Jump to ContentJump to Main Navigation
Show Summary Details
More options …

microRNA Diagnostics and Therapeutics

Ed. by Sempere, Lorenzo

1 Issue per year


Emerging Science

Open Access
Online
ISSN
2084-6843
See all formats and pricing
More options …

In situ hybridization-based detection of microRNAs in human diseases

Xinna Zhang
  • Center for RNA Interference and Non-coding RNAs, The University of Texas MD Anderson Cancer Center, Houston, Texas / Department of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Xiongbin Lu
  • Department of Cancer Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Gabriel Lopez-Berestein
  • Center for RNA Interference and Non-coding RNAs, The University of Texas MD Anderson Cancer Center, Houston, Texas Department of Cancer Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas / Department of Experimental Therapeutics, The University of Texas MD Anderson Cancer Center, Houston, Texas
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Anil K. Sood
  • Center for RNA Interference and Non-coding RNAs, The University of Texas MD Anderson Cancer Center, Houston, Texas / Department of Cancer Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas / Department of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ George Calin
  • Center for RNA Interference and Non-coding RNAs, The University of Texas MD Anderson Cancer Center, Houston, Texas / Department of Experimental Therapeutics, The University of Texas MD Anderson Cancer Center, Houston, Texas
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2013-07-29 | DOI: https://doi.org/10.2478/micrnat-2013-0002

Abstract

MicroRNAs (miRNAs) are small non-coding RNAs that regulate various aspects of gene expression in physiology and development. Links between miRNAs and the initiation and progression of human diseases are becoming increasingly apparent. The development of methods to detect the subcellular and tissue localization of miRNAs is essential for understanding their biological role in homeostasis. In this review, we discuss how in situ hybridization can complement tissuelevel miRNA expression profiling and its role as an investigational tool to better understand the etiology of human diseases. Furthermore, in situ hybridization of miRNAs represents a potent diagnostic assay that could be further refined and utilized for clinical applications.

Keywords: microRNA; in situ hybridization; human diseases; profiling

References

  • [1] Bagga S, Bracht J, Hunter S, Massirer K, Holtz J, Eachus R, Pasquinelli AE. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell. 2005; 122: 553-63.CrossrefGoogle Scholar

  • [2] Wang Y, Liang Y, Lu Q . MicroRNA epigenetic alterations: predicting biomarkers and therapeutic targets in human diseases. Clin. Genet. 2008; 74: 307-15.CrossrefGoogle Scholar

  • [3] Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat. Struct. Mol. Biol. 2006; 13: 1097-101.CrossrefGoogle Scholar

  • [4] Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. The Microprocessor complex mediates the genesis of microRNAs. Nature. 2004; 432: 235-40.Google Scholar

  • [5] Hutvagner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science. 2002; 297: 2056-60.Google Scholar

  • [6] Mattick JS, Makunin IV. Non-coding RNA. Hum. Mol. Genet. 2006; 15 Spec No 1: R17-29.Google Scholar

  • [7] Costa FF. Non-coding RNAs: lost in translation? Gene. 2007; 386: 1-10.Google Scholar

  • [8] Ikeda S, Kong SW, Lu J, Bisping E, Zhang H, Allen PD, Golub TR, Pieske B, Pu WT. Altered microRNA expression in human heart disease. Physiol Genomics. 2007; 31: 367-73.CrossrefGoogle Scholar

  • [9] Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA. 2003; 9: 1274-81.PubMedCrossrefGoogle Scholar

  • [10] Makeyev EV, Zhang J, Carrasco MA, Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell. 2007; 27: 435-48.CrossrefGoogle Scholar

  • [11] Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME. A brain-specific microRNA regulates dendritic spine development. Nature. 2006; 439: 283-89.Google Scholar

  • [12] Koshkin AA, Wengel J. Synthesis of Novel 2’,3’-Linked Bicyclic Thymine Ribonucleosides. J. Org. Chem. 1998; 63: 2778-81.CrossrefGoogle Scholar

  • [13] Koshkin AA, Fensholdt J, Pfundheller HM, Lomholt C. A simplified and efficient route to 2’-O, 4’-C-methylene-linked bicyclic ribonucleosides (locked nucleic acid). J. Org. Chem. 2001; 66: 8504-12.CrossrefGoogle Scholar

