Review Article

Urinary miRNAs: Technical Updates

Author(s): Santhi Raveendran*, Alia Al Massih, Muna Al Hashmi, Asma Saeed, Iman Al-Azwani, Rebecca Mathew and Sara Tomei

Volume 13, Issue 2, 2024

Published on: 20 May, 2024

Page: [110 - 123] Pages: 14

DOI: 10.2174/0122115366305985240502094814

Price: $65

Open Access Journals Promotions 2
Abstract

Due to its non-invasive nature and easy accessibility, urine serves as a convenient biological fluid for research purposes. Furthermore, urine samples are uncomplicated to preserve and relatively inexpensive.

MicroRNAs (miRNAs), small molecules that regulate gene expression post-transcriptionally, play vital roles in numerous cellular processes, including apoptosis, cell differentiation, development, and proliferation. Their dysregulated expression in urine has been proposed as a potential biomarker for various human diseases, including bladder cancer. To draw reliable conclusions about the roles of urinary miRNAs in human diseases, it is essential to have dependable and reproducible methods for miRNA extraction and profiling.

In this review, we address the technical challenges associated with studying urinary miRNAs and provide an update on the current technologies used for urinary miRNA isolation, quality control assessment, and miRNA profiling, highlighting both their advantages and limitations.

Keywords: miRNA, urine, isolation, profiling, cancer, biomarkers.

Next »
Graphical Abstract
[1]
Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75(5): 843-54.
[http://dx.doi.org/10.1016/0092-8674(93)90529-Y] [PMID: 8252621]
[2]
Reinhart BJ, Slack FJ, Basson M, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000; 403(6772): 901-6.
[http://dx.doi.org/10.1038/35002607] [PMID: 10706289]
[3]
Pal AS, Kasinski AL. Animal Models to Study MicroRNA Function. Adv Cancer Res 2017; 135: 53-118.
[http://dx.doi.org/10.1016/bs.acr.2017.06.006] [PMID: 28882225]
[4]
Ramaswamy P, Christopher R, Pal PK, Yadav R. MicroRNAs to differentiate Parkinsonian disorders: Advances in biomarkers and therapeutics. J Neurol Sci 2018; 394: 26-37.
[http://dx.doi.org/10.1016/j.jns.2018.08.032] [PMID: 30196132]
[5]
Ambros V. The functions of animal microRNAs. Nature 2004; 431(7006): 350-5.
[http://dx.doi.org/10.1038/nature02871] [PMID: 15372042]
[6]
Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116(2): 281-97.
[http://dx.doi.org/10.1016/S0092-8674(04)00045-5] [PMID: 14744438]
[7]
Lu M, Zhang Q, Deng M, et al. An analysis of human microRNA and disease associations. PLoS One 2008; 3(10): e3420.
[http://dx.doi.org/10.1371/journal.pone.0003420] [PMID: 18923704]
[8]
Peng Y, Croce CM. The role of MicroRNAs in human cancer. Signal Transduct Target Ther 2016; 1(1): 15004.
[http://dx.doi.org/10.1038/sigtrans.2015.4] [PMID: 29263891]
[9]
Li P, Shan JX, Chen XH, et al. Epigenetic silencing of microRNA-149 in cancer-associated fibroblasts mediates prostaglandin E2/interleukin-6 signaling in the tumor microenvironment. Cell Res 2015; 25(5): 588-603.
[http://dx.doi.org/10.1038/cr.2015.51] [PMID: 25916550]
[10]
Tomei S, Volontè A, Ravindran S, et al. MicroRNA Expression Profile Distinguishes Glioblastoma Stem Cells from Differentiated Tumor Cells. J Pers Med 2021; 11(4): 264.
[http://dx.doi.org/10.3390/jpm11040264] [PMID: 33916317]
[11]
Sharari S, Kabeer B, Mohammed I, et al. Understanding the Role of GLUT2 in Dysglycemia Associated with Fanconi–Bickel Syndrome. Biomedicines 2022; 10(9): 2114.
[http://dx.doi.org/10.3390/biomedicines10092114] [PMID: 36140215]
[12]
Mori MA, Ludwig RG, Martin GR, Brandão BB, Kahn CR. Extracellular miRNAs: From Biomarkers to Mediators of Physiology and Disease. Cell Metab 2019; 30(4): 656-73.
[http://dx.doi.org/10.1016/j.cmet.2019.07.011] [PMID: 31447320]
[13]
Cione E, Cannataro R, Gallelli L, Sarro DG, Caroleo MC. Exosome microRNAs in Metabolic Syndrome as Tools for the Early Monitoring of Diabetes and Possible Therapeutic Options. Pharmaceuticals 2021; 14(12): 1257.
[http://dx.doi.org/10.3390/ph14121257] [PMID: 34959658]
[14]
Cannataro R, Carbone L, Petro JL, et al. Sarcopenia: Etiology, Nutritional Approaches, and miRNAs. Int J Mol Sci 2021; 22(18): 9724.
[http://dx.doi.org/10.3390/ijms22189724] [PMID: 34575884]
[15]
Bhatt K, Mi QS, Dong Z. microRNAs in kidneys: Biogenesis, regulation, and pathophysiological roles. Am J Physiol Renal Physiol 2011; 300(3): F602-10.
[http://dx.doi.org/10.1152/ajprenal.00727.2010] [PMID: 21228106]
[16]
Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23(20): 4051-60.
