Home LiteratureArticle Details
PMID: 20037588 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Alterations in the ankyrin domain of TRPV4 cause congenital distal SMA, scapuloperoneal SMA and HMSN2C.

Nature genetics ·Vol. 42 ·No. 2 ·2010-02-00 ·Pages 160-4

Auer-Grumbach M, Olschewski A, Papić L, Kremer H, McEntagart ME, Uhrig S, Fischer C, Fröhlich E, Bálint Z, Tang B, Strohmaier H, Lochmüller H, Schlotter-Weigel B, Senderek J, Krebs A, Dick KJ, Petty R, Longman C, Anderson NE, Padberg GW, Schelhaas HJ, van Ravenswaaij-Arts CM, Pieber TR, Crosby AH, Guelly C

Abstract

Spinal muscular atrophies (SMA, also known as hereditary motor neuropathies) and hereditary motor and sensory neuropathies (HMSN) are clinically and genetically heterogeneous disorders of the peripheral nervous system. Here we report that mutations in the TRPV4 gene cause congenital distal SMA, scapuloperoneal SMA, HMSN 2C. We identified three missense substitutions (R269H, R315W and R316C) affecting the intracellular N-terminal ankyrin domain of the TRPV4 ion channel in five families. Expression of mutant TRPV4 constructs in cells from the HeLa line revealed diminished surface localization of mutant proteins. In addition, TRPV4-regulated Ca(2+) influx was substantially reduced even after stimulation with 4alphaPDD, a TRPV4 channel-specific agonist, and with hypo-osmotic solution. In summary, we describe a new hereditary channelopathy caused by mutations in TRPV4 and present evidence that the resulting substitutions in the N-terminal ankyrin domain affect channel maturation, leading to reduced surface expression of functional TRPV4 channels.

