Towards defining the substrate of orphan P5A-ATPases

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 3, 2015, Pages 524-535

  Sørensen, Danny Mollerup ^a   Holen, Henrik Waldal ^a   Holemans, Tine ^b   Vangheluwe, Peter ^b   Palmgren, Michael G ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Endoplasmic reticulum; Membrane transport; P5A ATPase; Primary active pump; Unfolded protein response

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ERGOSTEROL; GLYCOSYLPHOSPHATIDYLINOSITOL; MAGNESIUM; MANGANESE; MEMBRANE PROTEIN; OLIGOSACCHARIDE; P5A TYPE ADENOSINE TRIPHOSPHATASE; SECRETORY PROTEIN; SPF1P PROTEIN; TAIL ANCHORED PROTEIN; UNCLASSIFIED DRUG; ABC TRANSPORTER; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; SPF1 PROTEIN, S CEREVISIAE; STEROL;

AMINO TERMINAL SEQUENCE; BINDING SITE; CALCIUM TRANSPORT; CELL WALL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MEMBRANE; ENZYME SUBSTRATE; GENE INTERACTION; GOLGI COMPLEX; HUMAN; HYDROLYSIS; ION TRANSPORT; MEMBRANE TRANSPORT; MEMBRANE VESICLE; NONHUMAN; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; REVIEW; SACCHAROMYCES CEREVISIAE; STEROL METABOLISM; STRUCTURE ACTIVITY RELATION; UNFOLDED PROTEIN RESPONSE; BIOLOGICAL MODEL; ENZYME SPECIFICITY; GENETICS; METABOLISM; MUTATION; TRANSPORT AT THE CELLULAR LEVEL;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; ENDOPLASMIC RETICULUM; MODELS, BIOLOGICAL; MUTATION; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STEROLS; SUBSTRATE SPECIFICITY;

EID: 84921031064     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.05.008     Document Type: Review

References (130)

1. K.B. Axelsen, and M.G. Palmgren Evolution of substrate specificities in the P-type ATPase superfamily J. Mol. Evol. 46 1998 84 101
2. W. Kühlbrandt Biology, structure and mechanism of P-type ATPases Nat. Rev. Mol. Cell Biol. 5 2004 282 295
3. A.B. Møller, T. Asp, P.B. Holm, and M.G. Palmgren Phylogenetic analysis of P5 P-type ATPases, a eukaryotic lineage of secretory pathway pumps Mol. Phylogenet. Evol. 46 2008 619 634
4. B.P. Pedersen, G. Ifrim, P. Liboriussen, K.B. Axelsen, M.G. Palmgren, P. Nissen, C. Wiuf, and C.N.S. Pedersen Large scale identification and categorization of protein sequences using structured logistic regression PLoS One 9 2014 e85139
5. D.M. Sørensen, M.J. Buch-Pedersen, and M.G. Palmgren Structural divergence between the two subgroups of P5 ATPases Biochim. Biophys. Acta 1797 2010 846 855
6. S.R. Cronin, R. Rao, and R.Y. Hampton Cod1p/Spf1p is a P-type ATPase involved in ER function and Ca2+ homeostasis J. Cell Biol. 157 2002 1017 1028
7. S. Vashist, C.G. Frank, C.A. Jakob, and D.T. Ng Two distinctly localized p-type ATPases collaborate to maintain organelle homeostasis required for glycoprotein processing and quality control Mol. Biol. Cell 13 2002 3955 3966
8. C. Suzuki Immunochemical and mutational analyses of P-type ATPase Spf1p involved in the yeast secretory pathway Biosci. Biotechnol. Biochem. 65 2001 2405 2411
9. A.L. Façanha, H. Appelgren, M. Tabish, L. Okorokov, and K. Ekwall The endoplasmic reticulum cation P-type ATPase Cta4p is required for control of cell shape and microtubule dynamics J. Cell Biol. 157 2002 1029 1039
