J. Berman, and D. H. Kaplan. 2011. Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 35: 260-272.
3. Mathers, A. R., B. M. Janelsins, J. P. Rubin, O. A. Tkacheva, W. J. Shufesky, S. C. Watkins, A. E. Morelli, and A. T. Larregina. 2009. Differential capability of human cutaneous dendritic cell subsets to initiate Th17 responses. J. Immunol. 182: 921-933.
4. Morelli, A. E., J. P. Rubin, G. Erdos, O. A. Tkacheva, A. R. Mathers, A. F. Zahorchak, A. W. Thomson, L. D. Falo, Jr., and A. T. Larregina. 2005. CD4+ T cell responses elicited by different subsets of human skin migratory dendritic cells. J. Immunol. 175: 7905-7915.
5. Bianchi, M. E. 2007. DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 81: 1-5.
6. Ehrchen, J. M., C. Sunderkötter, D. Foell, T. Vogl, and J. Roth. 2009. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J. Leukoc. Biol. 86: 557-566.
7. Gallucci, S., M. Lolkema, and P. Matzinger. 1999. Natural adjuvants: endogenous activators of dendritic cells. Nat. Med. 5: 1249-1255.
8. Mizumoto, N., T. Kumamoto, S. C. Robson, J. Sévigny, H. Matsue, K. Enjyoji, and A. Takashima. 2002. CD39 is the dominant Langerhans cell-associated ecto-NTPDase: modulatory roles in inflammation and immune responsiveness. Nat. Med. 8: 358-365.
9. la Sala, A., D. Ferrari, F. Di Virgilio, M. Idzko, J. Norgauer, and G. Girolomoni. 2003. Alerting and tuning the immune response by extracellular nucleotides. J. Leukoc. Biol. 73: 339-343.
10. Idzko, M., S. Dichmann, D. Ferrari, F. Di Virgilio, A. la Sala, G. Girolomoni, E. Panther, and J. Norgauer. 2002. Nucleotides induce chemotaxis and actin polymerization in immature but not mature human dendritic cells via activation of pertussis toxin-sensitive P2y receptors. Blood 100: 925-932.
11. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8: 942-949.
12. Pizzirani, C., D. Ferrari, P. Chiozzi, E. Adinolfi, D. Sandonà, E. Savaglio, and F. Di Virgilio. 2007. Stimulation of P2 receptors causes release of IL-1beta-loaded microvesicles from human dendritic cells. Blood 109: 3856-3864.
13. Wilhelm, K., J. Ganesan, T. Müller, C. Dürr, M. Grimm, A. Beilhack, C. D. Krempl, S. Sorichter, U. V. Gerlach, E. Jüttner, et al. 2010. Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nat. Med. 16: 1434-1438.
14. Granstein, R. D., W. Ding, J. Huang, A. Holzer, R. L. Gallo, A. Di Nardo, and J. A. Wagner. 2005. Augmentation of cutaneous immune responses by ATP g S: purinergic agonists define a novel class of immunologic adjuvants. J. Immunol. 174: 7725-7731.
15. la Sala, A., D. Ferrari, S. Corinti, A. Cavani, F. Di Virgilio, and G. Girolomoni. 2001. Extracellular ATP induces a distorted maturation of dendritic cells and inhibits their capacity to initiate Th1 responses. J. Immunol. 166: 1611-1617.
16. McGeachy, M. J., Y. Chen, C. M. Tato, A. Laurence, B. Joyce-Shaikh, W. M. Blumenschein, T. K. McClanahan, J. J. O'Shea, and D. J. Cua. 2009. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10: 314-324.
17. Atarashi, K., J. Nishimura, T. Shima, Y. Umesaki, M. Yamamoto, M. Onoue, H. Yagita, N. Ishii, R. Evans, K. Honda, and K. Takeda. 2008. ATP drives lamina propria T(H)17 cell differentiation. Nature 455: 808-812.
18. Inoue, K., J. Hosoi, and M. Denda. 2007. Extracellular ATP has stimulatory effects on the expression and release of IL-6 via purinergic receptors in normal human epidermal keratinocytes. J. Invest. Dermatol. 127: 362-371.
