Cis-acting polymorphisms affect complex traits through modifications of MicroRNA regulation pathways

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Arnold, Matthias ^a   Ellwanger, Daniel C ^a,b   Hartsperger, Mara L ^a   Pfeufer, Arne ^a,b,c,d   Stümpflen, Volker ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE FOR RENEWABLE ENERGY   (Italy)

^d Affiliated Institute of the University Lübeck   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; NONHISTONE PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE MAPPING; GENE MUTATION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRAIT; GENETIC VARIABILITY; HUMAN; HUMAN CELL; LIPID METABOLISM; MUTAGENESIS; POLYADENYLATION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN SECONDARY STRUCTURE; SINGLE NUCLEOTIDE POLYMORPHISM; UPREGULATION; BILIARY CIRRHOSIS; BIOLOGICAL MODEL; GENETIC COMPLEMENTATION; GENETIC POLYMORPHISM; GENETICS; MUTATION; RNA SPLICING; RNA STABILITY; SYSTEMS BIOLOGY;

3' UNTRANSLATED REGIONS; CHROMOSOMAL PROTEINS, NON-HISTONE; GENETIC COMPLEMENTATION TEST; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LINKAGE DISEQUILIBRIUM; LIPID METABOLISM; LIVER CIRRHOSIS, BILIARY; MICRORNAS; MODELS, GENETIC; MUTATION; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA SPLICING; RNA STABILITY; SYSTEMS BIOLOGY;

EID: 84861001708     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036694     Document Type: Article

References (91)

1. Jiang Q, Wang Y, Hao Y, Juan L, Teng M, et al. (2009) mir2disease: a manually curated database for microrna deregulation in human disease. Nucleic Acids Res 37: D98-104.
2. Ruepp A, Kowarsch A, Schmidl D, Buggenthin F, Brauner B, et al. (2010) Phenomir: a knowledgebase for microrna expression in diseases and biological processes. Genome Biol 11: R6.
3. Gupta SK, Bang C, Thum T, (2010) Circulating micrornas as biomarkers and potential paracrine mediators of cardiovascular disease. Circ Cardiovasc Genet 3: 484-488.
4. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, et al. (2005) Microrna expression profiles classify human cancers. Nature 435: 834-838.
5. Rosenfeld N, Aharonov R, Meiri E, Rosenwald S, Spector Y, et al. (2008) Micrornas accurately identify cancer tissue origin. Nat Biotechnol 26: 462-469.
6. Eisenberg I, Eran A, Nishino I, Moggio M, Lamperti C, et al. (2007) Distinctive patterns of microrna expression in primary muscular disorders. Proc Natl Acad Sci U S A 104: 17016-17021.
7. Friedman RC, Farh KKH, Burge CB, Bartel DP, (2009) Most mammalian mrnas are conserved targets of micrornas. Genome Res 19: 92-105.
8. Hebert SS, Strooper BD, (2009) Alterations of the microrna network cause neurodegenerative disease. Trends Neurosci 32: 199-206.
9. Johnston RJ, Chang S, Etchberger JF, Ortiz CO, Hobert O, (2005) Micrornas acting in a doublenegative feedback loop to control a neuronal cell fate decision. Proc Natl Acad Sci U S A 102: 12449-12454.
10. Re A, Cora D, Taverna D, Caselle M, (2009) Genome-wide survey of microrna-transcription factor feed-forward regulatory circuits in human. Mol Biosyst 5: 854-867.
11. Wilbert ML, Yeo GW, (2010) Genome-wide approaches in the study of microrna biology. Wiley Interdiscip Rev Syst Biol Med.
12. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, et al. (2003) Clip identifies nova-regulated rna networks in the brain. Science 302: 1212-1215.
13. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, et al. (2008) Hits-clip yields genome-wide insights into brain alternative rna processing. Nature 456: 464-469.
14. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, et al. (2010) Transcriptome-wide identification of rna-binding protein and microrna target sites by par-clip. Cell 141: 129-141.
15. Chi SW, Zang JB, Mele A, Darnell RB, (2009) Argonaute hits-clip decodes microrna-mrna interaction maps. Nature 460: 479-486.
