DOI: 10.1242/jcs.108.11.3509. Yeast ypt51p and mammalian rab5: Counterparts with similar function in the early endocytic pathway

Yeast ypt51p and mammalian rab5: Counterparts with similar function in the early endocytic pathway

10.1242/jcs.108.11.3509

Crossref journal-article

The Company of Biologists

Journal of Cell Science (237)

Abstract

ABSTRACT Ypt51p, a small GTPase of Saccharomyces cerevisiae, has been previously identified as a structural homolog of mammalian Rab5. Although disruption analysis revealed that the protein is required for endocytic transport and for vacuolar protein sorting, the precise step controlled by Ypt51p was not determined. In this work we show that by heterologous expression in animal cells Ypt51p was targeted to Rab5-positive early endosomes and stimulated endocytosis. Furthermore, two Ypt51p mutants induced similar morphological alterations as the corresponding Rab5 mutants. Also in yeast cells Ypt51p was found to be required at an early step in endocytic membrane traffic, since α-factor accumulated in an early endocytic inter-mediate in the absence of Ypt51p. Cell fractionation analysis revealed cofractionation of Ypt51p with endocytic intermediates, while no association with the late Golgi com-partment could be detected. Indirect immunofluorescence microscopy allowed us to morphologically identify the Ypt51p-containing compartment. Similar to the mammalian system larger Ypt51p-positive structures were revealed upon expression of Ypt51p Q66L. These structures were also positive for α-factor receptor and for car-boxypeptidase Y, thus providing direct evidence for their endocytic nature and for the convergence of the vacuolar biosynthetic and endocytic pathways.

Bibliography

Singer-KrÃ¼ger, B., Stenmark, H., & Zerial, M. (1995). Yeast ypt51p and mammalian rab5: Counterparts with similar function in the early endocytic pathway. Journal of Cell Science, 108(11), 3509â3521.

Authors 3

Birgit Singer-Krüger (first)
Harald Stenmark (additional)
Marino Zerial (additional)

