Isolation and characterization of novel mutations in CDC50, the non-catalytic subunit of the Drs2p phospholipid flippase

Journal of Biochemistry

Volumn 149, Issue 4, 2011, Pages 423-432

  Takahashi, Yasuhiro ^a,b   Fujimura Kamada, Konomi ^a   Kondo, Satoshi ^b   Tanaka, Kazuma ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

flippase; phospholipid asymmetry; type 4 P type ATPase; yeast

Indexed keywords

MEMBRANE PROTEIN; MUTANT PROTEIN; PHOSPHOLIPASE; PHOSPHOLIPID FLIPPASE; PROTEIN CDC50; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; DELETION MUTANT; ENDOSOME; ENZYME SUBUNIT; GENE MUTATION; IMMUNOPRECIPITATION; NUCLEOTIDE SEQUENCE; PHOSPHOLIPID TRANSFER; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; TEMPERATURE; TRANS GOLGI NETWORK;

EID: 79953221826     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvq155     Document Type: Article

References (39)

1. Devaux, P.F. (1991) Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30, 1163-1173
2. Cerbon, J. and Calderon, V. (1991) Changes of the com-positional asymmetry of phospholipids associated to the increment in the membrane surface potential. Biochim. Biophys. Acta 1067, 139-144
3. Diaz, C. and Schroit, A.J. (1996) Role oftranslocases in the generation of phosphatidylserine asymmetry. J. Membr. Biol. 151, 1-9 (Pubitemid 26164252)
4. Paulusma, C.C. and Oude Elferink, R.P. (2005) The type 4 subfamily of P-type ATPases, putative aminophospho-lipid translocases with a role in human disease. Biochim. Biophys. Acta 1741, 11-24 (Pubitemid 40824985)
5. 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 (Pubitemid 35034253)
6. 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 mem-brane and serve a role in endocytosis. Mol. Biol. Cell 14, 1240-1254 (Pubitemid 36337466)
7. 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 (Pubitemid 38850134)
8. Natarajan, P., Wang, J., Hua, Z., and Graham, T.R. (2004) Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc. Natl. Acad. Sci. USA 101, 10614-10619 (Pubitemid 38955790)
9. Alder-Baerens, N., Lisman, Q., Luong, L., Pomorski, T., and Holthuis, J.C. (2006) Loss of P4 ATPases Drs2p and Dnf3p disrupts aminophospholipid transport and asym-metry in yeast post-Golgi secretory vesicles. Mol. Biol. Cell 17, 1632-1642 (Pubitemid 44011581)
10. Zhou, X. and Graham, T.R. (2009) Reconstitution of phospholipid translocase activity with purified Drs2p, a type-IV P-type ATPase from budding yeast. Proc. Natl. Acad. Sci. USA 106, 16586-16591
11. Coleman, J., Kwok, M., and Molday, R. (2009) Localization, purification, and functional reconstitution of the P4-ATPase Atp8a2, a phosphatidylserine flippase in photoreceptor disc membranes. J. Biol. Chem. 284, 32670-32679
12. 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 (Pubitemid 36237028)
13. Radji, M., Kim, J.M., Togan, T., Yoshikawa, H., and Shirahige, K. (2001) The cloning and characterization of the CDC50 gene family in Saccharomyces cerevisiae. Yeast 18, 195-205
14. Kato, U., Emoto, K., Fredriksson, C., Nakamura, H., Ohta, A., Kobayashi, T., Murakami-Murofushi, K., Kobayashi, T., and Umeda, M. (2002) A novel mem-brane protein, Ros3p, is required for phospholipid trans-location across the plasma membrane in Saccharomyces cerevisiae. J. Biol. Chem. 277, 37855-37862
15. Hanson, P., Malone, L., Birchmore, J., and Nichols, J. (2003) Lem3p is essential for the uptake and potency of alkylphosphocholine drugs, edelfosine and miltefosine. J. Biol. Chem. 278, 36041-36050 (Pubitemid 37139924)
16. Furuta, N., Fujimura-Kamada, K., Saito, K., Yamamoto, T., and Tanaka, K. (2007) Endocytic recy-cling in yeast is regulated by putative phospholipid trans-locases and the Ypt31p/32p-Rcy1p pathway. Mol. Biol. Cell 18, 295-312 (Pubitemid 46074966)
17. Chen, S., Wang, J., Muthusamy, B.P., Liu, K., Zare, S., Andersen, R.J., and Graham, T.R. (2006) Roles for the Drs2p-Cdc50p complex in protein transport and phos-phatidylserine asymmetry of the yeast plasma membrane. Traffic 7, 1503-1517 (Pubitemid 44524523)
