Genetic abnormalities in a large cohort of Coffin-Siris syndrome patients.


Journal

Journal of human genetics
ISSN: 1435-232X
Titre abrégé: J Hum Genet
Pays: England
ID NLM: 9808008

Informations de publication

Date de publication:
Dec 2019
Historique:
received: 15 07 2019
accepted: 25 08 2019
revised: 13 08 2019
pubmed: 19 9 2019
medline: 13 3 2020
entrez: 19 9 2019
Statut: ppublish

Résumé

Coffin-Siris syndrome (CSS, MIM#135900) is a congenital disorder characterized by coarse facial features, intellectual disability, and hypoplasia of the fifth digit and nails. Pathogenic variants for CSS have been found in genes encoding proteins in the BAF (BRG1-associated factor) chromatin-remodeling complex. To date, more than 150 CSS patients with pathogenic variants in nine BAF-related genes have been reported. We previously reported 71 patients of whom 39 had pathogenic variants. Since then, we have recruited an additional 182 CSS-suspected patients. We performed comprehensive genetic analysis on these 182 patients and on the previously unresolved 32 patients, targeting pathogenic single nucleotide variants, short insertions/deletions and copy number variations (CNVs). We confirmed 78 pathogenic variations in 78 patients. Pathogenic variations in ARID1B, SMARCB1, SMARCA4, ARID1A, SOX11, SMARCE1, and PHF6 were identified in 48, 8, 7, 6, 4, 1, and 1 patients, respectively. In addition, we found three CNVs including SMARCA2. Of particular note, we found a partial deletion of SMARCB1 in one CSS patient and we thoroughly investigated the resulting abnormal transcripts.

Identifiants

pubmed: 31530938
doi: 10.1038/s10038-019-0667-4
pii: 10.1038/s10038-019-0667-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1173-1186

Subventions

Organisme : Japan Agency for Medical Research and Development (AMED)
ID : JP19ek0109280, JP19dm0107090, JP19ek0109301, JP19ek0109348, and JP18kk020501

