Chitinase 3-like 1 regulates cellular and tissue responses via IL-13 receptor α2

Cell Reports

Volumn 4, Issue 4, 2013, Pages 830-841

  He, ChuanHua ^a   Lee, ChunGeun ^a   DelaCruz, Charles S ^a   Lee, Chang Min ^a   Zhou, Yang ^a   Ahangari, Farida ^a   Ma, Bing ^a   Herzog, EricaL ^a   Rosenberg, Stephen A ^a   Li, Yue ^b   Nour, Adel M ^b   Parikh, Chirag R ^a   Schmidt, Insa ^a,c   Modis, Yorgo ^b   Cantley, Lloyd ^a   Elias, Jack A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CHITINASE; CHITINASE 3 LIKE 1; INFLAMMASOME; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA2; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BACTERIAL INFECTION; CONTROLLED STUDY; ENZYME ACTIVATION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LUNG METASTASIS; MELANOCYTE; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE;

ANIMALS; APOPTOSIS; GLYCOPROTEINS; HUMANS; INFLAMMASOMES; INTERLEUKIN-13; INTERLEUKIN-13 RECEPTOR ALPHA2 SUBUNIT; LUNG NEOPLASMS; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MELANOMA; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PROTEIN BINDING; TRANSFORMING GROWTH FACTOR BETA; WNT SIGNALING PATHWAY;

BACTERIA (MICROORGANISMS);

EID: 84883265444     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.07.032     Document Type: Article

References (42)

1. Aerts J.M., van Breemen M.J., Bussink A.P., Ghauharali K., Sprenger R., Boot R.G., Groener J.E., Hollak C.E., Maas M., Smit S., et al. Biomarkers for lysosomal storage disorders: identification and application asexemplified by chitotriosidase in Gaucher disease. Acta Paediatr. Suppl. 2008, 97:7-14.
2. Allahverdian S., Harada N., Singhera G.K., Knight D.A., Dorscheid D.R. Secretion of IL-13 by airway epithelial cells enhances epithelial repair via HB-EGF. Am. J. Respir. Cell Mol. Biol. 2008, 38:153-160.
3. Areshkov P.O., Avdieiev S.S., Balynska O.V., Leroith D., Kavsan V.M. Two closely related human members of chitinase-like family, CHI3L1 and CHI3L2, activate ERK1/2 in 293 and U373 cells but have the different influence on cell proliferation. Int. J. Biol. Sci. 2012, 8:39-48.
4. Chen W., Tabata Y., Gibson A.M., Daines M.O., Warrier M.R., Wills-Karp M., Hershey G.K. Matrix metalloproteinase 8 contributes to solubilization of IL-13 receptor alpha2 invivo. J.Allergy Clin. Immunol. 2008, 122:625-632.
5. Chen W., Sivaprasad U., Tabata Y., Gibson A.M., Stier M.T., Finkelman F.D., Hershey G.K. IL-13R alpha 2 membrane and soluble isoforms differ in humans and mice. J.Immunol. 2009, 183:7870-7876.
6. Chen C.-C., Llado V., Eurich K., Tran H.T., Mizoguchi E. Carbohydrate-binding motif in chitinase 3-like 1 (CHI3L1/YKL-40) specifically activates Akt signaling pathway in colonic epithelial cells. Clin. Immunol. 2011, 140:268-275.
7. Chen C.C., Pekow J., Llado V., Kanneganti M., Lau C.W., Mizoguchi A., Mino-Kenudson M., Bissonnette M., Mizoguchi E. Chitinase 3-like-1 expression in colonic epithelial cells as a potentially novel marker for colitis-associated neoplasia. Am. J. Pathol. 2011, 179:1494-1503.
8. Chiaramonte M.G., Mentink-Kane M., Jacobson B.A., Cheever A.W., Whitters M.J., Goad M.E., Wong A., Collins M., Donaldson D.D., Grusby M.J., Wynn T.A. Regulation and function of the interleukin 13 receptor alpha 2 during a T helper cell type 2-dominant immune response. J.Exp. Med. 2003, 197:687-701.
9. Cho S.J., Kang M.J., Homer R.J., Kang H.R., Zhang X., Lee P.J., Elias J.A., Lee C.G. Role of early growth response-1 (Egr-1) in interleukin-13-induced inflammation and remodeling. J.Biol. Chem. 2006, 281:8161-8168.
10. Coffman F.D. Chitinase 3-Like-1 (CHI3L1): a putative disease marker at the interface of proteomics and glycomics. Crit. Rev. Clin. Lab. Sci. 2008, 45:531-562.
11. Daines M.O., Tabata Y., Walker B.A., Chen W., Warrier M.R., Basu S., Hershey G.K. Level of expression of IL-13R alpha 2 impacts receptor distribution and IL-13 signaling. J.Immunol. 2006, 176:7495-7501.
12. Dela Cruz C.S., Liu W., He C.H., Jacoby A., Gornitzky A., Ma B., Flavell R., Lee C.G., Elias J.A. Chitinase 3-like-1 promotes Streptococcus pneumoniae killing and augments host tolerance to lung antibacterial responses. Cell Host Microbe 2012, 12:34-46.
13. Eurich K., Segawa M., Toei-Shimizu S., Mizoguchi E. Potential role of chitinase 3-like-1 in inflammation-associated carcinogenic changes of epithelial cells. World J. Gastroenterol. 2009, 15:5249-5259.
14. Faibish M., Francescone R., Bentley B., Yan W., Shao R. AYKL-40-neutralizing antibody blocks tumor angiogenesis and progression: a potential therapeutic agent in cancers. Mol. Cancer Ther. 2011, 10:742-751.
15. 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 TGF-beta1 production and fibrosis. Nat. Med. 2006, 12:99-106.
16. Fichtner-Feigl S., Fuss I.J., Young C.A., Watanabe T., Geissler E.K., Schlitt H.J., Kitani A., Strober W. Induction of IL-13 triggers TGF-beta1-dependent tissue fibrosis in chronic 2,4,6-trinitrobenzene sulfonic acid colitis. J.Immunol. 2007, 178:5859-5870.
17. Fichtner-Feigl S., Strober W., Geissler E.K., Schlitt H.-J. Cytokines mediating the induction of chronic colitis and colitis-associated fibrosis. Mucosal Immunol. 2008, 1(Suppl 1):S24-S27.
18. Fichtner-Feigl S., Terabe M., Kitani A., Young C.A., Fuss I., Geissler E.K., Schlitt H.-J., Berzofsky J.A., Strober W. Restoration of tumor immunosurveillance via targeting of interleukin-13 receptor-alpha 2. Cancer Res. 2008, 68:3467-3475.
19. Funkhouser J.D., Aronson N.N. Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. BMC Evol. Biol. 2007, 7:96.
20. Goel S., Hidalgo M., Perez-Soler R. EGFR inhibitor-mediated apoptosis in solid tumors. J.Exp. Ther. Oncol. 2007, 6:305-320.
21. Kawada M., Seno H., Kanda K., Nakanishi Y., Akitake R., Komekado H., Kawada K., Sakai Y., Mizoguchi E., Chiba T. Chitinase 3-like 1 promotes macrophage recruitment and angiogenesis in colorectal cancer. Oncogene 2012, 31:3111-3123.
22. Kim M.N., Lee K.E., Hong J.Y., Heo W.I., Kim K.W., Kim K.E., Sohn M.H. Involvement of the MAPK and PI3K pathways in chitinase 3-like 1-regulated hyperoxia-induced airway epithelial cell death. Biochem. Biophys. Res. Commun. 2012, 421:790-796.
23. Kioi M., Seetharam S., Puri R.K. N-linked glycosylation of IL-13R alpha2 is essential for optimal IL-13 inhibitory activity. FASEB J. 2006, 20:2378-2380.
24. Konstantinidis A.K., Puddicombe S.M., Mochizuki A., Sheth P.D., Yang I.A., Yoshisue H., Wilson S.J., Davies D.E., Holgate S.T., Holloway J.W. Cellular localization of interleukin 13 receptor alpha2 in human primary bronchial epithelial cells and fibroblasts. J.Investig. Allergol. Clin. Immunol. 2008, 18:174-180.
25. Lee P.J., Zhang X., Shan P., Ma B., Lee C.G., Homer R.J., Zhu Z., Rincon M., Mossman B.T., Elias J.A. ERK1/2 mitogen-activated protein kinase selectively mediates IL-13-induced lung inflammation and remodeling invivo. J.Clin. Invest. 2006, 116:163-173.
26. Lee C.G., Hartl D., Lee G.R., Koller B., Matsuura H., Da Silva C.A., Sohn M.H., Cohn L., Homer R.J., Kozhich A.A., et al. Role of breast regression protein 39 (BRP-39)/chitinase 3-like-1 in Th2 and IL-13-induced tissue responses and apoptosis. J.Exp. Med. 2009, 206:1149-1166.
27. Lee C.G., Elias J.A. Role of breast regression protein-39/YKL-40 in asthma and allergic responses. Allergy Asthma Immunol. Res. 2010, 2:20-27.
28. Lee C.G., Da Silva C.A., Dela Cruz C.S., Ahangari F., Ma B., Kang M.J., He C.H., Takyar S., Elias J.A. Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu. Rev. Physiol. 2011, 73:479-501.
29. Lupardus P.J., Birnbaum M.E., Garcia K.C. Molecular basis forshared cytokine recognition revealed in the structure of an unusually high affinity complex between IL-13 and IL-13Ralpha2. Structure 2010, 18:332-342.
30. Moriya C., Jinnin M., Yamane K., Maruo K., Muchemwa F.C., Igata T., Makino T., Fukushima S., Ihn H. Expression of matrix metalloproteinase-13 is controlled by IL-13 via PI3K/Akt3 and PKC-δ in normal human dermal fibroblasts. J.Invest. Dermatol. 2011, 131:655-661.
31. Ooi A.T., Ram S., Kuo A., Gilbert J.L., Yan W., Pellegrini M., Nickerson D.W., Chatila T.A., Gomperts B.N. Identification of an interleukin 13-induced epigenetic signature in allergic airway inflammation. Am. J. Transl. Res. 2012, 4:219-228.
32. Rabinovich G.A., Croci D.O. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity 2012, 36:322-335.
33. Schmidt H., Johansen J.S., Gehl J., Geertsen P.F., Fode K., von der Maase H. Elevated serum level of YKL-40 is an independent prognostic factor for poor survival in patients with metastatic melanoma. Cancer 2006, 106:1130-1139.
34. Shao R., Hamel K., Petersen L., Cao Q.J., Arenas R.B., Bigelow C., Bentley B., Yan W. YKL-40, a secreted glycoprotein, promotes tumor angiogenesis. Oncogene 2009, 28:4456-4468.
35. Sohn M.H., Kang M.J., Matsuura H., Bhandari V., Chen N.Y., Lee C.G., Elias J.A. The chitinase-like proteins breast regression protein-39 andYKL-40 regulate hyperoxia-induced acute lung injury. Am. J. Respir. Crit. Care Med. 2010, 182:918-928.
36. Strober W., Kitani A., Fichtner-Feigl S., Fuss I.J. The signaling function of the IL-13Ralpha2 receptor in the development of gastrointestinal fibrosis and cancer surveillance. Curr. Mol. Med. 2009, 9:740-750.
37. Sulak O., Lameignere E., Wimmerova M., Imberty A. Specificity and affinity studies in lectin/carbohydrate interactions. Carbohydr. Chem. 2009, 35:356-371.
38. Wang M.L., Keilbaugh S.A., Cash-Mason T., He X.C., Li L., Wu G.D. Immune-mediated signaling in intestinal goblet cells via PI3-kinase- and AKT-dependent pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 295:G1122-G1130.
39. Wood N., Whitters M.J., Jacobson B.A., Witek J., Sypek J.P., Kasaian M.T., Eppihimer M.J., Unger M., Tanaka T., Goldman S.J., et al. Enhanced interleukin (IL)-13 responses in mice lacking IL-13 receptor alpha 2. J.Exp. Med. 2003, 197:703-709.
40. Yang J.S., Allahverdian S., Singhera G.K., MacRedmond R.E., Dorscheid D.R. IL-13Rα2/AP-1 complex signalling mediates airway epithelial repair without effects on remodeling pathways. Allergy Asthma Clin. Immunol. 2010, 6(Suppl 3):P27.
41. Yang J.S.Y., Wadsworth S.J., Singhera G.K., Dorscheid D. The regulation of IL-13ralpha1 and IL-13ralpha2 expression and distribution in airway epithelial repair. Am. J. Respir. Crit. Care Med. 2011, 183:A2812.
42. Zhu Z., Homer R.J., Wang Z., Chen Q., Geba G.P., Wang J., Zhang Y., Elias J.A. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J.Clin. Invest. 1999, 103:779-788.