Loss of SNAP29 Impairs Endocytic Recycling and Cell Motility

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2010 Mar 23

PMID 20305790

Citations 38

Authors

Debora Rapaport

Yevgenia Lugassy

Eli Sprecher

Mia Horowitz

Affiliations

Soon will be listed here.

Abstract

Intracellular membrane trafficking depends on the ordered formation and consumption of transport intermediates and requires that membranes fuse with each other in a tightly regulated and highly specific manner. Membrane anchored SNAREs assemble into SNARE complexes that bring membranes together to promote fusion. SNAP29 is a ubiquitous synaptosomal-associated SNARE protein. It interacts with several syntaxins and with the EH domain containing protein EHD1. Loss of functional SNAP29 results in CEDNIK syndrome (Cerebral Dysgenesis, Neuropathy, Ichthyosis and Keratoderma). Using fibroblast cell lines derived from CEDNIK patients, we show that SNAP29 mediates endocytic recycling of transferrin and beta1-integrin. Impaired beta1-integrin recycling affected cell motility, as reflected by changes in cell spreading and wound healing. No major changes were detected in exocytosis of VSVG protein from the Golgi apparatus, although the Golgi system acquired a dispersed morphology in SNAP29 deficient cells. Our results emphasize the importance of SNAP29 mediated membrane fusion in endocytic recycling and consequently, in cell motility.

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References

Koegel H, von Tobel L, Schafer M, Alberti S, Kremmer E, Mauch C . Loss of serum response factor in keratinocytes results in hyperproliferative skin disease in mice. J Clin Invest. 2009; 119(4):899-910. PMC: 2662566. DOI: 10.1172/JCI37771. View

Mitra S, Hanson D, Schlaepfer D . Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol. 2005; 6(1):56-68. DOI: 10.1038/nrm1549. View

Steegmaier M, Yang B, Yoo J, Huang B, Shen M, Yu S . Three novel proteins of the syntaxin/SNAP-25 family. J Biol Chem. 1998; 273(51):34171-9. DOI: 10.1074/jbc.273.51.34171. View

Jaglin X, Chelly J . Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects. Trends Genet. 2009; 25(12):555-66. DOI: 10.1016/j.tig.2009.10.003. View

Grant B, Zhang Y, Paupard M, Lin S, Hall D, Hirsh D . Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol. 2001; 3(6):573-9. DOI: 10.1038/35078549. View

Caswell P, Vadrevu S, Norman J . Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol. 2009; 10(12):843-53. DOI: 10.1038/nrm2799. View

Zhao C, Slevin J, Whiteheart S . Cellular functions of NSF: not just SNAPs and SNAREs. FEBS Lett. 2007; 581(11):2140-9. PMC: 1948069. DOI: 10.1016/j.febslet.2007.03.032. View

Verderio C, Pozzi D, Pravettoni E, Inverardi F, Schenk U, Coco S . SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron. 2004; 41(4):599-610. DOI: 10.1016/s0896-6273(04)00077-7. View

Smith R, Klein P, Koc-Schmitz Y, Waldvogel H, Faull R, Brundin P . Loss of SNAP-25 and rabphilin 3a in sensory-motor cortex in Huntington's disease. J Neurochem. 2007; 103(1):115-23. DOI: 10.1111/j.1471-4159.2007.04703.x. View

10.

Caswell P, Norman J . Integrin trafficking and the control of cell migration. Traffic. 2006; 7(1):14-21. DOI: 10.1111/j.1600-0854.2005.00362.x. View

11.

Pierini L, Lawson M, Eddy R, Hendey B, Maxfield F . Oriented endocytic recycling of alpha5beta1 in motile neutrophils. Blood. 2001; 95(8):2471-80. View

12.

Romer L, Birukov K, Garcia J . Focal adhesions: paradigm for a signaling nexus. Circ Res. 2006; 98(5):606-16. DOI: 10.1161/01.RES.0000207408.31270.db. View

13.

Luftman K, Hasan N, Day P, Hardee D, Hu C . Silencing of VAMP3 inhibits cell migration and integrin-mediated adhesion. Biochem Biophys Res Commun. 2009; 380(1):65-70. PMC: 2716655. DOI: 10.1016/j.bbrc.2009.01.036. View

14.

Hohenstein A, Roche P . SNAP-29 is a promiscuous syntaxin-binding SNARE. Biochem Biophys Res Commun. 2001; 285(2):167-71. DOI: 10.1006/bbrc.2001.5141. View

15.

Rapaport D, Auerbach W, Naslavsky N, Pasmanik-Chor M, Galperin E, Fein A . Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic. 2006; 7(1):52-60. DOI: 10.1111/j.1600-0854.2005.00359.x. View

16.

Galperin E, Benjamin S, Rapaport D, Rotem-Yehudar R, Tolchinsky S, Horowitz M . EHD3: a protein that resides in recycling tubular and vesicular membrane structures and interacts with EHD1. Traffic. 2002; 3(8):575-89. DOI: 10.1034/j.1600-0854.2002.30807.x. View

17.

Houben E, De Paepe K, Rogiers V . A keratinocyte's course of life. Skin Pharmacol Physiol. 2006; 20(3):122-32. DOI: 10.1159/000098163. View

18.

Mintz L, Galperin E, Pasmanik-Chor M, Tulzinsky S, Bromberg Y, Kozak C . EHD1--an EH-domain-containing protein with a specific expression pattern. Genomics. 1999; 59(1):66-76. DOI: 10.1006/geno.1999.5800. View

19.

Naslavsky N, Rahajeng J, Sharma M, Jovic M, Caplan S . Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport. Mol Biol Cell. 2005; 17(1):163-77. PMC: 1345656. DOI: 10.1091/mbc.e05-05-0466. View

20.

Schardt A, Brinkmann B, Mitkovski M, Sereda M, Werner H, Nave K . The SNARE protein SNAP-29 interacts with the GTPase Rab3A: Implications for membrane trafficking in myelinating glia. J Neurosci Res. 2009; 87(15):3465-79. DOI: 10.1002/jnr.22005. View