Phospholipid flippase ATP10A translocates phosphatidylcholine and is involved in plasma membrane dynamics

Journal of Biological Chemistry

Volumn 290, Issue 24, 2015, Pages 15004-15017

  Naito, Tomoki ^a   Takatsu, Hiroyuki ^a   Miyano, Rie ^a   Takada, Naoto ^a   Nakayama, Kazuhisa ^a   Shin, Hye Won ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION; CELLS; CYTOLOGY; ENZYME ACTIVITY; MEMBRANES; PHOSPHOLIPIDS;

CELL MORPHOLOGY; ENDOPLASMIC RETICULUM; EXTRACELLULAR MATRICES; LIPID COMPOSITION; MEMBRANE DYNAMICS; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE;

CELL MEMBRANES;

MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID; PROTEIN ATP10A; PROTEIN ATP10B; PROTEIN ATP10D; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; ATP10A PROTEIN, HUMAN; CARRIER PROTEIN; PRIMER DNA; PROTEIN BINDING; TMEM30A PROTEIN, HUMAN;

ARTICLE; BINDING AFFINITY; CELL ADHESION; CELL MEMBRANE; CELL SIZE; CELL SPREADING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; FLIPPASE ACTIVITY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; AMINO ACID SEQUENCE; CELL FRACTIONATION; CELL MOTION; CHEMISTRY; ENZYMOLOGY; HELA CELL LINE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BASE SEQUENCE; BIOLOGICAL TRANSPORT; CELL ADHESION; CELL MEMBRANE; CELL MOVEMENT; DNA PRIMERS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLCHOLINES; POLYMERASE CHAIN REACTION; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; SUBCELLULAR FRACTIONS;

EID: 84931291587     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.655191     Document Type: Article

References (44)

