Home LiteratureArticle Details
PMID: 20890276 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mutations in GRIN2A and GRIN2B encoding regulatory subunits of NMDA receptors cause variable neurodevelopmental phenotypes.

Nature genetics ·Vol. 42 ·No. 11 ·2010-11-00 ·Pages 1021-6

Endele S, Rosenberger G, Geider K, Popp B, Tamer C, Stefanova I, Milh M, Kortüm F, Fritsch A, Pientka FK, Hellenbroich Y, Kalscheuer VM, Kohlhase J, Moog U, Rappold G, Rauch A, Ropers HH, von Spiczak S, Tönnies H, Villeneuve N, Villard L, Zabel B, Zenker M, Laube B, Reis A, Wieczorek D, Van Maldergem L, Kutsche K

Abstract

N-methyl-D-aspartate (NMDA) receptors mediate excitatory neurotransmission in the mammalian brain. Two glycine-binding NR1 subunits and two glutamate-binding NR2 subunits each form highly Ca²(+)-permeable cation channels which are blocked by extracellular Mg²(+) in a voltage-dependent manner. Either GRIN2B or GRIN2A, encoding the NMDA receptor subunits NR2B and NR2A, was found to be disrupted by chromosome translocation breakpoints in individuals with mental retardation and/or epilepsy. Sequencing of GRIN2B in 468 individuals with mental retardation revealed four de novo mutations: a frameshift, a missense and two splice-site mutations. In another cohort of 127 individuals with idiopathic epilepsy and/or mental retardation, we discovered a GRIN2A nonsense mutation in a three-generation family. In a girl with early-onset epileptic encephalopathy, we identified the de novo GRIN2A mutation c.1845C>A predicting the amino acid substitution p.N615K. Analysis of NR1-NR2A(N615K) (NR2A subunit with the p.N615K alteration) receptor currents revealed a loss of the Mg²(+) block and a decrease in Ca²(+) permeability. Our findings suggest that disturbances in the neuronal electrophysiological balance during development result in variable neurological phenotypes depending on which NR2 subunit of NMDA receptors is affected.