Références

Coffin GS, Siris E. Mental retardation with absent fifth fingernail and terminal phalanx. Am J Dis Child. 1960;1970:433–9.
Tsurusaki Y, Okamoto N, Ohashi H, Kosho T, Imai Y, Hibi-Ko Y, et al. Mutations affecting components of the SWI/SNF complex cause Coffin-Siris syndrome. Nat Genet. 2012;44:376–8.
pubmed: 22426308
Santen GW, Aten E, Sun Y, Almomani R, Gilissen C, Nielsen M, et al. Mutations in SWI/SNF chromatin remodeling complex gene ARID1B cause Coffin-Siris syndrome. Nat Genet. 2012;44:379–80.
pubmed: 22426309
Wieczorek D, Bogershausen N, Beleggia F, Steiner-Haldenstatt S, Pohl E, Li Y, et al. A comprehensive molecular study on Coffin-Siris and Nicolaides-Baraitser syndromes identifies a broad molecular and clinical spectrum converging on altered chromatin remodeling. Hum Mol Genet. 2013;22:5121–35.
pubmed: 23906836
Tsurusaki Y, Koshimizu E, Ohashi H, Phadke S, Kou I, Shiina M, et al. De novo SOX11 mutations cause Coffin-Siris syndrome. Nat Commun. 2014;5:4011.
pubmed: 24886874
Zweier C, Kraus C, Brueton L, Cole T, Degenhardt F, Engels H, et al. A new face of Borjeson-Forssman-Lehmann syndrome? De novo mutations in PHF6 in seven females with a distinct phenotype. J Med Genet. 2013;50:838–47.
pubmed: 24092917
Bramswig NC, Caluseriu O, Ludecke HJ, Bolduc FV, Noel NC, Wieland T, et al. Heterozygosity for ARID2 loss-of-function mutations in individuals with a Coffin-Siris syndrome-like phenotype. Hum Genet. 2017;136:297–305.
pubmed: 28124119
Vasileiou G, Vergarajauregui S, Endele S, Popp B, Buttner C, Ekici AB, et al. Mutations in the BAF-complex subunit DPF2 are associated with Coffin-Siris syndrome. Am J Hum Genet. 2018;102:468–79.
pubmed: 29429572 pmcid: 5985265
The Deciphering Developmental Disorders S, Fitzgerald TW, Gerety SS, Jones WD, van Kogelenberg M, King DA, et al. Large-scale discovery of novel genetic causes of developmental disorders. Nature. 2014;519:223.
Cherot E, Keren B, Dubourg C, Carre W, Fradin M, Lavillaureix A, et al. Using medical exome sequencing to identify the causes of neurodevelopmental disorders: experience of two clinical units and 216 patients. Clin Genet. 2018;93:567–76.
pubmed: 28708303
Okamoto N, Ehara E, Tsurusaki Y, Miyake N, Matsumoto N. Coffin-Siris syndrome and cardiac anomaly with a novel SOX11 mutation. Congenit Anom. 2018;58:105–07.
Jahani-Asl A, Cheng C, Zhang C, Bonni A. Pathogenesis of Borjeson–Forssman–Lehmann syndrome: Insights from PHF6 function. Neurobiol Dis. 2016;96:227–35.
pubmed: 27633282 pmcid: 5102843
Mani U, Sankareswaran AS, Goutham RNA, Mohan SS. SWI/SNF infobase—an exclusive information portal for SWI/SNF remodeling complex subunits. PloS One. 2017;12:e0184445.
pubmed: 28961249 pmcid: 5621669
Sokpor G, Xie Y, Rosenbusch J, Tuoc T. Chromatin remodeling BAF (SWI/SNF) complexes in neural development and disorders. Front Mol Neurosci. 2017;10:243.
pubmed: 28824374 pmcid: 5540894
Hota SK, Bruneau BG. ATP-dependent chromatin remodeling during mammalian development. Development. 2016;143:2882–97.
pubmed: 27531948 pmcid: 5004879
Bevilacqua A, Willis MS, Bultman SJ. SWI/SNF chromatin-remodeling complexes in cardiovascular development and disease. Cardiovascular Pathol. 2014;23:85–91.
Bogershausen N, Wollnik B. Mutational landscapes and phenotypic spectrum of SWI/SNF-related intellectual disability disorders. Front Mol Neurosci. 2018;11:252.
pubmed: 30123105 pmcid: 6085491
Tsurusaki Y, Okamoto N, Ohashi H, Mizuno S, Matsumoto N, Makita Y, et al. Coffin-Siris syndrome is a SWI/SNF complex disorder. Clin Genet. 2014;85:548–54.
pubmed: 23815551
Schrier SA, Bodurtha JN, Burton B, Chudley AE, Chiong MA, D’Avanzo MG, et al. The Coffin-Siris syndrome: a proposed diagnostic approach and assessment of 15 overlapping cases. Am J Med Genet Part A. 2012;158A:1865–76.
pubmed: 22711679
Vergano SS, Deardorff MA. Clinical features, diagnostic criteria, and management of Coffin-Siris syndrome. Am J Med Genet Part C Semin Med Genet. 2014;166C:252–6.
pubmed: 25169447
Campeau PM, Hennekam RC. DOORS syndrome: phenotype, genotype and comparison with Coffin-Siris syndrome. Am J Med Genet Part C Semin Med Genet. 2014;166C:327–32.
pubmed: 25169651
Van Houdt JK, Nowakowska BA, Sousa SB, van Schaik BD, Seuntjens E, Avonce N, et al. Heterozygous missense mutations in SMARCA2 cause Nicolaides–Baraitser syndrome. Nat Genet. 2012;44:445–9.
pubmed: 22366787
Sekiguchi F, Nasiri J, Sedghi M, Salehi M, Hosseinzadeh M, Okamoto N, et al. A novel homozygous DPH1 mutation causes intellectual disability and unique craniofacial features. J Hum Genet. 2018;63:487–91.
pubmed: 29410513
Aoi H, Lei M, Mizuguchi T, Nishioka N, Goto T, Miyama S, et al. Nonsense variants in STAG2 result in distinct sex-dependent phenotypes. J Hum Genet. 2019;64:487–92.
pubmed: 30765867
