NF1 patient missense variants predict a role for ATM in modifying neurofibroma initiation.


Journal

Acta neuropathologica
ISSN: 1432-0533
Titre abrégé: Acta Neuropathol
Pays: Germany
ID NLM: 0412041

Informations de publication

Date de publication:
01 2020
Historique:
received: 20 05 2019
accepted: 15 10 2019
revised: 11 10 2019
pubmed: 31 10 2019
medline: 20 1 2021
entrez: 31 10 2019
Statut: ppublish

Résumé

In Neurofibromatosis type 1, NF1 gene mutations in Schwann cells (SC) drive benign plexiform neurofibroma (PNF), and no additional SC changes explain patient-to-patient variability in tumor number. Evidence from twin studies suggests that variable expressivity might be caused by unidentified modifier genes. Whole exome sequencing of SC and fibroblast DNA from the same resected PNFs confirmed biallelic SC NF1 mutations; non-NF1 somatic SC variants were variable and present at low read number. We identified frequent germline variants as possible neurofibroma modifier genes. Genes harboring variants were validated in two additional cohorts of NF1 patients and by variant burden test. Genes including CUBN, CELSR2, COL14A1, ATR and ATM also showed decreased gene expression in some neurofibromas. ATM-relevant DNA repair defects were also present in a subset of neurofibromas with ATM variants, and in some neurofibroma SC. Heterozygous ATM G2023R or homozygous S707P variants reduced ATM protein expression in heterologous cells. In mice, genetic Atm heterozygosity promoted Schwann cell precursor self-renewal and increased tumor formation in vivo, suggesting that ATM variants contribute to neurofibroma initiation. We identify germline variants, rare in the general population, overrepresented in NF1 patients with neurofibromas. ATM and other identified genes are candidate modifiers of PNF pathogenesis.

Identifiants

pubmed: 31664505
doi: 10.1007/s00401-019-02086-w
pii: 10.1007/s00401-019-02086-w
pmc: PMC7243727
mid: NIHMS1541618
doi:

Substances chimiques

Ataxia Telangiectasia Mutated Proteins EC 2.7.11.1

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

157-174

Subventions

Organisme : NINDS NIH HHS
ID : R37 NS083580
Pays : United States

Références

Am J Med Genet A. 2017 Mar;173(3):647-653
pubmed: 27862945
PLoS One. 2015 Sep 25;10(9):e0138568
pubmed: 26406308
Hum Mutat. 2006 Oct;27(10):1030-40
pubmed: 16941471
Pediatr Blood Cancer. 2012 Feb;58(2):173-80
pubmed: 21319287
Cancer Res. 1991 Sep 1;51(17):4671-6
pubmed: 1873812
EMBO Mol Med. 2009 Jul;1(4):236-48
pubmed: 20049725
Oncogene. 2017 Jun 1;36(22):3168-3177
pubmed: 28068329
Cell Rep. 2015 Nov 24;13(8):1598-609
pubmed: 26586426
Cell. 2015 Jul 16;162(2):391-402
pubmed: 26186192
J Pediatr. 2012 Mar;160(3):461-7
pubmed: 21996156
Neuromolecular Med. 2017 Mar;19(1):161-174
pubmed: 27664052
Neurogenetics. 2010 Oct;11(4):391-400
pubmed: 20358387
Philos Trans R Soc Lond B Biol Sci. 2017 Oct 5;372(1731):
pubmed: 28847820
Science. 2019 Mar 15;363(6432):1170-1175
pubmed: 30872516
J Clin Oncol. 2008 Jun 20;26(18):3057-62
pubmed: 18565893
J Nucleic Acids. 2010 Aug 03;2010:
pubmed: 20811597
Sci Rep. 2017 Sep 11;7(1):11144
pubmed: 28894253
Hum Pathol. 2017 Sep;67:1-10
pubmed: 28551330
J Biol Chem. 2006 Feb 17;281(7):3800-9
pubmed: 16316983
Science. 2013 Mar 29;339(6127):1546-58
pubmed: 23539594
Hum Mol Genet. 2009 Aug 1;18(15):2768-78
pubmed: 19417008
Clin Genet. 2016 Aug;90(2):105-17
pubmed: 26662178
Eur J Hum Genet. 2015 Jun;23(6):870-3
pubmed: 25293717
Lancet Oncol. 2016 Sep;17(9):1261-71
pubmed: 27498913
Am J Med Genet A. 2011 Mar;155A(3):478-85
pubmed: 21337692
Cancer Res. 1996 Sep 15;56(18):4130-3
pubmed: 8797579
FASEB J. 2012 Jul;26(7):2764-75
pubmed: 22441987
Cancer. 1982 Jan 15;49(2):273-87
pubmed: 7053827
Cancer Cell. 2008 Feb;13(2):105-16
pubmed: 18242511
Am J Hum Genet. 2003 May;72(5):1288-92
pubmed: 12660952
Biotechniques. 2017 Jan 1;62(1):18-30
pubmed: 28118812
Hum Mol Genet. 2003 Mar 15;12(6):685-98
pubmed: 12620974
Neuro Oncol. 2008 Aug;10(4):593-8
pubmed: 18559970
Sci Rep. 2017 Sep 6;7(1):10660
pubmed: 28878254
PLoS One. 2017 Jan 18;12(1):e0170348
pubmed: 28099461
Bioinformatics. 2011 Oct 1;27(19):2648-54
pubmed: 21828086
Oncogene. 2014 Jun 26;33(26):3351-60
pubmed: 23851492
Oncotarget. 2017 Jul 18;8(29):47574-47585
pubmed: 28548933
Br J Cancer. 2018 Jun;118(12):1539-1548
pubmed: 29695767
Genes Chromosomes Cancer. 2011 Dec;50(12):1021-32
pubmed: 21987445
PLoS Genet. 2012;8(4):e1002644
pubmed: 22511884
Mutat Res. 2007 Feb 3;615(1-2):98-110
pubmed: 17208258
Nat Rev Cancer. 2015 May;15(5):290-301
pubmed: 25877329
Oncogene. 2012 Mar 1;31(9):1117-29
pubmed: 21841825
Curr Genomics. 2008 May;9(3):137-46
pubmed: 19440510
Annu Rev Pathol. 2012;7:469-95
pubmed: 22077553
Am J Hum Genet. 1993 Aug;53(2):305-13
pubmed: 8328449
Am J Hum Genet. 2017 Aug 3;101(2):177-191
pubmed: 28777930
Cancer Cell. 2008 Feb;13(2):129-40
pubmed: 18242513
Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):925-30
pubmed: 11805335
Cancer Res. 2006 Nov 1;66(21):10505-12
pubmed: 17079472
Development. 2004 Nov;131(22):5599-612
pubmed: 15496445
Cell. 2017 Jun 29;170(1):17-33
pubmed: 28666118
Gene Ther. 2004 Jan;11(1):25-33
pubmed: 14681694
Sci Data. 2017 Apr 11;4:170045
pubmed: 28398289
Sarcoma. 2017;2017:7429697
pubmed: 28592921
Cell Rep. 2016 Mar 1;14(8):1979-90
pubmed: 26904939
J Neurosci Res. 2000 Sep 1;61(5):524-32
pubmed: 10956422
Cancer Discov. 2019 Jan;9(1):130-147
pubmed: 30348676
Proc Natl Acad Sci U S A. 2014 Jul 29;111(30):E3129-38
pubmed: 25024228
Cold Spring Harb Perspect Biol. 2013 Sep 01;5(9):
pubmed: 24003211
Nat Genet. 2017 Oct;49(10):1476-1486
pubmed: 28825726
Nat Commun. 2018 May 1;9(1):1744
pubmed: 29717121
Cell Stem Cell. 2008 Dec 4;3(6):658-69
pubmed: 19041782
Am J Epidemiol. 2000 Jan 1;151(1):33-40
pubmed: 10625171
Bioinformatics. 2014 Apr 1;30(7):1006-7
pubmed: 24351709
Cancer Cell. 2006 Dec;10(6):459-72
pubmed: 17157787
Proc Natl Acad Sci U S A. 2017 Jul 18;114(29):7665-7670
pubmed: 28659469
Cancer Res. 2017 Jan 15;77(2):509-519
pubmed: 28069802
Hum Mol Genet. 1999 Jan;8(1):69-79
pubmed: 9887333
J Med Genet. 2007 Feb;44(2):81-8
pubmed: 17105749
Hum Mutat. 2000;15(6):541-55
pubmed: 10862084
Oncotarget. 2014 Sep 30;5(18):8558-68
pubmed: 25261370
Genes Chromosomes Cancer. 1999 Dec;26(4):286-94
pubmed: 10534763
J Biol Chem. 1998 Mar 6;273(10):5858-68
pubmed: 9488723