10. M.K. Jakobsen, L.R. Poulsen, A. Schulz, P. Fleurat-Lessard, A. Møller, S. Husted, M. Schiøtt, A. Amtmann, and M.G. Palmgren Pollen development and fertilization in Arabidopsis is dependent on the male gametogenesis impaired anthers gene encoding a type V P-type ATPase Genes Dev. 19 2005 2757 2769
11. M.G. Palmgren, and P. Nissen P-type ATPases Annu. Rev. Biophys. 40 2011 243 266
12. J.V. Møller, C. Olesen, A.M. Winther, and P. Nissen The sarcoplasmic Ca2+-ATPase: design of a perfect chemi-osmotic pump Q. Rev. Biophys. 43 2010 501 566
13. P. Gourdon, X.Y. Liu, T. Skjørringe, J.P. Morth, L.B. Møller, B.P. Pedersen, and P. Nissen Crystal structure of a copper-transporting PIB-type ATPase Nature 475 2011 59 64
14. T. Padilla-Benavides, C.J. McCann, and J.M. Argüello The mechanism of Cu+ transport ATPases: interaction with Cu+ chaperones and the role of transient metal-binding sites J. Biol. Chem. 288 2013 69 78
15. N. Bal, E. Mintz, F. Guillain, and P. Catty A possible regulatory role for the metal-binding domain of CadA, the Listeria monocytogenes Cd2+-ATPase FEBS Lett. 506 2001 249 252
16. S. Mana-Capelli, A.K. Mandal, and J.M. Argüello Archaeoglobus fulgidus CopB is a thermophilic Cu2+-ATPase: functional role of its histidine-rich-N-terminal metal binding domain J. Biol. Chem. 278 2003 40534 40541
17. L. Baekgaard, M.D. Mikkelsen, D.M. Sørensen, J.N. Hegelund, D.P. Persson, R.F. Mills, Z. Yang, S. Husted, J.P. Andersen, M.J. Buch-Pedersen, J.K. Schjoerring, L.E. Williams, and M.G. Palmgren A combined zinc/cadmium sensor and zinc/cadmium export regulator in a heavy metal pump J. Biol. Chem. 285 2010 31243 31252
18. R. Pilankatta, D. Lewis, C.M. Adams, and G. Inesi High yield heterologous expression of wild-type and mutant Cu+-ATPase (ATP7B, Wilson disease protein) for functional characterization of catalytic activity and serine residues undergoing copper-dependent phosphorylation J. Biol. Chem. 284 2009 21307 21316
19. A. Goffeau, B.G. Barrell, H. Bussey, R.W. Davis, B. Dujon, H. Feldmann, F. Galibert, J.D. Hoheisel, C. Jacq, M. Johnston, E.J. Louis, H.W. Mewes, Y. Murakami, P. Philippsen, H. Tettelin, and S.G. Oliver Life with 6000 genes Science 274 1996 546 567
20. A. Goffeau Four years of post-genomic life with 6,000 yeast genes FEBS Lett. 480 2000 37 41
21. C. Suzuki, and Y.I. Shimma P-type ATPase spf1 mutants show a novel resistance mechanism for the killer toxin SMKT Mol. Microbiol. 32 1999 813 823
22. C. Suzuki, Y. Ando, and S. Machida Interaction of SMKT, a killer toxin produced by Pichia farinosa, with the yeast cell membranes Yeast 18 2001 1471 1478
23. S.R. Pfeffer, and J.E. Rothman Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi Annu. Rev. Biochem. 56 1987 829 852
24. T.A. Rapoport Transport of proteins across the endoplasmic reticulum membrane Science 258 1992 931 936
25. L. Ellgaard, and A. Helenius Quality control in the endoplasmic reticulum Nat. Rev. Mol. Cell Biol. 4 2003 181 191
26. A. Helenius, and M. Aebi Roles of N-linked glycans in the endoplasmic reticulum Annu. Rev. Biochem. 73 2004 1019 1049
27. M.C. Jonikas, S.R. Collins, V. Denic, E. Oh, E.M. Quan, V. Schmid, J. Weibezahn, B. Schwappach, P. Walter, J.S. Weissman, and M. Schuldiner Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum Science 323 2009 1693 1697
