Genetic Variants in MicroRNAs and Their Binding Sites Are Associated with the Risk of Parkinson Disease

Human Mutation

Volumn 37, Issue 3, 2016, Pages 292-300

  Ghanbari, Mohsen ^a,b   Darweesh, Sirwan K L ^a   de Looper, Hans W J ^a   van Luijn, Marvin M ^a   Hofman, Albert ^a,c   Ikram, M Arfan ^a   Franco, Oscar H ^a   Erkeland, Stefan J ^a   Dehghan, Abbas ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

GWAS; MiRNA variant; MiRNA binding site variant; Parkinson disease

Indexed keywords

MICRORNA;

ARTICLE; CONTROLLED STUDY; CTSB GENE; GENE; GENE CONTROL; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIABILITY; HUMAN; IGSF9B GENE; MICRORNA BINDING SITE; NUCLEOTIDE BINDING SITE; PARKINSON DISEASE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; QUANTITATIVE TRAIT LOCUS; RISK ASSESSMENT; RNA BINDING; SINGLE NUCLEOTIDE POLYMORPHISM; STX1B GENE; BINDING SITE; GENETICS;

BINDING SITES; HUMANS; MICRORNAS; PARKINSON DISEASE;

EID: 84957969751     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22943     Document Type: Article

References (71)

1. Ambros V. 2004. The functions of animal microRNAs. Nature 431:350-355.
2. Bao L, Zhou M, Wu L, Lu L, Goldowitz D, Williams RW, Cui Y. 2007. PolymiRTS Database: linking polymorphisms in microRNA target sites with complex traits. Nucleic Acids Res 35:D51-D54.
3. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-233.
4. Bellingham SA, Coleman BM, Hill AF. 2012. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res 40:10937-10949.
5. Capurro A, Bodea LG, Schaefer P, Luthi-Carter R, Perreau VM. 2014. Computational deconvolution of genome wide expression data from Parkinson's and Huntington's disease brain tissues using population-specific expression analysis. Front Neurosci 8:441.
6. Chandra S, Gallardo G, Fernandez-Chacon R, Schluter OM, Sudhof TC. 2005. Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123:383-396.
7. Chandrasekaran S, Bonchev D. 2013. A network view on Parkinson's disease. Comput Struct Biotechnol J 7:e201304004.
8. Cobb SA, Wider C, Ross OA, Mata IF, Adler CH, Rajput A, Rajput AH, Wu RM, Hauser R, Josephs KA, Carr J, Gwinn K, et al. 2009. GCH1 in early-onset Parkinson's disease. Mov Disord 24:2070-2075.
9. Cowan WM, Kandel ER. 2001. Prospects for neurology and psychiatry. JAMA 285:594-600.
10. Croisier E, Moran LB, Dexter DT, Pearce RK, Graeber MB. 2005. Microglial inflammation in the parkinsonian substantia nigra: relationship to alpha-synuclein deposition. J Neuroinflammation 2:14.
11. de Lau LM, Breteler MM. 2006. Epidemiology of Parkinson's disease. Lancet Neurol 5:525-535.
12. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. 2004. Processing of primary microRNAs by the Microprocessor complex. Nature 432:231-235.
13. Dorsey ER, Constantinescu R, Thompson JP, Biglan KM, Holloway RG, Kieburtz K, Marshall FJ, Ravina BM, Schifitto G, Siderowf A, Tanner CM. 2007. Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 68:384-386.
14. Elstner M, Morris CM, Heim K, Bender A, Mehta D, Jaros E, Klopstock T, Meitinger T, Turnbull DM, Prokisch H. 2011. Expression analysis of dopaminergic neurons in Parkinson's disease and aging links transcriptional dysregulation of energy metabolism to cell death. Acta Neuropathol 122:75-86.
15. Fischler B, Bodin K, Stjernman H, Olin M, Hansson M, Sjovall J, Bjorkhem I. 2007. Cholestatic liver disease in adults may be due to an inherited defect in bile acid biosynthesis. J Intern Med 262:254-262.
16. Friedman RC, Farh KK, Burge CB, Bartel DP. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92-105.
17. Ghanbari M, de Vries PS, de Looper H, Peters MJ, Schurmann C, Yaghootkar H, Dorr M, Frayling TM, Uitterlinden AG, Hofman A, van Meurs JB, Erkeland SJ, et al. 2014. A genetic variant in the seed region of miR-4513 shows pleiotropic effects on lipid and glucose homeostasis, blood pressure, and coronary artery disease. Hum Mutat 35:1524-1531.
18. Ghanbari M, Franco OH, de Looper H, Hofman A, Erkeland S, Dehghan A. 2015. Genetic variations in miRNA binding sites affect miRNA-mediated regulation of several genes associated with cardiometabolic phenotypes. Circ Cardiovasc Genet 8:473-486.
19. Gong J, Liu C, Liu W, Wu Y, Ma Z, Chen H, Guo AY. 2015. An update of miRNASNP database for better SNP selection by GWAS data, miRNA expression and online tools. Database (Oxford) 2015:bav029.
20. Gong J, Tong Y, Zhang HM, Wang K, Hu T, Shan G, Sun J, Guo AY. 2012. Genome-wide identification of SNPs in microRNA genes and the SNP effects on microRNA target binding and biogenesis. Hum Mutat 33:254-263.
21. Gong J, Wu Y, Zhang X, Liao Y, Sibanda VL, Liu W, Guo AY. 2014. Comprehensive analysis of human small RNA sequencing data provides insights into expression profiles and miRNA editing. RNA Biol 11:1375-1385.
22. Grundberg E, Small KS, Hedman AK, Nica AC, Buil A, Keildson S, Bell JT, Yang TP, Meduri E, Barrett A, Nisbett J, Sekowska M, et al. 2012. Mapping cis- and trans-regulatory effects across multiple tissues in twins. Nat Genet 44:1084-1089.
23. Haas A. 1998. NSF-fusion and beyond. Trends Cell Biol 8:471-473.
24. Harraz MM, Dawson TM, Dawson VL. 2011. MicroRNAs in Parkinson's disease. J Chem Neuroanat 42:127-130.
25. Hebert SS, De Strooper B. 2007. Molecular biology. miRNAs in neurodegeneration. Science 317:1179-1180.
26. Hong X, Sin WC, Harris AL, Naus CC. 2015. Gap junctions modulate glioma invasion by direct transfer of microRNA. Oncotarget 6:15566-15577.
27. Hughes AE, Bradley DT, Campbell M, Lechner J, Dash DP, Simpson DA, Willoughby CE. 2011. Mutation altering the miR-184 seed region causes familial keratoconus with cataract. Am J Hum Genet 89:628-633.
28. Issler O, Chen A. 2015. Determining the role of microRNAs in psychiatric disorders. Nat Rev Neurosci 16:201-212.
29. Khoo SK, Petillo D, Kang UJ, Resau JH, Berryhill B, Linder J, Forsgren L, Neuman LA, Tan AC. 2012. Plasma-based circulating MicroRNA biomarkers for Parkinson's disease. J Parkinsons Dis 2:321-331.
30. Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, Hannon G, Abeliovich A. 2007. A microRNA feedback circuit in midbrain dopamine neurons. Science 317:1220-1224.
31. Kozomara A, Griffiths-Jones S. 2014. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68-D73.
32. Lansbury PT, Lashuel HA. 2006. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 443:774-779.
33. Lencz T, Lambert C, DeRosse P, Burdick KE, Morgan TV, Kane JM, Kucherlapati R, Malhotra AK. 2007. Runs of homozygosity reveal highly penetrant recessive loci in schizophrenia. Proc Natl Acad Sci USA 104:19942-19947.
34. Lill CM, Roehr JT, McQueen MB, Kavvoura FK, Bagade S, Schjeide BM, Schjeide LM, Meissner E, Zauft U, Allen NC, Liu T, Schilling M, et al. 2012. Comprehensive research synopsis and systematic meta-analyses in Parkinson's disease genetics: the PDGene database. PLoS Genet 8:e1002548.
35. Liu X, Cheng R, Verbitsky M, Kisselev S, Browne A, Mejia-Sanatana H, Louis ED, Cote LJ, Andrews H, Waters C, Ford B, Frucht S, et al. 2011. Genome-wide association study identifies candidate genes for Parkinson's disease in an Ashkenazi Jewish population. BMC Med Genet 12:104.
36. Lohle M, Storch A, Reichmann H. 2009. Beyond tremor and rigidity: non-motor features of Parkinson's disease. J Neural Transm 116:1483-1492.
37. Lorenz R, Bernhart SH, Honer Zu Siederdissen C, Tafer H, Flamm C, Stadler PF, Hofacker IL. 2011. ViennaRNA Package 2.0. Algorithms Mol Biol 6:26.
38. Margis R, Margis R, Rieder CR. 2011. Identification of blood microRNAs associated to Parkinsonis disease. J Biotechnol 152:96-101.
39. Martins M, Rosa A, Guedes LC, Fonseca BV, Gotovac K, Violante S, Mestre T, Coelho M, Rosa MM, Martin ER, Vance JM, Outeiro TF, et al. 2011. Convergence of miRNA expression profiling, alpha-synuclein interaction and GWAS in Parkinson's disease. PLoS One 6:e25443.
40. Meenhuis A, van Veelen PA, de Looper H, van Boxtel N, van den Berge IJ, Sun SM, Taskesen E, Stern P, de Ru AH, van Adrichem AJ, Demmers J, Jongen-Lavrencic M, et al. 2011. MiR-17/20/93/106 promote hematopoietic cell expansion by targeting sequestosome 1-regulated pathways in mice. Blood 118:916-925.
41. Mizuta I, Satake W, Nakabayashi Y, Ito C, Suzuki S, Momose Y, Nagai Y, Oka A, Inoko H, Fukae J, Saito Y, Sawabe M, et al. 2006. Multiple candidate gene analysis identifies alpha-synuclein as a susceptibility gene for sporadic Parkinson's disease. Hum Mol Genet 15:1151-1158.
42. Momma K, Funayama M, Li Y, Ichinose H, Motoyoshi K, Hattori N, Mizuno Y, Kamakura K. 2009. A new mutation in the GCH1 gene presents as early-onset Parkinsonism. Parkinsonism Relat Disord 15:160-161.
43. Montag J, Hitt R, Opitz L, Schulz-Schaeffer WJ, Hunsmann G, Motzkus D. 2009. Upregulation of miRNA hsa-miR-342-3p in experimental and idiopathic prion disease. Mol Neurodegener 4:36.
44. Mueller JC, Fuchs J, Hofer A, Zimprich A, Lichtner P, Illig T, Berg D, Wullner U, Meitinger T, Gasser T. 2005. Multiple regions of alpha-synuclein are associated with Parkinson's disease. Ann Neurol 57:535-541.
45. Muller M, Jakel L, Bruinsma IB, Claassen JA, Kuiperij HB, Verbeek MM. 2015. MicroRNA-29a is a candidate biomarker for Alzheimer's disease in cell-free cerebrospinal fluid. Mol Neurobiol. doi:10.1007/s12035-015-9156-9158.
46. Nalls MA, Pankratz N, Lill CM, Do CB, Hernandez DG, Saad M, DeStefano AL, Kara E, Bras J, Sharma M, Schulte C, Keller MF, et al. 2014. Large-scale meta-analysis of genome-wide association data identifies six new risk loci for Parkinson's disease. Nat Genet 46:989-993.
47. Obsteter J, Dovc P, Kunej T. 2015. Genetic variability of microRNA regulome in human. Mol Genet Genomic Med 3:30-39.
48. Ogundare M, Theofilopoulos S, Lockhart A, Hall LJ, Arenas E, Sjovall J, Brenton AG, Wang Y, Griffiths WJ. 2010. Cerebrospinal fluid steroidomics: are bioactive bile acids present in brain? J Biol Chem 285:4666-4679.
49. Radfar MH, Wong W, Morris Q. 2011. Computational prediction of intronic microRNA targets using host gene expression reveals novel regulatory mechanisms. PLoS One 6:e19312.