19. Pastore, S., F. Mascia, S. Gulinelli, S. Forchap, C. Dattilo, E. Adinolfi, G. Girolomoni, F. Di Virgilio, and D. Ferrari. 2007. Stimulation of purinergic receptors modulates chemokine expression in human keratinocytes. J. Invest. Dermatol. 127: 660-667.
20. Holzer, A. M., and R. D. Granstein. 2004. Role of extracellular adenosine triphosphate in human skin. J. Cutan. Med. Surg. 8: 90-96.
21. Dixon, C. J., W. B. Bowler, A. Littlewood-Evans, J. P. Dillon, G. Bilbe, G. R. Sharpe, and J. A. Gallagher. 1999. Regulation of epidermal homeostasis through P2Y2 receptors. Br. J. Pharmacol. 127: 1680-1686.
22. Weber, F. C., P. R. Esser, T. Müller, J. Ganesan, P. Pellegatti, M. M. Simon, R. Zeiser, M. Idzko, T. Jakob, and S. F. Martin. 2010. Lack of the purinergic receptor P2X(7) results in resistance to contact hypersensitivity. J. Exp. Med. 207: 2609-2619.
23. Georgiou, J. G., K. K. Skarratt, S. J. Fuller, C. J. Martin, R. I. Christopherson, J. S. Wiley, and R. Sluyter. 2005. Human epidermal and monocyte-derived langerhans cells express functional P2X receptors. J. Invest. Dermatol. 125: 482-490.
24. Tran, J. N. S. N., A. Pupovac, R. M. Taylor, J. S. Wiley, S. N. Byrne, and R. Sluyter. 2010. Murine epidermal Langerhans cells and keratinocytes express functional P2X7 receptors. Exp. Dermatol. 19: e151-e157.
25. Larregina, A. T., A. E. Morelli, L. A. Spencer, A. J. Logar, S. C. Watkins, A. W. Thomson, and L. D. Falo, Jr. 2001. Dermal-resident CD14+ cells differentiate into Langerhans cells. Nat. Immunol. 2: 1151-1158.
26. Pope, M., M. G. Betjes, H. Hirmand, L. Hoffman, and R. M. Steinman. 1995. Both dendritic cells and memory T lymphocytes emigrate from organ cultures of human skin and form distinctive dendritic-T-cell conjugates. J. Invest. Dermatol. 104: 11-17.
27. Nestle, F. O., X. G. Zheng, C. B. Thompson, L. A. Turka, and B. J. Nickoloff. 1993. Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets [published erratum appears in 1994. J. Immunol. 152: 376].
28. J. Immunol. 151: 6535-6545.
29. Mariathasan, S., D. S. Weiss, K. Newton, J. McBride, K. O'Rourke, M. Roose-Girma, W. P. Lee, Y. Weinrauch, D. M. Monack, and V. M. Dixit. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
30. Wiley, J. S., R. Sluyter, B. J. Gu, L. Stokes, and S. J. Fuller. 2011. The human P2X7 receptor and its role in innate immunity. Tissue Antigens 78: 321-332.
31. Wei-yuan, M., L. Wen-ting, Z. Chen, and S. Qing. 2011. Significance of DC-LAMP and DC-SIGN expression in psoriasis vulgaris lesions. Exp. Mol. Pathol. 91: 461-465.
32. Guttman-Yassky, E., M. A. Lowes, J. Fuentes-Duculan, J. Whynot, I. Novitskaya, I. Cardinale, A. Haider, A. Khatcherian, J. A. Carucci, R. Bergman, and J. G. Krueger. 2007. Major differences in inflammatory dendritic cells and their products distinguish atopic dermatitis from psoriasis. J. Allergy Clin. Immunol. 119: 1210-1217.
33. Wollenberg, A., M. Mommaas, T. Oppel, E.-M. Schottdorf, S. Günther, and M. Moderer. 2002. Expression and function of the mannose receptor CD206 on epidermal dendritic cells in inflammatory skin diseases. J. Invest. Dermatol. 118: 327-334.
34. Fuentes-Duculan, J., M. Suárez-Fariñas, L. C. Zaba, K. E. Nograles, K. C. Pierson, H. Mitsui, C. A. Pensabene, J. Kzhyshkowska, J. G. Krueger, and M. A. Lowes. 2010. A subpopulation of CD163-positive macrophages is classically activated in psoriasis. J. Invest. Dermatol. 130: 2412-2422.
