Converting the yeast arginine Can1 permease to a lysine permease

Journal of Biological Chemistry

Volumn 289, Issue 10, 2014, Pages 7232-7246

  Ghaddar, Kassem ^a   Krammer, Eva Maria ^a   Mihajlovic, Natalija ^a   Brohée, Sylvain ^a   André, Bruno ^a   Prévost, Martine ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CELL MEMBRANES;

AMINO ACID TRANSPORTER; BINDING POCKETS; MOLECULAR LEVELS;

YEAST;

CAN1 PERMEASE; LYSINE PERMEASE; PERMEASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO ACID TRANSPORT; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ALIGNMENT;

AMINO ACID TRANSPORT; LIGAND DOCKING; MEMBRANE PROTEINS; MOLECULAR MODELING; PROTEIN ENGINEERING; PROTON TRANSPORT; SITE-DIRECTED MUTAGENESIS; TRANSPORTERS; YEAST PHYSIOLOGY;

AMINO ACID SEQUENCE; AMINO ACID TRANSPORT SYSTEMS, BASIC; ARGININE; BINDING SITES; BIOLOGICAL TRANSPORT; IMAGING, THREE-DIMENSIONAL; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84896741444     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.525915     Document Type: Article

References (69)

1. Jeschke, G. (2013) A comparative study of structures and structural transitions of secondary transporters with the LeuT fold. Eur. Biophys. J. 42, 181-197
2. Wong, F. H., Chen, J. S., Reddy, V., Day, J. L., Shlykov, M. A., Wakabayashi, S. T., and Saier, M. H., Jr. (2012) The amino acid-polyamine- organocation superfamily. J. Mol. Microbiol. Biotechnol. 22, 105-113
3. Van Belle D., and André, B. (2001) A genomic view of yeast membrane transporters. Curr. Opin. Cell Biol. 13, 389-398
4. Andre, B. (1995) An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast 11, 1575-1611
5. Ljungdahl, P. O., and Daignan-Fornier, B. (2012) Regulation of amino acid, nucleotide, and phosphate metabolism in Saccharomyces cerevisiae. Genetics 190, 885-929
6. Lauwers, E., Erpapazoglou, Z., Haguenauer-Tsapis, R., and André, B. (2010) The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20, 196-204
7. Gao, X., Lu, F., Zhou, L., Dang, S., Sun, L., Li, X., Wang, J., and Shi, Y. (2009) Structure and mechanism of an amino acid antiporter. Science 324, 1565-1568
8. Gao, X., Zhou, L., Jiao, X., Lu, F., Yan, C., Zeng, X., Wang, J., and Shi, Y. (2010) Mechanism of substrate recognition and transport by an amino acid antiporter. Nature 463, 828-832
9. Kowalczyk, L., Ratera, M., Paladino, A., Bartoccioni, P., Errasti-Murugarren, E., Valencia, E., Portella, G., Bial, S., Zorzano, A., Fita, I., Orozco, M., Carpena, X., Vázquez-Ibar, J. L., and Palacín, M. (2011) Molecular basis of substrate-induced permeation by an amino acid antiporter. Proc. Natl. Acad. Sci. U.S.A. 108, 3935-3940
10. Shaffer, P. L., Goehring, A., Shankaranarayanan, A., and Gouaux, E. (2009) Structure and mechanism of a Naindependent amino acid transporter. Science 325, 1010-1014
11. Ma, D., Lu, P., Yan, C., Fan, C., Yin, P., Wang, J., and Shi, Y. (2012) Structure and mechanism of a glutamate-GABA antiporter. Nature 483, 632-636
12. Krishnamurthy, H., Piscitelli, C. L., and Gouaux, E. (2009) Unlocking the molecular secrets of sodium-coupled transporters. Nature 459, 347-355
13. Khafizov, K., Staritzbichler, R., Stamm, M., and Forrest, L. R. (2010) A study of the evolution of inverted-topology repeats from LeuT-fold transporters using AlignMe. Biochemistry 49, 10702-10713
14. Grenson, M., Mousset, M., Wiame, J. M., and Bechet, J. (1966) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. I. Evidence for a specific arginine-transporting system. Biochim. Biophys. Acta 127, 325-338
15. Grenson, M. (1966) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. II. Evidence for a specific lysine-transporting system. Biochim. Biophys. Acta 127, 339-346
16. Hoffmann, W. (1985) Molecular characterization of the CAN1 locus in Saccharomyces cerevisiae. A transmembrane protein without N-terminal hydrophobic signal sequence. J. Biol. Chem. 260, 11831-11837
17. Sychrova, H., and Chevallier, M. R. (1993) Cloning and sequencing of the Saccharomyces cerevisiae gene LYP1 coding for a lysine-specific permease. Yeast 9, 771-782
18. Opekarová, M., Caspari, T., and Tanner, W. (1993) Unidirectional arginine transport in reconstituted plasma-membrane vesicles from yeast overexpressing CAN1. Eur. J. Biochem. 211, 683-688
19. Malinsky, J., Opekarová, M., and Tanner, W. (2010) The lateral compartmentation of the yeast plasma membrane. Yeast 27, 473-478
