Induction of IL-17 production from human peripheral blood CD4+ cells by asbestos exposure

Maeda,Megumi; Chen,Ying; Lee,Suni; Kumagai-Takei,Naoko; Yoshitome,Kei; Matsuzaki,Hidenori; Yamamoto,Shoko; Hatayama,Tamayo; Ikeda,Miho; Nishimura,Yasumitsu; Otsuki,Takemi

doi:10.3892/ijo.2017.3991

Induction of IL-17 production from human peripheral blood CD4+ cells by asbestos exposure

Authors:
- Megumi Maeda
- Ying Chen
- Suni Lee
- Naoko Kumagai-Takei
- Kei Yoshitome
- Hidenori Matsuzaki
- Shoko Yamamoto
- Tamayo Hatayama
- Miho Ikeda
- Yasumitsu Nishimura
- Takemi Otsuki
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Affiliations: Department of Biofunctional Chemistry, Division of Bioscience, Okayama University Graduate School of Natural Science and Technology, Okayama, Japan, Department of Hygiene, Kawasaki Medical School, Kurashiki, Japan
Published online on: May 9, 2017 https://doi.org/10.3892/ijo.2017.3991
Pages: 2024-2032

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Abstract

We have previously reported that chronic, recurrent and low-dose exposure to asbestos fibers causes a reduction in antitumor immunity. Investigation of natural killer (NK) cells using an in vitro cell line model and comprising in vitro activation using freshly isolated NK cells co-cultured with chrysotile fibers, as well as NK cells derived from asbestos-exposed patients with pleural plaque (PP) or malignant mesothelioma (MM), revealed decreased expression of NK cell activating receptors such as NKG2D, 2B4 and NKp46. An in vitro differentiation and clonal expansion model for CD8+ cytotoxic T lymphocytes (CTLs) showed reduced cytotoxicity with decreased levels of cytotoxic molecules such as granzyme B and perforin, as well as suppressed proliferation of CTLs. Additionally, analysis of T helper cells showed that surface CXCR3, chemokine receptor, and the productive potential of interferon (IFN)γ were reduced following asbestos exposure in an in vitro cell line model and in peripheral CD4+ cells of asbestos-exposed patients. Moreover, experiments revealed that asbestos exposure enhanced regulatory T cell (Treg) function. This study also focused on CXCR3 expression and the Th-17 cell fraction. Following activation with T-cell receptor and co-culture with various concentrations of chrysotile fibers using freshly isolated CD4+ surface CXCR3 positive and negative fractions, the intracellular expression of CXCR3, IFNγ and IL-17 remained unchanged when co-cultured with chrysotile. However, subsequent re-stimulation with phorbol 12-myristate 13-acetate (PMA) and ionomycin resulted in enhanced IL-17 production and expression, particularly in CD4+ surface CXCR3 positive cells. These results indicated that the balance and polarization between Treg and Th-17 fractions play an important role with respect to the immunological effects of asbestos and the associated reduction in antitumor immunity.

