IL-13 regulates Th17 secretion of IL-17A in an IL-10-dependent manner

Journal of Immunology

Volumn 188, Issue 3, 2012, Pages 1027-1035

  Newcomb, Dawn C ^a   Boswell, Madison G ^a   Huckabee, Matthew M ^a   Goleniewska, Kasia ^a   Dulek, Daniel E ^a   Reiss, Sara ^a   Lukacs, Nicholas W ^b   Kolls, Jay K ^c   Peebles, R Stokes ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 21; STAT1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL POLARITY; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; LUNG INFILTRATE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; TH17 CELL; VIRUS STRAIN;

EID: 84856560323     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102216     Document Type: Article

References (48)

1. Ruth, L. 2007. A breath of hope. Researchers are combining their efforts to study the genetic and environmental factors in asthma. EMBO Rep. 8: 319-321. (Pubitemid 46511029)
2. Hershey, G. K. 2003. IL-13 receptors and signaling pathways: an evolving web. J. Allergy Clin. Immunol. 111: 677-690, quiz 691.
3. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science 282: 2258-2261. (Pubitemid 29004074)
4. Saha, S. K., M. A. Berry, D. Parker, S. Siddiqui, A. Morgan, R. May, P. Monk, P. Bradding, A. J. Wardlaw, I. D. Pavord, and C. E. Brightling. 2008. Increased sputum and bronchial biopsy IL-13 expression in severe asthma. J. Allergy Clin. Immunol. 121: 685-691. (Pubitemid 351323866)
5. Bree, A., F. J. Schlerman, M. Wadanoli, L. Tchistiakova, K. Marquette, X. Y. Tan, B. A. Jacobson, A. Widom, T. A. Cook, N. Wood, et al. 2007. IL-13 blockade reduces lung inflammation after Ascaris suum challenge in cynomolgus monkeys. J. Allergy Clin. Immunol. 119: 1251-1257. (Pubitemid 46654187)
6. Corren, J., R. F. Lemanske, N. A. Hanania, P. E. Korenblat, M. V. Parsey, J. R. Arron, J. M. Harris, H. Scheerens, L. C. Wu, Z. Su, et al. 2011. Lebrikizumab treatment in adults with asthma. N. Engl. J. Med. 365: 1088-1098.
7. Gauvreau, G. M., L. P. Boulet, D. W. Cockcroft, J. M. Fitzgerald, C. Carlsten, B. E. Davis, F. Deschesnes, M. Duong, B. L. Durn, K. J. Howie, et al. 2011. Effects of interleukin-13 blockade on allergen-induced airway responses in mild atopic asthma. Am. J. Respir. Crit. Care Med. 183: 1007-1014.
8. Nicholson, G. C., H. H. Kariyawasam, A. J. Tan, J. M. Hohlfeld, D. Quinn, C. Walker, D. Rodman, J. Westwick, S. Jurcevic, O. M. Kon, et al. 2011. The effects of an anti-IL-13 mAb on cytokine levels and nasal symptoms following nasal allergen challenge. J. Allergy Clin. Immunol. 128: 800-807, e9.
9. Singh, D., B. Kane, N. A. Molfino, R. Faggioni, L. Roskos, and A. Woodcock. 2010. A phase 1 study evaluating the pharmacokinetics, safety and tolerability of repeat dosing with a human IL-13 antibody (CAT-354) in subjects with asthma. BMC Pulm. Med. 10: 3.
10. Wenzel, S., D. Wilbraham, R. Fuller, E. B. Getz, and M. Longphre. 2007. Effect of an interleukin-4 variant on late phase asthmatic response to allergen challenge in asthmatic patients: results of two phase 2a studies. Lancet 370: 1422-1431. (Pubitemid 47576168)
11. Corren, J., W. Busse, E. O. Meltzer, L. Mansfield, G. Bensch, J. Fahrenholz, S. E. Wenzel, Y. Chon, M. Dunn, H. H. Weng, and S. L. Lin. 2010. A randomized, controlled, phase 2 study of AMG 317, an IL-4Ralpha antagonist, in patients with asthma. Am. J. Respir. Crit. Care Med. 181: 788-796.
12. Wenzel, S. E. 2006. Asthma: defining of the persistent adult phenotypes. Lancet 368: 804-813. (Pubitemid 44279058)
13. Newcomb, D. C., W. Zhou, M. L. Moore, K. Goleniewska, G. K. Hershey, J. K. Kolls, and R. S. Peebles, Jr. 2009. A functional IL-13 receptor is expressed on polarized murine CD4+ Th17 cells and IL-13 signaling attenuates Th17 cytokine production. J. Immunol. 182: 5317-5321.