[http://dx.doi.org/10.1038/sj.emboj.7600385] [PMID: 15372072]
[17]
Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006; 13(12): 1097-101.
[http://dx.doi.org/10.1038/nsmb1167] [PMID: 17099701]
[18]
Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: MicroRNAs can up-regulate translation. Science 2007; 318(5858): 1931-4.
[http://dx.doi.org/10.1126/science.1149460] [PMID: 18048652]
[19]
Decramer S, de Peredo AG, Breuil B, et al. Urine in clinical proteomics. Mol Cell Proteomics 2008; 7(10): 1850-62.
[http://dx.doi.org/10.1074/mcp.R800001-MCP200] [PMID: 18667409]
[20]
DF P. Composition and concentrative properties of human urine. Washington, DC: National Aeronautics and Space Administration 1971.
[21]
Drangert J-O. Fighting urine blindness to provide more sanitation options. Water SA 1998; 24(2): 157-64.
[22]
Garrow JS. Human nutrition and dietetics. 1993.
[23]
Garrod AE. The incidence of alkaptonuria: A study in chemical individuality. 1902. Mol Med 1996; 2(3): 274-82.
[http://dx.doi.org/10.1007/BF03401625] [PMID: 8784780]
[24]
Bouatra S, Aziat F, Mandal R, et al. The human urine metabolome. PLoS One 2013; 8(9): e73076.
[http://dx.doi.org/10.1371/journal.pone.0073076] [PMID: 24023812]
[25]
Gheinani AH, Vögeli M, Baumgartner U, et al. Improved isolation strategies to increase the yield and purity of human urinary exosomes for biomarker discovery. Sci Rep 2018; 8(1): 3945.
[http://dx.doi.org/10.1038/s41598-018-22142-x] [PMID: 29500443]
[26]
Armstrong DA, Dessaint JA, Ringelberg CS, et al. Pre-Analytical Handling Conditions and Small RNA Recovery from Urine for miRNA Profiling. J Mol Diagn 2018; 20(5): 565-71.
[http://dx.doi.org/10.1016/j.jmoldx.2018.04.003] [PMID: 29936254]
[27]
Mall C, Rocke DM, Johnson DB, Weiss RH. Stability of miRNA in human urine supports its biomarker potential. Biomarkers Med 2013; 7(4): 623-31.
[http://dx.doi.org/10.2217/bmm.13.44] [PMID: 23905899]
[28]
Hanke M, Hoefig K, Merz H, et al. A robust methodology to study urine microRNA as tumor marker: MicroRNA-126 and microRNA-182 are related to urinary bladder cancer. Urol Oncol 2010; 28(6): 655-61.
[http://dx.doi.org/10.1016/j.urolonc.2009.01.027] [PMID: 19375957]
[29]
Chorley BN, Atabakhsh E, Doran G, et al. Methodological considerations for measuring biofluid-based microRNA biomarkers. Crit Rev Toxicol 2021; 51(3): 264-82.
[http://dx.doi.org/10.1080/10408444.2021.1907530] [PMID: 34038674]
[30]
Koritzinsky EH, Street JM, Chari RR, et al. Circadian variation in the release of small extracellular vesicles can be normalized by vesicle number or TSG101. Am J Physiol Renal Physiol 2019; 317(5): F1098-110.
[http://dx.doi.org/10.1152/ajprenal.00568.2017] [PMID: 31390267]
[31]
Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011; 13(4): 423-33.
[http://dx.doi.org/10.1038/ncb2210] [PMID: 21423178]
[32]
Marzi MJ, Montani F, Carletti RM, et al. Optimization and Standardization of Circulating MicroRNA Detection for Clinical Application: The miR-Test Case. Clin Chem 2016; 62(5): 743-54.
[http://dx.doi.org/10.1373/clinchem.2015.251942] [PMID: 27127244]
[33]
Vago R, Radano G, Zocco D, Zarovni N. Urine stabilization and normalization strategies favor unbiased analysis of urinary EV content. Sci Rep 2022; 12(1): 17663.
[http://dx.doi.org/10.1038/s41598-022-22577-3] [PMID: 36271135]
[34]
Merchant ML, Rood IM, Deegens JKJ, Klein JB. Isolation and characterization of urinary extracellular vesicles: Implications for biomarker discovery. Nat Rev Nephrol 2017; 13(12): 731-49.
[http://dx.doi.org/10.1038/nrneph.2017.148] [PMID: 29081510]
[35]
Mathew R, Mattei V, Hashmi AM, Tomei S. Updates on the Current Technologies for microRNA Profiling. MicroRNA 2020; 9(1): 17-24.
[http://dx.doi.org/10.2174/22115374OTkyrODMeTcVY] [PMID: 31264553]
[36]
Patnaik SK, Kumar P, Yadav P, et al. Can microRNA profiles predict corticosteroid responsiveness in childhood nephrotic syndrome? A study protocol. BMJ Paediatr Open 2018; 2(1): e000319.
[http://dx.doi.org/10.1136/bmjpo-2018-000319] [PMID: 30555935]
[37]
Guelfi G, Cochetti G, Stefanetti V, et al. Next Generation Sequencing of urine exfoliated cells: An approach of prostate cancer microRNAs research. Sci Rep 2018; 8(1): 7111.