Auteurs

Yanan Yu (Y)

Department of Experimental Hematology and Cancer Biology, Cincinati Children's Hospital Medical Center and Department of Pediatrics, University of Cincinanti School of Medicine, Cincinnati, OH, USA.
Graduate Program in Cancer and Cell Biology, University of Cincinnati, Cincinnati, OH, USA.

Kwangmin Choi (K)

Department of Experimental Hematology and Cancer Biology, Cincinati Children's Hospital Medical Center and Department of Pediatrics, University of Cincinanti School of Medicine, Cincinnati, OH, USA.

Jianqiang Wu (J)

Department of Experimental Hematology and Cancer Biology, Cincinati Children's Hospital Medical Center and Department of Pediatrics, University of Cincinanti School of Medicine, Cincinnati, OH, USA.

Paul R Andreassen (PR)

Department of Experimental Hematology and Cancer Biology, Cincinati Children's Hospital Medical Center and Department of Pediatrics, University of Cincinanti School of Medicine, Cincinnati, OH, USA.

Phillip J Dexheimer (PJ)

Division of Biomedical Informatics, Cincinnati Children's Hospital, Cincinnati, OH, USA.

Mehdi Keddache (M)

Division of Human Genetics, Cincinnati Children's Hospital Medical Center and the Department of Pediatrics, University of Cincinnati School of Medicine, Cincinnati, OH, USA.

Hilde Brems (H)

Department of Human Genetics, KU Leuven, Leuven, Belgium.

Robert J Spinner (RJ)

Department of Neurological Surgery, Mayo Clinic, Rochester, MN, USA.

Jose A Cancelas (JA)

Department of Experimental Hematology and Cancer Biology, Cincinati Children's Hospital Medical Center and Department of Pediatrics, University of Cincinanti School of Medicine, Cincinnati, OH, USA.
Hoxworth Blood Center, University of Cincinnati, Cincinnati, OH, USA.

Lisa J Martin (LJ)

Division of Human Genetics, Cincinnati Children's Hospital Medical Center and the Department of Pediatrics, University of Cincinnati School of Medicine, Cincinnati, OH, USA.

Margaret R Wallace (MR)

Department of Molecular Genetics and Microbiology, UF Genetics Institute, UF Health Cancer Center, University of Florida, Gainesville, FL, USA.

Eric Legius (E)

Department of Human Genetics, KU Leuven, Leuven, Belgium.

Kristine S Vogel (KS)

Department of Cell Systems and Anatomy, UT Health San Antonio, San Antonio, TX, USA.

Nancy Ratner (N)

Department of Experimental Hematology and Cancer Biology, Cincinati Children's Hospital Medical Center and Department of Pediatrics, University of Cincinanti School of Medicine, Cincinnati, OH, USA. Nancy.Ratner@cchmc.org.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH