A proteomics strategy to discover β-glucosidases from Aspergillus fumigatus with two-dimensional page in-gel activity assay and tandem mass spectrometry

Journal of Proteome Research

Volumn 6, Issue 12, 2007, Pages 4749-4757

  Kim, Kee Hong ^a,b   Brown, Kimberly M ^a   Harris, Paul V ^a   Langston, James A ^a   Cherry, Joel R ^a  

^a Novozymes Biotech Inc   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

glucosidases; 2 dimensional electrophoresis; Aspergillus fumigatus; Fungus; In gel activity; Proteomics tool

Indexed keywords

ALCOHOL; BETA GLUCOSIDASE;

ARTICLE; ASPERGILLUS FUMIGATUS; ASPERGILLUS NIGER; ASPERGILLUS ORYZAE; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEIN SECRETION; PROTEOMICS; STAINING; TANDEM MASS SPECTROMETRY; THERMOSTABILITY;

AMINO ACID SEQUENCE; ASPERGILLUS FUMIGATUS; CELLULASES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MOLECULAR SEQUENCE DATA; PROTEOMICS; TANDEM MASS SPECTROMETRY;

ASPERGILLUS FUMIGATUS; ASPERGILLUS NIGER; ASPERGILLUS ORYZAE; FUNGI;

EID: 38049060254     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr070355i     Document Type: Article

References (55)

