Detection and quantification of extracellular microRNAs in murine biofluids

Biological Procedures Online

Volumn 16, Issue 1, 2014, Pages

  Roberts, Thomas C ^a,b   Coenen Stass, Anna M L ^a   Betts, Corinne A ^a   Wood, Matthew J A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Biofluid; Extracellular microRNA; miRNA; Plasma; RT qPCR; Serum

Indexed keywords

MICRORNA; PLASMA PROTEIN; MICRORNA 1; MICRORNA 133A; MICRORNA 206; UNCLASSIFIED DRUG;

ARTICLE; EXTRACELLULAR SPACE; JUGULAR VEIN; MEASUREMENT ACCURACY; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEIC ACID AMPLIFICATION; PROTEIN BLOOD LEVEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA EXTRACTION; SENSITIVITY ANALYSIS; WILD TYPE; ABSORPTION; ACCURACY; ANALYZER; ANIMAL CELL; BLOOD; BODY FLUID; GENE EXPRESSION; LIMIT OF DETECTION; SENSITIVITY AND SPECIFICITY; SERUM; SPECTROPHOTOMETER; SPECTROPHOTOMETRY; TAIL VEIN; VALIDITY;

EUKARYOTA; MURINAE; MUS;

EID: 84899464103     PISSN: None     EISSN: 14809222     Source Type: Journal    
DOI: 10.1186/1480-9222-16-5     Document Type: Article

References (52)

