Recent progress toward the use of circulating microRNAs as clinical biomarkers

Archives of Toxicology

Volumn 90, Issue 12, 2016, Pages 2959-2978

  Ghai, Vikas ^a   Wang, Kai ^a  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

Biomarkers; Cancer; Cardiovascular disease; Diabetes; MiRNAs; Toxicology

Indexed keywords

BIOLOGICAL MARKER; MICRORNA; TUMOR MARKER;

BREAST CANCER; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL METABOLISM; CELL PROLIFERATION; COLORECTAL CANCER; DIABETES MELLITUS; EXTRACELLULAR FLUID; GENE SILENCING; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; LIPID VESICLE; LUNG CANCER; NERVE FIBER GROWTH; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TOXICITY TESTING; ANIMAL; BLOOD; CARDIOVASCULAR DISEASES; CHEMICALLY INDUCED; EARLY CANCER DIAGNOSIS; EARLY DIAGNOSIS; INTOXICATION; METABOLISM; NEOPLASMS; PROCEDURES; TOXICOLOGY; TRENDS;

ANIMALS; BIOMARKERS; BIOMARKERS, TUMOR; CARDIOVASCULAR DISEASES; DIABETES MELLITUS; EARLY DETECTION OF CANCER; EARLY DIAGNOSIS; HUMANS; MICRORNAS; NEOPLASMS; POISONING; TOXICOLOGY;

EID: 84984853922     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-016-1828-2     Document Type: Review

References (136)

1. Abue M, Yokoyama M, Shibuya R, Tamai K, Yamaguchi K, Sato I, Tanaka N, Hamada S, Shimosegawa T, Sugamura K et al (2015) Circulating miR-483-3p and miR-21 is highly expressed in plasma of pancreatic cancer. Int J Oncol 46:539–547
2. Akat KM, Moore-McGriff D, Morozov P, Brown M, Gogakos T, Correa Da Rosa J, Mihailovic A, Sauer M, Ji R, Ramarathnam A et al (2014) Comparative RNA-sequencing analysis of myocardial and circulating small RNAs in human heart failure and their utility as biomarkers. Proc Natl Acad Sci USA 111:11151–11156
3. Alemar B, Izetti P, Gregório C, Macedo GS, Castro MAA, Osvaldt AB, Matte U, Ashton-Prolla P (2016) miRNA-21 and miRNA-34a are potential minimally invasive biomarkers for the diagnosis of pancreatic ductal adenocarcinoma. Pancreas 45:84–92
4. Argyropoulos C, Wang K, McClarty S, Huang D, Bernardo J, Ellis D, Orchard T, Galas D, Johnson J (2013) Urinary microRNA profiling in the nephropathy of type 1 diabetes. PLoS ONE 8:e54662
5. Argyropoulos C, Wang K, Bernardo J, Ellis D, Orchard T, Galas D, Johnson JP (2015) Urinary microRNA profiling predicts the development of microalbuminuria in patients with type 1 diabetes. J Clin Med 4:1498–1517
6. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL et al (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108:5003–5008
7. Axtell MJ, Westholm JO, Lai EC (2011) Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12:221
8. Ayala W, Moore LV, Hess EL (1951) The purple color reaction given by diphenylamine reagent. I. With normal and rheumatic fever sera. J Clin Invest 30:781–785
9. Badrnya S, Baumgartner R, Assinger A (2014) Smoking alters circulating plasma microvesicle pattern and microRNA signatures. Thromb Haemost 112(1):128–136
10. Balasubramanyam M, Aravind S, Gokulakrishnan K, Prabu P, Sathishkumar C, Ranjani H, Mohan V (2011) Impaired miR-146a expression links subclinical inflammation and insulin resistance in Type 2 diabetes. Mol Cell Biochem 351:197–205
11. Bianchi F, Nicassio F, Marzi M, Belloni E, Dall’Olio V, Bernard L, Pelosi G, Maisonneuve P, Veronesi G, Di Fiore PP (2011) A serum circulating miRNA diagnostic test to identify asymptomatic high-risk individuals with early stage lung cancer: serum miRNAs to diagnose asymptomatic NSCLC. EMBO Mol Med 3:495–503
