A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lysosomal compartments: Class E vps phenotype in mammalian cells

Journal of Cell Science

Volumn 116, Issue 2, 2003, Pages 401-414

  Fujita, Hideaki ^a   Yamanaka, Motoko ^a   Imamura, Kanako ^a   Tanaka, Yoshitaka ^a   Nara, Atsuki ^b   Yoshimori, Tamotsu ^b   Yokota, Sadaki ^c   Himeno, Masaru ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c UNIVERSITY OF YAMANASHI   (Japan)

Author keywords

Class E vps; Hybrid organell; Lysosomes; Membrane traffic; SKD1

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ASIALOGLYCOPROTEIN RECEPTOR; CATHEPSIN D; EPIDERMAL GROWTH FACTOR RECEPTOR; LOW DENSITY LIPOPROTEIN; MUTANT PROTEIN; PROTEIN SKD1; UNCLASSIFIED DRUG;

ANIMAL CELL; CELL ACTIVITY; CELL COMPARTMENTALIZATION; CELL MEMBRANE TRANSPORT; CELL STRAIN; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; GOLGI COMPLEX; LIVER CELL; LYSOSOME; MAMMAL CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; YEAST;

ADENOSINE TRIPHOSPHATASES; ANIMALS; ANTIGENS, CD146; ANTIGENS, CD164; CATHEPSIN D; CELL COMPARTMENTATION; ENDOSOMES; EUKARYOTIC CELLS; HUMANS; INTRACELLULAR MEMBRANES; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MICROSCOPY, ELECTRON; MUTATION; PHENOTYPE; PROTEIN TRANSPORT; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CELL SURFACE; REPRESSOR PROTEINS; TUMOR CELLS, CULTURED;

ANIMALIA; MAMMALIA;

EID: 0037439880     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00213     Document Type: Review

References (50)

1. Babst, M., Sato, T. K., Banta, L. M. and Emr, S. D. (1997). Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. FMBO J. 16, 1820-1831.
2. Babst, M., Wendland, B., Estepa, E. J. and 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.
3. Babst, M., Odorizzi, G., Estepa, E. J. and 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.
4. Barbosa, M. D., Nguyen, Q. A., Tchernev, V. T., Ashley, J. A., Detter, J. C., Blaydes, S. M., Brandt, S. J., Chotai, D., Hodgman, C., Solari, R. C. et al. (1996). Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature 382, 262-265.
5. Bishop, N. and Woodman, P. (2000). ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell 11, 227-239.
6. Bishop, N. and Woodman, P. (2001). TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J. Biol. Chem. 276, 11735-11742.
7. Bright, N. A., Reaves, B. J., Mullock, B. M. and Luzio, J. P. (1997). Dense core lysosomes can fuse with late endosomes and are re-formed from the resultant hybrid organelles. J. Cell Sci. 110, 2027-2040.
8. Chan, J. Y., Lee-Prudhoe, J. E., Jorgensen, B., Ihrke, G., Doyonnas, R., Zannettino, A. C., Buckle, V. J., Ward, C. J., Simmons, P. J. and Watt, S. M. (2001). Relationship between novel isoforms, functionally important domains, and subcellular distribution of CD164/endolyn. J. Biol. Chem. 276, 2139-2152.
9. Croze, E., Ivanov, I. E., Kreibich, G., Adesnik, M., Sabatini, D. D. and Rosenfeld, M. G. (1989). Endolyn-78, a membrane glycoprotein present in morphologically diverse components of the endosomal and lysosomal compartments: implications for lysosome biogenesis. J. Cell Biol. 108, 1597-1613.
10. Fujita, H., Sasano, E., Yasunaga, K., Furuta, K., Yokota, S., Wada, I. and Himeno, M. (2001). Evidence for distinct membrane traffic pathways to melanosomes and lysosomes in melanocytes. J. Investig. Dermatol. Symp. Proc. 6, 19-24.
11. Furuno, K., Ishikawa, T., Akasaki, K., Yano, S., Tanaka, Y., Yamaguchi, Y., Tsuji, H., Himeno, M. and Kato, K. (1989). Morphological localization of a major lysosomal membrane glycoprotein in the endocytic membrane system. J. Biochem. (Tokyo) 106, 708-716.
12. Ghosh, R. N., Mallet, W. G., Soe, T. T., McGraw, T. E. and Maxfield, F. R. (1998). An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J. Cell Biol. 142, 923-936.
13. Gruenberg, J. and Maxfield, F. R. (1995). Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7, 552-563.
14. Hay, J. C. and Scheller, R. H. (1997). SNAREs and NSF in targeted membrane fusion. Curr. Opin. Cell Biol. 9, 505-512.
15. Howard, T. L., Stauffer, D. R., Degnin, C. R. and Hollenberg, S. M. (2001). CHMP1 functions as a member of a newly defined family of vesicle trafficking proteins. J. Cell Sci. 114, 2395-2404.
16. Ihrke, G., Neufeld, E. B., Meads, T., Shanks, M. R., Cassio, D., Laurent, M., Schroer, T. A., Pagano, R. E. and Hubbard, A. L. (1993). WIF-B cells: an in vitro model for studies of hepatocyte polarity. J. Cell Biol. 123, 1761-1775.
17. Ihrke, G., Martin, G. V., Shanks, M. R., Schrader, M., Schroer, T. A. and Hubbard, A. L. (1998). Apical plasma membrane proteins and endolyn-78 travel through a subapical compartment in polarized WIF-B hepatocytes. J. Cell Biol. 141, 115-133.
18. Ihrke, G., Gray, S. R. and Luzio, J. P. (2000). Endolyn is a mucin-like type I membrane protein targeted to lysosomes by its cytoplasmic tail. Biochem J. 345, 287-296.
19. Ihrke, G., Bruns, J. R., Luzio, J. P. and Weisz, O. A. (2001). Competing sorting signals guide endolyn along a novel route to lysosomes in MDCK cells. EMBO J. 20, 6256-6264.
20. Katzmann, D. J., Babst, M. and 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.
21. Kobayashi, T., Stang, E., Fang, K. S., de Moerloose, P., Parton, R. G. and Gruenberg, J. (1998). A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197.
22. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
23. Lippincott-Schwartz, J. and Fambrough, D. M. (1987). Cycling of the integral membrane glycoprotein, LEP100, between plasma membrane and lysosomes: kinetic and morphological analysis. Cell 49, 669-677.
24. Longva, K. E., Blystad, F. D., Stang, E., Larsen, A. M., Johannessen, L. E. and Madshus, I. H. (2002). Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J. Cell Biol. 156, 843-854.
25. Lowry, O. H., Rosenbrough, N. J., Farr, A. L. and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
26. Luzio, J. P., Rous, B. A., Bright, N. A., Pryor, P. R., Mullock, B. M. and Piper, R. C. (2000). Lysosome-endosome fusion and lysosome biogenesis. J. Cell Sci. 113, 1515-1524.
