{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,29]],"date-time":"2025-10-29T06:18:14Z","timestamp":1761718694415,"version":"3.37.3"},"reference-count":41,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2018,7,12]],"date-time":"2018-07-12T00:00:00Z","timestamp":1531353600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0200446","type":"journal-article","created":{"date-parts":[[2018,7,12]],"date-time":"2018-07-12T14:13:35Z","timestamp":1531404815000},"page":"e0200446","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":23,"title":["Whole exome sequencing identifies MRVI1 as a susceptibility gene for moyamoya syndrome in neurofibromatosis type 1"],"prefix":"10.1371","volume":"13","author":[{"given":"Claudia","family":"Santoro","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Teresa","family":"Giugliano","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Markus","family":"Kraemer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Annalaura","family":"Torella","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jan Claudius","family":"Schwitalla","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5350-7700","authenticated-orcid":true,"given":"Mario","family":"Cirillo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniela","family":"Melis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Peter","family":"Berlit","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Vincenzo","family":"Nigro","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Silverio","family":"Perrotta","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9418-125X","authenticated-orcid":true,"given":"Giulio","family":"Piluso","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2018,7,12]]},"reference":[{"issue":"3","key":"ref1","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1001\/archneur.1969.00480090076012","article-title":"Cerebrovascular &quot;moyamoya&quot; disease. Disease showing abnormal net-like vessels in base of brain","volume":"20","author":"J Suzuki","year":"1969","journal-title":"Arch Neurol"},{"issue":"12","key":"ref2","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1056\/NEJMra0804622","article-title":"Moyamoya disease and moyamoya syndrome","volume":"360","author":"RM Scott","year":"2009","journal-title":"The New England journal of medicine"},{"issue":"6","key":"ref3","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1212\/01.wnl.0000176066.33797.82","article-title":"Moyamoya disease in Washington State and California","volume":"65","author":"K Uchino","year":"2005","journal-title":"Neurology"},{"issue":"1","key":"ref4","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1161\/STROKEAHA.107.490714","article-title":"Prevalence and clinicoepidemiological features of moyamoya disease in Japan: findings from a nationwide epidemiological survey","volume":"39","author":"S Kuriyama","year":"2008","journal-title":"Stroke; a journal of cerebral circulation"},{"issue":"12","key":"ref5","doi-asserted-by":"crossref","first-page":"3193","DOI":"10.1161\/STROKEAHA.107.513408","article-title":"Moyamoya disease in Europeans","volume":"39","author":"M Kraemer","year":"2008","journal-title":"Stroke; a journal of cerebral circulation"},{"issue":"4","key":"ref6","doi-asserted-by":"crossref","first-page":"E4","DOI":"10.3171\/2009.1.FOCUS08302","article-title":"Pathophysiology and genetic factors in moyamoya disease","volume":"26","author":"AS Achrol","year":"2009","journal-title":"Neurosurgical focus"},{"issue":"7","key":"ref7","doi-asserted-by":"crossref","first-page":"e22542","DOI":"10.1371\/journal.pone.0022542","article-title":"Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development","volume":"6","author":"W Liu","year":"2011","journal-title":"PloS one"},{"issue":"8","key":"ref8","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1038\/ejhg.2017.92","article-title":"Rare RNF213 variants in the C-terminal region encompassing the RING-finger domain are associated with moyamoya angiopathy in Caucasians","volume":"25","author":"S Guey","year":"2017","journal-title":"European journal of human genetics: EJHG"},{"issue":"1","key":"ref9","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1161\/STROKEAHA.117.017430","article-title":"Novel Susceptibility Loci for Moyamoya Disease Revealed by a Genome-Wide Association Study","volume":"49","author":"L Duan","year":"2018","journal-title":"Stroke; a journal of cerebral circulation"},{"issue":"3","key":"ref10","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/j.ajhg.2014.01.018","article-title":"Loss of alpha1beta1 soluble guanylate cyclase, the major nitric oxide receptor, leads to moyamoya and achalasia","volume":"94","author":"D Herv\u00e9","year":"2014","journal-title":"American journal of human genetics"},{"article-title":"GeneReviews(R)","year":"1993","author":"JM