An Interferon Regulated MicroRNA Provides Broad Cell-Intrinsic Antiviral Immunity through Multihit Host-Directed Targeting of the Sterol Pathway

PLoS Biology

Volumn 14, Issue 3, 2016, Pages

  Robertson, Kevin A ^a   Hsieh, Wei Yuan ^a   Forster, Thorsten ^a   Blanc, Mathieu ^a,b   Lu, Hongjin ^a   Crick, Peter J ^c   Yutuc, Eylan ^c   Watterson, Steven ^a,d   Martin, Kimberly ^a,e   Griffiths, Samantha J ^a   Enright, Anton J ^f   Yamamoto, Mami ^a   Pradeepa, Madapura M ^g   Lennox, Kimberly A ^h   Behlke, Mark A ^h   Talbot, Simon ^a   Haas, Jürgen ^a   Dölken, Lars ^i,j   Griffiths, William J ^c   Wang, Yuqin ^c   Angulo, Ana ^k,l   Ghazal, Peter ^a   more..

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b EPFL   (Switzerland)

^c SWANSEA UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF ULSTER   (United Kingdom)

^e Centre for Integrative Physiology   (United Kingdom)

^f WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^g WESTERN GENERAL HOSPITAL   (United Kingdom)

^h INTEGRATED DNA TECHNOLOGIES   (United States)

ⁱ UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^j UNIVERSITY OF WÜRZBURG   (Germany)

^k INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^l UNIVERSITY OF BARCELONA   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; GAMMA INTERFERON; INTERFERON; INTERFERON REGULATORY FACTOR 1; MEVALONIC ACID; MICRORNA; MICRORNA 33; MICRORNA 342 5P; STEROL; UNCLASSIFIED DRUG; IRF1 PROTEIN, MOUSE; MIRN342 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOMEGALOVIRUS INFECTION; ENZYME ASSAY; FIBROBLAST; GENE; GENETIC TRANSCRIPTION; HERPES SIMPLEX VIRUS 1; HOST RESISTANCE; HUMAN CYTOMEGALOVIRUS; IDI1 GENE; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A VIRUS (H1N1); LIPIDOMICS; MACROPHAGE ACTIVATION; MOUSE; MURINE CYTOMEGALOVIRUS; NONHUMAN; RNA METABOLISM; RNA SYNTHESIS; SC4MOL GENE; SREBF2 GENE; STEROL SYNTHESIS; VIRUS IMMUNITY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIRUS INFECTION;

ANIMALS; INTERFERON REGULATORY FACTOR-1; INTERFERONS; MICE, INBRED C57BL; MICRORNAS; STEROLS; VIRUS DISEASES;

EID: 84962142408     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002364     Document Type: Article

References (72)