MeSH Terms
Adolescent Adult Amino Acid Substitution Calcium/metabolism Child Child, Preschool Epilepsy/genetics Female Humans Intellectual Disability/genetics Magnesium/metabolism Male Mutation Nervous System Diseases/genetics Pedigree Polymorphism, Single Nucleotide Protein Subunits/genetics Receptors, N-Methyl-D-Aspartate/genetics Transcription, Genetic
Chemicals
NR2B NMDA receptor Protein Subunits Receptors, N-Methyl-D-Aspartate Magnesium Calcium N-methyl D-aspartate receptor subtype 2A
Authors & Affiliations
28 authors, click to expand affiliations / ORCID
Endele Sabine
Institute of Human Genetics, University of Erlangen-Nuremberg, Erlangen, Germany.
Rosenberger Georg
Geider Kirsten
Popp Bernt
Tamer Ceyhun
Stefanova Irina
Milh Mathieu
Kortüm Fanny
Fritsch Angela
Pientka Friederike K
Hellenbroich Yorck
Kalscheuer Vera M
Kohlhase Jürgen
Moog Ute
Rappold Gudrun
Rauch Anita
Ropers Hans-Hilger
von Spiczak Sarah
Tönnies Holger
Villeneuve Nathalie
Villard Laurent
Zabel Bernhard
Zenker Martin
Laube Bodo
Reis André
Wieczorek Dagmar
Van Maldergem Lionel
Kutsche Kerstin
References (38)
38 references, click to expand
  1. An intramembrane aromatic network determines pentameric assembly of Cys-loop receptors.
    Nat Struct Mol Biol. 2010 Jan;17(1):90-8 PMID: 20023641
  2. Comparative genomic hybridization using oligonucleotide microarrays and total genomic DNA.
    Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17765-70 PMID: 15591353
  3. Genetic enhancement of memory and long-term potentiation but not CA1 long-term depression in NR2B transgenic rats.
    PLoS One. 2009 Oct 19;4(10):e7486 PMID: 19838302
  4. NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome.
    Nat Genet. 2004 Jun;36(6):636-41 PMID: 15146185
  5. Adjacent asparagines in the NR2-subunit of the NMDA receptor channel control the voltage-dependent block by extracellular Mg2+.
    J Physiol. 1998 Jan 1;506 ( Pt 1):13-32 PMID: 9481670
  6. A possible association of responsiveness to adrenocorticotropic hormone with specific GRIN1 haplotypes in infantile spasms.
    Dev Med Child Neurol. 2010 Nov;52(11):1028-32 PMID: 20722663
  7. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders.
    Nat Rev Neurosci. 2007 Jun;8(6):413-26 PMID: 17514195
  8. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm.
    Nat Protoc. 2009;4(7):1073-81 PMID: 19561590
  9. Potentiation of Glycine-Gated NR1/NR3A NMDA Receptors Relieves Ca-Dependent Outward Rectification.
    Front Mol Neurosci. 2010 Mar 23;3:6 PMID: 20407581
  10. Cloning of the breakpoint of an X;21 translocation associated with Duchenne muscular dystrophy.
    Nature. 1985 Dec 19-1986 Jan 1;318(6047):672-5 PMID: 3001530
  11. Deletions in 16p13 including GRIN2A in patients with intellectual disability, various dysmorphic features, and seizure disorders of the rolandic region.
    Epilepsia. 2010 Sep;51(9):1870-3 PMID: 20384727
  12. Human non-synonymous SNPs: server and survey.
    Nucleic Acids Res. 2002 Sep 1;30(17):3894-900 PMID: 12202775
  13. Formation of NR1/NR2 and NR1/NR3 heterodimers constitutes the initial step in N-methyl-D-aspartate receptor assembly.
    J Biol Chem. 2008 Jan 4;283(1):37-46 PMID: 17959602
  14. Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit.
    Neuron. 1997 Mar;18(3):493-503 PMID: 9115742
  15. Use of non-crystallographic symmetry in protein structure refinement.
    Acta Crystallogr D Biol Crystallogr. 1996 Jul 1;52(Pt 4):842-57 PMID: 15299650
  16. SNAP: predict effect of non-synonymous polymorphisms on function.
    Nucleic Acids Res. 2007;35(11):3823-35 PMID: 17526529
  17. NMDA receptor subunits: diversity, development and disease.
    Curr Opin Neurobiol. 2001 Jun;11(3):327-35 PMID: 11399431
  18. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity.
    Neuropharmacology. 2008 Dec;55(7):1081-94 PMID: 18755202
  19. Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit.
    Nature. 1995 Jan 12;373(6510):151-5 PMID: 7816096
  20. Modeller: generation and refinement of homology-based protein structure models.
    Methods Enzymol. 2003;374:461-91 PMID: 14696385
  21. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor epsilon1 subunit.
    J Neurosci. 1998 Sep 1;18(17):6704-12 PMID: 9712642
  22. Improved splice site detection in Genie.
    J Comput Biol. 1997 Fall;4(3):311-23 PMID: 9278062
  23. Oligonucleotide array-based comparative genomic hybridization (aCGH) of 90 neuroblastomas reveals aberration patterns closely associated with relapse pattern and outcome.
    Genes Chromosomes Cancer. 2006 Dec;45(12):1130-42 PMID: 16958102
  24. CGHPRO -- a comprehensive data analysis tool for array CGH.
    BMC Bioinformatics. 2005 Apr 05;6:85 PMID: 15807904
  25. Glutamate receptors at atomic resolution.
    Nature. 2006 Mar 23;440(7083):456-62 PMID: 16554805
  26. Subunit arrangement and function in NMDA receptors.
    Nature. 2005 Nov 10;438(7065):185-92 PMID: 16281028
  27. Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information.
    Nucleic Acids Res. 1996 Sep 1;24(17):3439-52 PMID: 8811101
  28. Splicing in disease: disruption of the splicing code and the decoding machinery.
    Nat Rev Genet. 2007 Oct;8(10):749-61 PMID: 17726481
  29. Molecular determinants of ligand discrimination in the glutamate-binding pocket of the NMDA receptor.
    Neuropharmacology. 2004 Dec;47(7):994-1007 PMID: 15555634
  30. Human Splicing Finder: an online bioinformatics tool to predict splicing signals.
    Nucleic Acids Res. 2009 May;37(9):e67 PMID: 19339519
  31. Haploinsufficiency of NSD1 causes Sotos syndrome.
    Nat Genet. 2002 Apr;30(4):365-6 PMID: 11896389
  32. Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice.
    Neuron. 1996 Feb;16(2):333-44 PMID: 8789948
  33. NMDA receptor GluN2B (GluR epsilon 2/NR2B) subunit is crucial for channel function, postsynaptic macromolecular organization, and actin cytoskeleton at hippocampal CA3 synapses.
    J Neurosci. 2009 Sep 2;29(35):10869-82 PMID: 19726645
  34. Genetic enhancement of learning and memory in mice.
    Nature. 1999 Sep 2;401(6748):63-9 PMID: 10485705
  35. Role of distinct NMDA receptor subtypes at central synapses.
    Sci STKE. 2004 Oct 19;2004(255):re16 PMID: 15494561
  36. Mutations of CASK cause an X-linked brain malformation phenotype with microcephaly and hypoplasia of the brainstem and cerebellum.
    Nat Genet. 2008 Sep;40(9):1065-7 PMID: 19165920
  37. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor.
    Nature. 2009 Dec 10;462(7274):745-56 PMID: 19946266
  38. PANTHER: a library of protein families and subfamilies indexed by function.
    Genome Res. 2003 Sep;13(9):2129-41 PMID: 12952881
Article Info
Journal
Nature genetics
Abbr.
Nat Genet
ISSN
1546-1718
Published
2010-11-00
Epub
2010-00-03
Pages
1021-6
Language
English
Region
United States
NLM ID
9216904
Subset
IM
Corrections
CommentIn
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]