Nord AS, Lee M, King MC, Walsh T. Accurate and exact CNV identification from targeted high-throughput sequence data. BMC Genom. 2011;12:184.
Fromer M, Moran JL, Chambert K, Banks E, Bergen SE, Ruderfer DM, et al. Discovery and statistical genotyping of copy-number variation from whole-exome sequencing depth. Am J Hum Genet. 2012;91:597–607.
pubmed: 23040492 pmcid: 3484655
Al-Shamsi A, Hertecant JL, Souid AK, Al-Jasmi FA. Whole exome sequencing diagnosis of inborn errors of metabolism and other disorders in United Arab Emirates. Orphanet J Rare Dis. 2016;11:94.
pubmed: 27391121 pmcid: 4939014
Tsuchida N, Nakashima M, Kato M, Heyman E, Inui T, Haginoya K, et al. Detection of copy number variations in epilepsy using exome data. Clin Genet. 2018;93:577–87.
pubmed: 28940419
Bogershausen N, Gatinois V, Riehmer V, Kayserili H, Becker J, Thoenes M, et al. Mutation update for kabuki syndrome genes KMT2D and KDM6A and further delineation of X-linked kabuki syndrome subtype 2. Hum Mutat. 2016;37:847–64.
pubmed: 27302555
Miyake N, Abdel-Salam G, Yamagata T, Eid MM, Osaka H, Okamoto N, et al. Clinical features of SMARCA2 duplication overlap with Coffin-Siris syndrome. Am J Med Genet Part A. 2016;170:2662–70.
pubmed: 27264538
Zarate YA, Bhoj E, Kaylor J, Li D, Tsurusaki Y, Miyake N, et al. SMARCE1, a rare cause of Coffin-Siris syndrome: clinical description of three additional cases. Am J Med Genet Part A. 2016;170:1967–73.
pubmed: 27264197
Yu Y, Yao R, Wang L, Fan Y, Huang X, Hirschhorn J, et al. De novo mutations in ARID1B associated with both syndromic and non-syndromic short stature. BMC Genom. 2015;16:701.
Mignot C, Moutard ML, Rastetter A, Boutaud L, Heide S, Billette T, et al. ARID1B mutations are the major genetic cause of corpus callosum anomalies in patients with intellectual disability. Brain. 2016;139:e64.
pubmed: 27474218
Farwell KD, Shahmirzadi L, El-Khechen D, Powis Z, Chao EC, Tippin Davis B, et al. Enhanced utility of family-centered diagnostic exome sequencing with inheritance model-based analysis: results from 500 unselected families with undiagnosed genetic conditions. Genet Med. 2014;17:578.
pubmed: 25356970
Santen GW, Aten E, Vulto-van Silfhout AT, Pottinger C, van Bon BW, van Minderhout IJ, et al. Coffin-Siris syndrome and the BAF complex: genotype-phenotype study in 63 patients. Hum Mutat 2013;34:1519–28.
pubmed: 23929686
Lower KM, Turner G, Kerr BA, Mathews KD, Shaw MA, Gedeon AK, et al. Mutations in PHF6 are associated with Borjeson–Forssman–Lehmann syndrome. Nat Genet. 2002;32:661–5.
pubmed: 12415272
Tzschach A, Grasshoff U, Beck-Woedl S, Dufke C, Bauer C, Kehrer M, et al. Next-generation sequencing in X-linked intellectual disability. Eur J Hum Genet. 2015;23:1513–8.
pubmed: 25649377 pmcid: 4613482
Mangelsdorf M, Chevrier E, Mustonen A, Picketts DJ. Borjeson–Forssman–Lehmann syndrome due to a novel plant homeodomain zinc finger mutation in the PHF6 gene. J child Neurol. 2009;24:610–4.
pubmed: 19264739
Sen P, Luo J, Hada A, Hailu SG, Dechassa ML, Persinger J, et al. Loss of Snf5 induces formation of an aberrant SWI/SNF complex. Cell Rep. 2017;18:2135–47.
pubmed: 28249160 pmcid: 5424545
Holsten T, Bens S, Oyen F, Nemes K, Hasselblatt M, Kordes U, et al. Germline variants in SMARCB1 and other members of the BAF chromatin-remodeling complex across human disease entities: a meta-analysis. Eur J Hum Genet. 2018;26:1083–93.
pubmed: 29706634 pmcid: 6057970
Shibata M, Kanda M, Tanaka H, Umeda S, Miwa T, Shimizu D, et al. Overexpression of Derlin 3 is associated with malignant phenotype of breast cancer cells. Oncol Rep. 2017;38:1760–66.
pubmed: 28713959
Prochasson P, Neely KE, Hassan AH, Li B, Workman JL. Targeting activity is required for SWI/SNF function in vivo and is accomplished through two partially redundant activator-interaction domains. Mol Cell. 2003;12:983–90.
pubmed: 14580348
Ferreira ME, Prochasson P, Berndt KD, Workman JL, Wright AP. Activator-binding domains of the SWI/SNF chromatin remodeling complex characterized in vitro are required for its recruitment to promoters in vivo. FEBS J. 2009;276:2557–65.
pubmed: 19476494
Ulirsch JC, Verboon JM, Kazerounian S, Guo MH, Yuan D, Ludwig LS, et al. The genetic landscape of Diamond–Blackfan anemia. Am J Hum Genet. 2018;103:930–47.
pubmed: 30503522 pmcid: 6288280
Sanchis-Juan A, Stephens J, French CE, Gleadall N, Megy K, Penkett C, et al. Complex structural variants in Mendelian disorders: identification and breakpoint resolution using short- and long-read genome sequencing. Genome Med. 2018;10:95.
pubmed: 30526634 pmcid: 6286558
Miao H, Zhou J, Yang Q, Liang F, Wang D, Ma N, et al. Long-read sequencing identified a causal structural variant in an exome-negative case and enabled preimplantation genetic diagnosis. Hereditas. 2018;155:32.
pubmed: 30279644 pmcid: 6162922

