Distinct subcellular localization of a group of synaptobrevin-like SNAREs in Paramecium tetraurelia and effects of silencing SNARE-specific chaperone NSF

Eukaryotic Cell

Volumn 9, Issue 2, 2010, Pages 288-305

  Schilde, Christina ^a   Schönemann, Barbara ^a   Sehring, Ivonne M ^a   Plattner, Helmut ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GREEN FLUORESCENT PROTEIN; PROTOZOAL PROTEIN; SNARE PROTEIN; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; SYNAPTOBREVIN;

AMINO ACID SEQUENCE; ARTICLE; CYTOPLASM VESICLE; GENETICS; METABOLISM; PARAMECIUM TETRAURELIA;

AMINO ACID SEQUENCE; CYTOPLASMIC VESICLES; GREEN FLUORESCENT PROTEINS; MOLECULAR CHAPERONES; PARAMECIUM TETRAURELIA; PROTOZOAN PROTEINS; R-SNARE PROTEINS; SNARE PROTEINS; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS;

CILIOPHORA; PARAMECIUM TETRAURELIA; PROTOZOA;

EID: 75849116774     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00220-09     Document Type: Article

References (63)

1. Adoutte, A., P. Delgado, A. Fleury, N. Levilliers, M. C. Laine, M. C. Marty, E. Boisvieux-Ulrich, and D. Sandoz. 1991. Microtubule diversity in ciliated cells: evidence for its generation by post-translational modification in the axonemes of Paramecium and quail oviduct cells. Biol. Cell 71:227-245.
2. Allen, R. D. 1984. Paramecium phagosome membrane: from oral region to cytoproct and back again. J. Protozool. 31:1-6.
3. Allen, R. D., and A. K. Fok. 1993. Endosomal membrane traffic of ciliates, p. 57-83. In H. Plattner (ed.), Advances in cell and molecular biology of membranes. JAI Press, Greenwich, CT.
4. Allen, R. D., and A. K. Fok. 2000. Membrane trafficking and processing in Paramecium. Int. Rev. Cytol. 198:277-318.
5. Allen, R. D., and L. A. Staehelin. 1981. Digestive system membranes: freeze-fracture evidence for differentiation and flow in Paramecium. J. Cell Biol. 89:9-20.
6. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
7. Antonin, W., D. Fasshauer, S. Becker, R. Jahn, and T. R. Schneider. 2002. Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat. Struct. Biol. 9:107-111.
8. Aury, J. M., O. Jaillon, L. Duret, B. Noel, C. Jubin, B. M. Porcel, B. Ségurens, V. Daubin, V. Anthouard, N. Aiach, O. Arnaiz, A. Billaut, J. Beisson, I. Blanc, K. Bouhouche, F. Câmara, S. Duharcourt, R. Guigo, D. Gogendeau, M. Katinka, A. M. Keller, R. Kissmehl, C. Klotz, F. Koll, M. A. Le, G. Lepère, S. Malinsky, M. Nowacki, J. K. Nowak, H. Plattner, J. Poulain, F. Ruiz, V. Serrano, M. Zagulski, P. Dessen, M. Bétermier, J. Weissenbach, C. Scarpelli, V. Schächter, L. Sperling, E. Meyer, J. Cohen, and P. Wincker. 2006. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171-178.
9. Bairoch, A., P. Bucher, and K. Hofmann. 1997. The PROSITE database, its status in 1997. Nucleic Acids Res. 25:217-221.
10. Baker, S. A., M. Haeri, P. Yoo, S. M. Gospe III, N. P. Skiba, B. E. Knox, and V. Y. Arshavsky. 2008. The outer segment serves as a default destination for the trafficking of membrane proteins in photoreceptors. J. Cell Biol. 183: 485-498.
11. Bowman, G. R., and A. P. Turkewitz. 2001. Analysis of a mutant exhibiting conditional sorting to dense core secretory granules in Tetrahymena thermophila. Genetics 159:1605-1616.
12. Capdeville, Y. 2000. Paramecium GPI proteins: variability of expression and localization. Protist 151:161-169.
13. Chuang, J. Z., Y. Zhao, and C. H. Sung. 2007. SARA-regulated vesicular targeting underlies formation of the light-sensing organelle in mammalian rods. Cell 130:535-547.
14. Dillon, P. J., and C. A. Rosen. 1993. Use of polymerase chain reaction for the rapid construction of synthetic genes. Methods Mol. Biol. 15:263-269.
15. Dittman, J. S., and J. M. Kaplan. 2006. Factors regulating the abundance and localization of synaptobrevin in the plasma membrane. Proc. Natl. Acad. Sci. U. S. A. 103:11399-11404.