1. Karlikow M, Goic B, Saleh M, RNAi and antiviral defense in Drosophila: Setting up a systemic immune response. Developmental and Comparative Immunology. 2014;42(1):85–92. doi: 10.1016/j.dci.2013.05.004 WOS:000328174200010. 23684730
2. Szittya G, Burgyan J, Cullen B, RNA Interference-Mediated Intrinsic Antiviral Immunity in Plants. Intrinsic Immunity. 2013;371:153–81. doi: 10.1007/978-3-642-37765-5_6 WOS:000330591400007.
3. Schoggins JW, Interferon-stimulated genes: roles in viral pathogenesis. Curr Opin Virol. 2014;6:40–6. doi: 10.1016/j.coviro.2014.03.00624713352; PubMed Central PMCID: PMCPMC4077717.
4. Sadler A, Williams B, Interferon-inducible antiviral effectors. Nature Reviews Immunology. 2008;8(7):559–68. doi: 10.1038/nri2314 WOS:000257089200016. 18575461
5. Santhakumar D, Forster T, Laqtom NN, Fragkoudis R, Dickinson P, Abreu-Goodger C, et al. Combined agonist-antagonist genome-wide functional screening identifies broadly active antiviral microRNAs. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(31):13830–5. Epub 2010/07/21. doi: 10.1073/pnas.100886110720643939; PubMed Central PMCID: PMC2922253.
6. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, et al. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature. 2007;449(7164):919–22. Epub 2007/10/19. doi: 10.1038/nature0620517943132; PubMed Central PMCID: PMC2748825.
7. Cazalla D, Yario T, Steitz J, Down-Regulation of a Host MicroRNA by a Herpesvirus saimiri Noncoding RNA. Science. 2010;328(5985):1563–6. doi: 10.1126/science.1187197 WOS:000278859200048. 20558719
8. Fu Y, Liu X, Li X, Shen Z, Yang B, Wu C, et al. MicroRNA miR-21 Attenuates Human Cytomegalovirus Replication in Neural Cells by Targeting Cdc25a. Journal of Virology. 2015;89(2):1070–82. doi: 10.1128/JVI01740-14 WOS:000347178900016. 25378484
9. Reinsbach S, Nazarov P, Philippidou D, Schmitt M, Wienecke-Baldacchino A, Muller A, et al. Dynamic regulation of microRNA expression following interferon gamma-induced gene transcription. Rna Biology. 2012;9(7):978–89. doi: 10.4161/rna.20494 WOS:000307078700009. 22767256
10. van der Ree M, van der Meer A, de Bruijne J, Maan R, van Vliet A, Welzel T, et al. Long-term safety and efficacy of microRNA-targeted therapy in chronic hepatitis C patients. Antiviral Research. 2014;111:53–9. doi: 10.1016/j.antiviral.2014.08.015 WOS:000345185100009. 25218783
11. Wang P, Hou J, Lin L, Wang C, Liu X, Li D, et al. Inducible microRNA-155 Feedback Promotes Type I IFN Signaling in Antiviral Innate Immunity by Targeting Suppressor of Cytokine Signaling 1. Journal of Immunology. 2010;185(10):6226–33. doi: 10.4049/jimmunol.1000491 WOS:000283848000061.
12. Ghazal P, Armas J, Garcia-Ramirez J, Kurz S, Angulo A, Viruses: Hostages to the cell. Virology. 2000;275(2):233–7. doi: 10.1006/viro.2000.0553 WOS:000089697900002. 10998321
13. Schoggins JW, Randall G, Lipids in innate antiviral defense. Cell Host Microbe. 2013;14(4):379–85. Epub 2013/10/22. doi: 10.1016/j.chom.2013.09.01024139397
14. del Real G, Jimenez-Baranda S, Mira E, Lacalle RA, Lucas P, Gomez-Mouton C, et al. Statins inhibit HIV-1 infection by down-regulating Rho activity. J Exp Med. 2004;200(4):541–7. Epub 2004/08/18. doi: 10.1084/jem.2004006115314078; PubMed Central PMCID: PMC2211926.
15. Potena L, Frascaroli G, Grigioni F, Lazzarotto T, Magnani G, Tomasi L, et al. Hydroxymethyl-glutaryl coenzyme a reductase inhibition limits cytomegalovirus infection in human endothelial cells. Circulation. 2004;109(4):532–6. Epub 2004/01/28. doi: 10.1161/01.CIR.0000109485.79183.8114744969.
16. Ye J, Wang C, Sumpter R, Jr.Brown MS, Goldstein JL, Gale M, JrDisruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(26):15865–70. Epub 2003/12/12. doi: 10.1073/pnas.223723810014668447; PubMed Central PMCID: PMC307659.