Auteurs

Futoshi Sekiguchi (F)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Yoshinori Tsurusaki (Y)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.
Faculty of Nutritional Science, Sagami Women's University, Sagamihara, Kanagawa, Japan.

Nobuhiko Okamoto (N)

Department of Medical Genetics, Osaka Women's and Children's Hospital, Osaka, Japan.

Keng Wee Teik (KW)

Department of Genetics, Hospital Kuala Lumpur, Kuala Lumpur, Malaysia.

Seiji Mizuno (S)

Department of Clinical Genetics, Central Hospital, Aichi Developmental Disability Center, Kasugai, Japan.

Hiroshi Suzumura (H)

Department of Pediatrics, Dokkyo Medical University, Tochigi, Japan.

Bertrand Isidor (B)

CHU Nantes, Service de Genetique Medicale, Nantes, France.

Winnie Peitee Ong (WP)

Department of Genetics, Hospital Kuala Lumpur, Kuala Lumpur, Malaysia.

Muzhirah Haniffa (M)

Department of Genetics, Hospital Kuala Lumpur, Kuala Lumpur, Malaysia.

Susan M White (SM)

Victorian Clinical Genetics Services, Murdoch Children's Research Institute, Melbourne, Australia.
Department of Paediatrics, University of Melbourne, Melbourne, Australia.