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1	Fujimura N: Pathology and pathophysiology of pneumoconiosis. Curr Opin Pulm Med. 6:140–144. 2000. View Article : Google Scholar : PubMed/NCBI
2	Mossman BT and Churg A: Mechanisms in the pathogenesis of asbestosis and silicosis. Am J Respir Crit Care Med. 157:1666–1680. 1998. View Article : Google Scholar : PubMed/NCBI
3	Seaman DM, Meyer CA and Kanne JP: Occupational and environmental lung disease. Clin Chest Med. 36:249–268. 2015. View Article : Google Scholar : PubMed/NCBI
4	Cassel SL, Eisenbarth SC, Iyer SS, Sadler JJ, Colegio OR, Tephly LA, Carter AB, Rothman PB, Flavell RA and Sutterwala FS: The Nalp3 inflammasome is essential for the development of silicosis. Proc Natl Acad Sci USA. 105:9035–9040. 2008. View Article : Google Scholar : PubMed/NCBI
5	Dostert C, Pétrilli V, Van Bruggen R, Steele C, Mossman BT and Tschopp J: Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science. 320:674–677. 2008. View Article : Google Scholar : PubMed/NCBI
6	Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, Fitzgerald KA and Latz E: Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol. 9:847–856. 2008. View Article : Google Scholar : PubMed/NCBI
7	Nishimura Y, Miura Y, Maeda M, Kumagai N, Murakami S, Hayashi H, Fukuoka K, Nakano T and Otsuki T: Impairment in cytotoxicity and expression of NK cell- activating receptors on human NK cells following exposure to asbestos fibers. Int J Immunopathol Pharmacol. 22:579–590. 2009. View Article : Google Scholar : PubMed/NCBI
8	Nishimura Y, Maeda M, Kumagai N, Hayashi H, Miura Y and Otsuki T: Decrease in phosphorylation of ERK following decreased expression of NK cell-activating receptors in human NK cell line exposed to asbestos. Int J Immunopathol Pharmacol. 22:879–888. 2009. View Article : Google Scholar
9	Nishimura Y, Maeda M, Kumagai-Takei N, Lee S, Matsuzaki H, Wada Y, Nishiike-Wada T, Iguchi H and Otsuki T: Altered functions of alveolar macrophages and NK cells involved in asbestos-related diseases. Environ Health Prev Med. 18:198–204. 2013. View Article : Google Scholar : PubMed/NCBI
10	Kumagai-Takei N, Nishimura Y, Maeda M, Hayashi H, Matsuzaki H, Lee S, Hiratsuka J and Otsuki T: Effect of asbestos exposure on differentiation of cytotoxic T lymphocytes in mixed lymphocyte reaction of human peripheral blood mononuclear cells. Am J Respir Cell Mol Biol. 49:28–36. 2013. View Article : Google Scholar : PubMed/NCBI
11	Kumagai-Takei N, Nishimura Y, Maeda M, Hayashi H, Matsuzaki H, Lee S, Kishimoto T, Fukuoka K, Nakano T and Otsuki T: Functional properties of CD8(+) lymphocytes in patients with pleural plaque and malignant mesothelioma. J Immunol Res. 2014:6701402014. View Article : Google Scholar : PubMed/NCBI
12	Kumagai-Takei N, Nishimura Y, Matsuzaki H, Maeda M, Lee S, Yoshitome K and Otsuki T: Effects of asbestos fibers on human cytotoxic T cells. Biological Effects of Fibrous and Particulate Substances (Series Title: Current Topics in Environmental Health and Preventive Medicine). Otsuki T, Holian A and Yoshioka Y: Springer-Japan; pp. 211–221. 2015
13	Kumagai-Takei N, Nishimura Y, Matsuzaki H, Lee S, Yoshitome K, Hayashi H and Otsuki T: The suppressed induction of human mature cytotoxic T lymphocytes caused by asbestos is not due to Interleukin-2 insufficiency. J Immunol Res. 2016:74848722016. View Article : Google Scholar : PubMed/NCBI
14	Hyodoh F, Takata-Tomokuni A, Miura Y, Sakaguchi H, Hatayama T, Hatada S, Katsuyama H, Matsuo Y and Otsuki T: Inhibitory effects of anti-oxidants on apoptosis of a human poly-clonal T-cell line, MT-2, induced by an asbestos, chrysotile-A. Scand J Immunol. 61:442–448. 2005. View Article : Google Scholar : PubMed/NCBI
15	Miura Y, Nishimura Y, Katsuyama H, Maeda M, Hayashi H, Dong M, Hyodoh F, Tomita M, Matsuo Y, Uesaka A, et al: Involvement of IL-10 and Bcl-2 in resistance against an asbestos-induced apoptosis of T cells. Apoptosis. 11:1825–1835. 2006. View Article : Google Scholar : PubMed/NCBI
