Evidence for natural antisense transcript-mediated inhibition of microRNA function

Faghihi, Mohammad Ali; Zhang, Ming; Huang, Jia; Modarresi, Farzaneh; Van der Brug, Marcel P.; Nalls, Michael A.; Cookson, Mark R.; St-Laurent III, Georges; Wahlestedt, Claes

doi:10.1186/gb-2010-11-5-r56

Title: Evidence for natural antisense transcript-mediated inhibition of microRNA function

Abstract

Background: MicroRNAs (miRNAs) have the potential to regulate diverse sets of mRNA targets. In addition, mammalian genomes contain numerous natural antisense transcripts, most of which appear to be non-protein-coding RNAs (ncRNAs). We have recently identified and characterized a highly conserved non-coding antisense transcript for beta-secretase-1 (BACE1), a critical enzyme in Alzheimer's disease pathophysiology. The BACE1-antisense transcript is markedly up-regulated in brain samples from Alzheimer's disease patients and promotes the stability of the (sense) BACE1 transcript. Results: We report here that BACE1-antisense prevents miRNA-induced repression of BACE1 mRNA by masking the binding site for miR-485-5p. Indeed, miR-485-5p and BACE1-antisense compete for binding within the same region in the open reading frame of the BACE1 mRNA. We observed opposing effects of BACE1-antisense and miR-485-5p on BACE1 protein in vitro and showed that Locked Nucleic Acid-antimiR mediated knockdown of miR-485-5p as well as BACE1-antisense over-expression can prevent the miRNA-induced BACE1 suppression. We found that the expression of BACE1-antisense as well as miR-485-5p are dysregulated in RNA samples from Alzheimer's disease subjects compared to control individuals. Conclusions: Our data demonstrate an interface between two distinct groups of regulatory RNAs in the computation of BACE1 gene expression. Moreover, bioinformatics analyses revealed a theoretical basis formore »« less

Authors:

Faghihi, Mohammad Ali ^[1]; Zhang, Ming ^[2]; Huang, Jia ^[3]; Modarresi, Farzaneh ^[1]; Van der Brug, Marcel P. ^[1]; Nalls, Michael A. ^[4]; Cookson, Mark R. ^[4]; St-Laurent III, Georges ^[5]; Wahlestedt, Claes ^[6]

Scripps Research Inst., Jupiter, FL (United States). Dept. of Neuroscience
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Miller School of Medicine, Miami, FL (United States). Miami Inst. for Human Genomics
National Institutes of Health (NIH), Bethesda, MD (United States). National Inst. on Aging, Intramural Research Program, Lab. of Neurogenetics
Brown Univ., Providence, RI (United States). Dept. of Biology
Scripps Research Inst., Jupiter, FL (United States). Dept. of Neuroscience and Dept. of Molecular Therapeutics

Publication Date:: Thu May 27 00:00:00 EDT 2010

Research Org.:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institute of Neurological Disorders and Stroke (NINDS); National Institute on Aging (NIA)

OSTI Identifier:: 1629353

Resource Type:: Accepted Manuscript

Journal Name:: Genome Biology (Online)

Additional Journal Information:: Journal Name: Genome Biology (Online); Journal Volume: 11; Journal Issue: 5; Journal ID: ISSN 1474-760X

Publisher:: BioMed Central

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Entorhinal Cortex; Superior Frontal Gyrus; miRNA Binding Site; Natural Antisense Transcript; BACE1 Protein

Citation Formats


                    Faghihi, Mohammad Ali, Zhang, Ming, Huang, Jia, Modarresi, Farzaneh, Van der Brug, Marcel P., Nalls, Michael A., Cookson, Mark R., St-Laurent III, Georges, and Wahlestedt, Claes. Evidence for natural antisense transcript-mediated inhibition of microRNA function.  United States: N. p., 2010. 
Web.  doi:10.1186/gb-2010-11-5-r56.

