Analysing the substrate multispecificity of a proton-coupled oligopeptide transporter using a dipeptide library

Nature Communications

Volumn 4, Issue , 2013, Pages

  Ito, Keisuke ^a   Hikida, Aya ^a   Kawai, Shun ^b   Lan, Vu Thi Tuyet ^a   Motoyama, Takayasu ^c   Kitagawa, Sayuri ^c   Yoshikawa, Yuko ^a   Kato, Ryuji ^b   Kawarasaki, Yasuaki ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c Fuji Oil Co Ltd   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIPEPTIDE; HISTIDINE; ISOLEUCINE; LEUCINE; PEPTIDE; PHENYLALANINE; PROTON COUPLED OLIGOPEPTIDE TRANSPORTER; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG; VALINE; CARRIER PROTEIN; PROTON; PTR2 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; PEPTIDE LIBRARY; PROTEIN BINDING;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; FLUORESCENCE BASED COMPETITIVE UPTAKE ASSAY; FLUORESCENCE MICROSCOPY; FUNGUS GROWTH; GENE EXPRESSION; GENE EXPRESSION SYSTEM; GENE INACTIVATION; IC50; NONHUMAN; PEPTIDE ANALYSIS; PEPTIDE LIBRARY; PREDICTION; SACCHAROMYCES CEREVISIAE; WESTERN BLOTTING; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; KINETICS; METABOLISM; PROTEIN BINDING; TRANSPORT AT THE CELLULAR LEVEL;

SACCHAROMYCES CEREVISIAE;

BIOLOGICAL TRANSPORT; DIPEPTIDES; GENE EXPRESSION REGULATION, FUNGAL; KINETICS; MEMBRANE TRANSPORT PROTEINS; PEPTIDE LIBRARY; PROTEIN BINDING; PROTONS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84894520813     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3502     Document Type: Article

References (50)