35. Lowes, M. A., F. Chamian, M. V. Abello, J. Fuentes-Duculan, S. L. Lin, R. Nussbaum, I. Novitskaya, H. Carbonaro, I. Cardinale, T. Kikuchi, et al. 2005. Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc. Natl. Acad. Sci. USA 102: 19057-19062.
36. Nair, R. P., K. C. Duffin, C. Helms, J. Ding, P. E. Stuart, D. Goldgar, J. E. Gudjonsson, Y. Li, T. Tejasvi, B.-J. Feng, et al; Collaborative Association Study of Psoriasis. 2009. Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat. Genet. 41: 199-204.
37. Tonel, G., C. Conrad, U. Laggner, P. Di Meglio, K. Grys, T. K. McClanahan, W. M. Blumenschein, J. Z. Qin, H. Xin, E. Oldham, et al. 2010. Cutting edge: A critical functional role for IL-23 in psoriasis. J. Immunol. 185: 5688-5691.
38. Belladonna, M. L., J. C. Renauld, R. Bianchi, C. Vacca, F. Fallarino, C. Orabona, M. C. Fioretti, U. Grohmann, and P. Puccetti. 2002. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J. Immunol. 168: 5448-5454.
39. Zheng, Y., D. M. Danilenko, P. Valdez, I. Kasman, J. Eastham-Anderson, J. Wu, and W. Ouyang. 2007. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445: 648-651.
40. Liu, J., Y. Duan, X. Cheng, X. Chen, W. Xie, H. Long, Z. Lin, and B. Zhu. 2011. IL-17 is associated with poor prognosis and promotes angiogenesis via stimulating VEGF production of cancer cells in colorectal carcinoma. Biochem. Biophys. Res. Commun. 407: 348-354.
41. Pickens, S. R., M. V. Volin, A. M. Mandelin, II, J. K. Kolls, R. M. Pope, and S. Shahrara. 2010. IL-17 contributes to angiogenesis in rheumatoid arthritis. J. Immunol. 184: 3233-3241.
42. Grigoryev, Y. A., S. M. Kurian, T. Hart, A. A. Nakorchevsky, C. Chen, D. Campbell, S. R. Head, J. R. Yates, III, and D. R. Salomon. 2011. MicroRNA regulation of molecular networks mapped by global microRNA, mRNA, and protein expression in activated T lymphocytes. J. Immunol. 187: 2233-2243.
43. Du, C., C. Liu, J. Kang, G. Zhao, Z. Ye, S. Huang, Z. Li, Z. Wu, and G. Pei. MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat. Immunol. 10: 1252-1259.
44. Liu, Y., Y. Xiao, and Z. Li. 2011. P2X7 receptor positively regulates MyD88-dependent NF-κB activation. Cytokine 55: 229-236.
45. Joyce, C. E., X. Zhou, J. Xia, C. Ryan, B. Thrash, A. Menter, W. Zhang, and A. M. Bowcock. 2011. Deep sequencing of small RNAs from human skin reveals major alterations in the psoriasis miRNAome. Hum. Mol. Genet. 20: 4025-4040.
46. Zibert, J. R., M. B. Løvendorf, T. Litman, J. Olsen, B. Kaczkowski, and L. Skov. 2010. MicroRNAs and potential target interactions in psoriasis. J. Dermatol. Sci. 58: 177-185.
47. Xia, Y. P., B. Li, D. Hylton, M. Detmar, G. D. Yancopoulos, and J. S. Rudge. 2003. Transgenic delivery of VEGF to mouse skin leads to an inflammatory condition resembling human psoriasis. Blood 102: 161-168.
48. Goodman, W. A., A. D. Levine, J. V. Massari, H. Sugiyama, T. S. McCormick, and K. D. Cooper. 2009. IL-6 signaling in psoriasis prevents immune suppression by regulatory T cells. J. Immunol. 183: 3170-3176.
49. Liu, L.-Z., C. Li, Q. Chen, Y. Jing, R. Carpenter, Y. Jiang, H.-F. Kung, L. Lai, and B.-H. Jiang. 2011. MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression. PLoS ONE 6: e19139.
