Construction of a robust and sensitive arginine biosensor through ancestral protein reconstruction

Protein Science

Volumn 24, Issue 9, 2015, Pages 1412-1422

  Whitfield, Jason H ^a   Zhang, William H ^a   Herde, Michel K ^b   Clifton, Ben E ^a   Radziejewski, Johanna ^b   Janovjak, Harald ^c   Henneberger, Christian ^b,d   Jackson, Colin J ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF BONN   (Germany)

^c INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

ancestral protein reconstruction; biosensor; fluorescence; F rster resonance energy transfer (FRET); neurobiology; nitric oxide; protein engineering

Indexed keywords

ARGININE; BINDING PROTEIN; NITRIC OXIDE; BACTERIAL PROTEIN; FLUORESCENT DYE; PERIPLASMIC BINDING PROTEIN;

AMINO ACID SEQUENCE; ANCESTRAL PROTEIN RECONSTRUCTION; ANIMAL TISSUE; ARTICLE; BIOSENSOR; BRAIN FUNCTION; BRAIN TISSUE; CEREBROSPINAL FLUID; CONFORMATIONAL TRANSITION; CYTOLOGY; ENERGY TRANSFER; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; FORSTER RESONANCE ENERGY TRANSFER BIOSENSOR; HUMAN; LIMIT OF QUANTITATION; MAXIMUM LIKELIHOOD METHOD; MEASUREMENT ACCURACY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; RAT; SENSITIVITY AND SPECIFICITY; THERMOSTABILITY; TISSUE LEVEL; CHEMISTRY; COMPUTER SIMULATION; DEVICES; GENETIC PROCEDURES; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PROCEDURES; SIGNAL TRANSDUCTION;

ARGININE; BACTERIAL PROTEINS; BIOSENSING TECHNIQUES; COMPUTER SIMULATION; EVOLUTION, MOLECULAR; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; NITRIC OXIDE; OPTICAL IMAGING; PERIPLASMIC BINDING PROTEINS; PHYLOGENY; PROTEIN ENGINEERING; SIGNAL TRANSDUCTION;

EID: 84950150124     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2721     Document Type: Article

References (52)

