Structure and function of nucleus-vacuole junctions: Outer-nuclear-membrane targeting of Nvj1p and a role in tryptophan uptake

Journal of Cell Science

Volumn 119, Issue 17, 2006, Pages 3622-3633

  Kvam, Erik ^a   Goldfarb, David S ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Endoplasmic reticulum; Nuclear envelope; Nucleus vacuole junctions; Nvj1p; Osh1p; Tryptophan permease; Tsc13p

Indexed keywords

MEMBRANE PROTEIN; PROTEIN NVJ1P; TRANSACTIVATOR PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL FUNCTION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE TARGETING; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; CELL NUCLEUS; MOLECULAR SEQUENCE DATA; NUCLEAR ENVELOPE; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; TRYPTOPHAN; VACUOLES;

SACCHAROMYCES CEREVISIAE;

EID: 33749375121     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03093     Document Type: Article

References (52)

1. Beck, T., Schmidt, A. and Hall, M. N. (1999). Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J. Cell Biol. 146, 1227-1238.
2. Beh, C. T. and Rine, J. (2004). A role for yeast oxysterol-binding protein homologs in endocytosis and in the maintenance of intracellular sterol-lipid distribution. J. Cell Sci. 117, 2983-2996.
3. Beilharz, T., Egan, B., Silver, P. A., Hofmann, K. and Lithgow, T. (2003). Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae. J. Biol. Chem. 278, 8219-8223.
4. Bendtsen, J. D., Nielsen, H., von Heijne, G. and Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J Mol. Biol. 340, 783-795.
5. Bi, E. and Pringle, J. R. (1996). ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 5264-5275.
6. Campbell, J. L., Lorenz, A., Witkin, K. L., Hays, T., Loidl, J. and Cohen-Fix, O. (2006): Yeast nuclear envelope subdomains with distinct abilities to resist membrane expansion. Mol. Biol. Cell 17, 1768-1778.
7. Chung, N., Mao, C., Heitman, J., Hannun, Y. A. and Obeid, L. M. (2001). Phytosphingosine as a specific inhibitor of growth and nutrient import in Saccharomyces cerevisiae. J. Biol. Chem. 276, 35614-35621.
8. Cliften, P. F., Hillier, L. W., Fulton, L., Graves, T., Miner, T., Gish, W. R., Waterston, R. H. and Johnston, M. (2001). Surveying Saccharomyces genomes to identify functional elements by comparative DNA sequence analysis. Genome Res. 11, 1175-1186.
9. Crisp, M., Liu, Q., Roux, K., Rattner, J. B., Shanahan, C., Burke, B., Stahl, P. D. and Hadzic, D. (2006). Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172, 41-53.
10. Dickson, K. C. (1998). Sphingolipid functions in Saccharomyces cerevisiae: comparison to mammals. Anna. Rev. Biochem. 67, 27-48.
11. Edinger, A. L. and Thompson, C. B. (2002). Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake. Mol. Biol. Cell 13, 2276-2288.
12. Eisenkolb, M., Zenzmaier, C., Leimer, E. and Schneiter, R. (2002). A specific structural requirement for ergosterol in long-chain fatty acid synthesis mutants important for maintaining raft domains in yeast. Mol. Biol. Cell 13, 4414-4428.
13. Fabrizio, P., Li, L. and Longo, V. D. (2005). Analysis of gene expression profile in yeast aging chronologically. Mech. Ageing Dev. 126, 11-16.
14. Gaber, R. F, Copple, D. M., Kennedy, B. K., Vidal, M. and Bard, M. (1989). The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol. Mol. Cell. Biol. 9, 3447-3456.
15. Giddings, T. H., O'Toole, E. T., Morphew, M., Mastronarde, D. N., McIntosh, J. R. and Winey, M. (2001). Using rapid freeze and freeze-substitution for the preparation of yeast cells for electron microscopy and three-dimensional analysis. Methods Cell Biol. 67, 27-42.
16. Harley, C. A. and Tipper, D. J. (1996). The role of charged residues in determining transmembrane protein insertion orientation in yeast. J. Biol. Chem. 271, 24625-24633.
17. Hemmi, K., Julmanop, C., Hirata, D., Tsuchiya, E., Takemoto, J. Y. and Miyakawa, T. (1995). The physiological roles of membrane ergosterol as revealed by the phenotypes of syr1/erg3 null mutant of Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 59, 482-486.
18. Hetzer, M. W., Walther, T. C. and Mattaj, I. W. (2005). Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annu. Rev. Cell Dev. Biol. 21, 347-380.
19. Holmer, L. and Worman, H. J. (2001). Inner nuclear membrane proteins: functions and targeting. Cell. Mol. Life Sci. 58, 1741-1747.
20. Im, Y. J., Raychaudhuri, S., Prinz, W. A. and Hurley, J. H. (2005). Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437, 154-158.
21. Jiang, B., Brown, J. L., Sheraton, J., Fortin, N. and Bussey, H. (1994). A new family of yeast genes implicated in ergosterol synthesis is related to the human oxysterol binding protein. Yeast 10, 341-353.
22. Kohlwein, S. D., Eder, S., Oh, C. S., Martin, C. E., Gable, K., Bacikova, D. and Dunn, T. (2001). Tsc13p is required for fatty acid elongation and localizes to a novel structure at the nuclear-vacuotar interface in Saccharomyces cerevisiae. Mol. Cell. Biol. 21, 109-125.
23. Kvam, E. and Goldfarb, D. S. (2004). Nvj1p is the outer-nuclear-membrane receptor for oxysterol-binding protein homolog Osh1p in Saccharomyces cerevisiae. J. Cell Sci. 117, 4959-4969.