28. A.H. Sims, M.E. Gent, K. Lanthaler, N.S. Dunn-Coleman, S.G. Oliver, and G.D. Robson Transcriptome analysis of recombinant protein secretion by Aspergillus nidulans and the unfolded-protein response in vivo Appl. Environ. Microbiol. 71 2005 2737 2747
29. C.A. Ticconi, R.D. Lucero, S. Sakhonwasee, A.W. Adamson, A. Creff, L. Nussaume, T. Desnos, and S. Abel ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability Proc. Natl. Acad. Sci. U. S. A. 106 2009 14174 14179
30. J.S. Cox, C.E. Shamu, and P. Walter Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase Cell 73 1993 1197 1206
31. K. Mori, W. Ma, M.J. Gething, and J. Sambrook A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus Cell 74 1993 743 756
32. R.J. Kaufman Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls Genes Dev. 13 1999 1211 1233
33. J.S. Cox, and P. Walter A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response Cell 87 1996 391 404
34. T. Kawahara, H. Yanagi, T. Yura, and K. Mori Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response Mol. Biol. Cell 8 1 1997 845 862
35. C. Patil, and P. Walter Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals Curr. Opin. Cell Biol. 13 2001 349 355
36. D.T. Ng, E.D. Spear, and P. Walter The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control J. Cell Biol. 150 2000 77 88
37. S. Shao, and R.S. Hegde Membrane protein insertion at the endoplasmic reticulum Annu. Rev. Cell Dev. Biol. 27 2011 25 56
38. D. Akopian, K. Shen, X. Zhang, and S.O. Shan Signal recognition particle: an essential protein-targeting machine Annu. Rev. Biochem. 82 2013 693 721
39. S.H. White, and G. von Heijne The machinery of membrane protein assembly Curr. Opin. Struct. Biol. 14 2004 397 404
40. S.H. White, and G. von Heijne Transmembrane helices before, during, and after insertion Curr. Opin. Struct. Biol. 15 2005 378 386
41. T. Hessa, H. Kim, K. Bihlmaier, C. Lundin, J. Boekel, H. Andersson, I.M. Nilsson, S.H. White, and G. von Heijne Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 433 2005 377 381
42. G. von Heijne Membrane-protein topology Nat. Rev. Mol. Cell Biol. 7 2006 909 918
43. H. Andersson, and G. von Heijne Membrane protein topology: effects of ΔμH + on the translocation of charged residues explain the 'positive inside' rule EMBO J. 13 1994 2267 2272
44. W. van Klompenburg, I. Nilsson, G. von Heijne, and B. de Kruijff Anionic phospholipids are determinants of membrane protein topology EMBO J. 16 1997 4261 4266
45. J. Strayle, T. Pozzan, and H.K. Rudolph Steady-state free Ca2+ in the yeast endoplasmic reticulum reaches only 10 microM and is mainly controlled by the secretory pathway pump pmr1 EMBO J. 18 1999 4733 4743
46. E. Hartmann, T.A. Rapoport, and H.F. Lodish Predicting the orientation of eukaryotic membrane-spanning proteins Proc. Natl. Acad. Sci. U. S. A. 86 1989 5786 5790
47. D.J. Tipper, and C.A. Harley Yeast genes controlling responses to topogenic signals in a model transmembrane protein Mol. Biol. Cell 13 2002 (11 sensitivity of yeast sensitivity of yeast-74)
48. S. Michaelis, and J. Barrowman Biogenesis of the Saccharomyces cerevisiae pheromone a-factor, from yeast mating to human disease Microbiol. Mol. Biol. Rev. 76 2012 626 651