Friedman","key":"ref11"},{"issue":"3","key":"ref12","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1097\/00125817-200205000-00002","article-title":"Cardiovascular disease in neurofibromatosis 1: report of the NF1 Cardiovascular Task Force","volume":"4","author":"JM Friedman","year":"2002","journal-title":"Genetics in medicine: official journal of the American College of Medical Genetics"},{"issue":"1","key":"ref13","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.pediatrneurol.2013.04.007","article-title":"Neurofibromatosis type 1 associated with moyamoya syndrome in children","volume":"50","author":"A Duat-Rodriguez","year":"2014","journal-title":"Pediatric neurology"},{"issue":"2","key":"ref14","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.jocn.2014.05.046","article-title":"Clinical characteristics and long-term outcomes of moyamoya syndrome associated with neurofibromatosis type 1","volume":"22","author":"C Han","year":"2015","journal-title":"Journal of clinical neuroscience: official journal of the Neurosurgical Society of Australasia"},{"issue":"6","key":"ref15","doi-asserted-by":"crossref","first-page":"1521","DOI":"10.1002\/ajmg.a.38212","article-title":"Moyamoya syndrome in children with neurofibromatosis type 1: Italian-French experience","volume":"173","author":"C Santoro","year":"2017","journal-title":"American journal of medical genetics Part A"},{"article-title":"Clinical and epidemiological features","year":"1999","author":"JM Friedman","key":"ref16"},{"issue":"1","key":"ref17","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1161\/01.STR.14.1.104","article-title":"Moyamoya disease\u2014a review","volume":"14","author":"J Suzuki","year":"1983","journal-title":"Stroke; a journal of cerebral circulation"},{"issue":"5","key":"ref18","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1001\/archneur.1988.00520290115023","article-title":"Neurofibromatosis: Conference Statement","volume":"45","year":"1988","journal-title":"Arch Neurol"},{"issue":"Suppl 3","key":"ref19","doi-asserted-by":"crossref","first-page":"S5","DOI":"10.1186\/1471-2164-15-S3-S5","article-title":"A community-based resource for automatic exome variant-calling and annotation in Mendelian disorders","volume":"15","author":"M Mutarelli","year":"2014","journal-title":"BMC genomics"},{"issue":"5","key":"ref20","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1038\/ng.806","article-title":"A framework for variation discovery and genotyping using next-generation DNA sequencing data","volume":"43","author":"MA DePristo","year":"2011","journal-title":"Nature genetics"},{"issue":"16","key":"ref21","doi-asserted-by":"crossref","first-page":"e164","DOI":"10.1093\/nar\/gkq603","article-title":"ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data","volume":"38","author":"K Wang","year":"2010","journal-title":"Nucleic acids research"},{"issue":"Database issue","key":"ref22","doi-asserted-by":"crossref","first-page":"D32","DOI":"10.1093\/nar\/gkn721","article-title":"NCBI Reference Sequences: current status, policy and new initiatives","volume":"37","author":"KD Pruitt","year":"2009","journal-title":"Nucleic acids research"},{"issue":"1","key":"ref23","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1093\/nar\/29.1.308","article-title":"dbSNP: the NCBI database of genetic variation","volume":"29","author":"ST Sherry","year":"2001","journal-title":"Nucleic acids research"},{"issue":"7319","key":"ref24","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1038\/nature09534","article-title":"A map of human genome variation from population-scale sequencing","volume":"467","author":"C Genomes Project","year":"2010","journal-title":"Nature"},{"issue":"1","key":"ref25","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1101\/gr.097857.109","article-title":"Detection of nonneutral substitution rates on mammalian phylogenies","volume":"20","author":"KS Pollard","year":"2010","journal-title":"Genome research"},{"issue":"8","key":"ref26","doi-asserted-by":"crossref","first-page":"894","DOI":"10.1002\/humu.21517","article-title":"dbNSFP: a lightweight database of human nonsynonymous SNPs and their functional predictions","volume":"32","author":"X Liu","year":"2011","journal-title":"Human mutation"},{"issue":"6","key":"ref27","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1016\/j.ajhg.2011.04.017","article-title":"Loss of BRCC3 deubiquitinating enzyme leads to abnormal angiogenesis and is associated with syndromic moyamoya","volume":"88","author":"S Miskinyte","year":"2011","journal-title":"American journal of human genetics"},{"issue":"2","key":"ref28","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.ajhg.2013.06.019","article-title":"Recurrent gain-of-function mutation in PRKG1 causes thoracic aortic aneurysms and acute aortic dissections","volume":"93","author":"DC Guo","year":"2013","journal-title":"American