12. Boeri M, Verri C, Conte D, Roz L, Modena P, Facchinetti F, Calabrò E, Croce CM, Pastorino U, Sozzi G (2011) MicroRNA signatures in tissues and plasma predict development and prognosis of computed tomography detected lung cancer. Proc Natl Acad Sci USA 108:3713–3718
13. Bollati V, Angelici L, Rizzo G, Pergoli L, Rota F, Hoxha M, Nordio F, Bonzini M, Tarantini L, Cantone L et al (2015) Microvesicle-associated microRNA expression is altered upon particulate matter exposure in healthy workers and in A549 cells. J Appl Toxicol JAT 35:59–67
14. Cha DJ, Franklin JL, Dou Y, Liu Q, Higginbotham JN, DemoryBeckler M, Weaver AM, Vickers K, Prasad N, Levy S et al (2015) KRAS-dependent sorting of miRNA to exosomes. eLife 4:e07197
15. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X et al (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18:997–1006
16. Chen W, Cai F, Zhang B, Barekati Z, Zhong XY (2013) The level of circulating miRNA-10b and miRNA-373 in detecting lymph node metastasis of breast cancer: potential biomarkers. Tumour Biol J Int Soc Oncodev Biol Med 34:455–462
17. Chen H, Lan H-Y, Roukos DH, Cho WC (2014a) Application of microRNAs in diabetes mellitus. J Endocrinol 222:R1–R10
18. Chen Q, Yang L, Xiao Y, Zhu J, Li Z (2014b) Circulating microRNA-182 in plasma and its potential diagnostic and prognostic value for pancreatic cancer. Med Oncol Northwood Lond Engl 31:225
19. Cheng H, Zhang L, Cogdell DE, Zheng H, Schetter AJ, Nykter M, Harris CC, Chen K, Hamilton SR, Zhang W (2011) Circulating plasma MiR-141 is a novel biomarker for metastatic colon cancer and predicts poor prognosis. PLoS ONE 6:e17745
20. Corsten MF, Dennert R, Jochems S, Kuznetsova T, Devaux Y, Hofstra L, Wagner DR, Staessen JA, Heymans S, Schroen B (2010) Circulating microRNA-208b and microRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet 3:499–506
21. Cote GA, Gore AJ, McElyea SD, Heathers LE, Xu H, Sherman S, Korc M (2014) A pilot study to develop a diagnostic test for pancreatic ductal adenocarcinoma based on differential expression of select miRNA in plasma and bile. Am J Gastroenterol 109:1942–1952
22. Cuk K, Zucknick M, Heil J, Madhavan D, Schott S, Turchinovich A, Arlt D, Rath M, Sohn C, Benner A et al (2013) Circulating microRNAs in plasma as early detection markers for breast cancer. Int J Cancer 132:1602–1612
23. D’Alessandra Y, Devanna P, Limana F, Straino S, Di Carlo A, Brambilla PG, Rubino M, Carena MC, Spazzafumo L, De Simone M et al (2010) Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur Heart J 31:2765–2773
24. De Rosa S, Fichtlscherer S, Lehmann R, Assmus B, Dimmeler S, Zeiher AM (2011) Transcoronary concentration gradients of circulating microRNAs. Circulation 124:1936–1944
25. Delić D, Eisele C, Schmid R, Baum P, Wiech F, Gerl M, Zimdahl H, Pullen SS, Urquhart R (2016) Urinary Exosomal miRNA Signature in Type II Diabetic Nephropathy Patients. PLoS ONE 11:e0150154
26. Demory Beckler M, Higginbotham JN, Franklin JL, Ham A-J, Halvey PJ, Imasuen IE, Whitwell C, Li M, Liebler DC, Coffey RJ (2013) Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol Cell Proteom MCP 12:343–355
27. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ (2000) Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113(Pt 19):3365–3374
28. Devaux Y, Vausort M, Goretti E, Nazarov PV, Azuaje F, Gilson G, Corsten MF, Schroen B, Lair M-L, Heymans S et al (2012) Use of circulating microRNAs to diagnose acute myocardial infarction. Clin Chem 58:559–567
29. El-Khoury V, Pierson S, Kaoma T, Bernardin F, Berchem G (2016) Assessing cellular and circulating miRNA recovery: the impact of the RNA isolation method and the quantity of input material. Sci Rep 6:19529