[http://dx.doi.org/10.1038/s41598-018-24236-y] [PMID: 29740090]
[38]
Amuran GG, Eyuboglu IP, Tinay I, Akkiprik M. New Insights in Bladder Cancer Diagnosis: Urinary miRNAs and Proteins. Med Sci 2018; 6(4): 113.
[http://dx.doi.org/10.3390/medsci6040113] [PMID: 30544619]
[39]
Kutwin P, Konecki T, Borkowska EM, Borszyńska TM, Jabłonowski Z. Urine miRNA as a potential biomarker for bladder cancer detection – A meta-analysis. Cent European J Urol 2018; 71(2): 177-85.
[http://dx.doi.org/10.5173/ceju.2018.1605] [PMID: 30038807]
[40]
von Siebenthal M, Besic M, Gheinani AH, et al. Urinary miRNA profiles discriminate between obstruction-induced bladder dysfunction and healthy controls. Sci Rep 2021; 11(1): 10204.
[http://dx.doi.org/10.1038/s41598-021-89535-3] [PMID: 33986358]
[41]
Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162(1): 156-9.
[http://dx.doi.org/10.1016/0003-2697(87)90021-2] [PMID: 2440339]
[42]
Cacheux J, Bancaud A, Leichlé T, Cordelier P. Technological Challenges and Future Issues for the Detection of Circulating MicroRNAs in Patients With Cancer. Front Chem 2019; 7: 815.
[http://dx.doi.org/10.3389/fchem.2019.00815] [PMID: 31850308]
[43]
Kim YK, Yeo J, Kim B, Ha M, Kim VN. Short structured RNAs with low GC content are selectively lost during extraction from a small number of cells. Mol Cell 2012; 46(6): 893-5.
[http://dx.doi.org/10.1016/j.molcel.2012.05.036] [PMID: 22749402]
[44]
Vlasov VV, Rykova EIu, Ponomareva AA, et al. Circulating microRNAs in lung cancer: Prospects for diagnostics, prognosis and prediction of antitumor treatment efficiency. Mol Biol 2015; 49(1): 55-66.
[PMID: 25916110]
[45]
Zaporozhchenko IA, Morozkin ES, Skvortsova TE, et al. A phenolfree method for isolation of microRNA from biological fluids. Anal Biochem 2015; 479: 43-7.
[http://dx.doi.org/10.1016/j.ab.2015.03.028] [PMID: 25843265]
[46]
Lekchnov EA, Zaporozhchenko IA, Morozkin ES, Bryzgunova OE, Vlassov VV, Laktionov PP. Protocol for miRNA isolation from biofluids. Anal Biochem 2016; 499: 78-84.
[http://dx.doi.org/10.1016/j.ab.2016.01.025] [PMID: 26874020]
[47]
Bryzgunova O, Konoshenko M, Zaporozhchenko I, Yakovlev A, Laktionov P. Isolation of Cell-Free miRNA from Biological Fluids: Influencing Factors and Methods. Diagnostics 2021; 11(5): 865.
[http://dx.doi.org/10.3390/diagnostics11050865] [PMID: 34064927]
[48]
Wang G, Szeto CC. Methods of microRNA quantification in urinary sediment. Methods Mol Biol 2013; 1024: 211-20.
[http://dx.doi.org/10.1007/978-1-62703-453-1_17] [PMID: 23719954]
[49]
Grimaldi AM, Lapucci C, Salvatore M, Incoronato M, Ferrari M. Urinary miRNAs as a Diagnostic Tool for Bladder Cancer: A Systematic Review. Biomedicines 2022; 10(11): 2766.
[http://dx.doi.org/10.3390/biomedicines10112766] [PMID: 36359288]
[50]
Wang G, Tam LS, Li EKM, et al. Serum and urinary cell-free MiR-146a and MiR-155 in patients with systemic lupus erythematosus. J Rheumatol 2010; 37(12): 2516-22.
[http://dx.doi.org/10.3899/jrheum.100308] [PMID: 20952466]
[51]
Zhang DZ, Lau KM, Chan ESY, et al. Cell-free urinary microRNA-99a and microRNA-125b are diagnostic markers for the non-invasive screening of bladder cancer. PLoS One 2014; 9(7): e100793.
[http://dx.doi.org/10.1371/journal.pone.0100793] [PMID: 25014919]
[52]
Han Q, Zhang Y, Jiao T, et al. Urinary sediment microRNAs can be used as potential noninvasive biomarkers for diagnosis, reflecting the severity and prognosis of diabetic nephropathy. Nutr Diabetes 2021; 11(1): 24.
[http://dx.doi.org/10.1038/s41387-021-00166-z] [PMID: 34193814]
[53]
Bellingham SA, Guo BB, Coleman BM, Hill AF. Exosomes: Vehicles for the transfer of toxic proteins associated with neurodegenerative diseases? Front Physiol 2012; 3: 124.
[http://dx.doi.org/10.3389/fphys.2012.00124] [PMID: 22563321]
[54]
Vojtech L, Woo S, Hughes S, et al. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res 2014; 42(11): 7290-304.
[http://dx.doi.org/10.1093/nar/gku347] [PMID: 24838567]
[55]
Perri M, Lucente M, Cannataro R, et al. Variation in Immune-Related microRNAs Profile in Human Milk Amongst Lactating Women. MicroRNA 2018; 7(2): 107-14.
[http://dx.doi.org/10.2174/2211536607666180206150503] [PMID: 29412128]
[56]
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9(6): 654-9.