1. Daniel, H., Spanier, B., Kottra, G. & Weitz, D. From bacteria to man: archaic proton-dependent peptide transporters at work. Physiology (Bethesda) 21, 93-102 (2006).
2. Gomolplitinant, K. M. & Saier, Jr. M. H. Evolution of the oligopeptide transporter family. J. Membr. Biol. 240, 89-110 (2011).
3. Steiner, H. Y., Naider, F. & Becker, J. M. The PTR family: a new group of peptide transporters. Mol. Microbiol. 16, 825-834 (1995).
4. Maebuchi, M. et al. Improvement in the intestinal absorpton of soy protein by enzymatic digestion to oligopeptide in healthy adult men. Food Sci. Technol. Res 13, 45-53 (2007).
5. Matthews, D. M. Intestinal absorption of peptides. Physiol. Rev. 55, 537-608 (1975).
6. Ito, K. et al. Soy peptides enhance heterologous membrane protein productivity during the exponential growth phase of Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 76, 628-631 (2012).
7. Biegel, A. et al. The renal type H+/peptide symporter PEPT2: structure-affinity relationships. Amino Acids 31, 137-156 (2006).
8. Fei, Y. J. et al. Expression cloning of a mammalian proton-coupled oligopeptide transporter. Nature 368, 563-566 (1994).
9. Liang, R. et al. Human intestinal H+/peptide cotransporter. Cloning, functional expression, and chromosomal localization. J. Biol. Chem. 270, 6456-6463 (1995).
10. Adibi, S. A. The oligopeptide transporter (Pept-1) in human intestine: biology and function. Gastroenterology 113, 332-340 (1997).
11. Liu, W. et al. Molecular cloning of PEPT 2, a new member of the H+/peptide cotransporter family, from human kidney. Biochim. Biophys. Acta. 1235, 461-466 (1995).
12. Boll, M. et al. Expression cloning and functional characterization of the kidney cortex high-affinity proton-coupled peptide transporter. Proc. Natl Acad. Sci. USA 93, 284-289 (1996).
13. Shen, H. et al. Localization of PEPT1 and PEPT2 proton-coupled oligopeptide transporter mRNA and protein in rat kidney. Am. J. Physiol. 276, F658-F665 (1999).
14. Newstead, S. et al. Crystal structure of a prokaryotic homologue of the mammalian oligopeptide-proton symporters, PepT1 and PepT2. EMBO J. 30, 417-426 (2011).
15. Solcan, N. et al. Alternating access mechanism in the POT family of oligopeptide transporters. EMBO J. 31, 3411-3421 (2012).
16. Rubio-Aliaga, I. & Daniel, H. Mammalian peptide transporters as targets for drug delivery. Trends Pharmacol. Sci. 23, 434-440 (2002).
17. Homann, O. R., Cai, H., Becker, J. M. & Lindquist, S. L. Harnessing natural diversity to probe metabolic pathways. PLoS Genet. 1, e80 (2005).
18. Cai, H., Kauffman, S., Naider, F. & Becker, J. M. Genomewide screen reveals a wide regulatory network for di/tripeptide utilization in Saccharomyces cerevisiae. Genetics 172, 1459-1476 (2006).
19. Perry, J. R., Basrai, M. A., Steiner, H. Y., Naider, F. & Becker, J. M. Isolation and characterization of a Saccharomyces cerevisiae peptide transport gene. Mol. Cell Biol. 14, 104-115 (1994).
20. Hauser, M., Narita, V., Donhardt, A. M., Naider, F. & Becker, J. M. Multiplicity and regulation of genes encoding peptide transporters in Saccharomyces cerevisiae. Mol. Membr. Biol. 18, 105-112 (2001).
21. Kitagawa, S. et al. Effect of soy peptide on brewing beer. J. Biosci. Bioeng. 105, 360-366 (2008).
22. Cai, H., Hauser, M., Naider, F. & Becker, J. M. Differential regulation and substrate preference in two peptide transporters of Saccharomyces cerevisiae. Eukaryot. Cell 6, 1805-1813 (2007).
23. Daniel, H. & Kottra, G. The proton oligopeptide cotransporter family SLC15 in physiology and pharmacology. Pflugers. Arch. 447, 610-618 (2004).
24. Thesis, S. et al. Synthesis and characterization of high affinity inhibitors of the H+/peptide transporter PEPT2. J. Biol. Chem 277, 7287-7292 (2002).
25. Biegel, A., Gebauer, S., Brandsch, M., Neubert, K. & Thondorf, I. Structural requirements for the substrates of the H+/peptide cotransporter PEPT2 determined by three-dimensional quantitative structure-activity relationship analysis. J. Med. Chem 49, 4286-4296 (2006).
26. Cheng, Y. & Prusoff, W. H. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108 (1973).
27. Nour-Eldin, H. H. et al. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488, 531-534 (2012).
28. Foltz, M., Meyer, A., Theis, S., Demuth, H. U. & Daniel, H. A rapid in vitro screening for delivery of peptide-derived peptidase inhibitors as potential drug candidates via epithelial peptide transporters. J. Pharmacol. Exp. Ther. 310, 695-702 (2004).
29. Geissler, S., Zwarg, M., Knütter, I., Markwardt, F. & Brandsch, M. The bioactive dipeptide anserine is transported by human proton-coupled peptide transporters. FEBS J. 277, 790-795 (2010).
30. Jensen, J. M. et al. Biophysical characterization of the proton-coupled oligopeptide transporter YjdL. Peptides 38, 89-93 (2012).
31. Byrd, C., Turner, G. C. & Varshavsky, A. The N-end rule pathway controls the import of peptides through degradation of a transcriptional repressor. EMBO J. 17, 269-277 (1998).
32. Turner, G. C., Du, F. & Varshavsky, A. Peptides accelerate their uptake by activating a ubiquitin-dependent proteolytic pathway. Nature 405, 579-583 (2000).
33. Hwang, C. S. & Varshavsky, A. Regulation of peptide import through phosphorylation of Ubr1, the ubiquitin ligase of the N-end rule pathway. Proc. Natl Acad. Sci. USA 105, 19188-19193 (2008).
34. Braus, G. H. Aromatic amino acid biosynthesis in the yeast Saccharomyces cerevisiae: a model system for the regulation of a eukaryotic biosynthetic pathway. Microbiol. Rev. 55, 349-370 (1991).
35. Foley, D. W., Rajamanickam, J., Bailey, P. D. & Meredith, D. Bioavailability through PepT1: the role of computer modelling in intelligent drug design. Curr. Comput. Aided Drug Des. 6, 68-78 (2010).
36. Brandsch, M., Knütter, I. & Bosse-Doenecke, E. Pharmaceutical and pharmacological importance of peptide transporters. J. Pharm. Pharmacol. 60, 543-585 (2008).
37. Terada, T. & Inui, K. Peptide transporters: structure, function, regulation and application for drug delivery. Curr. Drug Metab. 5, 85-94 (2004).
38. Zhang, L. et al. Synthesis and evaluation of a dipeptide-drug conjugate library as substrates for PEPT1. ACS Comb. Sci 14, 108-114 (2012).
39. Kouodom, M. N. et al. Toward the selective delivery of chemotherapeutics into tumor cells by targeting peptide transporters: tailored gold-based anticancer peptidomimetics. J. Med. Chem 55, 2212-2226 (2012).
40. Kaga, C., Okochi, M., Tomita, Y., Kato, R. & Honda, H. Computationally assisted screening and design of cell-interactive peptides by a cell-based assay using peptide arrays and a fuzzy neural network algorithm. Biotechniques 44, 393-402 (2008).
41. Ito, K. et al. Advanced method for high-throughput expression of mutated eukaryotic membrane proteins in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 371, 841-845 (2008).
42. Drew, D. et al. GFP-based optimization scheme for the overexpression and purification of eukaryotic membrane proteins in Saccharomyces cerevisiae. Nat. Protoc. 3, 784-798 (2008).
43. Newstead, S., Kim, H., von Heijne, G., Iwata, S. & Drew, D. High-throughput fluorescent-based optimization of eukaryotic membrane protein overexpression and purification in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 104, 13936-13941 (2007).
44. Kawashima, S. et al. AAindex: amino acid index database, progress report 2008. Nucleic Acids Res. 36, D202-D205 (2008).
45. Zimmerman, J. M., Eliezer, N. & Simha, R. The characterization of amino acid sequences in proteins by statistical methods. J. Theor. Biol. 21, 170-201 (1968).
46. Fauchere, J. L., Charton, M., Kier, L. B., Verloop, A. & Pliska, V. Amino acid side chain parameters for correlation studies in biology and pharmacology. Int. J. Pept. Protein Res. 32, 269-278 (1988).
47. Takano, K. & Yutani, K. A new scale for side-chain contribution to protein stability based on the empirical stability analysis of mutant proteins. Protein. Eng. 14, 525-528 (2001).
48. Kyte, J. & Doolittle, R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132 (1982).
49. Crawford, J. L., Lipscomb, W. N. & Schellman, C. G. The reverse turn as a polypeptide conformation in globular proteins. Proc. Natl Acad. Sci. USA 70, 538-542 (1973).
50. Krigbaum, W. R. & Komoriya, A. Local interactions as a structure determinant for protein molecules: II. Biochim. Biophys. Acta 576, 204-248 (1979).