A New Family of Intrinsically Disordered Proteins: Structural Characterization of the Major Phasin PhaF from Pseudomonas putida KT2440

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Maestro, Beatriz ^a   Galán, Beatriz ^b   Alfonso, Carlos ^b   Rivas, Germán ^b   Prieto, Maria A ^b   Sanz, Jesús M ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA; PHASIN; PROTEIN PHAF; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CIRCULAR DICHROISM; FLUORESCENCE SPECTROSCOPY; HYDRODYNAMICS; NONHUMAN; OLIGOMERIZATION; PREDICTION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PSEUDOMONAS PUTIDA; SPECTROSCOPY; THERMODYNAMICS; THERMOSTABILITY; ULTRACENTRIFUGATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA, BACTERIAL; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYHYDROXYALKANOATES; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING; PSEUDOMONAS PUTIDA; TEMPERATURE;

EID: 84874039779     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056904     Document Type: Article

References (69)

1. Findlay RH, White DC, (1983) Polymeric beta-hydroxyalkanoates from environmental samples and Bacillus megaterium. Appl Environ Microbiol 45: 71-78.
2. de Smet MJ, Eggink G, Witholt B, Kingma J, Wynberg H, (1983) Characterization of intracellular inclusion formed by Pseudomonas oleovorans during growth on octane. J Bacteriol 154: 870-878.
3. Steinbüchel A, Aerts K, Babel W, Follner C, Liebergesell M, et al. (1995) Considerations on the structure and biochemistry of bacterial polyhydroxyalkanoic acid inclusions. Can J Microbiol 41: 94-l05.
4. García B, Olivera ER, Miñambres B, Fernández-Valverde M, Cañedo LM, et al. (1999) Novel biodegradable aromatic plastics from a bacterial source. Genetic and biochemical studies on a route of the phenylacetyl-coA catabolon. J Biol Chem 274: 29228-29241.
5. Madison LL, Huisman GW, (1999) Metabolic engineering of poly(3-hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol Rev 63: 21-53.
6. Prieto MA, de Eugenio LI, Galán B, Luengo JM, Witholt B (2007) Synthesis and degradation of polyhydroxyalkanoates. In: Ramos JL, Filloux A, editors. Pseudomonas: a model system in biology. New York: Springer. pp. 397-428.
7. Pötter M, Steinbüchel A, (2005) Poly(3-hydroxybutyrate) granule-associated proteins: impacts on poly(3-hydroxybutyrate) synthesis and degradation. Biomacromolecules 6: 552-560.
8. Steinbüchel A, Füchstenbusch B, (1998) Bacterial and other biological systems for polyester production. Trends Biotechol 16: 419-427.
9. Zinn M, Witholt B, Egli T, (2001) Occurrence, synthesis and medical application of bacterial polyhydroxyalkanoate. Adv Drug Rev 55: 5-21.
10. Williams SF, Martin D (2002) Aplication of PHAs in medicine and pharmacy. In; Doi Y, Steinbüchel A, editors. Biopolymers, vol 4. Polyesters III: Applications and Commercial Products. Germany: Willey-VCH. pp 91-128.
11. Gao X, Chen J-C, Wu Q, Chen G-Q, (2010) Polyhydroxyalkanoates as a source of chemicals, polymers, and biofuels. Curr Op Biotechnol 22: 768-774.
12. Mayer F, Madkour MH, Pieper-Furst U, Wieczorek R, Liebergesell M, et al. (1996) Electron microscopic observation on the macromolecular organization of tha boundary layer of bacterial PHA inclusion bodies. J Gen Appl Microbiol 42: 445-455.
13. Wieczozorek R, Pries A, Steinbüchel A, Mayer F, (1995) Analysis of a 24-kilodalton protein associated with the polyhydroxyalkanoic acid granules in Alcaligenes eutrophus. J Bacteriol 177: 2425-2435.
14. McCool GJ, Cannon MC, (1999) Polyhydroxyalkanoate inclusion body-associated proteins and coding region in Bacillus megaterium. J Bacteriol 181: 585-592.
15. Pieper-Fürst U, Hussein Madkour M, Mayer F, Steinbüchel A, (1994) Purification and characterization of a 14-kilodalton protein that is bound to the surface of polyhidroxyalcanoic acid granules in Rhodococcus ruber. J Bacteriol 176: 4328-4337.
16. Maehara A, Ueda S, Nakano H, Yamane T, (1999) Analyses of a polyhydroxyalkanoic acid granule-associated 16-kilodalton protein and its putative regulator in the pha locus of Paracoccus denitrificans. J Bacteriol 181: 2914-2921.
17. Prieto MA, Bühler B, Jung K, Witholt B, Kessler B, (1999) PhaF, a polyhydroxyalkanoate-granule-associated protein of Pseudomonas oleovorans GPo1 involved in the regulatory expression system for pha genes. J Bacteriol 181: 858-868.
