ATPase reaction cycle of P4-ATPases affects their transport from the endoplasmic reticulum.
E1-E2 ATPase
P4-ATPase
flippase
lipid bilayer
membrane
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
25
07
2019
revised:
09
09
2019
accepted:
11
09
2019
pubmed:
2
10
2019
medline:
8
10
2020
entrez:
2
10
2019
Statut:
ppublish
Résumé
P4-ATPases belonging to the P-type ATPase superfamily mediate active transport of phospholipids across cellular membranes. Most P4-ATPases, except ATP9A and ATP9B proteins, form heteromeric complexes with CDC50 proteins, which are required for transport of P4-ATPases from the endoplasmic reticulum (ER) to their final destinations. P-type ATPases form autophosphorylated intermediates during the ATPase reaction cycle. However, the association of the catalytic cycle of P4-ATPases with their transport from the ER and their cellular localization has not been studied. Here, we show that transport of ATP9 and ATP11 proteins as well as that of ATP10A from the ER depends on the ATPase catalytic cycle, suggesting that conformational changes in P4-ATPases during the catalytic cycle are crucial for their transport from the ER.
Identifiants
pubmed: 31571211
doi: 10.1002/1873-3468.13629
doi:
Substances chimiques
Adenosine Triphosphatases
EC 3.6.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
412-423Informations de copyright
© 2019 Federation of European Biochemical Societies.
Références
Kuhlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5, 282-295.
Post RL, Hegyvary C and Kume S (1972) Activation by adenosine triphosphate in the phosphorylation kinetics of sodium and potassium ion transport adenosine triphosphatase. J Biol Chem 247, 6530-6540.
Albers RW (1967) Biochemical aspects of active transport. Ann Rev Biochem 36, 727-756.
Toyoshima C, Nakasako M, Nomura H and Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature 405, 647-655.
Danko S, Yamasaki K, Daiho T, Suzuki H and Toyoshima C (2001) Organization of cytoplasmic domains of sarcoplasmic reticulum Ca(2+)-ATPase in E(1)P and E(1)ATP states: a limited proteolysis study. FEBS Lett 505, 129-135.
Toyoshima C and Inesi G (2004) Structural basis of ion pumping by Ca2+-ATPase of the sarcoplasmic reticulum. Annu Rev Biochem 73, 269-292.
Palmgren MG and Nissen P (2011) P-type ATPases. Annu Rev Biophys 40, 243-266.
Toyoshima C and Mizutani T (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430, 529-535.
Toyoshima C (2009) How Ca2+-ATPase pumps ions across the sarcoplasmic reticulum membrane. Biochim Biophys Acta 1793, 941-946.
Devaux PF (1991) Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30, 1163-1173.
Takatsu H, Tanaka G, Segawa K, Suzuki J, Nagata S, Nakayama K and Shin HW (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.
Kobayashi T and Menon AK (2018) Transbilayer lipid asymmetry. Curr Biol 28, R386-R391.
Shin HW and Takatsu H (2019) Substrates of P4-ATPases: beyond aminophospholipids (phosphatidylserine and phosphatidylethanolamine). FASEB J 33, 3087-3096.
Roland BP, Naito T, Best JT, Arnaiz-Yepez C, Takatsu H, Yu RJ, Shin HW and Graham TR (2019) Yeast and human P4-ATPases transport glycosphingolipids using conserved structural motifs. J Biol Chem 294, 1794-1806.
Wang J, Molday LL, Hii T, Coleman JA, Wen T, Andersen JP and Molday RS (2018) Proteomic analysis and functional characterization of P4-ATPase phospholipid flippases from murine tissues. Sci Rep 8, 10795.
Naito T, Takatsu H, Miyano R, Takada N, Nakayama K and Shin HW (2015) Phospholipid flippase ATP10A translocates phosphatidylcholine and is involved in plasma membrane dynamics. J Biol Chem 290, 15004-15017.
Lee S, Uchida Y, Wang J, Matsudaira T, Nakagawa T, Kishimoto T, Mukai K, Inaba T, Kobayashi T, Molday RS et al. (2015) Transport through recycling endosomes requires EHD1 recruitment by a phosphatidylserine translocase. EMBO J 34, 669-688.
Coleman JA, Kwok MCM and Molday RS (2009) Localization, purification, and functional reconstitution of the P4-ATPase Atp8a2, a phosphatidylserine flippase in photoreceptor disc membranes. J Biol Chem 284, 32670-32679.