50. Schonthaler, H. B., R. Huggenberger, S. K. Wculek, M. Detmar, and E. F. Wagner. 2009. Systemic anti-VEGF treatment strongly reduces skin inflammation in a mouse model of psoriasis. Proc. Natl. Acad. Sci. USA 106: 21264-21269.
51. Zaba, L. C., M. Suarez-Farinas, J. Fuentes-Duculan, K. E. Nograles, E. Guttman-Yassky, I. Cardinale, M. A. Lowes, and J. G. Krueger. 2009. Effective treatment of psoriasis with etanercept is linked to suppression of IL-17 signaling, not immediate response TNF genes. J. Allergy Clin. Immunol. 124: 1022-1010. e1021-1395.
52. Lowes, M. A., A. M. Bowcock, and J. G. Krueger. 2007. Pathogenesis and therapy of psoriasis. Nature 445: 866-873.
53. Chiricozzi, A., E. Guttman-Yassky, M. Suárez-Fariñas, K. E. Nograles, S. Tian, I. Cardinale, S. Chimenti, and J. G. Krueger. 2011. Integrative responses to IL-17 and TNF-α in human keratinocytes account for key inflammatory pathogenic circuits in psoriasis. J. Invest. Dermatol. 131: 677-687.
54. Jung, K., D. Lee, H. S. Lim, S. I. Lee, Y. J. Kim, G. M. Lee, S. C. Kim, and G. Y. Koh. 2011. Double anti-angiogenic and anti-inflammatory protein Valpha targeting VEGF-A and TNF-alpha in retinopathy and psoriasis. J. Biol. Chem. 286: 14410-14418.
55. Zaba, L. C., J. Fuentes-Duculan, N. J. Eungdamrong, L. M. Johnson-Huang, K. E. Nograles, T. R. White, K. C. Pierson, T. Lentini, M. Suarez-Farinas, M. A. Lowes, and J. G. Krueger. 2010. Identification of TNF-related apoptosis-inducing ligand and other molecules that distinguish inflammatory from resident dendritic cells in patients with psoriasis. J. Allergy Clin. Immunol. 125: 1261-1268.e1269.
56. Barberà-Cremades, M., A. Baroja-Mazo, A. I. Gomez, F. Machado, F. Di Virgilio, and P. Pelegrín. 2012. P2X7 receptor-stimulation causes fever via PGE2 and IL-1β release. FASEB J. 26: 2951-2962.
57. Veglianese, P., D. Lo Coco, M. Bao Cutrona, R. Magnoni, D. Pennacchini, B. Pozzi, G. Gowing, J. P. Julien, M. Tortarolo, and C. Bendotti. 2006. Activation of the p38MAPK cascade is associated with upregulation of TNF alpha receptors in the spinal motor neurons of mouse models of familial ALS. Mol. Cell. Neurosci. 31: 218-231.
58. Shen, Q., R. Zhang, and N. R. Bhat. 2006. MAP kinase regulation of IP10/CXCL10 chemokine gene expression in microglial cells. Brain Res. 1086: 9-16.
59. Shimada, K., T. R. Crother, J. Karlin, S. Chen, N. Chiba, V. K. Ramanujan, L. Vergnes, D. M. Ojcius, and M. Arditi. 2011. Caspase-1 dependent IL-1β secretion is critical for host defense in a mouse model of Chlamydia pneumoniae lung infection. PLoS ONE 6: e21477.
60. León, B., and C. Ardavín. 2008. Monocyte-derived dendritic cells in innate and adaptive immunity. Immunol. Cell Biol. 86: 320-324.
61. Yang, D., Q. Chen, H. Yang, K. J. Tracey, M. Bustin, and J. J. Oppenheim. 2007. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J. Leukoc. Biol. 81: 59-66.
62. Dumitriu, I. E., M. E. Bianchi, M. Bacci, A. A. Manfredi, and P. Rovere-Querini. 2007. The secretion of HMGB1 is required for the migration of maturing dendritic cells. J. Leukoc. Biol. 81: 84-91.
63. Lamkanfi, M., A. Sarkar, L. Vande Walle, A. C. Vitari, A. O. Amer, M. D. Wewers, K. J. Tracey, T.-D. Kanneganti, and V. M. Dixit. 2010. Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J. Immunol. 185: 4385-4392.