17. Yu Y, Maguire TG, Alwine JC, Human cytomegalovirus infection induces adipocyte-like lipogenesis through activation of sterol regulatory element binding protein 1. Journal of virology. 2012;86(6):2942–9. Epub 2012/01/20. doi: 10.1128/JVI.06467-1122258239; PubMed Central PMCID: PMC3302344.
18. Blanc M, Hsieh WY, Robertson KA, Kropp KA, Forster T, Shui G, et al. The transcription factor STAT-1 couples macrophage synthesis of 25-hydroxycholesterol to the interferon antiviral response. Immunity. 2013;38(1):106–18. doi: 10.1016/j.immuni.2012.11.00423273843; PubMed Central PMCID: PMC3556782.
19. Rodgers M, Villareal V, Schaefer E, Peng L, Corey K, Chung R, et al. Lipid Metabolite Profiling Identifies Desmosterol Metabolism as a New Antiviral Target for Hepatitis C Virus. Journal of the American Chemical Society. 2012;134(16):6896–9. doi: 10.1021/ja207391q WOS:000303139800003. 22480142
20. Im SS, Yousef L, Blaschitz C, Liu JZ, Edwards RA, Young SG, et al. Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a. Cell metabolism. 2011;13(5):540–9. Epub 2011/05/03. doi: 10.1016/j.cmet.2011.04.00121531336; PubMed Central PMCID: PMC3090630.
21. Kidani Y, Elsaesser H, Hock MB, Vergnes L, Williams KJ, Argus JP, et al. Sterol regulatory element-binding proteins are essential for the metabolic programming of effector T cells and adaptive immunity. Nature immunology. 2013;14(5):489–99. Epub 2013/04/09. doi: 10.1038/ni.257023563690; PubMed Central PMCID: PMC3652626.
22. Seo YK, Jeon TI, Chong HK, Biesinger J, Xie X, Osborne TF, Genome-wide localization of SREBP-2 in hepatic chromatin predicts a role in autophagy. Cell metabolism. 2011;13(4):367–75. Epub 2011/04/05. doi: 10.1016/j.cmet.2011.03.00521459322; PubMed Central PMCID: PMC3086264.
23. Ogawa S, Lozach J, Benner C, Pascual G, Tangirala RK, Westin S, et al. Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell. 2005;122(5):707–21. Epub 2005/09/07. doi: 10.1016/j.cell.2005.06.02916143103; PubMed Central PMCID: PMC1430687.
24. Blanc M, Hsieh WY, Robertson KA, Watterson S, Shui G, Lacaze P, et al. Host Defense against Viral Infection Involves Interferon Mediated Down-Regulation of Sterol Biosynthesis. PLoS Biol. 2011;9(3):e1000598. Epub 2011/03/17. doi: 10.1371/journal.pbio.100059821408089; PubMed Central PMCID: PMC3050939.
25. Watterson S, Guerriero ML, Blanc M, Mazein A, Loewe L, Robertson KA, et al. A model of flux regulation in the cholesterol biosynthesis pathway: Immune mediated graduated flux reduction versus statin-like led stepped flux reduction. Biochimie. 2012. Epub 2012/06/06. doi: 10.1016/j.biochi.2012.05.02422664637.
26. Spann NJ, Garmire LX, McDonald JG, Myers DS, Milne SB, Shibata N, et al. Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell. 2012;151(1):138–52. Epub 2012/10/02. doi: 10.1016/j.cell.2012.06.05423021221; PubMed Central PMCID: PMC3464914.
27. Liu SY, Aliyari R, Chikere K, Li G, Marsden MD, Smith JK, et al. Interferon-inducible cholesterol-25-hydroxylase broadly inhibits viral entry by production of 25-hydroxycholesterol. Immunity. 2013;38(1):92–105. Epub 2013/01/01. doi: 10.1016/j.immuni.2012.11.00523273844; PubMed Central PMCID: PMC3698975.
28. Mazein A, Watterson S, Hsieh WY, Griffiths WJ, Ghazal P, A comprehensive machine-readable view of the mammalian cholesterol biosynthesis pathway. Biochem Pharmacol. 2013;86(1):56–66. doi: 10.1016/j.bcp.2013.03.02123583456; PubMed Central PMCID: PMC3912678.
29. Sato R, Inoue J, Kawabe Y, Kodama T, Takano T, Maeda M, Sterol-dependent transcriptional regulation of sterol regulatory element-binding protein-2. Journal of Biological Chemistry. 1996;271(43):26461–4. WOS:A1996VP23300005. 8900111
