MicroRNA-33 regulates the innate immune response via ATP binding cassette transporter-mediated remodeling of membrane microdomains

Journal of Biological Chemistry

Volumn 291, Issue 37, 2016, Pages 19651-19660

  Lai, Lihua ^a   Azzam, Kathleen M ^a   Lin, Wan Chi ^a   Rai, Prashant ^a   Lowe, Julie M ^a   Gabor, Kristin A ^a   Madenspacher, Jennifer H ^a   Madenspacher, Jim J Aloor ^a   Parks, John S ^b   Näär, Anders M ^c,d   Fessler, Michael B ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; CHOLESTEROL; CROSSTALK; GENE ENCODING; GENES; IMMUNE SYSTEM; INTERFERONS; MACROPHAGES; MAMMALS; PHYSIOLOGY; RNA;

ATP BINDING CASSETTE TRANSPORTERS; ATP-BINDING CASSETTE; INNATE IMMUNE RESPONSE; MEMBRANE MICRODOMAINS; PROINFLAMMATORY CYTOKINES; PROINFLAMMATORY RESPONSE; STEROL REGULATORY ELEMENT-BINDING PROTEINS; TOLL-LIKE RECEPTORS;

GENE EXPRESSION;

ABC TRANSPORTER A1; ABC TRANSPORTER G1; BETA INTERFERON; CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; LIGAND; LIPOPOLYSACCHARIDE; LIVER X RECEPTOR AGONIST; MICRORNA; MICRORNA 33; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; ABCA1 PROTEIN, MOUSE; ABCG1 PROTEIN, MOUSE; MIRN33 MICRORNA, MOUSE; SREBF2 PROTEIN, MOUSE; STEROL REGULATORY ELEMENT BINDING PROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL TRANSFORMATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE; GENE CONTROL; GENE FUNCTION; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; LIPID HOMEOSTASIS; LIPID RAFT; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION; SREBF 2 GENE; TRANSCRIPTION INITIATION; ANIMAL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MEMBRANE MICRODOMAIN; RAW 264.7 CELL LINE;

ANIMALS; ATP BINDING CASSETTE TRANSPORTER 1; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 1; IMMUNITY, INNATE; MACROPHAGES; MEMBRANE MICRODOMAINS; MICE; MICE, KNOCKOUT; MICRORNAS; RAW 264.7 CELLS; STEROL REGULATORY ELEMENT BINDING PROTEIN 2;

EID: 84986890507     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.723056     Document Type: Article

References (59)

