Further delineation of neuropsychiatric findings in Tatton-Brown-Rahman syndrome due to disease-causing variants in DNMT3A: seven new patients.
Journal
European journal of human genetics : EJHG
ISSN: 1476-5438
Titre abrégé: Eur J Hum Genet
Pays: England
ID NLM: 9302235
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
04
02
2019
accepted:
02
07
2019
revised:
20
06
2019
pubmed:
7
11
2019
medline:
1
5
2021
entrez:
6
11
2019
Statut:
ppublish
Résumé
Tatton-Brown-Rahman (TBRS) syndrome is a recently described overgrowth syndrome caused by loss of function variants in the DNMT3A gene. This gene encodes for a DNA methyltransferase 3 alpha, which is involved in epigenetic regulation, especially during embryonic development. Somatic variants in DNMT3A have been widely studied in different types of tumors, including acute myeloid leukemia, hematopoietic, and lymphoid cancers. Germline gain-of-function variants in this gene have been recently implicated in microcephalic dwarfism. Common clinical features of patients with TBRS include tall stature, macrocephaly, intellectual disability (ID), and a distinctive facial appearance. Differential diagnosis of TBRS comprises Sotos, Weaver, and Malan Syndromes. The majority of these disorders present other clinical features with a high clinical overlap, making necessary a molecular confirmation of the clinical diagnosis. We here describe seven new patients with variants in DNMT3A, four of them with neuropsychiatric disorders, including schizophrenia and psychotic behavior. In addition, one of the patients has developed a brain tumor in adulthood. This patient has also cerebral atrophy, aggressive behavior, ID, and abnormal facial features. Clinical evaluation of this group of patients should include a complete neuropsychiatric assessment together with psychological support in order to detect and manage abnormal behaviors such as aggressiveness, impulsivity, and attention deficit-hyperactivity disorder. TBRS should be suspected in patients with overgrowth, ID, tall stature, and macrocephaly, who also have some neuropsychiatric disorders without any genetic defects in the commonest overgrowth disorders. Molecular confirmation in these patients is mandatory.
Identifiants
pubmed: 31685998
doi: 10.1038/s41431-019-0485-3
pii: 10.1038/s41431-019-0485-3
pmc: PMC7080728
doi:
Substances chimiques
DNMT3A protein, human
0
DNA (Cytosine-5-)-Methyltransferases
EC 2.1.1.37
DNA Methyltransferase 3A
EC 2.1.1.37
Types de publication
Case Reports
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
469-479Subventions
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : PI15/1481
Pays : International
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : FIS PI15/01481
Pays : International
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : FIS PI15/01481
Pays : International
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : PI15/1481
Pays : International
Investigateurs
Alberto L Rosa
(AL)
Aleixandre Blanquer
(A)
Alfredo García Alix
(AG)
Alfredo Santana
(A)
Alicia Delicado
(A)
Almudena Alonso
(A)
Amaya Rodríguez
(A)
Amparo Sanchis
(A)
Ana Moreno
(A)
Ana Patiño García
(AP)
Ana Vega
(A)
Analía Bredani
(A)
Andrea Paula Solari
(AP)
Andrea Villavicencio
(A)
Angelina Acosta
(A)
Aníbal Nieto
(A)
Anna María Cueto González
(AMC)
Antonio Baldellon
(A)
Antonio González Meneses
(AG)
Antonio Martínez Carrascal
(AM)
Aranzazu Díaz de Bustamante
(AD)
Arteche Ocasar
(A)
Blanca Gener
(B)
Blasco González
(B)
Boris Groisman
(B)
Bradford Coffee
(B)
Carlos Alcalde Martín
(CA)
Carmen Aragón Fernández
(CA)
Carmen Benito
(C)
