A protective role for IL-13 receptor α 1 in bleomycin-induced pulmonary injury and repair

Mucosal Immunology

Volumn 9, Issue 1, 2016, Pages 240-253

  Karo Atar, D ^a   Bordowitz, A ^a   Wand, O ^a   Pasmanik Chor, M ^a   Fernandez, I E ^b   Itan, M ^a   Frenkel, R ^c   Herbert, D R ^d   Finkelman, F D ^e,f,g   Eickelberg, O ^b   Munitz, A ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF CINCINNATI   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA1; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; ISOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS MUCOSA; CONTROLLED STUDY; FEMALE; FIBROSING ALVEOLITIS; FLOW CYTOMETRY; GENE AMPLIFICATION; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; HOMEOSTASIS; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; LUNG INJURY; MALE; MOLECULAR DYNAMICS; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE; ADULT; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; CHEMICALLY INDUCED; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; MIDDLE AGED; PATHOLOGY;

ADULT; ANIMALS; BLEOMYCIN; CASE-CONTROL STUDIES; FEMALE; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; INTERLEUKIN-13; INTERLEUKIN-13 RECEPTOR ALPHA1 SUBUNIT; INTERLEUKIN-17; INTERLEUKIN-4; LUNG; LUNG INJURY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; PROTEIN ISOFORMS; RECEPTORS, INTERLEUKIN-4; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84953258250     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2015.56     Document Type: Article

References (52)

