Drs2p-related P-type ATPases Dnflp and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis

Molecular Biology of the Cell

Volumn 14, Issue 3, 2003, Pages 1240-1254

  Pomorski, Thomas ^a,b   Lombardi, Ruben ^c   Riezman, Howard ^c   Devaux, Philippe F ^d   Van Meer, Gerrit ^a   Holthuis, Joost C M ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMPHOTERICIN B; DNF1P PROTEIN; DNF2P PROTEIN; DRS2P PROTEIN; PHOSPHOLIPID; PHOSPHORUS 32; UNCLASSIFIED DRUG;

ARTICLE; CATTLE; CHROMAFFIN GRANULE; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME LOCALIZATION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GOLGI COMPLEX; INTERNALIZATION; MEMBRANE TRANSPORT; MEMBRANE VESICLE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; YEAST;

ADENOSINE TRIPHOSPHATASES; AMPHOTERICIN B; ANIMALS; ANTIBIOTICS, ANTIFUNGAL; CALCIUM-TRANSPORTING ATPASES; CELL FRACTIONATION; CELL MEMBRANE; ENDOCYTOSIS; HUMANS; MEMBRANE PROTEINS; MUTATION; PHENOTYPE; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSPORT VESICLES;

BOS TAURUS; BOVINAE; EUKARYOTA;

EID: 0037345029     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-08-0501     Document Type: Article

References (45)

