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
-
OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity.
Nat Cell Biol. 2000 Oct;2(10):695-702
PMID: 11025659
-
Confirmation of a hereditary motor and sensory neuropathy IIC locus at chromosome 12q23-q24.
Ann Neurol. 2005 Feb;57(2):293-7
PMID: 15668982
-
TRPV4 calcium entry channel: a paradigm for gating diversity.
Am J Physiol Cell Physiol. 2004 Feb;286(2):C195-205
PMID: 14707014
-
TRPV4-mediated calcium influx regulates terminal differentiation of osteoclasts.
Cell Metab. 2008 Sep;8(3):257-65
PMID: 18762026
-
Molecular mechanisms of TRPV4-mediated neural signaling.
Ann N Y Acad Sci. 2008 Nov;1144:42-52
PMID: 19076362
-
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
-
TRP channel and cardiovascular disease.
Pharmacol Ther. 2008 Jun;118(3):337-51
PMID: 18508125
-
Impaired pressure sensation in mice lacking TRPV4.
J Biol Chem. 2003 Jun 20;278(25):22664-8
PMID: 12692122
-
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
-
Trafficking and assembly of the cold-sensitive TRPM8 channel.
J Biol Chem. 2006 Dec 15;281(50):38396-404
PMID: 17065148
-
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
-
Transient receptor potential channels meet phosphoinositides.
EMBO J. 2008 Nov 5;27(21):2809-16
PMID: 18923420
-
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
-
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
-
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
-
A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels.
Neuron. 1999 Mar;22(3):537-48
PMID: 10197533
-
Gain-of-function mutations in TRPV4 cause autosomal dominant brachyolmia.
Nat Genet. 2008 Aug;40(8):999-1003
PMID: 18587396
-
Phospholipase Cgamma1 controls surface expression of TRPC3 through an intermolecular PH domain.
Nature. 2005 Mar 3;434(7029):99-104
PMID: 15744307
-
Homo- and heteromeric assembly of TRPV channel subunits.
J Cell Sci. 2005 Mar 1;118(Pt 5):917-28
PMID: 15713749
-
Crystal structure of the human TRPV2 channel ankyrin repeat domain.
Protein Sci. 2006 Sep;15(9):2201-6
PMID: 16882997
-
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
-
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
-
Abnormal osmotic regulation in trpv4-/- mice.
Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13698-703
PMID: 14581612
-
Transient receptor potential cation channels in disease.
Physiol Rev. 2007 Jan;87(1):165-217
PMID: 17237345
-
Structural analyses of the ankyrin repeat domain of TRPV6 and related TRPV ion channels.
Biochemistry. 2008 Feb 26;47(8):2476-84
PMID: 18232717
-
TRP channels as cellular sensors.
Nature. 2003 Dec 4;426(6966):517-24
PMID: 14654832
-
The TRPV4 channel: structure-function relationship and promiscuous gating behaviour.
Pflugers Arch. 2003 Jun;446(3):298-303
PMID: 12715179
-
Linkage of scapuloperoneal spinal muscular atrophy to chromosome 12q24.1-q24.31.
Hum Mol Genet. 1996 Sep;5(9):1377-82
PMID: 8872481
-
The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity.
Neuron. 2007 Jun 21;54(6):905-18
PMID: 17582331
-
TRP channels: an overview.
Cell Calcium. 2005 Sep-Oct;38(3-4):233-52
PMID: 16098585