[http://dx.doi.org/10.1038/ncb1596] [PMID: 17486113]
[57]
Alvarez ML. Isolation of urinary exosomes for RNA biomarker discovery using a simple, fast, and highly scalable method. Methods Mol Biol 2014; 1182: 145-70.
[http://dx.doi.org/10.1007/978-1-4939-1062-5_13] [PMID: 25055908]
[58]
Cheng L, Sun X, Scicluna BJ, Coleman BM, Hill AF. Characterization and deep sequencing analysis of exosomal and non-exosomal miRNA in human urine. Kidney Int 2014; 86(2): 433-44.
[http://dx.doi.org/10.1038/ki.2013.502] [PMID: 24352158]
[59]
Lv LL, Cao Y, Liu D, et al. Isolation and quantification of microRNAs from urinary exosomes/microvesicles for biomarker discovery. Int J Biol Sci 2013; 9(10): 1021-31.
[http://dx.doi.org/10.7150/ijbs.6100] [PMID: 24250247]
[60]
Ravi KR, Khosroheidari M, DiStefano JK. A modified precipitation method to isolate urinary exosomes. J Vis Exp 2015; 51158(95): 51158.
[http://dx.doi.org/10.3791/51158] [PMID: 25651044]
[61]
Li P, Kaslan M, Lee SH, Yao J, Gao Z. Progress in Exosome Isolation Techniques. Theranostics 2017; 7(3): 789-804.
[http://dx.doi.org/10.7150/thno.18133] [PMID: 28255367]
[62]
Alvarez ML, Khosroheidari M, Ravi KR, DiStefano JK. Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers. Kidney Int 2012; 82(9): 1024-32.
[http://dx.doi.org/10.1038/ki.2012.256] [PMID: 22785172]
[63]
Channavajjhala SK, Rossato M, Morandini F, et al. Optimizing the purification and analysis of miRNAs from urinary exosomes. Clinical Chem Laboratory Med (CCLM) 2014; 52(3): 345-54.
[http://dx.doi.org/10.1515/cclm-2013-0562] [PMID: 24101370]
[64]
Fleige S, Pfaffl MW. RNA integrity and the effect on the real-time qRT-PCR performance. Mol Aspects Med 2006; 27(2-3): 126-39.
[http://dx.doi.org/10.1016/j.mam.2005.12.003] [PMID: 16469371]
[65]
Becker C, Fickinger HA, Riedmaier I, Pfaffl MW. mRNA and microRNA quality control for RT-qPCR analysis. Methods 2010; 50(4): 237-43.
[http://dx.doi.org/10.1016/j.ymeth.2010.01.010] [PMID: 20079844]
[66]
Fleige S, Walf V, Huch S, Prgomet C, Sehm J, Pfaffl MW. Comparison of relative mRNA quantification models and the impact of RNA integrity in quantitative real-time RT-PCR. Biotechnol Lett 2006; 28(19): 1601-13.
[http://dx.doi.org/10.1007/s10529-006-9127-2] [PMID: 16900335]
[67]
Schroeder A, Mueller O, Stocker S, et al. The RIN: An RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 2006; 7(1): 3.
[http://dx.doi.org/10.1186/1471-2199-7-3] [PMID: 16448564]
[68]
Tomei S, Manjunath HS, Murugesan S, Khodor AS. The Salivary miRNome: A Promising Biomarker of Disease. MicroRNA 2021; 10(1): 29-38.
[http://dx.doi.org/10.2174/2211536610666210412154455] [PMID: 33845754]
[69]
Kang K, Peng X, Luo J, Gou D. Identification of circulating miRNA biomarkers based on global quantitative real-time PCR profiling. J Anim Sci Biotechnol 2012; 3(1): 4.
[http://dx.doi.org/10.1186/2049-1891-3-4] [PMID: 22958414]
[70]
Hunt EA, Broyles D, Head T, Deo SK. MicroRNA Detection: Current Technology and Research Strategies. Annu Rev Anal Chem 2015; 8(1): 217-37.
[http://dx.doi.org/10.1146/annurev-anchem-071114-040343] [PMID: 25973944]
[71]
Krichevsky AM. MicroRNA profiling: From dark matter to white matter, or identifying new players in neurobiology. ScientificWorldJournal 2007; 7: 155-66.
[http://dx.doi.org/10.1100/tsw.2007.201] [PMID: 17982589]
[72]
Chen C, Ridzon DA, Broomer AJ, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005; 33(20): e179.
[http://dx.doi.org/10.1093/nar/gni178] [PMID: 16314309]
[73]
Liu DZ, Tian Y, Ander BP, et al. Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 2010; 30(1): 92-101.
[http://dx.doi.org/10.1038/jcbfm.2009.186] [PMID: 19724284]
[74]
Siddika T, Heinemann IU. Bringing MicroRNAs to Light: Methods for MicroRNA Quantification and Visualization in Live Cells. Front Bioeng Biotechnol 2021; 8: 619583.
[http://dx.doi.org/10.3389/fbioe.2020.619583] [PMID: 33537295]
[75]
Mamdouh S, Sherif H, Romeih M, Elesaily K. Urine micro-RNA signature as a potential non-invasive diagnostic biomarker in bladder cancer. Asian Pac J Cancer Prev 2023; 24(1): 121-31.