References 51 Referenced 70

10.1083/jcb.103.6.2229 / J. Cell Biol / A microtubule-binding protein associated with membranes of the Golgi apparatus by Allan (1986)
10.1091/mbc.4.6.583 / Mol. Biol. Cell / Schizosaccharomyces pombe ypt5: a homologue of the rab5 endosome fusion regulator by Armstrong (1993)
10.1016/S0021-9258(17)32224-X / J. Biol. Chem / Rab5, an early acting endosomal GTPase, supports in vitro endosome fusion without GTP-hydrolysis by Barbieri (1994)
10.1038/362560a0 / Nature / Interactions of three domains distinguishing the Ras-related GTP-binding proteins Ypt1 and Sec4 by Brennwald (1993)
10.1016/0092-8674(92)90306-W / Cell / The small GTP-ase rab5a functions as a regulatory factor in the early endocytic pathway by Bucci (1992)
10.1073/pnas.91.11.5061 / Proc. Nat. Acad. Sci. USA / Rab5a is a common component of the apical and basolateral endocytic machinery in polarized epithelial cells by Bucci (1994)
10.1016/0092-8674(90)90369-P / Cell / Localization of low molecular weight GTP-binding proteins to exocytic and endocytic compartments by Chavrier (1990)
10.1038/353769a0 / Nature / Hypervariable C-terminal domain of rab proteins acts as a targeting signal by Chavrier (1991)
10.1083/jcb.122.1.53 / J. Cell Biol / Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors by Davis (1993)
{'key': '2023122622235573700_JOCES_108_11_3509C10', 'first-page': '679', 'article-title': 'Yeast endocytosis assays', 'volume': '194', 'author': 'Dulic', 'year': '1991', 'journal-title': 'Meth. Enzymol'} / Meth. Enzymol / Yeast endocytosis assays by Dulic (1991)
{'key': '2023122622235573700_JOCES_108_11_3509C11', 'first-page': '3610', 'article-title': 'Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product', 'volume': '5', 'author': 'Evan', 'year': '1985', 'journal-title': 'Mol. Cell. Biol'} / Mol. Cell. Biol / Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product by Evan (1985)
10.1016/0092-8674(91)90316-Q / Cell / Rab5 controls early endosome fusion in vitro by Gorvel (1991)
10.1083/jcb.114.2.207 / J. Cell Biol / Compartmental organization of Golgi-specific protein modification and vacuolar protein sorting events defined in a sec18 (NSF) mutant by Graham (1991)
10.1016/S0092-8674(88)80026-6 / Cell / The mannose 6-phoshate receptor and the biogenesis of lysosomes by Griffiths (1988)
10.1002/j.1460-2075.1994.tb06382.x / EMBO J / VPS21 encodes a rab5-like GTP binding protein that is required for the sorting of yeast vacuolar proteins by Horazdovsky (1994)
10.1016/0955-0674(89)90033-1 / Curr. Opin. Cell Biol / Endocytosis by Hubbard (1989)
10.1083/jcb.113.4.715 / J. Cell Biol / Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast by Jansen (1991)
10.1146/annurev.cb.05.110189.002411 / Annu. Rev. Cell Biol / The biogenesis of lysosomes by Kornfeld (1989)
10.1002/j.1460-2075.1993.tb05947.x / EMBO J / Actin and fimbrin are required for the internalization step of endocytosis in yeast by Kübler (1993)
10.1002/j.1460-2075.1994.tb06891.x / EMBO J / Calcium-independent calmodulin requirement for endocytosis in yeast by Kübler (1994)
10.1038/227680a0 / Nature / Cleavage of structural proteins during the assembly of the head of the bacteriophage T4 by Laemmli (1970)
10.1016/S0021-9258(20)80550-X / J. Biol. Chem / Structure-function relationship of the small GTPase rab5 by Li (1993)
10.1002/j.1460-2075.1983.tb01640.x / EMBO J / A monoclonal antibody to the heavy chain of clathrin by Louvard (1983)
10.1083/jcb.115.6.1561 / J. Cell Biol / Distribution of newly synthesized lysosomal enzymes in the endocytic pathway of normal rat kidney cells by Ludwig (1991)
10.1083/jcb.125.2.381 / J. Cell Biol / Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane by Mulholland (1994)
10.1083/jcb.127.2.373 / J. Cell Biol / Endocytosis is required for the growth of vacuolar H+-ATPase-defective yeast: identification of six new END genes by Munn (1994)
10.1242/jcs.106.4.1249 / J. Cell Sci / Molecular cloning and subcellular localization of three GTP-binding proteins of the rab subfamily by Olkkonen (1993)
10.1083/jcb.106.5.1453 / J. Cell Biol / Protein transport to the vacuole and receptor-mediated endocytosis by clathrin heavy chain-deficient yeast by Payne (1988)
10.1016/0003-2697(77)90043-4 / Anal. Biochem / A simplification of the protein assay of Lowry et al. which is more generally applicable by Peterson (1977)
10.1073/pnas.91.6.1987 / Proc. Nat. Acad. Sci. USA / Clues to brain function from bakers’ yeast by Pfeffer (1994)