20. Spira, F., Mueller, N. S., Beck, G., von Olshausen, P., Beig, J., and Wedlich-Söldner, R. (2012) Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat. Cell Biol. 14, 640-648
21. MacGurn, J. A., Hsu, P. C., Smolka, M. B., and Emr, S. D. (2011) TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147, 1104-1117
22. Opekarová, M., Robl, I., and Tanner, W. (2002) Phosphatidyl ethanolamine is essential for targeting the arginine transporter Can1p to the plasma membrane of yeast. Biochim. Biophys. Acta 1564, 9-13
23. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST. A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
24. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank. Nucleic Acids Res. 28, 235-242
25. UniProt Consortium (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 40, D71-D75
26. Pei, J., Kim, B. H., and Grishin, N. V. (2008) PROMALS3D. A tool for multiple protein sequence and structure alignments. Nucleic Acids Res. 36, 2295-2300
27. Huang, X., and Miller, W. (1991) A time-efficient, linear-space local similarity algorithm. Adv. Appl. Math. 12, 337-357
28. Tusnády, G. E., and Simon, I. (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics. 17, 849-850
29. Hofmann, K., and Stoffel, W. (1993) TMbase. A database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler 374, 166
30. Fiser, A., and Sali, A. (2003) Modeller. Generation and refinement of homology-based protein structure models. Methods Enzymol. 374, 461-491
31. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK. A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
32. Li, H., Robertson, A. D., and Jensen, J. H. (2005) Very fast empirical prediction and rationalization of protein pKa values. Proteins 61, 704-721
33. Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., Sanschagrin, P. C., and Mainz, D. T. (2006) Extra precision glide. Docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J. Med. Chem. 49, 6177-6196
34. Lyne, P. D., Lamb, M. L., and Saeh, J. C. (2006) Accurate prediction of the relative potencies of members of a series of kinase inhibitors using molecular docking and MM-GBSA scoring. J. Med. Chem. 49, 4805-4808
35. Graves, A. P., Shivakumar, D. M., Boyce, S. E., Jacobson, M. P., Case, D. A., and Shoichet, B. K. (2008) Rescoring docking hit lists for model cavity sites. Predictions and experimental testing. J. Mol. Biol. 377, 914-934
36. Hou, T., Wang, J., Li, Y., and Wang, W. (2011) Assessing the performance of the molecular mechanics/Poisson Boltzmann surface area and molecular mechanics/generalized Born surface area methods. II. The accuracy of ranking poses generated from docking. J. Comput. Chem. 32, 866-877
37. Du, J., Sun, H., Xi, L., Li, J., Yang, Y., Liu, H., and Yao, X. (2011) Molecula modeling study of checkpoint kinase 1 inhibitors by multiple docking strategies and prime/MM-GBSA calculation. J. Comput. Chem. 32, 2800-2809
38. Hayes, J. M., and Archontis, G. (2012) MM-GB(PB)SA calculations of protein-ligand binding free energies. in Molecular Dynamics: Studies of Synthetic and Biological Macromolecules (Wang, L., ed) InTech, Rijeka, Croatia
39. Hou, T., Wang, J., Li, Y., and Wang, W. (2011) Assessing the performance of the MM/PBSA and MM/GBSA methods. The accuracy of binding free energy calculations based on molecular dynamics simulations. J. Chem. Inf. Model. 51, 69-82
40. Greenidge, P. A., Kramer, C., Mozziconacci, J. C., and Wolf, R. M. (2013) MM/GBSAbinding energy prediction on the PDBbind data set. Successes, failures, and directions for further improvement. J. Chem. Inf. Model. 53, 201-209
41. Ullmann, R. T., and Ullmann, G. M. (2011) Coupling of protonation, reduction, and conformational change in azurin from Pseudomonas aeruginosa investigated with free energy measures of cooperativity. J. Phys. Chem. B 115, 10346-10359
42. Ullmann, R. T., Andrade, S. L., and Ullmann, G. M. (2012) Thermodynamics of transport through the ammonium transporter Amt-1 investigated with free energy calculations. J. Phys. Chem. B 116, 9690-9703
43. Ullmann, R. T., and Ullmann, G. M. (2012) GMCT. A Monte Carlo simulation package for macromolecular receptors. J. Comput. Chem. 33, 887-900
44. Brohée, S., Janky, R., Abdel-Sater, F., Vanderstocken, G., André, B., and van Helden J. (2011) Unraveling networks of co-regulated genes on the sole basis of genome sequences. Nucleic Acids Res. 39, 6340-6358
