Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk

PLoS Genetics

Volumn 6, Issue 12, 2010, Pages 1-15

  Burd, Christin E ^a   Jeck, William R ^a   Liu, Yan ^a   Sanoff, Hanna K ^b   Wang, Zefeng ^a   Sharpless, Norman E ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE NON CODING RNA IN THE INK4 LOCUS PROTEIN; ARF PROTEIN; COMPLEMENTARY DNA; CYCLIN DEPENDENT KINASE INHIBITOR 2B; ISOPROTEIN; MESSENGER RNA; RIBONUCLEASE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UNTRANSLATED RNA; CIRCULAR DNA; CYCLIN DEPENDENT KINASE INHIBITOR 2A;

ARTICLE; ATHEROSCLEROSIS; CELL CULTURE; CONTROLLED STUDY; DNA SEQUENCE; EXON; GENE AMPLIFICATION; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; HUMAN; HUMAN CELL; POLYMERASE CHAIN REACTION; PROTEIN STRUCTURE; RISK ASSESSMENT; RNA SEQUENCE; RNA SPLICING; RNA STRUCTURE; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; CHEMISTRY; CONFORMATION; GENE EXPRESSION; GENETICS; METABOLISM; RISK FACTOR; TUMOR CELL LINE;

ATHEROSCLEROSIS; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P15; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA, CIRCULAR; EXONS; GENE EXPRESSION; GENOME-WIDE ASSOCIATION STUDY; HUMANS; NUCLEIC ACID CONFORMATION; RISK FACTORS; RNA SPLICING; RNA, UNTRANSLATED;

EID: 78650696753     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001233     Document Type: Article

References (81)

