The biomarker and therapeutic potential of miRNA in Alzheimer's disease

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Hyman BT, Phelps CH, Beach TG et al. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease. Alzheimers Dement. 8(1), 1–13 (2012).
  MedlineGoogle Scholar
• 2 Perrin RJ, Fagan AM, Holtzman DM. Multimodal techniques for diagnosis and prognosis of Alzheimer's disease. Nature 461(7266), 916–922 (2009).
  Medline CASGoogle Scholar
• 3 Jack CR Jr. Alzheimer disease: new concepts on its neurobiology and the clinical role imaging will play. Radiology 263(2), 344–361 (2012).
  MedlineGoogle Scholar
• 4 Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 136(2), 215–233 (2009).
  Medline CASGoogle Scholar
• 5 Chalfie M, Horvitz HR, Sulston JE. Mutations that lead to reiterations in the cell lineages of C. elegans. Cell 24(1), 59–69 (1981).
  Medline CASGoogle Scholar
• 6 Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5), 843–854 (1993).
  Medline CASGoogle Scholar
• 7 Olsen PH, Ambros V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216(2), 671–680 (1999).
  Medline CASGoogle Scholar
• 8 Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75(5), 855–862 (1993).
  Medline CASGoogle Scholar
• 9 Ambros V, Bartel B, Bartel DP et al. A uniform system for microRNA annotation. RNA 9(3), 277–279 (2003).
  Medline CASGoogle Scholar
• 10 Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42(Database issue), D68–D73 (2014).
  Medline CASGoogle Scholar
• 11 Lee Y, Kim M, Han J et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23(20), 4051–4060 (2004).
  Medline CASGoogle Scholar
• 12 Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat. Struct. Mol. Biol. 13(12), 1097–1101 (2006).• Summary of miRNA processing.
  Medline CASGoogle Scholar
• 13 Lee EJ, Baek M, Gusev Y et al. Systematic evaluation of microRNA processing patterns in tissues, cell lines, and tumors. RNA 14(1), 35–42 (2008).
  Medline CASGoogle Scholar
• 14 Gregory RI, Yan KP, Amuthan G et al. The Microprocessor complex mediates the genesis of microRNAs. Nature 432(7014), 235–240 (2004).
  Medline CASGoogle Scholar
• 15 Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17(24), 3011–3016 (2003).
  Medline CASGoogle Scholar
• 16 Okada C, Yamashita E, Lee SJ et al. A high-resolution structure of the pre-microRNA nuclear export machinery. Science 326(5957), 1275–1279 (2009).
  Medline CASGoogle Scholar
• 17 Bohnsack MT, Czaplinski K, Gorlich D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10(2), 185–191 (2004).
  Medline CASGoogle Scholar
• 18 Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123(4), 631–640 (2005).
  Medline CASGoogle Scholar
• 19 Diederichs S, Haber DA. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 131(6), 1097–1108 (2007).•• TAR (HIV-1) RNA-binding protein 2 is involved in miRNA processing.
  Medline CASGoogle Scholar
• 20 Chendrimada TP, Gregory RI, Kumaraswamy E et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436(7051), 740–744 (2005).
  Medline CASGoogle Scholar
• 21 Meister G, Landthaler M, Patkaniowska A et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15(2), 185–197 (2004).
  Medline CASGoogle Scholar
• 22 Yao B, La LB, Chen YC, Chang LJ, Chan EK. Defining a new role of GW182 in maintaining miRNA stability. EMBO Rep. 13(12), 1102–1108 (2012).
  Medline CASGoogle Scholar
• 23 Braun JE, Huntzinger E, Izaurralde E. The role of GW182 proteins in miRNA-mediated gene silencing. Adv. Exp. Med. Biol. 768, 147–163 (2013).
  Medline CASGoogle Scholar
• 24 Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19(1), 92–105 (2009).
  Medline CASGoogle Scholar
• 25 Shin C, Nam JW, Farh KK et al. Expanding the microRNA targeting code: functional sites with centered pairing. Mol. Cell 38(6), 789–802 (2010).
  Medline CASGoogle Scholar
• 26 Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120(1), 15–20 (2005).
  Medline CASGoogle Scholar
• 27 Lytle JR, Yario TA, Steitz JA. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5’ UTR as in the 3’ UTR. Proc. Natl Acad. Sci. USA 104(23), 9667–9672 (2007).
  Medline CASGoogle Scholar
• 28 Lee I, Ajay SS, Yook JI et al. New class of microRNA targets containing simultaneous 5’-UTR and 3’-UTR interaction sites. Genome Res. 19(7), 1175–1183 (2009).
  Medline CASGoogle Scholar
• 29 Zhou X, Duan X, Qian J, Li F. Abundant conserved microRNA target sites in the 5’-untranslated region and coding sequence. Genetica 137(2), 159–164 (2009).
  Medline CASGoogle Scholar
• 30 Hausser J, Syed AP, Bilen B, Zavolan M. Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation. Genome Res. 23(4), 604–615 (2013).
  Medline CASGoogle Scholar
• 31 Eulalio A, Rehwinkel J, Stricker M et al. Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev. 21(20), 2558–2570 (2007).• Summary of miRNA mechanisms.
  Medline CASGoogle Scholar
• 32 Zhao S, Liu MF. Mechanisms of microRNA-mediated gene regulation. Sci. China C. Life Sci. 52(12), 1111–1116 (2009).• Reports miRNA as not only an inhibitor of translation but also as an enhancer of translation.
  Medline CASGoogle Scholar
• 33 Srikantan S, Marasa BS, Becker KG, Gorospe M, Abdelmohsen K. Paradoxical microRNAs: individual gene repressors, global translation enhancers. Cell Cycle 10(5), 751–759 (2011).
  Medline CASGoogle Scholar
• 34 Garza-Manero S, Pichardo-Casas I, Arias C, Vaca L, Zepeda A. Selective distribution and dynamic modulation of miRNAs in the synapse and its possible role in Alzheimer's disease. Brain Res. (1584), 80–93 (2013).
  MedlineGoogle Scholar
• 35 Poon VY, Goh C, Voorhoeve PM, Fivaz M. High-content imaging of presynaptic assembly. Front. Cell. Neurosci. 8, 66 (2014).
  MedlineGoogle Scholar
• 36 Goldie BJ, Dun MD, Lin M et al. Activity-associated miRNA are packaged in Map1b-enriched exosomes released from depolarized neurons. Nucleic Acids Res. 42(14), 9195–9208 (2014).•• Summarizes variability in levels of miRNA in different biofluids.
  Medline CASGoogle Scholar
• 37 Weber JA, Baxter DH, Zhang S et al. The microRNA spectrum in 12 body fluids. Clin. Chem. 56(11), 1733–1741 (2010).•• Reports the transfer of vesicle transfer of oligonucleotides.
  Medline CASGoogle Scholar
• 38 Ridder K, Keller S, Dams M et al. Extracellular vesicle-mediated transfer of genetic information between the hematopoietic system and the brain in response to inflammation. PLoS Biol. 12(6), e1001874 (2014).
  MedlineGoogle Scholar
• 39 Xi Y, Nakajima G, Gavin E et al. Systematic analysis of microRNA expression of RNA extracted from fresh frozen and formalin-fixed paraffin-embedded samples. RNA 13(10), 1668–1674 (2007).
  Medline CASGoogle Scholar
• 40 Patel RS, Jakymiw A, Yao B et al. High resolution of microRNA signatures in human whole saliva. Arch. Oral Biol. 56(12), 1506–1513 (2011).
  Medline CASGoogle Scholar
• 41 Li Y, Jiang Z, Xu L et al. Stability analysis of liver cancer-related microRNAs. Acta Biochim. Biophys. Sin. (Shanghai) 43(1), 69–78 (2011).
