Construction of a fluorescent biosensor family

Protein Science

Volumn 11, Issue 11, 2002, Pages 2655-2675

  De Lorimier, Robert M ^a   Jeff Smith, J ^b   Dwyer, Mary A ^c   Looger, Loren L ^a   Sali, Kevin M ^b   Paavola, Chad D ^c   Rizk, Shahir S ^a   Sadigov, Shamil ^b   Conrad, David W ^a   Loew, Leslie ^a   Hellinga, Homme W ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NASA AMES RESEARCH CENTER   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Bioinformatics; Biosensor; Conformational change; Fluorescence, ratiometry; Periplasmic binding proteins

Indexed keywords

AMINO ACID; ANION; ASPARTIC ACID; BACTERIAL PROTEIN; CATION; CYSTEINE; DIPEPTIDE; GLUTAMIC ACID; SUGAR; FLUORESCENT DYE; GLUCOSE; LIGAND; PERIPLASMIC BINDING PROTEIN;

ARTICLE; BIOINFORMATICS; BIOSENSOR; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; FLUORESCENCE; LIGAND BINDING; MUTATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN FAMILY; REPORTER GENE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; BACTERIAL GENE; CHEMICAL STRUCTURE; CHEMISTRY; GENETIC PROCEDURES; GENETICS; HUMAN; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MUTAGENESIS; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SYNTHESIS;

BACTERIA (MICROORGANISMS);

AMINO ACID SEQUENCE; BIOSENSING TECHNIQUES; CLONING, MOLECULAR; FLUORESCENT DYES; GENES, BACTERIAL; GLUCOSE; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MUTAGENESIS; PERIPLASMIC BINDING PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

EID: 0036838307     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.021860     Document Type: Article

References (90)