16. Dryl, S. 1959. Effect of adaptation to the environment on chemotaxis of Paramecium caudatum. Acta Biol. Exp. 19:83-93.
17. Fasshauer, D., R. B. Sutton, A. T. Brunger, and R. Jahn. 1998. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q-and R-SNAREs. Proc. Natl. Acad. Sci. U. S. A. 95:15781-15786.
18. Filippini, F., V. Rossi, T. Galli, A. Budillon, M. D'Urso, and M. D'Esposito. 2001. Longins: a new evolutionary conserved VAMP family sharing a novel SNARE domain. Trends Biochem. Sci. 26:407-409.
19. Flötenmeyer, M., M. Momayezi, and H. Plattner. 1999. Immunolabeling analysis of biosynthetic and degradative pathways of cell surface components (glycocalyx) in Paramecium cells. Eur. J. Cell Biol. 78:67-77.
20. Fok, A. K., and R. D. Allen. 1993. Membrane flow in the digestive cycle of Paramecium, p. 85-111. In H. Plattner (ed.), Advances in biochemistry and biology of membranes. JAI Press, Greenwich, CT.
21. Galvani, A., and L. Sperling. 2002. RNA interference by feeding in Paramecium. Trends Genet. 18:11-12.
22. Garreau de Loubresse, N., M. C. Gautier, and L. Sperling. 1994. Immature secretory granules are not acidic in Paramecium cells: implications for sorting to the regulated pathway. Biol. Cell 82:139-147.
23. Godiska, R., K. J. Aufderheide, D. Gilley, P. Hendrie, T. Fitzwater, L. B. Preer, B. Polisky, and J. R. Preer, Jr. 1987. Transformation of Paramecium by microinjection of a cloned serotype gene. Proc. Natl. Acad. Sci. U. S. A. 84:7590-7594.
24. Graf, C. T., D. Riedel, H. D. Schmitt, and R. Jahn. 2005. Identification of functionally interacting SNAREs by using complementary substitutions in the conserved 0 layer. Mol. Biol. Cell 16:2263-2274.
25. Gurkan, C., A. V. Koulov, and W. E. Balch. 2007. An evolutionary perspective on eukaryotic membrane trafficking. Adv. Exp. Med. Biol. 607:73-83.
26. 2 sensor protein of secretion. Biochemistry 47:13822-13830.
27. Hauser, K., W. J. Haynes, C. Kung, H. Plattner, and R. Kissmehl. 2000. Expression of the green fluorescent protein in Paramecium tetraurelia. Eur. J. Cell Biol. 79:144-149.
28. Hausmann, K., A. K. Fok, and R. D. Allen. 1988. Immunocytochemical analysis of trichocyst structure and development in Paramecium. J. Ultrastruct. Mol. Struct. Res. 99:213-225.
29. Haynes, W. J., K. Y. Ling, R. R. Preston, Y. Saimi, and C. Kung. 2000. The cloning and molecular analysis of pawn-B in Paramecium tetraurelia. Genetics 155:1105-1117.
30. Haynes, W. J., K. Y. Ling, Y. Saimi, and C. Kung. 1995. Induction of antibiotic resistance in Paramecium tetraurelia by the bacterial gene APH-3 -II. J. Eukaryot. Microbiol. 42:83-91.
31. Haynes, W. J., B. Vaillant, R. R. Preston, Y. Saimi, and C. Kung. 1998. The cloning by complementation of the pawn-A gene in Paramecium. Genetics 149:947-957.
32. Jahn, R., and R. H. Scheller. 2006. SNAREs: engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7:631-643.
33. Jones, D. T. 1998. Do transmembrane protein superfolds exist? FEBS Lett. 423:281-285.
34. Jones, D. T. 1999. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292:195-202.
35. Jones, D. T., W. R. Taylor, and J. M. Thornton. 1994. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33:3038-3049.
36. Kissmehl, R., M. Froissard, H. Plattner, M. Momayezi, and J. Cohen. 2002. NSF regulates membrane traffic along multiple pathways in Paramecium. J. Cell Sci. 115:3935-3946.
37. Kissmehl, R., C. Schilde, T. Wassmer, C. Danzer, K. Nuehse, K. Lutter, and H. Plattner. 2007. Molecular identification of 26 syntaxin genes and their assignment to the different trafficking pathways in Paramecium. Traffic 8:523-542.
38. Kissmehl, R., I. M. Sehring, E. Wagner, and H. Plattner. 2004. Immunolocalization of actin in Paramecium cells. J. Histochem. Cytochem. 52:1543-1559.
39. Kloepper, T. H., C. N. Kienle, and D. Fasshauer. 2007. An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell 18:3463-3471.
40. Kung, C., and Y. Saimi. 1982. The physiological basis of taxes in Paramecium. Annu. Rev. Physiol. 44:519-534.
41. Lipka, V., C. Kwon, and R. Panstruga. 2007. SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu. Rev. Cell Dev. Biol. 23: 147-174.
42. Lumpert, C. J., R. Glas-Albrecht, E. Eisenmann, and H. Plattner. 1992. Secretory organelles of Paramecium cells (trichocysts) are not remarkably acidic compartments. J. Histochem. Cytochem. 40:153-160.
43. Machemer, H. 1988. Electrophysiology, p. 185-215. In H. D. Görtz (ed.), Paramecium. Springer, Berlin, Germany.
44. Mancias, J. D., and J. Goldberg. 2007. The transport signal on Sec22 for packaging into COPII-coated vesicles is a conformational epitope. Mol. Cell 26:403-414.
45. McGuffin, L. J., K. Bryson, and D. T. Jones. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16:404-405.
46. Plattner, H. 2002. My favorite cell: Paramecium. Bioessays 24:649-658.
47. Plattner, H., and R. Kissmehl. 2003. Molecular aspects of membrane trafficking in Paramecium. Int. Rev. Cytol. 232:185-216.
48. Radek, R., and K. Hausmann. 1996. Phagotrophy of ciliates, p. 197-219. In K. Hausmann and P. C. Bradbury (ed.), Ciliates: cells as organisms. G. Fischer, Stuttgart, Germany.
49. Rossi, V., D. K. Banfield, M. Vacca, L. E. Dietrich, C. Ungermann, M. D'Esposito, T. Galli, and F. Filippini. 2004. Longins and their longin domains: regulated SNAREs and multifunctional SNARE regulators. Trends Biochem. Sci. 29:682-688.
50. Rossi, V., R. Picco, M. Vacca, M. D'Esposito, M. D'Urso, T. Galli, and F. Filippini. 2004. VAMP subfamilies identified by specific R-SNARE motifs. Biol. Cell 96:251-256.
51. Sambrook, J., E. Fritch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
52. Schilde, C., K. Lutter, R. Kissmehl, and H. Plattner. 2008. Molecular identification of a SNAP-25-like SNARE protein in Paramecium. Eukaryot. Cell 7:1387-1402.
53. Schilde, C., T. Wassmer, J. Mansfeld, H. Plattner, and R. Kissmehl. 2006. A multigene family encoding R-SNAREs in the ciliate Paramecium tetraurelia. Traffic 7:440-455.
54. Schroeder, C. C., A. K. Fok, and R. D. Allen. 1990. Vesicle transport along microtubular ribbons and isolation of cytoplasmic dynein from Paramecium. J. Cell Biol. 111:2553-2562.
55. Skouri, F., and J. Cohen. 1997. Genetic approach to regulated exocytosis using functional complementation in Paramecium: identification of the ND7 gene required for membrane fusion. Mol. Biol. Cell 8:1063-1071.
56. Sonneborn, T. M. 1974. Paramecium aurelia, p. 469-594. In R. C. Kung (ed.), Handbook of genetics. Plenum Press, New York, NY.
57. Sutton, R. B., D. Fasshauer, R. Jahn, and A. T. Brunger. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395:347-353.
58. Timmons, L., D. L. Court, and A. Fire. 2001. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263:103-112.
59. Vayssié, L., N. Garreau de Loubresse, and L. Sperling. 2001. Growth and form of secretory granules involves stepwise assembly but not differential sorting of a family of secretory proteins in Paramecium. J. Cell Sci. 114:875-886.
60. Wassmer, T., M. Froissard, H. Plattner, R. Kissmehl, and J. Cohen. 2005. The vacuolar proton-ATPase plays a major role in several membrane-bounded organelles in Paramecium. J. Cell Sci. 118:2813-2825.
61. Wassmer, T., R. Kissmehl, J. Cohen, and H. Plattner. 2006. Seventeen -subunit isoforms of Paramecium V-ATPase provide high specialization in localization and function. Mol. Biol. Cell 17:917-930.
62. Wirsel, S. G. R., R. V. Vögele, R. Bänninger, and K. W. Mentgen. 2004. Cloning of -tubulin and succinate dehydrogenase genes from Uromyces fabae and establishing selection conditions for their use in transformation. Eur. J. Plant Pathol. 110:767-777.
63. Zwilling, D., A. Cypionka, W. H. Pohl, D. Fasshauer, P. J. Walla, M. C. Wahl, and R. Jahn. 2007. Early endosomal SNAREs form a structurally conserved SNARE complex and fuse liposomes with multiple topologies. EMBO J. 26:9-18.