[http://dx.doi.org/10.31557/APJCP.2023.24.1.121] [PMID: 36708560]
[76]
Stuopelyte K, Daniunaite K, Bakavicius A, Lazutka JR, Jankevicius F, Jarmalaite S. The utility of urine-circulating miRNAs for detection of prostate cancer. Br J Cancer 2016; 115(6): 707-15.
[http://dx.doi.org/10.1038/bjc.2016.233] [PMID: 27490805]
[77]
Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: Approaches and considerations. Nat Rev Genet 2012; 13(5): 358-69.
[http://dx.doi.org/10.1038/nrg3198] [PMID: 22510765]
[78]
Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 2000; 25(2): 169-93.
[http://dx.doi.org/10.1677/jme.0.0250169] [PMID: 11013345]
[79]
Niu Y, Xia S, Su M, et al. Direct S-Poly(T) Plus assay in quantification of microRNAs without RNA extraction and its implications in colorectal cancer biomarker studies. J Transl Med 2019; 17(1): 316.
[http://dx.doi.org/10.1186/s12967-019-2061-6] [PMID: 31547825]
[80]
Dheda K, Huggett JF, Chang JS, et al. The implications of using an inappropriate reference gene for real-time reverse transcription PCR data normalization. Anal Biochem 2005; 344(1): 141-3.
[http://dx.doi.org/10.1016/j.ab.2005.05.022] [PMID: 16054107]
[81]
Sørby LA, Andersen SN, Bukholm IRK, Jacobsen MB. Evaluation of suitable reference genes for normalization of real-time reverse transcription PCR analysis in colon cancer. J Exp Clin Cancer Res 2010; 29(1): 144.
[http://dx.doi.org/10.1186/1756-9966-29-144] [PMID: 21059236]
[82]
Kiss T. Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 2002; 109(2): 145-8.
[http://dx.doi.org/10.1016/S0092-8674(02)00718-3] [PMID: 12007400]
[83]
Bratkovič T, Rogelj B. The many faces of small nucleolar RNAs. Biochim Biophys Acta Gene Regul Mech 2014; 1839(6): 438-43.
[http://dx.doi.org/10.1016/j.bbagrm.2014.04.009] [PMID: 24735946]
[84]
Galiveti CR, Rozhdestvensky TS, Brosius J, Lehrach H, Konthur Z. Application of housekeeping npcRNAs for quantitative expression analysis of human transcriptome by real-time PCR. RNA 2010; 16(2): 450-61.
[http://dx.doi.org/10.1261/rna.1755810] [PMID: 20040593]
[85]
Holley CL, Topkara VK. An introduction to small non-coding RNAs: MiRNA and snoRNA. Cardiovasc Drugs Ther 2011; 25(2): 151-9.
[http://dx.doi.org/10.1007/s10557-011-6290-z] [PMID: 21573765]
[86]
Liang J, Wen J, Huang Z, Chen X, Zhang B, Chu L. Small Nucleolar RNAs: Insight Into Their Function in Cancer. Front Oncol 2019; 9: 587.
[http://dx.doi.org/10.3389/fonc.2019.00587] [PMID: 31338327]
[87]
Shuai S, Suzuki H, Navarro DA, et al. The U1 spliceosomal RNA is recurrently mutated in multiple cancers. Nature 2019; 574(7780): 712-6.
[http://dx.doi.org/10.1038/s41586-019-1651-z] [PMID: 31597163]
[88]
Dong X, Ding S, Yu M, et al. Small Nuclear RNAs (U1, U2, U5) in Tumor-Educated Platelets Are Downregulated and Act as Promising Biomarkers in Lung Cancer. Front Oncol 2020; 10: 1627.
[http://dx.doi.org/10.3389/fonc.2020.01627] [PMID: 32903345]
[89]
Etheridge A, Lee I, Hood L, Galas D, Wang K. Extracellular microRNA: A new source of biomarkers. Mutat Res 2011; 717(1-2): 85-90.
[http://dx.doi.org/10.1016/j.mrfmmm.2011.03.004] [PMID: 21402084]
[90]
Veryaskina YA, Titov SE, Zhimulev IF. Reference Genes for qPCR Based miRNA Expression Profiling in 14 Human Tissues. Med Princ Pract 2022; 31(4): 322-32.
[http://dx.doi.org/10.1159/000524283] [PMID: 35354155]
[91]
Kang HW, Byun YJ, Moon SM, et al. Urinary hsv2-miR-H9 to hsa-miR-3659 ratio is an effective marker for discriminating prostate cancer from benign prostate hyperplasia in patients within the prostate-specific antigen grey zone. Investig Clin Urol 2022; 63(2): 238-44.
[http://dx.doi.org/10.4111/icu.20210493] [PMID: 35244999]
[92]
Motameny S, Wolters S, Nürnberg P, Schumacher B. Next Generation Sequencing of miRNAs – Strategies, Resources and Methods. Genes 2010; 1(1): 70-84.
[http://dx.doi.org/10.3390/genes1010070] [PMID: 24710011]
[93]
Wyman SK, Knouf EC, Parkin RK, et al. Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res 2011; 21(9): 1450-61.
[http://dx.doi.org/10.1101/gr.118059.110] [PMID: 21813625]
[94]
Bar M, Wyman SK, Fritz BR, et al. MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries. Stem Cells 2008; 26(10): 2496-505.