45. Bechet, J., Greenson, M., and Wiame, J. M. (1970) Mutations affecting the repressibility of arginine biosynthetic enzymes in Saccharomyces cerevisiae. Eur. J. Biochem. 12, 31-39
46. Jacobs, P., Jauniaux, J. C., and Grenson, M. (1980) A cis-dominant regulatory mutation linked to the argB-argC gene cluster in Saccharomyces cerevisiae. J. Mol. Biol. 139, 691-704
47. Godard, P., Urrestarazu, A., Vissers, S., Kontos, K., Bontempi, G., van Helden, J., and André, B. (2007) Effect of 21 different nitrogen sources on global gene expression in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 27, 3065-3086
48. Bonneaud, N., Ozier-Kalogeropoulos, O., Li, G. Y., Labouesse, M., Minvielle-Sebastia, L., and Lacroute, F. (1991) A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast 7, 609-615
49. Hein, C., Springael, J. Y., Volland, C., Haguenauer-Tsapis, R., and André, B. (1995) NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18, 77-87
50. De Craene, J. O., Soetens, O., and Andre, B. (2001) The Npr1 kinase controls biosynthetic and endocytic sorting of the yeast Gap1 permease. J. Biol. Chem. 276, 43939-43948
51. Liang, J., Naveed, H., Jimenez-Morales, D., Adamian, L., and Lin, M. (2012) Computational studies of membrane proteins. Models and predictions for biological understanding. Biochim. Biophys. Acta 1818, 927-941
52. Kozma, D., Simon, I., and Tusnády, G. E. (2013) PDBTM. Protein Data Bank of transmembrane proteins after 8 years. Nucleic Acids Res. 41, D524-D529
53. Nilsson, J., Persson, B., and von Heijne G. (2005) Comparative analysis of amino acid distributions in integral membrane proteins from 107 genomes. Proteins 60, 606-616
54. Killian, J. A., and von Heijne G. (2000)Howproteins adapt to a membranewater interface. Trends Biochem. Sci. 25, 429-434
55. Oh, B. H., Ames, G. F., and Kim, S. H. (1994) Structural basis for multiple ligand specificity of the periplasmic lysine-, arginine-, ornithine-binding protein. J. Biol. Chem. 269, 26323-26330
56. Cheng, T., Li, X., Li, Y., Liu, Z., and Wang, R. (2009) Comparative assessment of scoring functions on a diverse test set. J. Chem. Inf. Model. 49, 1079-1093
57. Li, J., Abel, R., Zhu, K., Cao, Y., Zhao, S., and Friesner, R. A. (2011) The VSGB 2.0 model. A next generation energy model for high resolution protein structure modeling. Proteins 79, 2794-2812
58. Malinská, K., Malinský, J., Opekarová, M., and Tanner, W. (2003) Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell 14, 4427-4436
59. Fischer, W. N., Loo, D. D., Koch, W., Ludewig, U., Boorer, K. J., Tegeder, M., Rentsch, D., Wright, E. M., and Frommer, W. B. (2002) Low and high affinity amino acid Hcotransporters for cellular import of neutral and charged amino acids. Plant J. 29, 717-731
60. Fang, Y., Jayaram, H., Shane, T., Kolmakova-Partensky, L., Wu, F., Williams, C., Xiong, Y., and Miller, C. (2009) Structure of a prokaryotic virtual proton pump at 3.2 A resolution. Nature 460, 1040-1043
61. Yamashita, A., Singh, S. K., Kawate, T., Jin, Y., and Gouaux, E. (2005) Crystal structure of a bacterial homologue of Na+/Cldependent neurotransmitter transporters. Nature 437, 215-223
62. Forrest, L. R., Krämer, R., and Ziegler, C. (2011) The structural basis of secondary active transport mechanisms. Biochim. Biophys. Acta 1807, 167-188
63. Law, C. J., Maloney, P. C., and Wang, D. N. (2008) Ins and outs of major facilitator superfamily antiporters. Annu. Rev. Microbiol. 62, 289-305
64. Law, C. J., Yang, Q., Soudant, C., Maloney, P. C., and Wang, D. N. (2007) Kinetic evidence is consistent with the rocker-switch mechanism of membrane transport by GlpT. Biochemistry 46, 12190-12197
65. Hein, C., and André, B. (1997) A C-terminal di-leucine motif and nearby sequences are required for NH4(+)-induced inactivation and degradation of the general amino acid permease, Gap1p, of Saccharomyces cerevisiae. Mol. Microbiol. 24, 607-616
66. Brohée, S., Barriot, R., Moreau, Y., and André, B. (2010) YTPdb. A wiki database of yeast membrane transporters. Biochim. Biophys. Acta 1798, 1908-1912
67. Frishman, D., and Argos, P. (1995) Knowledge-based protein secondary structure assignment. Proteins 23, 566-579
68. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD. Visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-28
69. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) ClustalW and ClustalX version 2.0. Bioinformatics 23, 2947-2948