IL-25 elicits innate lymphoid cells and multipotent progenitor type 2 cells that reduce renal ischemic/reperfusion injury

Journal of the American Society of Nephrology

Volumn 26, Issue 9, 2015, Pages 2199-2211

  Huang, Qingsong ^a   Niu, Zhiguo ^a   Tan, Jing ^a   Yang, Jun ^a   Liu, Yun ^a   Ma, Haijun ^a   Lee, Vincent W S ^b   Sun, Shuming ^a   Song, Xiangfeng ^a   Guo, Minghao ^a   Wang, Yiping ^b   Cao, Qi ^a,b  

^a XINXIANG MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; CELL MARKER; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 25; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MANNOSE RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; IMMUNOLOGIC FACTOR; INTERLEUKIN 17;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; HISTOPATHOLOGY; IMMUNOPHENOTYPING; IN VITRO STUDY; KIDNEY; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY ISCHEMIA; LYMPHOID CELL; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; TH2 CELL; ACUTE KIDNEY INJURY; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL SURVIVAL; COMPLICATION; CYTOLOGY; DRUG EFFECTS; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE; MALE; METABOLISM; VASCULARIZATION;

ACUTE KIDNEY INJURY; ADOPTIVE TRANSFER; ANIMALS; CELL SURVIVAL; CELLS, CULTURED; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; INTERLEUKIN-13; INTERLEUKIN-17; INTERLEUKIN-4; INTERLEUKIN-5; KIDNEY; LYMPHOCYTES; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MULTIPOTENT STEM CELLS; REPERFUSION INJURY; TH2 CELLS;

EID: 84940768022     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014050479     Document Type: Article

References (44)