49. M. Schuldiner, S.R. Collins, N.J. Thompson, V. Denic, A. Bhamidipati, T. Punna, J. Ihmels, B. Andrews, C. Boone, J.F. Greenblatt, J.S. Weissman, and N.J. Krogan Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile Cell 123 2005 507 519
50. M. Costanzo, A. Baryshnikova, J. Bellay, Y. Kim, E.D. Spear, C.S. Sevier, H. Ding, J.L. Koh, K. Toufighi, S. Mostafavi, J. Prinz, R.P. St Onge, B. VanderSluis, T. Makhnevych, F.J. Vizeacoumar, S. Alizadeh, S. Bahr, R.L. Brost, Y. Chen, M. Cokol, R. Deshpande, Z. Li, Z.Y. Lin, W. Liang, M. Marback, J. Paw, B.J. San Luis, E. Shuteriqi, A.H. Tong, N. van Dyk, I.M. Wallace, J.A. Whitney, M.T. Weirauch, G. Zhong, H. Zhu, W.A. Houry, M. Brudno, S. Ragibizadeh, B. Papp, C. Pál, F.P. Roth, G. Giaever, C. Nislow, O.G. Troyanskaya, H. Bussey, G.D. Bader, A.C. Gingras, Q.D. Morris, P.M. Kim, C.A. Kaiser, C.L. Myers, B.J. Andrews, and C. Boone The genetic landscape of a cell Science 327 2010 425 431
51. S. Hoppins, S.R. Collins, A. Cassidy-Stone, E. Hummel, R.M. Devay, L.L. Lackner, B. Westermann, M. Schuldiner, J.S. Weissman, and J. Nunnari A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria J. Cell Biol. 195 2011 323 340
52. M.A. Surma, C. Klose, D. Peng, M. Shales, C. Mrejen, A. Stefanko, H. Braberg, D.E. Gordon, D. Vorkel, C.S. Ejsing, R. Farese Jr., K. Simons, N.J. Krogan, and R. Ernst A lipid E-MAP identifies Ubx2 as a critical regulator of lipid saturation and lipid bilayer stress Mol. Cell 51 2013 519 530
53. M.S. Brown, and J.L. Goldstein A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood Proc. Natl. Acad. Sci. U. S. A. 96 1999 11041 11048
54. J.W. Chartron, W.M. Clemons Jr., and C.J. Suloway The complex process of GETting tail-anchored membrane proteins to the ER Curr. Opin. Struct. Biol. 22 2012 217 224
55. M. Mariappan, A. Mateja, M. Dobosz, E. Bove, R.S. Hegde, and R.J. Keenan The mechanism of membrane-associated steps in tail-anchored protein insertion Nature 477 2011 61 66
56. A. Ando, and C. Suzuki Cooperative function of the CHD5-like protein Mdm39p with a P-type ATPase Spf1p in the maintenance of ER homeostasis in Saccharomyces cerevisiae Mol. Genet. Genomics 273 2005 497 506
57. X. Pan, P. Ye, D.S. Yuan, X. Wang, J.S. Bader, and J.D. Boeke A DNA integrity network in the yeast Saccharomyces cerevisiae Cell 124 2006 1069 1081
58. K. Krumpe, I. Frumkin, Y. Herzig, N. Rimon, C. Özbalci, B. Brügger, D. Rapaport, and M. Schuldiner Ergosterol content specifies targeting of tail-anchored proteins to mitochondrial outer membranes Mol. Biol. Cell 23 2012 3927 3935
59. C. Kemper, S.J. Habib, G. Engl, P. Heckmeyer, K.S. Dimmer, and D. Rapaport Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components J. Cell Sci. 121 2008 1990 1998
60. R. Schneiter, B. Brügger, R. Sandhoff, G. Zellnig, A. Leber, M. Lampl, K. Athenstaedt, C. Hrastnik, S. Eder, G. Daum, F. Paltauf, F.T. Wieland, and S.D. Kohlwein Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane J. Cell Biol. 146 1999 741 754
61. A. Raturi, and T. Simmen Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM) Biochim. Biophys. Acta 1833 2013 213 224
62. N. Johnson, K. Powis, and S. High Post-translational translocation into the endoplasmic reticulum Biochim. Biophys. Acta 1833 2013 2403 2409