1. Fernandez Perez, E.R., et al. Incidence, prevalence, and clinical course of idiopathic pulmonary fibrosis: a population-based study. Chest 137, 129-137 (2010
2. Wynn, T.A. IL-13 effector functions. Annu. Rev. Immunol. 21, 425-456 (2003
3. LaPorte S.L., et al. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 132, 259-272 (2008
4. Miloux B., et al. Cloning of the human IL-13R alpha1 chain and reconstitution with the IL4R alpha of a functional IL-4/IL-13 receptor complex. FEBS Lett. 401, 163-166 (1997
5. Hilton, D.J., Zhang, J.G., Metcalf, D., Alexander, W.S., Nicola, N.A., & Willson, T.A. Cloning and characterization of a binding subunit of the interleukin 13 receptor that is also a component of the interleukin 4 receptor. Proc. Nat Acad. Sci. USA 93, 497-501 (1996
6. Aman, M.J., Tayebi, N., Obiri, N.I., Puri, R.K., Modi, W.S., & Leonard, W.J. cDNA cloning and characterization of the human interleukin 13 receptor alpha chain. J. Biol. Chem. 271, 29265-29270 (1996
7. Zhang, J., et al. Identification, Purification and characteristation of a soluble interleukin (IL)-13-binding protein. Evidence that it is distinct from the cloned IL-13 receptor and IL-4 receptor alpha chains. J. Biol. Chem. 272, 9474-9480 (1997
8. Munitz, A., Brandt, E.B., Mingler, M., Finkelman, F.D., & Rothenberg, M.E. Distinct roles for IL-13 and IL-4 via IL-13 receptor alpha1 and the type II IL-4 receptor in asthma pathogenesis. Proc. Natl Acad. Sci. USA 105, 7240-7245 (2008
9. Rothenberg, M.E., Wen, T., Shik, D., Cole, E.T., Mingler, M.M., & Munitz, A. IL-13 receptor alpha1 differentially regulates aeroallergen-induced lung responses. J. Immunol. 187, 4873-4880 (2011
10. Fichtner-Feigl, S., Strober, W., Kawakami, K., Puri, R.K., & Kitani, A. IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGFbeta1 production and fibrosis. Nat. Med. 12, 99-106 (2006
11. Junttila, I.S., et al. Tuning sensitivity to IL-4 and IL-13: differential expression of IL-4Ralpha, IL-13Ralpha1, and gammac regulates relative cytokine sensitivity. J. Exp. Med. 205, 2595-2608 (2008
12. Rock, J.R., & Hogan, B.L. Epithelial progenitor cells in lung development, maintenance, repair, and disease. Annu. Rev. Cell Dev. Biol. 27, 493-512 (2011
13. Chapman, H.A. Disorders of lung matrix remodeling. J. Clin. Invest. 113, 148-157 (2004
14. Herbert D.R., et al. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20, 623-635 (2004
15. Wynn, T.A., & Ramalingam, T.R. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat. Med. 18, 1028-1040 (2012
16. Pesce J.T., et al. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 5, e1000371 (2009
17. Nair M.G., et al Alternatively activated macrophage-derived RELM-{alpha} is a negative regulator of type 2 inflammation in the lung. J. Exp. Med. 206 937-952 2009
18. Konigshoff M., et al. WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J. Clin. Invest. 119, 772-787 (2009
19. Borensztajn, K., Crestani, B., & Kolb, M. Idiopathic pulmonary fibrosis: from epithelial injury to biomarkers-insights from the bench side. Respiration 86, 441-452 (2013
20. Sisson T.H., et al. Targeted injury of type II alveolar epithelial cells induces pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 181, 254-263 (2010
21. Sabo-Attwood T., et al. Gene expression profiles reveal increased mClca3 (Gob5) expression and mucin production in a murine model of asbestos-induced fibrogenesis. Am. J. Pathol. 167, 1243-1256 (2005
22. Li S., et al. Foxp1/4 control epithelial cell fate during lung development and regeneration through regulation of anterior gradient 2. Development 139, 2500-2509 (2012
23. Greeley, M.A., Van Winkle, L.S., Edwards, P.C., & Plopper, C.G. Airway trefoil factor expression during naphthalene injury and repair. Toxicol. Sci. 113, 453-467 (2010
24. Chen F., et al. An essential role for TH2-Type responses in limiting acute tissue damage during experimental helminth infection. Nat.Med. 18, 260-266 (2012
25. Wilson M.S., et al. Bleomycin and IL-1beta-mediated pulmonary fibrosis is IL-17A dependent. J. Exp. Med. 207, 535-552 (2010
26. Adamali, H.I., & Maher, T.M. Current and novel drug therapies for idiopathic pulmonary fibrosis. Drug Des. Dev. Ther. 6, 261-272 (2012
27. Wechsler, M.E. Inhibiting interleukin-4 and interleukin-13 in difficultto-control asthma. N. Engl. J. Med. 368, 2511-2513 (2013