1. Kozomara, A., and Griffiths-Jones, S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, D152-D157
2. Pasquinelli, A. E. (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat. Rev. Genet. 13, 271-282
3. O'Neill, L. A., Sheedy, F. J., and McCoy, C. E. (2011) MicroRNAs: the fine-tuners of Toll-like receptor signalling. Nat. Rev. Immunol. 11, 163-175
4. Quinn, S. R., and O'Neill, L. A. (2011) A trio of microRNAs that control Toll-like receptor signalling. Int. Immunol. 23, 421-425
5. Taganov, K. D., Boldin, M. P., Chang, K. J., and Baltimore, D. (2006) NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U.S.A. 103, 12481-12486
6. Tang, B., Xiao, B., Liu, Z., Li, N., Zhu, E. D., Li, B. S., Xie, Q. H., Zhuang, Y., Zou, Q. M., and Mao, X. H. (2010) Identification of MyD88 as a novel target of miR-155, involved in negative regulation of Helicobacter pyloriinduced inflammation. FEBS Lett. 584, 1481-1486
7. Huang, R. S., Hu, G. Q., Lin, B., Lin, Z. Y., and Sun, C. C. (2010) MicroRNA-155 silencing enhances inflammatory response and lipid uptake in oxidized low-density lipoprotein-stimulated human THP-1 macrophages. J. Investig. Med. 58, 961-967
8. Ceppi, M., Pereira, P. M., Dunand-Sauthier, I., Barras, E., Reith, W., Santos, M. A., and Pierre, P. (2009) MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 106, 2735-2740
9. Rayner, K. J., Suárez, Y., Dávalos, A., Parathath, S., Fitzgerald, M. L., Tamehiro, N., Fisher, E. A., Moore, K. J., and Fernández-Hernando, C. (2010) MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328, 1570-1573
10. Najafi-Shoushtari, S. H., Kristo, F., Li, Y., Shioda, T., Cohen, D. E., Gerszten, R. E., and Näär, A. M. (2010) MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328, 1566-1569
11. Marquart, T. J., Allen, R. M., Ory, D. S., and Baldán, A. (2010) miR-33 links SREBP-2 induction to repression of sterol transporters. Proc. Natl. Acad. Sci. U.S.A. 107, 12228-12232
12. Zhu, X., Owen, J. S., Wilson, M. D., Li, H., Griffiths, G. L., Thomas, M. J., Hiltbold, E. M., Fessler, M. B., and Parks, J. S. (2010) Macrophage ABCA1 reduces MyD88-dependent Toll-like receptor trafficking to lipid rafts by reduction of lipid raft cholesterol. J. Lipid Res. 51, 3196-3206
13. Yvan-Charvet, L., Welch, C., Pagler, T. A., Ranalletta, M., Lamkanfi, M., Han, S., Ishibashi, M., Li, R., Wang, N., and Tall, A. R. (2008) Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation 118, 1837-1847
14. Zhao, G. J., Tang, S. L., Lv, Y. C., Ouyang, X. P., He, P. P., Yao, F., Tang, Y. Y., Zhang, M., Tang, Y. L., Tang, D. P., Cayabyab, F. S., Tian, G. P., and Tang, C. K. (2014) NF-κB suppresses the expression of ATP-binding cassette transporter A1/G1 by regulating SREBP-2 and miR-33a in mice. Int. J. Cardiol. 171, e93- e95
15. Li, L. C., Varghese, Z., Moorhead, J. F., Lee, C. T., Chen, J. B., and Ruan, X. Z. (2013) Cross-talk between TLR4-MyD88-NF-κB and SCAP-SREBP2 pathways mediates macrophage foam cell formation. Am. J. Physiol. Heart Circ. Physiol. 304, H874-H884
16. Park, Y., Pham, T. X., and Lee, J. (2012) Lipopolysaccharide represses the expression of ATP-binding cassette transporter G1 and scavenger receptor class B, type I in murine macrophages. Inflamm. Res. 61, 465-472
17. Jeon, T. I., and Osborne, T. F. (2012) SREBPs: metabolic integrators in physiology and metabolism. Trends Endocrinol. Metab. 23, 65-72
18. O'Neill, L. A., and Bowie, A. G. (2007) The family of five: TIR-domaincontaining adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7, 353-364