63. A. Robb, and J.D. Brown Protein transport: two translocons are better than one Mol. Cell 8 2001 484 486
64. S.R. Cronin, A. Khoury, D.K. Ferry, and R.Y. Hampton Regulation of HMG-CoA reductase degradation requires the P-type ATPase Cod1p/Spf1p J. Cell Biol. 148 2000 915 924
65. J.J. Hulce, A.B. Cognetta, M.J. Niphakis, S.E. Tully, and B.F. Cravatt Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells Nat. Methods 10 2013 259 264
66. R.Y. Hampton Genetic analysis of hydroxymethylglutaryl-coenzyme A reductase regulated degradation Curr. Opin. Lipidol. 9 1998 93 97
67. W.M. Casey, G.A. Keesler, and L.W. Parks Regulation of partitioned sterol biosynthesis in Saccharomyces cerevisiae J. Bacteriol. 174 1992 7283 7288
68. A.B. Parsons, R.L. Brost, H. Ding, Z. Li, C. Zhang, B. Sheikh, G.W. Brown, P.M. Kane, T.R. Hughes, and C. Boone Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways Nat. Biotechnol. 22 2004 62 69
69. R.M. Garza, P.N. Tran, and R.Y. Hampton Geranylgeranyl pyrophosphate is a potent regulator of HRD-dependent 3-Hydroxy-3-methylglutaryl-CoA reductase degradation in yeast J. Biol. Chem. 284 2009 35368 35380
70. L.W. Parks, and W.M. Casey Physiological implications of sterol biosynthesis in yeast Annu. Rev. Microbiol. 49 1995 95 116
71. J. Henriksen, A.C. Rowat, E. Brief, Y.W. Hsueh, J.L. Thewalt, M.J. Zuckermann, and J.H. Ipsen Universal behavior of membranes with sterols Biophys. J. 90 2006 1639 1649
72. A.G. Shearer, and R.Y. Hampton Structural control of endoplasmic reticulum-associated degradation: effect of chemical chaperones on 3-hydroxy-3-methylglutaryl-CoA reductase J. Biol. Chem. 279 2004 188 196
73. A.G. Shearer, and R.Y. Hampton Lipid-mediated, reversible misfolding of a sterol-sensing domain protein EMBO J. 24 2005 149 159
74. M. Fegueur, L. Richard, A.D. Charles, and F. Karst Isolation and primary structure of the ERG9 gene of Saccharomyces cerevisiae encoding squalene synthetase Curr. Genet. 20 1991 365 372
75. D. Zhang, S.M. Jennings, G.W. Robinson, and C.D. Poulter Yeast squalene synthase: expression, purification, and characterization of soluble recombinant enzyme Arch. Biochem. Biophys. 304 1993 133 143
76. K. Kuranda, J. François, and G. Palamarczyk The isoprenoid pathway and transcriptional response to its inhibitors in the yeast Saccharomyces cerevisiae FEMS Yeast Res. 10 2010 14 27
77. M. Pittet, and A. Conzelmann Biosynthesis and function of GPI proteins in the yeast Saccharomyces cerevisiae Biochim. Biophys. Acta 1771 2007 405 420
78. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
79. M. Fujita, and T. Kinoshita Structural remodeling of GPI anchors during biosynthesis and after attachment to proteins FEBS Lett. 584 2010 1670 1677
80. D.H. Wolf, and G.R. Fink Proteinase C (carboxypeptidase Y) mutant of yeast J. Bacteriol. 123 1975 1150 1156
81. C.A. Jakob, P. Burda, J. Roth, and M. Aebi Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure J. Cell Biol. 142 1998 1223 1233
82. M.J. Massaad, and A. Herscovics Interaction of the endoplasmic reticulum alpha 1,2-mannosidase Mns1p with Rer1p using the split-ubiquitin system J. Cell Sci. 114 2001 4629 4635
83. N.P. Cottam, and D. Ungar Retrograde vesicle transport in the Golgi Protoplasma 249 2012 943 955