[http://dx.doi.org/10.1634/stemcells.2008-0356] [PMID: 18583537]
[95]
Hu Y, Lan W, Miller D. Next-Generation Sequencing for MicroRNA Expression Profile. Methods Mol Biol 2017; 1617: 169-77.
[http://dx.doi.org/10.1007/978-1-4939-7046-9_12] [PMID: 28540684]
[96]
Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol 2000; 7(1-2): 203-14.
[http://dx.doi.org/10.1089/10665270050081478] [PMID: 10890397]
[97]
Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10(3): R25.
[http://dx.doi.org/10.1186/gb-2009-10-3-r25] [PMID: 19261174]
[98]
Bedognetti D, Balwit JM, Wang E, et al. SITC/iSBTc Cancer Immunotherapy Biomarkers Resource Document: Online resources and useful tools - A compass in the land of biomarker discovery. J Transl Med 2011; 9(1): 155.
[http://dx.doi.org/10.1186/1479-5876-9-155] [PMID: 21929757]
[99]
Kong W, Zhao JJ, He L, Cheng JQ. Strategies for profiling MicroRNA expression. J Cell Physiol 2009; 218(1): 22-5.
[http://dx.doi.org/10.1002/jcp.21577] [PMID: 18767038]
[100]
Wang H, Ach RA, Curry B. Direct and sensitive miRNA profiling from low-input total RNA. RNA 2007; 13(1): 151-9.
[http://dx.doi.org/10.1261/rna.234507] [PMID: 17105992]
[101]
Geiss GK, Bumgarner RE, Birditt B, et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 2008; 26(3): 317-25.
[http://dx.doi.org/10.1038/nbt1385] [PMID: 18278033]
[102]
Jet T, Gines G, Rondelez Y, Taly V. Advances in multiplexed techniques for the detection and quantification of microRNAs. Chem Soc Rev 2021; 50(6): 4141-61.
[http://dx.doi.org/10.1039/D0CS00609B] [PMID: 33538706]
[103]
Manjunath HS, Khulaifi AM, Sidahmed H, et al. Gene Expression Profiling of FFPE Samples: A Titration Test. Technol Cancer Res Treat 2022; 21: 15330338221129710.
[http://dx.doi.org/10.1177/15330338221129710] [PMID: 36415121]
[104]
Reis PP, Waldron L, Goswami RS, et al. mRNA transcript quantification in archival samples using multiplexed, color-coded probes. BMC Biotechnol 2011; 11(1): 46.
[http://dx.doi.org/10.1186/1472-6750-11-46] [PMID: 21549012]
[105]
Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11(9): 597-610.
[http://dx.doi.org/10.1038/nrg2843] [PMID: 20661255]
[106]
Sun IO, Lerman LO. Urinary microRNA in kidney disease: Utility and roles. Am J Physiol Renal Physiol 2019; 316(5): F785-93.
[http://dx.doi.org/10.1152/ajprenal.00368.2018] [PMID: 30759023]
[107]
Garzon R, Heaphy CEA, Havelange V, et al. MicroRNA 29b functions in acute myeloid leukemia. Blood 2009; 114(26): 5331-41.
[http://dx.doi.org/10.1182/blood-2009-03-211938] [PMID: 19850741]
[108]
Enokida H, Yoshino H, Matsushita R, Nakagawa M. The role of microRNAs in bladder cancer. Investig Clin Urol 2016; 57(S1): S60-76.
[http://dx.doi.org/10.4111/icu.2016.57.S1.S60]
[109]
Hofbauer SL, de Martino M, Lucca I, et al. A urinary microRNA (miR) signature for diagnosis of bladder cancer. Urol Oncol 2018; 36(12): e531-8.
[http://dx.doi.org/10.1016/j.urolonc.2018.09.006]
[110]
Burk U, Schubert J, Wellner U, et al. A reciprocal repression between ZEB1 and members of the miR‐200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008; 9(6): 582-9.
[http://dx.doi.org/10.1038/embor.2008.74] [PMID: 18483486]
[111]
Adam L, Zhong M, Choi W, et al. miR-200 expression regulates epithelial-to-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res 2009; 15(16): 5060-72.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-2245] [PMID: 19671845]
[112]
Mongroo PS, Rustgi AK. The role of the miR-200 family in epithelial-mesenchymal transition. Cancer Biol Ther 2010; 10(3): 219-22.
[http://dx.doi.org/10.4161/cbt.10.3.12548] [PMID: 20592490]
[113]
Kim SM, Kang HW, Kim WT, et al. Cell-Free microRNA-214 From Urine as a Biomarker for Non-Muscle-Invasive Bladder Cancer. Korean J Urol 2013; 54(11): 791-6.
[http://dx.doi.org/10.4111/kju.2013.54.11.791] [PMID: 24255763]
[114]
Wang Y, Huang J, Yang T. Circulating miR-214 level and its correlation with the extent of coronary lesion in patients with acute myocardial infarction. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2015; 40(4): 362-6.
[http://dx.doi.org/10.11817/j.issn.1672-7347.2015.04.004] [PMID: 25931214]
[115]
Zhang X, Zhang Y, Liu X, et al. Direct quantitative detection for cell-free miR-155 in urine: A potential role in diagnosis and prognosis for non-muscle invasive bladder cancer. Oncotarget 2016; 7(3): 3255-66.
[http://dx.doi.org/10.18632/oncotarget.6487] [PMID: 26657502]
[116]
Xie Y, Ma X, Chen L, et al. MicroRNAs with prognostic significance in bladder cancer: A systematic review and meta-analysis. Sci Rep 2017; 7(1): 5619.