1. Abouhamad, W.N., Manson, M., Gibson, M.M., and Higgins, C.F. 1991.Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: Characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol. Microbiol. 5: 1035-1047.
2. Adhikari, P., Kirby, S. D., Nowalk, A.J., Veraldi, K.L., Schryvers, A.B., and Mietzner, T.A. 1995. Biochemical characterization of a Haemophilus influenzae periplasmic iron transport operon. J. Biol. Chem. 270: 25142-25149.
3. Anraku, Y. 1968. Transport of sugars and amino acids in bacteria. I. Purification and specificity of the galactose- and leucine-binding proteins. J. Biol. Chem. 243: 3116-3122.
4. AOAC. 1995. Official methods of analysis of AOAC International, 16th ed. AOAC International, Arlington, VA.
5. APHA. 1992. Standard methods for the examination of water and wastewater, 18th ed. American Public Health Association, Washington, D.C.
6. Barash, H. and Halpern, Y.S. 1975. Purification and properties of glutamate binding protein from the periplasmic space of Escherichia coli K-12. Biochim. Biophys. Acta 386: 168-180.
7. Benson, D.E., Conrad, D.W., de Lorimier, R.M.. Trammell, S.A., and Hellinga, H.W. 2001. Design of bioelectronic interfaces by exploiting hinge-bending motions in proteins. Science 293: 1641-1644.
8. 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.
9. Bjorkman, A.J. and Mowbray, S.L. 1998. Multiple open forms of ribose-binding protein trace the path of its conformational change. J. Mol. Biol. 279: 651-664.
10. Blattner, F.R., Plunkett, G., 3rd, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., Collado-Vides, J., Glasner. J.D., Rode, C.K., Mayhew, G.F., et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
11. Brosius, J. and Holy, A. 1984. Regulation of ribosomal RNA promoters with a synthetic lac operator. Proc. Natl. Acad. Sci. 81: 6929-6933.
12. Brune, M., Hunter, J.L., Corrie, J.E., and Webb, M.R. 1994. Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment I ATPase. Biochemistry 33: 8262-8271.
13. Bruns, C.M., Nowalk, A.J., Arvai, A.S., McTigue, M.A., Vaughan, K.G., Mietzner, T.A., and McRee, D.E. 1997. Structure of Haemophilus influenzae Fe(+3)-binding protein reveals convergent evolution within a superfamily. Nat. Struct. Biol. 4: 919-924.
14. Bruns, C.M., Anderson, D.S., Vaughan, K.G., Williams, P.A., Nowalk, A.J., McRee, D.E., and Mietzner, T.A. 2001. Crystallographic and biochemical analyses of the metal-free Haemophilus influenzae Fe3+-binding protein. Biochemistry 40: 15631-15637.
15. Burkhardt, R.T., Sheiko, M.C., and Batsakis, J.G. 1979. Clinical laboratory estimations of serum and urinary phosphate. Am. J. Clin. Pathol. 72: 326-329.
16. Burrin, J.M. and Price, C.P. 1985. Measurement of blood glucose. Ann. Clin. Biochem. 22: 327-342.
17. Burtis, C.A. and Ashwood, E.A. 1994. Teitz textbook of clinical chemistry, 2nd ed. W.B. Saunders Co., Philadelphia.
18. Clark, A.F., Gerken, T.A., and Hogg, R.W. 1982. Proton nuclear magnetic resonance spectroscopy and ligand binding dynamics of the Escherichia coli L-arabinose binding protein. Biochemistry 21: 2227-2233.
19. Dattelbaum, J.D. and Lakowicz, JR. 2001. Optical determination of glutamine using a genetically engineered protein. Anal. Biochem. 291: 89-95.
20. Deanda, K., Zhang, M., Eddy, C., and Picataggio, S. 1996. Development of an arabinose-fermenting Zymomonas mobilis strain by metabolic pathway engineering. Appl. Environ. Microbiol. 62: 4465-4470.
21. Doering, D.S. 1992. 'Functional and structural studies of a small f-actin binding domain.' Ph.D. thesis, Massachusetts Institute of Technology.
22. Dunten, P. and Mowbray, S.L. 1995. Crystal structure of the dipeptide binding protein from Escherichia coli involved in active transport and chemotaxis. Protein Sci. 4: 2327-2334.
23. Duplay, P., Bedouelle, H., Fowler, A., Zabin, I., Saurin, W., and Hofnung, M. 1984. Sequences of the malE gene and of its product, the maltose-binding protein of Escherichia coli K12. J. Biol. Chem. 259: 10606-10613.