50. Richardson K, Nettleton JA, Rotllan N, Tanaka T, Smith CE, Lai CQ, Parnell LD, Lee YC, Lahti J, Lemaitre RN, Manichaikul A, Keller M, et al. 2013. Gain-of-function lipoprotein lipase variant rs13702 modulates lipid traits through disruption of a microRNA-410 seed site. Am J Hum Genet 92:5-14.
51. Ritchie W, Flamant S, Rasko JE. 2010. mimiRNA: a microRNA expression profiler and classification resource designed to identify functional correlations between microRNAs and their targets. Bioinformatics 26:223-227.
52. Ruepp A, Kowarsch A, Schmidl D, Buggenthin F, Brauner B, Dunger I, Fobo G, Frishman G, Montrone C, Theis FJ. 2010. PhenomiR: a knowledgebase for microRNA expression in diseases and biological processes. Genome Biol 11:R6.
53. Ryan BM, Robles AI, Harris CC. 2010. Genetic variation in microRNA networks: the implications for cancer research. Nat Rev Cancer 10:389-402.
54. Saba R, Medina SJ, Booth SA. 2014. A functional SNP catalog of overlapping miRNA-binding sites in genes implicated in prion disease and other neurodegenerative disorders. Hum Mutat 35:1233-1248.
55. Schechter I, Ziv E. 2011. Cathepsins S, B and L with aminopeptidases display beta-secretase activity associated with the pathogenesis of Alzheimer's disease. Biol Chem 392:555-569.
56. Serafin A, Foco L, Zanigni S, Blankenburg H, Picard A, Zanon A, Giannini G, Pichler I, Facheris MF, Cortelli P, Pramstaller PP, Hicks AA, et al. 2015. Overexpression of blood microRNAs 103a, 30b, and 29a in L-dopa-treated patients with PD. Neurology 84:645-653.
57. Shulman JM, De Jager PL, Feany MB. 2011. Parkinson's disease: genetics and pathogenesis. Annu Rev Pathol 6:193-222.
58. Simunovic F, Yi M, Wang Y, Stephens R, Sonntag KC. 2010. Evidence for gender-specific transcriptional profiles of nigral dopamine neurons in Parkinson disease. PLoS One 5:e8856.
59. Smirnova T, Stinnakre J, Mallet J. 1993. Characterization of a presynaptic glutamate receptor. Science 262:430-433.
60. Stamova B, Ander BP, Barger N, Sharp FR, Schumann CM. 2015. Specific regional and age-related small noncoding RNA expression patterns within superior temporal gyrus of typical human brains are less distinct in autism brains. J Child Neurol 30:1930-1946.
61. Sun G, Yan J, Noltner K, Feng J, Li H, Sarkis DA, Sommer SS, Rossi JJ. 2009. SNPs in human miRNA genes affect biogenesis and function. RNA 15:1640-1651.
62. Sundelof J, Sundstrom J, Hansson O, Eriksdotter-Jonhagen M, Giedraitis V, Larsson A, Degerman-Gunnarsson M, Ingelsson M, Minthon L, Blennow K, Kilander L, Basun H, Lannfelt L. 2010. Higher cathepsin B levels in plasma in Alzheimer's disease compared to healthy controls. J Alzheimers Dis 22:1223-1230.
63. Tan EK, Skipper LM. 2007. Pathogenic mutations in Parkinson disease. Hum Mutat 28:641-653.
64. Tan L, Yu JT, Tan L. 2015. Causes and consequences of MicroRNA dysregulation in neurodegenerative diseases. Mol Neurobiol 51:1249-1262.
65. Tan L, Yu JT, Tan MS, Liu QY, Wang HF, Zhang W, Jiang T, Tan L. 2014. Genome-wide serum microRNA expression profiling identifies serum biomarkers for Alzheimer's disease. J Alzheimers Dis 40:1017-1027.
66. Villa C, Ridolfi E, Fenoglio C, Ghezzi L, Vimercati R, Clerici F, Marcone A, Gallone S, Serpente M, Cantoni C, Bonsi R, Cioffi S, et al. 2013. Expression of the transcription factor Sp1 and its regulatory hsa-miR-29b in peripheral blood mononuclear cells from patients with Alzheimer's disease. J Alzheimers Dis 35:487-494.
67. Westra HJ, Peters MJ, Esko T, Yaghootkar H, Schurmann C, Kettunen J, Christiansen MW, Fairfax BP, Schramm K, Powell JE, Zhernakova A, Zhernakova DV, et al. 2013. Systematic identification of trans eQTLs as putative drivers of known disease associations. Nat Genet 45:1238-1243.
68. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. 2009. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11:228-234.
69. Wong N, Wang X. 2015. miRDB: an online resource for microRNA target prediction and functional annotations. Nucleic Acids Res 43:D146-D152.
70. Woo J, Kwon SK, Nam J, Choi S, Takahashi H, Krueger D, Park J, Lee Y, Bae JY, Lee D, Ko J, Kim H, et al. 2013. The adhesion protein IgSF9b is coupled to neuroligin 2 via S-SCAM to promote inhibitory synapse development. J Cell Biol 201:929-944.
71. Zirn B, Steinberger D, Troidl C, Brockmann K, von der Hagen M, Feiner C, Henke L, Muller U. 2008. Frequency of GCH1 deletions in Dopa-responsive dystonia. J Neurol Neurosurg Psychiatry 79:183-186.