Carmen González Armengod
(CG)
Carmen Martín Seisdedos
(CM)
Carmen Roche
(C)
Claudia Arberas
(C)
Claudia Perandones
(C)
Claudia Toledo Pacheco
(CT)
Claudio Contessotto
(C)
Cristina Olivas
(C)
Daniel Armenta
(D)
Denise Cavalcanti
(D)
Dolores Elorza
(D)
Eduardo Castilla
(E)
Elena Zamora
(E)
Elisa Zambrano
(E)
Elisabeth Steichen
(E)
Encarna Guillén Navarro
(EG)
Enrique Caro Cruz
(EC)
Enrique Galán Gómez
(EG)
Enriqueta Román
(E)
Ernesto Goldschmidt
(E)
Esteban Marfil
(E)
Esther Gean
(E)
Eugenia Antolín
(E)
F Javier Gascón Jiménez
(FJG)
Fco Javier Martínez Sarries
(FJM)
Feliciano Ramos
(F)
Fermina López Grondona
(FL)
Fernández Córdoba
(F)
Fernando Santos
(F)
Fernando Vargas
(F)
Francisco Martínez
(F)
Giovannucci Uzielli
(G)
Gloria Gacio
(G)
Graciela Mercado
(G)
Hamilton Cassinelli
(H)
Ieda Orioli
(I)
Ignacio Arroyo
(I)
Ignacio Díez López
(ID)
Ignacio Onsurbe Ramírez
(IO)
Ignacio Pascual Castroviejo
(IP)
Ignacio Pascual Pascual
(IP)
Ignacio Vázquez Rio
(IV)
Inés Bueno
(I)
Isabel Espejo Portero
(IE)
Isabel Lorda Sánchez
(IL)
Jaime Sánchez Del Pozo
(JS)
Jaume Campistol
(J)
Javier Arcas
(J)
Javier Fernández
(J)
Javier García Planells
(JG)
Javier López Pisón
(JL)
Jesús Barreiro
(J)
Jesús Del Valle Núñez
(JDV)
Joaquín Fernández Toral
(JF)
Joaquín Ramírez
(J)
Jordi Rosell
(J)
Jorge Vilaplana
(J)
José Carlos Cabral de Almeida
(JCC)
José Ignacio Labarta
(JI)
José L Herranz
(JL)
José Luis Fernández Luna
(JLF)
José Luis Fuster
(JL)
José M Díaz
(JM)
José M Gairi
(JM)
José Miguel García Sagredo
(JMG)
Juan A Piñero
(JA)
Juan Carlos López Gutiérrez
(JCL)
Juan Manuel Fernández
(JM)
Juan P López Siguero
(JPL)
Juan Tovar
(J)
Judith Armstrong
(J)
Julián Lara
(J)
Laura Rodríguez Leandro Soriano
(LRL)
Leila Cardoso
(L)
Leonor Arranz
(L)
Liliana De Alba
(L)
Loreta Cimbalistiene
(L)
Loreto Martorell
(L)
Luis González Gutiérrez Solana
(LGG)
Luis Pérez Jurado
(LP)
M Asunción López Ariztegui
(MAL)
M Antonia Molina
(MA)
M Cruz García
(MC)
M Ferrer Lozano
(MF)
M Jesús Alija Merillas
(MJA)
M Luisa Martínez-Frías
(ML)
M Rocío Jadraque
(MR)
Mª Asunción García Pérez
(MAG)
Mª Montserrat Rodríguez Pedreira
(MMR)
Mª Nieves Martínez Guardia
(MNM)
Mª Pilar Ribate
(MP)
Mª Teresa González López
(MTG)
Mª Teresa Moral Pumarega
(MTM)
Mabel Segovia
(M)
Macarena Lizama
(M)
Manuel J Lorente
(MJ)
Manuel Pombo
(M)
Margarita Martínez
(M)
Margarita Tabernero
(M)
María Antonia Ramos
(MA)
María Ballesta
(M)
María Belar
(M)
María Jesús Lautre
(MJ)
Marta Cruz
(M)
Mercedes Artigas
(M)
Mercedes Villanueva
(M)
Meritxell Torrabías
(M)
Miguel Del Campo
(M)
Miguel Tomás Vila
(MT)
Miguel Urioste
(M)
Mónica Rosello
(M)
Nazneen Rahman
(N)
Nik Kantaputra
(N)
Pablo Prieto Matos
(PP)
Paloma Dorao
(P)
Paula Casano
(P)
Paula Lalaguna Mallada
(PL)
Pedro Olivares
(P)
Pilar Tirado
(P)
Pricila Bernardi
(P)
Rafael Camino León
(RC)
Ramón Cañete
(R)
Ramón Gaztañaga
(R)
Ramón Velazquez
(R)
Ramón Vidal Samahuja
(RV)
Raquel Pérez Delgado
(RP)
Raquel Sáez Villaverde
(RS)
Ricardo Gracia
(R)
Richard Scott
(R)
Rita Valdez
(R)
Rosa Arteaga
(R)
Rosa Cedeño
(R)
Rosario Cazorla
(R)
Rosario Marín Iglesias
(RM)
Rubén Bronberg
(R)
Salvador Climent
(S)
Santiago Conde Barreiro
(SC)
Seema Kapoor
(S)
Selma Vázquez Martín
(SV)
Sixto García Miñaur
(SG)
Soledad Kleppe
(S)
Sonia Santillán
(S)
Teresa Calvo
(T)
Teresa Vendrell
(T)
V López González
(VL)
Vanesa López
(V)
Vanesa Lotersztein
(V)
Vanesa Méndez
(V)
Vicente Albiach
(V)
Víctor M Navas López
(VMN)
Virginia Soler
(V)
Viviana Cosentino
(V)
Yoko Aoki
(Y)
Références
Lapunzina P. Risk of tumorigenesis in overgrowth syndromes: a comprehensive review. Am J Med Genet C Semin Med Genet. 2005;137C:53–71.