24. Ellman, G.L. 1958. A colorimetric method for determining low concentrations of mercaptans. Arch. Biochem. Biophys. 74: 443-450.
25. EPA. 1999. Health effects from exposure to high levels of sulfate in drinking water study. Publication No. 815R99001 (pp. 1-25). U.S. Environmental Protection Agency, Office of Drinking Water and Ground Water, Washington. DC.
26. Gilardi, G., Zhou, L.Q., Hibbert, L., and Cass, A.E. 1994. Engineering the maltose binding protein for reagentless fluorescence sensing. Anal. Chem. 66: 3840-3847.
27. Gilardi, G., Mei, G., Rosato, N., Agro, A.F., and Cass, A.E.G. 1997. Spectroscopic properties of an engineered maltose binding protein. Prot. Eng. 10: 479-486.
28. Groarke, J.M., Mahoney, W.C., Hope, J.N., Furlong, C.E., Robb, F.T., Zalkin. H., and Hermodson, M.A. 1983. The amino acid sequence of D-ribose-binding protein from Escherichia coli K12. J. Biol. Chem. 258: 12952-12956.
29. Guyer, C.A., Morgan, D.G., and Staros, J.V. 1986. Binding specificity of the periplasmic oligopeptide-binding protein from Escherichia coli. 2. Bacteriol. 168: 775-779.
30. Hall, E.E.H. 1991. Biosensors. Prentice-Hall, Englewood Cliffs, NJ.
31. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166: 557-580.
32. He, J.J. and Quiocho, F.A. 1993. Dominant role of local dipoles in stabilizing uncompensated charges on a sulfate sequestered in a periplasmic active transport protein. Protein Sci. 2: 1643-1647.
33. Hellinga, H.W. and Evans, P.R. 1985. Nucleotide sequence and high-level expression of the major Escherichia coli phosphofructokinase. Eur. J. Biochem. 149: 363-373.
34. Hellinga, H.W. and Marvin, J.S. 1998. Protein engineering and the development of generic biosensors. Trends Biotech. 16: 183-189.
35. Hellinga, H.W. and Richards, F.M. 1991. Construction of new ligand binding sites in proteins of known structure. I. Computer-aided modeling of sites with pre-defined geometry. J. Mol. Biol. 222: 763-785.
36. Hirshberg, M., Henrick, K., Haire, L.L., Vasisht, N., Brune, M., Corrie, J.E., and Webb, M.R. 1998. Crystal structure of phosphate binding protein labeled with a coumarin fluorophore, a probe for inorganic phosphate. Biochemistry 37: 10381-10385.
37. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
38. Hochuli, E., Dobeli, H., and Schacher, A. 1987. New metal chelate adsorbent selective for proteins and peptides containing neighbouring histidine residues. J. Chromatogr. A 411: 177-184.
39. Hsiao, C.D., Sun, Y.J., Rose, J., and Wang, B.C. 1996. The crystal structure of glutamine-binding protein from Escherichia coli. J. Mol. Biol. 262: 225-242.
40. Jacobson, B.L. and Quiocho, F.A. 1988. Sulfate-binding protein dislikes protonated oxyacids. A molecular explanation. J. Mol. Biol. 204: 783-787.
41. Kraulis, P.J. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946-950.
42. Lakowicz, J.R. 1999. Principles of fluorescence spectroscopy, 2nd ed., p. 698. Kluwer Academic Press, New York.
43. Ledvina, P.S., Yao, N., Choudhary, A., and Quiocho, F.A. 1996. Negative electrostatic surface potential of protein sites specific for anionic ligands. Proc. Natl. Acad. Sci. 93: 6786-6791.
44. Luecke, H. and Quiocho, F.A. 1990. High specificity of a phosphate transport protein determined by hydrogen bonds. Nature 347: 402-406.
45. Magota, K., Otsuji, N., Miki, T., Horiuchi, T.. Tsunasawa, S., Kondo, J., Sakiyama, F., Amemura, M., Morita, T., Shinagawa, H., et al. 1984. Nucleotide sequence of the phoS gene, the structural gene for the phosphate-binding protein of Escherichia coli. J. Bacteriol. 157: 909-917.
46. Martell, A.E. and Smith, R.M. 1977. Critical stability, constants. Plenum Press, New York.
47. Martin, J.H. 1992. Iron as a limiting factor. In Primary productivity and biogeochemical cycles in the sea (eds. P.G. Falkowski and A. Woodhead), pp. 123-137. Plenum Press, New York.
48. Marvin, J.S. and Hellinga, H.W. 1998. Engineering biosensors by introducing fluorescent allosteric signal transducers - construction of a novel glucose sensor. J. Am. Chem. Soc. 120: 7-11.
49. 2001a. Conversion of maltose-binding protein into a zinc biosensor by computational design. Proc. Natl. Acad. Sci. 98: 4955-4960.
50. 2001b. Manipulation of ligand binding affinity by exploitation of conformational coupling. Nat. Struct. Biol. 8: 795-798.
51. Marvin, J.S., Corcoran, E.E., Hattangadi, N.A., Zhang, J.V., Gere, S.A., and Hellinga, H.W. 1997. The rational design of allosteric interactions in a monomeric protein and its applications to the construction of biosensors. Proc. Natl. Acad. Sci. 94: 4366-4371.
52. Meadows, D. 1996. Recent developments with biosensing technology and applications in the pharmaceutical industry. Adv. Drug Deliv. Rev. 21: 177-189.
53. Medveczky, N. and Rosenberg. H. 1969. The binding and release of phosphate by a protein isolated from Escherichia coli. Biochim. Biophys. Acta 192: 369-371.
54. Miller III, D.M., Newcomer, M.E., and Quiocho, F.A. 1979. The thiol group of the L-arabinose-binding protein. Chromophoric labeling and chemical identification of the sugar-binding site. J. Biol. Chem. 254:7521-7528.
55. Miller III, D.M., Olson, J.S., Pflugrath, J.W.. and Quiocho. F.A. 1983. Rates of ligand binding to periplasmic proteins involved in bacterial transport and chemotaxis. J. Biol. Chem. 258: 13665-13672.
56. Mowbray, S.L. and Cole. L.B. 1992, 1.7 Å X-ray structure of the periplasmic ribose receptor from Escherichia coli. J. Mol. Biol. 225: 155-175.
57. Nelson, P.V., Carey, W.F., and Pollard, A.C. 1977. A micro-radiochemical assay for α-1,4-glucosidase and its use in the assessment of type II glycogenosis (Pompe's disease). Clin. Chim. Acta 77: 337-342.
58. Nickitenko, A.V., Trakhanov, S., and Quiocho, F.A. 1995. 2 Å resolution structure of DppA, a periplasmic dipeptide transport/chemosensory receptor. Biochemistry 34: 16585-16595.
59. Nohno, T., Saito, T., and Hong, J.S. 1986. Cloning and complete nucleotide sequence of the Escherichia coli glutamine permease operon (glnHPQ). Molec. Gen. Genet. 205: 260-269.
60. Oh, B.H., Kang, C.H., De, B.H., Kim, S.H., Nikaido, K.. Joshi, A.K., and Ames, G.F. 1994. The bacterial periplasmic histidine-binding protein. Structure/ function analysis of the ligand-binding site and comparison with related proteins. J. Biol. Chem. 269: 4135-4143.
61. Pellegrini, M., Marcotte, E.M., Thompson, M.J., Eisenberg, D., and Yeates, T.O. 1999. Assigning protein functions by comparative genome analysis: Protein phylogenetic profiles. Proc. Natl. Acad. Sci. 96: 4285-4288.
62. Pflugrath, J.W. and Quiocho, F.A. 1985. Sulphate sequestered in the sulphate-binding protein of Salmonella typhimurium is bound solely by hydrogen bonds. Nature 314: 257-260.
63. Quentin, Y., Fichant, G., and Denizot, F. 1999. Inventory, assembly and analysis of Bacillus subtilis ABC transport systems. J. Mol. Biol. 287: 467-484.
64. Quiocho, F.A. and Vyas, N.K. 1984. Novel stereos pecificity of the L-arabinose-binding protein. Nature 310: 381-386.
65. Quiocho, F.A. and Ledvina, P.S. 1996. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: Variation of common themes. Molec. Microbiol. 20: 17-25.
66. Quiocho, F.A., Spurlino, J.C., and Rodseth, L.E. 1997. Extensive features of tight oligosaccharide binding revealed in high-resolution structures of the maltodextrin transport/chemosensory receptor. Structure 5: 997-1015.
67. Rozaklis, T., Ramsay, S.L., Whitfield, P.D., Ranieri, E., Hopwood, J.J., and Meikle, P.J. 2002. Determination of oligosaccharides in Pompe disease by electrospray ionization tandem mass spectrometry. Clin. Chem. 48: 131-139.
68. Salins, L.L., Ware, R.A., Ensor, C.M., and Daunert, S. 2001. A novel reagentless sensing system for measuring glucose based on the galactose/glucose-binding protein. Anal. Biochem. 294: 19-26.
69. Sanders, J.D., Cope, L.D., and Hansen, E.J. 1994. Identification of a locus involved in the utilization of iron by Haemophilus influenzae. Infect. Immun. 62: 4515-4525.
70. Scheller, F.W., Wollenberger, U., Warsinke, A., and Lisdat, F. 2001. Research and development in biosensors. Curr. Opin. Biotech. 12: 35-40.
71. Scholle, A., Vreemann, J., Blank, V., Nold, A., Boos, W., and Manson, M.D. 1987. Sequence of the mglB gene from Escherichia coli K12: Comparison of wild-type and mutant galactose chemoreceptors. Mol. Gen. Genet. 208: 247-253.
72. Schwartz, M., Kellermann, O., Szmelcman, S., and Hazelbauer, G.L. 1976. Further studies on the binding of maltose to the maltose-binding protein of Escherichia coli. Eur. J. Biochem. 71: 167-170.
73. Scripture, J.B., Voelker, C., Miller, S., O'Donnell, R.T., Polgar, L., Rade, J., Horazdovsky, B.F., and Hogg, R.W. 1987. High-affinity L-arabinose transport operon. Nucleotide sequence and analysis of gene products. J. Mol. Biol. 197: 37-46.
74. Sharff, A.J., Rodseth, L.E., Spurlino, J.C., and Quiocho, F.A. 1992. Crystallographic evidence of a large ligand-induced hinge-twist motion between the two domains of the maltodextrin binding protein involved in active transport and chemotaxis. Biochemistry 31: 10657-10663.
75. Smith, M.W., Tyreman, D.R., Payne, G.M., Marshall, N.J., and Payne, J.W. 1999. Substrate specificity of the periplasmic dipeptide-binding protein from Escherichia coli: Experimental basis for the design of peptide prodrugs. Microbiology 145:2891-2901.
76. Smith, S.V. and Forman, D.T. 1994. Laboratory analysis of cerebrospinal fluid. Clin. Lab. Sci. 7: 32-38.
77. Spurlino, J.C., Lu, G.Y., and Quiocho, F.A. 1991. The 2.3-Å resolution structure of the maltose- or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis. J. Biol. Chem. 266: 5202-5219.
78. Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorff, J.W. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185: 60-89.
79. Sun, Y.-J., Rose, J., Wang, B.-C., and Hsiao, C.-D. 1998. The structure of glutamine-binding protein complexed with glutamine at 1.94 Å resolution: Comparisons with other amino acid binding proteins. J. Mol. Biol. 278: 219-229.
80. Tam, R. and Saier, Jr., M.H. 1993. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 57: 320-346.
81. Taylor, R.G., Levy, H.L., and McInnes, R.R. 1991. Histidase and histidinemia. Clinical and molecular considerations. Molec. Biol. Med. 8: 101-116.
82. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
83. Tolosa, L., Gryczynski, I., Eichhorn, L.R., Dattelbaum, J.D., Castellano, F.N., Rao, G., and Lakowicz, J.R. 1999. Glucose sensor for low-cost lifetime-based sensing using a genetically engineered protein. Anal. Biochem. 267: 114-120.
84. von Heijne, G. 1986. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14: 4683-4690.
85. Vyas, M.N., Vyas, N.K., and Quiocho, F.A. 1994. Crystallographic analysis of the epimeric and anomeric specificity of the periplasmic transport/chemosensory protein receptor for D-glucose and D-galactose. Biochemistry 33: 4762-4768.
86. Vyas, N.K., Vyas, M.N., and Quiocho, F.A. 1988. Sugar and signal-transducer binding sites of the Escherichia coli galactose chemoreceptor protein. Science 242: 1290-1295.
87. Weiner, J.H., Furlong, C.E., and Heppel, L.A. 1971. A binding protein for L-glutamine and its relation to active transport in E. coli. Arch. Biochem. Biophys. 142: 715-717.
88. Willis, R.C. and Furlong, C.E. 1974. Purification and properties of a ribose-binding protein from Escherichia coli. J. Biol. Chem. 249: 6926-6929.
89. 1975. Purification and properties of a periplasmic glutamate-aspartate binding protein from Escherichia coli K12 strain W3092. J. Biol. Chem. 250: 2574-2580.
90. Yao, N., Trakhanov, S., and Quiocho, F.A. 1994. Refined 1.89-Å structure of the histidine-binding protein complexed with histidine and its relationship with many other active transport/chemosensory proteins. Biochemistry 33:4769-4779.