1887

Abstract

The multivesicular body (MVB) sorting pathway is required for a number of biological processes, including downregulation of cell-surface proteins and protein sorting into the vacuolar lumen. The function of this pathway requires endosomal sorting complexes required for transport (ESCRT) composed of class E vacuolar protein sorting (Vps) proteins in , many of which are conserved in . Of these, / (homologous to ) and (similar to ) have been identified as suppressors of sterility in Δ (), although their functions have not been uncovered to date. In this report, these two genes are shown to be required for vacuolar sorting of carboxypeptidase Y (CPY) and an MVB marker, the ubiquitin–GFP–carboxypeptidase S (Ub–GFP–CPS) fusion protein, despite the lack of the ubiquitin E2 variant domain in Sst6p. Disruption mutants of a variety of other class E homologues also had defects in sorting of CPY and Ub–GFP–CPS. has a mammalian AMSH homologue, . Phenotypic analyses suggested that Sst2p is a class E Vps protein. Taken together, these results suggest that sorting into multivesicular bodies is dependent on class E Vps proteins, including Sst2p, in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/006072-0
2007-08-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/8/2753.html?itemId=/content/journal/micro/10.1099/mic.0.2007/006072-0&mimeType=html&fmt=ahah

References

  1. Agromayor M., Martin-Serrano J. 2006; Interaction of AMSH with ESCRT-III and deubiquitination of endosomal cargo. J Biol Chem 281:23083–23091
    [Google Scholar]
  2. Alfa C., Fantes P., Hyams J., McLeod M., Warbrick E. 1993 Experiments with Fission Yeast : a Laboratory Course Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  3. Alwan H. A. J., van Leeuwen J. E. M. 2007; UBPY-mediated EGFR deubiquitination promotes EGFR degradation. J Biol Chem 282:1658–1669
    [Google Scholar]
  4. Amerik A. Y., Nowak J., Swaminathan S., Hochstrasser M. 2000; The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol Biol Cell 11:3365–3380
    [Google Scholar]
  5. Babst M. 2005; A protein's final ESCRT. Traffic 6:2–9
    [Google Scholar]
  6. Babst M., Sato T. K., Banta L. M., Emr S. D. 1997; Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J 16:1820–1831
    [Google Scholar]
  7. Babst M., Wendland B., Estepa E. J., Emr S. D. 1998; The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 17:2982–2993
    [Google Scholar]
  8. Babst M., Odorizzi G., Estepa E. J., Emr S. D. 2000; Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1:248–258
    [Google Scholar]
  9. Babst M., Katzmann D. J., Estepa-Sabal E. J., Meerloo T., Emr S. D. 2002; ESCRT-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev Cell 3:271–282
    [Google Scholar]
  10. Bache K. G., Slagsvold T., Cabezas A., Rosendal K. R., Raiborg C., Stenmark H. 2004; The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol Biol Cell 15:4337–4346
    [Google Scholar]
  11. Banta L. M., Robinson J. S., Klionsky D. J., Emr S. D. 1988; Organelle assembly in yeast: characterization of yeast mutants defective in vacuolar biogenesis and protein sorting. J Cell Biol 107:1369–1383
    [Google Scholar]
  12. Bilodeau P. S., Urbanowski J. L., Winistorfer S. C., Piper R. C. 2002; The Vps27p-Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat Cell Biol 4:534–539
    [Google Scholar]
  13. Bishop N., Woodman P. 2001; TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J Biol Chem 276:11735–11742
    [Google Scholar]
  14. Bowers K., Stevens T. H. 2005; Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae . Biochim Biophys Acta 1744438–454
    [Google Scholar]
  15. Bowers K., Piper S. C., Edeling M. A., Gray S. R., Owen D. J., Lehner P. J., Luzio J. P. 2006; Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class I is independent of mammalian ESCRT II. J Biol Chem 281:5094–5105
    [Google Scholar]
  16. Burd C. G., Emr S. D. 1998; Phosphatidylinositol (3)-phosphate signaling mediated by specific binding to RING FYVE domains. Mol Cell 2:157–162
    [Google Scholar]
  17. Cheng H., Sugiura R., Wu W., Fujita M., Lu Y., Sio S. O., Kawai R., Takegawa K., Shuntoh H., Kuno T. 2002; Role of the Rab GTP-binding protein Ypt3 in the fission yeast exocytic pathway, and its connection to calcineurin function. Mol Biol Cell 13:2963–2976
    [Google Scholar]
  18. Dupré S., Haguenauer-Tsapis R. 2001; Deubiquitination in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol Cell Biol 21:4482–4494
    [Google Scholar]