Bull LN, van Eijk MJ, Pawlikowska L, DeYoung JA, Juijn JA, Liao M, Klomp LW, Lomri N, Berger R, Scharschmidt BF et al. (1998) A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat Genet 18, 219-224.
Folmer DE and Elferink RPJO (2009) Paulusma CC: P4 ATPases - Lipid flippases and their role in disease. Biochim Biophys Acta 1791, 628-635.
Onat OE, Gulsuner S, Bilguvar K, Nazli Basak A, Topaloglu H, Tan M, Tan U, Gunel M and Ozcelik T (2013) Missense mutation in the ATPase, aminophospholipid transporter protein ATP8A2 is associated with cerebellar atrophy and quadrupedal locomotion. Eur J Hum Genet 21, 281-285.
Arashiki N, Takakuwa Y, Mohandas N, Hale J, Yoshida K, Ogura H, Utsugisawa T, Ohga S, Miyano S, Ogawa S et al. (2016) ATP11C is a major flippase in human erythrocytes and its defect causes congenital hemolytic anemia. Haematologica 101, 559-565.
Bublitz M, Morth JP and Nissen P (2011) P-type ATPases at a glance. J Cell Sci 124, 2515-2519.
Vestergaard AL, Coleman JA, Lemmin T, Mikkelsen SA, Molday LL, Vilsen B, Molday RS, Dal Peraro M and Andersen JP (2014) Critical roles of isoleucine-364 and adjacent residues in a hydrophobic gate control of phospholipid transport by the mammalian P4-ATPase ATP8A2. Proc Natl Acad Sci USA 111, E1334-E1343.
Timcenko M, Lyons JA, Januliene D, Ulstrup JJ, Dieudonne T, Montigny C, Ash MR, Karlsen JL, Boesen T, Kuhlbrandt W et al. (2019) Structure and autoregulation of a P4-ATPase lipid flippase. Nature 571, 366-370.
Hiraizumi M, Yamashita K, Nishizawa T and Nureki O (2019) Cryo-EM structures capture the transport cycle of the P4-ATPase flippase. Science 365, 1149-1155.
Lopez-Marques RL, Poulsen LR, Hanisch S, Meffert K, Buch-Pedersen MJ, Jakobsen MK, Pomorski TG and Palmgren MG (2010) Intracellular targeting signals and lipid specificity determinants of the ALA/ALIS P4-ATPase complex reside in the catalytic ALA {alpha}-subunit. Mol Biol Cell 21, 791-801.
Bryde S, Hennrich H, Verhulst PM, Devaux PF, Lenoir G and Holthuis JC (2010) CDC50 proteins are critical components of the human class-1 P4-ATPase transport machinery. J Biol Chem 285, 40562-40572.
van der Velden LM, Wichers CGK, van Breevoort AED, Coleman JA, Molday RS, Berger R, Klomp LWJ and van de Graaf SFJ (2010) Heteromeric interactions required for abundance and subcellular localization of human CDC50 proteins and class 1 P4-ATPases. J Biol Chem 285, 40088-40096.
Palmgren M, Osterberg JT, Nintemann SJ, Poulsen LR and Lopez-Marques RL (2019) Evolution and a revised nomenclature of P4 ATPases, a eukaryotic family of lipid flippases. Biochim Biophys Acta Biomembr 1861, 1135-1151.
Lenoir G, Williamson P, Puts CF and Holthuis JCM (2009) Cdc50p plays a vital role in the atpase reaction cycle of the putative aminophospholipid transporter Drs2p. J Biol Chem 284, 17956-17967.
Theorin L, Faxen K, Sorensen DM, Migotti R, Dittmar G, Schiller J, Daleke DL, Palmgren M, Lopez-Marques RL and Gunther Pomorski T (2019) The lipid head group is the key element for substrate recognition by the P4 ATPase ALA2: a phosphatidylserine flippase. Biochem J 476, 783-794.
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.
Zhang Y, Werling U and Edelmann W (2012) SLiCE: a novel bacterial cell extract-based DNA cloning method. Nucleic Acids Res 40, e55.
Kelley LA, Mezulis S, Yates CM, Wass MN and Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10, 845-858.
Andersen JP, Vestergaard AL, Mikkelsen SA, Mogensen LS, Chalat M and Molday RS (2016) P4-ATPases as phospholipid flippases-structure, function, and enigmas. Front Physiol 7, 275.
