Loss of SNAP29 Impairs Endocytic Recycling and Cell Motility

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Rapaport, Debora ^a   Lugassy, Yevgenia ^c   Sprecher, Eli ^a,b,c   Horowitz, Mia ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CHOLERA TOXIN; QB SNARE PROTEIN; QC SNARE PROTEIN; SNAP29 PROTEIN, HUMAN; TRANSFERRIN;

ARTICLE; BIOLOGICAL MODEL; CELL LINE; CELL MOTION; CHEMISTRY; ENDOCYTOSIS; EXOCYTOSIS; FIBROBLAST; GOLGI COMPLEX; HUMAN; METABOLISM; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; WOUND HEALING;

ANTIGENS, CD29; CELL LINE; CELL MOVEMENT; CHOLERA TOXIN; ENDOCYTOSIS; EXOCYTOSIS; FIBROBLASTS; GOLGI APPARATUS; HUMANS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; QB-SNARE PROTEINS; QC-SNARE PROTEINS; TRANSFERRIN; WOUND HEALING;

EID: 79952117266     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009759     Document Type: Article

References (54)

1. Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116: 153-166.
2. Hohenstein AC, Roche PA (2001) SNAP-29 is a promiscuous syntaxin-binding SNARE. Biochem Biophys Res Commun 285: 167-171.
3. Malsam J, Kreye S, Sollner TH (2008) Membrane traffic in the secretory pathway: Membrane fusion: SNAREs and regulation. Cell Mol Life Sci 65: 2814-2832.
4. Littleton JT, Barnard RJ, Titus SA, Slind J, Chapman ER, et al. (2001) SNAREcomplex disassembly by NSF follows synaptic-vesicle fusion. Proc Natl Acad Sci U S A 98: 12233-12238.
5. Zhao C, Slevin JT, Whiteheart SW (2007) Cellular functions of NSF: not just SNAPs and SNAREs. FEBS Lett 581: 2140-2149.
6. Polgar J, Lane WS, Chung SH, Houng AK, Reed GL (2003) Phosphorylation of SNAP-23 in activated human platelets. J Biol Chem 278: 44369-44376.
7. Holt M, Varoqueaux F, Wiederhold K, Takamori S, Urlaub H, et al. (2006) Identification of SNAP-47, a novel Qbc-SNARE with ubiquitous expression. J Biol Chem 281: 17076-17083.
8. Steegmaier M, Yang B, Yoo JS, Huang B, Shen M, et al. (1998) Three novel proteins of the syntaxin/SNAP-25 family. J Biol Chem 273: 34171-34179.
9. Wong SH, Xu Y, Zhang T, Griffiths G, Lowe SL, et al. (1999) GS32, a novel Golgi SNARE of 32 kDa, interacts preferentially with syntaxin 6. Mol Biol Cell 10: 119-134.
10. Su Q, Mochida S, Tian JH, Mehta R, Sheng ZH (2001) SNAP-29: a general SNARE protein that inhibits SNARE disassembly and is implicated in synaptic transmission. Proc Natl Acad Sci U S A 98: 14038-14043.
11. Pan PY, Cai Q, Lin L, Lu PH, Duan S, et al. (2005) SNAP-29-mediated modulation of synaptic transmission in cultured hippocampal neurons. J Biol Chem 280: 25769-25779.
12. Rotem-Yehudar R, Galperin E, Horowitz M (2001) Association of insulin-like growth factor 1 receptor with EHD1 and SNAP29. J Biol Chem 276: 33054-33060.
13. Schardt A, Brinkmann BG, Mitkovski M, Sereda MW, Werner HB, et al. (2009) The SNARE protein SNAP-29 interacts with the GTPase Rab3A: Implications for membrane trafficking in myelinating glia. J Neurosci Res 87: 3465-3479.
14. Sprecher E, Ishida-Yamamoto A, Mizrahi-Koren M, Rapaport D, Goldsher D, et al. (2005) A mutation in SNAP29, coding for a SNARE protein involved in intracellular trafficking, causes a novel neurocutaneous syndrome characterized by cerebral dysgenesis, neuropathy, ichthyosis, and palmoplantar keratoderma. Am J Hum Genet 77: 242-251.
15. Bock JB, Matern HT, Peden AA, Scheller RH (2001) A genomic perspective on membrane compartment organization. Nature 409: 839-841.
16. Grant B, Zhang Y, Paupard MC, Lin SX, Hall DH, et al. (2001) Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol 3: 573-579.
17. Lin SX, Grant B, Hirsh D, Maxfield FR (2001) Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol 3: 567-572.
18. Rapaport D, Auerbach W, Naslavsky N, Pasmanik-Chor M, Galperin E, et al. (2006) Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic 7: 52-60.
19. Grant BD, Caplan S (2008) Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9: 2043-2052.
20. Mintz L, Galperin E, Pasmanik-Chor M, Tulzinsky S, Bromberg Y, et al. (1999) EHD1-an EH-domain-containing protein with a specific expression pattern. Genomics 59: 66-76.
21. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, et al. (2007) Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449: 923-927.
22. George M, Ying G, Rainey MA, Solomon A, Parikh PT, et al. (2007) Shared as well as distinct roles of EHD proteins revealed by biochemical and functional comparisons in mammalian cells and C. elegans. BMC Cell Biol 8: 3.
23. Guilherme A, Soriano NA, Bose S, Holik J, Bose A, et al. (2004) EHD2 and the novel EH domain binding protein EHBP1 couple endocytosis to the actin cytoskeleton. J Biol Chem 279: 10593-10605.
24. Galperin E, Benjamin S, Rapaport D, Rotem-Yehudar R, Tolchinsky S, et al. (2002) EHD3: a protein that resides in recycling tubular and vesicular membrane structures and interacts with EHD1. Traffic 3: 575-589.
