Neurocalcin Delta Suppression Protects against Spinal Muscular Atrophy in Humans and across Species by Restoring Impaired Endocytosis.

PubWeight™: 0.79‹?›

🔗 View Article (PMID 28132687)

Published in Am J Hum Genet on January 26, 2017

Authors

Markus Riessland1, Anna Kaczmarek1, Svenja Schneider1, Kathryn J Swoboda2, Heiko Löhr3, Cathleen Bradler4, Vanessa Grysko1, Maria Dimitriadi5, Seyyedmohsen Hosseinibarkooie1, Laura Torres-Benito1, Miriam Peters1, Aaradhita Upadhyay1, Nasim Biglari1, Sandra Kröber1, Irmgard Hölker1, Lutz Garbes1, Christian Gilissen6, Alexander Hoischen6, Gudrun Nürnberg7, Peter Nürnberg7, Michael Walter8, Frank Rigo9, C Frank Bennett9, Min Jeong Kye10, Anne C Hart5, Matthias Hammerschmidt11, Peter Kloppenburg4, Brunhilde Wirth12

Author Affiliations

1: Institute of Human Genetics, University of Cologne, 50931 Cologne, Germany; Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany; Institute for Genetics, University of Cologne, 50674 Cologne, Germany.
2: MassGeneral Hospital for Children, Boston, MA 02115, USA.
3: Institute for Zoology - Developmental Biology, University of Cologne, 50674 Cologne, Germany; Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD), University of Cologne, 50931 Cologne, Germany.
4: Institute for Zoology - Neurophysiology University of Cologne, 50674 Cologne, Germany; Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD), University of Cologne, 50931 Cologne, Germany.
5: Department of Neuroscience, Brown University, Providence, RI 02912, USA.
6: Department of Human Genetics, Donders Centre for Neuroscience, Radboud University Medical Center, 6525 Nijmegen, the Netherlands.
7: Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD), University of Cologne, 50931 Cologne, Germany; Center for Genomics Cologne, University of Cologne, 50931 Cologne, Germany.
8: Institute of Medical Genetics, University of Tübingen, 72076 Tübingen, Germany.
9: IONIS Pharmaceuticals, Carlsbad, CA 92008, USA.
10: Institute of Human Genetics, University of Cologne, 50931 Cologne, Germany; Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany.
11: Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany; Institute for Zoology - Developmental Biology, University of Cologne, 50674 Cologne, Germany; Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD), University of Cologne, 50931 Cologne, Germany.
12: Institute of Human Genetics, University of Cologne, 50931 Cologne, Germany; Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany; Institute for Genetics, University of Cologne, 50674 Cologne, Germany. Electronic address: brunhilde.wirth@uk-koeln.de.

Articles cited by this

An analysis of the end-plate potential recorded with an intracellular electrode. J Physiol (1951) 83.81

Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A (1976) 21.06

Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics (2002) 20.59

miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev (2002) 19.24

Identification and characterization of a spinal muscular atrophy-determining gene. Cell (1995) 17.41

Allegro, a new computer program for multipoint linkage analysis. Nat Genet (2000) 14.00

Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell (2006) 13.15

Charge movement associated with the opening and closing of the activation gates of the Na channels. J Gen Physiol (1974) 13.07

The synaptic vesicle cycle. Annu Rev Neurosci (2004) 12.25

A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci U S A (1999) 7.60

Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science (2007) 6.65

limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics (2004) 6.04

Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat Genet (2002) 5.80

The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy. Hum Mol Genet (2000) 5.38

The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell (1997) 5.28

Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am J Hum Genet (2001) 4.50

A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing. Cell (1998) 4.47

Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J (1993) 4.39

A mouse model for spinal muscular atrophy. Nat Genet (2000) 4.37

Peripheral SMN restoration is essential for long-term rescue of a severe spinal muscular atrophy mouse model. Nature (2011) 4.04

HaploPainter: a tool for drawing pedigrees with complex haplotypes. Bioinformatics (2004) 4.00

A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat Genet (2003) 3.84

Statistical issues in the analysis of Illumina data. BMC Bioinformatics (2008) 3.66

Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J Cell Biol (2003) 3.40

Secretory granule exocytosis. Physiol Rev (2003) 3.32

Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev Dyn (1992) 3.14

Selective vulnerability of motor neurons and dissociation of pre- and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum Mol Genet (2007) 3.09

Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J Cell Biol (2003) 2.94

Spinal muscular atrophy. Lancet (2008) 2.92

ALOHOMORA: a tool for linkage analysis using 10K SNP array data. Bioinformatics (2005) 2.90

Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy. Hum Mol Genet (2008) 2.82

An update of the mutation spectrum of the survival motor neuron gene (SMN1) in autosomal recessive spinal muscular atrophy (SMA). Hum Mutat (2000) 2.71

Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J Neurosci (2009) 2.71

Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell (2011) 2.56

Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science (2008) 2.51

Enhanced neuronal RNAi in C. elegans using SID-1. Nat Methods (2010) 2.50

Ca2+ signaling via the neuronal calcium sensor-1 regulates associative learning and memory in C. elegans. Neuron (2001) 2.36

Molecular analysis of candidate genes on chromosome 5q13 in autosomal recessive spinal muscular atrophy: evidence of homozygous deletions of the SMN gene in unaffected individuals. Hum Mol Genet (1995) 2.34

Deletions of the survival motor neuron gene in unaffected siblings of patients with spinal muscular atrophy. Am J Hum Genet (1995) 2.33

Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development (2005) 2.30

Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron (2011) 2.19

An SMN-dependent U12 splicing event essential for motor circuit function. Cell (2012) 1.94

Pan-ethnic carrier screening and prenatal diagnosis for spinal muscular atrophy: clinical laboratory analysis of >72,400 specimens. Eur J Hum Genet (2011) 1.88

SAHA ameliorates the SMA phenotype in two mouse models for spinal muscular atrophy. Hum Mol Genet (2010) 1.80

Homozygous SMN1 deletions in unaffected family members and modification of the phenotype by SMN2. Am J Med Genet A (2004) 1.79

Spinal muscular atrophy: going beyond the motor neuron. Trends Mol Med (2012) 1.63

Characterization of survival motor neuron (SMNT) gene deletions in asymptomatic carriers of spinal muscular atrophy. Hum Mol Genet (1996) 1.61

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis. Nat Rev Neurosci (2011) 1.61

Defective Ca2+ channel clustering in axon terminals disturbs excitability in motoneurons in spinal muscular atrophy. J Cell Biol (2007) 1.57

Mutations in BICD2 cause dominant congenital spinal muscular atrophy and hereditary spastic paraplegia. Am J Hum Genet (2013) 1.51

Identified motoneurons and their innervation of axial muscles in the zebrafish. J Neurosci (1986) 1.42

Calcium control of neurotransmitter release. Cold Spring Harb Perspect Biol (2012) 1.42

Rare missense and synonymous variants in UBE1 are associated with X-linked infantile spinal muscular atrophy. Am J Hum Genet (2008) 1.39

Altered intracellular Ca2+ homeostasis in nerve terminals of severe spinal muscular atrophy mice. J Neurosci (2010) 1.38

Identification of a battery of tests for drug candidate evaluation in the SMNDelta7 neonate model of spinal muscular atrophy. Exp Neurol (2008) 1.33

Mutations in BICD2, which encodes a golgin and important motor adaptor, cause congenital autosomal-dominant spinal muscular atrophy. Am J Hum Genet (2013) 1.32

Interaction of survival of motor neuron (SMN) and HuD proteins with mRNA cpg15 rescues motor neuron axonal deficits. Proc Natl Acad Sci U S A (2011) 1.32

Neurotransmitter release at central synapses. Neuron (2003) 1.31

Molecular defects in the motor adaptor BICD2 cause proximal spinal muscular atrophy with autosomal-dominant inheritance. Am J Hum Genet (2013) 1.26

Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. Eur J Paediatr Neurol (1999) 1.26

Bicaudal-D binds clathrin heavy chain to promote its transport and augments synaptic vesicle recycling. EMBO J (2010) 1.24

Spinal muscular atrophy: a motor neuron disorder or a multi-organ disease? J Anat (2013) 1.23

Neurocalcin delta modulation of ROS-GC1, a new model of Ca(2+) signaling. Biochemistry (2008) 1.19

Plastin 3 ameliorates spinal muscular atrophy via delayed axon pruning and improves neuromuscular junction functionality. Hum Mol Genet (2012) 1.17

Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice. Mol Ther (2013) 1.16

Molecular and functional analysis of intragenic SMN1 mutations in patients with spinal muscular atrophy. Hum Mutat (2005) 1.16

Calcium and membrane binding properties of bovine neurocalcin delta expressed in Escherichia coli. J Biol Chem (1995) 1.14

Deletion of smn-1, the Caenorhabditis elegans ortholog of the spinal muscular atrophy gene, results in locomotor dysfunction and reduced lifespan. Hum Mol Genet (2008) 1.08

Dysregulation of ubiquitin homeostasis and β-catenin signaling promote spinal muscular atrophy. J Clin Invest (2014) 1.08

Conserved genes act as modifiers of invertebrate SMN loss of function defects. PLoS Genet (2010) 1.07

Empty synaptic vesicles recycle and undergo exocytosis at vesamicol-treated motor nerve terminals. J Neurophysiol (1999) 1.06

Spinal muscular atrophy--clinical and genetic correlations. Neuromuscul Disord (1997) 1.00

SMN deficiency alters Nrxn2 expression and splicing in zebrafish and mouse models of spinal muscular atrophy. Hum Mol Genet (2013) 0.98

Identification of Ca2+-dependent binding partners for the neuronal calcium sensor protein neurocalcin delta: interaction with actin, clathrin and tubulin. Biochem J (2002) 0.96

Understanding the physiological roles of the neuronal calcium sensor proteins. Mol Brain (2012) 0.95

Neurocalcin family: a novel calcium-binding protein abundant in bovine central nervous system. Neurosci Res (1993) 0.94

Calcineurin homologous protein: a multifunctional Ca2+-binding protein family. Am J Physiol Renal Physiol (2011) 0.91

How genetic modifiers influence the phenotype of spinal muscular atrophy and suggest future therapeutic approaches. Curr Opin Genet Dev (2013) 0.89

A population-based study of genotypic and phenotypic variability in children with spinal muscular atrophy. Acta Paediatr (2009) 0.88

Systemic, postsymptomatic antisense oligonucleotide rescues motor unit maturation delay in a new mouse model for type II/III spinal muscular atrophy. Proc Natl Acad Sci U S A (2015) 0.85

Moving towards treatments for spinal muscular atrophy: hopes and limits. Expert Opin Emerg Drugs (2015) 0.85

The Power of Human Protective Modifiers: PLS3 and CORO1C Unravel Impaired Endocytosis in Spinal Muscular Atrophy and Rescue SMA Phenotype. Am J Hum Genet (2016) 0.85

Plastin 3 is upregulated in iPSC-derived motoneurons from asymptomatic SMN1-deleted individuals. Cell Mol Life Sci (2015) 0.83

Neurocalcin-immunopositive nerve terminals in the muscle spindle, Golgi tendon organ and motor endplate. Brain Res (1998) 0.83

Limits to the development of fast neuromuscular transmission in zebrafish. J Neurophysiol (2001) 0.83

Increasing SMN levels using the histone deacetylase inhibitor SAHA ameliorates defects in skeletal muscle microvasculature in a mouse model of severe spinal muscular atrophy. Neurosci Lett (2013) 0.80

Proteomics analysis of the temporal changes in axonal proteins during maturation. Dev Neurobiol (2010) 0.80

Investigational therapies for the treatment of spinal muscular atrophy. Expert Opin Investig Drugs (2015) 0.79

Endocytic membrane trafficking and neurodegenerative disease. Cell Mol Life Sci (2015) 0.78

Dominant spinal muscular atrophy is caused by mutations in BICD2, an important golgin protein. Front Neurosci (2015) 0.77

Decreased function of survival motor neuron protein impairs endocytic pathways. Proc Natl Acad Sci U S A (2016) 0.77

Hyperhomocysteinemia and bleomycin hydrolase modulate the expression of mouse brain proteins involved in neurodegeneration. J Alzheimers Dis (2014) 0.77

Data on the calcium-induced mobility shift of myristoylated and non-myristoylated forms of neurocalcin delta. Data Brief (2016) 0.75

Rescue of a Mouse Model of Spinal Muscular Atrophy With Respiratory Distress Type 1 by AAV9-IGHMBP2 Is Dose Dependent. Mol Ther (2016) 0.75