pubmed: 16010678
doi: 10.1002/ajmg.c.30064
Tatton-Brown K, Seal S, Ruark E, Harmer J, Ramsay E, Del Vecchio Duarte S, et al. Mutations in the DNA methyltransferase gene DNMT3A cause an overgrowth syndrome with intellectual disability. Nat Genet. 2014;46:385–8.
pubmed: 24614070
pmcid: 3981653
doi: 10.1038/ng.2917
Lemire G, Gauthier J, Soucy JF, Delrue MA. A case of familial transmission of the newly described DNMT3A-overgrowth syndrome. Am J Med Genet Part A. 2017;173:1887–90.
pubmed: 28449304
doi: 10.1002/ajmg.a.38119
Lyko F. The DNA methyltransferase family: a versatile toolkit for epigenetic regulation. Nat Rev Genet. 2018;19:81–92.
pubmed: 29033456
doi: 10.1038/nrg.2017.80
Rinaldi L, Datta D, Serrat J, Morey L, Solanas G, Avgustinova A, et al. Dnmt3a and Dnmt3b associate with enhancers to regulate human epidermal stem cell homeostasis. Cell Stem Cell. 2016;19:491–501.
pubmed: 27476967
doi: 10.1016/j.stem.2016.06.020
Melberg A, Hetta J, Dahl N, Nennesmo I, Bengtsson M, Wibom R, et al. Autosomal dominant cerebellar ataxia deafness and narcolepsy. J Neurol Sci. 1995;134:119–29.
pubmed: 8747854
doi: 10.1016/0022-510X(95)00228-0
Winkelmann J, Lin L, Schormair B, Kornum BR, Faraco J, Plazzi G, et al. Mutations in DNMT1 cause autosomal dominant cerebellar ataxia, deafness and narcolepsy. Hum Mol Genet. 2012;21:2205–10.
pubmed: 22328086
pmcid: 3465691
doi: 10.1093/hmg/dds035
Klein CJ, Botuyan MV, Wu Y, Ward CJ, Nicholson GA, Hammans S, et al. Mutations in DNMT1 cause hereditary sensory neuropathy with dementia and hearing loss. Nat Genet. 2011;43:595–600.
pubmed: 21532572
pmcid: 3102765
doi: 10.1038/ng.830
Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999;99:247–57.
pubmed: 10555141
doi: 10.1016/S0092-8674(00)81656-6
Tatton-Brown K, Zachariou A, Loveday C, Renwick A, Mahamdallie S, Aksglaede L, et al. The tatton-brown-rahman syndrome: a clinical study of 55 individuals with de novo constitutive DNMT3A variants. Wellcome Open Res. 2018;3:46.
pubmed: 29900417
pmcid: 5964628
doi: 10.12688/wellcomeopenres.14430.1
Okamoto N, Toribe Y, Shimojima K, Yamamoto T. Tatton-Brown-Rahman syndrome due to 2p23 microdeletion. Am J Med Genet Part A. 2016;170A:1339–42.
pubmed: 26866722
doi: 10.1002/ajmg.a.37588
Ley TJ, Ding L, Walter MJ, McLellan MD, Lamprecht T, Larson DE, et al. DNMT3A mutations in acute myeloid leukemia. New Engl J Med. 2010;363:2424–33.