28. Blackwell T.S., et al. Future directions in idiopathic pulmonary fibrosis research. An NHLBI workshop report. Am. J. Respir. Crit. Care Med. 189, 214-222 (2014
29. Wills-Karp M., et al. Interleukin-13: central mediator of allergic asthma. Science 282, 2258-2261 (1998
30. Grunig G., et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282, 2261-2263 (1998
31. Ramalingam T.R., et al. Unique functions of the type II interleukin 4 receptor identified in mice lacking the interleukin 13 receptor alpha1 chain. Nat. Immunol. 9, 25-33 (2008
32. Bhandari, V., Choo-Wing, R., Homer, R.J., & Elias, J.A. Increased hyperoxia-induced mortality and acute lung injury in IL-13 null mice. J. Immunol. 178, 4993-5000 (2007
33. Potter C.S., et al. Chronic proliferative dermatitis in sharpin null mice: development of an autoinflammatory disease in the absence of B and T lymphocytes and IL4/IL13 signaling. PLoS One 9, e85666 (2014
34. Karo-Atar, D., Moshkovits, I., Eickelberg, O., Konigshoff, M., & Munitz, A. Paired immunoglobulin-like receptor-B inhibits pulmonary fibrosis by suppressing profibrogenic properties of alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 48, 456-464 (2013
35. Brondijk T.H., et al. Crystal structure and collagen-binding site of immune inhibitory receptor LAIR-1: unexpected implications for collagen binding by platelet receptor GPVI. Blood 115, 1364-1373 (2010
36. Munitz, A. Inhibitory receptors on myeloid cells: new targets for therapy? Pharmacol. Ther. 125, 128-137 (2010
37. Park S.W., et al. Interleukin-13 and its receptors in idiopathic interstitial pneumonia: clinical implications for lung function. J. Korean Med. Sci. 24, 614-620 (2009
38. Murray, L.A., et al. Hyper-responsiveness of IPF/UIP fibroblasts: interplay between TGFbeta1, IL-13 and CCL2. Int. J. Biochem. Cell Biol. 40, 2174-2182 (2008
39. Murray L.A., et al. Targeting IL-13with tralokinumab attenuates lung fibrosis and epithelial damage in a humanized SCID IPF model. Am. J. Respir. Cell Mol. Biol. 50, 985-994 (2013
40. Zheng T., et al. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase-And cathepsin-dependent emphysema. J. Clin. Invest. 106, 1081-1093 (2000
41. Fichtner-Feigl, S., Young, C.A., Kitani, A., Geissler, E.K., Schlitt, H.J., & Strober, W. IL-13 signaling via IL-13R alpha2 induces major downstream fibrogenic factors mediating fibrosis in chronic TNBS colitis. Gastroenterology 135, 2003-2013. 2013 e2001-2007 (2008
42. Chandriani S., et al. Endogenously expressed IL-13R alpha 2 attenuates IL-13-mediated responses but does not activate signaling in human lung fibroblasts. J. Immunol. 193, 111-119 (2014
43. Zheng T., et al. IL-13 receptor alpha 2 selectively inhibits IL-13-induced responses in the murine lung. J. Immunol. 180, 522-529 (2008
44. Peljto A.L., et al. Association between theMUC5Bpromoter polymorphism and survival in patients with idiopathic pulmonary fibrosis. JAMA 309, 2232-2239 (2013
45. Park S.W., et al. The protein disulfide isomerase AGR2 is essential for production of intestinal mucus. Proc. Natl Acad. Sci. USA 106, 6950-6955 (2009
46. Young, F.D., Newbigging, S., Choi, C., Keet, M., Kent, G., & Rozmahel, R.F. Amelioration of cystic fibrosis intestinal mucous disease in mice by restoration of mCLCA3. Gastroenterology 133, 1928-1937 (2007
47. Usuki, J., & Fukuda, Y. Evolution of 3 patterns of intraalveolar fibrosis produced by bleomycin in rats. Pathol. Int. 45, 552-564 (1995
48. Izbicki, G., Segel, M.J., Christensen, T.G., Conner, M.W., & Breuer, R. Time course of bleomycin-induced lung fibrosis. Int. J. Exp. Pathol. 83, 111-119 (2002
49. Chua, F., Gauldie, J., & Laurent, G.J. Pulmonary fibrosis-searching for model answers. Am. J. Resp. Cell Mol. 33, 9-13 (2005
50. Moeller, A., Ask, K., Warburton, D., Gauldie, J., & Kolb, M. The bleomycin animal model: A useful tool to investigate treatment options for idiopathic pulmonary fibrosis? Int. J. Biochem. Cell Biol. 40, 362-382 (2008
51. Baruch-Morgenstern, N.B., Shik, D., Moshkovits, I., Itan, M., Karo-Atar, D., & Bouffi, C., et al. Paired immunoglobulin-like receptor A is an intrinsic, self-limiting suppressor of IL-5-induced eosinophil development. Nat. Immunol. 15, 36-44 (2013
52. Wynn T.A. Barron, L., Thompson, R.W., Madala, S.K., Wilson, M.S., & Cheever, A.W., et al. Quantitative assessment of macrophage functions in repair and fibrosis. Curr. Protoc. Immunol. Chapter 14: Unit14 22