Biallelic pathogenic variants in roundabout guidance receptor 1 associate with syndromic congenital anomalies of the kidney and urinary tract.


Journal

Kidney international
ISSN: 1523-1755
Titre abrégé: Kidney Int
Pays: United States
ID NLM: 0323470

Informations de publication

Date de publication:
05 2022
Historique:
received: 24 02 2021
revised: 30 11 2021
accepted: 11 01 2022
pubmed: 2 3 2022
medline: 27 4 2022
entrez: 1 3 2022
Statut: ppublish

Résumé

Congenital anomalies of the kidney and urinary tract (CAKUT) represent the most common cause of chronic kidney failure in children. Despite growing knowledge of the genetic causes of CAKUT, the majority of cases remain etiologically unsolved. Genetic alterations in roundabout guidance receptor 1 (ROBO1) have been associated with neuronal and cardiac developmental defects in living individuals. Although Slit-Robo signaling is pivotal for kidney development, diagnostic ROBO1 variants have not been reported in viable CAKUT to date. By next-generation-sequencing methods, we identified six unrelated individuals and two non-viable fetuses with biallelic truncating or combined missense and truncating variants in ROBO1. Kidney and genitourinary manifestation included unilateral or bilateral kidney agenesis, vesicoureteral junction obstruction, vesicoureteral reflux, posterior urethral valve, genital malformation, and increased kidney echogenicity. Further clinical characteristics were remarkably heterogeneous, including neurodevelopmental defects, intellectual impairment, cerebral malformations, eye anomalies, and cardiac defects. By in silico analysis, we determined the functional significance of identified missense variants and observed absence of kidney ROBO1 expression in both human and murine mutant tissues. While its expression in multiple tissues may explain heterogeneous organ involvement, variability of the kidney disease suggests gene dosage effects due to a combination of null alleles with mild hypomorphic alleles. Thus, comprehensive genetic analysis in CAKUT should include ROBO1 as a new cause of recessively inherited disease. Hence, in patients with already established ROBO1-associated cardiac or neuronal disorders, screening for kidney involvement is indicated.

Identifiants

pubmed: 35227688
pii: S0085-2538(22)00157-0
doi: 10.1016/j.kint.2022.01.028
pmc: PMC10010616
mid: NIHMS1874348
pii:
doi:

Substances chimiques

Nerve Tissue Proteins 0
Receptors, Immunologic 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1039-1053

Subventions

Organisme : NICHD NIH HHS
ID : F30 HD097967
Pays : United States
Organisme : NIBIB NIH HHS
ID : T32 EB001026
Pays : United States
Organisme : NHGRI NIH HHS
ID : UM1 HG006542
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS105078
Pays : United States
Organisme : NHGRI NIH HHS
ID : K08 HG008986
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R01 GM060992
Pays : United States

Informations de copyright

Copyright © 2022 International Society of Nephrology. Published by Elsevier Inc. All rights reserved.

Références

J Clin Endocrinol Metab. 2017 Jul 1;102(7):2401-2406
pubmed: 28402530
Pediatr Nephrol. 2014 Dec;29(12):2403-10
pubmed: 25039018
BMC Bioinformatics. 2012 Aug 10;13:198
pubmed: 22883815
Pediatr Res. 2016 Jul;80(1):72-6
pubmed: 27002985
Nat Genet. 2019 Jan;51(1):117-127
pubmed: 30578417
Dev Cell. 2012 Nov 13;23(5):925-38
pubmed: 23153492
Kidney Int. 2013 Aug;84(2):327-37
pubmed: 23536131
Kidney Int. 2019 Aug;96(2):267-269
pubmed: 31331462
Nucleic Acids Res. 2019 Jan 8;47(D1):D886-D894
pubmed: 30371827
Hum Mutat. 2015 Oct;36(10):928-30
pubmed: 26220891
Pediatr Nephrol. 2009 Aug;24(8):1501-8
pubmed: 19350278
Kidney Int. 2016 Feb;89(2):476-86
pubmed: 26489027
Nat Commun. 2016 Mar 22;7:11103
pubmed: 27002738
Subcell Biochem. 2019;93:291-319
pubmed: 31939155
Kidney Int. 2009 Sep;76(5):528-33
pubmed: 19536081
Cell. 2019 Apr 4;177(2):272-285.e16
pubmed: 30853216
J Am Soc Nephrol. 2018 Jan;29(1):36-50
pubmed: 29079659
Nature. 2020 May;581(7809):434-443
pubmed: 32461654
J Clin Invest. 2018 Jan 2;128(1):4-15
pubmed: 29293093
J Chem Theory Comput. 2016 Dec 13;12(12):6201-6212
pubmed: 27766851
Cell. 2011 Sep 30;147(1):32-43
pubmed: 21962505
J Am Soc Nephrol. 2008 Apr;19(4):825-31
pubmed: 18235093
J Med Genet. 2017 Dec;54(12):825-829
pubmed: 28592524
J Chem Inf Model. 2019 Apr 22;59(4):1508-1514
pubmed: 30759982
Am J Hum Genet. 2007 Apr;80(4):616-32
pubmed: 17357069
Mol Cell Neurosci. 2002 Dec;21(4):534-45
pubmed: 12504588
Kidney Int. 2019 Jul;96(1):222-230
pubmed: 31027891
Structure. 2018 Feb 6;26(2):320-328.e4
pubmed: 29307485
Nucleic Acids Res. 2012 Jul;40(Web Server issue):W294-7
pubmed: 22649060
Hum Genet. 2015 Aug;134(8):905-16
pubmed: 26026792
Pediatr Neurol. 2017 May;70:70-74
pubmed: 28286008
Cell. 1998 Jan 23;92(2):205-15
pubmed: 9458045
J Clin Res Pediatr Endocrinol. 2019 Aug 26;12(2):212-217
pubmed: 31448886
Kidney Int. 2020 Oct;98(4):1020-1030
pubmed: 32450157
Clin Genet. 2018 Apr;93(4):860-869
pubmed: 29194579
Angiogenesis. 2018 May;21(2):237-249
pubmed: 29299781
Mech Dev. 2000 Jun;94(1-2):213-7
pubmed: 10842075
BMC Nephrol. 2016 Jul 26;17(1):98
pubmed: 27460642
Nat Rev Nephrol. 2015 Dec;11(12):720-31
pubmed: 26281895
J Hum Genet. 2019 Apr;64(4):341-346
pubmed: 30692597
Nat Med. 2015 May;21(5):483-91
pubmed: 25894826
Am J Hum Genet. 2018 Aug 2;103(2):171-187
pubmed: 30032986
Proteins. 2011 Mar;79(3):830-8
pubmed: 21287615
Science. 2004 Jun 4;304(5676):1509-13
pubmed: 15105459
Eur J Hum Genet. 2020 Sep;28(9):1243-1264
pubmed: 32376988
Proc Natl Acad Sci U S A. 2007 Sep 18;104(38):14923-8
pubmed: 17848514
Dev Dyn. 2021 Sep;250(9):1340-1357
pubmed: 33347679

Auteurs

Johannes Münch (J)

Department of Nephrology and Medical Intensive Care, Charité-Universitätsmedizin Berlin, Berlin, Germany; Division of Nephrology, University of Leipzig Medical Center, Leipzig, Germany.

Marie Engesser (M)

Division of Nephrology, University of Leipzig Medical Center, Leipzig, Germany.

Ria Schönauer (R)

Department of Nephrology and Medical Intensive Care, Charité-Universitätsmedizin Berlin, Berlin, Germany; Division of Nephrology, University of Leipzig Medical Center, Leipzig, Germany.

J Austin Hamm (JA)

East Tennessee Children's Hospital, Genetic Center, Knoxville, Tennessee, USA.

Christin Hartig (C)

Division of Nephrology, University of Leipzig Medical Center, Leipzig, Germany.

Elena Hantmann (E)

Department of Nephrology and Medical Intensive Care, Charité-Universitätsmedizin Berlin, Berlin, Germany; Division of Nephrology, University of Leipzig Medical Center, Leipzig, Germany.

Gulsen Akay (G)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, USA; Department of Pediatrics, University of Utah, Salt Lake, Utah, USA.

Davut Pehlivan (D)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, USA; Division of Neurology and Developmental Neuroscience, Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USA; Texas Children's Hospital, Houston, Texas, USA.

Tadahiro Mitani (T)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, USA.

Zeynep Coban Akdemir (Z)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, USA; Department of Epidemiology, Human Genetics, and Environmental Sciences, Human Genetics Center, School of Public Health, University of Texas Health Science Center at Houston, Houston, Texas, USA.

Beyhan Tüysüz (B)

Department of Pediatric Genetics, Istanbul University Cerrahpasa Medical Faculty, Istanbul, Turkey.

Toshihiko Shirakawa (T)

Department of Pediatrics, Nagasaki University Hospital, Nagasaki, Japan.

Sumito Dateki (S)

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

Laura R Claus (LR)

Department of Genetics, University Medical Center Utrecht, Utrecht, the Netherlands.

Albertien M van Eerde (AM)

Department of Genetics, University Medical Center Utrecht, Utrecht, the Netherlands.
Genomics England Research Consortium (GEL) - 100,000 Genomes Project, London, UK.

Thomas Smol (T)

Centre Hospitalier Universitaire de Lille, Institut de Génétique Médicale, Lille, France.

Louise Devisme (L)

Centre Hospitalier Universitaire de Lille, Institut de Pathologie, Lille, France.

Hélène Franquet (H)

Centre Hospitalier Universitaire de Lille, Institut de Pathologie, Lille, France.

Tania Attié-Bitach (T)

Laboratoire de biologie médicale multisites SeqOIA, Paris, France; Service de Médecine Génomique des Maladies Rares, APHP.Centre, Université de Paris, Paris, France.

Timo Wagner (T)

Medizinische Genetik Mainz, Limbach Genetics, Mainz, Germany.

Carsten Bergmann (C)

Medizinische Genetik Mainz, Limbach Genetics, Mainz, Germany; Department of Medicine, Nephrology, University Hospital Freiburg, Freiburg, Germany.

Anne Kathrin Höhn (AK)

Division of Pathology, University of Leipzig Medical Center, Leipzig, Germany.

Shirlee Shril (S)

Division of Nephrology, Boston Children's Hospital, Boston, USA.

Ari Pollack (A)

Division of Genetic Medicine, University of Washington, Seattle, Washington, USA.

Tara Wenger (T)

Division of Genetic Medicine, University of Washington, Seattle, Washington, USA.

Abbey A Scott (AA)

Division of Genetic Medicine, Seattle Children's Hospital, Seattle, Washington, USA.

Sarah Paolucci (S)

Department of Laboratory Medicine and Pathology, University of Washington, Seattle, Washington, USA.

Jillian Buchan (J)

Department of Laboratory Medicine and Pathology, University of Washington, Seattle, Washington, USA.

George C Gabriel (GC)

Department of Developmental Biology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

Jennifer E Posey (JE)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, USA.

James R Lupski (JR)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, USA; Texas Children's Hospital, Houston, Texas, USA; Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USA.

Florence Petit (F)

Centre Hospitalier Universitaire de Lille, Clinique de Génétique Guy Fontaine, Lille, France.

Andrew A McCarthy (AA)

European Molecular Biology Laboratory, Grenoble, France.

Gregory J Pazour (GJ)

Program in Molecular Medicine, University of Massachusetts Medical School, Biotech II, Worcester, USA.

Cecilia W Lo (CW)

Department of Developmental Biology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA. Electronic address: cel36@pitt.edu.

Bernt Popp (B)

Institute for Human Genetics, University of Leipzig Medical Center, Leipzig, Germany. Electronic address: bernt.popp@medizin.uni.leipzig.de.

Jan Halbritter (J)

Department of Nephrology and Medical Intensive Care, Charité-Universitätsmedizin Berlin, Berlin, Germany; Division of Nephrology, University of Leipzig Medical Center, Leipzig, Germany. Electronic address: jan.halbritter@charite.de.

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