Bi-allelic LoF NRROS Variants Impairing Active TGF-β1 Delivery Cause a Severe Infantile-Onset Neurodegenerative Condition with Intracranial Calcification.


Journal

American journal of human genetics
ISSN: 1537-6605
Titre abrégé: Am J Hum Genet
Pays: United States
ID NLM: 0370475

Informations de publication

Date de publication:
02 04 2020
Historique:
received: 25 12 2019
accepted: 26 02 2020
pubmed: 21 3 2020
medline: 12 5 2020
entrez: 21 3 2020
Statut: ppublish

Résumé

Negative regulator of reactive oxygen species (NRROS) is a leucine-rich repeat-containing protein that uniquely associates with latent transforming growth factor beta-1 (TGF- β1) and anchors it on the cell surface; this anchoring is required for activation of TGF-β1 in macrophages and microglia. We report six individuals from four families with bi-allelic variants in NRROS. All affected individuals had neurodegenerative disease with refractory epilepsy, developmental regression, and reduced white matter volume with delayed myelination. The clinical course in affected individuals began with normal development or mild developmental delay, and the onset of seizures occurred within the first year of life, followed by developmental regression. Intracranial calcification was detected in three individuals. The phenotypic features in affected individuals are consistent with those observed in the Nrros knockout mouse, and they overlap with those seen in the human condition associated with TGF-β1 deficiency. The disease-causing NRROS variants involve two significant functional NRROS domains. These variants result in aberrant NRROS proteins with impaired ability to anchor latent TGF-β1 on the cell surface. Using confocal microscopy in HEK293T cells, we demonstrate that wild-type and mutant NRROS proteins co-localize with latent TGF-β1 intracellularly. However, using flow cytometry, we show that our mutant NRROS proteins fail to anchor latent TGF-β1 at the cell surface in comparison to wild-type NRROS. Moreover, wild-type NRROS rescues the defect of our disease-associated mutants in presenting latent TGF-β1 to the cell surface. Taken together, our findings suggest that loss of NRROS function causes a severe childhood-onset neurodegenerative condition with features suggestive of a disordered response to inflammation.

Identifiants

pubmed: 32197075
pii: S0002-9297(20)30056-2
doi: 10.1016/j.ajhg.2020.02.014
pmc: PMC7118692
pii:
doi:

Substances chimiques

Latent TGF-beta Binding Proteins 0
NRROS protein, human 0
TGFB1 protein, human 0
Transforming Growth Factor beta1 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

559-569

Informations de copyright

Crown Copyright © 2020. Published by Elsevier Inc. All rights reserved.

Références

Mol Cell Neurosci. 2014 Jul;61:123-32
pubmed: 24886986
Front Cell Neurosci. 2013 Apr 19;7:49
pubmed: 23626522
Front Cell Neurosci. 2018 Dec 18;12:488
pubmed: 30618635
Nucleic Acids Res. 2008 Jan;36(Database issue):D190-5
pubmed: 18045787
PLoS One. 2019 Oct 10;14(10):e0213482
pubmed: 31600200
Eur J Hum Genet. 2019 Aug;27(8):1315-1319
pubmed: 30976112
Autophagy. 2011 Sep;7(9):1082-4
pubmed: 21606681
EMBO J. 2015 Jun 12;34(12):1612-29
pubmed: 25896511
BMC Genomics. 2009 Mar 23;10:122
pubmed: 19309509
Mol Cells. 2015 Oct;38(10):904-10
pubmed: 26442864
Neuron. 2003 Dec 18;40(6):1133-45
pubmed: 14687548
Nat Genet. 2018 Mar;50(3):344-348
pubmed: 29483653
Cell. 2018 Jun 28;174(1):156-171.e16
pubmed: 29909984
J Neurochem. 2015 Jul;134(1):125-34
pubmed: 25827682
Biochem Biophys Res Commun. 2013 Apr 26;434(1):28-34
pubmed: 23545260
J Cell Biochem. 1993 Dec;53(4):314-22
pubmed: 8300749
Nat Genet. 2013 Sep;45(9):1077-82
pubmed: 23913003
J Allergy Clin Immunol. 2018 Jun;141(6):2234-2248
pubmed: 29128673
J Neuroimmune Pharmacol. 2017 Sep;12(3):433-446
pubmed: 28429275
Histol Histopathol. 2011 Apr;26(4):519-30
pubmed: 21360445
Hum Mutat. 2009 Feb;30(2):E395-403
pubmed: 18972565
Mol Syst Biol. 2011 Oct 11;7:539
pubmed: 21988835
Prog Neurobiol. 1998 Jan;54(1):71-85
pubmed: 9460794
Nat Methods. 2015 Jan;12(1):7-8
pubmed: 25549265
Nat Neurosci. 2014 Jan;17(1):131-43
pubmed: 24316888
J Radiol Case Rep. 2019 Aug 31;13(8):1-18
pubmed: 31558966
Am J Med Genet A. 2015 Feb;167A(2):296-312
pubmed: 25604658
Neuroradiology. 1995 May;37(4):331-3
pubmed: 7666975
Nature. 2014 May 8;509(7499):235-9
pubmed: 24739962
Hum Mutat. 2015 Oct;36(10):915-21
pubmed: 26295439
J Clin Pathol. 2018 Aug;71(8):687-694
pubmed: 29455155
Nucleic Acids Res. 2014 Jan;42(Database issue):D222-30
pubmed: 24288371
Nat Biotechnol. 2019 Apr;37(4):420-423
pubmed: 30778233
J Exp Med. 2016 Jun 27;213(7):1163-74
pubmed: 27325888
Dev Med Child Neurol. 2014 Jul;56(7):612-26
pubmed: 24372060
Proteomics. 2007 Aug;7(16):2833-42
pubmed: 17640003
Intern Med. 2017 Sep 15;56(18):2507-2512
pubmed: 28824062
Clin Endocrinol (Oxf). 2012 Aug;77(2):200-6
pubmed: 22288727
PLoS One. 2017 Aug 11;12(8):e0183067
pubmed: 28800621
Science. 2018 Nov 23;362(6417):952-956
pubmed: 30361387
J Virol. 2011 May;85(9):4510-9
pubmed: 21345952
Genetics. 2012 Mar;190(3):841-54
pubmed: 22419077
Proteins. 2008 Feb 1;70(2):394-403
pubmed: 17680692
Nat Rev Immunol. 2015 Jul;15(7):429-40
pubmed: 26052098
Nat Immunol. 2017 Jun;18(6):633-641
pubmed: 28459434