18. Galán B, Dijanksi N, Maestro B, de Eugenio LI, Escapa IF, et al. (2011) Nucleoid-associated PhaF phasin drives intracellular location and segregation of polyhydroxyalkanoate granules in Pseudomonas putida KT2442. Mol Microbiol 79: 402-418.
19. Sandoval A, Arias-Barrau E, Arcos M, Naharro G, Elías R, et al. (2007) Genetic and ultrastructural analysis of different mutants of Pseudomonas putida affected in the poly-3-hydroxy-n-alkanoate gene cluster. Environ Microbiol 9: 737-751.
20. Schembri MA, Woods AA, Bayly RC, Davies JK, (1995) Identification of a 13-kDa protein associated with the polyhydroxyalkanoic acid granules from Acinetobacter spp. FEMS Microbiol Lett 133: 277-283.
21. Jendrossek D, (2009) Polyhydroxyalkanoate granules are complex subcellular organelles (carbonosomes) J Bacteriol. 191: 3195-3202.
22. York GM, Junker BH, Stubbe J, Sinskey AJ, (2001) Accumulation of the PhaP phasin of Ralstonia eutropha is dependent on production of polyhydroxybutyrate in cells. J Bacteriol 183: 4217-4226.
23. York GM, Stubbe J, Sinskey AJ, (2002) The Ralstonia eutropha PhaR protein couples synthesis of the PhaP phasin to the presence of polyhydroxybutyrate in cells and promotes polyhydroxybutyrate production. J Bacteriol 184: 59-66.
24. Luengo JM, García B, Sandoval A, Naharro G, Olivera ER, (2003) Bioplastics from microorganisms. Curr Op Microbiol 6: 251-260.
25. Kuchta K, Chi L, Fuchs H, Pötter M, Steinbüchel A, (2007) Studies on the influence of phasins on accumulation and degradation of PHB and nanostructure of PHB granules in Ralstonia eutropha H16. Biomacromolecules 8: 657-662.
26. Qi Q, Steinbüchel A, Rehm BH, (2000) In vitro synthesis of poly(3-hydroxydecanoate): purication and enzymatic characterization of type II polyhydroxyalkanoate synthases PhaC1 and PhaC2 from Pseudomonas aeruginosa. Appl Microbiol Biotechnol 54: 37-43.
27. Moldes C, García P, García JL, Prieto MA, (2004) In vivo immobilization of fusion proteins on bioplastics by the novel tag BioF. Appl Environ Microbiol 70: 3205-3512.
28. Moldes C, Farinós GP, de Eugenio LI, García P, García JL, et al. (2006) New tool for spreading proteins to the environment: Cry1Ab toxin immobilized to bioplastics. Appl Microbiol Biotechnol 72: 88-93.
29. Rost B, Yachdav G, Liu J, (2004) The PredictProtein Server. Nucleic Acids Res 32 (Web Server issue) pp. W321-W326.
30. Cole C, Barber JD, Barton GJ, (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 35 (Web server issue) pp. W197-W201.
31. Guermeur Y, Geourjon C, Gallinari P, Deleage G, (1999) Improved performance in protein secondary structure prediction by inhomogeneous score combination. Bioinformatics 15: 413-421.
32. Lupas A, Van Dyke M, Stock J, (1991) Predicting coled coils from protein sequences. Science 252: 1162-1164.
33. Delorenzi M, Speed T, (2002) An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18: 617-625.
34. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
35. Medvedkin VN, Permyakov EA, Klimenko LV, Mitin YV, Matsushima N, et al. (1995) Interactions of (Ala*Ala*Lys*Pro)n and (Lys*Lys*Ser*Pro)n with DNA. Proposed coiled-coil structure of AlgR3 and AlgP from Pseudomonas aeruginosa. Protein Eng 8: 63-70.
36. Xue B, DunBrack RL, Williams RW, Dunker AK, Uversky VN, (2010) PONDR-Fit: A meta-predictor of intrinsically disordered amino acids. Biochim Biophys Acta 1804: 996-1010.
37. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT, (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337: 635-645.
38. Linding R, Jensen LJ, Diella F, Bork P, Gibson TJ, et al. (2003) Protein disorder prediction: implications for structural proteomics. Structure 11: 1453-1459.
39. Cheng J, Sweredoski M, Baldi P, (2005) Accurate prediction of protein disordered regions by mining protein structure data. Data mining and knowledge discovery 11: 213-222.
40. Schuck P, (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78: 1606-1619.
41. van Holde KE (1986) Sedimentation in physical biochemistry. In: Physical Biochemistry. Englewood Cliffs, NJ: Prentice Hall, Inc. pp.3-23.
42. Laue TM., Shah BD, Ridgeway TM, Pelletier SL (1992) Computer-aided interpretation of analytical sedimentation data for proteins. In: Harding S, Rowe A, Horton J, editors. Analytical Ultracentrifugation in Biochemistry and Polymer Science. Cambridge, UK: Royal Society of Chemistry. pp. 90-125.
