Human mast cells capture, store, and release bioactive, exogenous IL-17A

Journal of Leukocyte Biology

Volumn 100, Issue 3, 2016, Pages 453-462

  Noordenbos, Troy ^a   Blijdorp, Iris ^a   Chen, Sijia ^a   Stap, Jan ^b   Mul, Erik ^c   Cañete, Juan D ^d   Lubberts, Erik ^e   Yeremenko, Nataliya ^a   Baeten, Dominique ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d HOSPITAL CLÍNIC   (Spain)

^e ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

MRNA expression; Spondyloarthritis; Uptake

Indexed keywords

INTERLEUKIN 17; MEMBRANE RECEPTOR; IL17A PROTEIN, HUMAN;

ARTICLE; CELL GRANULE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOCYTOSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERNALIZATION; MAST CELL; PRIORITY JOURNAL; SYNOVIUM; TONSIL; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM; PALATINE TONSIL; PHYSIOLOGY; SYNOVIOCYTE;

CELLS, CULTURED; ENDOCYTOSIS; HUMANS; INTERLEUKIN-17; MAST CELLS; PALATINE TONSIL; SYNOVIOCYTES;

EID: 84985027805     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3HI1215-542R     Document Type: Article

References (60)

1. Korn, T., Bettelli, E., Oukka, M., Kuchroo, V. K. (2009) IL-17 and Th17 cells. Annu. Rev. Immunol. 27, 485-517.
2. Miossec, P., Korn, T., Kuchroo, V. K. (2009) Interleukin-17 and type 17 helper T cells. N. Engl. J. Med. 361, 888-898.
3. Cua, D. J., Sherlock, J., Chen, Y., Murphy, C. A., Joyce, B., Seymour, B., Lucian, L., To, W., Kwan, S., Churakova, T., Zurawski, S., Wiekowski, M., Lira, S. A., Gorman, D., Kastelein, R. A., Sedgwick, J. D. (2003) Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744-748.
4. Murphy, C. A., Langrish, C. L., Chen, Y., Blumenschein, W., McClanahan, T., Kastelein, R. A., Sedgwick, J. D., Cua, D. J. (2003) Divergent pro-and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198, 1951-1957.
5. Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y.-H., Wang, Y., Hood, L., Zhu, Z., Tian, Q., Dong, C. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141.
6. Ivanov, I. I., McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J., Littman, D. R. (2006) The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126, 1121-1133.
7. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L., Kuchroo, V. K. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238.
8. PHOENIX 1 Study Investigators. (2008) Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 1). Lancet 371, 1665-1674.
9. Gottlieb, A., Menter, A., Mendelsohn, A., Shen, Y.-K., Li, S., Guzzo, C., Fretzin, S., Kunynetz, R., Kavanaugh, A. (2009) Ustekinumab, a human interleukin 12/23 monoclonal antibody, for psoriatic arthritis: randomised, double-blind, placebo-controlled, crossover trial. Lancet 373, 633-640.
10. Sofen, H., Smith, S., Matheson, R. T., Leonardi, C. L., Calderon, C., Brodmerkel, C., Li, K., Campbell, K., Marciniak, Jr., S. J., Wasfi, Y., Wang, Y., Szapary, P., Krueger, J. G. (2014) Guselkumab (an IL-23-specific mAb) demonstrates clinical and molecular response in patients with moderateto-severe psoriasis. J. Allergy Clin. Immunol. 133, 1032-1040.
11. Psoriasis Study Group; Rheumatoid Arthritis Study Group; Uveitis Study Group. (2010) Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci. Transl. Med. 2, 52ra72.
12. Baeten, D., Baraliakos, X., Braun, J., Sieper, J., Emery, P., van der Heijde, D., McInnes, I., van Laar, J. M., Landewé, R., Wordsworth, P., Wollenhaupt, J., Kellner, H., Paramarta, J., Wei, J., Brachat, A., Bek, S., Laurent, D., Li, Y., Wang, Y. A., Bertolino, A. P., Gsteiger, S., Wright, A. M., Hueber, W. (2013) Anti-interleukin-17A monoclonal antibody secukinumab in treatment of ankylosing spondylitis: a randomised, double-blind, placebo-controlled trial. Lancet 382, 1705-1713.
13. ERASURE Study Group; FIXTURE Study Group. (2014) Secukinumab in plaque psoriasis-results of two phase 3 trials. N. Engl. J. Med. 371, 326-338.