19. Park, K., and Scott, A. L. (2010) Cholesterol 25-hydroxylase production by dendritic cells and macrophages is regulated by type I interferons. J. Leukoc. Biol. 88, 1081-1087
20. Diczfalusy, U., Olofsson, K. E., Carlsson, A. M., Gong, M., Golenbock, D. T., Rooyackers, O., Fläring, U., and Björkbacka, H. (2009) Marked upregulation of cholesterol 25-hydroxylase expression by lipopolysaccharide. J. Lipid Res. 50, 2258-2264
21. Cyster, J. G., Dang, E. V., Reboldi, A., and Yi, T. (2014) 25-Hydroxycholesterols in innate and adaptive immunity. Nat. Rev. Immunol. 14, 731-743
22. Caruso, R., Warner, N., Inohara, N., and Núñez, G. (2014) NOD1 and NOD2: signaling, host defense, and inflammatory disease. Immunity 41, 898-908
23. Iwaki, D., Mitsuzawa, H., Murakami, S., Sano, H., Konishi, M., Akino, T., and Kuroki, Y. (2002) The extracellular toll-like receptor 2 domain directly binds peptidoglycan derived from Staphylococcus aureus. J. Biol. Chem. 277, 24315-24320
24. Nilsen, N. J., Vladimer, G. I., Stenvik, J., Orning, M. P., Zeid-Kilani, M. V., Bugge, M., Bergstroem, B., Conlon, J., Husebye, H., Hise, A. G., Fitzgerald, K. A., Espevik, T., and Lien, E. (2015) A role for the adaptor proteins TRAM and TRIF in toll-like receptor 2 signaling. J. Biol. Chem. 290, 3209-3222
25. Zhu, X., Lee, J. Y., Timmins, J. M., Brown, J. M., Boudyguina, E., Mulya, A., Gebre, A. K., Willingham, M. C., Hiltbold, E. M., Mishra, N., Maeda, N., and Parks, J. S. (2008) Increased cellular free cholesterol in macrophagespecific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J. Biol. Chem. 283, 22930-22941
26. Triantafilou, M., Miyake, K., Golenbock, D. T., and Triantafilou, K. (2002) Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 115, 2603-2611
27. Schmitz, G., and Langmann, T. (2005) Transcriptional regulatory networks in lipid metabolism control ABCA1 expression. Biochim. Biophys. Acta 1735, 1-19
28. Smoak, K., Madenspacher, J., Jeyaseelan, S., Williams, B., Dixon, D., Poch, K. R., Nick, J. A., Worthen, G. S., and Fessler, M. B. (2008) Effects of liver X receptor agonist treatment on pulmonary inflammation and host defense. J. Immunol. 180, 3305-3312
29. Ghisletti, S., Huang, W., Ogawa, S., Pascual, G., Lin, M. E., Willson, T. M., Rosenfeld, M. G., and Glass, C. K. (2007) Parallel SUMOylation-dependent pathways mediate gene- and signal-specific transrepression by LXRs and PPARγ. Mol. Cell 25, 57-70
30. Tili, E., Michaille, J. J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., Fabbri, M., Alder, H., Liu, C. G., Calin, G. A., and Croce, C. M. (2007) Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-α stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 179, 5082-5089
31. O'Connell, R. M., Taganov, K. D., Boldin, M. P., Cheng, G., and Baltimore, D. (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. U.S.A. 104, 1604-1609
32. Liu, G., Friggeri, A., Yang, Y., Park, Y. J., Tsuruta, Y., and Abraham, E. (2009) miR-147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc. Natl. Acad. Sci. U.S.A. 106, 15819-15824
33. Ma, L., Dong, F., Zaid, M., Kumar, A., and Zha, X. (2012) ABCA1 protein enhances Toll-like receptor 4 (TLR4)-stimulated interleukin-10 (IL-10) secretion through protein kinase A (PKA) activation. J. Biol. Chem. 287, 40502-40512