16. de la Chapelle A, (2009) Genetic predisposition to human disease: allele-specific expression and low-penetrance regulatory loci. Oncogene 28: 3345-3348.
17. Meola N, Gennarino VA, Banfi S, (2009) micrornas and genetic diseases. Pathogenetics 2: 7.
18. Richardson K, Lai CQ, Parnell LD, Lee YC, Ordovas JM, (2011) A genome-wide survey for snps altering microrna seed sites identifies functional candidates in gwas. BMC Genomics 12: 504.
19. Bennett CL, Brunkow ME, Ramsdell F, O'Briant KC, Zhu Q, et al. (2001) A rare polyadenylation signal mutation of the foxp3 gene (aauaaa-¿aaugaa) leads to the ipex syndrome. Immunogenetics 53: 435-439.
20. Walters RW, Bradrick SS, Gromeier M, (2010) Poly(a)-binding protein modulates mrna susceptibility to cap-dependent mirna-mediated repression. RNA 16: 239-250.
21. Li X, Quon G, Lipshitz HD, Morris Q, (2010) Predicting in vivo binding sites of rna-binding proteins using mrna secondary structure. RNA 16: 1096-1107.
22. Waldispühl J, Clote P, (2007) Computing the partition function and sampling for saturated secondary structures of rna, with respect to the turner energy model. J Comput Biol 14: 190-215.
23. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E, (2007) The role of site accessibility in microrna target recognition. Nat Genet 39: 1278-1284.
24. Yang JO, Kim WY, Bhak J, (2009) sssnptarget: genome-wide splice-site single nucleotide polymorphism database. Hum Mutat 30: E1010-E1020.
25. Visscher PM, Montgomery GW, (2009) Genome-wide association studies and human disease: from trickle to ood. JAMA 302: 2028-2029.
26. Dickson SP, Wang K, Krantz I, Hakonarson H, Goldstein DB, (2010) Rare variants create synthetic genome-wide associations. PLoS Biol 8: e1000294.
27. Lowe CE, Cooper JD, Brusko T, Walker NM, Smyth DJ, et al. (2007) Large-scale genetic fine mapping and genotype-phenotype associations implicate polymorphism in the il2ra region in type 1 diabetes. Nat Genet 39: 1074-1082.
28. McCarthy MI, Hirschhorn JN, (2008) Genome-wide association studies: potential next steps on a genetic journey. Hum Mol Genet 17: R156-R165.
29. Hindorff LA, Junkins HA, Hall PN, Mehta JP, Manolio TA, (2011) A catalog of published genomewide association studies. Available at wwwgenomegov/gwastudies Accessed December 18th, 2011.
30. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, et al. (2009) Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci U S A 106: 9362-9367.
31. Consortium IH, (2003) The international hapmap project. Nature 426: 789-796.
32. Consortium IH, Frazer KA, Ballinger DG, Cox DR, Hinds DA, et al. (2007) A second generation human haplotype map of over 3.1 million snps. Nature 449: 851-861.
33. Consortium IH, Altshuler DM, Gibbs RA, Peltonen L, Altshuler DM, et al. (2010) Integrating common and rare genetic variation in diverse human populations. Nature 467: 52-58.
34. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using david bioinformatics resources. Nat Protoc 4: 44-57.
35. Huang DW, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13.
36. Becker KG, Barnes KC, Bright TJ, Wang SA, (2004) The genetic association database. Nat Genet 36: 431-432.
37. Heathcote J, (2000) Update on primary biliary cirrhosis. Can J Gastroenterol 14: 43-48.
38. Mackay IR, (2007) Autoimmune diseases of the liver, autoimmune hepatitis and primary biliary cirrhosis: Unfinished business. Hepatol Res 37 (Suppl 3): S357-S364.
39. Selmi C, Zuin M, Gershwin ME, (2008) The unfinished business of primary biliary cirrhosis. J Hepatol 49: 451-460.
40. Sawa T, Ohshima H, (2006) Nitrative dna damage in inammation and its possible role in carcinogenesis. Nitric Oxide 14: 91-100.