30. Ellis KL, Cameron VA, Troughton RW, Frampton CM, Ellmers LJ, Richards AM (2013) Circulating microRNAs as candidate markers to distinguish heart failure in breathless patients. Eur J Heart Fail 15:1138–1147
31. Erson AE, Petty EM (2008) MicroRNAs in development and disease. Clin Genet 74:296–306
32. Fabian MR, Sonenberg N, Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351–379
33. Feng X, Wang Z, Fillmore R, Xi Y (2014) MiR-200, a new star miRNA in human cancer. Cancer Lett 344:166–173
34. Fish JE, Santoro MM, Morton SU, Yu S, Yeh R-F, Wythe JD, Ivey KN, Bruneau BG, Stainier DYR, Srivastava D (2008) miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 15:272–284
35. Gao W, Yu Y, Cao H, Shen H, Li X, Pan S, Shu Y (2010) Deregulated expression of miR-21, miR-143 and miR-181a in non small cell lung cancer is related to clinicopathologic characteristics or patient prognosis. Biomed Pharmacother Bioméd Pharmacothérapie 64:399–408
36. Gidlöf O, Smith JG, Miyazu K, Gilje P, Spencer A, Blomquist S, Erlinge D (2013) Circulating cardio-enriched microRNAs are associated with long-term prognosis following myocardial infarction. BMC Cardiovasc Disord 13:12
37. Goonetilleke KS, Siriwardena AK (2007) Systematic review of carbohydrate antigen (CA 19-9) as a biochemical marker in the diagnosis of pancreatic cancer. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 33:266–270
38. Goren Y, Kushnir M, Zafrir B, Tabak S, Lewis BS, Amir O (2012) Serum levels of microRNAs in patients with heart failure. Eur J Heart Fail 14:147–154
39. Guay C, Regazzi R (2013) Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat Rev Endocrinol 9:513–521
40. Ha M, Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15:509–524
41. Hansen TF, Carlsen AL, Heegaard NHH, Sørensen FB, Jakobsen A (2015) Changes in circulating microRNA-126 during treatment with chemotherapy and bevacizumab predicts treatment response in patients with metastatic colorectal cancer. Br J Cancer 112:624–629
42. He Y, Lin J, Kong D, Huang M, Xu C, Kim T-K, Etheridge A, Luo Y, Ding Y, Wang K (2015) Current state of circulating microRNAs as cancer biomarkers. Clin Chem 61:1138–1155
43. Hergenreider E, Heydt S, Tréguer K, Boettger T, Horrevoets AJG, Zeiher AM, Scheffer MP, Frangakis AS, Yin X, Mayr M et al (2012) Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 14:249–256
44. Ho AS, Huang X, Cao H, Christman-Skieller C, Bennewith K, Le Q-T, Koong AC (2010) Circulating miR-210 as a novel hypoxia marker in pancreatic cancer. Transl Oncol 3:109–113
45. Hu Z, Chen X, Zhao Y, Tian T, Jin G, Shu Y, Chen Y, Xu L, Zen K, Zhang C et al (2010) Serum microRNA signatures identified in a genome-wide serum microRNA expression profiling predict survival of non-small-cell lung cancer. J Clin Oncol Off J Am Soc Clin Oncol 28:1721–1726
46. Huang Z, Huang D, Ni S, Peng Z, Sheng W, Du X (2010) Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. Int J Cancer 127:118–126
47. Huang Y, Shen XJ, Zou Q, Wang SP, Tang SM, Zhang GZ (2011) Biological functions of microRNAs: a review. J Physiol Biochem 67:129–139
48. Huang S, Chen M, Li L, He MA, Hu D, Zhang X, Li J, Tanguay RM, Feng J, Cheng L et al (2014) Circulating microRNAs and the occurrence of acute myocardial infarction in Chinese populations. Circ Cardiovasc Genet 7:189–198
49. Jansen F, Yang X, Hoelscher M, Cattelan A, Schmitz T, Proebsting S, Wenzel D, Vosen S, Franklin BS, Fleischmann BK et al (2013) Endothelial microparticle-mediated transfer of microRNA-126 promotes vascular endothelial cell repair via SPRED1 and is abrogated in glucose-damaged endothelial microparticles. Circulation 128:2026–2038