16	Maeda M, Chen Y, Kumagai-Takei N, Hayashi H, Matsuzaki H, Lee S, Hiratsuka J, Nishimura Y, Kimura Y and Otsuki T: Alteration of cytoskeletal molecules in a human T cell line caused by continuous exposure to chrysotile asbestos. Immunobiology. 218:1184–1191. 2013. View Article : Google Scholar : PubMed/NCBI
17	Maeda M, Nishimura Y, Hayashi H, Kumagai N, Chen Y, Murakami S, Miura Y, Hiratsuka J, Kishimoto T and Otsuki T: Reduction of CXC chemokine receptor 3 in an in vitro model of continuous exposure to asbestos in a human T-cell line, MT-2. Am J Respir Cell Mol Biol. 45:470–479. 2011. View Article : Google Scholar
18	Maeda M, Nishimura Y, Hayashi H, Kumagai N, Chen Y, Murakami S, Miura Y, Hiratsuka J, Kishimoto T and Otsuki T: Decreased CXCR3 expression in CD4⁺ T cells exposed to asbestos or derived from asbestos-exposed patients. Am J Respir Cell Mol Biol. 45:795–803. 2011. View Article : Google Scholar : PubMed/NCBI
19	Kumagai-Takei N, Maeda M, Chen Y, Matsuzaki H, Lee S, Nishimura Y, Hiratsuka J and Otsuki T: Asbestos induces reduction of tumor immunity. Clin Dev Immunol. 2011:4814392011. View Article : Google Scholar : PubMed/NCBI
20	Matsuzaki H, Maeda M, Lee S, Nishimura Y, Kumagai-Takei N, Hayashi H, Yamamoto S, Hatayama T, Kojima Y, Tabata R, et al: Asbestos-induced cellular and molecular alteration of immunocompetent cells and their relationship with chronic inflammation and carcinogenesis. J Biomed Biotechnol. 2012:4926082012. View Article : Google Scholar : PubMed/NCBI
21	Otsuki T, Matsuzaki H, Lee S, Kumagai-Takei N, Yamamoto S, Hatayama T, Yoshitome K and Nishimura Y: Environmental factors and human health: Fibrous and particulate substance-induced immunological disorders and construction of a health-promoting living environment. Environ Health Prev Med. 21:71–81. 2016. View Article : Google Scholar :
22	Craighead JE: Nonthoracic cancers possibly resulting from asbestos exposure. Asbestos and its Diseases. Craighead JE and Gibbs AR: Oxford University Press; New York: pp. 230–252. 2008, View Article : Google Scholar
23	Freidman GK: Malignant diseases attributed to asbestos exposure. Asbestos. Risk assessment, epidemiology, and health effects. Dodson RF and Hammar SP: CRC Press; Boca Raton: pp. 561–592. 2011, View Article : Google Scholar
24	Alizadeh D, Katsanis E and Larmonier N: The multifaceted role of Th17 lymphocytes and their associated cytokines in cancer. Clin Dev Immunol. 2013:9578782013. View Article : Google Scholar
25	Bailey SR, Nelson MH, Himes RA, Li Z, Mehrotra S and Paulos CM: Th17 cells in cancer: The ultimate identity crisis. Front Immunol. 5:2762014. View Article : Google Scholar : PubMed/NCBI
26	Lakshmi Narendra B, Eshvendar Reddy K, Shantikumar S and Ramakrishna S: Immune system: A double-edged sword in cancer. Inflamm Res. 62:823–834. 2013. View Article : Google Scholar : PubMed/NCBI
27	Zou W and Restifo NP: T(H)17 cells in tumour immunity and immunotherapy. Nat Rev Immunol. 10:248–256. 2010. View Article : Google Scholar : PubMed/NCBI
28	Ferro A, Zebedeo CN, Davis C, Ng KW and Pfau JC: Amphibole, but not chrysotile, asbestos induces anti-nuclear autoantibodies and IL-17 in C57BL/6 mice. J Immunotoxicol. 11:283–290. 2014. View Article : Google Scholar
29	Serve KM, Black B, Szeinuk J and Pfau JC: Asbestos-associated mesothelial cell autoantibodies promote collagen deposition in vitro. Inhal Toxicol. 25:774–784. 2013. View Article : Google Scholar : PubMed/NCBI
30	Pfau JC, Serve KM and Noonan CW: Autoimmunity and asbestos exposure. Autoimmune Dis. 2014:7820452014.PubMed/NCBI
31	Zebedeo CN, Davis C, Peña C, Ng KW and Pfau JC: Erionite induces production of autoantibodies and IL-17 in C57BL/6 mice. Toxicol Appl Pharmacol. 275:257–264. 2014. View Article : Google Scholar : PubMed/NCBI
