Abstract
Mutations in the functionally uncharacterized protein SH3TC2 are associated with the severe hereditary peripheral neuropathy, Charcot-Marie-Tooth disease type 4C (CMT4C). Similarly, to other proteins mutated in CMT, a role for SH3TC2 in endocytic membrane traffic has been previously proposed. However, recent descriptions of the intracellular localization of SH3TC2 are conflicting. Furthermore, no clear functional pathogenic mechanisms have so far been proposed to explain why both nonsense and missense mutations in SH3TC2 lead to similar clinical phenotypes. Here, we describe our intracellular localization studies, supported by biochemical and functional data, using wild-type and mutant SH3TC2. We show that wild-type SH3TC2 targets to the intracellular recycling endosome by associating with the small GTPase, Rab11, which is known to regulate the recycling of internalized membrane and receptors back to the plasma membrane. Furthermore, we demonstrate that SH3TC2 interacts preferentially with the GTP-bound form of Rab11, identifying SH3TC2 as a novel Rab11 effector. Of clinical pathological relevance, all SH3TC2 constructs harbouring disease-causing mutations are shown to be unable to associate with Rab11 with consequent loss of recycling endosome localization. Moreover, we show that wild-type SH3TC2, but not mutant SH3TC2, influences transferrin receptor dynamics, consistent with a functional role on the endocytic recycling pathway. Our data therefore implicate mistargeting of SH3TC2 away from the recycling endosome as the fundamental molecular defect that leads to CMT4C.
MeSH Terms
Animals
Blotting, Western
Cell Extracts
Cell Membrane/metabolism
Charcot-Marie-Tooth Disease/metabolism
Endocytosis
Endosomes/metabolism
Flow Cytometry
Fluorescent Antibody Technique
Green Fluorescent Proteins/metabolism
HeLa Cells
Humans
Intracellular Signaling Peptides and Proteins
Intracellular Space/metabolism
Microscopy, Confocal
Mutant Proteins/chemistry,metabolism
Protein Structure, Tertiary
Protein Transport
Proteins/chemistry,metabolism
Rats
Receptors, Transferrin/metabolism
Chemicals
Cell Extracts
Intracellular Signaling Peptides and Proteins
Mutant Proteins
Proteins
Receptors, Transferrin
SH3TC2 protein, human
Green Fluorescent Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Roberts Rhys C
Cambridge Institute for Medical Research, University of Cambridge, Cambridge CB2 0XY, UK. rcr20@cam.ac.uk
Peden Andrew A
Buss Folma
Bright Nicholas A
Latouche Morwena
Reilly Mary M
Kendrick-Jones John
Luzio J Paul
References (24)
24 references, click to expand
-
Missense mutations in the SH3TC2 protein causing Charcot-Marie-Tooth disease type 4C affect its localization in the plasma membrane and endocytic pathway.
Hum Mol Genet. 2009 Dec 1;18(23):4603-14
PMID: 19744956
-
Identification of Rab11 as a small GTPase binding protein for the Evi5 oncogene.
Proc Natl Acad Sci U S A. 2007 Jan 23;104(4):1236-41
PMID: 17229837
-
D-AKAP2 interacts with Rab4 and Rab11 through its RGS domains and regulates transferrin receptor recycling.
J Biol Chem. 2009 Nov 20;284(47):32869-80
PMID: 19797056
-
Pathways and mechanisms of endocytic recycling.
Nat Rev Mol Cell Biol. 2009 Sep;10(9):597-608
PMID: 19696797
-
Sorting out the inherited neuropathies.
Pract Neurol. 2007 Apr;7(2):93-105
PMID: 17430873
-
Study on the gene and phenotypic characterisation of autosomal recessive demyelinating motor and sensory neuropathy (Charcot-Marie-Tooth disease) with a gene locus on chromosome 5q23-q33.
J Neurol Neurosurg Psychiatry. 1999 May;66(5):569-74
PMID: 10209165
-
Class I FIPs, Rab11-binding proteins that regulate endocytic sorting and recycling.
Methods Enzymol. 2005;403:512-25
PMID: 16473616
-
Molecular characterization of Rab11 interactions with members of the family of Rab11-interacting proteins.
J Biol Chem. 2004 Aug 6;279(32):33430-7
PMID: 15173169
-
Genetic defects of intracellular-membrane transport.
N Engl J Med. 2000 Oct 12;343(15):1095-104
PMID: 11027745
-
Cell biology of membrane trafficking in human disease.
Int Rev Cytol. 2006;252:1-69
PMID: 16984815
-
Rab GTPases as coordinators of vesicle traffic.
Nat Rev Mol Cell Biol. 2009 Aug;10(8):513-25
PMID: 19603039
-
The phenotype of Charcot-Marie-Tooth disease type 4C due to SH3TC2 mutations and possible predisposition to an inflammatory neuropathy.
Neuromuscul Disord. 2009 Apr;19(4):264-9
PMID: 19272779
-
Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat.
J Cell Biol. 1991 Apr;113(1):123-35
PMID: 2007617
-
Mutations in a gene encoding a novel SH3/TPR domain protein cause autosomal recessive Charcot-Marie-Tooth type 4C neuropathy.
Am J Hum Genet. 2003 Nov;73(5):1106-19
PMID: 14574644
-
The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP-, N-CAM-, NGF-receptor-) depends on growth inhibition.
J Cell Biol. 1991 Feb;112(3):457-67
PMID: 1704008
-
Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo.
Nat Struct Mol Biol. 2005 Oct;12(10):879-85
PMID: 16155582
-
Epidemiology of peripheral neuropathy.
J Neurol Neurosurg Psychiatry. 1997 Apr;62(4):310-8
PMID: 9120441
-
Molecular mechanisms of inherited demyelinating neuropathies.
Glia. 2008 Nov 1;56(14):1578-89
PMID: 18803325
-
Identification of a novel Rab11/25 binding domain present in Eferin and Rip proteins.
J Biol Chem. 2001 Oct 19;276(42):38966-70
PMID: 11481332
-
Pathomechanisms of mutant proteins in Charcot-Marie-Tooth disease.
Neuromolecular Med. 2006;8(1-2):217-42
PMID: 16775378
-
Improving structural integrity of cryosections for immunogold labeling.
Histochem Cell Biol. 1996 Jul;106(1):41-58
PMID: 8858366
-
The RCP-Rab11 complex regulates endocytic protein sorting.
Mol Biol Cell. 2004 Aug;15(8):3530-41
PMID: 15181150
-
SH3TC2/KIAA1985 protein is required for proper myelination and the integrity of the node of Ranvier in the peripheral nervous system.
Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17528-33
PMID: 19805030
-
Spine deformities in Charcot-Marie-Tooth 4C caused by SH3TC2 gene mutations.
Neurology. 2006 Aug 22;67(4):602-6
PMID: 16924012