1. Aoki, Y., Uenaka, T., Aoki, J., Umeda, M., and Inoue, K. (1994). A novel peptide probe for studying the transbilayer movement of phosphatidylethanolamine. J. Biochem. 116, 291-297.
2. Bligh, E.G., and Dyer, W.J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol 37, 911-917.
3. Brajtburg, J., Powderly, W.G., Kobayashi, G.S., and Medoff, G. (1990). Amphotericin B: current understanding of mechanisms of action. Antimicrob. Agents Chemother. 34, 183-188.
4. Bull, L.N. et al. (1998). A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat. Genet. 18, 219-224.
5. Buton, X. et al. (2002). Transbilayer movement of monohexylsphingolipids in endoplasmic reticulum and Golgi membranes. Biochemistry 41, 13106-13115.
6. Catty, P., de Kerchove d'Exaerde, A., and Goffeau, A. (1997). The complete inventory of the yeast Saccharomyces cerevisiae P-type transport ATPases. FEBS Lett. 409, 325-332.
7. Cerbon, J., and Calderon, V. (1995). Generation, modulation and maintenance of the plasma membrane asymmetric phospholipid composition in yeast cells during growth: their relation to surface potential and membrane protein activity. Biochim. Biophys. Acta 1235, 100-106.
8. 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.
9. Cunningham, K.W., and Wickner, W.T. (1989). Yeast KEX2 protease and mannosyltransferase I are localized to distinct compartments of the secretory pathway. Yeast 5, 25-33.
10. Daleke, D.L., and Lyles, J.V. (2000). Identification and purification of aminophospholipid flippases. Biochim. Biophys. Acta 1486, 108-127.
11. Decottignies, A., Grant, A.M., Nichols, J.W., de Wet, H., McIntosh, D.B., and Goffeau, A. (1998). ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem. 273, 12612-12622.
12. Devaux, P.F. (1991). Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30, 1163-1173.
13. Dulic, V., Egerton, M., Elguindi, I., Raths, S., Singer, B., and Riezman, H. (1991). Yeast endocytosis assays. Methods Enzymol. 194, 697-710.
14. Fadok, V.A., Bratton, D.L., Rose, D.M., Pearson, A., Ezekewitz, R.A., and Henson, P.M. (2000). A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405, 85-90.
15. Farge, E., and Devaux, P.F. (1992). Shape changes of giant liposomes induced by an asymmetric transmembrane distribution of phospholipids. Biophys. J. 61, 347-357.
16. Farge, E., Ojcius, D.M., Subtil, A., and Dautry-Varsat, A. (1999). Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am. J. Physiol. 276, C725-C733.
17. Gall, W.E., Geething, N.C., Hua, Z., Ingram, M.F., Liu, K., Chen, S., and Graham, T.R. (2002). Drs2p-dependent budding of clathrin-coated vesicles in vivo. Curr. Biol. 12, 1623-1627.
18. Gomès, E., Jakobsen, M.K., Axelsen, K.B., Geisler, M., and Palmgren, M.G. (2000). Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases. Plant Cell 12, 2441-2454.
19. Grant, A.M., Hanson, P.K., Malone, L., and Nichols, J.W. (2001). NBD-labeled phosphatidylcholine and phosphatidylethanolamine are internalized by transbilayer transport across the yeast plasma membrane. Traffic 2, 37-50.
20. Hanson, P.K., and Nichols, J.W. (2001). Energy-dependent flip of fluorescence-labeled phospholipids is regulated by nutrient starvation and transcription factors, PDR1 and PDR3. J. Biol. Chem. 276, 9861-9867.
21. Hua, Z., Fatheddin, P., and Graham, T.R. (2002). An essential subfamily of Drs2-related P-type ATPases is required for protein trafficking between Golgi complex and endosomal/vacuolar system. Mol. Biol. Cell 13, 3162-3177.
22. Holthuis, J.C.M., Nichols, B.J., Dhruvakumar, S., and Pelham, H.R. (1998). Two syntaxin homologs in the TGN/endosomal system of yeast. EMBO J. 17, 113-126.
23. Kato, U., Emoto, K., Fredriksson, C., Nakamura, H., Ohta, A., Kobayashi, T., Murakami-Murofushi, K., Kobayashi, T., and Umeda, M. (2002). A novel membrane protein, Ros3p, is required for phospholipid translocation across the plasma membrane in Saccharomyces cerevisiae. J. Biol. Chem. 277, 37855-37862.
24. Marx, U., Polakowski, T., Pomorski, T., Lang, C., Nelson, H., Nelson, N., and Herrmann, A. (1999). Rapid transbilayer movement of fluorescent phospholipid analogs in the plasma membrane of endocytosis-deficient yeast cells does not require the Drs2 protein. Eur. J. Biochem 263, 254-263.
25. Meguro, M., Kashiwagi, A., Mitsuya, K., Nakao, M., Kondo, I., Saitoh, S., and Oshimura, M. (2002). A novel maternally expressed gene, ATP10C, encodes a putative aminophospholipid translocase associated with Angelman syndrome. Nat. Genet. 28, 19-20.
26. Menon, A.K. (1995). Flippases. Trends Cell Biol. 5, 355-360.
27. Morton, W.M., Ayscough, K.R., and McLaughlin, P.J. (2000). Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat. Cell Biol. 2, 376-378.
28. Pomorski, T., Herrmann, A., Muller, P., van Meer, G., and Burger, K. (1999). Protein-mediated inward translocation of phospholipids occurs in both the apical and basolateral plasma membrane domains of epithelial cells. Biochemistry 38, 142-150.
29. Raggers, R.J., Pomorski, T., Holthuis, J.C.M., Kalin, N., and van Meer, G. (2000). Lipid traffic: the ABC of transbilayer movement. Traffic 1, 226-234.
30. 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.
31. Robinson, J.S., Klionsky, D.J., Bata, L.M., and Emr, S.D. (1988). Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell. Biol. 8, 4936-4948.
32. Rosing, J., Tans, G., Govers-Riemslag, J.W., Zwaal, R.F., and Hemker, H.C. (1980). The role of phospholipids and factor Va in the prothrombinase complex. J. Biol. Chem. 255, 274-283.
33. Rouser, G., Fleischer, S., and Yamamoto, A. (1970). Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5, 494-496.
34. Sauer, B. (1987). Functional expression of the cre-lox site-specific recombination system in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 2087-2096.
35. Schmidt, A., Wolde, M., Thiele, C., Fest, W., Kratzin, W., Podtelejnikov, A.V., Witke, W., Huttner, W.B., and Soling, H.D. (1999). Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401, 133-141.
36. Seigneuret, M., and Devaux, P.F. (1984). ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl. Acad. Sci. USA 81, 3751-3755.
37. Sheetz, M.P., and Singer, S.J. (1974). Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA 71, 4457-4461.
38. Siegmund, A., Grant, A., Angeletti, C., Malone, L., Nichols, J.W., and Rudolph, H. K. (1998). Loss of Drs2p does not abolish transfer of fluorescence-labeled phospholipids across the plasma membrane of Saccharomyces cerevisiae. J. Biol. Chem. 273, 34399-34405.
39. Smaal, E.B., Mandersloot, J.G., de Kruijiff, B., and de Gier, J. (1986). Consequences of the interaction of calcium with dioleoylphosphatidate-containing model membranes: changes in membrane permeability. Biochim. Biophys. Acta 860, 99-108.
40. Takei, K., Haucke, V., Slepnev, V., Farsad, K., Salazar, M., Chen, H., and De Camilli, P. (1998). Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94, 131-141.
41. Tang, X., Halleck, M.S., Schlegel, R.A., and Williamson, P. (1996). A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 272, 1495-1497.
42. Trotter, P.J. (2000). A novel pathway for transport and metabolism of a fluorescent phosphatidic acid analog in yeast. Traffic 1, 425-434.
43. Wach, A., Brachat, A., Alberti-Segui, C., Rebischung, C., and Philippsen, P. (1997). Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast 13, 1065-1075.
44. Weigert, R. et al. (1999). CtBP/BARS induces fission of Golgi membranes by acylating lysophosphatidic acid. Nature 402, 429-33.
45. Zachowski, A., Henry, J.P, and Devaux, P.F. (1989). Control of transmembrane lipid asymmetry in chromaffin granules by an ATP-dependent protein. Nature 340, 75-76.