  • [14] Vester B, Wengel J. LNA (locked nucleic acid): high-affinity targeting of complementary RNA and DNA. Biochemistry. 2004; 43: 13233-41.CrossrefGoogle Scholar

  • [15] Petersen M, Wengel J. LNA: a versatile tool for therapeutics and genomics. Trends Biotechnol. 2003; 21: 74-81.CrossrefGoogle Scholar

  • [16] Braasch DA, Corey DR. Locked nucleic acid (LNA): finetuning the recognition of DNA and RNA. Chem. Biol. 2001; 8: 1-7.CrossrefGoogle Scholar

  • [17] Kurreck J, Wyszko E, Gillen C, Erdmann VA. Design of antisense oligonucleotides stabilized by locked nucleic acids. Nucleic Acids Res. 2002; 30: 1911-8.CrossrefGoogle Scholar

  • [18] Bondensgaard K, Petersen M, Singh SK, Rajwanshi VK, Kumar R, Wengel J, Jacobsen JP. Structural studies of LNA:RNA duplexes by NMR: conformations and implications for RNase H activity. Chemistry. 2000; 6: 2687-95.CrossrefGoogle Scholar

  • [19] Petersen M, Bondensgaard K, Wengel J, Jacobsen JP. Locked nucleic acid (LNA) recognition of RNA: NMR solution structures of LNA:RNA hybrids. J. Am. Chem. Soc. 2002; 124; 5974-82.CrossrefGoogle Scholar

  • [20] Grunweller A, Hartmann RK. Locked nucleic acid oligonucleotides: the next generation of antisense agents? BioDrugs. 2007; 21: 235-43.CrossrefGoogle Scholar

  • [21] Nuovo GJ. In situ detection of precursor and mature microRNAs in paraffin embedded, formalin fixed tissues and cell preparations. Methods. 2008; 44: 39-46.CrossrefGoogle Scholar

  • [22] Jorgensen S, Baker A, Moller S, Nielsen BS. Robust one-day in situ hybridization protocol for detection of microRNAs in paraffin samples using LNA probes. Methods. 2010; 52: 375-81.CrossrefGoogle Scholar

  • [23] Sempere LF, Preis M, Yezefski T, Ouyang H, Suriawinata AA, Silahtaroglu A, Conejo-Garcia JR, Kauppinen S, Wells W, Korc M. Fluorescence-based codetection with protein markers reveals distinct cellular compartments for altered MicroRNA expression in solid tumors. Clin. Cancer Res. 2010; 16: 4246-55.CrossrefGoogle Scholar

  • [24] Obernosterer G, Martinez J, Alenius M. Locked nucleic acid-based in situ detection of microRNAs in mouse tissue sections. Nat. Protoc. 2007; 2: 1508-14.CrossrefGoogle Scholar

  • [25] Silahtaroglu AN, Nolting D, Dyrskjot L, Berezikov E, Moller M, Tommerup N, Kauppinen S. Detection of microRNAs in frozen tissue sections by fluorescence in situ hybridization using locked nucleic acid probes and tyramide signal amplification. Nat. Protoc.2007; 2: 2520-28.CrossrefGoogle Scholar

  • [26] Thompson RC, Deo M, Turner DL. Analysis of microRNA expression by in situ hybridization with RNA oligonucleotide probes. Methods. 2007; 43: 153-61.CrossrefGoogle Scholar

  • [27] Pena JT, Sohn-Lee C, Rouhanifard SH, Ludwig J, Hafner M, Mihailovic A, Lim C, Holoch D, Berninger P, Zavolan M, Tuschl T. miRNA in situ hybridization in formaldehyde and EDC-fixed tissues. Nat. Methods. 2009; 6: 139-41.CrossrefGoogle Scholar

  • [28] Kloosterman WP, Wienholds E, de BE, Kauppinen S, Plasterk RH. In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat. Methods. 2006; 3: 27-9.CrossrefGoogle Scholar

  • [29] Pearson BJ, Eisenhoffer GT, Gurley KA, Rink JC, Miller DE, Sanchez AA. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev. Dyn. 2009; 238: 443-50.CrossrefGoogle Scholar

  • [30] Lu J, Tsourkas A. Imaging individual microRNAs in single mammalian cells in situ. Nucleic Acids Res. 2009; 37: e100.CrossrefGoogle Scholar

