Mannose-capped lipoarabinomannan from mycobacterium tuberculosis induces IL-37 production via upregulating ERK1/2 and p38 in human type ii alveolar epithelial cells

International Journal of Clinical and Experimental Medicine

Volumn 8, Issue 5, 2015, Pages 7279-7287

  Huang, Zhen ^a,b   Zhao, Gao Wei ^c   Gao, Chun Hai ^d   Chi, Xiu Wen ^e   Zeng, Tao ^e   Hu, Yan Wei ^a   Zheng, Lei ^a   Wang, Qian ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b Central Hospital of Longgang District   (China)

^c Linyi Blood Center   (China)

^d LINYI PEOPLE'S HOSPITAL   (China)

^e GUANGDONG MEDICAL UNIVERSITY   (China)

Author keywords

ERK1 2; IL 37; ManLAM; P38; TLR2; Tuberculosis

Indexed keywords

CYTOKINE; INTERLEUKIN 37; LIPOARABINOMANNAN; MANNOSE CAPPED LIPOARABINOMANNAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SMALL INTERFERING RNA; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM CELL; MYCOBACTERIUM TUBERCULOSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

MYCOBACTERIUM TUBERCULOSIS;

EID: 84937061126     PISSN: None     EISSN: 19405901     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. [1] Rasolofo Razanamparany V, Menard D, Auregan G, Gicquel B and Chanteau S. Extrapulmonary and pulmonary tuberculosis in antananarivo (madagascar): high clustering rate in female patients. J Clin Microbiol 2002; 40: 3964-3969.
2. [2] Zumla A, George A, Sharma V, Herbert RH, Oxley A and Oliver M. The WHO 2014 Global tuberculosis report-further to go. Lancet Glob Health 2015; 3: e10-12.
3. [3] Jozefowski S, Sobota A, Pawlowski A and Kwiatkowska K. Mycobacterium tuberculosis lipoarabinomannan enhances LPS-induced TNF-alpha production and inhibits NO secretion by engaging scavenger receptors. Microb Pathog 2011; 50: 350-359.
4. [4] Yonekawa A, Saijo S, Hoshino Y, Miyake Y, Ishikawa E, Suzukawa M, Inoue H, Tanaka M, Yoneyama M, Oh-Hora M, Akashi K and Yamasaki S. Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria. Immunity 2014; 41: 402-413.
5. [5] Fratti RA, Chua J, Vergne I and Deretic V. Mycobacterium tuberculosis glycosylated ph-osphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A 2003; 100: 5437-5442.
6. [6] Mahon RN, Sande OJ, Rojas RE, Levine AD, Harding CV and Boom WH. Mycobacterium tuberculosis ManLAM inhibits T-cell-receptor signaling by interference with ZAP-70, Lck and LAT phosphorylation. Cell Immunol 2012; 275: 98-105.
7. [7] Geijtenbeek TB, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, Appelmelk B and Van Kooyk Y. Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 2003; 197: 7-17.
8. [8] Sweet L, Singh PP, Azad AK, Rajaram MV, Schlesinger LS and Schorey JS. Mannose receptor-dependent delay in phagosome maturation by Mycobacterium avium glycopeptidolipids. Infect Immun 2010; 78: 518-526.
9. [9] Smith DE, Renshaw BR, Ketchem RR, Kubin M, Garka KE and Sims JE. Four new members expand the interleukin-1 superfamily. J Biol Chem 2000; 275: 1169-1175.
10. [10] McNamee EN, Masterson JC, Jedlicka P, McManus M, Grenz A, Collins CB, Nold MF, Nold-Petry C, Bufler P, Dinarello CA and Rivera-Nieves J. Interleukin 37 expression protects mice from colitis. Proc Natl Acad Sci U S A 2011; 108: 16711-16716.
11. [11] Zhao JJ, Pan QZ, Pan K, Weng DS, Wang QJ, Li JJ, Lv L, Wang DD, Zheng HX, Jiang SS, Zhang XF and Xia JC. Interleukin-37 mediates the antitumor activity in hepatocellular carcinoma: role for CD57+ NK cells. Sci Rep 2014; 4: 5177.
12. [12] Luo Y, Cai X, Liu S, Wang S, Nold-Petry CA, Nold MF, Bufler P, Norris D, Dinarello CA and Fujita M. Suppression of antigen-specific adaptive immunity by IL-37 via induction of tolerogenic dendritic cells. Proc Natl Acad Sci U S A 2014; 111: 15178-15183.
13. [13] Moretti S, Bozza S, Oikonomou V, Renga G, Casagrande A, Iannitti RG, Puccetti M, Garlanda C, Kim S, Li S, van de Veerdonk FL, Dinarello CA and Romani L. IL-37 inhibits inflammasome activation and disease severity in murine aspergillosis. PLoS Pathog 2014; 10: e1004462.