30. Reboldi A, Dang E, McDonald J, Liang G, Russell D, Cyster J, 25-Hydroxycholesterol suppresses interleukin-1-driven inflammation downstream of type I interferon. Science. 2014;345(6197):679–84. doi: 10.1126/science.1254790 WOS:000339962800041. 25104388
31. Shibata N, Carlin A, Spann N, Saijo K, Morello C, McDonald J, et al. 25-Hydroxycholesterol Activates the Integrated Stress Response to Reprogram Transcription and Translation in Macrophages. Journal of Biological Chemistry. 2013;288(50):35812–23. doi: 10.1074/jbc.M113.519637 WOS:000329814700019. 24189069
32. Rayner KJ, Suarez Y, Davalos A, Parathath S, Fitzgerald ML, Tamehiro N, et al. MiR-33 contributes to the regulation of cholesterol homeostasis. Science. 2010;328(5985):1570–3. Epub 2010/05/15. science.1189862 [pii] doi: 10.1126/science.118986220466885.
33. Hu Z, Shen WJ, Kraemer FB, Azhar S, MicroRNAs 125a and 455 repress lipoprotein-supported steroidogenesis by targeting scavenger receptor class B type I in steroidogenic cells. Molecular and cellular biology. 2012;32(24):5035–45. Epub 2012/10/10. doi: 10.1128/mcb.01002-1223045399; PubMed Central PMCID: PMC3510537.
34. Miller AM, Gilchrist DS, Nijjar J, Araldi E, Ramirez CM, Lavery CA, et al. MiR-155 has a protective role in the development of non-alcoholic hepatosteatosis in mice. PLoS ONE. 2013;8(8):e72324. Epub 2013/08/31. doi: 10.1371/journal.pone.007232423991091; PubMed Central PMCID: PMC3749101.
35. Larsen L, Rosenstierne MW, Gaarn LW, Bagge A, Pedersen L, Dahmcke CM, et al. Expression and localization of microRNAs in perinatal rat pancreas: role of miR-21 in regulation of cholesterol metabolism. PLoS ONE. 2011;6(10):e25997. Epub 2011/10/25. doi: 10.1371/journal.pone.002599722022489; PubMed Central PMCID: PMC3191174.
36. Yang M, Liu W, Pellicane C, Sahyoun C, Joseph B, Gallo-Ebert C, et al. Identification of miR-185 as a regulator of de novo cholesterol biosynthesis and low density lipoprotein uptake. Journal of Lipid Research. 2014;55(2):226–38. doi: 10.1194/jlr.M041335 WOS:000330535800007. 24296663
37. Ramirez CM, Rotllan N, Vlassov AV, Davalos A, Li M, Goedeke L, et al. Control of cholesterol metabolism and plasma high-density lipoprotein levels by microRNA-144. Circulation research. 2013;112(12):1592–601. Epub 2013/03/23. doi: 10.1161/circresaha.112.30062623519695.
38. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D, MicroRNA-155 is induced during the macrophage inflammatory response. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(5):1604–9. Epub 2007/01/24. doi: 10.1073/pnas.061073110417242365; PubMed Central PMCID: PMC1780072.
39. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ, miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008;36:D154–8. Epub 2007/11/10. doi: 10.1093/nar/gkm95217991681; PubMed Central PMCID: PMC2238936.
40. Wu C, Macleod I, Su AI, BioGPS and MyGene.info: organizing online, gene-centric information. Nucleic Acids Res. 2013;41(Database issue):D561–5. Epub 2012/11/24. doi: 10.1093/nar/gks111423175613; PubMed Central PMCID: PMC3531157.
41. Ghani S, Riemke P, Schonheit J, Lenze D, Stumm J, Hoogenkamp M, et al. Macrophage development from hematopoietic stem cells requires PU.1 coordinated microRNA expression. Blood. 2011. Epub 2011/07/07. doi: 10.1182/blood-2011-02-33514121730352.
42. Wei Y, Nazari-Jahantigh M, Chan L, Zhu M, Heyll K, Corbalan-Campos J, et al. The microRNA-342-5p fosters inflammatory macrophage activation through an Akt1- and microRNA-155-dependent pathway during atherosclerosis. Circulation. 2013;127(15):1609–19. Epub 2013/03/21. doi: 10.1161/CIRCULATIONAHA.112.00073623513069.