14. Newcomb, D. C., M. G. Boswell, W. Zhou, M. M. Huckabee, K. Goleniewska, C. M. Sevin, G. K. Hershey, J. K. Kolls, and R. S. Peebles, Jr. 2011. Human TH17 cells express a functional IL-13 receptor and IL-13 attenuates IL-17A production. J. Allergy Clin. Immunol. 127: 1006-1013, e1-e4.
15. Wilson, M. S., T. R. Ramalingam, A. Rivollier, K. Shenderov, M. M. Mentink-Kane, S. K. Madala, A. W. Cheever, D. Artis, B. L. Kelsall, and T. A. Wynn. 2011. Colitis and intestinal inflammation in IL10-/- mice results from IL-13Rα2-mediated attenuation of IL-13 activity. Gastroenterology 140: 254-264.
16. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141. (Pubitemid 41541791)
17. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132. (Pubitemid 41541790)
18. Cosmi, L., L. Maggi, V. Santarlasci, M. Capone, E. Cardilicchia, F. Frosali, V. Querci, R. Angeli, A. Matucci, M. Fambrini, et al. 2010. Identification of a novel subset of human circulating memory CD4(+) T cells that produce both IL-17A and IL-4. J. Allergy Clin. Immunol. 125: 222-230, e1-e4.
19. Wang, Y. H., K. S. Voo, B. Liu, C. Y. Chen, B. Uygungil, W. Spoede, J. A. Bernstein, D. P. Huston, and Y. J. Liu. 2010. A novel subset of CD4(+) T(H) 2 memory/effector cells that produce inflammatory IL-17 cytokine and promote the exacerbation of chronic allergic asthma. J. Exp. Med. 207: 2479-2491.
20. Chakir, J., J. Shannon, S. Molet, M. Fukakusa, J. Elias, M. Laviolette, L. P. Boulet, and Q. Hamid. 2003. Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-beta, IL-11, IL-17, and type I and type III collagen expression. J. Allergy Clin. Immunol. 111: 1293-1298. (Pubitemid 36683685)
21. Molet, S., Q. Hamid, F. Davoine, E. Nutku, R. Taha, N. Pagé, R. Olivenstein, J. Elias, and J. Chakir. 2001. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J. Allergy Clin. Immunol. 108: 430-438. (Pubitemid 32881066)
22. 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. (Pubitemid 351471762)
23. Aujla, S. J., Y. R. Chan, M. Zheng, M. Fei, D. J. Askew, D. A. Pociask, T. A. Reinhart, F. McAllister, J. Edeal, K. Gaus, et al. 2008. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 14: 275-281. (Pubitemid 351347908)
24. Cowley, S. C., A. I. Meierovics, J. A. Frelinger, Y. Iwakura, and K. L. Elkins. 2010. Lung CD4-CD8- double-negative T cells are prominent producers of IL-17A and IFN-gamma during primary respiratory murine infection with Francisella tularensis live vaccine strain. J. Immunol. 184: 5791-5801.
25. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27: 485-517.
26. Wu, Q., R. J. Martin, J. G. Rino, R. Breed, R. M. Torres, and H. W. Chu. 2007. IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes Infect. 9: 78-86. (Pubitemid 46149421)
27. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.
28. 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. (Pubitemid 47300011)
29. 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. (Pubitemid 47300008)
30. Kleinschek, M. A., A. M. Owyang, B. Joyce-Shaikh, C. L. Langrish, Y. Chen, D. M. Gorman, W. M. Blumenschein, T. McClanahan, F. Brombacher, S. D. Hurst, et al. 2007. IL-25 regulates Th17 function in autoimmune inflammation. J. Exp. Med. 204: 161-170. (Pubitemid 46148766)
31. Yang, X. O., S. H. Chang, H. Park, R. Nurieva, B. Shah, L. Acero, Y. H. Wang, K. S. Schluns, R. R. Broaddus, Z. Zhu, and C. Dong. 2008. Regulation of inflammatory responses by IL-17F. J. Exp. Med. 205: 1063-1075. (Pubitemid 351679682)
32. Wright, J. F., Y. Guo, A. Quazi, D. P. Luxenberg, F. Bennett, J. F. Ross, Y. Qiu, M. J. Whitters, K. N. Tomkinson, K. Dunussi-Joannopoulos, et al. 2007. Identification of an interleukin 17F/17A heterodimer in activated human CD4+ T cells. J. Biol. Chem. 282: 13447-13455. (Pubitemid 47100510)