Mari Matsuo (M)

Institute of Medical Genetics, Tokyo Women's Medical University, Tokyo, Japan.

Kayoko Saito (K)

Institute of Medical Genetics, Tokyo Women's Medical University, Tokyo, Japan.

Shubha Phadke (S)

Department of Medical Genetics, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India.

Tomoki Kosho (T)

Department of Medical Genetics, Shinshu University School of Medicine, Matsumoto, Japan.

Patrick Yap (P)

Genetic Health Service New Zealand, Auckland, New Zealand.
Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand.

Manisha Goyal (M)

Rare Disease Clinic, J K Lone Hospital, SMS Medical College, Jaipur, Rajasthan, India.

Lorne A Clarke (LA)

British Columbia Children's Hospital Research Institute, University of British Columbia, Vancouver, BC, Canada.

Rani Sachdev (R)

Centre for Clinical Genetics, Sydney Children's Hospital, Randwick, NSW, Australia.

George McGillivray (G)

Victorian Clinical Genetics Services, Murdoch Children's Research Institute, Melbourne, Australia.

Richard J Leventer (RJ)

Royal Children's Hospital Department of Neurology, Murdoch Children's Research Institute and University of Melbourne Department of Pediatrics, Parkville, 3052, Australia.

Chirag Patel (C)

Genetic Health Queensland, Royal Brisbane and Women's Hospital, Brisbane, QLD, Australia.

Takanori Yamagata (T)

Department of Pediatrics, Jichi Medical University, Tochigi, Japan.

Hitoshi Osaka (H)

Department of Pediatrics, Jichi Medical University, Tochigi, Japan.

Yoshiya Hisaeda (Y)

Department of Neonatology, Japanese Red Cross Medical Center, Tokyo, Japan.

Hirofumi Ohashi (H)

Division of Medical Genetics, Saitama Children's Medical Center, Saitama, Japan.

Kenji Shimizu (K)

Division of Medical Genetics, Saitama Children's Medical Center, Saitama, Japan.

Keisuke Nagasaki (K)

Department of Homeostatic Regulation and Development, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

Junpei Hamada (J)

Department of Pediatrics, Ehime University Graduate School of Medicine, Ehime, Japan.

Sumito Dateki (S)

Department of Pediatrics, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, Japan.

Takashi Sato (T)

Asahikawa-Kosei General Hospital, Hokkaido, Japan.

Yasutsugu Chinen (Y)

Department of Child Health and Welfare, Graduate School of Medicine, University of the Ryukyus, Nishihara, Japan.

Tomonari Awaya (T)

Department of Anatomy and Developmental Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Department of Pediatrics, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Takeo Kato (T)

Department of Pediatrics, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Kougoro Iwanaga (K)

Department of Pediatrics, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Masahiko Kawai (M)

Department of Pediatrics, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Takashi Matsuoka (T)

Department of General Pediatrics, Okinawa Prefectural Nanbu Medical Center and Children's Medical Center, Okinawa, Japan.

Yoshikazu Shimoji (Y)

Department of General Pediatrics, Okinawa Prefectural Nanbu Medical Center and Children's Medical Center, Okinawa, Japan.

Tiong Yang Tan (TY)

Victorian Clinical Genetics Services, Murdoch Children's Research Institute, Melbourne, Australia.
Department of Paediatrics, University of Melbourne, Melbourne, Australia.

Seema Kapoor (S)

Division of Genetics, Department of Pediatrics, Maulana Azad Medical College, New Delhi, India.

Nerine Gregersen (N)

Genetic Health Service New Zealand, Auckland, New Zealand.

Massimiliano Rossi (M)

Hospices Civils de Lyon, Service de Génétique, Centre de Référence Anomalies du Développement, and INSERM U1028, CNRS UMR5292, CRNL, GENDEV Team, UCBL1, Bron, France.

