Interleukin‑33 promotes obstructive renal injury via macrophages

Li,Yanlei; Liu,Jing; Yu,Ting; Yan,Bingdi; Li,Hongjun

doi:10.3892/mmr.2019.10324

Interleukin‑33 promotes obstructive renal injury via macrophages

Authors:
- Yanlei Li
- Jing Liu
- Ting Yu
- Bingdi Yan
- Hongjun Li
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Affiliations: Health Management Medical Center, China‑Japan Union Hospital of Jilin University, Changchun, Jilin 130033, P.R. China, Department of Respiratory and Critical Care Medicine, The Second Hospital of Jilin University, Changchun, Jilin 130041, P.R. China, Department of Clinical Laboratory, The Second Hospital of Jilin University, Changchun, Jilin 130041, P.R. China
Published online on: June 3, 2019 https://doi.org/10.3892/mmr.2019.10324
Pages: 1353-1362

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Abstract

Chronic kidney disease is the outcome of most kidney diseases, and renal fibrosis is a pathological process involved in the progression of these disorders. The role of interleukin (IL)‑33 was previously investigated in fibrotic disorders affecting various organs, including liver, lungs and heart; however, its role in renal fibrosis remains unclear. Previous studies have demonstrated that macrophages are involved in obstructive renal injury. In the present study, the roles of IL‑33 and macrophages on renal fibrosis were investigated using a mouse model of unilateral ureteral obstruction (UUO). Compared with non‑obstructed kidneys, the expression levels of IL‑33 and its receptor, interleukin 1 receptor like 1, increased after UUO. Furthermore, the infiltration of macrophages and the degree of renal fibrosis increased after treatment with IL‑33. Additionally, the expression level of arginase‑1, a marker of M2 macrophages, increased in renal tissue. After depletion of macrophages, the administration of exogenous IL‑33 was not sufficient to reverse the reduction in fibrosis caused by elimination of these cells. Collectively, the present results suggested that IL‑33 promoted renal fibrosis in UUO‑induced renal injury by regulating macrophage polarization.