50. Jansen F, Wang H, Przybilla D, Franklin BS, Dolf A, Pfeifer P, Schmitz T, Flender A, Endl E, Nickenig G, Werner N (2016) Vascular endothelial microparticles-incorporated microRNAs are altered in patients with diabetes mellitus. Cardiovasc Diabetol 15:49. doi:10.1186/s12933-016-0367-8
51. Ji X, Takahashi R, Hiura Y, Hirokawa G, Fukushima Y, Iwai N (2009) Plasma miR-208 as a biomarker of myocardial injury. Clin Chem 55:1944–1949
52. Kanki M, Moriguchi A, Sasaki D, Mitori H, Yamada A, Unami A, Miyamae Y (2014) Identification of urinary miRNA biomarkers for detecting cisplatin-induced proximal tubular injury in rats. Toxicology 324:158–168
53. Kong L, Zhu J, Han W, Jiang X, Xu M, Zhao Y, Dong Q, Pang Z, Guan Q, Gao L et al (2011a) Significance of serum microRNAs in pre-diabetes and newly diagnosed type 2 diabetes: a clinical study. Acta Diabetol 48:61–69
54. Kong X, Du Y, Wang G, Gao J, Gong Y, Li L, Zhang Z, Zhu J, Jing Q, Qin Y et al (2011b) Detection of differentially expressed microRNAs in serum of pancreatic ductal adenocarcinoma patients: miR-196a could be a potential marker for poor prognosis. Dig Dis Sci 56:602–609
55. Koppers-Lalic D, Hackenberg M, Bijnsdorp IV, van Eijndhoven MAJ, Sadek P, Sie D, Zini N, Middeldorp JM, Ylstra B, de Menezes RX et al (2014) Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep 8:1649–1658
56. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285:17442–17452
57. Kozakowska M, Ciesla M, Stefanska A, Skrzypek K, Was H, Jazwa A, Grochot-Przeczek A, Kotlinowski J, Szymula A, Bartelik A et al (2012) Heme oxygenase-1 inhibits myoblast differentiation by targeting myomirs. Antioxid Redox Signal 16:113–127
58. Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucl Acids Res 42:D68–D73
59. Krichevsky AM, Gabriely G (2009) miR-21: a small multi-faceted RNA. J Cell Mol Med 13:39–53
60. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854
61. Leroyer AS, Tedgui A, Boulanger CM (2008) Microparticles and type 2 diabetes. Diabetes Metab 34(Suppl 1):S27–32
62. Liu L-Z, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y, Kung H-F, Lai L, Jiang B-H (2011) MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression. PLoS ONE 6:e19139
63. Liu R, Chen X, Du Y, Yao W, Shen L, Wang C, Hu Z, Zhuang R, Ning G, Zhang C et al (2012a) Serum microRNA expression profile as a biomarker in the diagnosis and prognosis of pancreatic cancer. Clin Chem 58:610–618
64. Liu X-G, Zhu W-Y, Huang Y-Y, Ma L-N, Zhou S-Q, Wang Y-K, Zeng F, Zhou J-H, Zhang Y-K (2012b) High expression of serum miR-21 and tumor miR-200c associated with poor prognosis in patients with lung cancer. Med Oncol Northwood Lond Engl 29:618–626
65. Liu Y, Gao G, Yang C, Zhou K, Shen B, Liang H, Jiang X (2014) The role of circulating microRNA-126 (miR-126): a novel biomarker for screening prediabetes and newly diagnosed type 2 diabetes mellitus. Int J Mol Sci 15:10567–10577
66. Long G, Wang F, Duan Q, Yang S, Chen F, Gong W, Yang X, Wang Y, Chen C, Wang DW (2012) Circulating miR-30a, miR-195 and let-7b associated with acute myocardial infarction. PLoS ONE 7:e50926
67. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG, Teruya-Feldstein J, Bell GW, Weinberg RA (2010) Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol 28:341–347
68. Madhavan D, Peng C, Wallwiener M, Zucknick M, Nees J, Schott S, Rudolph A, Riethdorf S, Trumpp A, Pantel K et al (2016) Circulating miRNAs with prognostic value in metastatic breast cancer and for early detection of metastasis. Carcinogenesis 37:461