43. Minton AP (1994) Conservation of signal: a new algorithm for the elimination of the reference concentration as an independently variable parameter in the analysis of sedimentation equilibrium. In: Schuster T, Laue T, editors. Modern Analytical Ultracentrifugation. Cambridge, MA: Birkhauser Boston, Inc. pp 81-93.
44. Provencher SW, Glöckner J, (1981) Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20: 33-37.
45. Johnson WC Jr, (1999) Analyzing protein circular dichroism spectra for accurate secondary structures. Proteins: Struct Funct Genet 35: 307-312.
46. Whitmore L, Wallace BA, (2004) DICHROWEB: an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Research 32 (Web server issue) pp. W668-W673.
47. Whitmore L, Wallace BA, (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89: 392-400.
48. Backmann J, Schäfer G, Wyns L, Bönisch H, (1998) Thermodynamics and kinetics of unfolding of the thermostable trimeric adenylate kinase from the archaeon Sulfolobus acidocaldarius. J Mol Biol 284: 817-833.
49. Greene RF Jr, Pace CN, (1974) Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, alpha-chymotrypsin, and beta-lactoglobulin. J Biol Chem 249: 5388-5393.
50. Woody RW, (1995) Circular Dichroism. Methods Enzymol 246: 34-71.
51. Wang Z, Wu H, Chen J, Zhang J, Yao Y, et al. (2008) A novel self-cleaving phasin tag for purification of recombinant proteins based on hydrophobic polyhydroxyalkanoate nanoparticles. Lab Chip 8: 1957-1962.
52. Sreerama N, Woody RW, (1994) Poly(Pro)-II helices in globular proteins: identification and circular dichroic analysis. Biochemistry 33: 10022-10025.
53. Buck M, (1998) Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q Rev Biophys 31: 297-355.
54. Lumry R, Eyring H, (1954) Conformation changes of proteins. J Phys Chem 58: 110-120.
55. Sánchez-Ruiz JM, López-Lacomba JL, Cortijo M, Mateo PL, (1988) Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin. Biochemistry 27: 1648-1652.
56. Freire E, van Osdol WW, Mayorga OL, Sánchez-Ruiz JM, (1990) Calorimetrically determined dynamics of complex unfolding transitions in proteins. Annu Rev Biophys Biophys Chem 19: 159-188.
57. Swint L, Robertson AD, (1993) Thermodynamics of unfolding for turkey ovomucoid third domain: Thermal and chemical denaturation. Protein Sci 2: 2037-2049.
58. Myers JK, Pace CN, Scholtz JM, (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci 4: 2138-2148.
59. Phelan P, Gorfe AA, Jelesarov I, Marti DN, Warwicker J, et al. (2002) Salt bridges destabilize a leucine zipper designed for maximized ion pairing between helices. Biochemistry 41: 2998-3008.
60. Dürr E, Jelesarov I, Bosshard HR, (1999) Extremely fast folding of a very stable leucine zipper with a strengthened hydrophobic core and lacking electrostatic interactions between helices. Biochemistry 38: 870-880.
61. Privalov PL, Tiktopulo EI, Venyaminov SYu, Griko YuV, Makhatadze GI, et al. (1989) Heat capacity and conformation of proteins in the denatured state. J Mol Biol 205: 737-750.
62. Uversky VN, (2011) Intrinsically disordered proteins from A to Z. Int J Biochem Cell Biol 43: 1090-1103.
63. Dunker AK, Brown CJ, Obradovic Z, (2002) Identification and functions of usefully disordered proteins. Adv Protein Chem 62: 25-49.
64. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z, (2002) Intrinsic disorder and protein function. Biochemistry 41: 6573-6582.
65. Peng Z, Mizianty MJ, Xue B, Kurgana L, Uversky VN, (2012) More than just tails: intrinsic disorder in histone proteins. Mol BioSyst 8: 1886-1901.
66. Feng S, Chen JK, Yu H, Simon JA, Schreiber SL, (1994) Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266: 1241-1247.
67. Lewitzky M, Harkiolaki M, Domart M-C, Jones EY, Feller SM, (2004) Mona/Gads SH3C binding to hematopoietic progenitor kinase 1 (HPK1) combines an atypical SH3 binding motif, R/KXXK, with a classical PXXP motif embedded in a polyproline type II (PPII) helix. J Biol Chem 279: 28724-28732.
68. Venturi V, Otten M, Korse V, Brouwer B, Leong J, et al. (1995) Alginate regulatory and biosynthetic gene homologs in Pseudomonas putida WCS358: correlation with the siderophore regulatory gene pfrA. Gene 155: 83-88.
69. Fairman R, Chao H-G, Lavoie TB, Villafranca JJ, Matsueda GR, et al. (1996) Design of heterotetrameric coiled coils: evidence for increased stabilization by Glu--Lys+ ion pair interactions. Biochemistry 35: 2824-2829.