  • [31] Nuovo G, Lee EJ, Lawler S, Godlewski J, Schmittgen T. In situ detection of mature microRNAs by labeled extension on ultramer templates. Biotechniques. 2009; 46: 115-26.CrossrefGoogle Scholar

  • [32] Christodoulou F, Raible F, Tomer R, Simakov O, Trachana K, Klaus S, Snyman H, Hannon GJ, Bork P, Arendt D. Ancient animal microRNAs and the evolution of tissue identity. Nature. 2010; 463: 1084-8.CrossrefGoogle Scholar

  • [33] Schad A, Fahimi HD, Volkl A, Baumgart E. Expression of catalase mRNA and protein in adult rat brain: detection by nonradioactive in situ hybridization with signal amplification by catalyzed reporter deposition (ISH-CARD) and immunohistochemistry (IHC)/immunofluorescence (IF). J. Histochem. Cytochem. 2003; 51: 751-60. CrossrefGoogle Scholar

  • [34] Preis M, Gardner TB, Gordon SR, Pipas JM, Mackenzie TA, Klein EE, Longnecker DS, Gutmann EJ, Sempere LF, Korc M. MicroRNA-10b expression correlates with response to neoadjuvant therapy and survival in pancreatic ductal adenocarcinoma. Clin. Cancer Res. 2011; 17: 5812-21.CrossrefGoogle Scholar

  • [35] Nuovo GJ, Elton TS, Nana-Sinkam P, Volinia S, Croce CM, Schmittgen TD. A methodology for the combined in situ analyses of the precursor and mature forms of microRNAs and correlation with their putative targets. Nat. Protoc. 2009; 4: 107-15.CrossrefGoogle Scholar

  • [36] Nicoloso MS, Calin GA. MicroRNA involvement in brain tumors: from bench to bedside. Brain Pathol. 2008; 18: 122-9.CrossrefGoogle Scholar

  • [37] Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, Yuen ST, Chan TL, Kwong DL, Au GK, Liu CG, Calin GA, Croce CM, Harris CC. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA. 2008; 299: 425-36.Google Scholar

  • [38] Streit S, Michalski CW, Erkan M, Kleeff J, Friess H. Northern blot analysis for detection and quantification of RNA in pancreatic cancer cells and tissues. Nat. Protoc. 2009; 4: 37-43.Google Scholar

  • [39] Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004; 5: R13.CrossrefGoogle Scholar

  • [40] Liu CG, Spizzo R, Calin GA, Croce CM. Expression profiling of microRNA using oligo DNA arrays. Methods; 44: 22-30.Google Scholar

  • [41] Schmittgen TD, Jiang J, Liu Q, Yang L. A high-throughput method to monitor the expression of microRNA precursors. Nucleic Acids Res. 2004; 32: e43.CrossrefGoogle Scholar

  • [42] Nolan T, Hands RE, Bustin SA. Quantification of mRNA using real-time RT-PCR. Nat. Protoc. 2006; 1: 1559-82.CrossrefGoogle Scholar

  • [43] Chen J, Lozach J, Garcia EW, Barnes B, Luo S, Mikoulitch I, Zhou L, Schroth G, Fan JB. Highly sensitive and specific microRNA expression profiling using BeadArray technology. Nucleic Acids Res. 2008; 36: e87.CrossrefGoogle Scholar

  • [44] Shendure J, Ji H. Next-generation DNA sequencing. Nat. Biotechnol. 2008; 26: 1135-45.CrossrefGoogle Scholar

  • [45] Mardis ER. The impact of next-generation sequencing technology on genetics. Trends Genet. 2008; 24: 133-41.CrossrefGoogle Scholar

  • [46] Rung J, Brazma A. Reuse of public genome-wide gene expression data. Nat. Rev. Genet. 2013; 14: 89-99.Google Scholar

  • [47] ‘t Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, de Menezes RX, Boer JM, van Ommen GJ, den Dunnen JT. Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res. 2008; 36, e141.CrossrefGoogle Scholar

  • [48] Creighton CJ, Reid JG, Gunaratne PH. Expression profiling of microRNAs by deep sequencing. Brief. Bioinform. 2009; 10: 490-7.CrossrefGoogle Scholar

