Periplasmic Binding Proteins in Thermophiles: Characterization and Potential Application of an Arginine-Binding Protein from Thermotoga maritima: A Brief Thermo-Story
Arginine-binding protein from the extremophile Thermotoga maritima is a 27.7 kDa protein possessing the typical two-domain structure of the periplasmic binding proteins family. The protein is characterized by a very high specificity and affinity to bind to arginine, also at high temperatures. Due to its features, this protein could be taken into account as a potential candidate for the design of a biosensor for arginine. It is important to investigate the stability of proteins when they are used for biotechnological applications. In this article, we review the structural and functional features of an arginine-binding protein from the extremophile Thermotoga maritima with a particular eye on its potential biotechnological applications.
References
[1]
Higgins, C.F. ABC transporters: From microorganisms to man. Annu. Rev. Cell Biol.？1992, 8, 67–113, doi:10.1146/annurev.cb.08.110192.000435.
[2]
Jones, P.M.; George, A.M. The ABC transporter structure and mechanism: Perspectives on recent research. Cell Mol. Life Sci.？2004, 61, 682–699, doi:10.1007/s00018-003-3336-9.
[3]
Linton, K.J. Structure and function of ABC transporters. Physiology？2007, 22, 122–130, doi:10.1152/physiol.00046.2006.
[4]
Zolnerciks, J.K.; Andress, E.J.; Nicolaou, M.; Linton, K.J. Structure of ABC transporters. Essays Biochem.？2011, 50, 43–61, doi:10.1042/bse0500043.
[5]
Kos, V.; Ford, R.C. The ATP-binding cassette family: a structural perspective. Cell Mol. Life Sci.？2009, 66, 3111–3126, doi:10.1007/s00018-009-0064-9.
[6]
Davidson, A.L.; Dassa, E.; Orelle, C.; Chen, J. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev.？2008, 72, 317–364, doi:10.1128/MMBR.00031-07.
[7]
Rees, D.C.; Johnson, E.; Lewinson, O. ABC transporters: the power to change. Nat. Rev. Mol. Cell. Biol.？2009, 10, 218–227, doi:10.1038/nrm2646.
[8]
Oldham, M.L.; Davidson, A.L.; Chen, J. Structural insights into ABC transporter mechanism. Curr. Opin. Struct. Biol.？2008, 18, 726–733, doi:10.1016/j.sbi.2008.09.007.
[9]
Oldham, M.L.; Khare, D.; Quiocho, F.A.; Davidson, A.L.; Chen, J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature？2007, 450, 515–521, doi:10.1038/nature06264.
[10]
Gilson, E.; Alloing, G.; Schmidt, T.; Claverys, J.P.; Dudler, R.; Hofnung, M. Evidence for high affinity binding-protein dependent transport systems in gram-positive bacteria and in Mycoplasma. EMBO J.？1988, 7, 3971–3974. 3208757
[11]
Montesinos, M.L.; Herrero, A.; Flores, E. Amino acid transport in taxonomically diverse cyanobacteria and identification of two genes encoding elements of a neutral amino acid permease putatively involved in recapture of leaked hydrophobic amino acids. J. Bacteriol.？1997, 179, 853–862. 9006043
[12]
Quiocho, F.A.; Ledvina, P.S. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol. Microbiol.？1996, 20, 17–25, doi:10.1111/j.1365-2958.1996.tb02484.x.
[13]
Tam, R.; Saier, M.H., Jr. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bactera. Microbiol. Rev.？1993, 57, 320–346. 8336670
[14]
Dwyer, M.A.; Hellinga, H.W. Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr. Opin. Struct. Biol.？2004, 14, 495–504, doi:10.1016/j.sbi.2004.07.004.
[15]
Fukami-Kobayashi, K.; Tateno, Y.; Nishikawa, K. Domain dislocation: a change of core structure in periplasmic binding proteins in their evolutionary history. J. Mol. Biol.？1999, 286, 279–290, doi:10.1006/jmbi.1998.2454.
[16]
Lee, Y.H.; Dorwart, M.R.; Hazlett, K.R.; Deka, R.K.; Norgard, M.V.; Radolf, J.D.; Hasemann, C.A. The crystal structure of Zn(II)-free Treponema pallidum TroA, a periplasmic metal-binding protein, reveals a closed conformation. J. Bacteriol.？2002, 184, 2300–2304, doi:10.1128/JB.184.8.2300-2304.2002.