1. Post-transcriptional gene silencing by siRNAs and miRNAs. Filipowicz W, Jaskiewicz L, Kolb FA, Pillai RS, Curr Opin Struct Biol 2005 15 331 341 10.1016/j.sbi.2005.05.006 15925505
2. Serum microRNAs are promising novel biomarkers. Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D, Yerushalmi N, Benjamin H, Kushnir M, Cholakh H, Melamed N, Bentwich Z, Hod M, Goren Y, Chajut A, PLoS ONE 2008 3 3148 10.1371/journal.pone.0003148 18773077
3. Circulating microRNAs as stable blood-based markers for cancer detection. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M, Proc Natl Acad Sci USA 2008 105 10513 10518 10.1073/pnas.0804549105 18663219
4. A robust methodology to study urine microRNA as tumor marker: microRNA-126 and microRNA-182 are related to urinary bladder cancer. Hanke M, Hoefig K, Merz H, Feller AC, Kausch I, Jocham D, Warnecke JM, Sczakiel G, Urol Oncol 2010 28 655 661 10.1016/j.urolonc.2009.01.027 19375957
5. Identification of extracellular miRNA in human cerebrospinal fluid by next-generation sequencing. Burgos KL, Javaherian A, Bomprezzi R, Ghaffari L, Rhodes S, Courtright A, Tembe W, Kim S, Metpally R, Van Keuren-Jensen K, RNA 2013 19 712 722 10.1261/rna.036863.112 23525801
6. Identification of forensically relevant body fluids using a panel of differentially expressed microRNAs. Hanson EK, Lubenow H, Ballantyne J, Anal Biochem 2009 387 303 314 10.1016/j.ab.2009.01.037 19454234
7. miRandola: extracellular circulating microRNAs database. Russo F, Di Bella S, Nigita G, Macca V, Laganà A, Giugno R, Pulvirenti A, Ferro A, PLoS ONE 2012 7 47786 10.1371/journal.pone.0047786 23094086
8. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Lee RC, Feinbaum RL, Ambros V, Cell 1993 75 843 854 10.1016/0092-8674(93)90529-Y 8252621
9. Stability of endogenous and added RNA in blood specimens, serum, and plasma. Tsui NBY, Ng EKO, Lo YMD, Clin Chem 2002 48 1647 1653 12324479
10. Secretory mechanisms and intercellular transfer of microRNAs in living cells. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T, J Biol Chem 2010 285 17442 17452 10.1074/jbc.M110.107821 20353945
11. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO, Nat Cell Biol 2007 9 654 659 10.1038/ncb1596 17486113
12. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Köppel T, Jahantigh MN, Lutgens E, Wang S, Olson EN, Schober A, Weber C, Sci Signal 2009 2 a81 19996457
13. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, Tewari M, Proc Natl Acad Sci USA 2011 108 5003 5008 10.1073/pnas.1019055108 21383194
14. Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. Turchinovich A, Burwinkel B, RNA Biol 2012 9 1066 1075 10.4161/rna.21083 22858679
15. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT, Nat Cell Biol 2011 13 423 433 10.1038/ncb2210 21423178
16. microRNA (miRNA) speciation in Alzheimer's disease (AD) cerebrospinal fluid (CSF) and extracellular fluid (ECF). Alexandrov PN, Dua P, Hill JM, Bhattacharjee S, Zhao Y, Lukiw WJ, Int J Biochem Mol Biol 2012 3 365 373 23301201
17. Circulating miR-375 as a biomarker of β-cell death and diabetes in mice. Erener S, Mojibian M, Fox JK, Denroche HC, Kieffer TJ, Endocrinology 2013 154 603 608 10.1210/en.2012-1744 23321698
18. Circulating microRNAs: promising candidates serving as novel biomarkers of acute hepatitis. Elfimova N, Schlattjan M, Sowa J-P, Dienes HP, Canbay A, Odenthal M, Front Physiol 2012 3 476 23267332
19. MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease. Hulsmans M, Holvoet P, Cardiovasc Res 2013 100 7 18 10.1093/cvr/cvt161 23774505
20. miR-210 Inhibits Trophoblast Invasion and Is a Serum Biomarker for Preeclampsia. Anton L, Olarerin-George AO, Schwartz N, Srinivas S, Bastek J, Hogenesch JB, Elovitz MA, Am J Pathol 2013 183 1437 1445 10.1016/j.ajpath.2013. 07.021 24035613
21. Circulating and urinary microRNAs in kidney disease. Lorenzen JM, Thum T, Clin J Am Soc Nephrol 2012 7 1528 1533 10.2215/CJN.01170212 22580786
22. Identification of tissue-specific microRNAs from mouse. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T, Curr Biol 2002 12 735 739 12007417
23. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Zhang L, Hou D, Chen X, Li D, Zhu L, Zhang Y, Li J, Bian Z, Liang X, Cai X, Yin Y, Wang C, Zhang T, Zhu D, Zhang D, Xu J, Chen Q, Ba Y, Liu J, Wang Q, Chen J, Wang J, Wang M, Zhang Q, Zhang J, Zen K, Zhang C-Y, Cell Res 2012 22 107 126 10.1038/cr.2011.158 21931358
24. Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations. Williams Z, Ben-Dov IZ, Elias R, Mihailovic A, Brown M, Rosenwaks Z, Tuschl T, Proc Natl Acad Sci USA 2013 110 4255 4260 10.1073/pnas.1214046110 23440203
25. Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Sacco A, Mourkioti F, Tran R, Choi J, Llewellyn M, Kraft P, Shkreli M, Delp S, Pomerantz JH, Artandi SE, Blau HM, Cell 2010 143 1059 1071 10.1016/j.cell.2010.11.039 21145579
26. Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study. Cirak S, Arechavala-Gomeza V, Guglieri M, Feng L, Torelli S, Anthony K, Abbs S, Garralda ME, Bourke J, Wells DJ, Dickson G, Wood MJA, Wilton SD, Straub V, Kole R, Shrewsbury SB, Sewry C, Morgan JE, Bushby K, Muntoni F, Lancet 2011 378 595 605 10.1016/S0140-6736(11)60756-3 21784508
27. Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Kinali M, Arechavala-Gomeza V, Feng L, Cirak S, Hunt D, Adkin C, Guglieri M, Ashton E, Abbs S, Nihoyannopoulos P, Garralda ME, Rutherford M, McCulley C, Popplewell L, Graham IR, Dickson G, Wood MJA, Wells DJ, Wilton SD, Kole R, Straub V, Bushby K, Sewry C, Morgan JE, Muntoni F, Lancet Neurol 2009 8 918 928 10.1016/S1474-4422(09)70211-X 19713152