1. Op Den Kamp, J. A. (1979) Lipid asymmetry in membranes. Annu. Rev. Biochem. 48, 47-71
2. Van Meer, G., Voelker, D. R., and Feigenson, G. W. (2008) Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124
3. Leventis, P. A., and Grinstein, S. (2010) The distribution and function of phosphatidylserine in cellular membranes. Annu. Rev. Biophys. 39, 407-427
4. Schrier, S. L., Zachowski, A., and Devaux, P. F. (1992) Mechanisms of amphipath-induced stomatocytosis in human erythrocytes. Blood 79, 782-786
5. Zwaal, R. F., and Schroit, A. J. (1997) Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 89, 1121-1132
6. 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. U. S. A. 81, 3751-3755
7. 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
8. Daleke, D. L. (2003) Regulation of transbilayer plasma membrane phospholipid asymmetry. J. Lipid Res. 44, 233-242
9. 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
10. 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
11. Zhou, X., and Graham, T. R. (2009) Reconstitution of phospholipid translocase activity with purified Drs2p, atype-IV P-type ATPase from budding yeast. Proc. Natl. Acad. Sci. U. S. A. 106, 16586-16591
12. 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. U. S. A. 101, 10614-10619
13. 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
14. 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 accessory protein for endoplasmic reticulum exit and plasma membrane lipid flippase activity. Hepatology 47, 268-278
15. Bryde, S., Hennrich, H., Verhulst, P. M., Devaux, P. F., Lenoir, G., and Holthuis, J. C. (2010) CDC50 proteins are critical components of the human class-1 P4-ATPase transport machinery. J. Biol. Chem. 285, 40562-40572
16. Van Der Velden, L. M., Wichers, C. G., Van Breevoort, A. E., Coleman, J. A., Molday, R. S., Berger, R., Klomp, L. W., and Van De Graaf, S. F. (2010) Heteromeric interactions required for abundance and subcellular localization of human CDC50 proteins and class 1 P4-ATPases. J. Biol. Chem. 285, 40088-40096
17. Coleman, J. A., and Molday, R. S. (2011) Critical Role of the b-subunit CDC50A in the stable expression, assembly, subcellular localization, and lipid transport activity of the P4-ATPase ATP8A2. J. Biol. Chem. 286, 17205-17216
18. Takatsu, H., Baba, K., Shima, T., Umino, H., Kato, U., Umeda, M., Nakayama, K., and Shin, H. W. (2011) ATP9B, a P4-ATPase (a putative aminophospholipid translocase), localizes to the trans-Golgi network in a CDC50 protein-independent manner. J. Biol. Chem. 286, 38159-38167
19. Takatsu, H., Tanaka, G., Segawa, K., Suzuki, J., Nagata, S., Nakayama, K., and Shin, H. W. (2014) Phospholipid flippase activities and substrate specificities of human type IV P-type ATPases localized to the plasma membrane. J. Biol. Chem. 289, 33543-33556
20. Paulusma, C. C., Groen, A., Kunne, C., Ho-Mok, K. S., Spijkerboer, A. L., Rudi De Waart, D., Hoek, F. J., Vreeling, H., Hoeben, K. A., Van Marle, J., Pawlikowska, L., Bull, L. N., Hofmann, A. F., Knisely, A. S., and Oude Elferink, R. P. (2006) Atp8b1 deficiency in mice reduces resistance of the canalicular membrane to hydrophobic bile salts and impairs bile salt transport. Hepatology 44, 195-204
21. Folmer, D. E., Elferink, R. P., and Paulusma, C. C. (2009) P4ATPases-lipid flippases and their role in disease. Biochim. Biophys. Acta 1791, 628-635
22. Levano, K., Punia, V., Raghunath, M., Debata, P. R., Curcio, G. M., Mogha, A., Purkayastha, S., McCloskey, D., Fata, J., and Banerjee, P. (2012) Atp8a1 deficiency is associated with phosphatidylserine externalization in hippocampus and delayed hippocampus-dependent learning. J. Neurochem. 120, 302-313
23. Yabas, M., Teh, C. E., Frankenreiter, S., Lal, D., Roots, C. M., Whittle, B., Andrews, D. T., Zhang, Y., Teoh, N. C., Sprent, J., Tze, L. E., Kucharska, E. M., Kofler, J., Farell, G. C., Bröer, S., Goodnow, C. C., and Enders, A. (2011) ATP11C is critical for the internalization of phosphatidylserine and differentiation of B lymphocytes. Nat. Immunol. 12, 441-449
24. Yabas, M., Coupland, L. A., Cromer, D., Winterberg, M., Teoh, N. C., D'Rozario, J., Kirk, K., Bröer, S., Parish, C. R., and Enders, A. (2014) Mice deficient in the putative phospholipid flippase ATP11C eXHIBIT altered erythrocyte shape, anemia, and reduced erythrocyte life span. J. Biol. Chem. 289, 19531-19537