1. Angkasekwinai P, Park H,Wang YH,Wang YH, Chang SH, Corry DB, Liu YJ, Zhu Z, Dong C: Interleukin 25 promotes the initiation of proallergic type 2 responses. J ExpMed 204: 1509-1517, 2007
2. Ikeda K, Nakajima H, Suzuki K, Kagami S, Hirose K, Suto A, Saito Y, Iwamoto I:Mast cells produce interleukin-25 upon Fc epsilon RI-mediated activation. Blood 101: 3594-3596, 2003
3. Zaph C, Du Y, Saenz SA, Nair MG, Perrigoue JG, Taylor BC, Troy AE, Kobuley DE, Kastelein RA, Cua DJ, Yu Y, Artis D: Commensal-dependent expression of IL-25 regulates the IL-23-IL-17 axis in the intestine. J Exp Med 205: 2191-2198, 2008
4. FortMM, Cheung J, Yen D, Li J, Zurawski SM, Lo S,Menon S, Clifford T, Hunte B, Lesley R, Muchamuel T, Hurst SD, Zurawski G, Leach MW, Gorman DM, Rennick DM: IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15: 985-995, 2001
5. Tamachi T, Maezawa Y, Ikeda K, Kagami S, Hatano M, Seto Y, Suto A, Suzuki K,WatanabeN, Saito Y, Tokuhisa T, Iwamoto I,NakajimaH: IL-25 enhances allergic airway inflammation by amplifying a TH2 cell-dependent pathway in mice. J Allergy Clin Immunol 118: 606-614, 2006
6. Corrigan CJ,WangW, Meng Q, Fang C, Eid G, Caballero MR, Lv Z, An Y, Wang YH, Liu YJ, Kay AB, Lee TH, Ying S: Allergen-induced expression of IL-25 and IL-25 receptor in atopic asthmatic airways and late-phase cutaneous responses. J Allergy Clin Immunol 128: 116-124, 2011
7. Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A, Hewett DR,McIlgormA, Jolin HE,McKenzie AN: Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J ExpMed 203: 1105-1116, 2006
8. Zhao A, Urban JF Jr, Sun R, Stiltz J, Morimoto M, Notari L, Madden KB, Yang Z, Grinchuk V, Ramalingam TR, Wynn TA, Shea-Donohue T: Critical role of IL-25 in nematode infection-induced alterations in intestinal function. J Immunol 185: 6921-6929, 2010
9. ZaissMM, Maslowski KM, Mosconi I, Guenat N,Marsland BJ, Harris NL: IL-1b suppresses innate IL-25 and IL-33 production and maintains helminth chronicity. PLoS Pathog 9: e1003531, 2013
10. Kleinschek MA, Owyang AM, Joyce-Shaikh B, Langrish CL, Chen Y, Gorman DM, Blumenschein WM, McClanahan T, Brombacher F, Hurst SD, Kastelein RA, Cua DJ: IL-25 regulates Th17 function in autoimmune inflammation. J Exp Med 204: 161-170, 2007
11. Cao Q, Wang C, Zheng D, Wang Y, Lee VW, Wang YM, Zheng G, Tan TK, Yu D, Alexander SI, Harris DC,Wang Y: IL-25 induces M2 macrophages and reduces renal injury in proteinuric kidney disease.JAmSocNephrol 22: 1229-1239, 2011
12. Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, Furusawa J, Ohtani M, Fujii H, Koyasu S: Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463: 540-544, 2010
13. Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, Langford TK, Bucks C, Kane CM, Fallon PG, Pannell R, Jolin HE, McKenzie AN: Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367-1370, 2010
14. Price AE, Liang HE, Sullivan BM, Reinhardt RL, Eisley CJ, Erle DJ, Locksley RM: Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci U S A 107: 11489-11494, 2010
15. Saenz SA, Siracusa MC, Perrigoue JG, Spencer SP, Urban JF Jr, Tocker JE, Budelsky AL, Kleinschek MA, Kastelein RA, Kambayashi T, Bhandoola A, Artis D: IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 464: 1362-1366, 2010
16. Spits H, ArtisD, ColonnaM, Diefenbach A, Di Santo JP, EberlG, Koyasu S, Locksley RM, McKenzie AN, Mebius RE, Powrie F, Vivier E: Innate lymphoid cells-a proposal for uniform nomenclature. Nat Rev Immunol 13: 145-149, 2013
17. Licona-Limón P, KimLK, PalmNW, Flavell RA: TH2, allergy and group 2 innate lymphoid cells. Nat Immunol 14: 536-542, 2013
18. Barlow JL, Bellosi A, Hardman CS, Drynan LF, Wong SH, Cruickshank JP,McKenzie AN: Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J Allergy Clin Immunol 129: 191.e4-198.e4, 2012
19. Monticelli LA, Sonnenberg GF, Abt MC, Alenghat T, Ziegler CG, Doering TA, Angelosanto JM, Laidlaw BJ, Yang CY, Sathaliyawala T, Kubota M, Turner D, Diamond JM, Goldrath AW, Farber DL, Collman RG, Wherry EJ, Artis D: Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol 12: 1045-1054, 2011
20. Saenz SA, Siracusa MC, Monticelli LA, Ziegler CG, Kim BS, Brestoff JR, Peterson LW, Wherry EJ, Goldrath AW, Bhandoola A, Artis D: IL-25 simultaneously elicits distinct populations of innate lymphoid cells and multipotent progenitor type 2 (MPPtype2) cells. J ExpMed 210: 1823-1837, 2013
21. Li L, Okusa MD: Macrophages, dendritic cells, and kidney ischemiareperfusion injury. Semin Nephrol 30: 268-277, 2010
22. Lee S, Huen S,Nishio H,Nishio S, LeeHK,Choi BS, Ruhrberg C,Cantley LG: Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 22: 317-326, 2011