28. miRNAs as serum biomarkers for Duchenne muscular dystrophy. Cacchiarelli D, Legnini I, Martone J, Cazzella V, D'Amico A, Bertini E, Bozzoni I, EMBO Mol Med 2011 3 258 265 10.1002/emmm.201100133 21425469
29. Identification of muscle-specific microRNAs in serum of muscular dystrophy animal models: promising novel blood-based markers for muscular dystrophy. Mizuno H, Nakamura A, Aoki Y, Ito N, Kishi S, Yamamoto K, Sekiguchi M, Takeda S, Hashido K, PLoS ONE 2011 6 18388 10.1371/journal.pone.0018388 21479190
30. Expression analysis in multiple muscle groups and serum reveals complexity in the MicroRNA transcriptome of the mdx mouse with implications for therapy. Roberts TC, Blomberg KEM, McClorey G, Andaloussi SE, Godfrey C, Betts C, Coursindel T, Gait MJ, Smith CE, Wood MJ, Mol Ther Nucleic Acids 2012 1 39 10.1038/mtna.2012.26 23344181
31. Extracellular microRNAs are dynamic non-vesicular biomarkers of muscle turnover. Roberts TC, Godfrey C, McClorey G, Vader P, Briggs D, Gardiner C, Aoki Y, Sargent I, Morgan JE, Wood MJA, Nucl Acids Res 2013 41 9500 9513 10.1093/nar/gkt724 23945935
32. Rescue of severely affected dystrophin/utrophin-deficient mice through scAAV-U7snRNA-mediated exon skipping. Goyenvalle A, Babbs A, Wright J, Wilkins V, Powell D, Garcia L, Davies KE, Hum Mol Genet 2012 21 2559 2571 10.1093/hmg/dds082 22388933
33. Distinctive serum miRNA profile in mouse models of striated muscular pathologies. Vignier N, Amor F, Fogel P, Duvallet A, Poupiot J, Charrier S, Arock M, Montus M, Nelson I, Richard I, Carrier L, Servais L, Voit T, Bonne G, Israeli D, PLoS ONE 2013 8 55281 10.1371/journal.pone.0055281 23418438
34. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Chen J-F, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang D-Z, Nat Genet 2006 38 228 233 10.1038/ng1725 16380711
35. Muscle-specific microRNA miR-206 promotes muscle differentiation. Kim HK, Lee YS, Sivaprasad U, Malhotra A, Dutta A, J Cell Biol 2006 174 677 687 10.1083/jcb.200603008 16923828
36. The impact of hemolysis on cell-free microrna biomarkers. Kirschner MB, Edelman JJB, Kao SC-H, Vallely MP, Van Zandwijk N, Reid G, Front Genet 2013 4 94 23745127
37. Plasma processing conditions substantially influence circulating microRNA biomarker levels. Cheng HH, Yi HS, Kim Y, Kroh EM, Chien JW, Eaton KD, Goodman MT, Tait JF, Tewari M, Pritchard CC, PLoS ONE 2013 8 64795 10.1371/journal.pone. 0064795 23762257
38. Platelet activation and blood coagulation. Heemskerk JWM, Bevers EM, Lindhout T, Thromb Haemost 2002 88 186 193 12195687
39. An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Lehmann SM, Krüger C, Park B, Derkow K, Rosenberger K, Baumgart J, Trimbuch T, Eom G, Hinz M, Kaul D, Habbel P, Kälin R, Franzoni E, Rybak A, Nguyen D, Veh R, Ninnemann O, Peters O, Nitsch R, Heppner FL, Golenbock D, Schott E, Ploegh HL, Wulczyn FG, Lehnardt S, Nat Neurosci 2012 15 827 835 10.1038/nn.3113 22610069
40. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Chomczynski P, Sacchi N, Anal Biochem 1987 162 156 159 2440339
41. Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Blondal T, Jensby Nielsen S, Baker A, Andreasen D, Mouritzen P, Wrang Teilum M, Dahlsveen IK, Methods 2013 59 1 6 10.1016/j.ymeth.2012.09.015 23036329
42. Assessment of RT-qPCR normalization strategies for accurate quantification of extracellular microRNAs in murine serum. Roberts TC, Coenen-Stass AML, Wood MJA, PLoS ONE 2014 9 89237 10.1371/journal.pone.0089237 24586621
43. RAS is regulated by the let-7 MicroRNA family. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, Slack FJ, Cell 2005 120 635 647 10.1016/j.cell.2005.01.014 15766527
44. Real-time quantification of microRNAs by stem-loop RT-PCR. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ, Nucleic Acids Res 2005 33 179 10.1093/nar/gni178 16314309
45. A novel method to monitor the expression of microRNAs. Fu H-J, Zhu J, Yang M, Zhang Z-Y, Tie Y, Jiang H, Sun Z-X, Zheng X-F, Mol Biotechnol 2006 32 197 204 10.1385/MB:32:3:197 16632886
46. Specific and sensitive quantitative RT-PCR of miRNAs with DNA primers. Balcells I, Cirera S, Busk PK, BMC Biotechnol 2011 11 70 10.1186/1472-6750-11-70 21702990
47. Profiling microRNAs by real-time PCR. Jacobsen N, Andreasen D, Mouritzen P, Methods Mol Biol 2011 732 39 54 10.1007/978-1-61779-083-6-4 21431704
48. A new mathematical model for relative quantification in real-time RT-PCR. Pfaffl MW, Nucleic Acids Res 2001 29 45 10.1093/nar/29.9.e45 11328886
49. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Livak KJ, Schmittgen TD, Methods 2001 25 402 408 10.1006/meth.2001.1262 11846609
50. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM, Neurosci Lett 2003 339 62 66 10.1016/S0304-3940(02)01423-4 12618301
51. RDML: structured language and reporting guidelines for real-time quantitative PCR data. Lefever S, Hellemans J, Pattyn F, Przybylski DR, Taylor C, Geurts R, Untergasser A, Vandesompele J, RDML consortium, Nucleic Acids Res 2009 37 2065 2069 10.1093/nar/gkp056 19223324
52. RNA quantitation by fluorescence-based solution assay: RiboGreen reagent characterization. Jones LJ, Yue ST, Cheung CY, Singer VL, Anal Biochem 1998 265 368 374 10.1006/abio.1998.2914 9882416