  Medline CASGoogle Scholar
• 42 Liu A, Xu X. MicroRNA isolation from formalin-fixed, paraffin-embedded tissues. Methods Mol. Biol. 724, 259–267 (2011).
  Medline CASGoogle Scholar
• 43 Benson EA, Skaar TC. Incubation of whole blood at room temperature does not alter the plasma concentrations of microRNA-16 and -223. Drug Metab. Dispos. 41(10), 1778–1781 (2013).
  MedlineGoogle Scholar
• 44 Mall C, Rocke DM, Durbin-Johnson B, Weiss RH. Stability of miRNA in human urine supports its biomarker potential. Biomark. Med. 7(4), 623–631 (2013).
  CASGoogle Scholar
• 45 Zhu X, Lv M, Wang H, Guan W. Identification of circulating microRNAs as novel potential biomarkers for gastric cancer detection: a systematic review and meta-analysis. Dig. Dis. Sci. 59(5), 911–919 (2014).
  Medline CASGoogle Scholar
• 46 Yang X, Guo Y, Du Y et al. Serum microRNA-21 as a diagnostic marker for lung carcinoma: a systematic review and meta-analysis. PLoS ONE 9(5), e97460 (2014).
  MedlineGoogle Scholar
• 47 Li HG, Zhao LH, Bao XB, Sun PC, Zhai BP. Meta-analysis of the differentially expressed colorectal cancer-related microRNA expression profiles. Eur. Rev. Med. Pharmacol. Sci. 18(14), 2048–2057 (2014).
  MedlineGoogle Scholar
• 48 Fu W, Pang L, Chen Y et al. The microRNAs as prognostic biomarkers for survival in esophageal cancer: a meta-analysis. Scientific World J. (2014), 523979 (2014).
  MedlineGoogle Scholar
• 49 Liu L, Wang S, Cao X, Liu J. Analysis of circulating microRNA biomarkers for breast cancer detection: a meta-analysis. Tumour Biol. 35(12), 12245–12253 (2014).• Meta-analysis of CNS cancer miRNA.
  Medline CASGoogle Scholar
• 50 Wei D, Wan Q, Li L et al. MicroRNAs as potential biomarkers for diagnosing cancers of central nervous system: a meta-analysis. Mol. Neurobiol. (2014) (Epub ahead of print).
  Google Scholar
• 51 Calin GA, Dumitru CD, Shimizu M et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl Acad. Sci. USA 99(24), 15524–15529 (2002).
  Medline CASGoogle Scholar
• 52 Calin GA, Ferracin M, Cimmino A et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353(17), 1793–1801 (2005).
  Medline CASGoogle Scholar
• 53 Baraniskin A, Kuhnhenn J, Schlegel U et al. MicroRNAs in cerebrospinal fluid as biomarker for disease course monitoring in primary central nervous system lymphoma. J. Neurooncol. 109(2), 239–244 (2012).•• Reports CSF miRNA as biomarkers of glioma.
  Medline CASGoogle Scholar
• 54 Baraniskin A, Kuhnhenn J, Schlegel U et al. Identification of microRNAs in the cerebrospinal fluid as biomarker for the diagnosis of glioma. Neuro. Oncol. 14(1), 29–33 (2012).
  Medline CASGoogle Scholar
• 55 Ren J, Zhang J, Xu N et al. Signature of circulating microRNAs as potential biomarkers in vulnerable coronary artery disease. PLoS ONE 8(12), e80738 (2013).
  MedlineGoogle Scholar
• 56 D'Alessandra Y, Carena MC, Spazzafumo L et al. Diagnostic potential of plasmatic microRNA signatures in stable and unstable angina. PLoS ONE 8(11), e80345 (2013).
  MedlineGoogle Scholar
• 57 Li K, Zhang T, Fan H et al. The analysis of microRNA expression profiling for coronary artery disease. Cardiology 127(1), 62–69 (2014).
  Medline CASGoogle Scholar
• 58 Fukushima Y, Nakanishi M, Nonogi H, Goto Y, Iwai N. Assessment of plasma miRNAs in congestive heart failure. Circ. J. 75(2), 336–340 (2011).
  Medline CASGoogle Scholar
• 59 Greco S, Fasanaro P, Castelvecchio S et al. MicroRNA dysregulation in diabetic ischemic heart failure patients. Diabetes 61(6), 1633–1641 (2012).
  Medline CASGoogle Scholar
• 60 Vogel B, Keller A, Frese KS et al. Multivariate miRNA signatures as biomarkers for non-ischaemic systolic heart failure. Eur. Heart J. 34(36), 2812–2822 (2013).
  Medline CASGoogle Scholar
• 61 Tan JR, Tan KS, Koo YX et al. Blood microRNAs in low or no risk ischemic stroke patients. Int. J. Mol. Sci. 14(1), 2072–2084 (2013).
  Medline CASGoogle Scholar
• 62 Ward JA, Esa N, Pidikiti R et al. Circulating cell and plasma microRNA profiles differ between non-ST-segment and ST-segment-elevation myocardial infarction. Fam. Med. Med. Sci. Res. 2(2), 108 (2013).
  MedlineGoogle Scholar
• 63 Bronze-da-Rocha E. MicroRNAs expression profiles in cardiovascular diseases. Biomed. Res. Int. 985408 (2014).
  MedlineGoogle Scholar
• 64 de Pontual L, Yao E, Callier P et al. Germline deletion of the miR-17 approximately 92 cluster causes skeletal and growth defects in humans. Nat. Genet. 43(10), 1026–1030 (2011).
  Medline CASGoogle Scholar
• 65 Mencia A, Modamio-Hoybjor S, Redshaw N et al. Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat. Genet. 41(5), 609–613 (2009).
  Medline CASGoogle Scholar
• 66 Solda G, Robusto M, Primignani P et al. A novel mutation within the MIR96 gene causes non-syndromic inherited hearing loss in an Italian family by altering pre-miRNA processing. Hum. Mol. Genet. 21(3), 577–585 (2012).
  Medline CASGoogle Scholar
• 67 Hughes AE, Bradley DT, Campbell M et al. Mutation altering the miR-184 seed region causes familial keratoconus with cataract. Am. J. Hum. Genet. 89(5), 628–633 (2011).
  Medline CASGoogle Scholar
• 68 Bykhovskaya Y, Caiado Canedo AL, Wright KW, Rabinowitz YS. C.57 C > T mutation in MIR 184 is responsible for congenital cataracts and corneal abnormalities in a five-generation family from Galicia, Spain. Ophthalmic Genet. (2013).
  MedlineGoogle Scholar
• 69 Lechner J, Bae HA, Guduric-Fuchs J et al. Mutational analysis of MIR184 in sporadic keratoconus and myopia. Invest. Ophthalmol. Vis. Sci. 54(8), 5266–5272 (2013).
  Medline CASGoogle Scholar
• 70 Martins M, Rosa A, Guedes LC et al. Convergence of miRNA expression profiling, alpha-synuclein interacton and GWAS in Parkinson's disease. PLoS ONE 6(10), e25443 (2011).
  Medline CASGoogle Scholar
• 71 Margis R, Margis R, Rieder CR. Identification of blood microRNAs associated to Parkinsonis disease. J. Biotechnol. 152(3), 96–101 (2011).
  Medline CASGoogle Scholar
• 72 Cardo LF, Coto E, de Mena L et al. Profile of microRNAs in the plasma of Parkinson's disease patients and healthy controls. J. Neurol. 260(5), 1420–1422 (2013).
  MedlineGoogle Scholar
• 73 Khoo SK, Petillo D, Kang UJ et al. Plasma-based circulating MicroRNA biomarkers for Parkinson's disease. J. Parkinsons Dis. 2(4), 321–331 (2012).
  Medline CASGoogle Scholar
• 74 Soreq L, Salomonis N, Bronstein M et al. Small RNA sequencing-microarray analyses in Parkinson leukocytes reveal deep brain stimulation-induced splicing changes that classify brain region transcriptomes. Front. Mol. Neurosci. 6, 10 (2013).
  Medline CASGoogle Scholar
• 75 Hebert SS, Wang WX, Zhu Q, Nelson PT. A study of small RNAs from cerebral neocortex of pathology-verified Alzheimer's disease, dementia with lewy bodies, hippocampal sclerosis, frontotemporal lobar dementia, and non-demented human controls. J. Alzheimers Dis. 35(2), 335–348 (2013).
  Medline CASGoogle Scholar
• 76 De Felice B, Guida M, Guida M et al. A miRNA signature in leukocytes from sporadic amyotrophic lateral sclerosis. Gene 508(1), 35–40 (2012).
  Medline CASGoogle Scholar
• 77 Russell AP, Wada S, Vergani L et al. Disruption of skeletal muscle mitochondrial network genes and miRNAs in amyotrophic lateral sclerosis. Neurobiol. Dis. 49C, 107–117 (2012).
  Google Scholar
• 78 Campos-Melo D, Droppelmann CA, He Z, Volkening K, Strong MJ. Altered microRNA expression profile in amyotrophic lateral sclerosis: a role in the regulation of NFL mRNA levels. Mol. Brain 6, 26 (2013).
  Medline CASGoogle Scholar
• 79 Van Deerlin VM, Leverenz JB, Bekris LM et al. TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol. 7(5), 409–416 (2008).
  Medline CASGoogle Scholar
• 80 Kawahara Y, Mieda-Sato A. TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc. Natl Acad. Sci. USA 109(9), 3347–3352 (2012).
  Medline CASGoogle Scholar
• 81 Schipper HM, Maes OC, Chertkow HM, Wang E. MicroRNA expression in Alzheimer blood mononuclear cells. Gene Regul. Syst. Bio. 1, 263–274 (2007).
  MedlineGoogle Scholar
• 82 Lukiw WJ. Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus. Neuroreport 18(3), 297–300 (2007).
  Medline CASGoogle Scholar
• 83 Cogswell JP, Ward J, Taylor IA et al. Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers Dis. 14(1), 27–41 (2008).
  Medline CASGoogle Scholar
• 84 Shioya M, Obayashi S, Tabunoki H et al. Aberrant microRNA expression in the brains of neurodegenerative diseases: miR-29a decreased in Alzheimer disease brains targets neurone navigator 3. Neuropathol. Appl. Neurobiol. 36(4), 320–330 (2010).
  Medline CASGoogle Scholar
• 85 Wang WX, Huang Q, Hu Y, Stromberg AJ, Nelson PT. Patterns of microRNA expression in normal and early Alzheimer's disease human temporal cortex: white matter versus gray matter. Acta Neuropathol. 121(2), 193–205 (2011).
  MedlineGoogle Scholar
• 86 Alexandrov PN, Dua P, Hill JM et al. microRNA (miRNA) speciation in Alzheimer's disease (AD) cerebrospinal fluid (CSF) and extracellular fluid (ECF). Int. J. Biochem. Mol. Biol. 3(4), 365–373 (2012).
  Medline CASGoogle Scholar
• 87 Sala Frigerio C, Lau P, Salta E et al. Reduced expression of hsa-miR-27a-3p in CSF of patients with Alzheimer disease. Neurology 81(24), 2103–2106 (2013).
  Medline CASGoogle Scholar
• 88 Kumar P, Dezso Z, MacKenzie C et al. Circulating miRNA biomarkers for Alzheimer's disease. PLoS ONE 8(7), e69807 (2013).
  Medline CASGoogle Scholar
• 89 Bekris LM, Lutz F, Montine TJ et al. microRNA in Alzheimer's disease: an exploratory study in brain, cerebrospinal fluid and plasma. Biomarkers 18(5), 455–466 (2013).
  Medline CASGoogle Scholar
• 90 Tan L, Yu JT, Liu QY et al. Circulating miR-125b as a biomarker of Alzheimer's disease. J. Neurol. Sci. 336(1–2), 52–56 (2014).
  Medline CASGoogle Scholar
• 91 Bekris LM, Yu CE, Bird TD, Tsuang DW. Genetics of Alzheimer disease. J. Geriatr. Psychiatry Neurol. 23(4), 213–227 (2010).
  MedlineGoogle Scholar
• 92 Modarresi F, Faghihi MA, Patel NS et al. Knockdown of BACE1-AS nonprotein-coding transcript modulates beta-amyloid-related hippocampal neurogenesis. Int. J. Alzheimers Dis. 2011, 929042 (2011).
  MedlineGoogle Scholar
• 93 Long JM, Ray B, Lahiri DK. microRNA-339–5p down-regulates protein expression of beta-site amyloid precursor protein-cleaving enzyme 1 (BACE1) in human primary brain cultures and is reduced in brain tissue specimens of Alzheimer disease subjects. J. Biol. Chem. 289(8), 5184–5198 (2014).
  Medline CASGoogle Scholar
• 94 Zappia M, Cittadella R, Manna I et al. Genetic association of alpha2-macroglobulin polymorphisms with AD in southern Italy. Neurology 59(5), 756–758 (2002).
  Medline CASGoogle Scholar
• 95 Kanekiyo T, Cirrito JR, Liu CC et al. Neuronal clearance of amyloid-beta by endocytic receptor LRP1. J. Neurosci. 33(49), 19276–19283 (2013).
  Medline CASGoogle Scholar
• 96 Wang JZ, Xia YY, Grundke-Iqbal I, Iqbal K. Abnormal hyperphosphorylation of tau: sites, regulation, and molecular mechanism of neurofibrillary degeneration. J. Alzheimers Dis. 33(Suppl. 1), S123–S129 (2012).
  Google Scholar
• 97 Shirazi SK, Wood JG. The protein tyrosine kinase, fyn, in Alzheimer's disease pathology. Neuroreport 4(4), 435–437 (1993).
  Medline CASGoogle Scholar
• 98 Sontag JM, Nunbhakdi-Craig V, White CL, Halpain S, Sontag E. The protein phosphatase PP2A/Balpha binds to the microtubule-associated proteins Tau and MAP2 at a motif also recognized by the kinase Fyn: implications for tauopathies. J. Biol. Chem. 287(18), 14984–14993 (2012).
  Medline CASGoogle Scholar
• 99 microRNA. www.microRNA.org.
  Google Scholar
• 100 Wang WX, Rajeev BW, Stromberg AJ et al. 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. 28(5), 1213–1223 (2008).
  MedlineGoogle Scholar
• 101 Hebert SS, Nelson PT. Studying microRNAs in the brain: technical lessons learned from the first ten years. Exp. Neurol. 235(2), 397–401 (2012).•• Summarizes technical variability contributions to variability between studies.
  Medline CASGoogle Scholar
• 102 Nelson PT, Wang WX, Wilfred BR, Tang G. Technical variables in high-throughput miRNA expression profiling: much work remains to be done. Biochim. Biophys. Acta 1779(11), 758–765 (2008).
  Medline CASGoogle Scholar
• 103 Markou A, Sourvinou I, Vorkas PA, Yousef GM, Lianidou E. Clinical evaluation of microRNA expression profiling in non small cell lung cancer. Lung Cancer 81(3), 388–396 (2013).
  Medline CASGoogle Scholar
• 104 Abe M, Bonini NM. MicroRNAs and neurodegeneration: role and impact. Trends Cell Biol. 23(1), 30–36 (2013).
  Medline CASGoogle Scholar
• 105 Faghihi MA, Zhang M, Huang J et al. Evidence for natural antisense transcript-mediated inhibition of microRNA function. Genome Biol. 11(5), R56 (2010).
  MedlineGoogle Scholar
• 106 Liu T, Huang Y, Chen J et al. Attenuated ability of BACE1 to cleave the amyloid precursor protein via silencing long noncoding RNA BACE1AS expression. Mol. Med. Rep. 10(3), 1275–1281 (2014).
  Medline CASGoogle Scholar
• 107 Banks WA, Farr SA, Butt W et al. Delivery across the blood-brain barrier of antisense directed against amyloid beta: reversal of learning and memory deficits in mice overexpressing amyloid precursor protein. J. Pharmacol. Exp. Ther. 297(3), 1113–1121 (2001).
  Medline CASGoogle Scholar
• 108 Fu AL, Zhang XM, Sun MJ. Antisense inhibition of acetylcholinesterase gene expression for treating cognition deficit in Alzheimer's disease model mice. Brain Res. 1066(1–2), 10–15 (2005).
  Medline CASGoogle Scholar
• 109 Chauhan NB, Siegel GJ. Antisense inhibition at the beta-secretase-site of beta-amyloid precursor protein reduces cerebral amyloid and acetyl cholinesterase activity in Tg2576. Neuroscience 146(1), 143–151 (2007).
  Medline CASGoogle Scholar
• 110 Jaeger LB, Dohgu S, Hwang MC et al. Testing the neurovascular hypothesis of Alzheimer's disease: LRP-1 antisense reduces blood-brain barrier clearance, increases brain levels of amyloid-beta protein, and impairs cognition. J. Alzheimers Dis. 17(3), 553–570 (2009).
  Medline CASGoogle Scholar
• 111 Zovoilis A, Agbemenyah HY, Agis-Balboa RC et al. microRNA-34c is a novel target to treat dementias. EMBO J. 30(20), 4299–4308 (2011).
  Medline CASGoogle Scholar
• 112 Erickson MA, Niehoff ML, Farr SA et al. Peripheral administration of antisense oligonucleotides targeting the amyloid-beta protein precursor reverses AbetaPP and LRP-1 overexpression in the aged SAMP8 mouse brain. J. Alzheimers Dis. 28(4), 951–960 (2012).
  Medline CASGoogle Scholar
• 113 Fiorini A, Sultana R, Forster S et al. Antisense directed against PS-1 gene decreases brain oxidative markers in aged senescence accelerated mice (SAMP8) and reverses learning and memory impairment: a proteomics study. Free Radic. Biol. Med. 65, 1–14 (2013).
  Medline CASGoogle Scholar
• 114 Farr SA, Erickson MA, Niehoff ML, Banks WA, Morley JE. Central and peripheral administration of antisense oligonucleotide targeting amyloid-beta protein precursor improves learning and memory and reduces neuroinflammatory cytokines in Tg2576 (AbetaPPswe) mice. J. Alzheimers Dis. 40(4), 1005–1016 (2014).
  Medline CASGoogle Scholar
• 115 Farr SA, Ripley JL, Sultana R et al. Antisense oligonucleotide against GSK-3beta in brain of SAMP8 mice improves learning and memory and decreases oxidative stress: Involvement of transcription factor Nrf2 and implications for Alzheimer disease. Free Radic. Biol. Med. 67, 387–395 (2014).
  Medline CASGoogle Scholar
• 116 Lennox KA, Behlke MA. Chemical modification and design of anti-miRNA oligonucleotides. Gene Ther. 18(12), 1111–1120 (2011).