Mathieu Marie-Laure (M)

Hospices Civils de Lyon, Service de Génétique, Centre de Référence Anomalies du Développement, and INSERM U1028, CNRS UMR5292, CRNL, GENDEV Team, UCBL1, Bron, France.

Lesley McGregor (L)

South Australian Clinical Genetics Service, SA Pathology, Women's and Children's Hospital, Adelaide, Australia.

Kimihiko Oishi (K)

Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Lakshmi Mehta (L)

Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Greta Gillies (G)

Bruce Lefroy Centre for Genetic Health Research, Murdoch Children's Research Institute, Victoria, Australia.

Paul J Lockhart (PJ)

Bruce Lefroy Centre for Genetic Health Research, Murdoch Children's Research Institute, Victoria, Australia.

Kate Pope (K)

Bruce Lefroy Centre for Genetic Health Research, Murdoch Children's Research Institute, Victoria, Australia.

Anju Shukla (A)

Department of Medical Genetics, Kasturba Medical College, Manipal, Manipal Academy of Higher Education, Manipal, India.

Katta Mohan Girisha (KM)

Department of Medical Genetics, Kasturba Medical College, Manipal, Manipal Academy of Higher Education, Manipal, India.

Ghada M H Abdel-Salam (GMH)

Department of Clinical Genetics, Human Genetics and Genome Research Division, National Research Centre, Cairo, Egypt.

David Mowat (D)

Department of Medical Genetics, Sydney Children's Hospital, Sydney, NSW, Australia.

David Coman (D)

Department of Paediatrics, The Wesley Hospital, Brisbane, QLD, Australia.

Ok Hwa Kim (OH)

Department of Radiology, Ajou University Hospital, Suwon, Korea.

Marie-Pierre Cordier (MP)

Service de Genetique, Hospices Civils de Lyon, Bron, France.

Kate Gibson (K)

Genetic Health Service New Zealand, Christchurch Hospital, Christchurch, New Zealand.

Jeff Milunsky (J)

Center for Human Genetics Inc, Cambridge, MA, USA.

Jan Liebelt (J)

South Australian Clinical Genetics Services, Women's and Children's Hospital, North Adelaide, Australia.

Helen Cox (H)

West Midlands Regional Genetics Service, Birmingham Women's NHS Foundation Trust, Birmingham Women's Hospital, Edgbaston, Birmingham, B15 2TG, UK.

Salima El Chehadeh (S)

Service de Genetique Medicale, Hopital de Hautepierre, Strasbourg, France.

Annick Toutain (A)

Service de Genetique, CHRU de Tours, Tours, France.

Ken Saida (K)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Hiromi Aoi (H)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.
Department of Obstetrics and Gynecology, Juntendo University Faculty of Medicine, Tokyo, Japan.

Gaku Minase (G)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Naomi Tsuchida (N)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Kazuhiro Iwama (K)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Yuri Uchiyama (Y)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.
Department of Oncology, Yokohama City University Graduate School of Medicine, Yokohama, Japan.
Clinical Genetics Department, Yokohama City University Hospital, Yokohama, Kanagawa, Japan.

Toshifumi Suzuki (T)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.
Department of Obstetrics and Gynecology, Juntendo University Faculty of Medicine, Tokyo, Japan.

Kohei Hamanaka (K)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Yoshiteru Azuma (Y)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Atsushi Fujita (A)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Eri Imagawa (E)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Eriko Koshimizu (E)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Atsushi Takata (A)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Satomi Mitsuhashi (S)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Satoko Miyatake (S)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.
Clinical Genetics Department, Yokohama City University Hospital, Yokohama, Kanagawa, Japan.

Takeshi Mizuguchi (T)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Noriko Miyake (N)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan.

Naomichi Matsumoto (N)

Department of Human Genetics, Graduate school of medicine, Yokohama City University, Yokohama, Japan. naomat@yokohama-cu.ac.jp.

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