43. De Marchis ML, Ballarino M, Salvatori B, Puzzolo MC, Bozzoni I, Fatica A, A new molecular network comprising PU.1, interferon regulatory factor proteins and miR-342 stimulates ATRA-mediated granulocytic differentiation of acute promyelocytic leukemia cells. Leukemia. 2009;23(5):856–62. Epub 2009/01/20. leu2008372 [pii] doi: 10.1038/leu.2008.37219151778.
44. Li X, Chen YT, Josson S, Mukhopadhyay NK, Kim J, Freeman MR, et al. MicroRNA-185 and 342 inhibit tumorigenicity and induce apoptosis through blockade of the SREBP metabolic pathway in prostate cancer cells. PLoS ONE. 2013;8(8):e70987. Epub 2013/08/21. doi: 10.1371/journal.pone.007098723951060; PubMed Central PMCID: PMC3739799.
45. Kropp K, Robertson K, Sing G, Rodriguez-Martin S, Blanc M, Lacaze P, et al. Reversible Inhibition of Murine Cytomegalovirus Replication by Gamma Interferon (IFN-gamma) in Primary Macrophages Involves a Primed Type I IFN-Signaling Subnetwork for Full Establishment of an Immediate-Early Antiviral State. Journal of Virology. 2011;85(19):10286–99. doi: 10.1128/JVI.00373-11 WOS:000296253900061. 21775459
46. Spann N, Glass C, Sterols and oxysterols in immune cell function. Nature Immunology. 2013;14(9):893–900. doi: 10.1038/ni.2681 WOS:000323377700006. 23959186
47. Kapadia SB, Chisari FV, Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(7):2561–6. Epub 2005/02/09. doi: 10.1073/pnas.040983410215699349; PubMed Central PMCID: PMC549027.
48. Bordier BB, Ohkanda J, Liu P, Lee SY, Salazar FH, Marion PL, et al. In vivo antiviral efficacy of prenylation inhibitors against hepatitis delta virus. The Journal of clinical investigation. 2003;112(3):407–14. Epub 2003/08/05. doi: 10.1172/jci1770412897208; PubMed Central PMCID: PMC166292.
49. Liao Z, Cimakasky LM, Hampton R, Nguyen DH, Hildreth JE, Lipid rafts and HIV pathogenesis: host membrane cholesterol is required for infection by HIV type 1. AIDS research and human retroviruses. 2001;17(11):1009–19. Epub 2001/08/04. doi: 10.1089/08892220130034369011485618.
50. Bruce E, Digard P, Stuart A, The Rab11 Pathway Is Required for Influenza A Virus Budding and Filament Formation. Journal of Virology. 2010;84(12):5848–59. doi: 10.1128/JVI.00307-10 WOS:000277733900001. 20357086
51. Wang L, Qin Y, Tong L, Wu S, Wang Q, Jiao Q, et al. MiR-342-5p suppresses coxsackievirus B3 biosynthesis by targeting the 2C-coding region. Antiviral research. 2012;93(2):270–9. Epub 2011/12/27. doi: 10.1016/j.antiviral.2011.12.00422197249.
52. Lu H, Talbot S, Robertson K, Watterson S, Forster T, Roy D, et al. Rapid proteasomal elimination of 3-hydroxy-3-methylglutaryl-CoA reductase by interferon-gamma in primary macrophages requires endogenous 25-hydroxycholesterol synthesis. Steroids. 2015;99:219–29. doi: 10.1016/j.steroids.2015.02.022 WOS:000356985000016. 25759117
53. Thurnher M, Gruenbacher G, Nussbaumer O, Regulation of mevalonate metabolism in cancer and immune cells. Biochimica Et Biophysica Acta-Molecular and Cell Biology of Lipids. 2013;1831(6):1009–15. doi: 10.1016/j.bbalip.2013.03.003 WOS:000319309800001.
54. Roberts A, Kim C, Zhen L, Lowe J, Kapur R, Petryniak B, et al. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity. 1999;10(2):183–96. doi: 10.1016/S1074-7613(00)80019-9 WOS:000078972200006. 10072071
55. Philips M, The perplexing case of the geranylgeranyl transferase-deficient mouse. Journal of Clinical Investigation. 2011;121(2):510–3. doi: 10.1172/JCI45952 WOS:000286913800012. 21266773
56. Khan O, Ibrahim M, Jonsson I, Karlsson C, Liu M, Sjogren A, et al. Geranylgeranyltransferase type I (GGTase-I) deficiency hyperactivates macrophages and induces erosive arthritis in mice. Journal of Clinical Investigation. 2011;121(2):628–39. doi: 10.1172/JCI43758 WOS:000286913800027. 21266780
57. Wang C, Gale M, Jr.Keller BC, Huang H, Brown MS, Goldstein JL, et al. Identification of FBL2 as a geranylgeranylated cellular protein required for hepatitis C virus RNA replication. Molecular cell. 2005;18(4):425–34. Epub 2005/05/17. doi: 10.1016/j.molcel.2005.04.00415893726.
58. Gower TL, Graham BS, Antiviral activity of lovastatin against respiratory syncytial virus in vivo and in vitro. Antimicrobial agents and chemotherapy. 2001;45(4):1231–7. Epub 2001/03/21. doi: 10.1128/aac.45.4.1231-1237.200111257039; PubMed Central PMCID: PMC90448.
59. Turner M, Galloway A, Vigorito E, Noncoding RNA and its associated proteins as regulatory elements of the immune system. Nature Immunology. 2014;15(6):484–91. doi: 10.1038/ni.2887 WOS:000336419300002. 24840979
60. Maillard P, Ciaudo C, Marchais A, Li Y, Jay F, Ding S, et al. Antiviral RNA Interference in Mammalian Cells. Science. 2013;342(6155):235–8. doi: 10.1126/science.1241930 WOS:000325475200042. 24115438
61. Li Y, Lu J, Han Y, Fan X, Ding S, RNA Interference Functions as an Antiviral Immunity Mechanism in Mammals. Science. 2013;342(6155):231–4. doi: 10.1126/science.1241911 WOS:000325475200041. 24115437
62. Heiss B, Maximova O, Thach D, Speicher J, Pletnev A, MicroRNA Targeting of Neurotropic Flavivirus: Effective Control of Virus Escape and Reversion to Neurovirulent Phenotype. Journal of Virology. 2012;86(10):5647–59. doi: 10.1128/JVI.07125-11 WOS:000303787100022. 22419812
63. Angulo A, Ghazal P, Messerle M, The major immediate-early gene ie3 of mouse cytomegalovirus is essential for viral growth. Journal of virology. 2000;74(23):11129–36. Epub 2000/11/09. 11070009; PubMed Central PMCID: PMC113196.
64. Borst E, Messerle M, Development of a cytomegalovirus vector for somatic gene therapy. Bone Marrow Transplant. 2000;25Suppl 2:S80–2. 10933196.
65. Dolken L, Ruzsics Z, Radle B, Friedel CC, Zimmer R, Mages J, et al. High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA. 2008;14(9):1959–72. Epub 2008/07/29. rna.1136108 [pii] doi: 10.1261/rna.113610818658122; PubMed Central PMCID: PMC2525961.
66. Lennox K, Owczarzy R, Thomas D, Walder J, Behlke M, Improved Performance of Anti-miRNA Oligonucleotides Using a Novel Non-Nucleotide Modifier. Molecular Therapy-Nucleic Acids. 2013;2. doi: 10.1038/mtna.2013.46 WOS:000332467100005.
67. Lundberg P, Yang HJ, Jung SJ, Behlke MA, Rose SD, Cantin EM, Protection against TNFalpha-dependent liver toxicity by intraperitoneal liposome delivered DsiRNA targeting TNFalpha in vivo. J Control Release. 2012;160(2):194–9. Epub 2011/11/19. doi: 10.1016/j.jconrel.2011.10.03422094102; PubMed Central PMCID: PMC3321390.
68. Griffiths W, Crick P, Wang Y, Ogundare M, Tuschl K, Morris A, et al. Analytical strategies for characterization of oxysterol lipidomes: Liver X receptor ligands in plasma. Free Radical Biology and Medicine. 2013;59:69–84. doi: 10.1016/j.freeradbiomed.2012.07.027 WOS:000318202800008. 22846477
69. Bartel DP, MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215–33. Epub 2009/01/27. S0092-8674(09)00008-7 [pii] doi: 10.1016/j.cell.2009.01.00219167326.
70. Dweep H, Sticht C, Pandey P, Gretz N, miRWalk—database: prediction of possible miRNA binding sites by "walking" the genes of three genomes. Journal of biomedical informatics. 2011;44(5):839–47. doi: 10.1016/j.jbi.2011.05.00221605702.
71. Aerts S, Van Loo P, Thijs G, Mayer H, de Martin R, Moreau Y, et al. TOUCAN 2: the all-inclusive open source workbench for regulatory sequence analysis. Nucleic acids research. 2005;33(Web Server issue):W393–6. Epub 2005/06/28. doi: 10.1093/nar/gki35415980497; PubMed Central PMCID: PMC1160115.
72. Johnson DS, Mortazavi A, Myers RM, Wold B, Genome-wide mapping of in vivo protein-DNA interactions. Science. 2007;316(5830):1497–502. Epub 2007/06/02. doi: 10.1126/science.114131917540862.