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1	Barnes JL and Glass WFII: Renal interstitial fibrosis: A critical evaluation of the origin of myofibroblasts. Contrib Nephrol. 169:73–93. 2011. View Article : Google Scholar : PubMed/NCBI
2	Hill NR, Fatoba ST, Oke JL, Hirst JA, O'Callaghan CA, Lasserson DS and Hobbs FD: Global prevalence of chronic kidney disease-A systematic review and meta-analysis. PLoS One. 11:e01587652016. View Article : Google Scholar : PubMed/NCBI
3	Zhao J, Wang L, Cao A, Jiang M, Chen X and Peng W: Renal tubulointerstitial fibrosis: A review in animal models. J Integr Nephrol Androl. 2:75–80. 2015. View Article : Google Scholar
4	Imig JD and Ryan MJ: Immune and inflammatory role in renal disease. Compr Physiol. 3:957–976. 2013.PubMed/NCBI
5	Xiao X, Gaffar I, Guo P, Wiersch J, Fischbach S, Peirish L, Song Z, El-Gohary Y, Prasadan K, Shiota C and Gittes GK: M2 macrophages promote beta-cell proliferation by up-regulation of SMAD7. Proc Natl Acad Sci USA. 111:E1211–E1220. 2014. View Article : Google Scholar : PubMed/NCBI
6	Chevalier RL, Forbes MS and Thornhill BA: Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int. 75:1145–1152. 2009. View Article : Google Scholar : PubMed/NCBI
7	Forbes MS, Thornhill BA and Chevalier RL: Proximal tubular injury and rapid formation of atubular glomeruli in mice with unilateral ureteral obstruction: A new look at an old model. Am J Physiol Renal Physiol. 301:F110–F117. 2011. View Article : Google Scholar : PubMed/NCBI
8	Forbes MS, Thornhill BA, Minor JJ, Gordon KA, Galarreta CI and Chevalier RL: Fight-or-flight: Murine unilateral ureteral obstruction causes extensive proximal tubular degeneration, collecting duct dilatation, and minimal fibrosis. Am J Physiol Renal Physiol. 303:F120–F129. 2012. View Article : Google Scholar : PubMed/NCBI
9	Ferrario F, Castiglione A, Colasanti G, Barbiano di Belgioioso G, Bertoli S and D'Amico G: The detection of monocytes in human glomerulonephritis. Kidney Int. 28:513–519. 1985. View Article : Google Scholar : PubMed/NCBI
10	Meng XM, Nikolic-Paterson DJ and Lan HY: Inflammatory processes in renal fibrosis. Nat Rev Nephrol. 10:493–503. 2014. View Article : Google Scholar : PubMed/NCBI
11	Kim MG, Kim SC, Ko YS, Lee HY, Jo SK and Cho W: The role of M2 macrophages in the progression of chronic kidney disease following acute kidney injury. PLoS One. 10:e01439612015. View Article : Google Scholar : PubMed/NCBI
12	Mosser DM and Edwards JP: Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 8:958–969. 2008. View Article : Google Scholar : PubMed/NCBI
13	Guiteras R, Flaquer M and Cruzado JM: Macrophage in chronic kidney disease. Clin Kidney J. 9:765–771. 2016. View Article : Google Scholar : PubMed/NCBI
14	Guiteras R, Sola A, Flaquer M, Hotter G, Torras J, Grinyó JM and Cruzado JM: Macrophage overexpressing NGAL ameliorated kidney fibrosis in the UUO mice model. Cell Physiol Biochem. 42:1945–1960. 2017. View Article : Google Scholar : PubMed/NCBI
15	Colin S, Chinetti-Gbaguidi G and Staels B: Macrophage phenotypes in atherosclerosis. Immunol Rev. 262:153–166. 2014. View Article : Google Scholar : PubMed/NCBI
16	Flavell RA, Sanjabi S, Wrzesinski SH and Licona-Limón P: The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol. 10:554–567. 2010. View Article : Google Scholar : PubMed/NCBI
17	Liew FY, Girard JP and Turnquist HR: Interleukin-33 in health and disease. Nat Rev Immunol. 16:676–689. 2016. View Article : Google Scholar : PubMed/NCBI
18	Ricardo SD, van Goor H and Eddy AA: Macrophage diversity in renal injury and repair. J Clin Invest. 118:3522–3530. 2008. View Article : Google Scholar : PubMed/NCBI
19	Wynn TA and Ramalingam TR: Mechanisms of fibrosis: Therapeutic translation for fibrotic disease. Nat Med. 18:1028–1040. 2012. View Article : Google Scholar : PubMed/NCBI
20	Lott JM, Sumpter TL and Turnquist HR: New dog and new tricks: Evolving roles for IL-33 in type 2 immunity. J Leukoc Biol. 97:1037–1048. 2015. View Article : Google Scholar : PubMed/NCBI
21	Kurowska-Stolarska M, Hueber A, Stolarski B and McInnes IB: Interleukin-33: A novel mediator with a role in distinct disease pathologies. J Intern Med. 269:29–35. 2011. View Article : Google Scholar : PubMed/NCBI
22	Staurengo-Ferrari L, Trevelin SC, Fattori V, Nascimento DC, de Lima KA, Pelayo JS, Figueiredo F, Casagrande R, Fukada SY, Teixeira MM, et al: Interleukin-33 receptor (ST2) deficiency improves the outcome of staphylococcus aureus-induced septic arthritis. Front Immunol. 9:9622018. View Article : Google Scholar : PubMed/NCBI
23	Chen WY, Chang YJ, Su CH, Tsai TH, Chen SD, Hsing CH and Yang JL: Upregulation of Interleukin-33 in obstructive renal injury. Biochem Biophys Res Commun. 473:1026–1032. 2016. View Article : Google Scholar : PubMed/NCBI
24	Pan B, Liu G, Jiang Z and Zheng D: Regulation of renal fibrosis by macrophage polarization. Cell Physiol Biochem. 35:1062–1069. 2015. View Article : Google Scholar : PubMed/NCBI
25	Li D, Guabiraba R, Besnard AG, Komai-Koma M, Jabir MS, Zhang L, Graham GJ, Kurowska-Stolarska M, Liew FY, McSharry C and Xu D: IL-33 promotes ST2-dependent lung fibrosis by the induction of alternatively activated macrophages and innate lymphoid cells in mice. J Allergy Clin Immunol. 134:1422–1432.e11. 2014. View Article : Google Scholar : PubMed/NCBI
26	Inada T, Yamanouchi Y, Jomura S, Sakamoto S, Takahashi M, Kambara T and Shingu K: Effect of propofol and isoflurane anaesthesia on the immune response to surgery. Anaesthesia. 59:954–959. 2004. View Article : Google Scholar : PubMed/NCBI
27	Zhang WL, Liu MY, Zhang ZC and Duan CY: Effect of different anesthesia methods on erythrocyte immune function in mice. Asian Pac J Trop Med. 6:995–998. 2013. View Article : Google Scholar : PubMed/NCBI
28	Hohlbaum K, Bert B, Dietze S, Palme R, Fink H and Thöne-Reineke C: Severity classification of repeated isoflurane anesthesia in C57BL/6JRj mice-Assessing the degree of distress. PLoS One. 12:e01795882017. View Article : Google Scholar : PubMed/NCBI
29	van Rooijen N and Hendrikx E: Liposomes for specific depletion of macrophages from organs and tissues. Methods Mol Biol. 605:189–203. 2010. View Article : Google Scholar : PubMed/NCBI
30	Ferenbach DA, Sheldrake TA, Dhaliwal K, Kipari TM, Marson LP, Kluth DC and Hughes J: Macrophage/monocyte depletion by clodronate, but not diphtheria toxin, improves renal ischemia/reperfusion injury in mice. Kidney Int. 82:928–933. 2012. View Article : Google Scholar : PubMed/NCBI
31	Aimo A, Migliorini P, Vergaro G, Franzini M, Passino C, Maisel A and Emdin M: The IL-33/ST2 pathway, inflammation and atherosclerosis: Trigger and target? Int J Cardiol. 267:188–192. 2018. View Article : Google Scholar : PubMed/NCBI
32	Sanson M, Distel E and Fisher EA: HDL induces the expression of the M2 macrophage markers arginase 1 and Fizz-1 in a STAT6-dependent process. PLoS One. 8:e746762013. View Article : Google Scholar : PubMed/NCBI
33	Molofsky AB, Savage AK and Locksley RM: Interleukin-33 in tissue homeostasis, injury, and inflammation. Immunity. 42:1005–1019. 2015. View Article : Google Scholar : PubMed/NCBI
34	Yu CC, Chien CT and Chang TC: M2 macrophage polarization modulates epithelial-mesenchymal transition in cisplatin-induced tubulointerstitial fibrosis. Biomedicine (Taipei). 6:52016. View Article : Google Scholar : PubMed/NCBI
35	Biernacka A, Dobaczewski M and Frangogiannis NG: TGF-β signaling in fibrosis. Growth Factors. 29:196–202. 2011. View Article : Google Scholar : PubMed/NCBI
36	Ramalingam TR, Gieseck RL, Acciani TH, M Hart K, Cheever AW, Mentink-Kane MM, Vannella KM and Wynn TA: Enhanced protection from fibrosis and inflammation in the combined absence of IL-13 and IFN-γ. J Pathol. 239:344–354. 2016. View Article : Google Scholar : PubMed/NCBI
37	Wang S, Meng XM, Ng YY, Ma FY, Zhou S, Zhang Y, Yang C, Huang XR, Xiao J, Wang YY, et al: TGF-β/Smad3 signalling regulates the transition of bone marrow-derived macrophages into myofibroblasts during tissue fibrosis. Oncotarget. 7:8809–8822. 2016.PubMed/NCBI
38	Ikezumi Y, Suzuki T, Yamada T, Hasegawa H, Kaneko U, Hara M, Yanagihara T, Nikolic-Paterson DJ and Saitoh A: Alternatively activated macrophages in the pathogenesis of chronic kidney allograft injury. Pediatr Nephrol. 30:1007–1017. 2015. View Article : Google Scholar : PubMed/NCBI
39	Lu J, Cao Q, Zheng D, Sun Y, Wang C, Yu X, Wang Y, Lee VW, Zheng G, Tan TK, et al: Discrete functions of M2a and M2c macrophage subsets determine their relative efficacy in treating chronic kidney disease. Kidney Int. 84:745–755. 2013. View Article : Google Scholar : PubMed/NCBI
40	Tecklenborg J, Clayton D, Siebert S and Coley SM: The role of the immune system in kidney disease. Clin Exp Immunol. 192:142–150. 2018. View Article : Google Scholar : PubMed/NCBI
41	Yatim KM and Lakkis FG: A brief journey through the immune system. Clin J Am Soc Nephrol. 10:1274–1281. 2015. View Article : Google Scholar : PubMed/NCBI
42	Kurts C, Panzer U, Anders HJ and Rees AJ: The immune system and kidney disease: Basic concepts and clinical implications. Nat Rev Immunol. 13:738–753. 2013. View Article : Google Scholar : PubMed/NCBI
43	Li L, Huang L, Ye H, Song SP, Bajwa A, Lee SJ, Moser EK, Jaworska K, Kinsey GR, Day YJ, et al: Dendritic cells tolerized with adenosine A2AR agonist attenuate acute kidney injury. J Clin Invest. 122:3931–3942. 2012. View Article : Google Scholar : PubMed/NCBI
44	Lai LW, Yong KC and Lien YH: Pharmacologic recruitment of regulatory T cells as a therapy for ischemic acute kidney injury. Kidney Int. 81:983–992. 2012. View Article : Google Scholar : PubMed/NCBI
45	Sean Eardley K and Cockwell P: Macrophages and progressive tubulointerstitial disease. Kidney Int. 68:437–455. 2005. View Article : Google Scholar : PubMed/NCBI