journal of human genetics"},{"issue":"6","key":"ref29","doi-asserted-by":"crossref","first-page":"C1445","DOI":"10.1152\/ajpcell.00304.2010","article-title":"Truncated IRAG variants modulate cGMP-mediated inhibition of human colonic smooth muscle cell contraction","volume":"301","author":"A Werder","year":"2011","journal-title":"American journal of physiology Cell physiology"},{"issue":"3","key":"ref30","doi-asserted-by":"crossref","first-page":"H672","DOI":"10.1152\/ajpheart.00198.2011","article-title":"IRAG and novel PKG targeting in the cardiovascular system","volume":"301","author":"J Schlossmann","year":"2011","journal-title":"American journal of physiology Heart and circulatory physiology"},{"issue":"2","key":"ref31","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1086\/302243","article-title":"Mapping of a familial moyamoya disease gene to chromosome 3p24.2-p26","volume":"64","author":"H Ikeda","year":"1999","journal-title":"American journal of human genetics"},{"issue":"3","key":"ref32","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1177\/088307380001500307","article-title":"Linkage analysis of moyamoya disease on chromosome 6","volume":"15","author":"TK Inoue","year":"2000","journal-title":"Journal of child neurology"},{"issue":"5","key":"ref33","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1007\/s10038-004-0143-6","article-title":"A novel susceptibility locus for moyamoya disease on chromosome 8q23","volume":"49","author":"K Sakurai","year":"2004","journal-title":"Journal of human genetics"},{"issue":"4","key":"ref34","doi-asserted-by":"crossref","first-page":"930","DOI":"10.1161\/01.STR.31.4.930","article-title":"Linkage of familial moyamoya disease (spontaneous occlusion of the circle of Willis) to chromosome 17q25","volume":"31","author":"T Yamauchi","year":"2000","journal-title":"Stroke; a journal of cerebral circulation"},{"issue":"4","key":"ref35","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1161\/01.HYP.0000208330.68355.72","article-title":"Genome-wide linkage study of retinal vessel diameters in the Beaver Dam Eye Study","volume":"47","author":"C Xing","year":"2006","journal-title":"Hypertension"},{"issue":"26","key":"ref36","doi-asserted-by":"crossref","first-page":"24153","DOI":"10.1074\/jbc.M101530200","article-title":"Molecular determinants of the interaction between the inositol 1,4,5-trisphosphate receptor-associated cGMP kinase substrate (IRAG) and cGMP kinase Ibeta","volume":"276","author":"A Ammendola","year":"2001","journal-title":"The Journal of biological chemistry"},{"issue":"21","key":"ref37","doi-asserted-by":"crossref","first-page":"4222","DOI":"10.1038\/sj.emboj.7600440","article-title":"IRAG is essential for relaxation of receptor-triggered smooth muscle contraction by cGMP kinase","volume":"23","author":"A Geiselhoringer","year":"2004","journal-title":"The EMBO journal"},{"issue":"7","key":"ref38","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1038\/ng.604","article-title":"Genome-wide meta-analyses identifies seven loci associated with platelet aggregation in response to agonists","volume":"42","author":"AD Johnson","year":"2010","journal-title":"Nature genetics"},{"issue":"1","key":"ref39","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.jstrokecerebrovasdis.2016.09.003","article-title":"Exome Sequencing Identified CCER2 as a Novel Candidate Gene for Moyamoya Disease","volume":"26","author":"M Mukawa","year":"2017","journal-title":"Journal of stroke and cerebrovascular diseases: the official journal of National Stroke Association"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.freeradbiomed.2016.06.002","article-title":"Neurofibromin is a novel regulator of Ras-induced reactive oxygen species production in mice and humans","volume":"97","author":"WK Bessler","year":"2016","journal-title":"Free radical biology & medicine"},{"issue":"6","key":"ref41","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1016\/j.celrep.2013.08.011","article-title":"Nf1 loss and Ras hyperactivation in oligodendrocytes induce NOS-driven defects in myelin and vasculature","volume":"4","author":"DA Mayes","year":"2013","journal-title":"Cell reports"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0200446","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2018,10,22]],"date-time":"2018-10-22T10:34:40Z","timestamp":1540204480000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0200446"}},"subtitle":[],"editor":[{"given":"Obul Reddy","family":"Bandapalli","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2018,7,12]]},"references-count":41,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2018,7,12]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0200446","relation":{},"ISSN":["1932-6203"],"issn-type":[{"type":"electronic","value":"1932-6203"}],"subject":[],"published":{"date-parts":[[2018,7,12]]}}}