pubmed: 21067377
doi: 10.1056/NEJMoa1005143
Yamashita Y, Yuan J, Suetake I, Suzuki H, Ishikawa Y, Choi YL, et al. Array-based genomic resequencing of human leukemia. Oncogene. 2010;29:3723–31.
pubmed: 20400977
doi: 10.1038/onc.2010.117
Emperle M, Rajavelu A, Kunert S, Arimondo PB, Reinhardt R, Jurkowska RZ, et al. The DNMT3A R882H mutant displays altered flanking sequence preferences. Nucleic acids Res. 2018;46:3130–9.
pubmed: 29518238
pmcid: 5887309
doi: 10.1093/nar/gky168
Hollink I, van den Ouweland AMW, Beverloo HB, Arentsen-Peters S, Zwaan CM, Wagner A. Acute myeloid leukaemia in a case with Tatton-Brown-Rahman syndrome: the peculiar DNMT3A R882 mutation. J Med Genet. 2017;54:805–8.
pubmed: 28432085
doi: 10.1136/jmedgenet-2017-104574
Shen W, Heeley JM, Carlston CM, Acuna-Hidalgo R, Nillesen WM, Dent KM, et al. The spectrum of DNMT3A variants in Tatton-Brown-Rahman syndrome overlaps with that in hematologic malignancies. Am J Med Genet Part A. 2017;173:3022–8.
pubmed: 28941052
doi: 10.1002/ajmg.a.38485
Middleton FA, Mirnics K, Pierri JN, Lewis DA, Levitt P. Gene expression profiling reveals alterations of specific metabolic pathways in schizophrenia. J Neurosci. 2002;22:2718–29.
pubmed: 11923437
pmcid: 6758309
doi: 10.1523/JNEUROSCI.22-07-02718.2002
Saradalekshmi KR, Neetha NV, Sathyan S, Nair IV, Nair CM, Banerjee M. DNA methyl transferase (DNMT) gene polymorphisms could be a primary event in epigenetic susceptibility to schizophrenia. PloS ONE. 2014;9:e98182
pubmed: 24859147
pmcid: 4032286
doi: 10.1371/journal.pone.0098182
Zhubi A, Veldic M, Puri NV, Kadriu B, Caruncho H, Loza I, et al. An upregulation of DNA-methyltransferase 1 and 3a expressed in telencephalic GABAergic neurons of schizophrenia patients is also detected in peripheral blood lymphocytes. Schizophr Res. 2009;111:115–22.
pubmed: 19386473
pmcid: 3031301
doi: 10.1016/j.schres.2009.03.020
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–303.
pubmed: 20644199
pmcid: 2928508
doi: 10.1101/gr.107524.110
Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38:e164.
pubmed: 20601685
pmcid: 2938201
doi: 10.1093/nar/gkq603
Liu X, Wu C, Li C, Boerwinkle E. dbNSFPv3.0: a one-stop database of functional predictions and annotations for human nonsynonymous and splice-site SNVs. Hum Mutat. 2016;37:235–41.
pubmed: 26555599
pmcid: 4752381
doi: 10.1002/humu.22932
Lek M, Karczewski KJ, Minikel EV, Samocha KE, Banks E, Fennell T, et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature. 2016;536:285–91.
pubmed: 27535533
pmcid: 5018207
doi: 10.1038/nature19057
Richards S, Aziz N, Bale S, Bick D, Das S, Gastier-Foster J, et al. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet Med. 2015;17:405–24.
pubmed: 25741868
pmcid: 4544753
doi: 10.1038/gim.2015.30
Cancer Genome Atlas Research N. Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474:609–15.
doi: 10.1038/nature10166
Fickie MR, Lapunzina P, Gentile JK, Tolkoff-Rubin N, Kroshinsky D, Galan E, et al. Adults with Sotos syndrome: review of 21 adults with molecularly confirmed NSD1 alterations, including a detailed case report of the oldest person. Am J Med Genet Part A. 2011;155A:2105–11.
pubmed: 21834047
doi: 10.1002/ajmg.a.34156
Tatton-Brown K, Murray A, Hanks S, Douglas J, Armstrong R, Banka S, et al. Weaver syndrome and EZH2 mutations: Clarifying the clinical phenotype. Am J Med Genet Part A. 2013;161A:2972–80.