[17]
Karpowich, N.K.; Huang, H.H.; Smith, P.C.; Hunt, J.F. Crystal structures of the BtuF periplasmic-binding protein for vitamin B12 suggest a functionally important reduction in protein mobility upon ligand binding. J. Biol. Chem.？2003, 278, 8429–8434, doi:10.1074/jbc.M212239200. 12468528
[18]
Wissenbach, U.; Six, S.; Bongaerts, J.; Ternes, D.; Steinwachs, S.; Unden, G. A third periplasmic transport system for L-arginine in Escherichia coli: molecular characterization of the artPIQMJ genes, arginine binding and transport. Mol. Microbiol.？1995, 17, 675–686, doi:10.1111/j.1365-2958.1995.mmi_17040675.x. 8801422
[19]
Stamp, A.L.; Owen, P.; El Omari, K.; Lockyer, M.; Lamb, H.K.; Charles, I.G.; Hawkins, A.R.; Stammers, D.K. Crystallographic and microcalorimetric analyses reveal the structural basis for high arginine specificity in the Salmonella enterica serovar Typhimurium periplasmic binding protein STM4351. Proteins？2011, 79, 2352–2357, doi:10.1002/prot.23060.
[20]
Oh, B.H.; Pandit, J.; Kang, C.H.; Nikaido, K.; Gokcen, S.; Ames, G.F.; Kim, S.H. Three-dimensional structures of the periplasmic lysine/arginine/ornithine-binding protein with and without a ligand. J. Biol. Chem.？1993, 268, 11348–11355. 8496186
[21]
Celis, R.T.; Leadlay, P.F.; Roy, I.; Hansen, A. Phosphorylation of the periplasmic binding protein in two transport systems for arginine incorporation in Escherichia coli K-12 is unrelated to the function of the transport system. J. Bacteriol.？1998, 180, 4828–4833. 9733684
[22]
De Wolf, F.A.; Brett, G.M. Ligand-binding proteins: their potential for application in systems for controlled delivery and uptake of ligands. Pharmacol. Rev.？2000, 52, 207–236. 10835100
[23]
Jain-Ghai, S.; Nagamani, S.C.; Blaser, S.; Siriwardena, K.; Feigenbaum, A. Arginase I deficiency: severe infantile presentation with hyperammonemia: more common than reported? Mol. Genet. Metab.？2011, 104, 107–111, doi:10.1016/j.ymgme.2011.06.025.
[24]
Brusilov, S.W.; Horwich, A.L. Urea cycle enzymes. In The Metabolic Basis of Inherited Disease; Scriver, C.R., Beaudet, A.L., Sly, W.S., Valle, D., Eds.; McGraw-Hill: New York, NY, USA, 1989; pp. 629–663.
[25]
Rees, D.D.; Palmer, R.M.; Moncada, S. Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proc. Natl. Acad. Sci. USA？1989, 86, 3375–3378, doi:10.1073/pnas.86.9.3375.
[26]
Cooke, J.P. Does ADMA cause endothelial dysfunction? Arterioscler. Thromb. Vasc. Biol.？2000, 20, 2032–2037, doi:10.1161/01.ATV.20.9.2032.
[27]
Vallance, P.; Collier, J.; Moncada, S. Effects of endothelium-derived nitric oxide on peripheral arteriolar tone in man. Lancet？1989, 2, 997–1000. 2572793
[28]
Dattelbaum, J.D.; Lakowicz, J.R. Optical determination of glutamine using a genetically engineered protein. Anal. Biochem.？2001, 291, 89–95, doi:10.1006/abio.2001.4998.
[29]
Amiss, T.J.; Sherman, D.B.; Nycz, C.M.; Andaluz, S.A.; Pitner, J.B. Engineering and rapid selection of a low-affinity glucose/galactose-binding protein for a glucose biosensor. Protein Sci.？2007, 16, 2350–2359, doi:10.1110/ps.073119507.
[30]
Staiano, M.; Bazzicalupo, P.; Rossi, M.; D'Auria, S. Glucose biosensors as models for the development of advanced protein-based biosensors. Mol. Biosyst.？2005, 1, 354–362, doi:10.1039/b513385h.
[31]
Huber, R.; Langworthy, T.A.; K？nig, H.; Thomm, M.; Woese, C.R.; Sleytr, U.B.; Stetter, K.O. Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90 °C. Arch. Microbiol.？1986, 144, 324–333, doi:10.1007/BF00409880.
[32]
Nelson, K.E.; Clayton, R.A.; Gill, S.R.; Gwinn, M.L.; Dodson, R.J.; Haft, D.H.; Hickey, E.K.; Peterson, J.D.; Nelson, W.C.; Ketchum, K.A.; et al. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature？1999, 399, 323–329, doi:10.1038/20601.
[33]
Worning, P.; Jensen, L.J.; Nelson, K.E.; Brunak, S.; Ussery, D.W. Structural analysis of DNA sequence: evidence for lateral gene transfer in Thermotoga maritima. Nucleic Acids Res.？2000, 28, 706–709, doi:10.1093/nar/28.3.706.
[34]
Tian, Y.; Cuneo, M.J.; Changela, A.; Hocker, B.; Beese, L.S.; Hellinga, H.W. Structure-based design of robust glucose biosensors using a Thermotoga maritima periplasmic glucose-binding protein. Protein Sci.？2007, 16, 2240–2250, doi:10.1110/ps.072969407.
[35]
Fox, J.D.; Routzahn, K.M.; Bucher, M.H.; Waugh, D.S. Maltodextrin-binding proteins from diverse bacteria and archaea are potent solubility enhancers. FEBS Lett.？2003, 537, 53–57, doi:10.1016/S0014-5793(03)00070-X.
[36]
Nanavati, D.M.; Thirangoon, K.; Noll, K.M. Several archaeal homologs of putative oligopeptide-binding proteins encoded by Thermotoga maritima bind sugars. Appl Environ. Microbiol.？2006, 72, 1336–1345, doi:10.1128/AEM.72.2.1336-1345.2006.
[37]
Luchansky, M.S.; Der, B.S.; D'Auria, S.; Pocsfalvi, G.; Iozzino, L.; Marasco, D.; Dattelbaum, J.D. Amino acid transport in thermophiles: characterization of an arginine-binding protein in Thermotoga maritima. Mol. Biosyst.？2010, 6, 142–151, doi:10.1039/b908412f.
[38]
Sun, Y.J.; Rose, J.; Wang, B.C.; Hsiao, C.D. The structure of glutamine-binding protein complexed with glutamine at 1.94 A resolution: Comparisons with other amino acid binding proteins. J. Mol. Biol.？1998, 278, 219–229, doi:10.1006/jmbi.1998.1675.
[39]
Cuneo, M.J.; Changela, A.; Miklos, A.E.; Beese, L.S.; Krueger, J.K.; Hellinga, H.W. Structural analysis of a periplasmic binding protein in the tripartite ATP-independent transporter family reveals a tetrameric assembly that may have a role in ligand transport. J. Biol. Chem.？2008, 283, 32812–32820, doi:10.1074/jbc.M803595200. 18723845
[40]
Gonin, S.; Arnoux, P.; Pierru, B.; Lavergne, J.; Alonso, B.; Sabaty, M.; Pignol, D. Crystal structures of an Extracytoplasmic Solute Receptor from a TRAP transporter in its open and closed forms reveal a helix-swapped dimer requiring a cation for α-keto acid binding. BMC Struct. Biol.？2007, doi:10.1186/1472-6807-7-11.
[41]
Fang, Y.; Kolmakova-Partensky, L.; Miller, C. A bacterial arginine-agmatine exchange transporter involved in extreme acid resistance. J. Biol. Chem.？2007, 282, 176–182, doi:10.1074/jbc.M610075200. 17099215
[42]
Scire, A.; Marabotti, A.; Staiano, M.; Iozzino, L.; Luchansky, M.S.; Der, B.S.; Dattelbaum, J.D.; Tanfani, F.; D'Auria, S. Amino acid transport in thermophiles: characterization of an arginine-binding protein in Thermotoga maritima. 2. Molecular organization and structural stability. Mol. Biosyst.？2010, 6, 687–698, doi:10.1039/b922092e.
[43]
Vahedi-Faridi, A.; Eckey, V.; Scheffel, F.; Alings, C.; Landmesser, H.; Schneider, E.; Saenger, W. Crystal structures and mutational analysis of the arginine-, lysine-, histidine-binding protein ArtJ from Geobacillus stearothermophilus. Implications for interactions of ArtJ with its cognate ATP-binding cassette transporter, Art(MP)2. J. Mol. Biol.？2008, 375, 448–459, doi:10.1016/j.jmb.2007.10.049.
[44]
Hsiao, C.D.; Sun, Y.J.; Rose, J.; Wang, B.C. The crystal structure of glutamine-binding protein from Escherichia coli. J. Mol. Biol.？1996, 262, 225–242, doi:10.1006/jmbi.1996.0509.
[45]
Ausili, A.; Pennacchio, A.; Staiano, M.; Dattelbaum, J.D.; Fessas, D.; Schiraldi, A.; D'Auria, S. Amino acid transport in thermophiles: Characterization of an arginine-binding protein from Thermotoga maritima. 3. Conformational dynamics and stability. J. Photochem. Photobiol. B？2012. in press.
[46]
Ruggiero, A.; Dattelbaum, J.D.; Pennacchio, A.; Iozzino, L.; Staiano, M.; Luchansky, M.S.; Der, B.S.; Berisio, R.; D'Auria, S.; Vitagliano, L. Crystallization and preliminary X-ray crystallographic analysis of ligand-free and arginine-bound forms of Thermotoga maritima arginine-binding protein. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun.？2011, 67, 1462–1465, doi:10.1107/S1744309111037341.