33. Korn, T., E. Bettelli, W. Gao, A. Awasthi, A. Jäger, T. B. Strom, M. Oukka, and V. K. Kuchroo. 2007. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448: 484-487. (Pubitemid 47123515)
34. McGeachy, M. J., K. S. Bak-Jensen, Y. Chen, C. M. Tato, W. Blumenschein, T. McClanahan, and D. J. Cua. 2007. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8: 1390-1397. (Pubitemid 350138974)
35. Hashimoto, K., J. E. Durbin, W. Zhou, R. D. Collins, S. B. Ho, J. K. Kolls, P. J. Dubin, J. R. Sheller, K. Goleniewska, J. F. O'Neal, et al. 2005. Respiratory syncytial virus infection in the absence of STAT 1 results in airway dysfunction, airway mucus, and augmented IL-17 levels. J. Allergy Clin. Immunol. 116: 550-557. (Pubitemid 41267127)
36. Durbin, J. E., T. R. Johnson, R. K. Durbin, S. E. Mertz, R. A. Morotti, R. S. Peebles, and B. S. Graham. 2002. The role of IFN in respiratory syncytial virus pathogenesis. J. Immunol. 168: 2944-2952.
37. McKenzie, G. J., C. L. Emson, S. E. Bell, S. Anderson, P. Fallon, G. Zurawski, R. Murray, R. Grencis, and A. N. McKenzie. 1998. Impaired development of Th2 cells in IL-13-deficient mice. Immunity 9: 423-432. (Pubitemid 28462763)
38. Graham, B. S., M. D. Perkins, P. F. Wright, and D. T. Karzon. 1988. Primary respiratory syncytial virus infection in mice. J. Med. Virol. 26: 153-162.
39. Steinhauser, M. L., C. M. Hogaboam, S. L. Kunkel, N.W. Lukacs, R. M. Strieter, and T. J. Standiford. 1999. IL-10 is a major mediator of sepsis-induced impairment in lung antibacterial host defense. J. Immunol. 162: 392-399. (Pubitemid 29018946)
40. Peebles, R. S., Jr., J. R. Sheller, R. D. Collins, A. K. Jarzecka, D. B. Mitchell, R. A. Parker, and B. S. Graham. 2001. Respiratory syncytial virus infection does not increase allergen-induced type 2 cytokine production, yet increases airway hyperresponsiveness in mice. J. Med. Virol. 63: 178-188.
41. Zhou, W., T. S. Blackwell, K. Goleniewska, J. F. O'Neal, G. A. Fitzgerald, M. Lucitt, R. M. Breyer, and R. S. Peebles, Jr. 2007. Prostaglandin I2 analogs inhibit Th1 and Th2 effector cytokine production by CD4 T cells. J. Leukoc. Biol. 81: 809-817. (Pubitemid 46393559)
42. Gu, Y., J. Yang, X. Ouyang, W. Liu, H. Li, J. Yang, J. Bromberg, S. H. Chen, L. Mayer, J. C. Unkeless, and H. Xiong. 2008. Interleukin 10 suppresses Th17 cytokines secreted by macrophages and T cells. Eur. J. Immunol. 38: 1807-1813.
43. O'Shea, J. J., and P. J. Murray. 2008. Cytokine signaling modules in inflammatory responses. Immunity 28: 477-487. (Pubitemid 351467044)
44. Laan, M., Z. H. Cui, H. Hoshino, J. Lötvall, M. Sjöstrand, D. C. Gruenert, B. E. Skoogh, and A. Lindén. 1999. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J. Immunol. 162: 2347-2352. (Pubitemid 29288861)
45. Arase, H., T. Saito, J. H. Phillips, and L. L. Lanier. 2001. Cutting edge: the mouse NK cell-associated antigen recognized by DX5 monoclonal antibody is CD49b (alpha 2 integrin, very late antigen-2). J. Immunol. 167: 1141-1144. (Pubitemid 32703106)
46. Riol-Blanco, L., V. Lazarevic, A. Awasthi, M. Mitsdoerffer, B. S. Wilson, A. Croxford, A. Waisman, V. K. Kuchroo, L. H. Glimcher, and M. Oukka. 2010. IL-23 receptor regulates unconventional IL-17-producing T cells that control bacterial infections. J. Immunol. 184: 1710-1720.
47. - and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34: 554-565.
48. Wenzel, S. E., and W. W. Busse; National Heart, Lung, and Blood Institute's Severe Asthma Research Program. 2007. Severe asthma: lessons from the Severe Asthma Research Program. J. Allergy Clin. Immunol. 119: 14-21, quiz 22-23.