27. Mallet, W. G. and Maxfield, F. R. (1999). Chimeric forms of furin and TGN38 are transported with the plasma membrane in the trans-Golgi network via distinct endosomal pathways. J. Cell Biol. 146, 345-359.
28. Mellman, I. (1996). Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12, 575-625.
29. Mullock, B. M., Bright, N. A., Fearon, C. W., Gray, S. R. and Lazio, J. P. (1998). Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. J. Cell Biol. 140, 591-601.
30. Nakada, H., Sawamura, T. and Tashiro, Y. (1984). Glycosylation of a receptor specific for asialoglycoproteins in rat liver. J. Biochem. (Tokyo) 96, 1609-1617.
31. Nara, A., Mizushima, M., Yamamoto, A., Kabeya, Y., Ohsumi, Y. and Yoshimori, T. (2002). SKD1 AAA ATPase-Dependent endosomal transport is involved in autolysosome formation. Cell Struct. Funct. 27, 29-37.
32. Odorizzi, G., Babst, M. and Emr, S. D. (1998). Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847-858.
33. Parton, R. G., Schrotz, P., Bucci, C. and Gruenberg, J. (1992). Plasticity of early endosomes. J. Cell Sci. 103, 335-348.
34. Perier, F., Coulter, K. L., Liang, H., Radeke, C. M., Gaber, R. F. and Vandenberg, C. A. (1994). Identification of a novel mammalian member of the NSF/CDC48p/Pas1p/TBP-1 family through heterologous expression in yeast. FEBS Lett. 351, 286-290.
35. Piper, R. C., Cooper, A. A., Yang, H. and Stevens, T. H. (1995). VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. J. Cell Biol. 131, 603-617.
36. Pryor, P. R., Mullock, B. M., Bright, N. A., Gray, S. R. and Luzio, J. P. (2000). The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 149, 1053-1062.
37. Raymond, C. K., Howald-Stevenson, I., Vater, C. A. and 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.
38. Reaves, B., Horn, M. and Banting, G. (1993). TGN38/41 recycles between the cell surface and the TGN: brefeldin A affects its rate of return to the TGN. Mol. Biol. Cell 4, 93-105.
39. Reaves, B. J., Row, P. E., Bright, N. A., Luzio, J. P., Davidson, H. W., Ihrke, G., Bruns, J. R. and Weisz, O. A. (2000). Loss of cation-independent mannose 6-phosphate receptor expression promotes the accumulation of lysobisphosphatidic acid in multilamellar bodies. J. Cell Sci. 113, 4099-4108.
40. Rieder, S. E., Banta, L. M., Kohrer, K., McCaffery, J. M. and Emr, S. D. (1996). Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol. Biol. Cell 7, 985-999.
41. Robinson, M. S. and Bonifacino, J. S. (2001). Adaptor-related proteins. Curr Opin. Cell Biol. 13, 444-453.
42. Romagnoli, P., Layet, C., Yewdell, J., Bakke, O. and Germain, R. N. (1993). Relationship between invariant chain expression and major histocompatibility complex class II transport into early and late endocytic compartments. J. Exp. Med. 177, 583-596.
43. Shanks, M. R., Cassio, D., Lecoq, O. and Hubbard, A. L. (1994). An improved polarized rat hepatoma hybrid cell line. Generation and comparison with its hepatoma relatives and hepatocytes in vivo. J. Cell Sci. 107, 813-825.
44. Stenmark, H. and Zerial, H. (2001). Molecular mechanisms of membrane fusion in the endocytic pathway: Oxford University Press.
45. Takahashi, S., Nakagawa, T., Banno, T., Watanabe, T., Murakami, K. and Nakayama, K. (1995). Localization of furin to the trans-Golgi network and recycling from the cell surface involves Set and Tyr residues within the cytoplasmic domain. J. Biol. Chem. 270, 28397-28401.
46. Tanaka, Y., Tanaka, R., Kawabata, T., Noguchi, Y. and Himeno, M. (2000). Lysosomal cysteine protease, cathepsin B, is targeted to lysosomes by the mannose 6-phosphate-independent pathway in rat hepatocytes: site-specific phosphorylation in oligosaccharides of the proregion. J. Biochem. (Tokyo) 128, 39-48.
47. Voorhees, P., Deignan, E., van Donselaar, E., Humphrey, J., Marks, M. S., Peters, P. J. and Bonifacino, J. S. (1995). An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J. 14, 4961-4975.
48. White, J. G. (1966). The Chediak-Higashi syndrome: a possible lysosomal disease. Blood 28, 143-156.
49. Yoshimori, T., Yamagata, F., Yamamoto, A., Mizushima, N., Kabeya, Y., Nara, A., Miwako, I., Ohashi, M., Ohsumi, M. and Ohsumi, Y. (2000). The mouse SKD1, a homologue of yeast Vps4p, is required for normal endosomal trafficking and morphology in mammalian cells. Mol. Biol. Cell 11, 747-763.
50. Zahn, R., Stevenson, B. J., Schroder-Kohne, S., Zanolari, B., Riezman, H. and Munn, A. L. (2001). End13p/Vps4p is required for efficient transport from early to late endosomes in Saccharomyces cerevisiae. J. Cell Sci. 114, 1935-1947.