ATP-induced inflammation drives tissue-resident Th17 cells in metabolically unhealthy obesity

Journal of Immunology

Volumn 196, Issue 8, 2016, Pages 3287-3296

  Pandolfi, Julieta B ^a   Ferraro, Ariel A ^a   Sananez, Inés ^a   Gancedo, Maria C ^a   Baz, Plácida ^a   Billordo, Luis A ^a   Fainboim, Leonardo ^a   Arruvito, Lourdes ^a  

^a HOSPITAL DE CLÍNICAS JOSÉ DE SAN MARTÍN   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD39 ANTIGEN; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 6; PURINERGIC P2X7 RECEPTOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; APYRASE; IL17A PROTEIN, HUMAN; IL1B PROTEIN, HUMAN; IL23R PROTEIN, HUMAN; IL6 PROTEIN, HUMAN; INTERLEUKIN RECEPTOR; LEUKOCYTE ANTIGEN; P2XR RECEPTOR, HUMAN; RORC PROTEIN, HUMAN;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL COMMUNICATION AND CELL CONTACT; CELL DEATH; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; INFLAMMATION; INTRAABDOMINAL FAT; MALE; MICROENVIRONMENT; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURINERGIC SIGNALING; TH17 CELL; APOPTOSIS; BIOSYNTHESIS; CYTOLOGY; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

ADENOSINE TRIPHOSPHATE; ADULT; ANTIGENS, CD; APOPTOSIS; APYRASE; CELLULAR MICROENVIRONMENT; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-17; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTRA-ABDOMINAL FAT; MALE; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; OBESITY; RECEPTORS, INTERLEUKIN; RECEPTORS, PURINERGIC P2X7; TH17 CELLS;

EID: 84974814547     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502506     Document Type: Article

References (78)

1. Gregor, M. F., and G. S. Hotamisligil. 2011. Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 29: 415-445.
2. Ng, M., T. Fleming, M. Robinson, B. Thomson, N. Graetz, C. Margono, E. C. Mullany, S. Biryukov, C. Abbafati, S. F. Abera, et al. 2014. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384: 766-781.
3. Hossain, P., B. Kawar, and M. El Nahas. 2007. Obesity and diabetes in the developing world-a growing challenge. N. Engl. J. Med. 356: 213-215.
4. Stefan, N., H. U. Häring, F. B. Hu, and M. B. Schulze. 2013. Metabolically healthy obesity: epidemiology, mechanisms, and clinical implications. Lancet Diabetes Endocrinol. 1: 152-162.
5. Kaminski, D. A., and T. D. Randall. 2010. Adaptive immunity and adipose tissue biology. Trends Immunol. 31: 384-390.
6. Kanneganti, T. D., and V. D. Dixit. 2012. Immunological complications of obesity. Nat. Immunol. 13: 707-712.
7. Kim, H. Y., H. J. Lee, Y. J. Chang, M. Pichavant, S. A. Shore, K. A. Fitzgerald, Y. Iwakura, E. Israel, K. Bolger, J. Faul, et al. 2014. Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesityassociated airway hyperreactivity. Nat. Med. 20: 54-61.
8. Mauer, J., B. Chaurasia, J. Goldau, M. C. Vogt, J. Ruud, K. D. Nguyen, S. Theurich, A. C. Hausen, J. Schmitz, H. S. Brönneke, et al. 2014. Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin. Nat. Immunol. 15: 423-430.
9. Stienstra, R., J. A. van Diepen, C. J. Tack, M. H. Zaki, F. L. van de Veerdonk, D. Perera, G. A. Neale, G. J. Hooiveld, A. Hijmans, I. Vroegrijk, et al. 2011. Inflammasome is a central player in the induction of obesity and insulin resistance. Proc. Natl. Acad. Sci. USA 108: 15324-15329.
10. Winer, D. A., S. Winer, L. Shen, P. P. Wadia, J. Yantha, G. Paltser, H. Tsui, P. Wu, M. G. Davidson, M. N. Alonso, et al. 2011. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 17: 610-617.