69. Maegdefessel L (2014) The emerging role of microRNAs in cardiovascular disease. J Intern Med 276(6):633–644
70. Mandel P, Metais P (1948) Comptes rendus séances société. Biol Ses Fil 142:241–243
71. Mar-Aguilar F, Mendoza-Ramírez JA, Malagón-Santiago I, Espino-Silva PK, Santuario-Facio SK, Ruiz-Flores P, Rodríguez-Padilla C, Reséndez-Pérez D (2013) Serum circulating microRNA profiling for identification of potential breast cancer biomarkers. Dis Markers 34:163–169
72. Matamala N, Vargas MT, González-Cámpora R, Miñambres R, Arias JI, Menéndez P, Andrés-León E, Gómez-López G, Yanowsky K, Calvete-Candenas J et al (2015) Tumor microRNA expression profiling identifies circulating microRNAs for early breast cancer detection. Clin Chem 61:1098–1106
73. Melman YF, Shah R, Danielson K, Xiao J, Simonson B, Barth A, Chakir K, Lewis GD, Lavender Z, Truong QA et al (2015) Circulating microRNA-30d is associated with response to cardiac resynchronization therapy in heart failure and regulates cardiomyocyte Apoptosis A translational pilot study. Circulation 131:2202–2216
74. Meng X, Müller V, Milde-Langosch K, Trillsch F, Pantel K, Schwarzenbach H (2016) Diagnostic and prognostic relevance of circulating exosomal miR-373, miR-200a, miR-200b and miR-200c in patients with epithelial ovarian cancer. Oncotarget 7:16923
75. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O’Briant KC, Allen A et al (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105:10513–10518
76. Morimura R, Komatsu S, Ichikawa D, Takeshita H, Tsujiura M, Nagata H, Konishi H, Shiozaki A, Ikoma H, Okamoto K et al (2011) Novel diagnostic value of circulating miR-18a in plasma of patients with pancreatic cancer. Br J Cancer 105:1733–1740
77. Motta V, Angelici L, Nordio F, Bollati V, Fossati S, Frascati F, Tinaglia V, Bertazzi PA, Battaglia C, Baccarelli AA (2013) Integrative analysis of miRNA and inflammatory gene expression after acute particulate matter exposure. Toxicol Sci Off J Soc Toxicol 132:307–316
78. Nassirpour R, Mathur S, Gosink MM, Li Y, Shoieb AM, Wood J, O’Neil SP, Homer BL, Whiteley LO (2014) Identification of tubular injury microRNA biomarkers in urine: comparison of next-generation sequencing and qPCR-based profiling platforms. BMC Genom 15:485
79. Nielsen LB, Wang C, Sørensen K, Bang-Berthelsen CH, Hansen L, Andersen M-LM, Hougaard P, Juul A, Zhang C-Y et al (2012) Circulating levels of microRNA from children with newly diagnosed type 1 diabetes and healthy controls: evidence that miR-25 associates to residual beta-cell function and glycaemic control during disease progression. J Diabetes Res 2012:e896362
80. Ng EKO, Chong WWS, Jin H, Lam EKY, Shin VY, Yu J, Poon TCW, Ng SSM, Sung JJY (2009) Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut 58:1375–1381
81. Ng EKO, Li R, Shin VY, Jin HC, Leung CPH, Ma ESK, Pang R, Chua D, Chu K-M, Law WL et al (2013) Circulating microRNAs as specific biomarkers for breast cancer detection. PLoS ONE 8:e53141
82. Nishimura Y, Kondo C, Morikawa Y, Tonomura Y, Torii M, Yamate J, Uehara T (2015) Plasma miR-208 as a useful biomarker for drug-induced cardiotoxicity in rats. J Appl Toxicol JAT 35:173–180
83. Ogata-Kawata H, Izumiya M, Kurioka D, Honma Y, Yamada Y, Furuta K, Gunji T, Ohta H, Okamoto H, Sonoda H et al (2014) Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS ONE 9:e92921
84. Olivieri F, Antonicelli R, Lorenzi M, D’Alessandra Y, Lazzarini R, Santini G, Spazzafumo L, Lisa R, La Sala L, Galeazzi R et al (2013) Diagnostic potential of circulating miR-499-5p in elderly patients with acute non ST-elevation myocardial infarction. Int J Cardiol 167:531–536