84. V.J. Miller, and D. Ungar Re'COG'nition at the Golgi Traffic 13 2012 891 897
85. R. Willett, D. Ungar, and V. Lupashin The Golgi puppet master: COG complex at center stage of membrane trafficking interactions Histochem. Cell Biol. 140 2013 271 283
86. S.R. Collins, K.M. Miller, N.L. Maas, A. Roguev, J. Fillingham, C.S. Chu, M. Schuldiner, M. Gebbia, J. Recht, M. Shales, H. Ding, H. Xu, J. Han, K. Ingvarsdottir, B. Cheng, B. Andrews, C. Boone, S.L. Berger, P. Hieter, Z. Zhang, G.W. Brown, C.J. Ingles, A. Emili, C.D. Allis, D.P. Toczyski, J.S. Weissman, J.F. Greenblatt, and N.J. Krogan Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map Nature 446 2007 806 810
87. U. Kutay, E. Hartmann, and T.A. Rapoport A class of membrane proteins with a C-terminal anchor Trends Cell Biol. 3 1993 72 75
88. A.P. Newman, J. Shim, and S. Ferro-Novick BET1, BOS1, and SEC22 are members of a group of interacting yeast genes required for transport from the endoplasmic reticulum to the Golgi complex Mol. Cell. Biol. 10 1990 3405 3414
89. M. Sacher, S. Stone, and S. Ferro-Novick The synaptobrevin-related domains of Bos1p and Sec22p bind to the syntaxin-like region of Sed5p J. Biol. Chem. 272 1997 17134 17138
90. D.W. Kim, M. Sacher, A. Scarpa, A.M. Quinn, and S. Ferro-Novick High-copy suppressor analysis reveals a physical interaction between Sec34p and Sec35p, a protein implicated in vesicle docking Mol. Biol. Cell 10 1999 3317 3329
91. D. Fiedler, H. Braberg, M. Mehta, G. Chechik, G. Cagney, P. Mukherjee, A.C. Silva, M. Shales, S.R. Collins, S. van Wageningen, P. Kemmeren, F.C. Holstege, J.S. Weissman, M.C. Keogh, D. Koller, K.M. Shokat, and N.J. Krogan Functional organization of the S. cerevisiae phosphorylation network Cell 136 2009 952 963
92. D. Dogic, B. de Chassey, E. Pick, D. Cassel, Y. Lefkir, S. Hennecke, P. Cosson, and F. Letourneur The ADP-ribosylation factor GTPase-activating protein Glo3p is involved in ER retrieval Eur. J. Cell Biol. 78 1999 305 310
93. J. Butler, H.R. Watson, A.G. Lee, H.J. Schuppe, and J.M. East Retrieval from the ER-golgi intermediate compartment is key to the targeting of c-terminally anchored ER-resident proteins J. Cell. Biochem. 112 2011 3543 3548
94. S.J. Free Fungal cell wall organization and biosynthesis Adv. Genet. 81 2013 33 82
95. A.F. Ram, A. Wolters, R. Ten Hoopen, and F.M. Klis A new approach for isolating cell wall mutants in Saccharomyces cerevisiae by screening for hypersensitivity to calcofluor white Yeast 10 1994 1019 1030
96. M. Lussier, A.M. White, J. Sheraton, T. di Paolo, J. Treadwell, S.B. Southard, C.I. Horenstein, J. Chen-Weiner, A.F. Ram, J.C. Kapteyn, T.W. Roemer, D.H. Vo, D.C. Bondoc, J. Hall, W.W. Zhong, A.M. Sdicu, J. Davies, F.M. Klis, P.W. Robbins, and H. Bussey Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae Genetics 147 1997 435 450
97. F. Meinhardt, and R. Klassen Yeast killer toxins: fundamentals and applications T. Anke, D. Weber, The Mycota vol. 15 2009 Springer-Verlag Berlin, Heidelberg 107 130
98. H. Bussey K1 killer toxin, a pore-forming protein from yeast Mol. Microbiol. 5 1991 2339 2343
99. F. Breinig, D.J. Tipper, and M.J. Schmitt Kre1p, the plasma membrane receptor for the yeast K1 viral toxin Cell 108 2002 395 405