1. World Health Organization W (2009) Cardiovascular diseases Fact Sheet.
2. Biros E, Cooper M, Palmer LJ, Walker PJ, Norman PE, et al. (2010) Association of an allele on chromosome 9 and abdominal aortic aneurysm. Atherosclerosis.
3. Bown MJ, Braund PS, Thompson J, London NJ, Samani NJ, et al. (2008) Association between the coronary artery disease risk locus on chromosome 9p21.3 and abdominal aortic aneurysm. Circ Cardiovasc Genet 1: 39-42.
4. Thompson AR, Golledge J, Cooper JA, Hafez H, Norman PE, et al. (2009) Sequence variant on 9p21 is associated with the presence of abdominal aortic aneurysm disease but does not have an impact on aneurysmal expansion. Eur J Hum Genet 17: 391-394.
5. Helgadottir A, Thorleifsson G, Manolescu A, Gretarsdottir S, Blondal T, et al. (2007) A common variant on chromosome 9p21 affects the risk of myocardial infarction. Science 316: 1491-1493.
6. Helgadottir A, Thorleifsson G, Magnusson KP, Gretarsdottir S, Steinthorsdottir V, et al. (2008) The same sequence variant on 9p21 associates with myocardial infarction, abdominal aortic aneurysm and intracranial aneurysm. Nat Genet 40: 217-224.
7. McPherson R, Pertsemlidis A, Kavaslar N, Stewart A, Roberts R, et al. (2007) A common allele on chromosome 9 associated with coronary heart disease. Science 316: 1488-1491.
8. Matarin M, Brown WM, Singleton A, Hardy JA, Meschia JF (2008) Whole genome analyses suggest ischemic stroke and heart disease share an association with polymorphisms on chromosome 9p21. Stroke 39: 1586-1589.
9. Gschwendtner A, Bevan S, Cole JW, Plourde A, Matarin M, et al. (2009) Sequence variants on chromosome 9p21.3 confer risk for atherosclerotic stroke. Ann Neurol 65: 531-539.
10. Smith JG, Melander O, Lovkvist H, Hedblad B, Engstrom G, et al. (2009) Common genetic variants on chromosome 9p21 confers risk of ischemic stroke: a large-scale genetic association study. Circ Cardiovasc Genet 2: 159-164.
11. Cluett C, McDermott MM, Guralnik J, Ferrucci L, Bandinelli S, et al. (2009) The 9p21 myocardial infarction risk allele increases risk of peripheral artery disease in older people. Circ Cardiovasc Genet 2: 347-353.
12. Ye S, Willeit J, Kronenberg F, Xu Q, Kiechl S (2008) Association of genetic variation on chromosome 9p21 with susceptibility and progression of atherosclerosis: a population-based, prospective study. J Am Coll Cardiol 52: 378-384.
13. Broadbent HM, Peden JF, Lorkowski S, Goel A, Ongen H, et al. (2008) Susceptibility to coronary artery disease and diabetes is encoded by distinct, tightly linked SNPs in the ANRIL locus on chromosome 9p. Hum Mol Genet 17: 806-814.
14. Seidelmann SB, Kuo C, Pleskac N, Molina J, Sayers S, et al. (2008) Athsq1 is an atherosclerosis modifier locus with dramatic effects on lesion area and prominent accumulation of versican. Arterioscler Thromb Vasc Biol 28: 2180-2186.
15. Kim WY, Sharpless NE (2006) The regulation of INK4/ARF in cancer and aging. Cell 127: 265-275.
16. Liu Y, Sanoff HK, Cho H, Burd CE, Torrice C, et al. (2009) INK4/ARF transcript expression is associated with chromosome 9p21 variants linked to atherosclerosis. PLoS One 4: e5027.
17. Wessely R (2010) Atherosclerosis and cell cycle: put the brakes on! Critical role for cyclin-dependent kinase inhibitors. J Am Coll Cardiol 55: 2269-2271.
18. Boehm M, Nabel EG (2003) The cell cycle and cardiovascular diseases. Prog Cell Cycle Res 5: 19-30.
19. Gizard F, Amant C, Barbier O, Bellosta S, Robillard R, et al. (2005) PPAR alpha inhibits vascular smooth muscle cell proliferation underlying intimal hyperplasia by inducing the tumor suppressor p16INK4a. J Clin Invest 115: 3228-3238.
20. Gonzalez-Navarro H, Abu Nabah YN, Vinue A, Andres-Manzano MJ, Collado M, et al. (2010) P19(ARF) deficiency reduces macrophage and vascular smooth muscle cell apoptosis and aggravates atherosclerosis. J Am Coll Cardiol 55: 2258-2268.
21. Kalinina N, Agrotis A, Antropova Y, Ilyinskaya O, Smirnov V, et al. (2004) Smad expression in human atherosclerotic lesions: evidence for impaired TGFbeta/ Smad signaling in smooth muscle cells of fibrofatty lesions. Arterioscler Thromb Vasc Biol 24: 1391-1396.
22. Reynisdottir I, Polyak K, Iavarone A, Massague J (1995) Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev 9: 1831-1845.
23. Grainger DJ (2004) Transforming growth factor beta and atherosclerosis: so far, so good for the protective cytokine hypothesis. Arterioscler Thromb Vasc Biol 24: 399-404.