85. Ortega FJ, Mercader JM, Catalán V, Moreno-Navarrete JM, Pueyo N, Sabater M, Gómez-Ambrosi J, Anglada R, Fernández-Formoso JA, Ricart W et al (2013) Targeting the circulating microRNA signature of obesity. Clin Chem 59:781–792
86. Ortega FJ, Mercader JM, Moreno-Navarrete JM, Rovira O, Guerra E, Esteve E, Xifra G, Martínez C, Ricart W, Rieusset J et al (2014) Profiling of circulating microRNAs reveals common microRNAs linked to type 2 diabetes that change with insulin sensitization. Diabet Care 37:1375–1383
87. Osipova J, Fischer D-C, Dangwal S, Volkmann I, Widera C, Schwarz K, Lorenzen JM, Schreiver C, Jacoby U, Heimhalt M et al (2014) Diabetes-associated microRNAs in pediatric patients with type 1 diabetes mellitus: a cross-sectional cohort study. J Clin Endocrinol Metab 99:E1661–1665
88. Pavkovic M, Riefke B, Ellinger-Ziegelbauer H (2014) Urinary microRNA profiling for identification of biomarkers after cisplatin-induced kidney injury. Toxicology 324:147–157
89. Pavkovic M, Riefke B, Frisk A-L, Gröticke I, Ellinger-Ziegelbauer H (2015) Glomerulonephritis-induced changes in urinary and kidney microRNA profiles in rats. Toxicol Sci Off J Soc Toxicol 145:348–359
90. Pavkovic M, Robinson-Cohen C, Chua AS, Nicoara O, Cárdenas-González M, Bijol V, Ramachandran K, Hampson L, Pirmohamed M, Antoine DJ et al (2016) Detection of drug-induced acute kidney injury in humans using urinary KIM-1, miR-21, -200c, and -423. Toxicol Sci Off J Soc Toxicol 152:205–213
91. Pescador N, Pérez-Barba M, Ibarra JM, Corbatón A, Martínez-Larrad MT, Serrano-Ríos M (2013) Serum circulating microRNA profiling for identification of potential type 2 diabetes and obesity biomarkers. PLoS ONE 8:e77251
92. Petriella D, De Summa S, Lacalamita R, Galetta D, Catino A, Logroscino AF, Palumbo O, Carella M, Zito FA, Simone G et al (2015) miRNA profiling in serum and tissue samples to assess noninvasive biomarkers for NSCLC clinical outcome. Tumour Biol J Int Soc Oncodev Biol, Med
93. Pezzolesi MG, Satake E, McDonnell KP, Major M, Smiles AM, Krolewski AS (2015) Circulating TGF-β1-regulated miRNAs and the risk of rapid progression to ESRD in type 1 diabetes. Diabetes 64:3285–3293
94. Pillai RS (2005) MicroRNA function: Multiple mechanisms for a tiny RNA? RNA 11:1753–1761
95. Qing S, Yuan S, Yun C, Hui H, Mao P, Wen F, Ding Y, Liu Q (2014) Serum MiRNA biomarkers serve as a fingerprint for proliferative diabetic retinopathy. Cell Physiol Biochem 34(5):1733–1740
96. Romaine SP, Tomaszewski M, Condorelli G, Samani NJ (2015) MicroRNAs in cardiovascular disease: an introduction for clinicians. Heart 101(12):921–928
97. Rong Y, Bao W, Shan Z, Liu J, Yu X, Xia S, Gao H, Wang X, Yao P, Hu FB et al (2013) Increased microRNA-146a levels in plasma of patients with newly diagnosed type 2 diabetes mellitus. PLoS ONE 8:e73272
98. Salas-Pérez F, Codner E, Valencia E, Pizarro C, Carrasco E, Pérez-Bravo F (2013) MicroRNAs miR-21a and miR-93 are down regulated in peripheral blood mononuclear cells (PBMCs) from patients with type 1 diabetes. Immunobiology 218:733–737
99. Schultz NA, Dehlendorff C, Jensen BV et al (2014) MicroRNA biomarkers in whole blood for detection of pancreatic cancer. JAMA 311:392–404
100. Shan L, Ji Q, Cheng G, Xia J, Liu D, Wu C, Zhu B, Ding Y (2015) Diagnostic value of circulating miR-21 for colorectal cancer: a meta-analysis. Cancer Biomark Sect Dis Markers 15:47–56
101. Shen J, Todd NW, Zhang H, Yu L, Lingxiao X, Mei Y, Guarnera M, Liao J, Chou A, Lu CL et al (2011) Plasma microRNAs as potential biomarkers for non-small-cell lung cancer. Lab Investig J Tech Methods Pathol 91:579–587