18. Paulusma, C.C., Folmer, D.E., Ho-Mok, K.S., de Waart, D.R., Hilarius, P.M., Verhoeven, A.J., and Oude Elferink, R.P. (2008) ATP8B1 requires an acces-sory protein for endoplasmic reticulum exit and plasma membrane lipid flippase activity. Hepatology 47, 268-278 (Pubitemid 351171064)
19. Poulsen, L., Lopez-Marques, R., McDowell, S., Okkeri, J., Licht, D., Schulz, A., Pomorski, T., Harper, J., and Palmgren, M. (2008) The Arabidopsis P4-ATPase ALA3 localizes to the Golgi and requires a β-subunit to func-tion in lipid translocation and secretory vesicle forma-tion. Plant Cell 20, 658-676 (Pubitemid 352844000)
20. Lopez-Marques, R., Poulsen, L., Hanisch, S., Meffert, K., Buch-Pedersen, M., Jakobsen, M., Pomorski, T., and Palmgren, M. (2010) Intracellular targeting signals and lipid specificity determinants of the ALA/ALIS P4-ATPase complex reside in the catalytic ALA α-subunit. Mol. Biol. Cell 21, 791-801
21. Perez-Victoria, F.J., Sanchez-Canete, M.P., Castanys, S., and Gamarro, F. (2006) Phospholipid translocation and miltefosine potency require both L. donovani miltefosine transporter and the new protein LdRos3 in Leishmania parasites. J. Biol. Chem. 281, 23766-23775 (Pubitemid 44274152)
22. Lenoir, G., Williamson, P., Puts, C.F., and Holthuis, J.C. (2009) Cdc50p plays a vital role in the ATPase re-action cycle of the putative aminophospholipid trans-porter Drs2p. J. Biol. Chem. 284, 17956-17967
23. Rose, M.D., Winston, F., and Hieter, P. (1990) Methods in Yeast Genetics A Laboratory Course Mnual., Cold Spring Harbor Press, Cold Spring Harbor, NY
24. Guthrie, C. and Fink, G.R. (1991) Guide to Yeast Genetics and Molecular Biology. Academic Press, San Diego, CA
25. Elble, R. (1992) A simple and efficient procedure for transformation ofyeasts. Biotechniques 13, 18-20
26. 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 (Pubitemid 34619485)
27. Longtine, M.S., McKenzie, A. 3rd, Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J.R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961 (Pubitemid 28328001)
28. Tong, A.H., Evangelista, M., Parsons, A.B., Xu, H., Bader, G.D., Page, N., Robinson, M., Raghibizadeh, S., Hogue, C.W., Bussey, H., Andrews, B., Tyers, M., and Boone, C. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368 (Pubitemid 33140562)
29. Cadwell, R.C. and Joyce, G.F. (1992) Randomization of genes by PCR mutagenesis. PCR Methods Appl. 2, 28-33
30. 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 (Pubitemid 36724317)
31. Franzusoff, A., Redding, K., Crosby, J., Fuller, R.S., and Schekman, R. (1991) Localization of components involved in protein transport and processing through the yeast Golgi apparatus. J. Cell Biol. 112, 27-37 (Pubitemid 21909597)
32. Chuang, J.S. and Schekman, R.W. (1996) Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J. Cell Biol. 135, 597-610 (Pubitemid 26372918)
33. Ziman, M., Chuang, J.S., Tsung, M., Hamamoto, S., and Schekman, R. (1998) Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae. Mol. Biol. Cell 9, 1565-1576 (Pubitemid 28303497)
34. Valdivia, R., Baggott, D., Chuang, J., and Schekman, R. (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 (Pubitemid 34266114)
35. Liu, K., Surendhran, K., Nothwehr, S., and Graham, T.R. (2008) P4-ATPase requirement for AP-1/clathrin function in protein transport from the trans-Golgi net-work and early endosomes. Mol. Biol. Cell 19, 3526-3535
36. 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 endo-somes. Mol. Biol. Cell 11, 23-38 (Pubitemid 30075503)
37. Geering, K. (2001) The functional role of β subunits in oligomeric P-type ATPases. J. Bioenerg. Biomembr. 33, 425-438 (Pubitemid 32988630)
38. Sikorski, R.S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient ma-nipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27
39. 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 (Pubitemid 19060666)