1. Coruzzi G, Bush DR, (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125: 61-64.
2. Meijer AJ, Dubbelhuis PF, (2004) Amino acid signalling and the integration of metabolism. Biochem Biophys Res Commun 313: 397-403.
3. Gensert JM, Ratan RR, (2006) The metabolic coupling of arginine metabolism to nitric oxide generation by astrocytes. Antioxidants Redox Signal 8: 919-928.
4. Prast H, Philippu A, (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64: 51-68.
5. Miller M, Megson I, (2007) Recent developments in nitric oxide donor drugs. Br J Pharmacol 151: 305-321.
6. Molokanova E, Akhtar MW, Sanz-Blasco S, Tu S, Piña-Crespo JC, McKercher SR, Lipton SA, (2014) Differential effects of synaptic and extrasynaptic NMDA receptors on Aβ-induced nitric oxide production in cerebrocortical neurons. J Neurosci 34: 5023-5028.
7. Wang Q, Rowan MJ, Anwyl R, (2004) β-amyloid-mediated inhibition of NMDA receptor-dependent long-term potentiation induction involves activation of microglia and stimulation of inducible nitric oxide synthase and superoxide. J Neurosci 24: 6049-6056.
8. Deckel AW, (2001) Nitric oxide and nitric oxide synthase in Huntington's disease. J Neurosci Research 64: 99-107.
9. Rundfeldt C, Koch R, Richter A, Mevissen M, Gerecke U, Löscher W, (1995) Dose-dependent anticonvulsant and proconvulsant effects of nitric oxide synthase inhibitors on seizure threshold in a cortical stimulation model in rats. Eur J Pharmacol 274: 73-81.
10. Bode-Böger SM, Scalera F, Ignarro LJ, (2007) The L-arginine paradox: importance of the L-arginine/asymmetrical dimethylarginine ratio. Pharmacol Therapeut 114: 295-306.
11. Bosch OJ, Sartori SB, Singewald N, Neumann ID, (2007) Extracellular amino acid levels in the paraventricular nucleus and the central amygdala in high-and low-anxiety dams rats during maternal aggression: regulation by oxytocin. Research report. Stress 10: 261-270.
12. Silva E, Hernandez L, Contreras Q, Guerrero F, Alba G, (2000) Noxious stimulation increases glutamate and arginine in the periaqueductal gray matter in rats: a microdialysis study. Pain 87: 131-135.
13. Lallemand F, Ward RJ, Dravolina O, De Witte P, (2006) Nicotine-induced changes of glutamate and arginine in naive and chronically alcoholized rats: an in vivo microdialysis study. Brain Res 1111: 48-60.
14. Tarbit I, Perry E, Perry R, Blessed G, Tomlinson B, (1980) Hippocampal free amino acids in Alzheimer's disease. J Neurochem 35: 1246-1249.
15. Hires SA, Zhu Y, Tsien RY, (2008) Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters. Proc Natl Acad Sci USA 105: 4411-4416.
16. Okumoto S, Looger LL, Micheva KD, Reimer RJ, Smith SJ, Frommer WB, (2005) Detection of glutamate release from neurons by genetically encoded surface-displayed FRET nanosensors. Proc Natl Acad Sci USA 102: 8740-8745.
17. Dwyer MA, Hellinga HW, (2004) Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr Opin Struct Biol 14: 495-504.
18. Quiocho FA, Ledvina PS, (1996) Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol Microbiol 20: 17-25.
19. Namiki S, Sakamoto H, Iinuma S, Iino M, Hirose K, (2007) Optical glutamate sensor for spatiotemporal analysis of synaptic transmission. Eur J Neurosci 25: 2249-2259.
20. Okada S, Ota K, Ito T, (2009) Circular permutation of ligand-binding module improves dynamic range of genetically encoded FRET-based nanosensor. Protein Sci 18: 2518-2527.
21. Ruggiero A, Dattelbaum JD, Staiano M, Berisio R, D'Auria S, Vitagliano L, (2014) A loose domain swapping organization confers a remarkable stability to the dimeric structure of the arginine binding protein from Thermotoga maritima. Plos One 9: 11.
22. Kanemaru Y, Hasebe F, Tomita T, Kuzuyama T, Nishiyama M, (2013) Two ATP-binding cassette transporters involved in (S)-2-aminoethyl-cysteine uptake in Thermus thermophilus. J Bacteriology 195: 3845-3853.
23. Vahedi-Faridi A, Eckey V, Scheffel F, Alings C, Landmesser H, Schneider E, Saenger W, (2008) 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). J Mol Biol 375: 448-459.
24. Bogner M, Ludewig U, (2007) Visualization of arginine influx into plant cells using a specific FRET-sensor. J Fluor 17: 350-360.
25. Gaucher EA, Govindarajan S, Ganesh OK, (2008) Palaeotemperature trend for Precambrian life inferred from resurrected proteins. Nature 451: U702-U704.
26. Gaucher EA, Thomson JM, Burgan MF, Benner SA, (2003) Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins. Nature 425: 285-288.
27. Risso VA, Gavira JA, Mejia-Carmona DF, Gaucher EA, Sanchez-Ruiz JM, (2013) Hyperstability and substrate promiscuity in laboratory resurrections of precambrian beta-lactamases. J Am Chem Soc 135: 2899-2902.
28. Thornton JW, (2004) Resurrecting ancient genes: experimental analysis of extinct molecules. Nat Rev Genet 5: 366-375.
29. Williams PD, Pollock DD, Blackburne BP, Goldstein RA, (2006) Assessing the accuracy of ancestral protein reconstruction methods. PLoS Comput Biol 2: 598-605.
30. Felder CB, Graul RC, Lee AY, Merkle HP, Sadee W, (1999) The Venus flytrap of periplasmic binding proteins: an ancient protein module present in multiple drug receptors. AAPS PharmSci 1: E2.
31. Berntsson RPA, Smits SHJ, Schmitt L, Slotboom DJ, Poolman B, (2010) A structural classification of substrate-binding proteins. FEBS Lett 584: 2606-2617.
32. Greenfield NJ, (2006) Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat Protoc 1: 2527-2535.
33. Kreimer DI, Malak H, Lakowicz JR, Trakhanov S, Villar E, Shnyrov VL, (2000) Thermodynamics and dynamics of histidine-binding protein, the water-soluble receptor of histidine permease. Implications for the transport of high and low affinity ligands. Eur J Biochem 4252: 4242-4252.
34. Ausili A, Staiano M, Dattelbaum J, Varriale A, Capo A, D'Auria S, (2013) Periplasmic binding proteins in thermophiles: characterization and potential application of an arginine-binding protein from Thermotoga maritima: a brief thermo-story. Life 3: 149-160.
35. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
36. Armengou A, Hurtado O, Leira R, Obõn M, Pascual C, Moro MA, Lizasoain I, Castillo J, Dávalos A, (2003) l-Arginine levels in blood as a marker of nitric oxide-mediated brain damage in acute stroke: a clinical and experimental study. J Cereb Blood Flow Metab 23: 978-984.
37. Waldron TT, Murphy KP, (2003) Stabilization of proteins by ligand binding: application to drug screening and determination of unfolding energetics. Biochemistry 42: 5058-5064.
38. Okubo Y, Sekiya H, Namiki S, Sakamoto H, Iinuma S, Yamasaki M, Watanabe M, Hirose K, Iino M, (2010) Imaging extrasynaptic glutamate dynamics in the brain. Proc Natl Acad Sci USA 107: 6526-6531.
39. Hardingham N, Dachtler J, Fox K, (2013) The role of nitric oxide in pre-synaptic plasticity and homeostasis. Front Cell Neurosci 7: 1-19.
40. Lerma J, Herranz AS, Herreras O, Abraira V, Del R RM, (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384: 145-155.
41. Beernink PT, Yang YR, Graf R, King DS, Shah SS, Schachman HK, (2001) Random circular permutation leading to chain disruption within and near α helices in the catalytic chains of aspartate transcarbamoylase: effects on assembly, stability, and function. Protein Sci 10: 528-537.
42. Heinemann U, Hahn M, (1995) Circular permutation of polypeptide chains: implications for protein folding and stability. Prog Biophys Mol Biol 64: 121-143.
43. Semyanov A, Walker MC, Kullmann DM, (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6: 484-490.
44. Henneberger C, Papouin T, Oliet SH, Rusakov DA, (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463: 232-236.
45. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
46. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
47. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O, (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biol 59: 307-321.
48. Yang ZH, (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
49. Neylon C, Brown SE, Kralicek AV, Miles CS, Love CA, Dixon NE, (2000) Interaction of the Escherichia coli replication terminator protein (Tus) with DNA: a model derived from DNA-binding studies of mutant proteins by surface plasmon resonance. Biochemistry 39: 11989-11999.
50. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO, (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Meth 6: 343-345.
51. Engler C, Kandzia R, Marillonnet S, (2008) A one pot, one step, precision cloning method with high throughput capability. PLoS One 3: e3647.
52. Henneberger C, Rusakov DA, (2012) Monitoring local synaptic activity with astrocytic patch pipettes. Nat Protoc 7: 2171-2179.