  19. Eastman S. W., Martin-Serrano J., Chung W., Zang T., Bieniasz P. D. 2005; Identification of human VPS37C, a component of endosomal sorting complex required for transport-I important for viral budding. J Biol Chem 280:628–636
    [Google Scholar]
  20. Hicke L. 1999; Gettin' down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol 9:107–112
    [Google Scholar]
  21. Hirota K., Tanaka K., Watanabe Y., Yamamoto M. 2001; Functional analysis of the C-terminal cytoplasmic region of the M-factor receptor in fission yeast. Genes Cells 6:201–214
    [Google Scholar]
  22. Iwaki T., Takegawa K. 2004; A set of loxP marker cassettes for Cre-mediated multiple gene disruption in Schizosaccharomyces pombe . Biosci Biotechnol Biochem 68:545–550
    [Google Scholar]
  23. Iwaki T., Tanaka N., Takagi H., Giga-Hama Y., Takegawa K. 2004; Characterization of end4+ , a gene required for endocytosis in Schizosaccharomyces pombe . Yeast 21:867–881
    [Google Scholar]
  24. Jin Y., Mancuso J. J., Cronembold D., Cande W. Z. 2005; The fission yeast homolog of the human transcription factor EAP30 blocks meiotic spindle pole body amplification. Dev Cell 9:63–73
    [Google Scholar]
  25. Katz M., Shtiegman K., Tal-Or P., Yakir L., Mosesson Y., Harari D., Machluf Y., Asao H., Jovin T. other authors 2002; Ligand-independent degradation of epidermal growth factor receptor involves receptor ubiquitylation and Hgs, an adaptor whose ubiquitin-interacting motif targets ubiquitylation by Nedd4. Traffic 3:740–751
    [Google Scholar]
  26. Katzmann D. J., Babst M., Emr S. D. 2001; Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106:145–155
    [Google Scholar]
  27. Katzmann D. J., Sarkar S., Chu T., Audhya A., Emr S. D. 2004; Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase S. Mol Biol Cell 15:468–480
    [Google Scholar]
  28. Koga T., Onishi M., Nakamura Y., Hirata A., Nakamura T., Shimoda C., Iwaki T., Takegawa K., Fukui Y. 2004; Sorting nexin homologues are targets of phosphatidylinositol 3-phosphate in sporulation of Schizosaccharomyces pombe . Genes Cells 9:561–574
    [Google Scholar]
  29. Krsmanović T., Pawelec A., Sydor T., Kölling R. 2005; Control of Ste6 recycling by ubiquitination in the early endocytic pathway in yeast. Mol Biol Cell 16:2809–2821
    [Google Scholar]
  30. Lohi O., Poussu A., Mao Y., Quiocho F., Lehto V.-P. 2002; VHS domain – a longshoreman of vesicle lines. FEBS Lett 513:19–23
    [Google Scholar]
  31. McCullough J., Clague M. J., Urbé S. 2004; AMSH is an endosome-associated ubiquitin isopeptidase. J Cell Biol 166:487–492
    [Google Scholar]
  32. McEwen R. K., Dove S. K., Cooke F. T., Painter G. F., Holmes A. B., Shisheva A., Ohya Y., Parker P. J., Michell R. H. 1999; Complementation analysis in PrdIns P kinase-deficient yeast mutants demonstrates that Schizosaccharomyces pombe and murine Fab1p homologues are phosphatidylinositol 3-phosphate 5-kinases. J Biol Chem 274:33905–33912
    [Google Scholar]
  33. Mitra P., Zhang Y., Rameh L. E., Ivshina M. P., McCollum D., Nunnari J. J., Hendricks G. M., Kerr M. L., Field S. J. other authors 2004; A novel phosphatidylinositol(3,4,5)P3 pathway in fission yeast. J Cell Biol 166:205–211
    [Google Scholar]
  34. Mizuno E., Iura T., Mukai A., Yoshimori T., Kitamura N., Komada M. 2005; Regulation of epidermal growth factor receptor down-regulation by UBPY-mediated deubiquitination at endosomes. Mol Biol Cell 16:5163–5174
    [Google Scholar]
  35. Mizuno E., Kobayashi K., Yamamoto A., Kitamura N., Komada M. 2006; A deubiquitinating enzyme UBPY regulates the level of protein ubiquitination on endosomes. Traffic 7:1017–1031
    [Google Scholar]
  36. Moreno S., Klar A., Nurse P. 1991; Molecular genetic analysis of fission yeast Schizosaccharomyces pombe . Methods Enzymol 194:795–823
    [Google Scholar]
  37. Morishita M., Morimoto F., Kitamura K., Koga T., Fukui Y., Maekawa H., Yamashita I., Shimoda C. 2002; Phosphatidylinositol 3-phosphate 5-kinase is required for the cellular response to nutritional starvation and mating pheromone signals in Schizosaccharomyces pombe . Genes Cells 7:199–215
    [Google Scholar]
  38. Morita T., Takegawa K. 2004; A simple and efficient procedure for transformation of Schizosaccharomyces pombe . Yeast 21:613–617
    [Google Scholar]
  39. Murray J. M., Johnson D. I. 2001; The Cdc42p GTPase and its regulators of Nrf1p and Scd1p are involved in endocytic trafficking in the fission yeast Schizosaccharomyces pombe . J Biol Chem 276:3004–3009
    [Google Scholar]