  • [49] Branton D, Deamer DW, Marziali A, Bayley H, Benner SA, Butler T, Di VM, Garaj S, Hibbs A, Huang X, Jovanovich SB, Krstic PS, Lindsay S, Ling XS, Mastrangelo CH, Meller A, Oliver JS, Pershin YV, Ramsey JM, Riehn R, Soni GV, Tabard- Cossa V, Wanunu M, Wiggin M, Schloss JA. The potential and challenges of nanopore sequencing. Nat. Biotechnol. 2008; 26: 1146-53.CrossrefGoogle Scholar

  • [50] Wolber PK, Collins PJ, Lucas AB, De WA, Shannon KW. The Agilent in situ-synthesized microarray platform. Methods Enzymol. 2006; 410: 28-57.CrossrefGoogle Scholar

  • [51] Hughes TR, Hiley SL, Saltzman AL, Babak T, Blencowe BJ. Microarray analysis of RNA processing and modification. Methods Enzymol. 2006; 410: 300-16.CrossrefGoogle Scholar

  • [52] Kong W, Zhao JJ, He L, Cheng JQ . Strategies for profiling microRNA expression. J. Cell Physiol. 2009; 218: 22-5.CrossrefGoogle Scholar

  • [53] Murphy J, Bustin SA. Reliability of real-time reversetranscription PCR in clinical diagnostics: gold standard or substandard? Expert. Rev. Mol. Diagn. 2009; 9: 187-97.CrossrefGoogle Scholar

  • [54] Lee YS, Dutta A. MicroRNAs in cancer. Annu. Rev. Pathol. 2009; 4: 199-227.CrossrefGoogle Scholar

  • [55] Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, Croce CM. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. U. S. A. 2004; 101: 2999-3004.CrossrefGoogle Scholar

  • [56] Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat. Rev. Cancer. 2006; 6: 857-66.CrossrefGoogle Scholar

  • [57] Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Menard S, Palazzo JP, Rosenberg A, Musiani P, Volinia S, Nenci I, Calin GA, Querzoli P, Negrini M, Croce CM. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005; 65: 7065-70.CrossrefGoogle Scholar

  • [58] Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. U. S. A. 2006; 103: 2257-61.CrossrefGoogle Scholar

  • [59] Yamamichi N, Shimomura R, Inada K, Sakurai K, Haraguchi T, Ozaki Y, Fujita S, Mizutani T, Furukawa C, Fujishiro M, Ichinose M, Shiogama K, Tsutsumi Y, Omata M, Iba H. Locked nucleic acid in situ hybridization analysis of miR-21 expression during colorectal cancer development. Clin. Cancer Res. 2009; 15: 4009-16.CrossrefGoogle Scholar

  • [60] Dillhoff M, Liu J, Frankel W, Croce C, Bloomston M. MicroRNA-21 is overexpressed in pancreatic cancer and a potential predictor of survival. J. Gastrointest. Surg. 2008; 12: 2171-76.CrossrefGoogle Scholar

  • [61] Hermansen SK, Dahlrot RH, Nielsen BS, Hansen S, Kristensen BW. MiR-21 expression in the tumor cell compartment holds unfavorable prognostic value in gliomas. J. Neurooncol. 2013; 111: 71-81.CrossrefGoogle Scholar

  • [62] Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T, Calin GA, Liu CG, Croce CM, Harris CC. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 2006; 9: 189-98. CrossrefGoogle Scholar

  • [63] Donnem T, Eklo K, Berg T, Sorbye SW, Lonvik K, Al-Saad S, Al-Shibli K, Andersen S, Stenvold H, Bremnes RM, Busund LT. Prognostic impact of MiR-155 in non-small cell lung cancer evaluated by in situ hybridization. J. Transl. Med. 2011; 9: 6.CrossrefGoogle Scholar

  • [64] Ryu JK, Hong SM, Karikari CA, Hruban RH, Goggins MG, Maitra A. Aberrant MicroRNA-155 expression is an early event in the multistep progression of pancreatic adenocarcinoma. Pancreatolog. 2010; 10: 66-73.CrossrefGoogle Scholar

  • [65] Quesne JL, Jones J, Warren J, Dawson SJ, Ali HR, Bardwell H, Blows F, Pharoah P, Caldas C. Biological and prognostic associations of miR-205 and let-7b in breast cancer revealed by in situ hybridization analysis of micro-RNA expression in arrays of archival tumour tissue. J. Pathol. 2012; 227: 306-14.CrossrefGoogle Scholar

  • [66] Hanna JA, Hahn L, Agarwal S, Rimm DL. In situ measurement of miR-205 in malignant melanoma tissue supports its role as a tumor suppressor microRNA. Lab Invest. 2012; 92: 1390-97.CrossrefGoogle Scholar

  • [67] Hansen TF, Sorensen FB, Lindebjerg J, Jakobsen A. The predictive value of microRNA-126 in relation to first line treatment with capecitabine and oxaliplatin in patients with metastatic colorectal cancer. BMC. Cancer. 2012; 12: 83.CrossrefGoogle Scholar

  • [68] Catalucci D, Gallo P, Condorelli G. MicroRNAs in cardiovascular biology and heart disease. Circ. Cardiovasc. Genet. 2009; 2: 402-8.CrossrefGoogle Scholar

  • [69] Chen JF, Murchison EP, Tang R, Callis TE, Tatsuguchi M, Deng Z, Rojas M, Hammond SM, Schneider MD, Selzman CH, Meissner G, Patterson C, Hannon GJ, Wang DZ. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 2111-6.CrossrefGoogle Scholar

  • [70] Malizia AP, Wang DZ. MicroRNAs in cardiomyocyte development. Wiley. Interdiscip. Rev. Syst. Biol. Med. 2011; 3: 183-90.CrossrefGoogle Scholar

  • [71] Kuwabara Y, Ono K, Horie T, Nishi H, Nagao K, Kinoshita M, Watanabe S, Baba O, Kojima Y, Shizuta S, Imai M, Tamura T, Kita T, Kimura T. Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate myocardial damage. Circ. Cardiovasc. Genet. 2011; 4: 446-54.Google Scholar

  • [72] Torella D, Iaconetti C, Catalucci D, Ellison GM, Leone A, Waring CD, Bochicchio A, Vicinanza C, Aquila I, Curcio A, Condorelli G, Indolfi C. MicroRNA-133 controls vascular smooth muscle cell phenotypic switch in vitro and vascular remodeling in vivo. Circ. Res. 2011; 109: 880-93.CrossrefGoogle Scholar

  • [73] Wang YS, Wang HY, Liao YC, Tsai PC, Chen KC, Cheng HY, Lin RT, Juo SH. MicroRNA-195 regulates vascular smooth muscle cell phenotype and prevents neointimal formation. Cardiovasc. Res. 2012; 95: 517-26.CrossrefGoogle Scholar

  • [74] Gambardella S, Rinaldi F, Lepore SM, Viola A, Loro E, Angelini C, Vergani L, Novelli G, Botta A. Overexpression of microRNA-206 in the skeletal muscle from myotonic dystrophy type 1 patients. J. Transl. Med. 2010; 8: 48. Google Scholar

  • [75] Larsson E, Fredlund FP, Heldin J, Barkefors I, Bondjers C, Genove G, Arrondel C, Gerwins P, Kurschat C, Schermer B, Benzing T, Harvey SJ, Kreuger J, Lindahl P. Discovery of microvascular miRNAs using public gene expression data: miR-145 is expressed in pericytes and is a regulator of Fli1. Genome Med. 2009; 1: 108.Google Scholar

  • [76] Schneider M, Andersen DC, Silahtaroglu A, Lyngbaek S, Kauppinen S, Hansen JL, Sheikh SP. Cell-specific detection of microRNA expression during cardiomyogenesis by combined in situ hybridization and immunohistochemistry. J. Mol. Histol. 2011; 42: 289-99.CrossrefGoogle Scholar

  • [77] Junn E, Mouradian MM. MicroRNAs in neurodegenerative diseases and their therapeutic potential. Pharmacol. Ther. 2012; 133: 142-50.Google Scholar

  • [78] Nelson PT, Wang WX, Rajeev BW. MicroRNAs (miRNAs) in neurodegenerative diseases. Brain Pathol. 2008; 18: 130-8.CrossrefGoogle Scholar

  • [79] Wang WX, Rajeev BW, Stromberg AJ, Ren N, Tang G, Huang Q, Rigoutsos I, Nelson PT. The expression of microRNA miR-107 decreases early in Alzheimer’s disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. J. Neurosci. 2008; 28: 1213-23.Google Scholar

