MicroRNA-181b regulates ALX/FPR2 receptor expression and proresolution signaling in human macrophages

Journal of Biological Chemistry

Volumn 290, Issue 6, 2015, Pages 3592-3600

  Pierdomenico, Anna Maria ^a   Recchiuti, Antonio ^a   Simiele, Felice ^a   Codagnone, Marilina ^a   Mari, Veronica Cecilia ^a   Davì, Giovanni ^a   Romano, Mario ^a  

^a UNIVERSITY OF CHIETI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; GENE EXPRESSION; MACROPHAGES;

ANTI-INFLAMMATORIES; HUMAN MACROPHAGES; IMMUNE RESPONSE; MICRORNAS; RECEPTOR EXPRESSION;

GENE EXPRESSION REGULATION;

FORMYLPEPTIDE RECEPTOR LIKE 1; LIPOXIN A; MICRORNA; MICRORNA 181B; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; DOCOSAHEXAENOIC ACID; FORMYLPEPTIDE RECEPTOR; FPR2 PROTEIN, HUMAN; LIPOXIN; LIPOXIN RECEPTOR; MIRN181 MICRORNA, HUMAN; RESOLVIN D1;

3' UNTRANSLATED REGION; ARTICLE; CELL DIFFERENTIATION; COMPUTER MODEL; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; MONOCYTE; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN RNA BINDING; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; DOCOSAHEXAENOIC ACIDS; HUMANS; LIPOXINS; MACROPHAGES; MICRORNAS; PHAGOCYTOSIS; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, LIPOXIN; SIGNAL TRANSDUCTION;

EID: 84922454171     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.592352     Document Type: Article

References (54)

1. Serhan, C. N., Brain, S. D., Buckley, C. D., Gilroy, D. W., Haslett, C., O'Neill, L. A., Perretti, M., Rossi, A. G., and Wallace, J. L. (2007) Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21, 325-332.
2. Alessandri, A. L., Sousa, L. P., Lucas, C. D., Rossi, A. G., Pinho, V., and Teixeira, M. M. (2013) Resolution of inflammation: mechanisms and opportunity for drug development. Pharmacol. Ther. 139, 189-212.
3. Shimizu, T. (2009) Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 49, 123-150.
4. Romano, M. (2010) Lipoxin and aspirin-triggered lipoxins. Scientific- World Journal 10, 1048-1064.
5. Serhan, C. N., Hamberg, M., and Samuelsson, B. (1984) Trihydroxytetraenes: A novel series of compounds formed from arachidonic acid in human leukocytes. Biochem. Biophys. Res. Commun. 118, 943-949.
6. Levy, B. D., Clish, C. B., Schmidt, B., Gronert, K., and Serhan, C. N. (2001) Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2, 612-619.
7. Romano, M., Chen, X. S., Takahashi, Y., Yamamoto, S., Funk, C. D., and Serhan, C. N. (1993) Lipoxin synthase activity of human platelet 12-lipoxygenase. Biochem. J. 296, 127-133.
8. Romano, M., Recchia, I., and Recchiuti, A. (2007) Lipoxin receptors. Scientific World Journal 7, 1393-1412.
9. Maderna, P., and Godson, C. (2009) Lipoxins: resolutionary road. Br. J. Pharmacol. 158, 947-959.
10. Clària, J., and Serhan, C. N. (1995) Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc. Natl. Acad. Sci. U.S.A. 92, 9475-9479.
11. Perretti, M., Chiang, N., La, M., Fierro, I. M., Marullo, S., Getting, S. J., Solito, E., and Serhan, C. N. (2002) Endogenous lipid- And peptide-derived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin A4 receptor. Nat. Med. 8, 1296-1302.
12. Morris, T., Stables, M., Hobbs, A., de Souza, P., Colville-Nash, P., Warner, T., Newson, J., Bellingan, G., and Gilroy, D. W. (2009) Effects of low-dose aspirin on acute inflammatory responses in humans. J. Immunol. 183, 2089-2096.
13. Fiore, S., Maddox, J. F., Perez, H. D., and Serhan, C. N. (1994) Identification of a human cDNA encoding a functional high affinity lipoxin A4 receptor. J. Exp. Med. 180, 253-260.
14. Devchand, P. R., Arita, M., Hong, S., Bannenberg, G., Moussignac, R. L., Gronert, K., and Serhan, C. N. (2003) Human ALX receptor regulates neutrophil recruitment in transgenic mice: roles in inflammation and host defense. FASEB J. 17, 652-659.
15. Krishnamoorthy, S., Recchiuti, A., Chiang, N., Yacoubian, S., Lee, C. H., Yang, R., Petasis, N. A., and Serhan, C. N. (2010) Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc. Natl. Acad. Sci. U.S.A. 107, 1660-1665.
16. Krishnamoorthy, S., Recchiuti, A., Chiang, N., Fredman, G., and Serhan, C. N. (2012) Resolvin D1 receptor stereoselectivity and regulation of inflammation and proresolving microRNAs. Am. J. Pathol. 180, 2018-2027.
17. Dufton, N., Hannon, R., Brancaleone, V., Dalli, J., Patel, H. B., Gray, M., D'Acquisto, F., Buckingham, J. C., Perretti, M., and Flower, R. J. (2010) Anti-inflammatory role of the murine formyl-peptide receptor 2: ligandspecific effects on leukocyte responses and experimental inflammation. J. Immunol. 184, 2611-2619.
18. Norling, L. V., Dalli, J., Flower, R. J., Serhan, C. N., and Perretti, M. (2012) Resolvin D1 limits polymorphonuclear leukocyte recruitment to inflammatory loci: receptor-dependent actions. Arterioscler. Thromb. Vasc. Biol. 32, 1970-1978.
19. Morris, T., Stables, M., Colville-Nash, P., Newson, J., Bellingan, G., de Souza, P. M., and Gilroy, D. W. (2010) Dichotomy in duration and severity of acute inflammatory responses in humans arising from differentially expressed proresolution pathways. Proc. Natl. Acad. Sci. U.S.A. 107, 8842-8847.
20. Levy, B. D., Bonnans, C., Silverman, E. S., Palmer, L. J., Marigowda, G., and Israel, E. (2005) Diminished lipoxin biosynthesis in severe asthma. Am. J. Respir. Crit. Care Med. 172, 824-830.
21. Planagumà, A., Kazani, S., Marigowda, G., Haworth, O., Mariani, T. J., Israel, E., Bleecker, E. R., Curran-Everett, D., Erzurum, S. C., Calhoun, W. J., Castro, M., Chung, K. F., Gaston, B., Jarjour, N. N., Busse, W. W., Wenzel, S. E., and Levy, B. D. (2008) Airway lipoxin A4 generation and lipoxin A4 receptor expression are decreased in severe asthma. Am. J. Respir. Crit. Care Med. 178, 574-582.
22. Barnig, C., Cernadas, M., Dutile, S., Liu, X., Perrella, M. A., Kazani, S., Wechsler, M. E., Israel, E., and Levy, B. D. (2013) Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci. Transl. Med. 5, 174ra26.
23. Karp, C. L., Flick, L. M., Park, K. W., Softic, S., Greer, T. M., Keledjian, R., Yang, R., Uddin, J., Guggino, W. B., Atabani, S. F., Belkaid, Y., Xu, Y., Whitsett, J. A., Accurso, F. J., Wills-Karp, M., and Petasis, N. A. (2004) Defective lipoxin-mediated anti-inflammatory activity in the cystic fibrosis airway. Nat. Immunol. 5, 388-392.
24. Bensalem, N., Ventura, A. P., Vallée, B., Lipecka, J., Tondelier, D., Davezac, N., Dos Santos, A., Perretti, M., Fajac, A., Sermet-Gaudelus, I., Renouil, M., Lesure, J. F., Halgand, F., Laprévote, O., and Edelman, A. (2005) Downregulation of the anti-inflammatory protein annexin A1 in cystic fibrosis knock-out mice and patients. Mol. Cell. Proteomics 4, 1591-1601.
25. Mattoscio, D., Evangelista, V., De Cristofaro, R., Recchiuti, A., Pandolfi, A., Di Silvestre, S., Manarini, S., Martelli, N., Rocca, B., Petrucci, G., Angelini, D. F., Battistini, L., Robuffo, I., Pensabene, T., Pieroni, L., Furnari, M. L., Pardo, F., Quattrucci, S., Lancellotti, S., Davì, G., and Romano, M. (2010) Cystic fibrosis transmembrane conductance regulator (CFTR) expression in human platelets: impact on mediators and mechanisms of the inflammatory response. FASEB J. 24, 3970-3980.
26. Ringholz, F. C., Buchanan, P. J., Clarke, D. T., Millar, R. G., McDermott, M., Linnane, B., Harvey, B. J., McNally, P., and Urbach, V. (2014) Reduced 15-lipoxygenase 2 and lipoxin A4/leukotriene B4 ratio in children with cystic fibrosis. Eur. Respir. J. 44, 394-404.
27. Kosicka, A., Cunliffe, A. D., Mackenzie, R., Zariwala, M. G., Perretti, M., Flower, R. J., and Renshaw, D. (2013) Attenuation of plasma annexin A1 in human obesity. FASEB J. 27, 368-378.
28. Ho, K. J., Spite, M., Owens, C. D., Lancero, H., Kroemer, A. H., Pande, R., Creager, M. A., Serhan, C. N., and Conte, M. S. (2010) Aspirin-triggered lipoxin and resolvin e1 modulate vascular smooth muscle phenotype and correlate with peripheral atherosclerosis. Am. J. Pathol. 177, 2116-2123.
29. Simiele, F., Recchiuti, A., Mattoscio, D., De Luca, A., Cianci, E., Franchi, S., Gatta, V., Parolari, A., Werba, J. P., Camera, M., Favaloro, B., and Romano, M. (2012) Transcriptional regulation of the human FPR2/ALX gene: evidence of a heritable genetic variant that impairs promoter activity. FASEB J. 26, 1323-1333.
30. Lee, R. C., Feinbaum, R. L., and Ambros, V. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854.
31. Lau, N. C., Lim, L. P., Weinstein, E. G., and Bartel, D. P. (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858-862.
32. Baek, D., Villén, J., Shin, C., Camargo, F. D., Gygi, S. P., and Bartel, D. P. (2008) The impact of microRNAs on protein output. Nature 455, 64-71.
33. Recchiuti, A., Krishnamoorthy, S., Fredman, G., Chiang, N., and Serhan, C. N. (2011) MicroRNAs in resolution of acute inflammation: identification of novel resolvin D1-miRNA circuits. FASEB J. 25, 544-560.
34. Fredman, G., Li, Y., Dalli, J., Chiang, N., and Serhan, C. N. (2012) Selflimited versus delayed resolution of acute inflammation: Aemporal regulation of pro-resolving mediators and microRNA. Sci. Rep. 2, 639.
35. Li, Y., Dalli, J., Chiang, N., Baron, R. M., Quintana, C., and Serhan, C. N. (2013) Plasticity of leukocytic exudates in resolving acute inflammation is regulated by microRNA and proresolving mediators. Immunity 39, 885-898.
36. Sheedy, F. J., Palsson-McDermott, E., Hennessy, E. J., Martin, C., O'Leary, J. J., Ruan, Q., Johnson, D. S., Chen, Y., and O'Neill, L. A. (2010) Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat. Immunol. 11, 141-147.
37. Brennan, E. P., Nolan, K. A., Börgeson, E., Gough, O. S., McEvoy, C. M., Docherty, N. G., Higgins, D. F., Murphy, M., Sadlier, D. M., Ali-Shah, S. T., Guiry, P. J., Savage, D. A., Maxwell, A. P., Martin, F., Godson, C., and GENIE Consortium (2013) Lipoxins attenuate renal fibrosis by inducing let-7c and suppressing TGFβR1. J. Am. Soc. Nephrol. 24, 627-637.
38. Visone, R., Veronese, A., Rassenti, L. Z., Balatti, V., Pearl, D. K., Acunzo, M., Volinia, S., Taccioli, C., Kipps, T. J., and Croce, C. M. (2011) miR-181b is a biomarker of disease progression in chronic lymphocytic leukemia. Blood 118, 3072-3079.
39. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-Ct method. Methods 25, 402-408.
40. Recchiuti, A., Codagnone, M., Pierdomenico, A. M., Rossi, C., Mari, V. C., Cianci, E., Simiele, F., Gatta, V., and Romano, M. (2014) Immunoresolving actions of oral resolvin D1 include selective regulation of the transcription machinery in resolution-phase mouse macrophages. FASEB J. 28, 3090-3102.
41. Sheedy, F. J., and O'Neill, L. A. (2008) Adding fuel to fire: microRNAs as a new class of mediators of inflammation. Ann. Rheum. Dis. 67, iii50-iii5.
42. Kozomara, A., and Griffiths-Jones, S. (2014) miRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42, D68-D73.
43. Iliopoulos, D., Jaeger, S. A., Hirsch, H. A., Bulyk, M. L., and Struhl, K. (2010) STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol. Cell. 39, 493-506.
44. Ma, X., Becker Buscaglia, L. E., Barker, J. R., and Li, Y. (2011) MicroRNAs in NF-κB signaling. J. Mol. Cell. Biol. 3, 159-166.
45. Sun, X., Icli, B., Wara, A. K., Belkin, N., He, S., Kobzik, L., Hunninghake, G. M., Vera, M. P., MICU, Registry, Blackwell, T. S., Baron, R. M., and Feinberg, M. W. (2012) MicroRNA-181b regulates NF-κB-mediated vascular inflammation. J. Clin. Invest. 122, 1973-1990.
46. Shi, Z. M., Wang, X. F., Qian, X., Tao, T., Wang, L., Chen, Q. D., Wang, X. R., Cao, L., Wang, Y. Y., Zhang, J. X., Jiang, T., Kang, C. S., Jiang, B. H., Liu, N., and You, Y. P. (2013) MiRNA-181b suppresses IGF-1R and functions as a tumor suppressor gene in gliomas. RNA 19, 552-560.
47. Wu, S. H., Chen, X. Q., Liu, B., Wu, H. J., and Dong, L. (2013) Efficacy and safety of 15(R/S)-methyl-lipoxin A(4) in topical treatment of infantile eczema. Br. J. Dermatol. 168, 172-178.
48. Li, S., Moffett, H. F., Lu, J., Werner, L., Zhang, H., Ritz, J., Neuberg, D., Wucherpfennig, K. W., Brown, J. R., and Novina, C. D. (2011) MicroRNA expression profiling identifies activated B cell status in chronic lymphocytic leukemia cells. PLoS ONE 6, e16956.
49. Visone, R., Veronese, A., Balatti, V., and Croce, C. M. (2012) MiR-181b: new perspective to evaluate disease progression in chronic lymphocytic leukemia. Oncotarget 3, 195-202.
50. Wang, B., Li, W., Guo, K., Xiao, Y., Wang, Y., and Fan, J. (2012) miR-181b promotes hepatic stellate cells proliferation by targeting p27 and is elevated in the serum of cirrhosis patients. Biochem. Biophys. Res. Commun. 421, 4-8.
51. Chen, Y. J., Zhu, J. M., Wu, H., Fan, J., Zhou, J., Hu, J., Yu, Q., Liu, T. T., Yang, L., Wu, C. L., Guo, X. L., Huang, X. W., and Shen, X. Z. (2013) Circulating microRNAs as a fingerprint for liver cirrhosis. PLoS ONE 8, e66577.
52. Song, J., Lee, M., Kim, D., Han, J., Chun, C. H., and Jin, E. J. (2013) MicroRNA- 181b regulates articular chondrocytes differentiation and cartilage integrity. Biochem. Biophys. Res. Commun. 431, 210-214.
53. Lee, Y. H., Na, H. S., Jeong, S. Y., Jeong, S. H., Park, H. R., and Chung, J. (2011) Comparison of inflammatory microRNA expression in healthy and periodontitis tissues. Biocell 35, 43-49.
54. Peng, Z., Li, J., Li, Y., Yang, X., Feng, S., Han, S., and Li, J. (2013) Downregulation of miR-181b in mouse brain following ischemic stroke induces neuroprotection against ischemic injury through targeting heat shock protein A5 and ubiquitin carboxyl-terminal hydrolase isozyme L1. J. Neurosci. Res. 91, 1349-1362.