  Medline CASGoogle Scholar
• 117 Yan Y, Yan J, Piao X, Zhang T, Guan Y. Effect of LNA- and OMeN-modified oligonucleotide probes on the stability and discrimination of mismatched base pairs of duplexes. J. Biosci. 37(2), 233–241 (2012).
  Medline CASGoogle Scholar
• 118 Murphy BL, Obad S, Bihannic L et al. Silencing of the miR-17˜92 cluster family inhibits medulloblastoma progression. Cancer Res. 73(23), 7068–7078 (2013).
  Medline CASGoogle Scholar
• 119 Koval ED, Shaner C, Zhang P et al. Method for widespread microRNA-155 inhibition prolongs survival in ALS-model mice. Hum. Mol. Genet. 22(20), 4127–4135 (2013).
  Medline CASGoogle Scholar
• 120 Nolan K, Mitchem MR, Jimenez-Mateos EM et al. Increased expression of microRNA-29a in ALS mice: functional analysis of its inhibition. J. Mol. Neurosci. 53(2), 231–241 (2014).
  Medline CASGoogle Scholar
• 121 Miller TM, Pestronk A, David W et al. An antisense oligonucleotide against SOD1 delivered intrathecally for patients with SOD1 familial amyotrophic lateral sclerosis: a Phase 1, randomised, first-in-man study. Lancet Neurol. 12(5), 435–442 (2013).
  Medline CASGoogle Scholar
• 122 Ebert MS, Sharp PA. MicroRNA sponges: progress and possibilities. RNA 16(11), 2043–2050 (2010).
  Medline CASGoogle Scholar
• 123 Barbato C, Pezzola S, Caggiano C et al. A lentiviral sponge for miR-101 regulates RanBP9 expression and amyloid precursor protein metabolism in hippocampal neurons. Front. Cell. Neurosci. 8, 37 (2014).
  MedlineGoogle Scholar
• 124 Wilton SD, Fletcher S. RNA splicing manipulation: strategies to modify gene expression for a variety of therapeutic outcomes. Curr. Gene. Ther. 5(5), 467–483 (2005).
  Medline CASGoogle Scholar
• 125 Rodriguez-Martin T, Anthony K, Garcia-Blanco MA et al. Correction of tau mis-splicing caused by FTDP-17 MAPT mutations by spliceosome-mediated RNA trans-splicing. Hum. Mol. Genet. 18(17), 3266–3273 (2009).• Reports an antisense therapeutic for modulation of exon skipping in Tau.
  Medline CASGoogle Scholar
• 126 Sud R, Geller ET, Schellenberg GD. Antisense-mediated exon skipping decreases tau protein expression: a potential therapy for tauopathies. Mol. Ther. Nucleic Acids 3, e180 (2014).
  Medline CASGoogle Scholar
• 127 Marwick C. First “antisense” drug will treat CMV retinitis. JAMA 280(10), 871 (1998).
  Medline CASGoogle Scholar
• 128 Sullivan JM, Yau EH, Taggart RT, Butler MC, Kolniak TA. Relieving bottlenecks in RNA drug discovery for retinal diseases. Adv. Exp. Med. Biol. 723, 145–153 (2012).•• Summarizes mipomersen, an antisense, as a therapeutic.
  Medline CASGoogle Scholar
• 129 Li N, Li Q, Tian XQ, Qian HY, Yang YJ. Mipomersen is a promising therapy in the management of hypercholesterolemia: a meta-analysis of randomized controlled trials. Am. J. Cardiovasc. Drugs 14(5), 367–376 (2014).
  Medline CASGoogle Scholar
• 130 Cuchel M, Bruckert E, Ginsberg HN et al. Homozygous familial hypercholesterolaemia: new insights and guidance for clinicians to improve detection and clinical management. A position paper from the Consensus Panel on Familial Hypercholesterolaemia of the European Atherosclerosis Society. Eur. Heart J. 35(32), 2146–2157 (2014).
  Medline CASGoogle Scholar