14. [14] Bufler P, Gamboni-Robertson F, Azam T, Kim SH and Dinarello CA. Interleukin-1 homologues IL-1F7b and IL-18 contain functional mRNA instability elements within the coding region responsive to lipopolysaccharide. Biochem J 2004; 381: 503-510.
15. [15] Imaeda H, Takahashi K, Fujimoto T, Kasumi E, Ban H, Bamba S, Sonoda H, Shimizu T, Fujiyama Y and Andoh A. Epithelial expression of interleukin-37b in inflammatory bowel disease. Clin Exp Immunol 2013; 172: 410-416.
16. [16] Nold MF, Nold-Petry CA, Zepp JA, Palmer BE, Bufler P and Dinarello CA. IL-37 is a fundamental inhibitor of innate immunity. Nat Immunol 2010; 11: 1014-1022.
17. [17] He L, Liang Z, Zhao F, Peng L and Chen Z. Modulation of IL-37 expression by triptolide and triptonide in THP-1 cells. Cell Mol Immunol 2014; [Epub ahead of print].
18. [18] Yanagawa Y and Onoe K. Enhanced IL-10 production by TLR4-and TLR2-primed dendritic cells upon TLR restimulation. J Immunol 2007; 178: 6173-6180.
19. [19] Qian C, Jiang X, An H, Yu Y, Guo Z, Liu S, Xu H and Cao X. TLR agonists promote ERK-mediated preferential IL-10 production of regulatory dendritic cells (diffDCs), leading to NK-cell activation. Blood 2006; 108: 2307-2315.
20. [20] Elass E, Coddeville B, Kremer L, Mortuaire M, Mazurier J and Guerardel Y. Mycobacterial lipomannan induces MAP kinase phosphatase-1 expression in macrophages. FEBS Lett 2008; 582: 445-450.
21. [21] Mazurek J, Ignatowicz L, Kallenius G, Svenson SB, Pawlowski A and Hamasur B. Divergent effects of mycobacterial cell wall glycolipids on maturation and function of human monocyte-derived dendritic cells. PLoS One 2012; 7: e42515.
22. [22] Heldwein KA and Fenton MJ. The role of Toll-like receptors in immunity against mycobacterial infection. Microbes Infect 2002; 4: 937-944.
23. [23] Rajaram MV, Brooks MN, Morris JD, Torrelles JB, Azad AK and Schlesinger LS. Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor ga-mma linking mannose receptor recognition to regulation of immune responses. J Immunol 2010; 185: 929-942.
24. [24] Chan ED, Morris KR, Belisle JT, Hill P, Remigio LK, Brennan PJ and Riches DW. Induction of inducible nitric oxide synthase-NO* by lipoarabinomannan of Mycobacterium tuberculosis is mediated by MEK1-ERK, MKK7-JNK, and NF-kappaB signaling pathways. Infect Immun 2001; 69: 2001-2010.
25. [25] Pan Q, Wang Q, Sun X, Xia X, Wu S, Luo F and Zhang XL. Aptamer against mannose-capped lipoarabinomannan inhibits virulent Mycobac-terium tuberculosis infection in mice and rhesus monkeys. Mol Ther 2014; 22: 940-951.
26. [26] Torrelles JB, Azad AK and Schlesinger LS. Fine discrimination in the recognition of individual species of phosphatidyl-myo-inositol mannosides from Mycobacterium tuberculosis by C-type lectin pattern recognition receptors. J Immunol 2006; 177: 1805-1816.
27. [27] Ballak DB, van Diepen JA, Moschen AR, Jansen HJ, Hijmans A, Groenhof GJ, Leenders F, Bufler P, Boekschoten MV, Muller M, Kersten S, Li S, Kim S, Eini H, Lewis EC, Joosten LA, Tilg H, Netea MG, Tack CJ, Dinarello CA and Stienstra R. IL-37 protects against obesity-induced inflammation and insulin resistance. Nat Commun 2014; 5: 4711.
28. [28] Guo XG, Ji TX, Xia Y and Ma YY. Autophagy protects type II alveolar epithelial cells from Mycobacterium tuberculosis infection. Bio-chem Biophys Res Commun 2013; 432: 308-313.
29. [29] Devaraj S and Jialal I. Increased secretion of IP-10 from monocytes under hyperglycemia is via the TLR2 and TLR4 pathway. Cytokine 2009; 47: 6-10.
30. [30] Wang JP, Kurt-Jones EA, Shin OS, Manchak MD, Levin MJ and Finberg RW. Varicella-zoster virus activates inflammatory cytokines in human monocytes and macrophages via Toll-like receptor 2. J Virol 2005; 79: 12658-12666.
31. [31] Leopold K and Fischer W. Molecular analysis of the lipoglycans of Mycobacterium tuberculosis. Anal Biochem 1993; 208: 57-64.
32. [32] Boraschi D, Lucchesi D, Hainzl S, Leitner M, Maier E, Mangelberger D, Oostingh GJ, Pfaller T, Pixner C, Posselt G, Italiani P, Nold MF, Nold-Petry CA, Bufler P and Dinarello CA. IL-37: a new anti-inflammatory cytokine of the IL-1 family. Eur Cytokine Netw 2011; 22: 127-147.