25. Segawa, K., Kurata, S., Yanagihashi, Y., Brummelkamp, T. R., Matsuda, F., and Nagata, S. (2014) Caspase-mediated cleavage of phospholipid flippase for apoptotic phosphatidylserine exposure. Science 344, 1164-1168
26. Dhar, M. S., Sommardahl, C. S., Kirkland, T., Nelson, S., Donnell, R., Johnson, D. K., and Castellani, L. W. (2004) Mice heterozygous for Atp10c, a putative amphipath, represent a novel model of obesity and type 2 diabetes. J. Nutr. 134, 799-805
27. Hurst, S. E., Minkin, S. C., Biggerstaff, J., and Dhar, M. S. (2012) Transient silencing of a type IV P-type ATPase, Atp10c, results in decreased glucose uptake in C2C12 myotubes. JNutr. Metab. 2012, 152902
28. Dhar, M. S., Yuan, J. S., Elliott, S. B., and Sommardahl, C. (2006) A type IV P-type ATPase affects insulin-mediated glucose uptake in adipose tissue and skeletal muscle in mice. J Nutr. Biochem. 17, 811-820
29. Yamamoto, H., Koga, H., Katoh, Y., Takahashi, S., Nakayama, K., and Shin, H. W. (2010) Functional cross-talk between Rab14 and Rab4 through a dual effector, RUFY1/Rabip4. Mol. Biol. Cell 21, 2746-2755
30. Shin, H. W., Kobayashi, H., Kitamura, M., Waguri, S., Suganuma, T., Uchiyama, Y., and Nakayama, K. (2005) Roles of ARFRP1 (ADP-ribosylation factor-related protein 1) in post-Golgi membrane trafficking. J. Cell Sci. 118, 4039-4048
31. Shin, H. W., Morinaga, N., Noda, M., and Nakayama, K. (2004) BIG2, a Guanine Nucleotide Exchange Factor for ADP-Ribosylation Factors: Its Localization to Recycling Endosomes and Implication in the Endosome Integrity. Mol. Biol. Cell 15, 5283-5294
32. Anthonisen, A. N., Clausen, J. D., and Andersen, J. P. (2006) Mutational analysis of the conserved TGES loop of sarcoplasmic reticulum Ca2+-ATPase. J. Biol. Chem. 281, 31572-31582
33. Morita, S. Y., Kobayashi, A., Takanezawa, Y., Kioka, N., Handa, T., Arai, H., Matsuo, M., and Ueda, K. (2007) Bile salt-dependent efflux of cellular phospholipids mediated by ATP-binding cassette protein B4. Hepatology 46, 188-199
34. Folmer, D. E., Van Der Mark, V. A., Ho-Mok, K. S., Oude Elferink, R. P., and Paulusma, C. C (2009) Differential effects of progressive familial intrahepatic cholestasis type 1 and benign recurrent intrahepatic cholestasis type 1 mutations on canalicular localization of ATP8B1. Hepatology 50, 1597-1605
35. 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
36. Baldridge, R. D., and Graham, T. R. (2013) Two-gate mechanism for phospholipid selection and transport by type IV P-type ATPases. Proc. Natl. Acad. Sci. U. S. A. 110, E358-E367
37. Baldridge, R. D., and Graham, T. R. (2012) Identification of residues defining phospholipid flippase substrate specificity of type IV P-type ATPases. Proc. Natl. Acad. Sci. U. S. A. 109, E290-E298
38. Lee, S., Uchida, Y., Wang, J., Matsudaira, T., Nakagawa, T., Kishimoto, T., Mukai, K., Inaba, T., Kobayashi, T., Molday, R. S., Taguchi, T., and Arai, H. (2015) Transport through recycling endosomes requires EHD1 recruitment by a phosphatidylserine translocase. EMBO J. 34, 669-688
39. Fairn, G. D., Hermansson, M., Somerharju, P., and Grinstein, S. (2011) Phosphatidylserine is polarized and required for proper Cdc42 localization and for development of cell polarity. Nat. Cell Biol. 13, 1424-1430
40. Das, A., Slaughter, B. D., Unruh, J. R., Bradford, W. D., Alexander, R., Rubinstein, B., and Li, R. (2012) Flippase-mediated phospholipid asymmetry promotes fast Cdc42 recycling indynamic maintenance of cell polarity. Nat. Cell Biol. 14, 304-310
41. Riekhof, W. R., and Voelker, D. R. (2009) The yeast plasma membrane P4-ATPases are major transporters for lysophospholipids. Biochim. Biophys. Acta 1791, 620-627
42. Klomp, L. W., Vargas, J. C., Van Mil, S. W., Pawlikowska, L., Strautnieks, S. S., Van Eijk, M. J., Juijn, J. A., Pabón-Peña, C., Smith, L. B., DeYoung, J. A., Byrne, J. A., Gombert, J., Van Der Brugge, G., Berger, R., Jankowska, I., Pawlowska, J., Villa, E., Knisely, A. S., Thompson, R. J., Freimer, N. B., Houwen, R. H., and Bull, L. N. (2004) Characterization of mutations in ATP8B1 associated with hereditary cholestasis. Hepatology 40, 27-38
43. Nakano, K., Yamamoto, T., Kishimoto, T., Noji, T., and Tanaka, K. (2008) Protein kinases Fpk1p and Fpk2p are novel regulators of phospholipid asymmetry. Mol. Biol. Cell 19, 1783-1797
44. 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