25. Naslavsky N, Rahajeng J, Sharma M, Jovic M, Caplan S (2006) Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport. Mol Biol Cell 17: 163-177.
26. Sharma M, Naslavsky N, Caplan S (2008) A role for EHD4 in the regulation of early endosomal transport. Traffic 9: 995-1018.
27. Massol RH, Larsen JE, Fujinaga Y, Lencer WI, Kirchhausen T (2004) Cholera toxin toxicity does not require functional Arf6-and dynamin-dependent endocytic pathways. Mol Biol Cell 15: 3631-3641.
28. Luftman K, Hasan N, Day P, Hardee D, Hu C (2009) Silencing of VAMP3 inhibits cell migration and integrin-mediated adhesion. Biochem Biophys Res Commun 380: 65-70.
29. Skalski M, Coppolino MG (2005) SNARE-mediated trafficking of alpha5beta1 integrin is required for spreading in CHO cells. Biochem Biophys Res Commun 335: 1199-1210.
30. Tayeb MA, Skalski M, Cha MC, Kean MJ, Scaife M, et al. (2005) Inhibition of SNARE-mediated membrane traffic impairs cell migration. Exp Cell Res 305: 63-73.
31. Caswell PT, Norman JC (2006) Integrin trafficking and the control of cell migration. Traffic 7: 14-21.
32. Caswell PT, Vadrevu S, Norman JC (2009) Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol 10: 843-853.
33. Koegel H, von Tobel L, Schafer M, Alberti S, Kremmer E, et al. (2009) Loss of serum response factor in keratinocytes results in hyperproliferative skin disease in mice. J Clin Invest 119: 899-910.
34. Gambardella L, Barrandon Y (2003) The multifaceted adult epidermal stem cell. Curr Opin Cell Biol 15: 771-777.
35. Cayre M, Canoll P, Goldman JE (2009) Cell migration in the normal and pathological postnatal mammalian brain. Prog Neurobiol 88: 41-63.
36. Romer LH, Birukov KG, Garcia JG (2006) Focal adhesions: paradigm for a signaling nexus. Circ Res 98: 606-616.
37. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, et al. (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709.
38. Wickner W, Schekman R (2008) Membrane fusion. Nat Struct Mol Biol 15: 658-664.
39. Pozzi D, Condliffe S, Bozzi Y, Chikhladze M, Grumelli C, et al. (2008) Activitydependent phosphorylation of Ser187 is required for SNAP-25-negative modulation of neuronal voltage-gated calcium channels. Proc Natl Acad Sci U S A 105: 323-328.
40. Verderio C, Pozzi D, Pravettoni E, Inverardi F, Schenk U, et al. (2004) SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41: 599-610.
41. Pierini LM, Lawson MA, Eddy RJ, Hendey B, Maxfield FR (2000) Oriented endocytic recycling of alpha5beta1 in motile neutrophils. Blood 95: 2471-2480.
42. Mitra SK, Hanson DA, Schlaepfer DD (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6: 56-68.
43. Proux-Gillardeaux V, Gavard J, Irinopoulou T, Mege RM, Galli T (2005) Tetanus neurotoxin-mediated cleavage of cellubrevin impairs epithelial cell migration and integrin-dependent cell adhesion. Proc Natl Acad Sci U S A 102: 6362-6367.
44. Gu LH, Coulombe PA (2007) Keratin function in skin epithelia: a broadening palette with surprising shades. Curr Opin Cell Biol 19: 13-23.
45. Houben E, De Paepe K, Rogiers V (2007) A keratinocyte's course of life. Skin Pharmacol Physiol 20: 122-132.
46. Jaglin XH, Chelly J (2009) Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects. Trends Genet 25: 555-566.
47. Etain B, Dumaine A, Mathieu F, Chevalier F, Henry C, et al. (2009) A SNAP25 promoter variant is associated with early-onset bipolar disorder and a high expression level in brain. Mol Psychiatry.
48. Smith R, Klein P, Koc-Schmitz Y, Waldvogel HJ, Faull RL, et al. (2007) Loss of SNAP-25 and rabphilin 3a in sensory-motor cortex in Huntington's disease. J Neurochem 103: 115-123.
49. Gissen P, Johnson CA, Morgan NV, Stapelbroek JM, Forshew T, et al. (2004) Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunction-cholestasis (ARC) syndrome. Nat Genet 36: 400-404.
50. Hucthagowder V, Morava E, Kornak U, Lefeber DJ, Fischer B, et al. (2009) Loss-of-function mutations in ATP6V0A2 impair vesicular trafficking, tropoelastin secretion and cell survival. Hum Mol Genet 18: 2149-2165.
51. Sakai K, Akiyama M, Sugiyama-Nakagiri Y, McMillan JR, Sawamura D, et al. (2007) Localization of ABCA12 from Golgi apparatus to lamellar granules in human upper epidermal keratinocytes. Exp Dermatol 16: 920-926.
52. Henderson IC, Livingston DM (1974) Partial purification and characterization of the SV40 T antigen. Cell 3: 65-70.
53. Hirschberg K, Miller CM, Ellenberg J, Presley JF, Siggia ED, et al. (1998) Kinetic analysis of secretory protein traffic and characterization of golgi to plasma membrane transport intermediates in living cells. J Cell Biol 143: 1485-1503.
54. Bark IC, Wilson MC (1994) Human cDNA clones encoding two different isoforms of the nerve terminal protein SNAP-25. Gene 139: 291-292.