24. Kvam, E., Gable, K., Dunn, T. M. and Goldfarb, D. S. (2005). Targeting of Tsc13p to nucleus-vacuole junctions: a role for very-long-chain fatty acids in the biogenesis of microautophagic vesicles. Mol. Biol. Cell 16, 3987-3998.
25. Lee, M. C., Orci, L., Hamamoto, S., Futai, E., Ravazzola, M. and Schekman, R. (2005). Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122, 605-617.
26. Levine, T. (2004). Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions. Trends Cell Biol. 14, 483-490.
27. Levine, T. and Rabouille, C. (2005). Endoplasmic reticulum: one continuous network compartmentalized by extrinsic cues. Curr. Opin. Cell Biol. 17, 362-368.
28. Levine, T. P. and Munro, S. (2001). Dual targeting of Osh1p, a yeast homologue of oxysterol-binding protein, to both the Golgi and the nucleus-vacuole junction. Mol. Biol. Cell 12, 1633-1644.
29. Li, G., Yan, Q., Oen, H. O. and Lennarz, W. J. (2003). A specific segment of the transmembrane domain of Wbp1p is essential for its incorporation into the oligosaccharyl transferase complex. Biochemistry 42, 11032-11039.
30. Loewen, C. J., Roy, A. and Levine, T. P. (2003). A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAR EMBO J. 22, 2025-2035.
31. Nakamura, H., Miura, K., Fukuda, Y., Shibuya, I., Ohta, A. and Takagi, M. (2000). Phosphatidylserine synthesis required for the maximal tryptophan transport activity in Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 64, 167-172.
32. Niedenthal, R. K., Riles, L., Johnston, M. and Regemann, J. H. (1996). Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast 12, 773-786.
33. Nielsen, H., Engelbrecht, J., Burnak, S. and von Heijne, G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6.
34. Ohba, T., Schirmer, E. C., Nishimoto, T. and Gerace, L. (2004). Energy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. J. Cell Biol. 167, 1051-1062.
35. Okamoto, M., Yoko-o, T., Umemura, M., Nakayama, K. and Jigami, Y. (2006). Glycosylphosphatidylinositol-anchored proteins are required for the transport of detergent-resistant microdomain-associated membrane proteins Tat2p and Fur4p. J Biol. Chem. 281, 4013-4023.
36. Ostlund, C., Sullivan, T., Stewart, C. L. and Worman, H. J. (2006). Dependence of diffusional mobility of integral inner nuclear membrane proteins on A-type lamins. Biochemistry 45, 1374-1382.
37. Pan, X. and Goldfarb, D. S. (1998). YEB3/VAC8 encodes a myristylated armadillo protein of the Saccharomyces cerevisiae vacuolar membrane that functions in vacuole fusion and inheritance. J. Cell Sci. 111, 2137-2147.
38. Pan, X., Roberts, P., Chen, Y., Kvam, E., Shulga, N., Huang, K., Lemmon, S. and Goldfarb, D. S. (2000). Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1p. Mol. Biol. Cell 11, 2445-2457.
39. Patel, S., Rose, A., Meulia, T., Dixit, R., Cyr, R. J. and Meier, I. (2004). Arabidopsis WPP-domain proteins are developmentally associated with the nuclear envelope and promote cell division. Plant Cell 16, 3260-3273.
40. Powers, R. W., III, Kaeberlein, M., Caldwell, S. D., Kennedy, B. K. and Fields, S. (2006). Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 20, 174-184.
41. Roberts, P., Moshitch-Moshkovitz, S., Kvam, E., O'Toole, E., Winey, M. and Goldfarb, D. S. (2003). Piecemeal microautophagy of the nucleus in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 129-141.
42. Schmidt, A., Hall, M. N. and Koller, A. (1994). Two FK506 resistance-conferring genes in Saccharomyces cerevisiae, TAT1 and TAT2, encode amino acid permeases mediating tyrosine and tryptophan uptake. Mol. Cell. Biol. 14, 6597-6606.
43. Schmidt, A., Beck, T., Koller, A., Kunz, J. and Hall, M. N. (1998). The TOR nutrient signaling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J. 17, 6924-6931.
44. Sherman, F. (1991). Getting started with yeast. Meth. Enzymol. 194, 3-21.
45. Somech, R., Shaklai, S., Amoriglio, N., Rechavi, G. and Simon, A. J. (2005). Nuclear envelopathies-raising the nuclear veil. Pediatr Res. 57, 8R-15R.
46. Starr, D. A. and Fischer, I A. (2005). KASH 'n Kany: the KASH domain family of cargo-specific cytoskeletal adaptor proteins. BioEssays 27, 1136-1146.
47. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
48. Tyers, M., Tokiwa, G., Nash, R. and Futcher, B. (1992). The Cln3-Cdc28 kinase complex of S. cerevisiae is regulated by proteolysis and phosphorylation. EMBO J 11, 1773-1784.
49. Umebayashi, K. and Nakano, A. (2003). Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. J. Cell Biol. 161, 1117-1131.
50. Voeltz, G. K., Rolls, M. M. and Rapoport, T. A. (2002). Structural organization of the endoplasmic reticulum. EMBO Rep. 3, 944-950.
51. Waizenegger, T., Stan, T., Neupert, W. and Rapaport, D. (2003). Signal-anchor domains of proteins of the outer membrane of mitochondria: structural and functional characteristics. J. Biol. Chem. 278, 42064-42071.
52. Worman, H. J. and Gundersen, G. G. (2006). Here come the SUNs: a nucleocytoskeletal missing link. Trends Cell Biol. 16, 67-69.