102. Shifeng H, Danni W, Pu C, Ping Y, Ju C, Liping Z (2013) Circulating liver-specific miR-122 as a novel potential biomarker for diagnosis of cholestatic liver injury. PLoS ONE 8:73133
103. Starkey Lewis PJ, Dear J, Platt V, Simpson KJ, Craig DGN, Antoine DJ, French NS, Dhaun N, Webb DJ, Costello EM et al (2011) Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatol Baltim Md 54:1767–1776
104. Takahashi K, Yokota S-I, Tatsumi N, Fukami T, Yokoi T, Nakajima M (2013) Cigarette smoking substantially alters plasma microRNA profiles in healthy subjects. Toxicol Appl Pharmacol 272:154–160
105. Théry C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. In: Board Juan Bonifacino Al (ed) Curr Protoc Cell Biol Chapter 3, Unit 3.22
106. Turchinovich A, Weiz L, Langheinz A, Burwinkel B (2011) Characterization of extracellular circulating microRNA. Nucl Acids Res 39:7223–7233
107. Tushuizen ME, Nieuwland R, Rustemeijer C, Hensgens BE, Sturk A, Heine RJ, Diamant M (2007) Elevated endothelial microparticles following consecutive meals are associated with vascular endothelial dysfunction in type 2 diabetes. Diabet Care 30:728–730
108. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659
109. van Schooneveld E, Wouters MC, Van der Auwera I, Peeters DJ, Wildiers H, Van Dam PA, Vergote I, Vermeulen PB, Dirix LY, Van Laere SJ (2012) Expression profiling of cancerous and normal breast tissues identifies microRNAs that are differentially expressed in serum from patients with (metastatic) breast cancer and healthy volunteers. Breast Cancer Res BCR 14:R34
110. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13:423–433
111. Villarroya-Beltri C, Gutiérrez-Vázquez C, Sánchez-Cabo F, Pérez-Hernández D, Vázquez J, Martin-Cofreces N, Martinez-Herrera DJ, Pascual-Montano A, Mittelbrunn M, Sánchez-Madrid F (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4:2980
112. Vliegenthart ADB, Shaffer JM, Clarke JI, Peeters LEJ, Caporali A, Bateman DN, Wood DM, Dargan PI, Craig DG, Moore JK et al (2015) Comprehensive microRNA profiling in acetaminophen toxicity identifies novel circulating biomarkers for human liver and kidney injury. Sci Rep 5:15501
113. Wagner J, Riwanto M, Besler C, Knau A, Fichtlscherer S, Röxe T, Zeiher AM, Landmesser U, Dimmeler S (2013) Characterization of levels and cellular transfer of circulating lipoprotein-bound microRNAs. Arterioscler Thromb Vasc Biol 33:1392–1400
114. Wang L-G, Gu J (2012) Serum microRNA-29a is a promising novel marker for early detection of colorectal liver metastasis. Cancer Epidemiol 36:e61–67
115. Wang J, Chen J, Chang P, LeBlanc A, Li D, Abbruzzesse JL, Frazier ML, Killary AM, Sen S (2009) MicroRNAs in plasma of pancreatic ductal adenocarcinoma patients as novel blood-based biomarkers of disease. Cancer Prev Res Phila Pa 2:807–813
116. Wang G-K, Zhu J-Q, Zhang J-T, Li Q, Li Y, He J, Qin Y-W, Jing Q (2010a) Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J 31:659–666
117. Wang K, Zhang S, Weber J, Baxter D, Galas DJ (2010b) Export of microRNAs and microRNA-protective protein by mammalian cells. Nucl Acids Res 38:7248–7259
118. Wang Z-X, Bian H-B, Wang J-R, Cheng Z-X, Wang K-M, De W (2011) Prognostic significance of serum miRNA-21 expression in human non-small cell lung cancer. J Surg Oncol 104:847–851
119. Wang J, Zhang Y, Zhang W, Jin Y, Dai J (2012) Association of perfluorooctanoic acid with HDL cholesterol and circulating miR-26b and miR-199-3p in workers of a fluorochemical plant and nearby residents. Environ Sci Technol 46:9274–9281