MeSH Terms
Amino Acid Substitution/genetics Ankyrin Repeat Calcium/metabolism HeLa Cells Hereditary Sensory and Motor Neuropathy/complications,genetics,physiopathology Humans Immunohistochemistry Intracellular Space/metabolism Ion Channel Gating Models, Molecular Molecular Sequence Data Muscular Atrophy, Spinal/complications,congenital,genetics,physiopathology Mutant Proteins/metabolism Mutation/genetics Osmosis TRPV Cation Channels/chemistry,genetics Transfection
Chemicals
Mutant Proteins TRPV Cation Channels TRPV4 protein, human Calcium
Authors & Affiliations
25 authors, click to expand affiliations / ORCID
Auer-Grumbach Michaela
Institute of Human Genetics, Medical University of Graz, Austria. michaela.auergrumbach@medunigraz.at
Olschewski Andrea
Papić Lea
Kremer Hannie
McEntagart Meriel E
Uhrig Sabine
Fischer Carina
Fröhlich Eleonore
Bálint Zoltán
Tang Bi
Strohmaier Heimo
Lochmüller Hanns
Schlotter-Weigel Beate
Senderek Jan
Krebs Angelika
Dick Katherine J
Petty Richard
Longman Cheryl
Anderson Neil E
Padberg George W
Schelhaas Helenius J
van Ravenswaaij-Arts Conny M A
Pieber Thomas R
Crosby Andrew H
Guelly Christian
References (30)
30 references, click to expand
  1. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity.
    Nat Cell Biol. 2000 Oct;2(10):695-702 PMID: 11025659
  2. Confirmation of a hereditary motor and sensory neuropathy IIC locus at chromosome 12q23-q24.
    Ann Neurol. 2005 Feb;57(2):293-7 PMID: 15668982
  3. TRPV4 calcium entry channel: a paradigm for gating diversity.
    Am J Physiol Cell Physiol. 2004 Feb;286(2):C195-205 PMID: 14707014
  4. TRPV4-mediated calcium influx regulates terminal differentiation of osteoclasts.
    Cell Metab. 2008 Sep;8(3):257-65 PMID: 18762026
  5. Molecular mechanisms of TRPV4-mediated neural signaling.
    Ann N Y Acad Sci. 2008 Nov;1144:42-52 PMID: 19076362
  6. PACSINs bind to the TRPV4 cation channel. PACSIN 3 modulates the subcellular localization of TRPV4.
    J Biol Chem. 2006 Jul 7;281(27):18753-62 PMID: 16627472
  7. TRP channel and cardiovascular disease.
    Pharmacol Ther. 2008 Jun;118(3):337-51 PMID: 18508125
  8. Impaired pressure sensation in mice lacking TRPV4.
    J Biol Chem. 2003 Jun 20;278(25):22664-8 PMID: 12692122
  9. Mutations in the gene encoding the calcium-permeable ion channel TRPV4 produce spondylometaphyseal dysplasia, Kozlowski type and metatropic dysplasia.
    Am J Hum Genet. 2009 Mar;84(3):307-15 PMID: 19232556
  10. Trafficking and assembly of the cold-sensitive TRPM8 channel.
    J Biol Chem. 2006 Dec 15;281(50):38396-404 PMID: 17065148
  11. Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange.
    Proc Natl Acad Sci U S A. 2006 Dec 12;103(50):19093-8 PMID: 17142322
  12. Transient receptor potential channels meet phosphoinositides.
    EMBO J. 2008 Nov 5;27(21):2809-16 PMID: 18923420
  13. Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100 Suppl 2:14531-6 PMID: 14581619
  14. Human TRPV4 channel splice variants revealed a key role of ankyrin domains in multimerization and trafficking.
    J Biol Chem. 2006 Jan 20;281(3):1580-6 PMID: 16293632
  15. Ca2+-selective transient receptor potential V channel architecture and function require a specific ankyrin repeat.
    J Biol Chem. 2004 Aug 13;279(33):34456-63 PMID: 15192090
  16. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels.
    Neuron. 1999 Mar;22(3):537-48 PMID: 10197533
  17. Gain-of-function mutations in TRPV4 cause autosomal dominant brachyolmia.
    Nat Genet. 2008 Aug;40(8):999-1003 PMID: 18587396
  18. Phospholipase Cgamma1 controls surface expression of TRPC3 through an intermolecular PH domain.
    Nature. 2005 Mar 3;434(7029):99-104 PMID: 15744307
  19. Homo- and heteromeric assembly of TRPV channel subunits.
    J Cell Sci. 2005 Mar 1;118(Pt 5):917-28 PMID: 15713749
  20. Crystal structure of the human TRPV2 channel ankyrin repeat domain.
    Protein Sci. 2006 Sep;15(9):2201-6 PMID: 16882997
  21. A dominantly inherited lower motor neuron disorder presenting at birth with associated arthrogryposis.
    J Neurol Neurosurg Psychiatry. 1985 Oct;48(10):1037-48 PMID: 4056805
  22. Localisation of the gene for a dominant congenital spinal muscular atrophy predominantly affecting the lower limbs to chromosome 12q23-q24.
    Eur J Hum Genet. 1998 Jul-Aug;6(4):376-82 PMID: 9781046
  23. Abnormal osmotic regulation in trpv4-/- mice.
    Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13698-703 PMID: 14581612
  24. Transient receptor potential cation channels in disease.
    Physiol Rev. 2007 Jan;87(1):165-217 PMID: 17237345
  25. Structural analyses of the ankyrin repeat domain of TRPV6 and related TRPV ion channels.
    Biochemistry. 2008 Feb 26;47(8):2476-84 PMID: 18232717
  26. TRP channels as cellular sensors.
    Nature. 2003 Dec 4;426(6966):517-24 PMID: 14654832
  27. The TRPV4 channel: structure-function relationship and promiscuous gating behaviour.
    Pflugers Arch. 2003 Jun;446(3):298-303 PMID: 12715179
  28. Linkage of scapuloperoneal spinal muscular atrophy to chromosome 12q24.1-q24.31.
    Hum Mol Genet. 1996 Sep;5(9):1377-82 PMID: 8872481
  29. The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity.
    Neuron. 2007 Jun 21;54(6):905-18 PMID: 17582331
  30. TRP channels: an overview.
    Cell Calcium. 2005 Sep-Oct;38(3-4):233-52 PMID: 16098585
Article Info
Journal
Nature genetics
Abbr.
Nat Genet
ISSN
1546-1718
Published
2010-02-00
Epub
2009-00-27
Pages
160-4
Language
English
Region
United States
NLM ID
9216904
PMCID
PMC3272392
Subset
IM
Grants
Medical Research Council · G0600983 · United Kingdom
Austrian Science Fund FWF · P 19455 · Austria
Databases
GENBANK
NM021625, NP067638
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: product@genelibs.com