Characterization of the biochemical and biophysical properties of the Saccharomyces cerevisiae phosphate transporter Pho89

Biochemical and Biophysical Research Communications

Volumn 436, Issue 3, 2013, Pages 551-556

  Sengottaiyan, Palanivelu ^a,d   Petrlova, Jitka ^b   Lagerstedt, Jens O ^b   Ruiz Pavon, Lorena ^a   Budamagunta, Madhu S ^c   Voss, John C ^c   Persson, Bengt L ^a  

^a LINNAEUS UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Circular dichroism; Oligomer; Pho89; Phosphate transport; Pichia pastoris; Reconstitution

Indexed keywords

PHOSPHATE TRANSPORTER; PROTEOLIPOSOME;

ARTICLE; CONFORMATIONAL TRANSITION; ELECTRON SPIN RESONANCE; ENZYME SPECIFICITY; NONHUMAN; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION;

ΔPNA(+); CD; CIRCULAR DICHROISM; ELECTROCHEMICAL NA(+) CONCENTRATION GRADIENT; ELECTRON PARAMAGNETIC RESONANCE; EPR; OLIGOMER; PHO89; PHOSPHATE TRANSPORT; PICHIA PASTORIS; RECONSTITUTION;

BIOLOGICAL TRANSPORT; CELL MEMBRANE; CIRCULAR DICHROISM; ELECTRON SPIN RESONANCE SPECTROSCOPY; PHOSPHORYLCHOLINE; PICHIA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEOLIPIDS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE III; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

MAMMALIA; PICHIA PASTORIS; SACCHAROMYCES CEREVISIAE;

EID: 84879889835     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.06.011     Document Type: Article

References (35)