14. Mease, P. J., Genovese, M. C., Greenwald, M. W., Ritchlin, C. T., Beaulieu, A. D., Deodhar, A., Newmark, R., Feng, J., Erondu, N., Nirula, A. (2014) Brodalumab, an anti-IL17RA monoclonal antibody, in psoriatic arthritis. N. Engl. J. Med. 370, 2295-2306.
15. Papp, K. A., Leonardi, C., Menter, A., Ortonne, J.-P., Krueger, J. G., Kricorian, G., Aras, G., Li, J., Russell, C. B., Thompson, E. H., Baumgartner, S. (2012) Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N. Engl. J. Med. 366, 1181-1189.
16. Secukinumab in Crohn’s Disease Study Group. (2012) Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn’s disease: unexpected results of a randomised, double-blind placebocontrolled trial. Gut 61, 1693-1700.
17. Ustekinumab Crohn’s Disease Study Group. (2008) A randomized trial of Ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with moderate-to-severe Crohn’s disease. Gastroenterology 135, 1130-1141.
18. Dougados, M., Baeten, D. (2011) Spondyloarthritis. Lancet 377, 2127-2137.
19. Kenna, T. J., Davidson, S. I., Duan, R., Bradbury, L. A., McFarlane, J., Smith, M., Weedon, H., Street, S., Thomas, R., Thomas, G. P., Brown, M. A. (2012) Enrichment of circulating interleukin-17-secreting interleukin-23 receptor-positive g/d T cells in patients with active ankylosing spondylitis. Arthritis Rheum. 64, 1420-1429.
20. Coffre, M., Roumier, M., Rybczynska, M., Sechet, E., Law, H. K. W., Gossec, L., Dougados, M., Bianchi, E., Rogge, L. (2013) Combinatorial control of Th17 and Th1 cell functions by genetic variations in genes associated with the interleukin-23 signaling pathway in spondyloarthritis. Arthritis Rheum. 65, 1510-1521.
21. Bowness, P., Ridley, A., Shaw, J., Chan, A. T., Wong-Baeza, I., Fleming, M., Cummings, F., McMichael, A., Kollnberger, S. (2011) Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J. Immunol. 186, 2672-2680.
22. Hueber, A. J., Asquith, D. L., Miller, A. M., Reilly, J., Kerr, S., Leipe, J., Melendez, A. J., McInnes, I. B. (2010) Mast cells express IL-17A in rheumatoid arthritis synovium. J. Immunol. 184, 3336-3340.
23. Moran, E. M., Heydrich, R., Ng, C. T., Saber, T. P., McCormick, J., Sieper, J., Appel, H., Fearon, U., Veale, D. J. (2011) IL-17A expression is localised to both mononuclear and polymorphonuclear synovial cell infiltrates. PLoS One 6, e24048.
24. Appel, H., Maier, R., Wu, P., Scheer, R., Hempfing, A., Kayser, R., Thiel, A., Radbruch, A., Loddenkemper, C., Sieper, J. (2011) Analysis of IL-17(+) cells in facet joints of patients with spondyloarthritis suggests that the innate immune pathway might be of greater relevance than the Th17-mediated adaptive immune response. Arthritis Res. Ther. 13, R95.
25. Noordenbos, T., Yeremenko, N., Gofita, I., van de Sande, M., Tak, P. P., Caňete, J. D., Baeten, D. (2012) Interleukin-17-positive mast cells contribute to synovial inflammation in spondylarthritis. Arthritis Rheum. 64, 99-109.
26. Suurmond, J., Dorjée, A. L., Boon, M. R., Knol, E. F., Huizinga, T. W. J., Toes, R. E. M., Schuerwegh, A. J. (2011) Mast cells are the main interleukin 17-positive cells in anticitrullinated protein antibody-positive and-negative rheumatoid arthritis and osteoarthritis synovium. Arthritis Res. Ther. 13, R150.
27. Truchetet, M.-E., Brembilla, N.-C., Montanari, E., Lonati, P., Raschi, E., Zeni, S., Fontao, L., Meroni, P. L., Chizzolini, C. (2013) Interleukin-17A+ cell counts are increased in systemic sclerosis skin and their number is inversely correlated with the extent of skin involvement. Arthritis Rheum. 65, 1347-1356.
28. Lin, A. M., Rubin, C. J., Khandpur, R., Wang, J. Y., Riblett, M., Yalavarthi, S., Villanueva, E. C., Shah, P., Kaplan, M. J., Bruce, A. T. (2011) Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 187, 490-500.