[http://dx.doi.org/10.1038/s41598-017-05801-3] [PMID: 28717125]
[117]
Wang H, Men CP. Correlation of Increased Expression of MicroRNA-155 in Bladder Cancer and Prognosis. Lab Med 2015; 46(2): 118-22.
[http://dx.doi.org/10.1309/LMWR9CEA2K2XVSOX] [PMID: 25918190]
[118]
Yun SJ, Jeong P, Kim WT, et al. Cell-free microRNAs in urine as diagnostic and prognostic biomarkers of bladder cancer. Int J Oncol 2012; 41(5): 1871-8.
[http://dx.doi.org/10.3892/ijo.2012.1622] [PMID: 22961325]
[119]
Zhang HH, Qi F, Cao YH, Zu XB, Chen MF. Expression and clinical significance of microRNA-21, maspin and vascular endothelial growth factor-C in bladder cancer. Oncol Lett 2015; 10(4): 2610-6.
[http://dx.doi.org/10.3892/ol.2015.3540] [PMID: 26622898]
[120]
Eissa S, Matboli M, Hegazy MGA, Kotb YM, Essawy NOE. Evaluation of urinary microRNA panel in bladder cancer diagnosis: Relation to bilharziasis. Transl Res 2015; 165(6): 731-9.
[http://dx.doi.org/10.1016/j.trsl.2014.12.008] [PMID: 25620614]
[121]
Long JD, Sullivan TB, Humphrey J, et al. A non-invasive miRNA based assay to detect bladder cancer in cell-free urine. Am J Transl Res 2015; 7(11): 2500-9.
[PMID: 26807194]
[122]
Sasaki H, Yoshiike M, Nozawa S, et al. Expression Level of Urinary MicroRNA-146a-5p Is Increased in Patients With Bladder Cancer and Decreased in Those After Transurethral Resection. Clin Genitourin Cancer 2016; 14(5): e493-9.
[http://dx.doi.org/10.1016/j.clgc.2016.04.002] [PMID: 27157639]
[123]
Piao XM, Jeong P, Kim YH, et al. Urinary cell‐free microRNA biomarker could discriminate bladder cancer from benign hematuria. Int J Cancer 2019; 144(2): 380-8.
[http://dx.doi.org/10.1002/ijc.31849] [PMID: 30183088]
[124]
Mengual L, Lozano JJ, Torres IM, Gazquez C, Ribal MJ, Alcaraz A. Using microRNA profiling in urine samples to develop a non-invasive test for bladder cancer. Int J Cancer 2013; 133(11): n/a.
[http://dx.doi.org/10.1002/ijc.28274] [PMID: 23686449]
[125]
Pardini B, Cordero F, Naccarati A, et al. microRNA profiles in urine by next-generation sequencing can stratify bladder cancer subtypes. Oncotarget 2018; 9(29): 20658-69.
[http://dx.doi.org/10.18632/oncotarget.25057] [PMID: 29755679]
[126]
Lin H, Shi X, Li H, et al. Urinary Exosomal miRNAs as biomarkers of bladder Cancer and experimental verification of mechanism of miR-93-5p in bladder Cancer. BMC Cancer 2021; 21(1): 1293.
[http://dx.doi.org/10.1186/s12885-021-08926-x] [PMID: 34861847]
[127]
Garrastacho RM, Santos BC, Line A, et al. Extracellular vesicles as a source of prostate cancer biomarkers in liquid biopsies: A decade of research. Br J Cancer 2022; 126(3): 331-50.
[http://dx.doi.org/10.1038/s41416-021-01610-8] [PMID: 34811504]
[128]
Bryant RJ, Pawlowski T, Catto JWF, et al. Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer 2012; 106(4): 768-74.
[http://dx.doi.org/10.1038/bjc.2011.595] [PMID: 22240788]
[129]
Foj L, Ferrer F, Serra M, et al. Exosomal and Non-Exosomal Urinary miRNAs in Prostate Cancer Detection and Prognosis. Prostate 2017; 77(6): 573-83.
[http://dx.doi.org/10.1002/pros.23295] [PMID: 27990656]
[130]
Selth LA, Das R, Townley SL, et al. A ZEB1-miR-375-YAP1 pathway regulates epithelial plasticity in prostate cancer. Oncogene 2017; 36(1): 24-34.
[http://dx.doi.org/10.1038/onc.2016.185] [PMID: 27270433]
[131]
Paiva RM, Zauli DAG, Neto BS, Brum IS. Urinary microRNAs expression in prostate cancer diagnosis: A systematic review. Clin Transl Oncol 2020; 22(11): 2061-73.
[http://dx.doi.org/10.1007/s12094-020-02349-z] [PMID: 32323148]
[132]
Ghorbanmehr N, Gharbi S, Korsching E, Tavallaei M, Einollahi B, Mowla SJ. miR‐21‐5p, miR‐141‐3p, and miR‐205‐5p levels in urine—promising biomarkers for the identification of prostate and bladder cancer. Prostate 2019; 79(1): 88-95.
[http://dx.doi.org/10.1002/pros.23714] [PMID: 30194772]
[133]
Guadarrama SAI, Montor MJG, Escareño RC, et al. Urinary microRNA-based signature improves accuracy of detection of clinically relevant prostate cancer within the prostate-specific antigen grey zone. Mol Med Rep 2016; 13(6): 4549-60.