1. Saier M.H. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 2000, 64:354-411.
2. Forster I.C., Hernando N., Biber J., Murer H. Phosphate transport kinetics and structure-function relationships of SLC34 and SLC20 proteins. Curr. Top. Membr. 2012, 70:313-356.
3. Pattison-Granberg J., Persson B.L. Regulation of cation-coupled high-affinity phosphate uptake in the yeast Saccharomyces cerevisiae. J. Bacteriol. 2000, 182:5017-5019.
4. Serrano R., Ruiz A., Bernal D., Chambers J.R., Arino J. The transcriptional response to alkaline pH in Saccharomyces cerevisiae: evidence for calcium-mediated signalling. Mol. Microbiol. 2002, 46:1319-1333.
5. Wiesenberger G., Steinleitner K., Malli R., Graier W.F., Vormann J., Schweyen R.J., Stadler J.A. Mg2+ deprivation elicits rapid Ca2+ uptake and activates Ca2+/calcineurin signaling in Saccharomyces cerevisiae. Eukaryot. Cell 2007, 6:592-599.
6. Roomans G.M., Blasco F., Borst-Pauwels G.W. Cotransport of phosphate and sodium by yeast. Biochim. Biophys. Acta 1977, 467:65-71.
7. Kavanaugh M.P., Kabat D. Identification and characterization of a widely expressed phosphate transporter/retrovirus receptor family. Kidney Int. 1996, 49:959-963.
8. Daram P., Brunner S., Rausch C., Steiner C., Amrhein N., Bucher M. Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. Plant Cell 1999, 11:2153-2166.
9. Versaw W.K., Metzenberg R.L. Repressible cation-phosphate symporters in Neurospora crassa. Proc. Natl. Acad. Sci. USA 1995, 92:3884-3887.
10. Andersson M.R., Samyn D.R., Persson B.L. Mutational analysis of conserved glutamic acids of Pho89, a Saccharomyces cerevisiae high-affinity inorganic phosphate:Na+ symporter. Biologia 2012, 67:1056-1061.
11. Persson B.L., Petersson J., Fristedt U., Weinander R., Berhe A., Pattison J. Phosphate permeases of Saccharomyces cerevisiae: structure, function and regulation. Biochim. Biophys. Acta 1999, 1422:255-272.
12. Martinez P., Persson B.L. Identification, cloning and characterization of a derepressible Na+-coupled phosphate transporter in Saccharomyces cerevisiae. Mol. Gen. Genet. 1998, 258:628-638.
13. Bottger P., Pedersen L. Two highly conserved glutamate residues critical for type III sodium-dependent phosphate transport revealed by uncoupling transport function from retroviral receptor function. J. Biol. Chem. 2002, 277:42741-42747.
14. Sengottaiyan P., Ruiz-Pavon L., Persson B.L. Functional expression, purification and reconstitution of the recombinant phosphate transporter Pho89 of Saccharomyces cerevisiae. FEBS J. 2013, 280:965-975.
15. Salaun C., Marechal V., Heard J.M. Transport-deficient Pit2 phosphate transporters still modify cell surface oligomers structure in response to inorganic phosphate. J. Mol. Biol. 2004, 340:39-47.
16. Jono S., McKee M.D., Murry C.E., Shioi A., Nishizawa Y., Mori K., Morii H., Giachelli C.M. Phosphate regulation of vascular smooth muscle cell calcification. Circ. Res. 2000, 87:E10-E17.
17. Wang C., Li Y., Shi L., Ren J., Patti M., Wang T., de Oliveira J.R., Sobrido M.J., Quintans B., Baquero M., Cui X., Zhang X.Y., Wang L., Xu H., Wang J., Yao J., Dai X., Liu J., Zhang L., Ma H., Gao Y., Ma X., Feng S., Liu M., Wang Q.K., Forster I.C., Zhang X., Liu J.Y. Mutations in SLC20A2 link familial idiopathic basal ganglia calcification with phosphate homeostasis. Nat. Genet. 2012, 44:254-256.
18. Oda M.N., Forte T.M., Ryan R.O., Voss J.C. The C-terminal domain of apolipoprotein A-I contains a lipid-sensitive conformational trigger. Nat. Struct. Biol. 2003, 10:455-460.
19. Fristedt U., van Der Rest M., Poolman B., Konings W.N., Persson B.L. Studies of cytochrome c oxidase-driven H+-coupled phosphate transport catalyzed by the Saccharomyces cerevisiae Pho84 permease in coreconstituted vesicles. Biochemistry 1999, 38:16010-16015.
20. Fristedt U., Weinander R., Martinsson H.S., Persson B.L. Characterization of purified and unidirectionally reconstituted Pho84 phosphate permease of Saccharomyces cerevisiae. FEBS Lett. 1999, 458:1-5.
21. Petrlova J., Duong T., Cochran M.C., Axelsson A., Morgelin M., Roberts L.M., Lagerstedt J.O. The fibrillogenic L178H variant of apolipoprotein A-I forms helical fibrils. J. Lipid Res. 2012, 53:390-398.
22. Morrow J.A., Segall M.L., Lund-Katz S., Phillips M.C., Knapp M., Rupp B., Weisgraber K.H. Differences in stability among the human apolipoprotein E isoforms determined by the amino-terminal domain. Biochemistry 2000, 39:11657-11666.
23. Kefala G., Ahn C., Krupa M., Esquivies L., Maslennikov I., Kwiatkowski W., Choe S. Structures of the OmpF porin crystallized in the presence of foscholine-12. Protein Sci. 2010, 19:1117-1125.
24. Moncoq K., Kemp G., Li X., Fliegel L., Young H.S. Dimeric structure of human Na+/H+ exchanger isoform 1 overproduced in Saccharomyces cerevisiae. J. Biol. Chem. 2008, 283:4145-4154.
25. Hwang P.M., Choy W.Y., Lo E.I., Chen L., Forman-Kay J.D., Raetz C.R., Prive G.G., Bishop R.E., Kay L.E. Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl. Acad. Sci. USA 2002, 99:13560-13565.
26. Zvyagilskaya R.A., Lundh F., Samyn D., Pattison-Granberg J., Mouillon J.M., Popova Y., Thevelein J.M., Persson B.L. Characterization of the Pho89 phosphate transporter by functional hyperexpression in Saccharomyces cerevisiae. FEMS Yeast Res. 2008, 8:685-696.
27. Pourcher T., Leclercq S., Brandolin G., Leblanc G. Melibiose permease of Escherichia coli: large scale purification and evidence that H+, Na+, and Li+ sugar symport is catalyzed by a single polypeptide. Biochemistry 1995, 34:4412-4420.
28. Arino J., Ramos J., Sychrova H. Alkali metal cation transport and homeostasis in yeasts. Microbiol. Mol. Biol. Rev. 2010, 74:95-120.
29. Pratt J.R., Mouillon J.M., Lagerstedt J.O., Pattison-Granberg J., Lundh K.I., Persson B.L. Effects of methylphosphonate, a phosphate analogue, on the expression and degradation of the high-affinity phosphate transporter Pho84, in Saccharomyces cerevisiae. Biochemistry 2004, 43:14444-14453.
30. Popova Y., Thayumanavan P., Lonati E., Agrochao M., Thevelein J.M. Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor. Proc. Natl. Acad. Sci. USA 2010, 107:2890-2895.
31. Martin S.R., Schilstra M.J. Circular dichroism and its application to the study of biomolecules. Methods Cell Biol. 2008, 84:263-293.
32. Berliner L.J., Grunwald J., Hankovszky H.O., Hideg K. A novel reversible thiolspecific spin label - papain active site labeling and inhibition. Anal. Biochem. 1982, 119:450-455.
33. Guo Z.F., Cascio D., Hideg K., Kalai T., Hubbell W.L. Structural determinants of nitroxide motion in spin-labeled proteins: Tertiary contact and solvent-inaccessible sites in helix G of T4 lysozyme. Protein Sci. 2007, 16:1069-1086.
34. Hess J.F., Budamagunta M.S., Aziz A., Fitzgerald P.G., Voss J.C. Electron paramagnetic resonance analysis of the vimentin tail domain reveals points of order in a largely disordered region and conformational adaptation upon filament assembly. Protein Sci. 2013, 22:47-55.
35. Columbus L., Hubbell W.L. A new spin on protein dynamics. Trends Biochem. Sci. 2002, 27:288-295.