64. Telusma, G., S. Datta, I. Mihajlov, W. Ma, J. Li, H. Yang, W. Newman, B. T. Messmer, B. Minev, I. G. Schmidt-Wolf, et al. 2006. Dendritic cell activating peptides induce distinct cytokine profiles. Int. Immunol. 18: 1563-1573.
65. Lohwasser, C., D. Neureiter, B. Weigle, T. Kirchner, and D. Schuppan. 2006. The receptor for advanced glycation end products is highly expressed in the skin and upregulated by advanced glycation end products and tumor necrosis factor-alpha. J. Invest. Dermatol. 126: 291-299.
66. Shubbar, E., J. Vegfors, M. Carlström, S. Petersson, and C. Enerbäck. 2012. Psoriasin (S100A7) increases the expression of ROS and VEGF and acts through RAGE to promote endothelial cell proliferation. Breast Cancer Res. Treat. 134: 71-80.
67. Krueger, J. G., S. Fretzin, M. Suarez-Farinas, P. A. Haslett, K. M. Phipps, G. S. Cameron, J. McColm, A. Katcherian, I. Cueto, T. White, S. Banerjee, and R. W. Hoffman. 2012. IL-17A is essential for cell activation and inflammatory gene circuits in subjects with psoriasis. J. Allergy Clin. Immunol. 130: 145-154.e149.
68. Li, J., X. Chen, Z. Liu, Q. Yue, and H. Liu. 2007. Expression of Th17 cytokines in skin lesions of patients with psoriasis. J. Huazhong Univ. Sci. Technolog. Med. Sci. 27: 330-332.
69. Choi, J. P., Y. S. Kim, Y. M. Tae, E. J. Choi, B. S. Hong, S. G. Jeon, Y. S. Gho, Z. Zhu, and Y. K. Kim. 2010. A viral PAMP double-stranded RNA induces allergen-specific Th17 cell response in the airways which is dependent on VEGF and IL-6. Allergy 65: 1322-1330.
70. Sluyter, R., and L. Stokes. 2011. Significance of P2X7 receptor variants to human health and disease. Recent Pat. DNA Gene Seq. 5: 41-54.
71. Adinolfi, E., M. Cirillo, R. Woltersdorf, S. Falzoni, P. Chiozzi, P. Pellegatti, M. G. Callegari, D. Sandonà, F. Markwardt, G. Schmalzing, and F. Di Virgilio. 2010. Trophic activity of a naturally occurring truncated isoform of the P2X7 receptor. FASEB J. 24: 3393-3404.
72. Aizu, T., K. Tamai, H. Nakano, D. Rokunohe, Y. Toyomaki, J. Uitto, and D. Sawamura. 2008. Calcineurin/NFAT-dependent regulation of 230-kDa bullous pemphigoid antigen (BPAG1) gene expression in normal human epidermal keratinocytes. J. Dermatol. Sci. 51: 45-51.
73. Hampton, P. J., R. Jans, R. J. Flockhart, G. Parker, and N. J. Reynolds. 2012. Lithium regulates keratinocyte proliferation via glycogen synthase kinase 3 and NFAT2 (nuclear factor of activated T cells 2). J. Cell. Physiol. 227: 1529-1537.
74. Mankus, C., C. Rich, M. Minns, and V. Trinkaus-Randall. 2011. Corneal epithelium expresses a variant of P2X(7) receptor in health and disease. PLoS ONE 6: e28541.
75. Zhou, L., X. Qi, J. A. Potashkin, F. W. Abdul-Karim, and G. I. Gorodeski. 2008. MicroRNAs miR-186 and miR-150 down-regulate expression of the proapoptotic purinergic P2X7 receptor by activation of instability sites at the 39-untranslated region of the gene that decrease steady-state levels of the transcript. J. Biol. Chem. 283: 28274-28286.
76. Lerman, G., C. Avivi, C. Mardoukh, A. Barzilai, A. Tessone, B. Gradus, F. Pavlotsky, I. Barshack, S. Polak-Charcon, A. Orenstein, et al. 2011. MiRNA expression in psoriatic skin: reciprocal regulation of hsa-miR-99a and IGF-1R. PLoS ONE 6: e20916.