29. Keijsers, R. R. M. C., Hendriks, A. G. M., van Erp, P. E. J., van Cranenbroek, B., van de Kerkhof, P. C. M., Koenen, H. J. P. M., Joosten, I. (2014) In vivo induction of cutaneous inflammation results in the accumulation of extracellular trap-forming neutrophils expressing RORgt and IL-17. J. Invest. Dermatol. 134, 1276-1284.
30. Velden, J., Paust, H.-J., Hoxha, E., Turner, J.-E., Steinmetz, O. M., Wolf, G., Jabs, W. J., Ö zcan, F., Beige, J., Heering, P. J., Schröder, S., Kneißler, U., Disteldorf, E., Mittrücker, H. W., Stahl, R. A., Helmchen, U., Panzer, U. (2012) Renal IL-17 expression in human ANCA-associated glomerulonephritis. Am. J. Physiol. Renal Physiol. 302, F1663-F1673.
31. Yapici, Ü., Kers, J., Bemelman, F. J., Roelofs, J. J. T. H., Groothoff, J. W., van der Loos, C. M., vanDonselaar-vander Pant, K. A., Idu, M. M., Claessen, N., ten Berge, I. J., Florquin, S. (2011) Interleukin-17 positive cells accumulate in renal allografts during acute rejection and are independent predictors of worse graft outcome. Transpl. Int. 24, 1008-1017.
32. de Boer, O. J., van der Meer, J. J., Teeling, P., van der Loos, C. M., Idu, M. M., van Maldegem, F., Aten, J., van der Wal, A. C. (2010) Differential expression of interleukin-17 family cytokines in intact and complicated human atherosclerotic plaques. J. Pathol. 220, 499-508.
33. Fiala, M., Chattopadhay, M., La Cava, A., Tse, E., Liu, G., Lourenco, E., Eskin, A., Liu, P. T., Magpantay, L., Tse, S., Mahanian, M., Weitzman, R., Tong, J., Nguyen, C., Cho, T., Koo, P., Sayre, J., Martinez-Maza, O., Rosenthal, M. J., Wiedau-Pazos, M. (2010) IL-17A is increased in the serum and in spinal cord CD8 and mast cells of ALS patients. J. Neuroinflammation 7, 76.
34. Jain, P., Javdan, M., Feger, F. K., Chiu, P. Y., Sison, C., Damle, R. N., Bhuiya, T. A., Sen, F., Abruzzo, L. V., Burger, J. A., Rosenwald, A., Allen, S. L., Kolitz, J. E., Rai, K. R., Chiorazzi, N., Sherry, B. (2012) Th17 and non-Th17 interleukin-17-expressing cells in chronic lymphocytic leukemia: delineation, distribution, and clinical relevance. Haematologica 97, 599-607.
35. Wang, B., Li, L., Liao, Y., Li, J., Yu, X., Zhang, Y., Xu, J., Rao, H., Chen, S., Zhang, L., Zheng, L. (2013) Mast cells expressing interleukin 17 in the muscularis propria predict a favorable prognosis in esophageal squamous cell carcinoma. Cancer Immunol. Immunother. 62, 1575-1585.
36. Liu, X., Jin, H., Zhang, G., Lin, X., Chen, C., Sun, J., Zhang, Y., Zhang, Q., Yu, J. (2014) Intratumor IL-17-positive mast cells are the major source of the IL-17 that is predictive of survival in gastric cancer patients. PLoS One 9, e106834.
37. Price, A. E., Reinhardt, R. L., Liang, H.-E., Locksley, R. M. (2012) Marking and quantifying IL-17A-producing cells in vivo. PLoS One 7, e39750.
38. Awasthi, A., Riol-Blanco, L., Jäger, A., Korn, T., Pot, C., Galileos, G., Bettelli, E., Kuchroo, V. K., Oukka, M. (2009) Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J. Immunol. 182, 5904-5908.
39. Eberl, G., Marmon, S., Sunshine, M.-J., Rennert, P. D., Choi, Y., Littman, D. R. (2004) An essential function for the nuclear receptor RORgamma (t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5, 64-73.
40. Croxford, A. L., Kurschus, F. C., Waisman, A. (2009) Cutting edge: an IL-17F-CreEYFP reporter mouse allows fate mapping of Th17 cells. J. Immunol. 182, 1237-1241.
41. Huppler, A. R., Verma, A. H., Conti, H. R., Gaffen, S. L. (2015) Neutrophils do not express IL-17A in the context of acute oropharyngeal candidiasis. Pathogens 4, 559-572.
42. Baeten, D., Van den Bosch, F., Elewaut, D., Stuer, A., Veys, E. M., De Keyser, F. (1999) Needle arthroscopy of the knee with synovial biopsy sampling: technical experience in 150 patients. Clin. Rheumatol. 18, 434-441.
43. Bachelet, I., Munitz, A., Levi-Schaffer, F. (2006) Co-culture of mast cells with fibroblasts: a tool to study their crosstalk. Methods Mol. Biol. 315, 295-317.