pubmed: 24214728
doi: 10.1002/ajmg.a.36229
Akawi N, Ben-Salem S, Lahti L, Partanen J, Ali BR, Al-Gazali L. A recessive syndrome of intellectual disability, moderate overgrowth, and renal dysplasia predisposing to Wilms tumor is caused by a mutation in FIBP gene. Am J Med Genet Part A. 2016;170:2111–8.
pubmed: 27183861
doi: 10.1002/ajmg.a.37741
Luscan A, Laurendeau I, Malan V, Francannet C, Odent S, Giuliano F, et al. Mutations in SETD2 cause a novel overgrowth condition. J Med Genet. 2014;51:512–7.
pubmed: 24852293
doi: 10.1136/jmedgenet-2014-102402
Soellner L, Begemann M, Mackay DJ, Gronskov K, Tumer Z, Maher ER, et al. Recent advances in imprinting disorders. Clin Genet. 2017;91:3–13.
pubmed: 27363536
doi: 10.1111/cge.12827
Heyn P, Logan CV, Fluteau A, Challis RC, Auchynnikava T, Martin CA, et al. Gain-of-function DNMT3A mutations cause microcephalic dwarfism and hypermethylation of Polycomb-regulated regions. Nat Genet. 2018;51:96–105.
pubmed: 30478443
pmcid: 6520989
doi: 10.1038/s41588-018-0274-x
Faludi G, Mirnics K. Synaptic changes in the brain of subjects with schizophrenia. Int J Dev Neurosci. 2011;29:305–9.
pubmed: 21382468
pmcid: 3074034
doi: 10.1016/j.ijdevneu.2011.02.013
Arion D, Unger T, Lewis DA, Levitt P, Mirnics K. Molecular evidence for increased expression of genes related to immune and chaperone function in the prefrontal cortex in schizophrenia. Biol Psychiatry. 2007;62:711–21.
pubmed: 17568569
pmcid: 2080683
doi: 10.1016/j.biopsych.2006.12.021
Hashimoto T, Arion D, Unger T, Maldonado-Aviles JG, Morris HM, Volk DW, et al. Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol psychiatry. 2008;13:147–61.
pubmed: 17471287
doi: 10.1038/sj.mp.4002011
Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD, et al. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci USA. 2001;98:4746–51.
pubmed: 11296301
doi: 10.1073/pnas.081071198
pmcid: 31905
Guidotti A, Ruzicka W, Grayson DR, Veldic M, Pinna G, Davis JM, et al. S-adenosyl methionine and DNA methyltransferase-1 mRNA overexpression in psychosis. Neuroreport. 2007;18:57–60.
pubmed: 17259861
doi: 10.1097/WNR.0b013e32800fefd7
Karen C, Rajan KE. Social behaviour and epigenetic status in adolescent and adult rats: the contribution of early-life stressful social experience. Cell Mol Neurobiol. 2019;39:371–85.
pubmed: 30710320
doi: 10.1007/s10571-019-00655-x
Xin B, Cruz Marino T, Szekely J, Leblanc J, Cechner K, Sency V, et al. Novel DNMT3A germline mutations are associated with inherited Tatton-Brown-Rahman syndrome. Clin Genet. 2017;91:623–8.
pubmed: 27701732
doi: 10.1111/cge.12878
Yang Y, Muzny DM, Xia F, Niu Z, Person R, Ding Y, et al. Molecular findings among patients referred for clinical whole-exome sequencing. JAMA. 2014;312:1870–9.
pubmed: 25326635
pmcid: 4326249
doi: 10.1001/jama.2014.14601
Yang Y, Muzny DM, Reid JG, Bainbridge MN, Willis A, Ward PA, et al. Clinical whole-exome sequencing for the diagnosis of mendelian disorders. New Engl J Med. 2013;369:1502–11.
pubmed: 24088041
doi: 10.1056/NEJMoa1306555
Tarailo-Graovac M, Shyr C, Ross CJ, Horvath GA, Salvarinova R, Ye XC, et al. Exome sequencing and the management of neurometabolic disorders. New Engl J Med. 2016;374:2246–55.
pubmed: 27276562
doi: 10.1056/NEJMoa1515792
Posey JE, Harel T, Liu P, Rosenfeld JA, James RA, Coban Akdemir ZH, et al. Resolution of disease phenotypes resulting from multilocus genomic variation. New Engl J Med. 2017;376:21–31.
pubmed: 27959697
doi: 10.1056/NEJMoa1516767