100. A. Santos, D. Marquina, J.A. Leal, and J.M. Peinado (1- > 6)-β-d-glucan as cell wall receptor for Pichia membranifaciens killer toxin Appl. Environ. Microbiol. 66 2000 1809 1813
101. N. Pagé, M. Gérard-Vincent, P. Ménard, M. Beaulieu, M. Azuma, G.J. Dijkgraaf, H. Li, J. Marcoux, T. Nguyen, T. Dowse, A.M. Sdicu, and H. Bussey A Saccharomyces cerevisiae genome-wide mutant screen for altered sensitivity to K1 killer toxin Genetics 163 2003 875 894
102. T. Kashiwagi, N. Kunishima, C. Suzuki, F. Tsuchiya, S. Nikkuni, Y. Arata, and K. Morikawa The novel acidophilic structure of the killer toxin from halotolerant yeast demonstrates remarkable folding similarity with a fungal killer toxin Structure 5 1997 81 94
103. C. Suzuki, and S. Nikkuni The primary and subunit structure of a novel type killer toxin produced by a halotolerant yeast, Pichia farinosa J. Biol. Chem. 269 1994 3041 3046
104. P.N. Lipke, and R. Ovalle Cell wall architecture in yeast: new structure and new challenges J. Bacteriol. 180 1998 3735 3740
105. P. Orlean Architecture and biosynthesis of the Saccharomyces cerevisiae cell wall Genetics 192 2012 775 818
106. G. Lesage, and H. Bussey Cell wall assembly in Saccharomyces cerevisiae Microbiol. Mol. Biol. Rev. 70 2006 317 343
107. G. Lesage, A.M. Sdicu, P. Ménard, J. Shapiro, S. Hussein, and H. Bussey Analysis of β-1,3-glucan assembly in Saccharomyces cerevisiae using a synthetic interaction network and altered sensitivity to caspofungin Genetics 167 2004 35 49
108. A.H. Tong, G. Lesage, G.D. Bader, H. Ding, H. Xu, X. Xin, J. Young, G.F. Berriz, R.L. Brost, M. Chang, Y. Chen, X. Cheng, G. Chua, H. Friesen, D.S. Goldberg, J. Haynes, C. Humphries, G. He, S. Hussein, L. Ke, N. Krogan, Z. Li, J.N. Levinson, H. Lu, P. Ménard, C. Munyana, A.B. Parsons, O. Ryan, R. Tonikian, T. Roberts, A.M. Sdicu, J. Shapiro, B. Sheikh, B. Suter, S.L. Wong, L.V. Zhang, H. Zhu, C.G. Burd, S. Munro, C. Sander, J. Rine, J. Greenblatt, M. Peter, A. Bretscher, G. Bell, F.P. Roth, G.W. Brown, B. Andrews, H. Bussey, and C. Boone Global mapping of the yeast genetic interaction network Science 303 2004 808 813
109. S. Kawai, T.A. Pham, H.T. Nguyen, H. Nankai, T. Utsumi, Y. Fukuda, and K. Murata Molecular insights on DNA delivery into Saccharomyces cerevisiae Biochem. Biophys. Res. Commun. 317 2004 100 107
110. T.A. Pham, S. Kawai, E. Kono, and K. Murata The role of cell wall revealed by the visualization of Saccharomyces cerevisiae transformation Curr. Microbiol. 62 2011 956 961
111. Y. Cohen, M. Megyeri, O.C. Chen, G. Condomitti, I. Riezman, U. Loizides-Mangold, A. Abdul-Sada, N. Rimon, H. Riezman, F.M. Platt, A.H. Futerman, and M. Schuldiner The yeast p5 type ATPase, spf1, regulates manganese transport into the endoplasmic reticulum PLoS One 8 2013 e85519
112. Q. Yu, H. Wang, N. Xu, X. Cheng, Y. Wang, B. Zhang, L. Xing, and M. Li Spf1 strongly influences calcium homeostasis, hyphal development, biofilm formation and virulence in Candida albicans Microbiology 158 2012 2272 2282
113. A. Camirand, A. Heysen, B. Grondin, and A. Herscovics Glycoprotein biosynthesis in Saccharomyces cerevisiae. Isolation and characterization of the gene encoding a specific processing alpha-mannosidase J. Biol. Chem. 266 1991 15120 15127