Axelsen KB and Palmgren MG (1998) Evolution of substrate specificities in the P-Type ATPase superfamily. J Mol Evol 46, 84-101.
Anthonisen AN, Clausen JD and Andersen JP (2006) Mutational analysis of the conserved TGES loop of sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem 281, 31572-31582.
Wang G, Yamasaki K, Daiho T and Suzuki H (2005) Critical hydrophobic interactions between phosphorylation and actuator domains of Ca2+-ATPase for hydrolysis of phosphorylated intermediate. J Biol Chem 280, 26508-26516.
Marchand A, Winther A-ML, Holm PJ, Olesen C, Montigny C, Arnou B, Champeil P, Clausen JD, Vilsen B, Andersen JP et al. (2008) Crystal structure of D351A and P312A mutant forms of the mammalian sarcoplasmic reticulum Ca2+-ATPase reveals key events in phosphorylation and Ca2+ release. J Biol Chem 283, 14867-14882.
Coleman JA and Molday RS (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.
Ding J, Wu Z, Crider BP, Ma Y, Li X, Slaughter C, Gong L and Xie X-S (2000) Identification and functional expression of four isoforms of ATPase II, the putative aminophospholipid translocase. J Biol Chem 275, 23378-23386.
Coleman JA, Vestergaard AL, Molday RS, Vilsen B and Peter Andersen J (2012) Critical role of a transmembrane lysine in aminophospholipid transport by mammalian photoreceptor P4-ATPase ATP8A2. Proc Natl Acad Sci USA 109, 1449-1454.
Segawa K, Kurata S and Nagata S (2016) Human type IV P-type ATPases that work as plasma membrane phospholipid flippases and their regulation by caspase and calcium. J Biol Chem 291, 762-772.
Azouaoui H, Montigny C, Ash MR, Fijalkowski F, Jacquot A, Gronberg C, Lopez-Marques RL, Palmgren MG, Garrigos M, le Maire M et al. (2014) A high-yield co-expression system for the purification of an intact drs2p-cdc50p lipid flippase complex, critically dependent on and stabilized by phosphatidylinositol-4-phosphate. PLoS ONE 9, e112176.
Takatsu H, Takayama M, Naito T, Takada N, Tsumagari K, Ishihama Y, Nakayama K and Shin HW (2017) Phospholipid flippase ATP11C is endocytosed and downregulated following Ca2+-mediated protein kinase C activation. Nat Commun 8, 1423.
Takayama M, Takatsu H, Hamamoto A, Inoue H, Naito T, Nakayama K and Shin HW (2019) C-terminal cytoplasmic region of ATP11C variant determines its localization at the polarized plasma membrane. J Cell Sci 132, jcs.231270.
Holemans T, Sorensen DM, van Veen S, Martin S, Hermans D, Kemmer GC, Van den Haute C, Baekelandt V, Gunther Pomorski T, Agostinis P et al. (2015) A lipid switch unlocks Parkinson's disease-associated ATP13A2. Proc Natl Acad Sci USA 112, 9040-9045.
Braiterman L, Nyasae L, Leves F and Hubbard AL (2011) Critical roles for the COOH terminus of the Cu-ATPase ATP7B in protein stability, trans-Golgi network retention, copper sensing, and retrograde trafficking. Am J Physiol Gastrointest Liver Physiol 301, G69-G81.
Chalat M, Moleschi K and Molday RS (2017) C-terminus of the P4-ATPase ATP8A2 functions in protein folding and regulation of phospholipid flippase activity. Mol Biol Cell 28, 452-462.
Azouaoui H, Montigny C, Dieudonne T, Champeil P, Jacquot A, Vazquez-Ibar JL, Le Marechal P, Ulstrup J, Ash MR, Lyons JA et al. (2017) High phosphatidylinositol 4-phosphate (PI4P)-dependent ATPase activity for the Drs2p-Cdc50p flippase after removal of its N- and C-terminal extensions. J Biol Chem 292, 7954-7970.
Natarajan P, Liu K, Patil DV, Sciorra VA, Jackson CL and Graham TR (2009) Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat Cell Biol 11, 1421-1426.
Segawa K, Kurata S and Nagata S (2018) The CDC50A extracellular domain is required for forming a functional complex with and chaperoning phospholipid flippases to the plasma membrane. J Biol Chem 293, 2172-2182.