120. Wang J, Raimondo M, Guha S, Chen J, Diao L, Dong X, Wallace MB, Killary AM, Frazier ML, Woodward TA et al (2014) Circulating microRNAs in pancreatic juice as candidate biomarkers of pancreatic cancer. J Cancer 5:696–705
121. Wang C, Wan S, Yang T, Niu D, Zhang A, Yang C, Cai J, Wu J, Song J, Zhang C-Y, et al. (2016) Increased serum microRNAs are closely associated with the presence of microvascular complications in type 2 diabetes mellitus. Sci Rep 6:20032. doi:10.1038/srep20032
122. Witwer KW, Buzás EI, Bemis LT, Bora A, Lässer C, Lötvall J, Nolte-’t Hoen EN, Piper MG, Sivaraman S, Skog J, et al. (2013) Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2. doi:10.3402/jev.v2i0.20360
123. Wozniak MB, Scelo G, Muller DC, Mukeria A, Zaridze D, Brennan P (2015) Circulating microRNAs as non-invasive biomarkers for early detection of non-small-cell lung cancer. PLoS ONE 10:e0125026
124. Wu J, Yang T, Li X, Yang Q, Liu R, Huang J, Li Y, Yang C, Jiang Y (2013) Alteration of serum miR-206 and miR-133b is associated with lung carcinogenesis induced by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Toxicol Appl Pharmacol 267:238–246
125. Xie Y, Todd NW, Liu Z, Zhan M, Fang H, Peng H, Alattar M, Deepak J, Stass SA, Jiang F (2010) Altered miRNA expression in sputum for diagnosis of non-small cell lung cancer. Lung Cancer Amst Neth 67:170–176
126. Xin H, Li Y, Buller B, Katakowski M, Zhang Y, Wang X, Shang X, Zhang ZG, Chopp M (2012) Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells Dayt Ohio 30:1556–1564
127. Yang M, Chen J, Su F, Yu B, Su F, Lin L, Liu Y, Huang J-D, Song E (2011) Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 10:117
128. Yu S-L, Chen H-Y, Chang G-C, Chen C-Y, Chen H-W, Singh S, Cheng C-L, Yu C-J, Lee Y-C, Chen H-S et al (2008) MicroRNA signature predicts survival and relapse in lung cancer. Cancer Cell 13:48–57
129. Yuan T, Huang X, Woodcock M, Du M, Dittmar R, Wang Y, Tsai S, Kohli M, Boardman L, Patel T et al (2016) Plasma extracellular RNA profiles in healthy and cancer patients. Sci Rep 6:19413
130. Yuchuan H, Ya D, Jie Z, Jingqiu C, Yanrong L, Dongliang L, Changguo W, Kuoyan M, Guangneng L, Fang X et al (2014) Circulating miRNAs might be promising biomarkers to reflect the dynamic pathological changes in smoking-related interstitial fibrosis. Toxicol Ind Health 30:182–191
131. Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, Mayr A, Weger S, Oberhollenzer F, Bonora E et al (2010) Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res 107:810–817
132. Zampetaki A, Willeit P, Burr S, Yin X, Langley SR, Kiechl S, Klein R, Rossing P, Chaturvedi N, Mayr M (2016) Angiogenic microRNAs linked to incidence and progression of diabetic retinopathy in type 1 diabetes. Diabetes 65:216–227
133. Zhang Y, Jia Y, Zheng R, Guo Y, Wang Y, Guo H, Fei M, Sun S (2010) Plasma microRNA-122 as a biomarker for viral-, alcohol-, and chemical-related hepatic diseases. Clin Chem 56:1830–1838
134. Zhao F-L, Hu G-D, Wang X-F, Zhang X-H, Zhang Y-K, Yu Z-S (2012) Serum overexpression of microRNA-10b in patients with bone metastatic primary breast cancer. J Int Med Res 40(3):859–866
135. Zhao Z, He J, Zhang J, Liu M, Yang S, Li N, Li X (2014) Dysregulated miR1254 and miR579 for cardiotoxicity in patients treated with bevacizumab in colorectal cancer. Tumour Biol J Int Soc Oncodev Biol Med 35:5227–5235
136. Zhong J, He Y, Chen W, Shui X, Chen C, Lei W (2014) Circulating microRNA-19a as a potential novel biomarker for diagnosis of acute myocardial infarction. Int J Mol Sci 15:20355–20364