[http://dx.doi.org/10.3892/mmr.2016.5095] [PMID: 27081843]
[134]
Markert L, Holdmann J, Klinger C, et al. Small RNAs as biomarkers to differentiate benign and malign prostate diseases: An alternative for transrectal punch biopsy of the prostate? PLoS One 2021; 16(3): e0247930.
[http://dx.doi.org/10.1371/journal.pone.0247930] [PMID: 33760831]
[135]
Tian L, Fang Y, Xue J, Chen J. Four microRNAs promote prostate cell proliferation with regulation of PTEN and its downstream signals in vitro. PLoS One 2013; 8(9): e75885.
[http://dx.doi.org/10.1371/journal.pone.0075885] [PMID: 24098737]
[136]
Boyerinas B, Park SM, Hau A, Murmann AE, Peter ME. The role of let-7 in cell differentiation and cancer. Endocr Relat Cancer 2010; 17(1): F19-36.
[http://dx.doi.org/10.1677/ERC-09-0184] [PMID: 19779035]
[137]
Siegel RL, Miller KD, Jemal A. Cancer statistics CA Cancer J Clin 2020; 70(1): 7-30.
[http://dx.doi.org/10.3322/caac.21590] [PMID: 31912902]
[138]
von Brandenstein M, Pandarakalam JJ, Kroon L, et al. MicroRNA 15a, inversely correlated to PKCα, is a potential marker to differentiate between benign and malignant renal tumors in biopsy and urine samples. Am J Pathol 2012; 180(5): 1787-97.
[http://dx.doi.org/10.1016/j.ajpath.2012.01.014] [PMID: 22429968]
[139]
Mytsyk Y, Dosenko V, Borys Y, et al. MicroRNA-15a expression measured in urine samples as a potential biomarker of renal cell carcinoma. Int Urol Nephrol 2018; 50(5): 851-9.
[http://dx.doi.org/10.1007/s11255-018-1841-x] [PMID: 29549624]
[140]
Li G, Zhao A, Péoch M, Cottier M, Mottet N. Detection of urinary cell-free miR-210 as a potential tool of liquid biopsy for clear cell renal cell carcinoma. Urol Oncol 2017; 35(5): 294-9.
[http://dx.doi.org/10.1016/j.urolonc.2016.12.007] [PMID: 28089386]
[141]
Cochetti G, Cari L, Nocentini G, et al. Detection of urinary miRNAs for diagnosis of clear cell renal cell carcinoma. Sci Rep 2020; 10(1): 21290.
[http://dx.doi.org/10.1038/s41598-020-77774-9] [PMID: 33277569]
[142]
Yamada Y, Enokida H, Kojima S, et al. MiR‐96 and miR‐183 detection in urine serve as potential tumor markers of urothelial carcinoma: correlation with stage and grade, and comparison with urinary cytology. Cancer Sci 2011; 102(3): 522-9.
[http://dx.doi.org/10.1111/j.1349-7006.2010.01816.x] [PMID: 21166959]
[143]
Trionfini P, Benigni A, Remuzzi G. MicroRNAs in kidney physiology and disease. Nat Rev Nephrol 2015; 11(1): 23-33.
[http://dx.doi.org/10.1038/nrneph.2014.202] [PMID: 25385286]
[144]
Li YF, Jing Y, Hao J, et al. MicroRNA-21 in the pathogenesis of acute kidney injury. Protein Cell 2013; 4(11): 813-9.
[http://dx.doi.org/10.1007/s13238-013-3085-y] [PMID: 24214874]
[145]
Fan PC, Chen CC, Chen YC, Chang YS, Chu PH. MicroRNAs in acute kidney injury. Hum Genomics 2016; 10(1): 29.
[http://dx.doi.org/10.1186/s40246-016-0085-z] [PMID: 27608623]
[146]
Du J, Cao X, Zou L, et al. MicroRNA-21 and risk of severe acute kidney injury and poor outcomes after adult cardiac surgery. PLoS One 2013; 8(5): e63390.
[http://dx.doi.org/10.1371/journal.pone.0063390] [PMID: 23717419]
[147]
Lan YF, Chen HH, Lai PF, et al. MicroRNA-494 reduces ATF3 expression and promotes AKI. J Am Soc Nephrol 2012; 23(12): 2012-23.
[http://dx.doi.org/10.1681/ASN.2012050438] [PMID: 23160513]
[148]
Gildea JJ, Carlson JM, Schoeffel CD, Carey RM, Felder RA. Urinary exosome miRNome analysis and its applications to salt sensitivity of blood pressure. Clin Biochem 2013; 46(12): 1131-4.
[http://dx.doi.org/10.1016/j.clinbiochem.2013.05.052] [PMID: 23726803]
[149]
Donadio JV, Grande JP. IgA Nephropathy. N Engl J Med 2002; 347(10): 738-48.
[http://dx.doi.org/10.1056/NEJMra020109] [PMID: 12213946]
[150]
Wang G, Kwan BCH, Lai FMM, Chow KM, Li PKT, Szeto CC. Elevated levels of miR-146a and miR-155 in kidney biopsy and urine from patients with IgA nephropathy. Dis Markers 2011; 30(4): 171-9.
[http://dx.doi.org/10.1155/2011/304852] [PMID: 21694443]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy