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Year : 2016  |  Volume : 7  |  Issue : 2  |  Page : 68-74

MicroRNA therapeutics: Discovering novel targets and developing specific therapy

Division of Clinical Research, University Centre of Excellence in Research, Baba Farid University of Health Science, Faridkot, Punjab, India

Date of Web Publication31-Mar-2016

Correspondence Address:
Parveen Bansal
Division of Clinical Research, University Centre of Excellence in Research, Baba Farid University of Health Science, Faridkot - 151 203, Punjab
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2229-3485.179431

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MicroRNAs (miRNAs) are small non-coding RNA molecules that regulate gene expression in diverse biological process. They act as intracellular mediators that are necessary for various biological processes. MicroRNAs targeting pathways of human disease provide a new and potential powerful candidate for therapeutic intervention against various pathological conditions. Even though, the information about miRNA biology has significantly enriched but we still do not completely understand the mechanism of miRNA gene regulation. Various groups across the globe and pharmaceutical companies are conducting research and developments to explore miRNA based therapy and build a whole new area of miroRNA therapeutics. Consequently, few miRNAs have entered the preclinical and clinical stage and soon might be available in the market for use in humans.

Keywords: Clinical stage, gene expression, microRNA, therapeutics

How to cite this article:
Christopher AF, Kaur RP, Kaur G, Kaur A, Gupta V, Bansal P. MicroRNA therapeutics: Discovering novel targets and developing specific therapy. Perspect Clin Res 2016;7:68-74

How to cite this URL:
Christopher AF, Kaur RP, Kaur G, Kaur A, Gupta V, Bansal P. MicroRNA therapeutics: Discovering novel targets and developing specific therapy. Perspect Clin Res [serial online] 2016 [cited 2023 Mar 23];7:68-74. Available from: http://www.picronline.org/text.asp?2016/7/2/68/179431

   Introduction Top

MicroRNAs (miRNAs) are small noncoding RNAs that are approximately 20–25 nucleotides in length. They regulate the expression of multiple target genes through sequence-specific hybridization to the 3′ untranslated region (UTR) of messenger RNAs. These microRNAs block the translation or they can cause direct degradation of their target messenger RNAs. miRNAs do not require perfect complementarity for target recognition, so a single miRNA is responsible for the regulation of multiple messenger RNAs. Although miRNAs exert slight effects on each individual messenger RNA target, the combined effect is significant and produces measurable phenotypic results. miRNAs play integral roles in several biological processes, including immune modulation, metabolic control, neuronal development, cell cycle, muscle differentiation, and stem cell differentiation. Most miRNAs are conserved across multiple animal species, indicating the evolutionary importance of these molecules as modulators of critical biological pathways and processes.

It has been seen that expressions of many miRNAs are altered in different diseases. Some miRNAs are overexpressed whereas some are underexpressed in a particular disease giving rise to signature miRNA pattern. With the discovery of miRNAs and its critical role as regulators in various diseases, it is quiet relevant to explore and understand the possibility of using miRNA as therapeutic agents. Recent studies in animals and humans conducted in different laboratories present data that strengthen the candidature of miRNAs to establish the candidature of miRNAs to establish as a novel class of drugs, i.e., miRNA therapeutics.[1],[2] The miRNAs possess a unique characteristic which is very attractive in terms of drug development, i.e.,. they are small, with known sequences and are often conserved among species. Based on antisense technology, very potent oligonucleotide targeted against miRNA known as anti-miR is being developed. An ideal design for an active synthetic miRNA is that it should bind to its respective targeted miRNA with high affinity and specificity.

This review will focus on miRNA and its biogenesis, importance in various diseases, the potential of using miRNAs as a therapeutic modality, and finally an update on the status of clinical trials.

   History Top

In 1993, first miRNA was discovered during a study on gene Lin-4 of Caenorhabditiselegans.[3] It was seen after the isolation of Lin-4 that the gene encodes a protein that binds to 3′ UTR of Lin-14 mRNA and hence prevents translation of Lin-14. In 2000, second small RNA let-7 was discovered; it repressed Lin-4 mRNA to promote a later developmental transition in C.elegans.[4] Subsequently, it was discovered that lin-4 and let-7 were found in Drosophila and human cells, respectively. Most of the RNAs of this class resembled the Lin-4 and let-7 RNAs, however they had no role in regulating the timing of development thereby suggesting that most of miRNAs were involved in other types of regulatory pathways. Following this, the term “miRNA” to refer to this class of small regulatory RNAs came into existence.

MicroRNAs: Tiny master regulators

The miRNAs are known to be expressed in most organisms from plant to vertebrates (including viruses) and are conserved in all organisms. They regulate gene expression by either degrading or making the targeted mRNAs “silence” rendering their translation into proteins. The miRNAs regulate gene expressions, which affect various biological processes such as cell proliferation, differentiation, survival, and motility. The miRNAs do not require perfect complementarity for target recognition, so a single miRNA is able to regulate multiple mRNAs. On average, a given miRNA can regulate several hundred transcripts whose effector molecules function at various sites within cellular pathways and networks. Consequently, miRNAs are able to switch instantly between cellular programs and are therefore often viewed as tiny master regulators of the human genome.

The miRNAs are predicted using different approaches such as experimental method, computational approach, expressed sequence tag, and genomic survey sequence analysis. However, only a few predicted miRNAs have undergone validation experimentally. Computational analysis indicates that the total number of miRNAs could be more that 1% of total translated genes and more than 30% of protein-coding genes may be targeted by miRNAs.

MicroRNA biogenesis

The miRNA genes are expressed in the cell nucleus. About 70% of the human miRNAs are transcribed from introns and/or exons. A brief overview of miRNA biogenesis is shown in [Figure 1].
Figure 1: Schematic overview of microRNA biogenesis

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Association of microRNA with various diseases

miRNAs are becoming increasingly recognized as their expressions are altered in different diseases such as cancer, hepatitis C infection, myocardial infarction, and metabolic disease. Some miRNAs are overexpressed whereas some are underexpressed in a particular disease giving rise to a signature miRNA pattern. In case of tumors, the miRNAs which are overexpressed may be considered as oncogenes and are called “oncomirs.”[5] They are considered to be involved in tumor development by reciprocally inhibiting tumor suppressor genes (genes that control cell differentiation and apoptosis), for example, miR-17–192 is significantly overexpressed in lung cancer and several other lymphomas. On the other hand, expression of some miRNAs (tumor suppressor) is lower in cancerous cells and usually prevents tumor development by negatively inhibiting oncogenes, for example, let-7 is a tumor suppressor miRNA and aberrant expression of let-7 results in oncogenic loss of differentiation.[6] An overview of the association of signature miRNA with some disease condition is given in [Table 1]. The signature miRNAs associated with disease are discussed in the following sections.
Table 1: Differentially expressed microRNAs (signature microRNAs) in various diseases

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MiR-122 in hepatitis C virus

MiR-122 is the most commonly found miRNA in the adult liver and plays a key role in liver biology that includes development, differentiation, homeostasis, and functions. It controls the metabolism, i.e., cholesterol biosynthesis. miR-122 is involved in the replication of hepatitis C virus (HCV). It binds to the viral genome and enhances viral translation and replication. The binding site in the 5′ end of HCV genome provided the evidence of the direct role of miR-122 into HCV replication.[7],[8]

MiR-33a in metabolic disease

miR-33a targets genes involved in cholesterol export such as the adenosine triphosphate-binding cassette (ABC) transporters ABCA1 and ABCG1 and the endolysosomal transport protein Niemann-Pick C1 (Npc1). In agreement with the regulation of ABCA1 by miR-33, modulation of miR-33a levels results in encompassing effects in cholesterol efflux in macrophages thus suggesting that miR-33 may participate in the regulation of high-density lipoprotein (HDL) levels in vivo. Indeed, three independent studies have demonstrated that endogenous inhibition of miR-33 using different strategies leads to a significant increase in hepatic ABCA1 expression and plasma HDL levels, and these findings were later confirmed in the miR-33 knockout mice.[9]

MiR-155 in inflammatory disease

miR-155 is overexpressed in atopic dermatitis and contributes to chronic skin inflammation by increasing the proliferative response of T-helper cells through the downregulation of cytotoxic T-lymphocyte antigen-4.[10] In autoimmune disorders such as rheumatoid arthritis, miR-155 showed higher expression in patients' tissues and synovial fibroblasts.[11] In multiple sclerosis, increased expression of miR-155 has also been measured in peripheral and central nervous system-resident myeloid cells, including circulating blood monocytes and activated microglia. Overexpression of miR-155 leads to chronic inflammatory state in human.

MiR-10b in glioblastoma

The levels of miR-10b are upregulated in human glioblastoma tissues, glioblastoma cell, and stem cell lines as compared to normal human tissues or astrocytes [12] Inhibition of miR-10b inhibits glioblastoma proliferation, reduces cell invasion, and migration in glioblastoma cell and stem cell lines whereas overexpression of miR-10b induced cell migration and invasion.

MiR-33 in atherosclerosis

Plasma HDL levels have a protective role in atherosclerosis. miR-33, an intronic miRNA located within the SREBF2 gene, suppresses the expression of the cholesterol transporter ABC transporter A1 (ABCA1) and lowers HDL levels. Conversely, mechanisms that inhibit miR-33 increase ABCA1 and circulating HDL levels, suggesting that antagonism of miR-33 may be atheroprotective. In a study, mice deficient for the low-density lipoprotein receptor (LDLr–/– mice), with established atherosclerotic plaques treated with anti-miR33 for 4 weeks, showed an increase in circulating HDL levels and enhanced reverse cholesterol transport to the plasma, liver, and feces.[13] Consistent with this, anti-miR33-treated mice showed reductions in plaque size and lipid content, increased markers of plaque stability, and decreased inflammatory gene expression. Notably, in addition to raising ABCA1 levels in the liver, anti-miR33 oligonucleotides directly targeted the plaque macrophages, in which they enhanced ABCA1 expression and cholesterol removal. Thus, raising HDL levels by anti-miR33 oligonucleotide treatment promotes reverse cholesterol transport and atherosclerosis regression.

MiR-21 in hepatocellular carcinoma

Deregulated expressions of several miRNAs were found to correlate with the pathologic and clinical characteristics of hepatocellular carcinoma HCC.[14] The miRNA microarray analysis has revealed that miR-21 was dramatically elevated in HCC tumor cells, with significant reductions of the expressions of several tumor suppressor genes, including PTEN, PDCD4, RECK, and TPM1 (PTEN).[15] MAP2K3 has also been identified as a novel direct target of miR-21. The study of loss-of-function of miR-21 by transduction of miR-21 sponge in HepG2 cells indicated that miR-21 might regulate cell proliferation, apoptosis, and invasiveness partially by targeting MAP2K3.

MicroRNA as therapeutic target and tool

The expression of miRNAs is altered in various diseases and it is now feasible to manipulate miRNA expression by injecting miRNAs similar to the use of antisense mRNAs and RNAi (widely used techniques for investigating gene function and in gene therapy).[16] As the activation of oncogenes could cause cancer, artificial antisense miRNAs could be synthesized and employed to block their targeted oncomirs to prevent the formation of cancer. However, various critical prerequisite data must be available, for example, identification of signature miRNAs, their mechanism of action, applicability by RNAi, delivery of miRNAs, and their active form in vivo. Once this information is available, miRNA will have a bright future and become a novel therapeutic tool. The process of building miRNA therapeutics is similar to drug discovery and development. Following steps are involved in the discovery and development of miRNA therapeutics [Figure 2]:
Figure 2: Process of microRNA discovery and development

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  • Identification of signature miRNA (done by miRNA profiling in disease)
  • Validation of signature miRNA (loss/gain of function studies in vitro and in animal models)
  • Pharmacological analysis (in vivo miRNA delivery studies, pharmacokinetics/pharmacodynamics, (absorption, distribution, metabolism, excretion, and toxicity studies)
  • Clinical trials (studies on the evaluation of efficacy and safety).

Strategies for microRNA manipulation

There are two main strategies to manipulate miRNAs which are dependent on whether the targeted miRNA expression needs to be downregulated or to re-introduce miRNAs function to restore loss of function. The strategies for miRNA manipulation are summarized in [Table 2].
Table 2: Various microRNAs-based therapeutic strategies investigated in cancer

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Antisense inhibition of mature microRNA (inhibiting oncomirs)

The miRNA antagonists are oligonucleotides containing the complementary sequences of endogenous miRNAs. Antisense oligonucleotide (AMO), also called antagomir, is the most commonly used anti-miRNA antisense oligomer.[2] The locked nucleic acid possess stronger affinity to targeted miRNA, more resistant to nucleases, and have lower toxicity. The peptide nucleic acid (PNA) is an artificial synthesized peptide-structured polymer and is similar to DNA and RNA. The PNA binds the targeted nucleotide more tightly than the nucleotide/nucleotide binding, are relatively stable, have low toxicity, and could be administered systematically.[17] The latest new strategy available is miRNA sponge and miRNA masking. The miRNA sponge downregulates the targeted miRNA and possesses multiple complementary sites to the targeted miRNA,[18] whereas miRNA masking have complimentary miRNA binding site in the 3′ UTR of the target mRNA to inhibit competitively and decreases the activity of endogenous miRNA. The various antisense inhibitors employed for downregulating various miRNAs are depicted in [Table 3].
Table 3: Various methods available for the delivery of microRNAs

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Replacement of microRNAs

In diseases such as cancer, expression levels of downregulated miRNAs or altered miRNA could be done using vector, overexpressing the targeted miRNA or by the transfection of double-stranded miRNAs. Therefore, studies have been conducted by introducing artificial double-stranded miRNA (mimic of targeted downregulated miRNA). For example, overexpression of downregulated miR-26a in hepatocellular carcinoma (HCC) in mouse liver resulted in inhibition of cancer proliferation and initiation of apoptosis. Subsequently in another study, the downregulated miR-34a level was increased by delivering artificial miR-34a with NOV340 liposome in an orthotopic model of HCC.[19] This resulted in significant tumor reduction, prolonged survival, and disease protection in animals.

Patent and clinical trial status of microRNA therapeutics

There is a great excitement regarding miRNA use as therapeutic entities. In terms of scientific perspective, miRNA represents a novel and an attractive target which could manipulate the body functions. Consequently, there has been considerable increase in the number of patent applications filed over the decade. The annual number of US and European published patent applications and issued patents related to miRNAs is close to 500. A snapshot of the current development status of miRNA-based therapeutics is summarized in [Table 4].
Table 4: Overview of microRNAs therapeutics development status

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Future perspectives of microRNA therapeutics

The functionality of miRNA in controlling diverse gene expression in cancer and various other important diseases makes miRNA an ideal candidate for therapeutic applications. Recent data demonstrate that the miRNA expression is altered in various human diseases and its selective modulation through antisense inhibition or replacement could significantly affect the prognosis of a disease. With the technological advancement and ease of administration of miRNA through local or parenteral injection routes and its sufficient uptake in the tissue without the need of developing formulation gives miRNA therapeutics an extra edge. We hope that with increasing research and development on miRNA, increase in the filed patents and increased attention and interest of the biotechnology companies in miRNA-based therapeutics would follow suit. This promises the availability of miRNA therapeutics in the market in the coming years for the treatment of various diseases.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3], [Table 4]

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38 Epigenetics, microRNA and Metabolic Syndrome: A Comprehensive Review
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40 miRNAs as Therapeutic Tools in Alzheimer’s Disease
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84 microRNAs: New-Age Panacea in Cancer Therapeutics
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85 Cardiomyocyte microvesicles: proinflammatory mediators after myocardial ischemia?
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86 MicroRNAs (miRNAs) and Long Non-Coding RNAs (lncRNAs) as New Tools for Cancer Therapy: First Steps from Bench to Bedside
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87 Targeting SARS CoV2 (Indian isolate) genome with miRNA: An in silico study
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88 iDrug: Integration of drug repositioning and drug-target prediction via cross-network embedding
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89 Regulation of hepatic microRNAs in response to early stage Echinococcus multilocularis egg infection in C57BL/6 mice
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90 Epigenetic Marks in Polycystic Ovary Syndrome
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91 Mesenchymal Stem Cell and MicroRNA Therapy of Musculoskeletal Diseases
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92 MiRNAs: A New Approach to Predict and Overcome Resistance to Anticancer Drugs
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93 Let-7i-5p Regulation of Cell Morphology and Migration Through Distinct Signaling Pathways in Normal and Pathogenic Urethral Fibroblasts
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94 The Enigmatic Role of Serum & Glucocorticoid Inducible Kinase 1 in the Endometrium
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95 microRNA-137 downregulates MCL1 in ovarian cancer cells and mediates cisplatin-induced apoptosis
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96 The roles of miRNAs’ clinical efficiencies in the colorectal cancer pathobiology: A review article
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97 Epigenetic regulation by polyphenols in diabetes and related complications
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98 Structural Insights on Tiny Peptide Nucleic Acid (PNA) Analogues of miRNA-34a: An in silico and Experimental Integrated Approach
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99 Small-Medium Extracellular Vesicles and Their miRNA Cargo in Retinal Health and Degeneration: Mediators of Homeostasis, and Vehicles for Targeted Gene Therapy
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100 Tick Salivary Compounds for Targeted Immunomodulatory Therapy
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101 Editorial: Regulation of Soluble Immune Mediators by Non-Coding RNAs
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102 Revisiting Traumatic Brain Injury: From Molecular Mechanisms to Therapeutic Interventions
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103 miR-98 Regulates TMPRSS2 Expression in Human Endothelial Cells: Key Implications for COVID-19
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104 Up-regulation of MicroRNAs-21 and -223 in a Sprague-Dawley Rat Model of Traumatic Spinal Cord Injury
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105 MicroRNAs in Rectal Cancer: Functional Significance and Promising Therapeutic Value
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106 snoRNAs Offer Novel Insight and Promising Perspectives for Lung Cancer Understanding and Management
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107 The Promise and Challenges of Developing miRNA-Based Therapeutics for Parkinson’s Disease
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108 MiR-337-3p Promotes Adipocyte Browning by Inhibiting TWIST1
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109 miR-615 Fine-Tunes Growth and Development and Has a Role in Cancer and in Neural Repair
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110 miR-7 Regulates GLP-1-Mediated Insulin Release by Targeting ß-Arrestin 1
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111 MicroRNA Regulatory Pathways in the Control of the Actin–Myosin Cytoskeleton
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112 Current Status of microRNA-Based Therapeutic Approaches in Neurodegenerative Disorders
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113 miR-196B-5P and miR-200B-3P Are Differentially Expressed in Medulloblastomas of Adults and Children
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114 miR-146a-5p and miR-193a-5p Synergistically Inhibited the Proliferation of Human Colorectal Cancer Cells (HT-29 cell line) through ERK Signaling Pathway
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115 Otoimmün tiroid hastaliklarinda CTLA-4 geninin in silico analizinin degerlendirilmesi
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116 Identification of Acute Myeloid Leukemia Bone Marrow Circulating MicroRNAs
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119 Improved annotation of Lutzomyia longipalpis genome using bioinformatics analysis
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121 RAF Kinase Inhibitor Protein in Myeloid Leukemogenesis
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122 A Brief Overview of lncRNAs in Endothelial Dysfunction-Associated Diseases: From Discovery to Characterization
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125 Cytokine Targeting by miRNAs in Autoimmune Diseases
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126 Novel Treatments for Polycystic Kidney Disease
Ameya Patil,William E. Sweeney,Cynthia G. Pan,Ellis D. Avner,Meral Gunay-Aygun
Translational Science of Rare Diseases. 2019; 4(1-2): 77
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127 Application of microRNA in the therapy of ischemic stroke
I. F. Gareev,L. B. Novikova,O. A. Beylerli
Cardiovascular Therapy and Prevention. 2019; 18(5): 66
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128 miR-181a/b downregulation exerts a protective action on mitochondrial disease models
Alessia Indrieri,Sabrina Carrella,Alessia Romano,Alessandra Spaziano,Elena Marrocco,Erika Fernandez-Vizarra,Sara Barbato,Mariateresa Pizzo,Yulia Ezhova,Francesca M Golia,Ludovica Ciampi,Roberta Tammaro,Jorge Henao-Mejia,Adam Williams,Richard A Flavell,Elvira De Leonibus,Massimo Zeviani,Enrico M Surace,Sandro Banfi,Brunella Franco
EMBO Molecular Medicine. 2019; 11(5)
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129 Molecular Docking Study for Analyzing the Inhibitory Effect of Anti-inflammatory Plant Compound Against Tumour Necrosis Factor (TNF-a)
Sagarika Biswas
Current Drug Therapy. 2019; 14(1): 85
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130 Applications of miRNAs in cardiac development, disease progression and regeneration
Jeremy Kah Sheng Pang,Qian Hua Phua,Boon-Seng Soh
Stem Cell Research & Therapy. 2019; 10(1)
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131 The therapeutic effects of microRNAs in preclinical studies of acute kidney injury: a systematic review protocol
Sarah Zankar,Rosendo A. Rodriguez,Jose Luis Vinas,Kevin D. Burns
Systematic Reviews. 2019; 8(1)
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132 A novel miR-365-3p/EHF/keratin 16 axis promotes oral squamous cell carcinoma metastasis, cancer stemness and drug resistance via enhancing ß5-integrin/c-met signaling pathway
Wei-Chieh Huang,Te-Hsuan Jang,Shiao-Lin Tung,Tzu-Chen Yen,Shih-Hsuan Chan,Lu-Hai Wang
Journal of Experimental & Clinical Cancer Research. 2019; 38(1)
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133 Screening of microRNAs controlling body fat in Drosophila melanogaster and identification of miR-969 and its target, Gr47b
William Redmond,Dylan Allen,M. Christian Elledge,Russell Arellanes,Lucille Redmond,Jared Yeahquo,Shuyin Zhang,Morgan Youngblood,Austin Reiner,Jin Seo,Gregg Roman
PLOS ONE. 2019; 14(7): e0219707
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134 Demonstrating specificity of bioactive peptide nucleic acids (PNAs) targeting microRNAs for practical laboratory classes of applied biochemistry and pharmacology
Jessica Gasparello,Chiara Papi,Matteo Zurlo,Roberto Corradini,Roberto Gambari,Alessia Finotti,Maxim Antopolsky
PLOS ONE. 2019; 14(9): e0221923
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135 MicroRNA-193a and taxol combination: A new strategy for treatment of colorectal cancer
Maryam Hejazi,Elham Baghbani,Mohammad Amini,Tayebeh Rezaei,Ayuob Aghanejad,Jafar Mosafer,Ahad Mokhtarzadeh,Behzad Baradaran
Journal of Cellular Biochemistry. 2019;
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136 miR-146b Reverses epithelial-mesenchymal transition via targeting PTP1B in cisplatin-resistance human lung adenocarcinoma cells
Qian Han,Peng Cheng,Hongjie Yang,Hengpo Liang,Fengchun Lin
Journal of Cellular Biochemistry. 2019;
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137 Dgcr8 knockout approaches to understand microRNA functions in vitro and in vivo
Wen-Ting Guo,Yangming Wang
Cellular and Molecular Life Sciences. 2019;
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138 Current Evidence on Potential Uses of MicroRNA Biomarkers for Migraine: From Diagnosis to Treatment
Parisa Gazerani
Molecular Diagnosis & Therapy. 2019;
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139 Therapeutic microRNAs in human cancer
Gizem Ors-Kumoglu,Sultan Gulce-Iz,Cigir Biray-Avci
Cytotechnology. 2019;
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140 A cross-cancer metastasis signature in the microRNA–mRNA axis of paired tissue samples
Samuel C. Lee,Alistair Quinn,Thin Nguyen,Svetha Venkatesh,Thomas P. Quinn
Molecular Biology Reports. 2019;
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141 miR-146a-5p: Expression, regulation, and functions in cancer
Joseph R. Iacona,Carol S. Lutz
Wiley Interdisciplinary Reviews: RNA. 2019; : e1533
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142 Early-onset preeclampsia, plasma microRNAs, and endothelial cell function
Simone V. Lip,Mark V. Boekschoten,Guido J. Hooiveld,Mariëlle G. van Pampus,Sicco A. Scherjon,Torsten Plösch,Marijke M. Faas
American Journal of Obstetrics and Gynecology. 2019;
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143 Developmental origins of type 2 diabetes: Focus on epigenetics
Alexander Vaiserman,Oleh Lushchak
Ageing Research Reviews. 2019; 55: 100957
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144 Small non-coding RNAs as important players, biomarkers and therapeutic targets in multiple sclerosis: A comprehensive overview
Eliane Piket,Galina Yurevna Zheleznyakova,Lara Kular,Maja Jagodic
Journal of Autoimmunity. 2019;
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145 Preclinical Targeting of MicroRNA-214 in Cutaneous T-Cell Lymphoma
Rebecca Kohnken,Betina McNeil,Jing Wen,Kathleen McConnell,Leah Grinshpun,Ashleigh Keiter,Luxi Chen,Basem William,Pierluigi Porcu,Anjali Mishra
Journal of Investigative Dermatology. 2019;
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146 Diabetic Nephropathy: the regulatory interplay between Epigenetics and microRNAs
Himanshu Sankrityayan,Yogesh A. Kulkarni,Anil Bhanudas Gaikwad
Pharmacological Research. 2019;
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147 Efferocytosis and Atherosclerosis: Regulation of Phagocyte Function by MicroRNAs
Amir Tajbakhsh,Vanessa Bianconi,Matteo Pirro,Seyed Mohammad Gheibi Hayat,Thomas P. Johnston,Amirhossein Sahebkar
Trends in Endocrinology & Metabolism. 2019;
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Alejandro Fulgencio-Covián,Esmeralda Alonso-Barroso,Adam J Guenzel,Ana Rivera-Barahona,Magdalena Ugarte,Belén Pérez,Michael A Barry,Celia Pérez-Cerdá,Eva Richard,Lourdes R Desviat
Translational Research. 2019;
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149 miRNAs and their roles in KSHV pathogenesis
Hosni A.M. Hussein,Mohammad A. Alfhili,Pranaya Pakala,Sandra Simon,Jaffer Hussain,James A. McCubrey,Shaw M. Akula
Virus Research. 2019; 266: 15
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150 Regulación por micro RNA de la respuesta angiogénica en la retina diabética
Helena Cristina Campos-Borges,Silvia María Sanz-González,Vicente Zanón-Moreno,Jose María Millán Salvador,María Dolores Pinazo-Duran
Archivos de la Sociedad Española de Oftalmología. 2019;
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151 Micro-RNA regulation of the angiogenic response in the diabetic retina
H.C. Campos-Borges,S.M. Sanz-González,V. Zanón-Moreno,J.M. Millán Salvador,M.D. Pinazo-Duran
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152 A Sendai Virus-Based Cytoplasmic RNA Vector as a Novel Platform for Long-Term Expression of MicroRNAs
Masayuki Sano,Asako Nakasu,Manami Ohtaka,Mahito Nakanishi
Molecular Therapy - Methods & Clinical Development. 2019; 15: 371
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153 Abnormal Expression of miR-21 in Kidney Tissue of Dogs With X-Linked Hereditary Nephropathy: A Canine Model of Chronic Kidney Disease
Sabrina D. Clark,Wenping Song,Rachel Cianciolo,George Lees,Mary Nabity,Shiguang Liu
Veterinary Pathology. 2019; 56(1): 93
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154 Encapsulated miR-200c and Nkx2.1 in a nuclear/mitochondria transcriptional regulatory network of non-metastatic and metastatic lung cancer cells
Olga D’Almeida,Omar Mothar,Esther Apraku Bondzie,Yolande Lieumo,Laure Tagne,Sumeet Gupta,Thomas Volkert,Stuart Levine,Jean-Bosco Tagne
BMC Cancer. 2019; 19(1)
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155 Adipokines Regulate the Expression of Tumor-Relevant MicroRNAs
Simon Jasinski-Bergner, Heike Kielstein
Obesity Facts. 2019; 12(2): 211
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156 MicroRNA-let-7c suppresses hepatitis C virus replication by targeting Bach1 for induction of haem oxygenase-1 expression
Wei-Chun Chen,Chih-Ku Wei,Jin-Ching Lee
Journal of Viral Hepatitis. 2019;
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157 The Purinergic System as a Pharmacological Target for the Treatment of Immune-Mediated Inflammatory Diseases
Luca Antonioli,Corrado Blandizzi,Pál Pacher,György Haskó,Clive Page
Pharmacological Reviews. 2019; 71(3): 345
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158 Efficient Delivery of MicroRNA and AntimiRNA Molecules Using an Argininocalix[4]arene Macrocycle
Jessica Gasparello,Michela Lomazzi,Chiara Papi,Elisabetta D’Aversa,Francesco Sansone,Alessandro Casnati,Gaetano Donofrio,Roberto Gambari,Alessia Finotti
Molecular Therapy - Nucleic Acids. 2019; 18: 748
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159 miR-146a targeted to splenic macrophages prevents sepsis-induced multiple organ injury
Yoshio Funahashi,Noritoshi Kato,Tomohiro Masuda,Fumitoshi Nishio,Hiroki Kitai,Takuji Ishimoto,Tomoki Kosugi,Naotake Tsuboi,Naoyuki Matsuda,Shoichi Maruyama,Kenji Kadomatsu
Laboratory Investigation. 2019;
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160 Molecular mechanism of miR-204 regulates proliferation, apoptosis and autophagy of cervical cancer cells by targeting ATF2
Nan Li,XiaoRong Guo,Lei Liu,Lu Wang,Rongjie Cheng
Artificial Cells, Nanomedicine, and Biotechnology. 2019; 47(1): 2529
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161 Dysregulated Expression of microRNA-21 and Disease-Related Genes in Human Patients and in a Mouse Model of Alport Syndrome
Jifan Guo,Wenping Song,Joseph Boulanger,Ethan Y. Xu,Fang Wang,Yanqin Zhang,Qun He,Suxia Wang,Li Yang,Cynthia Pryce,Lucy Phillips,Deidre MacKenna,Ekkehard Leberer,Oxana Ibraghimov-Beskrovnaya,Jie Ding,Shiguang Liu
Human Gene Therapy. 2019;
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162 Pathogenesis and treatment of autoimmune rheumatic diseases
Eric Liu,Andras Perl
Current Opinion in Rheumatology. 2019; 31(3): 307
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163 MicroRNA-519d-3p inhibits cell proliferation and cell cycle G1/S transition in glioma by targeting CCND1
Lishan Ma,Jin Li
Bioscience, Biotechnology, and Biochemistry. 2019; : 1
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164 A journey through the emergence of nanomedicines with poly(alkylcyanoacrylate) based nanoparticles
Christine Vauthier
Journal of Drug Targeting. 2019; : 1
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165 Transcriptomic studies provide insights into the tumor suppressive role of miR-146a-5p in non-small cell lung cancer (NSCLC) cells
Joseph R. Iacona,Nicholas J. Monteleone,Alexander D. Lemenze,Ashley L. Cornett,Carol S. Lutz
RNA Biology. 2019; : 1
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166 Inhibition of microRNA-711 limits angiopoietin-1 and Akt changes, tissue damage, and motor dysfunction after contusive spinal cord injury in mice
Boris Sabirzhanov,Jessica Matyas,Marina Coll-Miro,Laina Lijia Yu,Alan I. Faden,Bogdan A. Stoica,Junfang Wu
Cell Death & Disease. 2019; 10(11)
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167 Adipocyte metabolism is improved by TNF receptor-targeting small RNAs identified from dried nuts
Katia Aquilano,Veronica Ceci,Angelo Gismondi,Susanna De Stefano,Federico Iacovelli,Raffaella Faraonio,Gabriele Di Marco,Noemi Poerio,Antonella Minutolo,Giuseppina Minopoli,Antonia Marcone,Maurizio Fraziano,Flavia Tortolici,Simona Sennato,Stefano Casciardi,Marina Potestà,Roberta Bernardini,Maurizio Mattei,Mattia Falconi,Carla Montesano,Stefano Rufini,Antonella Canini,Daniele Lettieri-Barbato
Communications Biology. 2019; 2(1)
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168 TGF-ß induces miR-100 and miR-125b but blocks let-7a through LIN28B controlling PDAC progression
Silvia Ottaviani,Justin Stebbing,Adam E. Frampton,Sladjana Zagorac,Jonathan Krell,Alexander de Giorgio,Sara M. Trabulo,Van T. M. Nguyen,Luca Magnani,Hugang Feng,Elisa Giovannetti,Niccola Funel,Thomas M. Gress,Long R. Jiao,Ylenia Lombardo,Nicholas R. Lemoine,Christopher Heeschen,Leandro Castellano
Nature Communications. 2018; 9(1)
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169 Diabetes induces the activation of pro-ageing miR-34a in the heart, but has differential effects on cardiomyocytes and cardiac progenitor cells
Ingrid Fomison-Nurse,Eugene Eng Leng Saw,Sophie Gandhi,Pujika Emani Munasinghe,Isabelle Van Hout,Michael J. A Williams,Ivor Galvin,Richard Bunton,Philip Davis,Vicky Cameron,Rajesh Katare
Cell Death & Differentiation. 2018;
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170 The silent healer: miR-205-5p up-regulation inhibits epithelial to mesenchymal transition in colon cancer cells by indirectly up-regulating E-cadherin expression
Diana Gulei,Lorand Magdo,Ancuta Jurj,Lajos Raduly,Roxana Cojocneanu-Petric,Alin Moldovan,Cristian Moldovan,Adrian Florea,Sergiu Pasca,Laura-Ancuta Pop,Vlad Moisoiu,Liviuta Budisan,Cecilia Pop-Bica,Cristina Ciocan,Rares Buiga,Mihai-Stefan Muresan,Rares Stiufiuc,Calin Ionescu,Ioana Berindan-Neagoe
Cell Death & Disease. 2018; 9(2)
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171 PTBP1 enhances miR-101-guided AGO2 targeting to MCL1 and promotes miR-101-induced apoptosis
Jia Cui,William J. Placzek
Cell Death & Disease. 2018; 9(5)
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172 New insights into the genetics and epigenetics of systemic sclerosis
Chiara Angiolilli,Wioleta Marut,Maarten van der Kroef,Eleni Chouri,Kris A. Reedquist,Timothy R. D. J. Radstake
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173 Muscle miRNAome shows suppression of chronic inflammatory miRNAs with both prednisone and vamorolone
Alyson A. Fiorillo,Christopher B. Tully,Jesse M. Damsker,Kanneboyina Nagaraju,Eric P. Hoffman,Christopher R. Heier
Physiological Genomics. 2018; 50(9): 735
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174 Role of microRNA-223 in the regulation of poly(ADP-ribose) polymerase in pediatric patients with Crohn’s disease
Nóra Judit Béres,Zoltán Kiss,Katalin E. Müller,Áron Cseh,Apor Veres-Székely,Rita Lippai,Rita Benko,Árpád Bartha,Szabolcs Heininger,Ádám Vannay,Erna Sziksz,Gábor Veres,Eszter M. Horváth
Scandinavian Journal of Gastroenterology. 2018; : 1
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175 MicroRNA-based therapeutics in central nervous system injuries
Ping Sun,Da Zhi Liu,Glen C Jickling,Frank R Sharp,Ke-Jie Yin
Journal of Cerebral Blood Flow & Metabolism. 2018; 38(7): 1125
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176 Liquid biopsy in mice bearing colorectal carcinoma xenografts: gateways regulating the levels of circulating tumor DNA (ctDNA) and miRNA (ctmiRNA)
Jessica Gasparello,Matteo Allegretti,Elisa Tremante,Enrica Fabbri,Carla Azzurra Amoreo,Paolo Romania,Elisa Melucci,Katia Messana,Monica Borgatti,Patrizio Giacomini,Roberto Gambari,Alessia Finotti
Journal of Experimental & Clinical Cancer Research. 2018; 37(1)
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177 MicroRNAs: Roles in Regulating Neuroinflammation
Andrew D. Gaudet,Laura K. Fonken,Linda R. Watkins,Randy J. Nelson,Phillip G. Popovich
The Neuroscientist. 2018; 24(3): 221
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178 Enhancer Remodeling and MicroRNA Alterations Are Associated with Acquired Resistance to ALK Inhibitors
Mi Ran Yun,Sun Min Lim,Seon-Kyu Kim,Hun Mi Choi,Kyoung-Ho Pyo,Seong Keun Kim,Ji Min Lee,You Won Lee,Jae Woo Choi,Hye Ryun Kim,Min Hee Hong,Keeok Haam,Nanhyung Huh,Jong-Hwan Kim,Yong Sung Kim,Hyo Sup Shim,Ross Andrew Soo,Jin-Yuan Shih,James Chih-Hsin Yang,Mirang Kim,Byoung Chul Cho
Cancer Research. 2018; 78(12): 3350
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179 miRTissue: a web application for the analysis of miRNA-target interactions in human tissues
Antonino Fiannaca,Massimo La Rosa,Laura La Paglia,Alfonso Urso
BMC Bioinformatics. 2018; 19(S15)
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180 Predictive modeling of miRNA-mediated predisposition to alcohol-related phenotypes in mouse
Pratyaydipta Rudra,Wen J. Shi,Pamela Russell,Brian Vestal,Boris Tabakoff,Paula Hoffman,Katerina Kechris,Laura Saba
BMC Genomics. 2018; 19(1)
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181 Exosome-Mediated Small RNA Delivery: A Novel Therapeutic Approach for Inflammatory Lung Responses
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182 At the heart of programming: the role of micro-RNAs
B. Siddeek,C. Mauduit,C. Yzydorczyk,M. Benahmed,U. Simeoni
Journal of Developmental Origins of Health and Disease. 2018; : 1
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183 Combined Therapy in Cancer: The Non-coding Approach
Diana Gulei,Ioana Berindan-Neagoe
Molecular Therapy - Nucleic Acids. 2018; 12: 787
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184 Multifunctional nanocarrier as a potential micro-RNA delivery vehicle for neuroblastoma treatment
Ndumiso Vukile Mdlovu,Yun Chen,Kuen-Song Lin,Ming-Wei Hsu,Steven S.-S. Wang,Chun-Ming Wu,You-Sheng Lin,Kazuki Ohishi
Journal of the Taiwan Institute of Chemical Engineers. 2018;
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185 Expression Analysis of microRNA-21 and microRNA-122 in Hepatocellular Carcinoma
Dipu Bharali,Basu Dev Banerjee,Mausumi Bharadwaj,Syed Akhtar Husain,Premashis Kar
Journal of Clinical and Experimental Hepatology. 2018;
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186 Reproductive role of miRNA in the hypothalamic-pituitary axis
Chunyu Cao,Yifei Ding,Xiangjun Kong,Guangde Feng,Wei Xiang,Long Chen,Fang Yang,Ke Zhang,Mingxing Chu,Pingqing Wang,Baoyun Zhang
Molecular and Cellular Neuroscience. 2018; 88: 130
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187 MicroRNA-124 and microRNA-146a both attenuate persistent neuropathic pain induced by morphine in male rats
Peter M. Grace,Keith A. Strand,Erika L. Galer,Steven F. Maier,Linda R. Watkins
Brain Research. 2018; 1692: 9
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188 Perspectives on the physiological roles of microRNAs in immune-metabolism: Where are we now?
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Cancer Letters. 2018; 426: 1
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189 Epigenetic Changes in Airway Smooth Muscle as a Driver of Airway Inflammation and Remodeling in Asthma
Klaudia A. Kaczmarek,Rachel L. Clifford,Alan J. Knox
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190 Analysis of microRNA and modified oligonucleotides with the use of ultra high performance liquid chromatography coupled with mass spectrometry
Sylwia Studzinska,Boguslaw Buszewski
Journal of Chromatography A. 2018;
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191 Therapeutic applications of zebrafish (Danio rerio) miRNAs linked with human diseases: A prospective review
Manojit Bhattacharya,Soumendu Ghosh,Ramesh Chandra Malick,Bidhan Chandra Patra,Basanta Kumar Das
Gene. 2018; 679: 202
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192 An innovative paradigm of methods in microRNAs detection: highlighting DNAzymes, the illuminators
Mojdeh Mahdiannasser,Zahra Karami
Biosensors and Bioelectronics. 2018; 107: 123
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193 Biomarkers in Spinal Cord Injury: from Prognosis to Treatment
Leonardo Fonseca Rodrigues,Vivaldo Moura-Neto,Tania Cristina Leite de Sampaio e Spohr
Molecular Neurobiology. 2018;
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194 Calcium-Binding Nanoparticles for Vascular Disease
Deborah D. Chin,Sampreeti Chowdhuri,Eun Ji Chung
Regenerative Engineering and Translational Medicine. 2018;
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195 A physiologically relevant 3D collagen-based scaffold–neuroblastoma cell system exhibits chemosensitivity similar to orthotopic xenograft models
C. Curtin,J.C. Nolan,R. Conlon,L. Deneweth,C. Gallagher,Y.J. Tan,B.L. Cavanagh,A.Z. Asraf,H. Harvey,S. Miller-Delaney,J. Shohet,I. Bray,F.J. OæBrien,R.L. Stallings,O. Piskareva
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196 Emerging ways to treat breast cancer: will promises be met?
Pouria Samadi,Sahar Saki,Fatemeh Karimi Dermani,Mona Pourjafar,Massoud Saidijam
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197 The MicroRNA-326: Autoimmune diseases, diagnostic biomarker, and therapeutic target
Golamreza Jadideslam,Khalil Ansarin,Ebrahim Sakhinia,Shahriar Alipour,Farhad Pouremamali,Alireza Khabbazi
Journal of Cellular Physiology. 2018;
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198 miRNAs regulate the HIF switch during hypoxia: a novel therapeutic target
Marcin Serocki,Sylwia Bartoszewska,Anna Janaszak-Jasiecka,Renata J. Ochocka,James F. Collawn,Rafal Bartoszewski
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199 miR-30a-5p inhibition promotes interaction of Fas+ endothelial cells and FasL+ microglia to decrease pathological neovascularization and promote physiological angiogenesis
Salome Murinello,Yoshihiko Usui,Susumu Sakimoto,Maki Kitano,Edith Aguilar,H. Maura Friedlander,Amelia Schricker,Carli Wittgrove,Yoshihiro Wakabayashi,Michael I. Dorrell,Peter D. Westenskow,Martin Friedlander
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200 MicroRNAs regulate survival in oxygen-deprived environments
Simon G. English,Hanane Hadj-Moussa,Kenneth B. Storey
The Journal of Experimental Biology. 2018; 221(23): jeb190579
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201 MicroRNA expression in melanocytes and melanoma cells
A. A. Petkevich,I. Sh. Shubina,A. A. Abramov,L. T. Mamedova,I. V. Samoilenko,M. V. Kiselevsky
Russian Journal of Biotherapy. 2018; 17(3): 6
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202 Pentafluoropropionic Anhydride Functionalized PAMAM Dendrimer as miRNA Delivery Reagent