41. Kryston TB, Georgiev AB, Pissis P, Georgakilas AG, (2011) Role of oxidative stress and dna damage in human carcinogenesis. Mutat Res.
42. Hirschfield GM, Liu X, Xu C, Lu Y, Xie G, et al. (2009) Primary biliary cirrhosis associated with hla, il12a, and il12rb2 variants. N Engl J Med 360: 2544-2555.
43. Onn I, Aono N, Hirano M, Hirano T, (2007) Reconstitution and subunit geometry of human condensing complexes. EMBO J 26: 1024-1034.
44. Zindy P, Andrieux L, Bonnier D, Musso O, Langouet S, et al. (2005) Upregulation of dna repair genes in active cirrhosis associated with hepatocellular carcinoma. FEBS Lett 579: 95-99.
45. Heale JT, Ball AR, Schmiesing JA, Kim JS, Kong X, et al. (2006) Condensin i interacts with the parp-1-xrcc1 complex and functions in dna single-strand break repair. Mol Cell 21: 837-848.
46. Padgett KA, Lan RY, Leung PC, Lleo A, Dawson K, et al. (2009) Primary biliary cirrhosis is associated with altered hepatic microrna expression. J Autoimmun 32: 246-253.
47. Ellwanger DC, Büttner FA, Mewes HW, Stümpen V, (2011) The sufficient minimal set of mirna seed types. Bioinformatics 27: 1346-1350.
48. Nica AC, Parts L, Glass D, Nisbet J, Barrett A, et al. (2011) The architecture of gene regulatory variation across multiple human tissues: the muther study. PLoS Genet 7: e1002003.
49. Turissini SB, Kaplan MM, (1997) Hepatocellular carcinoma in primary biliary cirrhosis. Am J Gastroenterol 92: 676-678.
50. Howel D, Metcalf JV, Gray J, Newman WL, Jones DE, et al. (1999) Cancer risk in primary biliary cirrhosis: a study in northern england. Gut 45: 756-760.
51. Sage E, Harrison L, (2010) Clustered dna lesion repair in eukaryotes: Relevance to mutagenesis and cell survival. Mutat Res.
52. Li SX, Sjolund A, Harris L, Sweasy JB, (2010) Dna repair and personalized breast cancer therapy. Environ Mol Mutagen 51: 897-908.
53. Kirschner K, Melton DW, (2010) Multiple roles of the ercc1-xpf endonuclease in dna repair and resistance to anticancer drugs. Anticancer Res 30: 3223-3232.
54. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, et al. (2009) Finding the missing heritability of complex diseases. Nature 461: 747-753.
55. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, et al. (2008) The impact of micrornas on protein output. Nature 455: 64-71.
56. Guo H, Ingolia NT, Weissman JS, Bartel DP, (2010) Mammalian micrornas predominantly act to decrease target mrna levels. Nature 466: 835-840.
57. Friedman JM, Jones PA, (2009) Micrornas: critical mediators of differentiation, development and disease. Swiss Med Wkly 139: 466-472.
58. Sheedy FJ, O'Neill LAJ, (2008) Adding fuel to fire: micrornas as a new class of mediators of inammation. Ann Rheum Dis 67 (Suppl 3): iii50-iii55.
59. McCarthy MI, Abecasis GR, Cardon LR, Goldstein DB, Little J, et al. (2008) Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nat Rev Genet 9: 356-369.
60. modE N C O D E Consortium, Roy S, Ernst J, Kharchenko PV, Kheradpour P, et al. (2010) Identification of functional elements and regulatory circuits by drosophila modencode. Science 330: 1787-1797.
61. Gerstein MB, Lu ZJ, Nostrand ELV, Cheng C, Arshinoff BI, et al. (2010) Integrative analysis of the caenorhabditis elegans genome by the modencode project. Science 330: 1775-1787.
62. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O'Donnell CJ, et al. (2008) Snap: a web-based tool for identification and annotation of proxy snps using hapmap. Bioinformatics 24: 2938-2939.
63. Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, et al. (2001) dbsnp: the ncbi database of genetic variation. Nucleic Acids Res 29: 308-311.
64. Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, et al. (2004) The ucsc table browser data retrieval tool. Nucleic Acids Res 32: D493-D496.
65. Pruitt KD, Tatusova T, Maglott DR, (2007) Ncbi reference sequences (refseq): a curated nonredundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35: D61-D65.
66. Griffiths-Jones S, (2004) The microrna registry. Nucleic Acids Res 32: D109-D111.
67. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ, (2006) mirbase: microrna sequences, targets and gene nomenclature. Nucleic Acids Res 34: D140-D144.
68. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ, (2008) mirbase: tools for microrna genomics. Nucleic Acids Res 36: D154-D158.
69. Rhead B, Karolchik D, Kuhn RM, Hinrichs AS, Zweig AS, et al. (2010) The ucsc genome browser database: update 2010. Nucleic Acids Res 38: D613-D619.
70. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
71. Betel D, Wilson M, Gabow A, Marks DS, Sander C, (2008) The microrna.org resource: targets and expression. Nucleic Acids Res 36: D149-D153.
72. Yang JH, Li JH, Shao P, Zhou H, Chen YQ, et al. (2011) starbase: a database for exploring microrna-mrna interaction maps from argonaute clip-seq and degradome-seq data. Nucleic Acids Res 39: D202-D209.
73. Zhang H, Hu J, Recce M, Tian B, (2005) Polya db: a database for mammalian mrna polyadenylation. Nucleic Acids Res 33: D116-D120.
74. Lee JY, Yeh I, Park JY, Tian B, (2007) Polya db 2: mrna polyadenylation sites in vertebrate genes. Nucleic Acids Res 35: D165-D168.
75. Beaudoing E, Freier S, Wyatt JR, Claverie JM, Gautheret D, (2000) Patterns of variant polyadenylation signal usage in human genes. Genome Res 10: 1001-1010.
76. Reese MG, Eeckman FH, Kulp D, Haussler D, (1997) Improved splice site detection in genie. J Comput Biol 4: 311-323.
77. Schwarz JM, Rödelsperger C, Schuelke M, Seelow D, (2010) Mutationtaster evaluates diseasecausing potential of sequence alterations. Nat Methods 7: 575-576.
78. Hofacker IL, (2003) Vienna rna secondary structure server. Nucleic Acids Res 31: 3429-3431.
79. Halvorsen M, Martin JS, Broadaway S, Laederach A, (2010) Disease-associated mutations that alter the rna structural ensemble. PLoS Genet 6: e1001074.
80. R Development Core Team (2011) R: A Language and Environment for Statistica Computing. R Foundation for Statistical Computing, Vienna, Austria. 18 URL http://www.R-project.org. ISBN 3-900051-07-0. Accessed 2011 Dec.
81. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.
82. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, et al. (2003) Pgc-1alpharesponsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273.
83. Consortium GO, (2010) The gene ontology in 2010: extensions and refinements. Nucleic Acids Res 38: D331-D335.
84. Aranda B, Achuthan P, Alam-Faruque Y, Armean I, Bridge A, et al. (2010) The intact molecular interaction database in 2010. Nucleic Acids Res 38: D525-D531.
85. Ruepp A, Waegele B, Lechner M, Brauner B, Dunger-Kaltenbach I, et al. (2010) Corum: the comprehensive resource of mammalian protein complexes-2009. Nucleic Acids Res 38: D497-D501.
86. Kanehisa M, Goto S, (2000) Kegg: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
87. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, et al. (2006) From genomics to chemical genomics: new developments in kegg. Nucleic Acids Res 34: D354-D357.
88. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M, (2010) Kegg for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38: D355-D360.
89. Yang TP, Beazley C, Montgomery SB, Dimas AS, Gutierrez-Arcelus M, et al. (2010) Genevar: a database and java application for the analysis and visualization of snp-gene associations in eqtl studies. Bioinformatics 26: 2474-2476.
90. Hess A, Iyer H, (2007) Fisher's combined p-value for detecting differentially expressed genes using affymetrix expression arrays. BMC Genomics 8: 96.
91. Benjamini Y, Yekutieli D, (2001) The control of the false discovery rate in multiple testing under dependency. Annals of Statistics 29: 1165-1188.