44. Kirshenbaum, A. S., Akin, C., Wu, Y., Rottem, M., Goff, J. P., Beaven, M. A., Rao, V. K., Metcalfe, D. D. (2003) Characterization of novel stem cell factor responsive human mast cell lines LAD 1 and 2 established from a patient with mast cell sarcoma/leukemia; activation following aggregation of FcepsilonRI or FcgammaRI. Leuk. Res. 27, 677-682.
45. Acosta-Rodriguez, E. V., Napolitani, G., Lanzavecchia, A., Sallusto, F. (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.
46. Joshi, S., Perera, S., Gilbert, J., Smith, C. M., Mariana, A., Gordon, C. P., Sakoff, J. A., McCluskey, A., Robinson, P. J., Braithwaite, A. W., Chircop, M. (2010) The dynamin inhibitors MiTMAB and OcTMAB induce cytokinesis failure and inhibit cell proliferation in human cancer cells. Mol. Cancer Ther. 9, 1995-2006.
47. Yao, Z., Fanslow, W. C., Seldin, M. F., Rousseau, A. M., Painter, S. L., Comeau, M. R., Cohen, J. I., Spriggs, M. K. (1995) Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3, 811-821.
48. Hot, A., Zrioual, S., Lenief, V., Miossec, P. (2012) IL-17 and tumour necrosis factor a combination induces a HIF-1a-dependent invasive phenotype in synoviocytes. Ann. Rheum. Dis. 71, 1393-1401.
49. Hamada, H., Garcia-Hernandez, Mde. L., Reome, J. B., Misra, S. K., Strutt, T. M., McKinstry, K. K., Cooper, A. M., Swain, S. L., Dutton, R. W. (2009) Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J. Immunol. 182, 3469-3481.
50. Stark, M. A., Huo, Y., Burcin, T. L., Morris, M. A., Olson, T. S., Ley, K. (2005) Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22, 285-294.
51. Cupedo, T., Crellin, N. K., Papazian, N., Rombouts, E. J., Weijer, K., Grogan, J. L., Fibbe, W. E., Cornelissen, J. J., Spits, H. (2009) Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat. Immunol. 10, 66-74.
52. Reich, K., Papp, K. A., Matheson, R. T., Tu, J. H., Bissonnette, R., Bourcier, M., Gratton, D., Kunynetz, R. A., Poulin, Y., Rosoph, L. A., Stingl, G., Bauer, W. M., Salter, J. M., Falk, T. M., Blödorn-Schlicht, N. A., Hueber, W., Sommer, U., Schumacher, M. M., Peters, T., Kriehuber, E., Lee, D. M., Wieczorek, G. A., Kolbinger, F., Bleul, C. C. (2015) Evidence that a neutrophil-keratinocyte crosstalk is an early target of IL-17A inhibition in psoriasis. Exp. Dermatol. 24, 529-535.
53. Mashiko, S., Bouguermouh, S., Rubio, M., Baba, N., Bissonnette, R., Sarfati, M. (2015) Human mast cells are major IL-22 producers in patients with psoriasis and atopic dermatitis. J. Allergy Clin. Immunol. 136, 351.e1-359.e1.
54. Sibilano, R., Frossi, B., Calvaruso, M., Danelli, L., Betto, E., Dall’Agnese, A., Tripodo, C., Colombo, M. P., Pucillo, C. E., Gri, G. (2012) The aryl hydrocarbon receptor modulates acute and late mast cell responses. J. Immunol. 189, 120-127.
55. Taylor, P. R., Roy, S., Leal, S. M., Sun, Y., Howell, S. J., Cobb, B. A., Li, X., Pearlman, E. (2014) Activation of neutrophils by autocrine IL-17A-IL-17RC interactions during fungal infection is regulated by IL-6, IL-23, RORgt and dectin-2. Nat. Immunol. 15, 143-151.
56. Tamarozzi, F., Wright, H. L., Thomas, H. B., Edwards, S. W., Taylor, M. J. (2014) A lack of confirmation with alternative assays questions the validity of IL-17A expression in human neutrophils using immunohistochemistry. Immunol. Lett. 162, 194-198.
57. Olszewski, M. B., Groot, A. J., Dastych, J., Knol, E. F. (2007) TNF trafficking to human mast cell granules: mature chain-dependent endocytosis. J. Immunol. 178, 5701-5709.
58. Hafez, M. M., Costlow, M. E. (1988) Prolactin binding and localization in rat mammary tumor mast cells. Cancer Res. 48, 3765-3771.
59. Ely, L. K., Fischer, S., Garcia, K. C. (2009) Structural basis of receptor sharing by interleukin 17 cytokines. Nat. Immunol. 10, 1245-1251.
60. Mellett, M., Atzei, P., Horgan, A., Hams, E., Floss, T., Wurst, W., Fallon, P. G., Moynagh, P. N. (2012) Orphan receptor IL-17RD tunes IL-17A signalling and is required for neutrophilia. Nat. Commun. 3, 1119.