Interaction of the phospholipid flippase Drs2p with the F-box protein Rcy1p plays an important role in early endosome to trans-Golgi network vesicle transport in yeast

Journal of Biochemistry

Volumn 155, Issue 1, 2014, Pages 51-62

  Hanamatsu, Hisatoshi ^a   Fujimura Kamada, Konomi ^a,b   Yamamoto, Takaharu ^a   Furuta, Nobumichi ^a,c   Tanaka, Kazuma ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^c Yamagata Mogami Livestock Hygiene Center   (Japan)

Author keywords

endocytic recycling; flippases; P4 ATPases; phospholipid asymmetry; yeast

Indexed keywords

DRS2P PROTEIN; F BOX PROTEIN; PHOSPHOLIPID; RCY1P PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; ENDOSOME; GENOTYPE; IMMUNOPRECIPITATION; NONHUMAN; PHENOTYPE; POINT MUTATION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; TRANS GOLGI NETWORK; TRANSPORT VESICLE; WESTERN BLOTTING; YEAST;

ENDOCYTIC RECYCLING; FLIPPASES; P4-ATPASES; PHOSPHOLIPID ASYMMETRY; YEAST;

AMINO ACID SEQUENCE; BASE SEQUENCE; BLOTTING, WESTERN; CALCIUM-TRANSPORTING ATPASES; CYTOPLASM; DNA PRIMERS; ENDOSOMES; F-BOX PROTEINS; GOLGI APPARATUS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 84892756328     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvt094     Document Type: Article

References (39)

