Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk
Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with susceptibility to atherosclerotic vascular disease (ASVD). Although this locus encodes three well-characterized tumor suppressors, p16(INK4a), p15(INK...
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| Published in | PLoS genetics Vol. 6; no. 12; p. e1001233 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.12.2010
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with susceptibility to atherosclerotic vascular disease (ASVD). Although this locus encodes three well-characterized tumor suppressors, p16(INK4a), p15(INK4b), and ARF, the SNPs most strongly associated with ASVD are ∼120 kb from the nearest coding gene within a long non-coding RNA (ncRNA) known as ANRIL (CDKN2BAS). While individuals homozygous for the atherosclerotic risk allele show decreased expression of ANRIL and the coding INK4/ARF transcripts, the mechanism by which such distant genetic variants influence INK4/ARF expression is unknown. Here, using rapid amplification of cDNA ends (RACE) and analysis of next-generation RNA sequencing datasets, we determined the structure and abundance of multiple ANRIL species. Each of these species was present at very low copy numbers in primary and cultured cells; however, only the expression of ANRIL isoforms containing exons proximal to the INK4/ARF locus correlated with the ASVD risk alleles. Surprisingly, RACE also identified transcripts containing non-colinear ANRIL exonic sequences, whose expression also correlated with genotype and INK4/ARF expression. These non-polyadenylated RNAs resisted RNAse R digestion and could be PCR amplified using outward-facing primers, suggesting they represent circular RNA structures that could arise from by-products of mRNA splicing. Next-generation DNA sequencing and splice prediction algorithms identified polymorphisms within the ASVD risk interval that may regulate ANRIL splicing and circular ANRIL (cANRIL) production. These results identify novel circular RNA products emanating from the ANRIL locus and suggest causal variants at 9p21.3 regulate INK4/ARF expression and ASVD risk by modulating ANRIL expression and/or structure. |
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| AbstractList | Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the
INK4/ARF (CDKN2a/b)
locus with susceptibility to atherosclerotic vascular disease (ASVD). Although this locus encodes three well-characterized tumor suppressors,
p16
INK4a
,
p15
INK4b
, and
ARF
, the SNPs most strongly associated with ASVD are ∼120 kb from the nearest coding gene within a long non-coding RNA (ncRNA) known as
ANRIL
(
CDKN2BAS
). While individuals homozygous for the atherosclerotic risk allele show decreased expression of
ANRIL
and the coding
INK4/ARF
transcripts, the mechanism by which such distant genetic variants influence
INK4/ARF
expression is unknown. Here, using rapid amplification of cDNA ends (RACE) and analysis of next-generation RNA sequencing datasets, we determined the structure and abundance of multiple
ANRIL
species. Each of these species was present at very low copy numbers in primary and cultured cells; however, only the expression of
ANRIL
isoforms containing exons proximal to the
INK4/ARF
locus correlated with the ASVD risk alleles. Surprisingly, RACE also identified transcripts containing non-colinear
ANRIL
exonic sequences, whose expression also correlated with genotype and
INK4/ARF
expression. These non-polyadenylated RNAs resisted RNAse R digestion and could be PCR amplified using outward-facing primers, suggesting they represent circular RNA structures that could arise from by-products of mRNA splicing. Next-generation DNA sequencing and splice prediction algorithms identified polymorphisms within the ASVD risk interval that may regulate
ANRIL
splicing and circular
ANRIL
(
cANRIL
) production. These results identify novel circular RNA products emanating from the
ANRIL
locus and suggest causal variants at 9p21.3 regulate
INK4/ARF
expression and ASVD risk by modulating
ANRIL
expression and/or structure.