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                    Faghihi, Mohammad Ali, Zhang, Ming, Huang, Jia, Modarresi, Farzaneh, Van der Brug, Marcel P., Nalls, Michael A., Cookson, Mark R., St-Laurent III, Georges, & Wahlestedt, Claes. Evidence for natural antisense transcript-mediated inhibition of microRNA function.  United States.  https://doi.org/10.1186/gb-2010-11-5-r56

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                    Faghihi, Mohammad Ali, Zhang, Ming, Huang, Jia, Modarresi, Farzaneh, Van der Brug, Marcel P., Nalls, Michael A., Cookson, Mark R., St-Laurent III, Georges, and Wahlestedt, Claes. Thu .  
"Evidence for natural antisense transcript-mediated inhibition of microRNA function".  United States.  https://doi.org/10.1186/gb-2010-11-5-r56.  https://www.osti.gov/servlets/purl/1629353.

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@article{osti_1629353,

  title        = {Evidence for natural antisense transcript-mediated inhibition of microRNA function},

  author       = {Faghihi, Mohammad Ali and Zhang, Ming and Huang, Jia and Modarresi, Farzaneh and Van der Brug, Marcel P. and Nalls, Michael A. and Cookson, Mark R. and St-Laurent III, Georges and Wahlestedt, Claes},

  abstractNote = {Background: MicroRNAs (miRNAs) have the potential to regulate diverse sets of mRNA targets. In addition, mammalian genomes contain numerous natural antisense transcripts, most of which appear to be non-protein-coding RNAs (ncRNAs). We have recently identified and characterized a highly conserved non-coding antisense transcript for beta-secretase-1 (BACE1), a critical enzyme in Alzheimer's disease pathophysiology. The BACE1-antisense transcript is markedly up-regulated in brain samples from Alzheimer's disease patients and promotes the stability of the (sense) BACE1 transcript. Results: We report here that BACE1-antisense prevents miRNA-induced repression of BACE1 mRNA by masking the binding site for miR-485-5p. Indeed, miR-485-5p and BACE1-antisense compete for binding within the same region in the open reading frame of the BACE1 mRNA. We observed opposing effects of BACE1-antisense and miR-485-5p on BACE1 protein in vitro and showed that Locked Nucleic Acid-antimiR mediated knockdown of miR-485-5p as well as BACE1-antisense over-expression can prevent the miRNA-induced BACE1 suppression. We found that the expression of BACE1-antisense as well as miR-485-5p are dysregulated in RNA samples from Alzheimer's disease subjects compared to control individuals. Conclusions: Our data demonstrate an interface between two distinct groups of regulatory RNAs in the computation of BACE1 gene expression. Moreover, bioinformatics analyses revealed a theoretical basis for many other potential interactions between natural antisense transcripts and miRNAs at the binding sites of the latter.},

  doi          = {10.1186/gb-2010-11-5-r56},

  journal      = {Genome Biology (Online)},

  number       = 5,

  volume       = 11,

  place        = {United States},

  year         = {Thu May 27 00:00:00 EDT 2010},

  month        = {Thu May 27 00:00:00 EDT 2010}

}

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Title: Evidence for natural antisense transcript-mediated inhibition of microRNA function

Abstract

Citation Formats

MicroRNAs: Target Recognition and Regulatory Functions journal, January 2009

Partial Reduction of BACE1 Has Dramatic Effects on Alzheimer Plaque and Synaptic Pathology in APP Transgenic Mice journal, September 2007

Regulating Gene Expression through RNA Nuclear Retention journal, October 2005

Natural antisense and noncoding RNA transcripts as potential drug targets journal, June 2006

A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence journal, September 2008

A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance journal, August 2007

Prediction of Plant MicroRNA Targets journal, August 2002

A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep journal, June 2006

The complexity of the mammalian transcriptome: The complexity of the mammalian transcriptome journal, August 2006

A SNP in a let-7 microRNA Complementary Site in the KRAS 3′ Untranslated Region Increases Non–Small Cell Lung Cancer Risk journal, October 2008

Increased expression of the amyloid precursor ?-secretase in Alzheimer's disease journal, May 2002

A Greedy Algorithm for Aligning DNA Sequences journal, February 2000

Noncoding RNAs: couplers of analog and digital information in nervous system function? journal, December 2007

Oxidative stress potentiates BACE1 gene expression and A? generation journal, December 2004

Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays journal, June 2005

aHIF but not HIF-1α transcript is a poor prognostic marker in human breast cancer journal, September 2003

Human MicroRNA Targets journal, October 2004

Transcriptional and translational regulation of BACE1 expression—Implications for Alzheimer's disease journal, June 2006

Molecular Rationale for the Pharmacological Treatment of Alzheimer??s Disease journal, January 2005

Natural antisense transcripts of hypoxia-inducible factor 1alpha are detected in different normal and tumour human tissues journal, October 2002

β-Secretase Protein and Activity Are Increased in the Neocortex in Alzheimer Disease journal, September 2002

Increased ?-Secretase activity in cerebrospinal fluid of Alzheimer's disease subjects journal, January 2004

Prolonged Hypoxia Differentially Regulates Hypoxia-inducible Factor (HIF)-1α and HIF-2α Expression in Lung Epithelial Cells journal, April 2004

microRNAs: A Safeguard against Turmoil? journal, August 2007

Relief of microRNA-Mediated Translational Repression in Human Cells Subjected to Stress journal, June 2006

Function and Localization of MicroRNAs in Mammalian Cells journal, January 2006

The increased activity of BACE1 correlates with oxidative stress in Alzheimer's disease journal, July 2007

Natural antisense transcripts of HIF-1α are conserved in rodents journal, September 2004

Complex Loci in Human and Mouse Genomes journal, January 2006

MiRSNPs or MiR-polymorphisms, new players in microRNA mediated regulation of the cell: Introducing microRNA pharmacogenomics journal, April 2008

Control of APP processing and Aβ generation level by BACE1 enzymatic activity and transcription journal, December 2005

Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of β-secretase journal, June 2008

miR-148 targets human DNMT3b protein coding region journal, March 2008

Recent Developments of Structure Based β-Secretase Inhibitors for Alzheimers Disease journal, December 2005

Control of Peripheral Nerve Myelination by the -Secretase BACE1 journal, October 2006

The various aggregation states of β-amyloid 1–42 mediate different effects on oxidative stress, neurodegeneration, and BACE-1 expression journal, July 2006

Non-coding RNAs in the nervous system: Non-coding RNA in the nervous system journal, August 2006

Non-coding RNA journal, April 2006

miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments journal, May 2009

miRBase: tools for microRNA genomics journal, December 2007

Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR journal, May 2007

Bace1 modulates myelination in the central and peripheral nervous system journal, November 2006

Amyloid peptide load is correlated with increased -secretase activity in sporadic Alzheimer's disease patients journal, February 2004

100 Years and Counting: Prospects for Defeating Alzheimer's Disease journal, November 2006

RNA interference is not involved in natural antisense mediated regulation of gene expression in mammals journal, January 2006

Sequence Variants in SLITRK1 Are Associated with Tourette's Syndrome journal, October 2005

A Family of MicroRNAs Present in Plants and Animals journal, December 2006

Aquabacterium terrae sp. nov., isolated from soil journal, April 2021

Human MicroRNA targets. text, January 2004

miRBase: tools for microRNA genomics. text, January 2008

Increased expression of the amyloid precursor ?-secretase in Alzheimer's disease journal, May 2002

Regulating Gene Expression through RNA Nuclear Retention journal, October 2005

Relief of microRNA-Mediated Translational Repression in Human Cells Subjected to Stress journal, June 2006

microRNAs: A Safeguard against Turmoil? journal, August 2007

Natural antisense and noncoding RNA transcripts as potential drug targets journal, June 2006

Natural antisense transcripts of HIF-1α are conserved in rodents journal, September 2004

β-Secretase (BACE) as a drug target for alzheimer’s disease journal, December 2002

Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of β-secretase journal, June 2008

Bace1 modulates myelination in the central and peripheral nervous system journal, November 2006

Amyloid peptide load is correlated with increased -secretase activity in sporadic Alzheimer's disease patients journal, February 2004

Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR journal, May 2007

A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance journal, August 2007

A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence journal, September 2008

miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments journal, May 2009

Control of APP processing and Aβ generation level by BACE1 enzymatic activity and transcription journal, December 2005

Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays journal, June 2005

Function and Localization of MicroRNAs in Mammalian Cells journal, January 2006

The complexity of the mammalian transcriptome: The complexity of the mammalian transcriptome journal, August 2006

aHIF but not HIF-1α transcript is a poor prognostic marker in human breast cancer journal, September 2003

miR-148 targets human DNMT3b protein coding region journal, March 2008

Complex Loci in Human and Mouse Genomes journal, January 2006

Temporal Relations Among Amyloid β-Peptide-Induced Free-Radical Oxidative Stress, Neuronal Toxicity, and Neuronal Defensive Responses journal, January 1998

The β-Secretase, BACE: A Prime Drug Target for Alzheimer's Disease journal, January 2001

Mechanisms of ß-Amyloid Neurotoxicity: Perspectives of Pharmacotherapy journal, January 2000

BACE1, a Major Determinant of Selective Vulnerability of the Brain to Amyloid- Amyloidogenesis, is Essential for Cognitive, Emotional, and Synaptic Functions journal, December 2005

miRBase: tools for microRNA genomics. text, January 2008

Molecular Rationale for the Pharmacological Treatment of Alzheimer??s Disease journal, January 2005

MicroRNAs: Target Recognition and Regulatory Functions
journal, January 2009

Partial Reduction of BACE1 Has Dramatic Effects on Alzheimer Plaque and Synaptic Pathology in APP Transgenic Mice
journal, September 2007

Regulating Gene Expression through RNA Nuclear Retention
journal, October 2005

Natural antisense and noncoding RNA transcripts as potential drug targets
journal, June 2006

A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence
journal, September 2008

A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance
journal, August 2007

Prediction of Plant MicroRNA Targets
journal, August 2002

A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep
journal, June 2006

The complexity of the mammalian transcriptome: The complexity of the mammalian transcriptome
journal, August 2006

A SNP in a let-7 microRNA Complementary Site in the KRAS 3′ Untranslated Region Increases Non–Small Cell Lung Cancer Risk
journal, October 2008

Increased expression of the amyloid precursor ?-secretase in Alzheimer's disease
journal, May 2002

A Greedy Algorithm for Aligning DNA Sequences
journal, February 2000

Noncoding RNAs: couplers of analog and digital information in nervous system function?
journal, December 2007

Oxidative stress potentiates BACE1 gene expression and A? generation
journal, December 2004

Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays
journal, June 2005

aHIF but not HIF-1α transcript is a poor prognostic marker in human breast cancer
journal, September 2003

Human MicroRNA Targets
journal, October 2004

Transcriptional and translational regulation of BACE1 expression—Implications for Alzheimer's disease
journal, June 2006

Molecular Rationale for the Pharmacological Treatment of Alzheimer??s Disease
journal, January 2005

Natural antisense transcripts of hypoxia-inducible factor 1alpha are detected in different normal and tumour human tissues
journal, October 2002

β-Secretase Protein and Activity Are Increased in the Neocortex in Alzheimer Disease
journal, September 2002

Increased ?-Secretase activity in cerebrospinal fluid of Alzheimer's disease subjects
journal, January 2004

Prolonged Hypoxia Differentially Regulates Hypoxia-inducible Factor (HIF)-1α and HIF-2α Expression in Lung Epithelial Cells
journal, April 2004

microRNAs: A Safeguard against Turmoil?
journal, August 2007

Relief of microRNA-Mediated Translational Repression in Human Cells Subjected to Stress
journal, June 2006

Function and Localization of MicroRNAs in Mammalian Cells
journal, January 2006

The increased activity of BACE1 correlates with oxidative stress in Alzheimer's disease
journal, July 2007

Natural antisense transcripts of HIF-1α are conserved in rodents
journal, September 2004

Complex Loci in Human and Mouse Genomes
journal, January 2006

MiRSNPs or MiR-polymorphisms, new players in microRNA mediated regulation of the cell: Introducing microRNA pharmacogenomics
journal, April 2008

Control of APP processing and Aβ generation level by BACE1 enzymatic activity and transcription
journal, December 2005

Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of β-secretase
journal, June 2008

miR-148 targets human DNMT3b protein coding region
journal, March 2008

Recent Developments of Structure Based β-Secretase Inhibitors for Alzheimers Disease
journal, December 2005

Control of Peripheral Nerve Myelination by the -Secretase BACE1
journal, October 2006

The various aggregation states of β-amyloid 1–42 mediate different effects on oxidative stress, neurodegeneration, and BACE-1 expression
journal, July 2006

Non-coding RNAs in the nervous system: Non-coding RNA in the nervous system
journal, August 2006

Non-coding RNA
journal, April 2006

miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments
journal, May 2009

miRBase: tools for microRNA genomics
journal, December 2007

Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR
journal, May 2007

Bace1 modulates myelination in the central and peripheral nervous system
journal, November 2006

Amyloid peptide load is correlated with increased -secretase activity in sporadic Alzheimer's disease patients
journal, February 2004

100 Years and Counting: Prospects for Defeating Alzheimer's Disease
journal, November 2006

RNA interference is not involved in natural antisense mediated regulation of gene expression in mammals
journal, January 2006

Sequence Variants in SLITRK1 Are Associated with Tourette's Syndrome
journal, October 2005

A Family of MicroRNAs Present in Plants and Animals
journal, December 2006

Aquabacterium terrae sp. nov., isolated from soil
journal, April 2021

Human MicroRNA targets.
text, January 2004

miRBase: tools for microRNA genomics.
text, January 2008

Increased expression of the amyloid precursor ?-secretase in Alzheimer's disease
journal, May 2002

Regulating Gene Expression through RNA Nuclear Retention
journal, October 2005

Relief of microRNA-Mediated Translational Repression in Human Cells Subjected to Stress
journal, June 2006

microRNAs: A Safeguard against Turmoil?
journal, August 2007

Natural antisense and noncoding RNA transcripts as potential drug targets
journal, June 2006

Natural antisense transcripts of HIF-1α are conserved in rodents
journal, September 2004

β-Secretase (BACE) as a drug target for alzheimer’s disease
journal, December 2002

Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of β-secretase
journal, June 2008

Bace1 modulates myelination in the central and peripheral nervous system
journal, November 2006

Amyloid peptide load is correlated with increased -secretase activity in sporadic Alzheimer's disease patients
journal, February 2004

Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR
journal, May 2007

A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance
journal, August 2007

A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence
journal, September 2008

miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments
journal, May 2009

Control of APP processing and Aβ generation level by BACE1 enzymatic activity and transcription
journal, December 2005

Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays
journal, June 2005

Function and Localization of MicroRNAs in Mammalian Cells
journal, January 2006

The complexity of the mammalian transcriptome: The complexity of the mammalian transcriptome
journal, August 2006

aHIF but not HIF-1α transcript is a poor prognostic marker in human breast cancer
journal, September 2003

miR-148 targets human DNMT3b protein coding region
journal, March 2008

Complex Loci in Human and Mouse Genomes
journal, January 2006

Temporal Relations Among Amyloid β-Peptide-Induced Free-Radical Oxidative Stress, Neuronal Toxicity, and Neuronal Defensive Responses
journal, January 1998

The β-Secretase, BACE: A Prime Drug Target for Alzheimer's Disease
journal, January 2001

Mechanisms of ß-Amyloid Neurotoxicity: Perspectives of Pharmacotherapy
journal, January 2000

BACE1, a Major Determinant of Selective Vulnerability of the Brain to Amyloid- Amyloidogenesis, is Essential for Cognitive, Emotional, and Synaptic Functions
journal, December 2005

miRBase: tools for microRNA genomics.
text, January 2008

Molecular Rationale for the Pharmacological Treatment of Alzheimer??s Disease
journal, January 2005

MiRSNPs or MiR-polymorphisms, new players in microRNA mediated regulation of the cell: Introducing microRNA pharmacogenomics
journal, April 2008

Integrative analysis of genome-wide lncRNA and mRNA expression in newly synthesized Brassica hexaploids
journal, May 2018

Long non‐coding RNA PlncRNA‐1 promotes cell proliferation and hepatic metastasis in colorectal cancer
journal, May 2018