  • [80] Kapsimali M, Kloosterman WP, de BE, Rosa F, Plasterk RH, Wilson SW. MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system.Genome Bio. 2007; 8: R173.CrossrefGoogle Scholar

  • [81] Hebert SS, Sergeant N, Buee L. MicroRNAs and the Regulation of Tau Metabolism. Int. J. Alzheimers. Dis. 2012; 2012: 406561.Google Scholar

  • [82] Hebert SS, Papadopoulou AS, Smith P, Galas MC, Planel E, Silahtaroglu AN, Sergeant N, Buee L, De SB. Genetic ablation of Dicer in adult forebrain neurons results in abnormal tau hyperphosphorylation and neurodegeneration. Hum. Mol. Genet. 2010; 19: 3959-69.CrossrefGoogle Scholar

  • [83] Cogswell JP, Ward J, Taylor IA, Waters M, Shi Y, Cannon B, Kelnar K, Kemppainen J, Brown D, Chen C, Prinjha RK, Richardson JC, Saunders AM, Roses AD, Richards CA. Identification of miRNA changes in Alzheimer’s disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers. Dis. 2008; 14: 27-41. Google Scholar

  • [84] Lukiw WJ. Micro-RNA speciation in fetal, adult and Alzheimer’s disease hippocampus. Neuroreport. 2007; 18: 297-300.CrossrefGoogle Scholar

  • [85] Delay C, Mandemakers W, Hebert SS. MicroRNAs in Alzheimer’s disease. Neurobiol. Dis. 2012; 46: 285-90.CrossrefGoogle Scholar

  • [86] Hebert SS, Horre K, Nicolai L, Papadopoulou AS, Mandemakers W, Silahtaroglu AN, Kauppinen S, Delacourte A, De SB. Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer’s disease correlates with increased BACE1/beta-secretase expression.Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 6415-20.Google Scholar

  • [87] Liu W, Liu C, Zhu J, Shu P, Yin B, Gong Y, Qiang B, Yuan J, Peng X. MicroRNA-16 targets amyloid precursor protein to potentially modulate Alzheimer’s-associated pathogenesis in SAMP8 mice. Neurobiol. Aging. 2012; 33: 522-34.Google Scholar

  • [88] Nelson PT, Dimayuga J, Wilfred BR. MicroRNA in Situ Hybridization in the Human Entorhinal and Transentorhinal Cortex. Front Hum. Neurosci. 2012; 4: 7.Google Scholar

  • [89] Minones-Moyano E, Porta S, Escaramis G, Rabionet R, Iraola S, Kagerbauer B, Espinosa-Parrilla Y, Ferrer I, Estivill X, Marti E. MicroRNA profiling of Parkinson’s disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum. Mol. Genet. 2011; 20: 3067-78.CrossrefGoogle Scholar

  • [90] Packer AN, Xing Y, Harper SQ, Jones L, Davidson BL. The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington’s disease. J.Neurosci. 2008; 28: 14341-6.Google Scholar

  • [91] Tan SL, Ohtsuka T, Gonzalez A, Kageyama R. MicroRNA9 regulates neural stem cell differentiation by controlling Hes1 expression dynamics in the developing brain. Genes Cells. 2012; 17: 952-61.Google Scholar

  • [92] Nelson PT, Wilfred BR. In situ hybridization is a necessary experimental complement to microRNA (miRNA) expression profiling in the human brain. Neurosci. Lett. 2009; 466: 69-72.CrossrefGoogle Scholar

  • [93] Karginov FV, Conaco C, Xuan Z, Schmidt BH, Parker JS, Mandel G, Hannon GJ. A biochemical approach to identifying microRNA targets. Proc. Natl. Acad. Sci. U. S. A. 2007; 104: 19291-6.CrossrefGoogle Scholar

  • [94] Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 2009; 10: 155-9.CrossrefGoogle Scholar

  • [95] Esteller M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011; 12: 861-74. CrossrefGoogle Scholar

About the article

Received: 2013-03-05

Accepted: 2013-05-31

Published Online: 2013-07-29

Published in Print: 2014-01-01


Citation Information: microRNA Diagnostics and Therapeutics, ISSN (Online) 2084-6843, DOI: https://doi.org/10.2478/micrnat-2013-0002.

Export Citation

© 2013 Xinna Zhang et al.. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Comments (0)

Please log in or register to comment.
Log in