Unbiased studies of the human genome have identified strong genetic determinants of atherosclerotic vascular disease (ASVD) on chromosome 9p21.3. This region of the genome does not encode genes previously linked to ASVD, but does contain the
INK4/ARF
tumor suppressor locus. Products of the
INK4/ARF
locus regulate cell division, a process thought to be important in ASVD pathology. We and others have suggested that genetic variants in 9p21.3 influence
INK4/ARF
gene expression; however, the mechanisms by which these distant polymorphisms (>100,000 bp away) influence transcription of the locus is unknown. The ASVD–associated genetic variants lie within the predicted structure of a non-coding RNA (ncRNA) called
ANRIL
. Based upon recent work suggesting that other ncRNAs can repress nearby coding genes, we considered the possibility that
ANRIL
structure may regulate
INK4/ARF
gene expression. Coupling molecular analysis with state-of-the-art sequencing technologies in a wide variety of cell types from normal human donors and cancer cells, we found that
ANRIL
encodes a heterogeneous species of rare RNA transcripts. Moreover, we identified novel, circular
ANRIL
isoforms (
cANRIL
) whose expression correlated with
INK4/ARF
transcription and ASVD risk. These studies suggest a new model wherein
ANRIL
structure influences
INK4/ARF
expression and susceptibility to atherosclerosis. Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with susceptibility to atherosclerotic vascular disease (ASVD). Although this locus encodes three well-characterized tumor suppressors, p16INK4a, p15INK4b, and ARF, the SNPs most strongly associated with ASVD are similar to 120 kb from the nearest coding gene within a long non-coding RNA (ncRNA) known as ANRIL (CDKN2BAS). While individuals homozygous for the atherosclerotic risk allele show decreased expression of ANRIL and the coding INK4/ARF transcripts, the mechanism by which such distant genetic variants influence INK4/ARF expression is unknown. Here, using rapid amplification of cDNA ends (RACE) and analysis of next-generation RNA sequencing datasets, we determined the structure and abundance of multiple ANRIL species. Each of these species was present at very low copy numbers in primary and cultured cells; however, only the expression of ANRIL isoforms containing exons proximal to the INK4/ARF locus correlated with the ASVD risk alleles. Surprisingly, RACE also identified transcripts containing non-colinear ANRIL exonic sequences, whose expression also correlated with genotype and INK4/ARF expression. These non-polyadenylated RNAs resisted RNAse R digestion and could be PCR amplified using outward-facing primers, suggesting they represent circular RNA structures that could arise from by-products of mRNA splicing. Next-generation DNA sequencing and splice prediction algorithms identified polymorphisms within the ASVD risk interval that may regulate ANRIL splicing and circular ANRIL (cANRIL) production. These results identify novel circular RNA products emanating from the ANRIL locus and suggest causal variants at 9p21.3 regulate INK4/ARF expression and ASVD risk by modulating ANRIL expression and/or structure. Unbiased studies of the human genome have identified strong genetic determinants of atherosclerotic vascular disease (ASVD) on chromosome 9p21.3. This region of the genome does not encode genes previously linked to ASVD, but does contain the INK4/ARF tumor suppressor locus. Products of the INK4/ARF locus regulate cell division, a process thought to be important in ASVD pathology. We and others have suggested that genetic variants in 9p21.3 influence INK4/ARF gene expression; however, the mechanisms by which these distant polymorphisms (>100,000 bp away) influence transcription of the locus is unknown. The ASVD-associated genetic variants lie within the predicted structure of a non-coding RNA (ncRNA) called ANRIL. Based upon recent work suggesting that other ncRNAs can repress nearby coding genes, we considered the possibility that ANRIL structure may regulate INK4/ARF gene expression. Coupling molecular analysis with state-of-the-art sequencing technologies in a wide variety of cell types from normal human donors and cancer cells, we found that ANRIL encodes a heterogeneous species of rare RNA transcripts. Moreover, we identified novel, circular ANRIL isoforms (cANRIL) whose expression correlated with INK4/ARF transcription and ASVD risk. These studies suggest a new model wherein ANRIL structure influences INK4/ARF expression and susceptibility to atherosclerosis. Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with susceptibility to atherosclerotic vascular disease (ASVD). Although this locus encodes three well-characterized tumor suppressors, p16(INK4a), p15(INK4b), and ARF, the SNPs most strongly associated with ASVD are ∼120 kb from the nearest coding gene within a long non-coding RNA (ncRNA) known as ANRIL (CDKN2BAS). While individuals homozygous for the atherosclerotic risk allele show decreased expression of ANRIL and the coding INK4/ARF transcripts, the mechanism by which such distant genetic variants influence INK4/ARF expression is unknown. Here, using rapid amplification of cDNA ends (RACE) and analysis of next-generation RNA sequencing datasets, we determined the structure and abundance of multiple ANRIL species. Each of these species was present at very low copy numbers in primary and cultured cells; however, only the expression of ANRIL isoforms containing exons proximal to the INK4/ARF locus correlated with the ASVD risk alleles. Surprisingly, RACE also identified transcripts containing non-colinear ANRIL exonic sequences, whose expression also correlated with genotype and INK4/ARF expression. These non-polyadenylated RNAs resisted RNAse R digestion and could be PCR amplified using outward-facing primers, suggesting they represent circular RNA structures that could arise from by-products of mRNA splicing. Next-generation DNA sequencing and splice prediction algorithms identified polymorphisms within the ASVD risk interval that may regulate ANRIL splicing and circular ANRIL (cANRIL) production. These results identify novel circular RNA products emanating from the ANRIL locus and suggest causal variants at 9p21.3 regulate INK4/ARF expression and ASVD risk by modulating ANRIL expression and/or structure. Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with susceptibility to atherosclerotic vascular disease (ASVD). Although this locus encodes three well-characterized tumor suppressors, p16INK4a, p15INK4b, and ARF, the SNPs most strongly associated with ASVD are ~120 kb from the nearest coding gene within a long non-coding RNA (ncRNA) known as ANRIL (CDKN2BAS). While individuals homozygous for the atherosclerotic risk allele show decreased expression of ANRIL and the coding INK4/ARF transcripts, the mechanism by which such distant genetic variants influence INK4/ARF expression is unknown. Here, using rapid amplification of cDNA ends (RACE) and analysis of next-generation RNA sequencing datasets, we determined the structure and abundance of multiple ANRIL species. Each of these species was present at very low copy numbers in primary and cultured cells; however, only the expression of ANRIL isoforms containing exons proximal to the INK4/ARF locus correlated with the ASVD risk alleles. Surprisingly, RACE also identified transcripts containing non-colinear ANRIL exonic sequences, whose expression also correlated with genotype and INK4/ARF expression. These non-polyadenylated RNAs resisted RNAse R digestion and could be PCR amplified using outward-facing primers, suggesting they represent circular RNA structures that could arise from by-products of mRNA splicing. Next-generation DNA sequencing and splice prediction algorithms identified polymorphisms within the ASVD risk interval that may regulate ANRIL splicing and circular ANRIL (cANRIL) production. These results identify novel circular RNA products emanating from the ANRIL locus and suggest causal variants at 9p21.3 regulate INK4/ARF expression and ASVD risk by modulating ANRIL expression and/or structure. Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with susceptibility to atherosclerotic vascular disease (ASVD). Although this locus encodes three well-characterized tumor suppressors, [p16.sup.INK4a], [p15.sup.INK4b], and ARF, the SNPs most strongly associated with ASVD are ~120 kb from the nearest coding gene within a long non-coding RNA (ncRNA) known as ANRIL (CDKN2BAS). While individuals homozygous for the atherosclerotic risk allele show decreased expression of ANRIL and the coding INK4/ARF transcripts, the mechanism by which such distant genetic variants influence INK4/ARF expression is unknown. Here, using rapid amplification of cDNA ends (RACE) and analysis of next-generation RNA sequencing datasets, we determined the structure and abundance of multiple ANRIL species. Each of these species was present at very low copy numbers in primary and cultured cells; however, only the expression of ANRIL isoforms containing exons proximal to the INK4/ARF locus correlated with the ASVD risk alleles. Surprisingly, RACE also identified transcripts containing non- colinear ANRIL exonic