11. Nishimura, S., I. Manabe, M. Nagasaki, K. Eto, H. Yamashita, M. Ohsugi, M. Otsu, K. Hara, K. Ueki, S. Sugiura, et al. 2009. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 15: 914-920.
12. Feuerer, M., L. Herrero, D. Cipolletta, A. Naaz, J. Wong, A. Nayer, J. Lee, A. B. Goldfine, C. Benoist, S. Shoelson, and D. Mathis. 2009. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 15: 930-939.
13. Yang, H., Y. H. Youm, B. Vandanmagsar, A. Ravussin, J. M. Gimble, F. Greenway, J. M. Stephens, R. L. Mynatt, and V. D. Dixit. 2010. Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance. J. Immunol. 185: 1836-1845.
14. Burzyn, D., C. Benoist, and D. Mathis. 2013. Regulatory T cells in nonlymphoid tissues. Nat. Immunol. 14: 1007-1013.
15. Manel, N., D. Unutmaz, and D. R. Littman. 2008. The differentiation of human T(H)-17 cells requires transforming growth factor-βeta and induction of the nuclear receptor RORgammat. Nat. Immunol. 9: 641-649.
16. Ivanov, I. I., B. S. McKenzie, L. Zhou, C. E. Tadokoro, A. Lepelley, J. J. Lafaille, D. J. Cua, and D. R. Littman. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133.
17. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 cells. Annu. Rev. Immunol. 27: 485-517.
18. Valmori, D., C. Raffin, I. Raimbaud, and M. Ayyoub. 2010. Human RORgt+ TH17 cells preferentially differentiate from naive FOXP3+Treg in the presence of lineage-specific polarizing factors. Proc. Natl. Acad. Sci. USA 107: 19402-19407.
19. Hirahara, K., K. Ghoreschi, A. Laurence, X. P. Yang, Y. Kanno, and J. J. O'Shea. 2010. Signal transduction pathways and transcriptional regulation in Th17 cell differentiation. Cytokine Growth Factor Rev. 21: 425-434.
20. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1beta and 6 but not transforming growth factor-βeta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8: 942-949.
21. Zhou, L., I. I. Ivanov, R. Spolski, R. Min, K. Shenderov, T. Egawa, D. E. Levy, W. J. Leonard, and D. R. Littman. 2007. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8: 967-974.
22. Stritesky, G. L., N. Yeh, and M. H. Kaplan. 2008. IL-23 promotes maintenance but not commitment to the Th17 lineage. J. Immunol. 181: 5948-5955.
23. Sherlock, J. P., B. Joyce-Shaikh, S. P. Turner, C. C. Chao, M. Sathe, J. Grein, D. M. Gorman, E. P. Bowman, T. K. McClanahan, J. H. Yearley, et al. 2012. IL-23 induces spondyloarthropathy by acting on ROR-gt+ CD3+CD4-CD8-entheseal resident T cells. Nat. Med. 18: 1069-1076.
24. Lee, Y., A. Awasthi, N. Yosef, F. J. Quintana, S. Xiao, A. Peters, C. Wu, M. Kleinewietfeld, S. Kunder, D. A. Hafler, et al. 2012. Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 13: 991-999.
25. Milner, J. D., J. M. Brenchley, A. Laurence, A. F. Freeman, B. J. Hill, K. M. Elias, Y. Kanno, C. Spalding, H. Z. Elloumi, M. L. Paulson, et al. 2008. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452: 773-776.
26. Ouyang, W., J. K. Kolls, and Y. Zheng. 2008. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467.
27. Khader, S. A., S. L. Gaffen, and J. K. Kolls. 2009. Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol. 2: 403-411.
28. Hu, Y., F. Shen, N. K. Crellin, andW. Ouyang. 2011. The IL-17 pathway as a major therapeutic target in autoimmune diseases. Ann. N. Y. Acad. Sci. 1217: 60-76.
29. Jagannathan-Bogdan, M., M. E. McDonnell, H. Shin, Q. Rehman, H. Hasturk, C. M. Apovian, and B. S. Nikolajczyk. 2011. Elevated proinflammatory cytokine production by a skewed T cell compartment requires monocytes and promotes inflammation in type 2 diabetes. J. Immunol. 186: 1162-1172.
30. Fabbrini, E., M. Cella, S. A. McCartney, A. Fuchs, N. A. Abumrad, T. A. Pietka, Z. Chen, B. N. Finck, D. H. Han, F. Magkos, et al. 2013. Association between specific adipose tissue CD4+ T-cell populations and insulin resistance in obese individuals. Gastroenterology 145: 366-374.e361-e363.
31. Sumarac-Dumanovic, M., D. Stevanovic, A. Ljubic, J. Jorga, M. Simic, D. Stamenkovic-Pejkovic, V. Starcevic, V. Trajkovic, and D. Micic. 2009. Increased activity of interleukin-23/interleukin-17 proinflammatory axis in obese women. Int. J. Obes. 33: 151-156.
32. Endo, Y., H. K. Asou, N. Matsugae, K. Hirahara, K. Shinoda, D. J. Tumes, H. Tokuyama, K. Yokote, and T. Nakayama. 2015. Obesity drives Th17 cell differentiation by inducing the lipid metabolic kinase, ACC1. Cell Reports 12: 1042-1055.
33. Eltzschig, H. K., M. V. Sitkovsky, and S. C. Robson. 2012. Purinergic signaling during inflammation. N. Engl. J. Med. 367: 2322-2333.
34. Ferrari, D., C. Pizzirani, E. Adinolfi, R. M. Lemoli, A. Curti, M. Idzko, E. Panther, and F. Di Virgilio. 2006. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176: 3877-3883.
35. 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.
36. Killeen, M. E., L. Ferris, E. A. Kupetsky, L. Falo, Jr., and A. R. Mathers. 2013. Signaling through purinergic receptors for ATP induces human cutaneous innate and adaptive Th17 responses: implications in the pathogenesis of psoriasis. J. Immunol. 190: 4324-4336.
37. Reutershan, J., I. Vollmer, S. Stark, R. Wagner, K. C. Ngamsri, and H. K. Eltzschig. 2009. Adenosine and inflammation: CD39 and CD73 are critical mediators in LPS-induced PMN trafficking into the lungs. FASEB J. 23: 473-482.
38. Goepfert, C., M. Imai, S. Brouard, E. Csizmadia, E. Kaczmarek, and S. C. Robson. 2000. CD39 modulates endothelial cell activation and apoptosis. Mol. Med. 6: 591-603.
39. Kuhny, M., T. Hochdörfer, C. K. Ayata, M. Idzko, and M. Huber. 2014. CD39 is a negative regulator of P2X7-mediated inflammatory cell death in mast cells. Cell Commun. Signal. 12: 40.
40. Moncrieffe, H., K. Nistala, Y. Kamhieh, J. Evans, A. Eddaoudi, S. Eaton, and L. R. Wedderburn. 2010. High expression of the ectonucleotidase CD39 on T cells from the inflamed site identifies two distinct populations, one regulatory and one memory T cell population. J. Immunol. 185: 134-143.
41. Zhou, Q., J. Yan, P. Putheti, Y. Wu, X. Sun, V. Toxavidis, J. Tigges, N. Kassam, K. Enjyoji, S. C. Robson, et al. 2009. Isolated CD39 expression on CD4+ T cells denotes both regulatory and memory populations. Am. J. Transplant. 9: 2303-2311.
42. Bai, A., A. Moss, E. Kokkotou, A. Usheva, X. Sun, A. Cheifetz, Y. Zheng, M. S. Longhi, W. Gao, Y. Wu, and S. C. Robson. 2014. CD39 and CD161 modulate Th17 responses in Crohn's disease. J. Immunol. 193: 3366-3377.
43. Pandolfi, J., A. Ferraro, M. Lerner, J. R. Serrano, A. Dueck, L. Fainboim, and L. Arruvito. 2015. Purinergic signaling modulates human visceral adipose inflammatory responses: implications in metabolically unhealthy obesity. J. Leukoc. Biol. 97: 941-949.
44. Alberti, K. G., R. H. Eckel, S. M. Grundy, P. Z. Zimmet, J. I. Cleeman, K. A. Donato, J. C. Fruchart, W. P. James, C. M. Loria, and S. C. Smith, Jr., International Diabetes Federation Task Force on Epidemiology and Prevention, Hational Heart, Lung, and Blood Institute, American Heart Association, World Heart Federation, International Atherosclerosis Society, International Association for the Study of Obesity. 2009. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120: 1640-1645.
45. Grundy, S. M., J. I. Cleeman, S. R. Daniels, K. A. Donato, R. H. Eckel, B. A. Franklin, D. J. Gordon, R. M. Krauss, P. J. Savage, S. C. Smith, Jr., et al. 2006. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute scientific statement. Curr. Opin. Cardiol. 21: 1-6.
46. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
47. Sakaguchi, S. 2004. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22: 531-562.
48. Fain, J. N., and A. K. Madan. 2005. Regulation of monocyte chemoattractant protein 1 (MCP-1) release by explants of human visceral adipose tissue. Int. J. Obes. 29: 1299-1307.
49. Fain, J. N., A. K. Madan, M. L. Hiler, P. Cheema, and S. W. Bahouth. 2004. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145: 2273-2282.
50. Vatier, C., S. Kadiri, A. Muscat, C. Chapron, J. Capeau, and B. Antoine. 2012. Visceral and subcutaneous adipose tissue from lean women respond differently to lipopolysaccharide-induced alteration of inflammation and glyceroneogenesis. Nutr. Diabetes 2: e51.
51. Alvarez-Llamas, G., E. Szalowska, M. P. de Vries, D. Weening, K. Landman, A. Hoek, B. H. Wolffenbuttel, H. Roelofsen, and R. J. Vonk. 2007. Characterization of the human visceral adipose tissue secretome. Mol. Cell. Proteomics 6: 589-600.
52. Solinas, G., and M. Karin. 2010. JNK1 and IKKbeta: molecular links between obesity and metabolic dysfunction. FASEB J. 24: 2596-2611.
53. Weisberg, S. P., D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante, Jr. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112: 1796-1808.
54. Odegaard, J. I., R. R. Ricardo-Gonzalez, M. H. Goforth, C. R. Morel, V. Subramanian, L. Mukundan, A. Red Eagle, D. Vats, F. Brombacher, A. W. Ferrante, and A. Chawla. 2007. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447: 1116-1120.
55. Wentworth, J. M., G. Naselli, W. A. Brown, L. Doyle, B. Phipson, G. K. Smyth, M. Wabitsch, P. E. O'Brien, and L. C. Harrison. 2010. Pro-inflammatory CD11c+CD206+ adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes 59: 1648-1656.
56. Nijhuis, J., S. S. Rensen, Y. Slaats, F. M. van Dielen, W. A. Buurman, and J. W. Greve. 2009. Neutrophil activation in morbid obesity, chronic activation of acute inflammation. Obesity (Silver Spring) 17: 2014-2018.
57. Carlow, D. A., M. R. Gold, and H. J. Ziltener. 2009. Lymphocytes in the peritoneum home to the omentum and are activated by resident dendritic cells. J. Immunol. 183: 1155-1165.
58. Patsouris, D., P. P. Li, D. Thapar, J. Chapman, J. M. Olefsky, and J. G. Neels. 2008. Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab. 8: 301-309.
59. Bertola, A., T. Ciucci, D. Rousseau, V. Bourlier, C. Duffaut, S. Bonnafous, C. Blin-Wakkach, R. Anty, A. Iannelli, J. Gugenheim, et al. 2012. Identification of adipose tissue dendritic cells correlated with obesity-associated insulin-resistance and inducing Th17 responses in mice and patients. Diabetes 61: 2238-2247.
60. Altintas, M. M., A. Azad, B. Nayer, G. Contreras, J. Zaias, C. Faul, J. Reiser, and A. Nayer. 2011. Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice. J. Lipid Res. 52: 480-488.
61. Sathaliyawala, T., M. Kubota, N. Yudanin, D. Turner, P. Camp, J. J. Thome, K. L. Bickham, H. Lerner, M. Goldstein, M. Sykes, et al. 2013. Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity 38: 187-197.
62. Kullberg, M. C., D. Jankovic, C. G. Feng, S. Hue, P. L. Gorelick, B. S. McKenzie, D. J. Cua, F. Powrie, A. W. Cheever, K. J. Maloy, and A. Sher. 2006. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J. Exp. Med. 203: 2485-2494.
63. Huber, S., N. Gagliani, and R. A. Flavell. 2012. Life, death, and miracles: Th17 cells in the intestine. Eur. J. Immunol. 42: 2238-2245.
64. Kimura, A., and T. Kishimoto. 2010. IL-6: regulator of Treg/Th17 balance. Eur. J. Immunol. 40: 1830-1835.
65. 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.
66. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
67. Ahern, P. P., C. Schiering, S. Buonocore, M. J. McGeachy, D. J. Cua, K. J. Maloy, and F. Powrie. 2010. Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 33: 279-288.
68. Yen, D., J. Cheung, H. Scheerens, F. Poulet, T. McClanahan, B. McKenzie, M. A. Kleinschek, A. Owyang, J. Mattson, W. Blumenschein, et al. 2006. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 116: 1310-1316.
69. Vandanmagsar, B., Y. H. Youm, A. Ravussin, J. E. Galgani, K. Stadler, R. L. Mynatt, E. Ravussin, J. M. Stephens, and V. D. Dixit. 2011. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17: 179-188.
70. Priceman, S. J., M. Kujawski, S. Shen, G. A. Cherryholmes, H. Lee, C. Zhang, L. Kruper, J. Mortimer, R. Jove, A. D. Riggs, and H. Yu. 2013. Regulation of adipose tissue T cell subsets by Stat3 is crucial for diet-induced obesity and insulin resistance. Proc. Natl. Acad. Sci. USA 110: 13079-13084.
71. Lumeng, C. N., J. L. Bodzin, and A. R. Saltiel. 2007. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117: 175-184.
72. Suganami, T., J. Nishida, and Y. Ogawa. 2005. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler. Thromb. Vasc. Biol. 25: 2062-2068.
73. Neves, A. R., M. T. Castelo-Branco, V. R. Figliuolo, C. Bernardazzi, F. Buongusto, A. Yoshimoto, H. F. Nanini, C. M. Coutinho, A. J. Carneiro, R. Coutinho-Silva, and H. S. de Souza. 2014. Overexpression of ATP-activated P2X7 receptors in the intestinal mucosa is implicated in the pathogenesis of Crohn's disease. Inflamm. Bowel Dis. 20: 444-457.
74. Xavier, R. J., and D. K. Podolsky. 2007. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
75. Leonardi, C., R. Matheson, C. Zachariae, G. Cameron, L. Li, E. Edson-Heredia, D. Braun, and S. Banerjee. 2012. Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N. Engl. J. Med. 366: 1190-1199.
76. Coccia, M., O. J. Harrison, C. Schiering, M. J. Asquith, B. Becher, F. Powrie, and K. J. Maloy. 2012. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells. J. Exp. Med. 209: 1595-1609.
77. Nylander, A., and D. A. Hafler. 2012. Multiple sclerosis. J. Clin. Invest. 122: 1180-1188.
78. Łuczyński, W., K. Grubczak, M. Moniuszko, B. Głowińska-Olszewska, and A. Bossowski. 2015. Elevated levels of Th17 cells in children with central obesity. Scand. J. Clin. Lab. Invest. 75: 595-601.