34. Distel, E., Barrett, T. J., Chung, K., Girgis, N. M., Parathath, S., Essau, C. C., Murphy, A. J., Moore, K. J., and Fisher, E. A. (2014) miR33 inhibition overcomes deleterious effects of diabetes mellitus on atherosclerosis plaque regression in mice. Circ. Res. 115, 759-769
35. Ouimet, M., Ediriweera, H. N., Gundra, U. M., Sheedy, F. J., Ramkhelawon, B., Hutchison, S. B., Rinehold, K., van Solingen, C., Fullerton, M. D., Cecchini, K., Rayner, K. J., Steinberg, G. R., Zamore, P. D., Fisher, E. A., Loke, P., et al. (2015) MicroRNA-33-dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis. J. Clin. Investig. 125, 4334- 4348
36. Rayner, K. J., Sheedy, F. J., Esau, C. C., Hussain, F. N., Temel, R. E., Parathath, S., van Gils, J. M., Rayner, A. J., Chang, A. N., Suarez, Y., Fernandez-Hernando, C., Fisher, E. A., and Moore, K. J. (2011) Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J. Clin. Investig. 121, 2921-2931
37. Rayner, K. J., Esau, C. C., Hussain, F. N., McDaniel, A. L., Marshall, S. M., van Gils, J. M., Ray, T. D., Sheedy, F. J., Goedeke, L., Liu, X., Khatsenko, O. G., Kaimal, V., Lees, C. J., Fernandez-Hernando, C., Fisher, E. A., et al. (2011) Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 478, 404- 407
38. Azzam, K. M., and Fessler, M. B. (2012) Crosstalk between reverse cholesterol transport and innate immunity. Trends Endocrinol. Metab. 23, 169-178
39. Yvan-Charvet, L., Pagler, T., Gautier, E. L., Avagyan, S., Siry, R. L., Han, S., Welch, C. L., Wang, N., Randolph, G. J., Snoeck, H. W., and Tall, A. R. (2010) ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 328, 1689-1693
40. Li, Y., Schwabe, R. F., DeVries-Seimon, T., Yao, P. M., Gerbod-Giannone, M. C., Tall, A. R., Davis, R. J., Flavell, R., Brenner, D. A., and Tabas, I. (2005) Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-α and interleukin-6: model of NF-κB- and MAP kinasedependent inflammation in advanced atherosclerosis. J. Biol. Chem. 280, 21763-21772
41. Duewell, P., Kono, H., Rayner, K. J., Sirois, C. M., Vladimer, G., Bauernfeind, F. G., Abela, G. S., Franchi, L., Nuñez, G., Schnurr, M., Espevik, T., Lien, E., Fitzgerald, K. A., Rock, K. L., Moore, K. J., et al. (2010) NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361
42. Ramirez, C. M., Dávalos, A., Goedeke, L., Salerno, A. G., Warrier, N., Cirera-Salinas, D., Suárez, Y., and Fernández-Hernando, C. (2011) MicroRNA-758 regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Arterioscler. Thromb. Vasc. Biol. 31, 2707-2714
43. Sun, D., Zhang, J., Xie, J., Wei, W., Chen, M., and Zhao, X. (2012) MiR-26 controls LXR-dependent cholesterol efflux by targeting ABCA1 and ARL7. FEBS Lett. 586, 1472-1479
44. Kim, J., Yoon, H., Ramírez, C. M., Lee, S. M., Hoe, H. S., Fernández-Hernando, C., and Kim, J. (2012) MiR-106b impairs cholesterol efflux and increases Aβ levels by repressing ABCA1 expression. Exp. Neurol. 235, 476- 483
45. Wang, D., Xia, M., Yan, X., Li, D., Wang, L., Xu, Y., Jin, T., and Ling, W. (2012) Gut microbiota metabolism of anthocyanin promotes reverse cholesterol transport in mice via repressing miRNA-10b. Circ. Res. 111, 967-981
46. de Aguiar Vallim, T. Q., Tarling, E. J., Kim, T., Civelek, M., Baldán, Á., Esau, C., and Edwards, P. A. (2013) MicroRNA-144 regulates hepatic ATP binding cassette transporter A1 and plasma high-density lipoprotein after activation of the nuclear receptor farnesoid X receptor. Circ. Res. 112, 1602-1612