23. Lin SL, Li B, Rao S, Yeo EJ, Hudson TE, Nowlin BT, Pei H, Chen L, Zheng JJ, Carroll TJ, Pollard JW, McMahon AP, Lang RA, Duffield JS: MacrophageWnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci U S A 107: 4194-4199, 2010
24. Halim TY, Krauss RH, Sun AC, Takei F: Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36: 451-463, 2012
25. Caruso R, Stolfi C, Sarra M, Rizzo A, Fantini MC, Pallone F, MacDonald TT, Monteleone G: Inhibition of monocyte-derived inflammatory cytokines by IL-25 occurs via p38 Map kinase-dependent induction of Socs-3. Blood 113: 3512-3519, 2009
26. Hams E, Locksley RM, McKenzie AN, Fallon PG: Cutting edge: IL-25 elicits innate lymphoid type 2 and type IINKT cells that regulate obesity in mice. J Immunol 191: 5349-5353, 2013
27. Jang HR, Ko GJ, Wasowska BA, Rabb H: The interaction between ischemia-reperfusion and immune responses in the kidney. J Mol Med (Berl) 87: 859-864, 2009
28. Tam FW, Smith J, Karkar AM, Pusey CD, Rees AJ: Interleukin-4 ameliorates experimental glomerulonephritis and up-regulates glomerular gene expression of IL-1 decoy receptor. Kidney Int 52: 1224-1231, 1997
29. Tipping PG, Kitching AR, Huang XR, Mutch DA, Holdsworth SR: Immune modulation with interleukin-4 and interleukin-10 prevents crescent formation and glomerular injury in experimental glomerulonephritis. Eur J Immunol 27: 530-537, 1997
30. Kitching AR, Turner AL, Wilson GR, Edgtton KL, Tipping PG, Holdsworth SR: Endogenous IL-13 limits humoral responses and injury in experimental glomerulonephritis but does not regulate Th1 cellmediated crescentic glomerulonephritis. J Am SocNephrol 15: 2373-2382, 2004
31. Sandovici M, Henning RH, van Goor H, Helfrich W, de Zeeuw D, Deelman LE: Systemic gene therapy with interleukin-13 attenuates renal ischemia-reperfusion injury. Kidney Int 73: 1364-1373, 2008
32. Yokota N, Burne-Taney M, Racusen L, Rabb H: Contrasting roles for STAT4 and STAT6 signal transduction pathways in murine renal ischemia-reperfusion injury. Am J Physiol Renal Physiol 285: F319-F325, 2003
33. Bajwa A, Huang L, Ye H, Dondeti K, Song S, Rosin DL, Lynch KR, Lobo PI, Li L, Okusa MD: Dendritic cell sphingosine 1-phosphate receptor-3 regulates Th1-Th2 polarity in kidney ischemia-reperfusion injury. J Immunol 189: 2584-2596, 2012
34. Yang Z, Grinchuk V, Urban JF Jr, Bohl J, Sun R, Notari L, Yan S, Ramalingam T, Keegan AD, Wynn TA, Shea-Donohue T, Zhao A: Macrophages as IL-25/IL-33-responsive cells play an important role in the induction of type 2 immunity. PLoS ONE 8: e59441, 2013
35. Wang Y,Wang YP, Zheng G, Lee VW,Ouyang L,ChangDH,MahajanD, Coombs J, Wang YM, Alexander SI, Harris DC: Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int 72: 290-299, 2007
36. Cao Q, Wang Y, Zheng D, Sun Y, Wang Y, Lee VW, Zheng G, Tan TK, Ince J, Alexander SI, Harris DC: IL-10/TGF-beta-modified macrophages induce regulatory T cells and protect against adriamycin nephrosis. J Am Soc Nephrol 21: 933-942, 2010
37. Ferenbach DA, Ramdas V, Spencer N, Marson L, Anegon I, Hughes J, Kluth DC: Macrophages expressing heme oxygenase-1 improve renal function in ischemia/reperfusion injury. Mol Ther 18: 1706-1713, 2010
38. JungM, Sola A, Hughes J, Kluth DC, Vinuesa E, Viñas JL, Pérez-Ladaga A, Hotter G: Infusion of IL-10-expressing cells protects against renal ischemia through induction of lipocalin-2. Kidney Int 81: 969-982, 2012
39. Molofsky AB, Nussbaum JC, Liang HE, Van Dyken SJ, Cheng LE, Mohapatra A, Chawla A, Locksley RM: Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med 210: 535-549, 2013
40. Johnson CR, Kitz D, Little JR: Amethod for the derivation and continuous propagation of cloned murine bone marrow macrophages. J Immunol Methods 65: 319-332, 1983
41. Doctor RB, Chen J, Peters LL, Lux SE, Mandel LJ: Distribution of epithelial ankyrin (Ank3) spliceoforms in renal proximal and distal tubules. Am J Physiol 274: F129-F138, 1998
42. Meldrum KK, Meldrum DR, Hile KL, Burnett AL, Harken AH: A novel model of ischemia in renal tubular cells which closely parallels in vivo injury. J Surg Res 99: 288-293, 2001
43. Cao Q,Wang L,Du F, ShengH, Zhang Y,Wu J, Shen B, Shen T, Zhang J, Li D, Li N: Downregulation of CD4+CD25+ regulatory T cells may underlie enhanced Th1 immunity caused by immunization with activated autologous T cells. Cell Res 17: 627-637, 2007
44. Alikhan MA, Jones CV, Williams TM, Beckhouse AG, Fletcher AL, Kett MM, Sakkal S, Samuel CS, Ramsay RG, Deane JA, Wells CA, Little MH, Hume DA, Ricardo SD: Colony-stimulating factor-1 promotes kidney growth and repair via alteration ofmacrophage responses. AmJ Pathol 179: 1243-1256, 2011