1. Lenoir, G., Williamson, P., and Holthuis, J.C. (2007) On the origin of lipid asymmetry: the flip side of ion transport. Curr. Opin. Chem. Biol. 11, 654-661
2. Tanaka, K., Fujimura-Kamada, K., and Yamamoto, T. (2011) Functions of phospholipid flippases. J. Biochem. 149, 131-143
3. Sebastian, T.T., Baldridge, R.D., Xu, P., and Graham, T.R. (2012) Phospholipid flippases: Building asymmetric membranes and transport vesicles. Biochim. Biophys. Acta 1821, 1068-1077
4. Saito, K., Fujimura-Kamada, K., Furuta, N., Kato, U., Umeda, M., and Tanaka, K. (2004) Cdc50p, a protein required for polarized growth, associates with the Drs2p P-type ATPase implicated in phospholipid translocation in Saccharomyces cerevisiae. Mol. Biol. Cell 15, 3418-3432
5. Furuta, N., Fujimura-Kamada, K., Saito, K., Yamamoto, T., and Tanaka, K. (2007) Endocytic recycling in yeast is regulated by putative phospholipid translocases and the Ypt31p/32p-Rcy1p pathway. Mol. Biol. Cell 18, 295-312
6. Chen, C.Y., Ingram, M.F., Rosal, P.H., and Graham, T.R. (1999) Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J. Cell Biol. 147, 1223-1236
7. Hua, Z., Fatheddin, P., and Graham, T.R. (2002) An essential subfamily of Drs2p-related P-type ATPases is required for protein trafficking between Golgi complex and endosomal/vacuolar system. Mol. Biol. Cell 13, 3162-3177
8. Pomorski, T., Lombardi, R., Riezman, H., Devaux, P.F., van Meer, G., and Holthuis, J.C. (2003) Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol. Biol. Cell 14, 1240-1254
9. Misu, K., Fujimura-Kamada, K., Ueda, T., Nakano, A., Katoh, H., and Tanaka, K. (2003) Cdc50p, a conserved endosomal membrane protein, controls polarized growth in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 730-747
10. Kelly, B.T. and Owen, D.J. (2011) Endocytic sorting of transmembrane protein cargo. Curr. Opin. Cell Biol. 23, 404-412
11. Valdivia, R.H., Baggott, D., Chuang, J.S., and Schekman, R.W. (2002) The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev. Cell 2, 283-294
12. Foote, C. and Nothwehr, S.F. (2006) The clathrin adaptor complex 1 directly binds to a sorting signal in Ste13p to reduce the rate of its trafficking to the late endosome of yeast. J. Cell Biol. 173, 615-626
13. Sakane, H., Yamamoto, T., and Tanaka, K. (2006) The functional relationship between the Cdc50p-Drs2p putative aminophospholipid translocase and the Arf GAP Gcs1p in vesicle formation in the retrieval pathway from yeast early endosomes to the TGN. Cell Struct. Funct. 31, 87-108
14. Liu, K., Surendhran, K., Nothwehr, S.F., and Graham, T.R. (2008) P4-ATPase requirement for AP-1/clathrin function in protein transport from the trans-Golgi network and early endosomes. Mol. Biol. Cell 19, 3526-3535
15. Wiederkehr, A., Avaro, S., Prescianotto-Baschong, C., Haguenauer-Tsapis, R., and Riezman, H. (2000) The F-box protein Rcy1p is involved in endocytic membrane traffic and recycling out of an early endosome in Saccharomyces cerevisiae. J. Cell Biol. 149, 397-410
16. Galan, J.M., Wiederkehr, A., Seol, J.H., Haguenauer-Tsapis, R., Deshaies, R.J., Riezman, H., and Peter, M. (2001) Skp1p and the F-box protein Rcy1p form a non-SCF complex involved in recycling of the SNARE Snc1p in yeast. Mol. Cell. Biol. 21, 3105-3117
17. Chen, S.H., Chen, S., Tokarev, A.A., Liu, F., Jedd, G., and Segev, N. (2005) Ypt31/32 GTPases and their novel F-box effector protein Rcy1 regulate protein recycling. Mol. Biol. Cell 16, 178-192
18. Jackson, P.K. and Eldridge, A.G. (2002) The SCF ubiquitin ligase: an extended look. Mol. Cell 9, 923-925
19. Cardozo, T. and Pagano, M. (2004) The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751
20. Kus, B.M., Caldon, C.E., Andorn-Broza, R., and Edwards, A.M. (2004) Functional interaction of 13 yeast SCF complexes with a set of yeast E2 enzymes in vitro. Proteins 54, 455-467
21. Rose, M.D., Winston, F., and Hieter, P. (1990) Methods in Yeast Genetics: A Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
22. Guthrie, C. and Fink, G.R. (1991) Guide to Yeast Genetics and Molecular Biology. Academic Press, San Diego, CA
23. Elble, R. (1992) A simple and efficient procedure for transformation of yeasts. Biotechniques 13, 18-20
24. Gietz, R.D. and Woods, R.A. (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96
25. Goldstein, A.L. and McCusker, J.H. (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553
26. Durfee, T., Becherer, K., Chen, P.L., Yeh, S.H., Yang, Y., Kilburn, A.E., Lee, W.H., and Elledge, S.J. (1993) The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 7, 555-569
27. Gietz, R.D. and Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534
28. Lewis, M.J., Nichols, B.J., Prescianotto-Baschong, C., Riezman, H., and Pelham, H.R. (2000) Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol. Biol. Cell 11, 23-38
29. James, P., Halladay, J., and Craig, E.A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436
30. Imamura, H., Tanaka, K., Hihara, T., Umikawa, M., Kamei, T., Takahashi, K., Sasaki, T., and Takai, Y. (1997) Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J. 16, 2745-2755
31. Hollenberg, S.M., Sternglanz, R., Cheng, P.F., and Weintraub, H. (1995) Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol. Cell. Biol. 15, 3813-3822
32. Toi, H., Fujimura-Kamada, K., Irie, K., Takai, Y., Todo, S., and Tanaka, K. (2003) She4p/Dim1p interacts with the motor domain of unconventional myosins in the budding yeast, Saccharomyces cerevisiae. Mol. Biol. Cell 14, 2237-2249
33. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59
34. Ripmaster, T.L., Vaughn, G.P., and Woolford, J.L. Jr (1993) DRS1 to DRS7, novel genes required for ribosome assembly and function in Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 7901-7912
35. Chantalat, S., Park, S.K., Hua, Z., Liu, K., Gobin, R., Peyroche, A., Rambourg, A., Graham, T.R., and Jackson, C.L. (2004) The Arf activator Gea2p and the P-type ATPase Drs2p interact at the Golgi in Saccharomyces cerevisiae. J. Cell. Sci. 117, 711-722
36. Park, S.K., Hartnell, L.M., and Jackson, C.L. (2005) Mutations in a highly conserved region of the Arf1p activator GEA2 block anterograde Golgi transport but not COPI recruitment to membranes. Mol. Biol. Cell 16, 3786-3799
37. Tsai, P.C., Hsu, J.W., Liu, Y.W., Chen, K.Y., and Lee, F.J. (2013) Arl1p regulates spatial membrane organization at the trans-Golgi network through interaction with Arf-GEF Gea2p and flippase Drs2p. Proc. Natl Acad. Sci. USA 110, E668-E677
38. Natarajan, P., Liu, K., Patil, D.V., Sciorra, V.A., Jackson, C.L., and Graham, T.R. (2009) Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat. Cell Biol. 11, 1421-1426
39. Chen, S.H., Shah, A.H., and Segev, N. (2011) Ypt31/32 GTPases and their F-Box effector Rcy1 regulate ubiquitination of recycling proteins. Cell. Logist. 1, 21-31