24. Janzen V, Forkert R, Fleming HE, Saito Y, Waring MT, et al. (2006) Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 443: 421-426.
25. Yvan-Charvet L, Pagler T, Gautier EL, Avagyan S, Siry RL, et al. (2010) ATPbinding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 328: 1689-1693.
26. Visel A, Zhu Y, May D, Afzal V, Gong E, et al. (2010) Targeted deletion of the 9p21 non-coding coronary artery disease risk interval in mice. Nature 464: 409-412.
27. Pasmant E, Laurendeau I, Heron D, Vidaud M, Vidaud D, et al. (2007) Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARF. Cancer Res 67: 3963-3969.
28. Folkersen L, Kyriakou T, Goel A, Peden J, Malarstig A, et al. (2009) Relationship between CAD risk genotype in the chromosome 9p21 locus and gene expression. Identification of eight new ANRIL splice variants. PLoS One 4: e7677.
29. Kyriakou T, Pal A, Peden J, Green F, Gloyn A, et al. (2009) ANRIL, The noncoding RNA present in the chromosome 9 CAD associated locus, has multiple splice variants and a potential regulatory role in CDKN2B expression. Atherosclerosis 207: e3.
30. Jarinova O, Stewart AF, Roberts R, Wells G, Lau P, et al. (2009) Functional analysis of the chromosome 9p21.3 coronary artery disease risk locus. Arterioscler Thromb Vasc Biol 29: 1671-1677.
31. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168.
32. Dhawan S, Tschen SI, Bhushan A (2009) Bmi-1 regulates the Ink4a/Arf locus to control pancreatic beta-cell proliferation. Genes Dev 23: 906-911.
33. Chen H, Gu X, Su IH, Bottino R, Contreras JL, et al. (2009) Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev 23: 975-985.
34. Kotake Y, Cao R, Viatour P, Sage J, Zhang Y, et al. (2007) PRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev 21: 49-54.
35. Bracken AP, Kleine-Kohlbrecher D, Dietrich N, Pasini D, Gargiulo G, et al. (2007) The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev 21: 525-530.
36. Gil J, Peters G (2006) Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat Rev Mol Cell Biol 7: 667-677.
37. Terranova R, Yokobayashi S, Stadler MB, Otte AP, van Lohuizen M, et al. (2008) Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev Cell 15: 668-679.
38. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
39. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750-756.
40. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, et al. (2008) Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 32: 232-246.
41. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, et al. (2010) Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464: 1071-1076.
42. Liu Y, Sanoff HK, Cho H, Burd CE, Torrice C, et al. (2009) Expression of p16(INK4a) in peripheral blood T-cells is a biomarker of human aging. Aging Cell 8: 439-448.
43. Hara E, Smith R, Parry D, Tahara H, Stone S, et al. (1996) Regulation of p16CDKN2 expression and its implications for cell immortalization and senescence. Mol Cell Biol 16: 859-867.
44. Krishnamurthy J, Torrice C, Ramsey MR, Kovalev GI, Al-Regaiey K, et al. (2004) Ink4a/Arf expression is a biomarker of aging. J Clin Invest 114: 1299-1307.
45. Au KF, Jiang H, Lin L, Xing Y, Wong WH. (2010) Detection of splice junctions from paired-end RNA-seq data by SpliceMap. Nucleic Acids Res.
46. Nielsen GP, Stemmer-Rachamimov AO, Shaw J, Roy JE, Koh J, et al. (1999) Immunohistochemical survey of p16INK4A expression in normal human adult and infant tissues. Lab Invest 79: 1137-1143.
47. Schmid M, Sen M, Rosenbach MD, Carrera CJ, Friedman H, et al. (2000) A methylthioadenosine phosphorylase (MTAP) fusion transcript identifies a new gene on chromosome 9p21 that is frequently deleted in cancer. Oncogene 19: 5747-5754.
48. Chen K, Wallis JW, McLellan MD, Larson DE, Kalicki JM, et al. (2009) BreakDancer: an algorithm for high-resolution mapping of genomic structural variation. Nat Methods 6: 677-681.
49. Zaphiropoulos PG (1996) Circular RNAs from transcripts of the rat cytochrome P450 2C24 gene: correlation with exon skipping. Proc Natl Acad Sci U S A 93: 6536-6541.
50. Suzuki H, Zuo Y, Wang J, Zhang MQ, Malhotra A, et al. (2006) Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing. Nucleic Acids Res 34: e63.
51. Dixon RJ, Eperon IC, Hall L, Samani NJ (2005) A genome-wide survey demonstrates widespread non-linear mRNA in expressed sequences from multiple species. Nucleic Acids Res 33: 5904-5913.
52. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 25: 1754-1760.
53. Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713-714.
54. Wang Z, Rolish ME, Yeo G, Tung V, Mawson M, et al. (2004) Systematic identification and analysis of exonic splicing silencers. Cell 119: 831-845.
55. Fairbrother WG, Yeh RF, Sharp PA, Burge CB (2002) Predictive identification of exonic splicing enhancers in human genes. Science 297: 1007-1013.
56. Wang Z, Burge CB (2008) Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. Rna 14: 802-813.
57. Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851-861.
58. Nigro JM, Cho KR, Fearon ER, Kern SE, Ruppert JM, et al. (1991) Scrambled exons. Cell 64: 607-613.
59. Holdt LM, Beutner F, Scholz M, Gielen S, Gabel G, et al. (2010) ANRIL expression is associated with atherosclerosis risk at chromosome 9p21. Arterioscler Thromb Vasc Biol 30: 620-627.
60. Cunnington MS, Santibanez Koref M, Mayosi BM, Burn J, Keavney B (2010) Chromosome 9p21 SNPs Associated with Multiple Disease Phenotypes Correlate with ANRIL Expression. PLoS Genet 6: e1000899.
61. Messaoudi-Aubert SE, Nicholls J, Maertens GN, Brookes S, Bernstein E, et al. (2010) Role for the MOV10 RNA helicase in polycomb-mediated repression of the INK4a tumor suppressor. Nat Struct Mol Biol 17: 862-868.
62. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, et al. (2010) Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38: 662-674.
63. Mancini-Dinardo D, Steele SJ, Levorse JM, Ingram RS, Tilghman SM (2006) Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev 20: 1268-1282.
64. Kanduri C, Thakur N, Pandey RR (2006) The length of the transcript encoded from the Kcnq1ot1 antisense promoter determines the degree of silencing. Embo J 25: 2096-2106.
65. Dixon RJ, Eperon IC, Samani NJ (2007) Complementary intron sequence motifs associated with human exon repetition: a role for intragenic, inter-transcript interactions in gene expression. Bioinformatics 23: 150-155.
66. Cocquerelle C, Daubersies P, Majerus MA, Kerckaert JP, Bailleul B (1992) Splicing with inverted order of exons occurs proximal to large introns. Embo J 11: 1095-1098.
67. Bonen L, Vogel J (2001) The ins and outs of group II introns. Trends Genet 17: 322-331.
68. Kos A, Dijkema R, Arnberg AC, van der Meide PH, Schellekens H (1986) The hepatitis delta (delta) virus possesses a circular RNA. Nature 323: 558-560.
69. Tsagris EM, Martinez de Alba AE, Gozmanova M, Kalantidis K (2008) Viroids. Cell Microbiol 10: 2168-2179.
70. Zeggini E, Weedon MN, Lindgren CM, Frayling TM, Elliott KS, et al. (2007) Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science 316: 1336-1341.
71. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, et al. (2007) A genomewide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316: 1341-1345.
72. Shete S, Hosking FJ, Robertson LB, Dobbins SE, Sanson M, et al. (2009) Genome-wide association study identifies five susceptibility loci for glioma. Nat Genet 41: 899-904.
73. Wrensch M, Jenkins RB, Chang JS, Yeh RF, Xiao Y, et al. (2009) Variants in the CDKN2B and RTEL1 regions are associated with high-grade glioma susceptibility. Nat Genet 41: 905-908.
74. Uno S, Zembutsu H, Hirasawa A, Takahashi A, Kubo M, et al. (2010) A genome-wide association study identifies genetic variants in the CDKN2BAS locus associated with endometriosis in Japanese. Nat Genet 42: 707-710.
75. Bei JX, Li Y, Jia WH, Feng BJ, Zhou G, et al. (2010) A genome-wide association study of nasopharyngeal carcinoma identifies three new susceptibility loci. Nat Genet 42: 599-603.
76. Emanuele E, Fontana JM, Minoretti P, Geroldi D (2010) Preliminary evidence of a genetic association between chromosome 9p21.3 and human longevity. Rejuvenation Res 13: 23-26.
77. Sebastiani P, Solovieff N, Puca A, Hartley SW, Melista E, et al. (2010) Genetic Signatures of Exceptional Longevity in Humans. Science.
78. Hanker AB, Morita S, Repasky GA, Ross DT, Seitz RS, et al. (2008) Tools to study the function of the Ras-related, estrogen-regulated growth inhibitor in breast cancer. Methods Enzymol 439: 53-72.
79. Brookes S, Rowe J, Ruas M, Llanos S, Clark PA, et al. (2002) INK4a-deficient human diploid fibroblasts are resistant to RAS-induced senescence. Embo J 21: 2936-2945.
80. Shields JM, Thomas NE, Cregger M, Berger AJ, Leslie M, et al. (2007) Lack of extracellular signal-regulated kinase mitogen-activated protein kinase signaling shows a new type of melanoma. Cancer Res 67: 1502-1512.
81. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.