sequences, whose expression also correlated with genotype and INK4/ARF expression. These non- polyadenylated RNAs resisted RNAse R digestion and could be PCR amplified using outward-facing primers, suggesting they represent circular RNA structures that could arise from by-products of mRNA splicing. Next-generation DNA sequencing and splice prediction algorithms identified polymorphisms within the ASVD risk interval that may regulate ANRIL splicing and circular ANRIL (cANRIL) production. These results identify novel circular RNA products emanating from the ANRIL locus and suggest causal variants at 9p21.3 regulate INK4/ARF expression and ASVD risk by modulating ANRIL expression and/or structure. |
| Audience | Academic |
| Author | Liu, Yan Jeck, William R Sanoff, Hanna K Sharpless, Norman E Wang, Zefeng Burd, Christin E |
| AuthorAffiliation | 5 Department of Medicine, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America 1 The Curriculum in Toxicology, The Lineberger Comprehensive Cancer Center, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America 2 Department of Genetics, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America Stanford, United States of America 3 The Division of Hematology and Oncology, University of Virginia, Charlottesville, Virginia, United States of America 4 Department of Pharmacology, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America |
| AuthorAffiliation_xml | – name: 1 The Curriculum in Toxicology, The Lineberger Comprehensive Cancer Center, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America – name: 3 The Division of Hematology and Oncology, University of Virginia, Charlottesville, Virginia, United States of America – name: 2 Department of Genetics, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America – name: 4 Department of Pharmacology, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America – name: 5 Department of Medicine, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America – name: Stanford, United States of America |
| Author_xml | – sequence: 1 givenname: Christin E surname: Burd fullname: Burd, Christin E organization: The Curriculum in Toxicology, The Lineberger Comprehensive Cancer Center, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America – sequence: 2 givenname: William R surname: Jeck fullname: Jeck, William R – sequence: 3 givenname: Yan surname: Liu fullname: Liu, Yan – sequence: 4 givenname: Hanna K surname: Sanoff fullname: Sanoff, Hanna K – sequence: 5 givenname: Zefeng surname: Wang fullname: Wang, Zefeng – sequence: 6 givenname: Norman E surname: Sharpless fullname: Sharpless, Norman E |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21151960$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2010 Public Library of Science Burd et al. 2010 2010 Burd et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Burd CE, Jeck WR, Liu Y, Sanoff HK, Wang Z, et al. (2010) Expression of Linear and Novel Circular Forms of an INK4/ARF-Associated Non-Coding RNA Correlates with Atherosclerosis Risk. PLoS Genet 6(12): e1001233. doi:10.1371/journal.pgen.1001233 |
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| Snippet | Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with... Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with... Human genome-wide association studies have linked single nucleotide polymorphisms (SNPs) on chromosome 9p21.3 near the INK4/ARF (CDKN2a/b) locus with... |
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| SubjectTerms | Atherosclerosis Atherosclerosis - epidemiology Atherosclerosis - genetics Atherosclerosis - metabolism Cardiovascular disease Cardiovascular Disorders/Peripheral Vascular Disease Cell Biology/Gene Expression Cell division Cell Line, Tumor Cyclin-Dependent Kinase Inhibitor p15 - genetics Cyclin-Dependent Kinase Inhibitor p15 - metabolism Cyclin-Dependent Kinase Inhibitor p16 - genetics Cyclin-Dependent Kinase Inhibitor p16 - metabolism DNA, Circular - chemistry DNA, Circular - genetics DNA, Circular - metabolism Exons Gene Expression Genetic aspects Genetics Genetics and Genomics/Cancer Genetics Genome-Wide Association Study Genomes Humans Influence Molecular Biology/RNA Splicing Mortality Nucleic Acid Conformation Physiological aspects Risk Factors RNA RNA Splicing RNA, Untranslated - chemistry RNA, Untranslated - genetics RNA, Untranslated - metabolism Single nucleotide polymorphisms Tumor suppressor genes |
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| Title | Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk |
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