Auteurs

Xiaomin Dong (X)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Paediatrics, University of Melbourne, Parkville, Victoria 3052, Australia.

Natalie B Tan (NB)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Paediatrics, University of Melbourne, Parkville, Victoria 3052, Australia; Victorian Clinical Genetics Services, Parkville, Victoria 3052, Australia.

Katherine B Howell (KB)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Paediatrics, University of Melbourne, Parkville, Victoria 3052, Australia; Department of Neurology, Royal Children's Hospital, Parkville, Victoria 3052, Australia.

Sabina Barresi (S)

Genetics and Rare Diseases Research Division, Ospedale Pediatrico Bambino Gesù, Rome 00146, Italy.

Jeremy L Freeman (JL)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Neurology, Royal Children's Hospital, Parkville, Victoria 3052, Australia.

Davide Vecchio (D)

Genetics and Rare Diseases Research Division, Ospedale Pediatrico Bambino Gesù, Rome 00146, Italy.

Maria Piccione (M)

Department of Science for Health Promotion and Mother and Child Care, Università degli Studi di Palermo, Palermo 90127, Italy.

Francesca Clementina Radio (FC)

Genetics and Rare Diseases Research Division, Ospedale Pediatrico Bambino Gesù, Rome 00146, Italy.

Daniel Calame (D)

Baylor College of Medicine, Houston, TX 77030, USA; Texas Children's Hospital, Houston, TX 77030, USA.

Shan Zong (S)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia.

Stefanie Eggers (S)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Victorian Clinical Genetics Services, Parkville, Victoria 3052, Australia.

Ingrid E Scheffer (IE)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Paediatrics, University of Melbourne, Parkville, Victoria 3052, Australia; Department of Neurology, Royal Children's Hospital, Parkville, Victoria 3052, Australia; Department of Medicine, University of Melbourne, Austin Health, Heidelberg, Victoria 3084, Australia.

Tiong Y Tan (TY)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Paediatrics, University of Melbourne, Parkville, Victoria 3052, Australia; Victorian Clinical Genetics Services, Parkville, Victoria 3052, Australia.

Nicole J Van Bergen (NJ)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Paediatrics, University of Melbourne, Parkville, Victoria 3052, Australia.

Marco Tartaglia (M)

Genetics and Rare Diseases Research Division, Ospedale Pediatrico Bambino Gesù, Rome 00146, Italy.

John Christodoulou (J)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Paediatrics, University of Melbourne, Parkville, Victoria 3052, Australia; Victorian Clinical Genetics Services, Parkville, Victoria 3052, Australia. Electronic address: john.christodoulou@mcri.edu.au.

Susan M White (SM)

Murdoch Children's Research Institute, Parkville, Victoria 3052, Australia; Department of Paediatrics, University of Melbourne, Parkville, Victoria 3052, Australia; Victorian Clinical Genetics Services, Parkville, Victoria 3052, Australia. Electronic address: sue.white@vcgs.org.au.

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