Chitinase 3-like 1 Regulates Cellular and Tissue Responses via IL-13 Receptor α2

Abstract

Members of the 18 glycosyl hydrolase (GH 18) gene family have been conserved over species and time and are dysregulated in inflammatory, infectious, remodeling, and neoplastic disorders. This is particularly striking for the prototypic chitinase-like protein chitinase 3-like 1 (Chi3l1), which plays a critical role in antipathogen responses where it augments bacterial killing while stimulating disease tolerance by controlling cell death, inflammation, and remodeling. However, receptors that mediate the effects of GH 18 moieties have not been defined. Here, we demonstrate that Chi3l1 binds to interleukin-13 receptor α2 (IL-13Rα2) and that Chi3l1, IL-13Rα2, and IL-13 are in a multimeric complex. We also demonstrate that Chi3l1 activates macrophage mitogen-activated protein kinase, protein kinase B/AKT, and Wnt/β-catenin signaling and regulates oxidant injury, apoptosis, pyroptosis, inflammasome activation, antibacterial responses, melanoma metastasis, and TGF-β1 production via IL-13Rα2-dependent mechanisms. Thus, IL-13Rα2 is a GH 18 receptor that plays a critical role in Chi3l1 effector responses.

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References 42

1. 1.

   Aerts JM, van Breemen MJ, Bussink AP, Ghauharali K, Sprenger R, Boot RG, Groener JE, Hollak CE, Maas M, Smit S, et al. Biomarkers for lysosomal storage disorders: identification and application as exemplified by chitotriosidase in Gaucher disease. Acta Paediatr Suppl. 2008;97:7-14.

   Not in our library10.1111/j.1651-2227.2007.00641.x

2. 2.

   Allahverdian S, Harada N, Singhera GK, Knight DA, Dorscheid DR. Secretion of IL-13 by airway epithelial cells enhances epithelial repair via HB-EGF. Am J Respir Cell Mol Biol. 2008;38:153-160.

   Not in our library10.1165/rcmb.2007-0173oc

3. 3.

   Areshkov PO, Avdieiev SS, Balynska OV, Leroith D, Kavsan VM. 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.

   Not in our library10.7150/ijbs.8.39

4. 4.

   Chen W, Tabata Y, Gibson AM, Daines MO, Warrier MR, Wills-Karp M, Hershey GK. Matrix metalloproteinase 8 contributes to solubilization of IL-13 receptor alpha2 in vivo. J Allergy Clin Immunol. 2008;122:625-632.

   Not in our library10.1016/j.jaci.2008.06.022

5. 5.

   Chen W, Sivaprasad U, Tabata Y, Gibson AM, Stier MT, Finkelman FD, Hershey GK. IL-13R alpha 2 membrane and soluble isoforms differ in humans and mice. J Immunol. 2009;183:7870-7876.

   Not in our library10.4049/jimmunol.0901028

6. 6.

   Chen CC, Llado V, Eurich K, Tran HT, Mizoguchi E. Carbohydrate-binding motif in chitinase 3-like 1 (CHI3L1/YKL-40) specifically activates Akt signaling pathway in colonic epithelial cells. Clin Immunol. 2011a;140:268-275.

   Not in our library10.1016/j.clim.2011.04.007

7. 7.

   Chen CC, Pekow J, Llado V, Kanneganti M, Lau CW, 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. 2011b;179:1494-1503.

   Not in our library10.1016/j.ajpath.2011.05.038

8. 8.

   Chiaramonte MG, Mentink-Kane M, Jacobson BA, Cheever AW, Whitters MJ, Goad ME, Wong A, Collins M, Donaldson DD, Grusby MJ, Wynn TA. 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.

   Not in our library10.1084/jem.20020903

9. 9.

   Cho SJ, Kang MJ, Homer RJ, Kang HR, Zhang X, Lee PJ, Elias JA, Lee CG. Role of early growth response-1 (Egr-1) in interleukin-13-induced inflammation and remodeling. J Biol Chem. 2006;281:8161-8168.

   Not in our library10.1074/jbc.m506770200

10. 10.

    Coffman FD. 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.

    Not in our library10.1080/10408360802334743

11. 11.

    Daines MO, Tabata Y, Walker BA, Chen W, Warrier MR, Basu S, Hershey GK. Level of expression of IL-13R alpha 2 impacts receptor distribution and IL-13 signaling. J Immunol. 2006;176:7495-7501.

    Not in our library10.4049/jimmunol.176.12.7495

12. 12.

    Dela Cruz CS, Liu W, He CH, Jacoby A, Gornitzky A, Ma B, Flavell R, Lee CG, Elias JA. Chitinase 3-like-1 promotes Streptococcus pneumoniae killing and augments host tolerance to lung antibacterial responses. Cell Host Microbe. 2012;12:34-46.

    Not in our library10.1016/j.chom.2012.05.017

13. 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.

    Not in our library10.3748/wjg.15.5249

14. 14.

    Faibish M, Francescone R, Bentley B, Yan W, Shao R. A YKL-40-neutralizing antibody blocks tumor angiogenesis and progression: a potential therapeutic agent in cancers. Mol Cancer Ther. 2011;10:742-751.

    Not in our library10.1158/1535-7163.mct-10-0868

15. 15.

    Fichtner-Feigl S, Strober W, Kawakami K, Puri RK, 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.

    Not in our library10.1038/nm1332

16. 16.

    Fichtner-Feigl S, Fuss IJ, Young CA, Watanabe T, Geissler EK, Schlitt HJ, 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.

    Not in our library10.4049/jimmunol.178.9.5859

17. 17.

    Fichtner-Feigl S, Strober W, Geissler EK, Schlitt HJ. Cytokines mediating the induction of chronic colitis and colitis-associated fibrosis. Mucosal Immunol. 2008a;1(Suppl 1):S24-S27.

    Not in our library10.1038/mi.2008.41

18. 18.

    Fichtner-Feigl S, Terabe M, Kitani A, Young CA, Fuss I, Geissler EK, Schlitt HJ, Berzofsky JA, Strober W. Restoration of tumor immunosurveillance via targeting of interleukin-13 receptor-alpha 2. Cancer Res. 2008b;68:3467-3475.

    Not in our library10.1158/0008-5472.can-07-5301

19. 19.
    Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family · 2007

    No notice
20. 20.

    Goel S, Hidalgo M, Perez-Soler R. EGFR inhibitor-mediated apoptosis in solid tumors. J Exp Ther Oncol. 2007;6:305-320.

    Not in our library

21. 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.

    Not in our library10.1038/onc.2011.498

22. 22.

    Kim MN, Lee KE, Hong JY, Heo WI, Kim KW, Kim KE, Sohn MH. 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.

    Not in our library10.1016/j.bbrc.2012.04.085

23. 23.

    Kioi M, Seetharam S, Puri RK. N-linked glycosylation of IL-13R alpha2 is essential for optimal IL-13 inhibitory activity. FASEB J. 2006;20:2378-2380.

    Not in our library10.1096/fj.06-5995fje

24. 24.

    Konstantinidis AK, Puddicombe SM, Mochizuki A, Sheth PD, Yang IA, Yoshisue H, Wilson SJ, Davies DE, Holgate ST, Holloway JW. Cellular localization of interleukin 13 receptor alpha2 in human primary bronchial epithelial cells and fibroblasts. J Investig Allergol Clin Immunol. 2008;18:174-180.

    Not in our library

25. 25.

    Lee PJ, Zhang X, Shan P, Ma B, Lee CG, Homer RJ, Zhu Z, Rincon M, Mossman BT, Elias JA. ERK1/2 mitogen-activated protein kinase selectively mediates IL-13-induced lung inflammation and remodeling in vivo. J Clin Invest. 2006;116:163-173.

    Not in our library10.1172/jci25711

26. 26.

    Lee CG, Hartl D, Lee GR, Koller B, Matsuura H, Da Silva CA, Sohn MH, Cohn L, Homer RJ, Kozhich AA, 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.

    Not in our library10.1084/jem.20081271

27. 27.

    Lee CG, Elias JA. Role of breast regression protein-39/YKL-40 in asthma and allergic responses. Allergy Asthma Immunol Res. 2010;2:20-27.

    Not in our library10.4168/aair.2010.2.1.20

28. 28.

    Lee CG, Da Silva CA, Dela Cruz CS, Ahangari F, Ma B, Kang MJ, He CH, Takyar S, Elias JA. Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu Rev Physiol. 2011;73:479-501.

    Not in our library10.1146/annurev-physiol-012110-142250

29. 29.

    Lupardus PJ, Birnbaum ME, Garcia KC. Molecular basis for shared cytokine recognition revealed in the structure of an unusually high affinity complex between IL-13 and IL-13Ralpha2. Structure. 2010;18:332-342.

    Not in our library10.1016/j.str.2010.01.003

30. 30.

    Moriya C, Jinnin M, Yamane K, Maruo K, Muchemwa FC, 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.

    Not in our library10.1038/jid.2010.361

31. 31.

    Ooi AT, Ram S, Kuo A, Gilbert JL, Yan W, Pellegrini M, Nickerson DW, Chatila TA, Gomperts BN. Identification of an interleukin 13-induced epigenetic signature in allergic airway inflammation. Am J Transl Res. 2012;4:219-228.

    Not in our library

32. 32.

    Rabinovich GA, Croci DO. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity. 2012;36:322-335.

    Not in our library10.1016/j.immuni.2012.03.004

33. 33.

    Schmidt H, Johansen JS, Gehl J, Geertsen PF, 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.

    Not in our library10.1002/cncr.21678

34. 34.

    Shao R, Hamel K, Petersen L, Cao QJ, Arenas RB, Bigelow C, Bentley B, Yan W. YKL-40, a secreted glycoprotein, promotes tumor angiogenesis. Oncogene. 2009;28:4456-4468.

    Not in our library10.1038/onc.2009.292

35. 35.

    Sohn MH, Kang MJ, Matsuura H, Bhandari V, Chen NY, Lee CG, Elias JA. The chitinase-like proteins breast regression protein-39 and YKL-40 regulate hyperoxia-induced acute lung injury. Am J Respir Crit Care Med. 2010;182:918-928.

    Not in our library10.1164/rccm.200912-1793oc

36. 36.

    Strober W, Kitani A, Fichtner-Feigl S, Fuss IJ. The signaling function of the IL-13Ralpha2 receptor in the development of gastrointestinal fibrosis and cancer surveillance. Curr Mol Med. 2009;9:740-750.

    Not in our library10.2174/156652409788970652

37. 37.

    Sulak O, Lameignere E, Wimmerova M, Imberty A. Specificity and affinity studies in lectin/carbohydrate interactions. Carbohydr Chem. 2009;35:356-371.

    Not in our library

38. 38.

    Wang ML, Keilbaugh SA, Cash-Mason T, He XC, Li L, Wu GD. Immune-mediated signaling in intestinal goblet cells via PI3-kinase-and AKT-dependent pathways. Am J Physiol Gastrointest Liver Physiol. 2008;295:G1122-G1130.

    Not in our library10.1152/ajpgi.90430.2008

39. 39.

    Wood N, Whitters MJ, Jacobson BA, Witek J, Sypek JP, Kasaian MT, Eppihimer MJ, Unger M, Tanaka T, Goldman SJ, et al. Enhanced interleukin (IL)-13 responses in mice lacking IL-13 receptor alpha 2. J Exp Med. 2003;197:703-709.

    Not in our library10.1084/jem.20020906

40. 40.

    Yang JS, Allahverdian S, Singhera GK, MacRedmond RE, Dorscheid DR. IL-13Rα2/AP-1 complex signalling mediates airway epithelial repair without effects on remodeling pathways. Allergy Asthma Clin Immunol. 2010;6(Suppl 3):27.

    Not in our library

41. 41.

    Yang JSY, Wadsworth SJ, Singhera GK, 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.

    Not in our library

42. 42.

    Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J, Zhang Y, Elias JA. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest. 1999;103:779-788.

    Not in our library10.1172/jci5909

Cited by papers we hold 4

• Chitinase-3 like-protein-1 function and its role in diseases · 2020
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• The Intriguing Role of Interleukin 13 in the Pathophysiology of Asthma · 2019
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• Tumor-recruited M2 macrophages promote gastric and breast cancer metastasis via M2 macrophage-secreted CHI3L1 protein · 2017
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• IL-13Rα2 uses TMEM219 in chitinase 3-like-1-induced signalling and effector responses · 2016
  Corrected

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