Ali Oztuna,Hasan Nazir
Journal of the Turkish Chemical Society, Section A: Chemistry. 2018; : 1295
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203 Prognostic Value of MicroRNAs in Coronary Artery Diseases: A Meta-Analysis
Ji Suk Kim,Kyoungjune Pak,Tae Sik Goh,Dae Cheon Jeong,Myoung-Eun Han,Jihyun Kim,Sae-Ock Oh,Chi Dae Kim,Yun Hak Kim
Yonsei Medical Journal. 2018; 59(4): 495
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204 The Emerging Role of microRNAs in Aquaporin Regulation
André Gomes,Inês V. da Silva,Cecília M. P. Rodrigues,Rui E. Castro,Graça Soveral
Frontiers in Chemistry. 2018; 6
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205 miRNA in a multiomic context for diagnosis, treatment monitoring and personalized management of metastatic breast cancer
Pavol Zubor,Peter Kubatka,Zuzana Dankova,Alexandra Gondova,Karol Kajo,Jozef Hatok,Marek Samec,Marianna Jagelkova,Stefan Krivus,Veronika Holubekova,Jan Bujnak,Zuzana Laucekova,Katarina Zelinova,Igor Stastny,Marcela Nachajova,Jan Danko,Olga Golubnitschaja
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206 Temporal Integrative Analysis of mRNA and microRNAs Expression Profiles and Epigenetic Alterations in Female SAMP8, a Model of Age-Related Cognitive Decline
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Frontiers in Genetics. 2018; 9
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207 miR-182 and miR-183 Promote Cell Proliferation and Invasion by Targeting FOXO1 in Mesothelioma
Rui Suzuki,Vishwa Jeet Amatya,Kei Kushitani,Yuichiro Kai,Takahiro Kambara,Yukio Takeshima
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208 Targeting Non-coding RNA in Vascular Biology and Disease
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209 Downregulated microRNAs in the colorectal cancer: diagnostic and therapeutic perspectives
Rosa Hernández,Ester Sánchez-Jiménez,Consolación Melguizo,Jose Prados,Ana Rosa Rama
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210 Unique interstitial miRNA signature drives fibrosis in a murine model of autosomal dominant polycystic kidney disease
Ameya Patil,William E Sweeney Jr,Cynthia G Pan,Ellis D Avner
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211 MicroRNAs in the prognosis and therapy of colorectal cancer: From bench to bedside
Kenneth KW To,Christy WS Tong,Mingxia Wu,William CS Cho
World Journal of Gastroenterology. 2018; 24(27): 2949
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212 MicroRNA-124-3p attenuates severe community-acquired pneumonia progression in macrophages by targeting tumor necrosis factor receptor-associated factor 6
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213 MicroRNA-766 inhibits the malignant biological behaviours of pancreatic ductal adenocarcinoma by directly targeting ETS1
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214 Establishment of an miR-137-knockout cell model using CRISPR/Cas9 genome editing
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216 Non-coding RNA Contribution to Thoracic and Abdominal Aortic Aneurysm Disease Development and Progression
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217 Role of Non-Coding RNAs in the Etiology of Bladder Cancer
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224 A Circulating microRNA Signature Predicts Age-Based Development of Lymphoma
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229 Triangle of AKT2, miRNA, and Tumorigenesis in Different Cancers
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230 A Concise Review of MicroRNA Exploring the Insights of MicroRNA Regulations in Bacterial, Viral and Metabolic Diseases
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231 MicroRNAs in injury and repair
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232 Microvesicle-mediated delivery of miR-1343: impact on markers of fibrosis
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233 MicroRNA-467g inhibits new bone regeneration by targeting Ihh/Runx-2 signaling
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234 MTDH and MAP3K1 are direct targets of apoptosis-regulating miRNAs in colorectal carcinoma
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235 Small non coding RNAs in adipocyte biology and obesity
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236 Potent Anti-seizure Effects of Locked Nucleic Acid Antagomirs Targeting miR-134 in Multiple Mouse and Rat Models of Epilepsy
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238 Inflammasome Priming in Sterile Inflammatory Disease
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240 MicroRNAs as future therapeutic targets in COPD?
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245 The Potential of MicroRNAs as Novel Biomarkers for Transplant Rejection
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246 Colorectal Cancer: From the Genetic Model to Posttranscriptional Regulation by Noncoding RNAs
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247 Systems genetics identifies a co-regulated module of liver microRNAs associated with plasma LDL cholesterol in murine diet-induced dyslipidemia
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248 New Dancing Couple: PD-L1 and MicroRNA
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249 Dysregulated miRNAs and their pathogenic implications for the neurometabolic disease propionic acidemia
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252 Epigenetics in multiple myeloma: From mechanisms to therapy
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253 MicroRNAs in the skin: role in development, homoeostasis and regeneration
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254 Inflammation-induced miRNA-155 inhibits self-renewal of neural stem cells via suppression of CCAAT/enhancer binding protein ß (C/EBPß) expression
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256 TGFß as a therapeutic target in cystic fibrosis
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257 Shields Up—Systemic Protection Provided by microRNA-21 During Sepsis?*
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258 MicroRNA-29b Overexpression Decreases Extracellular Matrix mRNA and Protein Production in Human Corneal Endothelial Cells
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260 Excerpts from the 1st international NTNU symposium on current and future clinical biomarkers of cancer: innovation and implementation, June 16th and 17th 2016, Trondheim, Norway
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261 Trying to understand the genetics of atopic dermatitis
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262 miR-15a/miR-16 induces mitochondrial dependent apoptosis in breast cancer cells by suppressing oncogene BMI1
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263 Therapeutic Resistance in Acute Myeloid Leukemia: The Role of Non-Coding RNAs
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