33. [33] Tapping RI and Tobias PS. Mycobacterial lipoarabinomannan mediates physical interactions between TLR1 and TLR2 to induce signaling. J Endotoxin Res 2003; 9: 264-268.
34. [34] Mishra AK, Driessen NN, Appelmelk BJ and Besra GS. Lipoarabinomannan and related glycoconjugates: structure, biogenesis and role in Mycobacterium tuberculosis physiology and host-pathogen interaction. FEMS Microbiol Rev 2011; 35: 1126-1157.
35. [35] Kumar S, McDonnell PC, Lehr R, Tierney L, Tzimas MN, Griswold DE, Capper EA, Tal-Singer R, Wells GI, Doyle ML and Young PR. Identification and initial characterization of four novel members of the interleukin-1 family. J Biol Chem 2000; 275: 10308-10314.
36. [36] Fujita H, Inoue Y, Seto K, Komitsu N and Aihara M. Interleukin-37 is elevated in subjects with atopic dermatitis. J Dermatol Sci 2013; 69: 173-175.
37. [37] Ye L, Ji L, Wen Z, Zhou Y, Hu D, Li Y, Yu T, Chen B, Zhang J, Ding L, Du J and Huang Z. IL-37 inhibits the production of inflammatory cytokines in peripheral blood mononuclear cells of patients with systemic lupus erythematosus: its correlation with disease activity. J Transl Med 2014; 12: 69.
38. [38] Adlakha N, Vir P and Verma I. Effect of mycobacterial secretory proteins on the cellular integrity and cytokine profile of type II alveolar epithelial cells. Lung India 2012; 29: 313-318.
39. [39] Chatterjee D, Roberts AD, Lowell K, Brennan PJ and Orme IM. Structural basis of capacity of lipoarabinomannan to induce secretion of tumor necrosis factor. Infect Immun 1992; 60: 1249-1253.
40. [40] Briken V, Porcelli SA, Besra GS and Kremer L. Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol Microbiol 2004; 53: 391-403.
41. [41] Fortune SM, Solache A, Jaeger A, Hill PJ, Belisle JT, Bloom BR, Rubin EJ and Ernst JD. Mycobacterium tuberculosis inhibits macrophage responses to IFN-gamma through myeloid differentiation factor 88-dependent and-independent mechanisms. J Immunol 2004; 172: 6272-6280.
42. [42] Gehring AJ, Dobos KM, Belisle JT, Harding CV and Boom WH. Mycobacterium tuberculosis LprG (Rv1411c): a novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J Immunol 2004; 173: 2660-2668.
43. [43] Li Y, Wang Z, Yu T, Chen B, Zhang J, Huang K and Huang Z. Increased expression of IL-37 in patients with Graves’ disease and its contribution to suppression of proinflammatory cytokines production in peripheral blood mononuclear cells. PLoS One 2014; 9: e107183.
44. [44] Fratti RA, Chua J and Deretic V. Induction of p38 mitogen-activated protein kinase reduces early endosome autoantigen 1 (EEA1) recruitment to phagosomal membranes. J Biol Chem 2003; 278: 46961-46967.
45. [45] Vergne I, Chua J, Singh SB and Deretic V. Cell biology of mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol 2004; 20: 367-394.
46. [46] Appelmelk BJ, den Dunnen J, Driessen NN, Ummels R, Pak M, Nigou J, Larrouy-Maumus G, Gurcha SS, Movahedzadeh F, Geurtsen J, Brown EJ, Eysink Smeets MM, Besra GS, Willemsen PT, Lowary TL, van Kooyk Y, Maaskant JJ, Stoker NG, van der Ley P, Puzo G, Vandenbroucke-Grauls CM, Wieland CW, van der Poll T, Geijtenbeek TB, van der Sar AM and Bitter W. The mannose cap of mycobacterial lipoarabinomannan does not dominate the Mycobacterium-host interaction. Cell Microbiol 2008; 10: 930-944.
47. [47] Zhang CY, Bai N, Zhang ZH, Liang N, Dong L, Xiang R and Liu CH. TLR2 signaling subpathways regulate TLR9 signaling for the effective induction of IL-12 upon stimulation by heat-killed Brucella abortus. Cell Mol Immunol 2012; 9: 324-333.
48. [48] Jarnicki AG, Conroy H, Brereton C, Donnelly G, Toomey D, Walsh K, Sweeney C, Leavy O, Fletcher J, Lavelle EC, Dunne P and Mills KH. Attenuating regulatory T cell induction by TLR agonists through inhibition of p38 MAPK signaling in dendritic cells enhances their efficacy as vaccine adjuvants and cancer immunotherapeutics. J Immunol 2008; 180: 3797-3806.