10.1083/jcb.120.1.55 / J. Cell Biol / end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae by Raths (1993)
10.1091/mbc.3.12.1389 / Mol. Biol. Cell / Morphological classification of the yeast vacuolar protein sorting mutants: Evidence for a prevacuolar compartment in class E vps mutants by Raymond (1992)
10.1016/0092-8674(85)90360-5 / Cell / Endocytosis in yeast: several of the yeast secretory mutants are defective in endocytosis by Riezman (1985)
10.1016/0076-6879(91)94047-G / Meth. Enzymol / Methods for studying the yeast vacuole by Roberts (1991)
10.1242/jcs.106.3.823 / J. Cell Sci / Involvement of Ypt7p, a small GTP-binding protein, in traffic from late endosome to the vacuole in yeast by Schimmöller (1993)
10.1083/jcb.110.6.1911 / J. Cell Biol / Detection of an intermediate compartment involved in transport of α-factor from the plasma membrane to the vacuole in yeast by Singer (1990)
10.1016/S0021-9258(19)85250-X / J. Biol. Chem / Partial purification and characterization of early and late endosomes from yeast by Singer-Krüger (1993)
10.1083/jcb.125.2.283 / J. Cell Biol / Role of three rab5-like GTPases, Ypt51p, Ypt52p, and Ypt53p, in the endocytic and vacuolar protein sorting pathways of yeast by Singer-Krüger (1994)
10.1002/j.1460-2075.1994.tb06295.x / EMBO J / Distinct structural elements of rab5 define its functional specificity by Stenmark (1994)
10.1002/j.1460-2075.1994.tb06381.x / EMBO J / Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis by Stenmark (1994)
10.1016/S0076-6879(95)57021-7 / Meth. Enzymol / Expression of Rab GTPases using recombinant vaccinia viruses by Stenmark (1995)
{'key': '2023122622235573700_JOCES_108_11_3509C42', 'first-page': '197', 'article-title': 'A new method using p-benzoquinone for coupling antigens and antibodies to marker substances', 'volume': '127C', 'author': 'Ternynck', 'year': '1976', 'journal-title': 'Annu. Immunol. (Inst. Pasteur)'} / Annu. Immunol. (Inst. Pasteur) / A new method using p-benzoquinone for coupling antigens and antibodies to marker substances by Ternynck (1976)
10.1073/pnas.76.9.4350 / Proc. Nat. Acad. Sci. USA / Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications by Towbin (1979)
10.1016/S0021-9258(17)46822-0 / J. Biol. Chem / Rab GDI as a general regulator for the membrane association of rab proteins by Ullrich (1993)
10.1177/35.3.3546482 / J. Histochem. Cytochem / Immunolocalization of glyceraldehyde-3-phosphate dehydrogenase, hexokinase, and carboxypeptidase Y in yeast cells at the ultrastructural level by van Tuinen (1987)
10.1083/jcb.121.6.1245 / J. Cell Biol / Yeast vacuolar proenzymes are sorted in the late Golgi complex and transported to the vacuole via a prevacuolar endosome-like compartment by Vida (1993)
10.1016/S0092-8674(05)80062-5 / Cell / Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p) by Wichmann (1992)
{'key': '2023122622235573700_JOCES_108_11_3509C48', 'first-page': '5251', 'article-title': 'Quantitation of α-factor internalization and response during the Saccharomyces cerevisiae cell cycle', 'volume': '11', 'author': 'Zanolari', 'year': '1991', 'journal-title': 'Mol. Cell. Biol'} / Mol. Cell. Biol / Quantitation of α-factor internalization and response during the Saccharomyces cerevisiae cell cycle by Zanolari (1991)
10.1016/0092-8674(92)90552-N / Cell / Yeast pheromone receptor endocytosis and hyperphosphorylation are independent of G protein-mediated signal transduction by Zanolari (1992)
10.1016/0076-6879(92)19039-9 / Meth. Enzymol / Localization of Rab family members in animal cells by Zerial (1992)
10.1016/0955-0674(93)90130-I / Curr. Opin. Cell Biol / Rab GTPases in vesicular transport by Zerial (1993)

Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 10:30 p.m.)
Deposited	1 year, 8 months ago (Dec. 26, 2023, 5:24 p.m.)
Indexed	1 year, 6 months ago (Feb. 16, 2024, 7:32 p.m.)
Issued	29 years, 9 months ago (Nov. 1, 1995)
Published	29 years, 9 months ago (Nov. 1, 1995)
Published Online	29 years, 9 months ago (Nov. 1, 1995)
Published Print	29 years, 9 months ago (Nov. 1, 1995)

Funders 0

None

BibTeX

@article{Singer_Kr_ger_1995, title={Yeast ypt51p and mammalian rab5: Counterparts with similar function in the early endocytic pathway}, volume={108}, ISSN={1477-9137}, url={http://dx.doi.org/10.1242/jcs.108.11.3509}, DOI={10.1242/jcs.108.11.3509}, number={11}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Singer-Krüger, Birgit and Stenmark, Harald and Zerial, Marino}, year={1995}, month=nov, pages={3509–3521} }

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