114. F. Lipari, and A. Herscovics Calcium binding to the class I alpha-1,2-mannosidase from Saccharomyces cerevisiae occurs outside the EF hand motif Biochemistry 38 1999 1111 1118
115. H.K. Rudolph, A. Antebi, G.R. Fink, C.M. Buckley, T.E. Dorman, J. LeVitre, L.S. Davidow, J.I. Mao, and D.T. Moir The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family Cell 58 1989 133 145
116. A. Antebi, and G.R. Fink The yeast Ca2+-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution Mol. Biol. Cell 3 1992 633 654
117. A.C. Lustoza, L.M. Palma, A.R. Façanha, L.A. Okorokov, and A.L. Okorokova-Façanha P5A-type ATPase Cta4p is essential for Ca2+ transport in the endoplasmic reticulum of Schizosaccharomyces pombe PLoS One 6 2011 e27843
118. J.C. Cortés, R. Katoh-Fukui, K. Moto, J.C. Ribas, and J. Ishiguro Schizosaccharomyces pombe Pmr1p is essential for cell wall integrity and is required for polarized cell growth and cytokinesis Eukaryot. Cell 3 2004 1124 1135
119. G.R. Corradi, F. de Tezanos Pinto, L.R. Mazzitelli, and H.P. Adamo Shadows of an absent partner: ATP hydrolysis and phosphoenzyme turnover of the Spf1 (sensitivity to Pichia farinosa killer toxin) P5-ATPase J. Biol. Chem. 287 2012 30477 30484
120. D.M. Sørensen, A.B. Møller, M.K. Jakobsen, M.K. Jensen, P. Vangheluwe, M.J. Buch-Pedersen, and M.G. Palmgren Ca2+ induces spontaneous dephosphorylation of a novel P5A-type ATPase J. Biol. Chem. 287 2012 28336 28348
121. S. Heuck, U.C. Gerstmann, B. Michalke, and U. Kanter Genome-wide analysis of caesium and strontium accumulation in Saccharomyces cerevisiae Yeast 27 2010 817 835
122. M.C. Lee, E.A. Miller, J. Goldberg, L. Orci, and R. Schekman Bi-directional protein transport between the ER and Golgi Annu. Rev. Cell Dev. Biol. 20 2004 87 123
123. A. Spang Retrograde traffic from the Golgi to the endoplasmic reticulum Cold Spring Harb. Perspect. Biol. 5 2013 a013391
124. L.R. Poulsen, R.L. López-Marqués, and M.G. Palmgren Flippases: still more questions than answers Cell. Mol. Life Sci. 65 2008 3119 3125
125. T.T. Sebastian, R.D. Baldridge, P. Xu, and T.R. Graham Phospholipid flippases: building asymmetric membranes and transport vesicles Biochim. Biophys. Acta 1821 2012 1068 1077
126. S. Sanyal, C.G. Frank, and A.K. Menon Distinct flippases translocate glycerophospholipids and oligosaccharide diphosphate dolichols across the endoplasmic reticulum Biochemistry 47 2008 7937 7946
127. S. Sanyal, and A.K. Menon Specific transbilayer translocation of dolichol-linked oligosaccharides by an endoplasmic reticulum flippase Proc. Natl. Acad. Sci. U. S. A. 106 2009 767 772
128. S. Sanyal, and A.K. Menon Stereoselective transbilayer translocation of mannosyl phosphoryl dolichol by an endoplasmic reticulum flippase Proc. Natl. Acad. Sci. U. S. A. 107 2010 11289 11294
129. J.A. Coleman, A.L. Vestergaard, R.S. Molday, B. Vilsen, and J.P. Andersen Critical role of a transmembrane lysine in aminophospholipid transport by mammalian photoreceptor P4-ATPase ATP8A2 Proc. Natl. Acad. Sci. U. S. A. 109 2012 1449 1454
130. Y. Hatori, A. Hirata, C. Toyoshima, D. Lewis, R. Pilankatta, and G. Inesi Intermediate phosphorylation reactions in the mechanism of ATP utilization by the copper ATPase (CopA) of Thermotoga maritima J. Biol. Chem. 283 2008 22541 22549