  40. Nakamura T., Nakamura-Kubo M., Hirata A., Shimoda C. 2001; The Schizosaccharomyces pombe spo3 + gene is required for assembly of the forespore membrane and genetically interacts with psy1 +-encoding syntaxin-like protein. Mol Biol Cell 12:3955–3972
    [Google Scholar]
  41. Odorizzi G., Babst M., Emr S. D. 1998; Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95:847–858
    [Google Scholar]
  42. Okazaki K., Okazaki N., Kume K., Jinno S., Tanaka K., Okayama H. 1990; High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe . Nucleic Acids Res 18:6485–6489
    [Google Scholar]
  43. Onishi M., Nakamura Y., Koga T., Takegawa K., Fukui Y. 2003; Isolation of suppressor mutants of phosphatidylinositol 3-phosphate 5-kinase deficient cells in Schizosaccharomyces pombe . Biosci Biotechnol Biochem 67:1772–1779
    [Google Scholar]
  44. Piper R. C., Luzio J. P. 2001; Late endosomes: sorting and partitioning in multivesicular bodies. Traffic 2:612–621
    [Google Scholar]
  45. Piper R. C., Cooper A. A., Yang H., Stevens T. H. 1995; VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae . J Cell Biol 131:603–617
    [Google Scholar]
  46. Polo S., Sigismund S., Faretta M., Guidi M., Capua M. R., Bossi G., Chen H., De Camilli P., Di Fiore P. P. 2002; A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416:451–455
    [Google Scholar]
  47. Raymond C. K., Howald-Stevenson I., Vater C. A., Stevens T. H. 1992; Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell 3:1389–1402
    [Google Scholar]
  48. Reggiori F., Pelham H. R. B. 2001; Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J 20:5176–5186
    [Google Scholar]
  49. Rieder S. E., Banta L. M., Kohrer K., McCaffery J. M., Emr S. D. 1996; Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol Biol Cell 7:985–999
    [Google Scholar]
  50. Row P. E., Prior I. A., McCullough J., Clague M. J., Urbé S. 2006; The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J Biol Chem 281:12618–12624
    [Google Scholar]
  51. Shih S. C., Katzmann D. J., Schnell J. D., Sutanto M., Emr S. D., Hicke L. 2002; Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat Cell Biol 4:389–393
    [Google Scholar]
  52. Soetens O., De Craene J.-O., André B. 2001; Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J Biol Chem 276:43949–43957
    [Google Scholar]
  53. Suga M., Hatakeyama T. 2001; High efficiency transformation of Schizosaccharomyces pombe pretreated with thiol compounds by electroporation. Yeast 18:1015–1021
    [Google Scholar]
  54. Suga M., Isobe M., Hatakeyama T. 2000; Cryopreservation of competent intact yeast cells for efficient electroporation. Yeast 16:889–896
    [Google Scholar]
  55. Tabuchi M., Iwaihara O., Ohtani Y., Ohuchi N., Sakurai J., Morita T., Iwahara S., Takegawa K. 1997; Vacuolar protein sorting in fission yeast: cloning, biosynthesis, transport, and processing of carboxypeptidase Y from Schizosaccharomyces pombe . J Bacteriol 179:4179–4189
    [Google Scholar]
  56. Takegawa K., DeWald D. B., Emr S. D. 1995; Schizosaccharomyces pombe Vps34p, a phosphatidylinositol-specific PI 3-kinase essential for normal cell growth and vacuole morphology. J Cell Sci 108:3745–3756
    [Google Scholar]
  57. Takegawa K., Iwaki T., Fujita Y., Morita T., Hosomi A., Tanaka N. 2003; Vesicle-mediated protein transport pathways to the vacuole in Schizosaccharomyces pombe . Cell Struct Funct 28:399–417
    [Google Scholar]
  58. Tanaka N., Kaneko K., Asao H., Kasai H., Endo Y., Fujita T., Takeshita T., Sugamura K. 1999; Possible involvement of a novel STAM-associated molecule ‘AMSH’ in intracellular signal transduction mediated by cytokines. J Biol Chem 274:19129–19135
    [Google Scholar]
  59. Tsang H. T. H., Connell J. W., Brown S. E., Thompson A., Reid E., Sanderson C. M. 2006; A systematic analysis of human CHMP protein interactions: additional MIT domain-containing proteins bind to multiple components of the human ESCRT III complex. Genomics 88:333–346
    [Google Scholar]
  60. Vida T. A., Emr S. D. 1995; A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128:779–792
    [Google Scholar]
  61. Winter V., Hauser M.-T. 2006; Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci 11:115–123
    [Google Scholar]
  62. Young P., Deveraux Q., Beal R. E., Pickart C. M., Rechsteiner M. 1998; Characterization of two polyubiquitin binding sites in the 26 S protease subunit 5a. J Biol Chem 273:5461–5467
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/006072-0
Loading
/content/journal/micro/10.1099/mic.0.2007/006072-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error