47. Ramírez, C. M., Rotllan, N., Vlassov, A. V., Dávalos, A., Li, M., Goedeke, L., Aranda, J. F., Cirera-Salinas, D., Araldi, E., Salerno, A., Wanschel, A., Zavadil, J., Castrillo, A., Kim, J., Suárez, Y., et al. (2013) Control of cholesterol metabolism and plasma high-density lipoprotein levels by microRNA-144. Circ. Res. 112, 1592-1601
48. Zhang, N., Lei, J., Lei, H., Ruan, X., Liu, Q., Chen, Y., and Huang, W. (2015) MicroRNA-101 overexpression by IL-6 and TNF-α inhibits cholesterol efflux by suppressing ATP-binding cassette transporter A1 expression. Exp. Cell Res. 336, 33-42
49. Fu, Y., Zhou, E., Wei, Z., Wang, W., Wang, T., Yang, Z., and Zhang, N. (2014) Cyanidin-3-O-β-glucoside ameliorates lipopolysaccharide-induced acute lung injury by reducing TLR4 recruitment into lipid rafts. Biochem. Pharmacol. 90, 126-134
50. Herrera-Merchan, A., Cerrato, C., Luengo, G., Dominguez, O., Piris, M. A., Serrano, M., and Gonzalez, S. (2010) miR-33-mediated downregulation of p53 controls hematopoietic stem cell self-renewal. Cell Cycle 9, 3277-3285
51. Madenspacher, J. H., Azzam, K. M., Gowdy, K. M., Malcolm, K. C., Nick, J. A., Dixon, D., Aloor, J. J., Draper, D. W., Guardiola, J. J., Shatz, M., Menendez, D., Lowe, J., Lu, J., Bushel, P., Li, L., et al. (2013) p53 integrates host defense and cell fate during bacterial pneumonia. J. Exp. Med. 210, 891-904
52. Komarova, E. A., Krivokrysenko, V., Wang, K., Neznanov, N., Chernov, M. V., Komarov, P. G., Brennan, M. L., Golovkina, T. V., Rokhlin, O. W., Kuprash, D. V., Nedospasov, S. A., Hazen, S. L., Feinstein, E., and Gudkov, A. V. (2005) p53 is a suppressor of inflammatory response in mice. FASEB J. 19, 1030-1032
53. Ho, P. C., Chang, K. C., Chuang, Y. S., and Wei, L. N. (2011) Cholesterol regulation of receptor-interacting protein 140 via microRNA-33 in inflammatory cytokine production. FASEB J. 25, 1758-1766
54. Allen, R. M., Marquart, T. J., Albert, C. J., Suchy, F. J., Wang, D. Q., Ananthanarayanan, M., Ford, D. A., and Baldán, A. (2012) miR-33 controls the expression of biliary transporters, and mediates statin- and diet-induced hepatotoxicity. EMBO Mol. Med. 4, 882- 895
55. Doan, J. E., Windmiller, D. A., and Riches, D. W. (2004) Differential regulation of TNF-R1 signaling: lipid raft dependency of p42MAPK/ERK2 activation, but not NF-κB activation. J. Immunol. 172, 7654-7660
56. Draper, D. W., Gowdy, K. M., Madenspacher, J. H., Wilson, R. H., Whitehead, G. S., Nakano, H., Pandiri, A. R., Foley, J. F., Remaley, A. T., Cook, D. N., and Fessler, M. B. (2012) ATP binding cassette transporter G1 deletion induces IL-17-dependent dysregulation of pulmonary adaptive immunity. J. Immunol. 188, 5327-5336
57. Smoak, K. A., Aloor, J. J., Madenspacher, J., Merrick, B. A., Collins, J. B., Zhu, X., Cavigiolio, G., Oda, M. N., Parks, J. S., and Fessler, M. B. (2010) Myeloid differentiation primary response protein 88 couples reverse cholesterol transport to inflammation. Cell Metab. 11, 493-502
58. Bauman, D. R., Bitmansour, A. D., McDonald, J. G., Thompson, B. M., Liang, G., and Russell, D. W. (2009) 25-Hydroxycholesterol secreted by macrophages in response to Toll-like receptor activation suppresses immunoglobulin A production. Proc. Natl. Acad. Sci. U.S.A. 106, 16764-16769
59. Blanc, M., Hsieh, W. Y., Robertson, K. A., Watterson, S., Shui, G., Lacaze, P., Khondoker, M., Dickinson, P., Sing, G., Rodríguez-Martín, S., Phelan, P., Forster, T., Strobl, B., Müller, M., Riemersma, R., et al. (2011) Host defense against viral infection involves interferon mediated down-regulation of sterol biosynthesis. PLoS Biol. 9, e1000598