32	Maeda M, Yamamoto S, Chen Y, Kumagai-Takei N, Hayashi H, Matsuzaki H, Lee S, Hatayama T, Miyahara N, Katoh M, et al: Resistance to asbestos-induced apoptosis with continuous exposure to crocidolite on a human T cell. Sci Total Environ. 429:174–182. 2012. View Article : Google Scholar : PubMed/NCBI
33	Huang SX, Jaurand MC, Kamp DW, Whysner J and Hei TK: Role of mutagenicity in asbestos fiber-induced carcinogenicity and other diseases. J Toxicol Environ Health B Crit Rev. 14:179–245. 2011. View Article : Google Scholar : PubMed/NCBI
34	Mossman BT and Craighead JE: Mechanisms of asbestos carcinogenesis. Environ Res. 25:269–280. 1981. View Article : Google Scholar : PubMed/NCBI
35	Moyer VD, Cistulli CA, Vaslet CA and Kane AB: Oxygen radicals and asbestos carcinogenesis. Environ Health Perspect. 102(Suppl 10): 131–136. 1994. View Article : Google Scholar : PubMed/NCBI
36	Toyokuni S: Iron overload as a major targetable pathogenesis of asbestos-induced mesothelial carcinogenesis. Redox Rep. 19:1–7. 2014. View Article : Google Scholar
37	LaFave LM, Béguelin W, Koche R, Teater M, Spitzer B, Chramiec A, Papalexi E, Keller MD, Hricik T, Konstantinoff K, et al: Loss of BAP1 function leads to EZH2-dependent transformation. Nat Med. 21:1344–1349. 2015. View Article : Google Scholar : PubMed/NCBI
38	Sekido Y: Molecular pathogenesis of malignant mesothelioma. Carcinogenesis. 34:1413–1419. 2013. View Article : Google Scholar : PubMed/NCBI
39	Singhi AD, Krasinskas AM, Choudry HA, Bartlett DL, Pingpank JF, Zeh HJ, Luvison A, Fuhrer K, Bahary N, Seethala RR, et al: The prognostic significance of BAP1, NF2, and CDKN2A in malignant peritoneal mesothelioma. Mod Pathol. 29:14–24. 2016. View Article : Google Scholar
40	Maeda M, Yamamoto S, Hatayama T, Matsuzaki H, Lee S, Kumagai-Takei N, Yoshitome K, Nishimura Y, Kimura Y and Otsuki T: T cell alteration caused by exposure to asbestos. Biological Effects of Fibrous and Particulate Substances, (Series Title: Current Topics in Environmental Health and Preventive Medicine). Otsuki T, Holian A and Yoshioka Y: Springer; Tokyo: pp. 195–210. 2015
41	O'Connor RA, Taams LS and Anderton SM: Translational mini-review series on Th17 cells: CD4 T helper cells: functional plasticity and differential sensitivity to regulatory T cell-mediated regulation. Clin Exp Immunol. 159:137–147. 2010. View Article : Google Scholar :
42	Olson NC, Sallam R, Doyle MF, Tracy RP and Huber SA: T helper cell polarization in healthy people: Implications for cardiovascular disease. J Cardiovasc Transl Res. 6:772–786. 2013. View Article : Google Scholar : PubMed/NCBI
43	Ying C, Maeda M, Nishimura Y, Kumagai-Takei N, Hayashi H, Matsuzaki H, Lee S, Yoshitome K, Yamamoto S, Hatayama T, et al: Enhancement of regulatory T cell-like suppressive function in MT-2 by long-term and low-dose exposure to asbestos. Toxicology. 338:86–94. 2015. View Article : Google Scholar : PubMed/NCBI
44	Lee S, Matsuzaki H, Maeda M, Yamamoto S, Kumagai-Takei N, Hatayama T, Ikeda M, Yoshitome K, Nishimura Y and Otsuki T: Accelerated cell cycle progression of human regulatory T cell-like cell line caused by continuous exposure to asbestos fibers. Int J Oncol. 50:66–74. 2017.
45	Tsujioka T, Miura Y, Otsuki T, Nishimura Y, Hyodoh F, Wada H and Sugihara T: The mechanisms of vitamin K2-induced apoptosis of myeloma cells. Haematologica. 91:613–619. 2006.PubMed/NCBI
46	Otsuki T, Yata K, Takata-Tomokuni A, Hyodoh F, Miura Y, Sakaguchi H, Hatayama T, Hatada S, Tsujioka T, Sato Y, et al: Expression of protein gene product 9.5 (PGP9.5)/ubiquitin-C-terminal hydrolase 1 (UCHL-1) in human myeloma cells. Br J Haematol. 127:292–298. 2004. View Article : Google Scholar : PubMed/NCBI
47	Otsuki T, Yamada O, Kurebayashi J, Moriya T, Sakaguchi H, Kunisue H, Yata K, Uno M, Yawata Y and Ueki A: Estrogen receptors in human myeloma cells. Cancer Res. 60:1434–1441. 2000.PubMed/NCBI