1. Duff, S. J. B.; Murray, W. D. Bioconversion of forest products industry waste cellulosics to fuel ethanol: a review. Bioresour. Technol. 1996, 55 (1), 1-33.
2. Galbe, M.; Zacchi, G. A review of the production of ethanol from softwood. Appl. Microbiol. Biotechnol. 2002, 59 (6), 618-628.
3. Ragauskas, A. J.; Williams, C. K.; Davison, B. H.; Britovsek, G.; Cairney, J.; Eckert, C. A.; Frederick, W. J.; Hallett, J. P.; Leak, D. J.; Liotta, C. L.; Mielenz, J. R.; Murphy, R.; Templer, R.; Tschaplinski, T. The path forward for biofuels and biomaterials. Science 2006, 311 (5760), 484-489.
4. Sternberg, D. β-Glucosidase of Trichoderma reesei: its biosynthesis and role in the saccharification of cellulose. Appl. Environ. Microbiol. 1976, 31, 648-654.
5. Nidetzky, B.; Steiner, W.; Hayn, M.; Claeyssens, M. Cellulose hydrolysis by the cellulases from Trichoderma reesei: a new model for synergistic interaction. Biochem. J. 1994, 298, 705-710.
6. Woodward, J. Synergism in cellulase systems. Bioresour. Technol. 1991, 36, 61-75.
7. Eriksson, T.; Karlsson, J.; Tjerneld, F. A model explaining declining rate in hydrolysis of lignocellulose substrates with cellobiohydrolase I (Cel7A) and endoglucanase I (Cel7B) of Trichoderma reesei. Appl. Biochem. Biotechnol. 2002, 101 (1), 41-60.
8. Kim, D. W.; Jeong, Y. K.; Jang, Y. H.; Lee, J. K. Purification and characterization of endoglucanase and exoglucanase components from trichoderma-viride. J. Ferment. Bioeng. 1994, 77 (4), 363-369.
9. Valjamae, P.; Pettersson, G.; Johansson, G. Mechanism of substrate inhibition in cellulose synergistic degradation. Eur. J. Biochem. 2001, 268, 4520-4526.
10. Medve, J.; Karlsson, J.; Lee, D.; Tjerneld, F. Hydrolysis of microcrystalline cellulose by cellobiohydrolase I and endoglucanase II from Trichoderma reesei: adsorption, sugar production pattern, and synergism of the enzymes. Biotechnol. Bioeng. 1998, 59, 621-634.
11. Medve, J.; Stahlberg, J.; Tjerneld, F. Adsorption and synergism of cellobiohydrolase-i and cellobiohydrolase-ii of trichoderma-reesei during hydrolysis of microcrystalline cellulose. Biotechnol. Bioeng. 1994, 44 (9), 1064-1073.
12. Wood, T. M.; McCrae, S. I. The cellulase of Trichoderma koningii. Purification and properties of some endoglucanase components with special reference to their action on cellulose when acting alone and in synergism with the cellobiohydrolase. Biochem. J. 1978, 171 (1), 61-72.
13. Sternberg, D.; Vijayakumar, P.; Reese, E. T. β-Glucosidase: microbial production and effect on enzymatic hydrolysis of cellulose. Can. J. Microbiol. 1977, 23, 139-147.
14. Kim, E.; Irwin, D. C.; Walker, L. P.; Wilson, D. B. Factorial optimization of a 6-cellulase mixture. Biotechnol. Bioeng. 1998, 58 (5), 494-501.
15. Aebersold, R.; Mann, M. Mass spectrometry-based proteomics. Nature 2003, 422 (6928), 198-207.
16. Gorg, A.; Weiss, W.; Dunn, M. J. Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004, 4 (12), 3665-3685.
17. Fey, S. J.; Nawrocki, A.; Larsen, M. R.; Gorg, A.; Roepstorff, P.; Skews, G. N.; Williams, R.; Larsen, P. M. Proteome analysis of Saccharomyces cerevisiae: a methodological outline. Electrophoresis 1997, 18 (8), 1361-1372.
18. Yates, J. R., 3rd; McCormack, A. L.; Link, A. J.; Schieltz, D.; Eng, J.; Hays, L. Future prospects for the analysis of complex biological systems using micro-column liquid chromatography-electrospray tandem mass spectrometry. Analyst 1996, 121 (7), 65R-76R.
19. McCormack, A. L.; Schieltz, D. M.; Goode, B.; Yang, S.; Barnes, G.; Drubin, D.; Yates, J. R., III. Direct analysis and identification of proteins in mixtures by LC/MS/MS and database searching at the low-femtomole level. Anal. Chem. 1997, 69 (4), 767-776.
20. Serrano, S. M.; Shannon, J. D.; Wang, D.; Camargo, A. C.; Fox, J. W. A multifaceted analysis of viperid snake venoms by two-dimensional gel electrophoresis: an approach to understanding venom proteomics. Proteomics 2005, 5 (2), 501-510.
21. Lee, K.; Kye, M.; Jang, J. S.; Lee, O. J.; Kim, T.; Lim, D. Proteomic analysis revealed a strong association of a high level of alpha1-antitrypsin in gastric juice with gastric cancer. Proteomics 2004, 4 (11), 3343-3352.
22. Choi, N. S.; Yoo, K. H.; Yoon, K. S.; Maeng, P. J.; Kim, S. H. Nanoscale proteomics approach using two-dimensional fibrin zymography combined with fluorescent SYPRO ruby dye. J. Biochem. Mol. Biol. 2004, 37 (3), 298-303.
23. Bok, R. A.; Hansell, E. J.; Nguyen, T. P.; Greenberg, N. M.; McKerrow, J. H.; Shuman, M. A. Patterns of protease production during prostate cancer progression: proteomic evidence for cascades in a transgenic model. Prostate Cancer Prostatic Dis. 2003, 6 (4), 272-280.
24. van Tilbeurgh, H.; Claeyssens, M.; De Bruyne, C. K. FEBS Lett. 1982, 149 (2), 152-156.
25. van Tilbeurgh, H.; Claeyssens, M. Detection and differentiation of cellulase components using low molecular mass fluorogenic substrates. FEBS Lett. 1985, 187 (2), 283-288.
26. Kyriacou, A.; MacKenzie, C. R.; Neufeld, R. J. Detection and characterization of the specific and nonspecific endoglucanases of Trichoderma reesei: evidence demonstrating endoglucanase activity by cellobiohydrolase II. Enzyme Microb. Technol. 1987, 9 (1), 25-32.
27. Mathew, R.; Rao, K. Activity staining of endoglucanases in Polyacrylamide gels. Anal. Biochem. 1992, 206, 50-52.
28. Loginova, L. G.; Tashpulatov, Z. h. Multicomponent cellulolytic enzymes of thermotolerant and mesophylic fungi related to Aspergillus fumigatus. Mikrobiologiia 1967, 36, 988-992.
29. Trivedi, L. S.; Rao, K. K. Cellulase induction in Aspergillus fumigatus M 216. Indian J. Exp. Biol. 1980, 18, 240-242.
30. Rudick, M. J.; Elbein, A. D. Glycoprotein enzymes secreted by Aspergillus fumigatus: purification and properties of a second beta-glucosidase. J. Bacteriol. 1975, 124, 534-541.
31. Rudick, M. J.; Elbein, A. D. Glycoprotein enzymes secreted by Aspergillus fumigatus. Purification and properties of β-glucosidase. J. Biol. Chem. 1973, 248, 6506-6513.
32. Stewart, J. C.; Parry, J. B. Factors influencing the production of cellulase by Aspergillus fumigatus (Fresenius). J. Gen. Microbiol. 1981, 125, 33-39.
33. Elbein, A. D.; Mitchell, M.; Molyneux, R. J. Effect of castanospermine on the structure and secretion of glycoprotein enzymes in Aspergillus fumigatus. J. Bacteriol. 1984, 160, 67-75.
34. Malone, J. P.; Radabaugh, M. R.; Leimgruber, R. M.; Gerstenecker, G. S. Practical aspects of fluorescent staining for proteomics applications. Electrophoresis 2001, 22, 919-932.
35. Hellman, U.; Wernstedt, C.; Gonez, J.; Heldin, C. H. Improvement of an "In-Gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 1995, 224 (1), 451-455.
36. Rosenfeld, J.; Capdevielle, J.; Guillemot, J. C.; Ferrara, P. In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 1992, 203 (1), 173-9.
37. Mackey, A. J.; Haystead, T. A. J.; Pearson, W. R. Getting more from less: algorithms for rapid protein identification with multiple short peptide sequences. Mol. Cell. Proteomics 2002, 1 (2), 139-147.
38. Harris, P. V.; Golightly, E. J. Polypeptides having beta-glucosidase activity and polynucleotides encoding same. United States Patent Application 20050214920 A1, 2005.
39. Lamsa, M.; Fidantsef, A.; Gorre-Clancy, B. New variant of a parent beta-glucosidase, having beta-glucosidase activity, useful in degrading or converting cellulose- and hemicellulose-containing biomass. PCT international patent WO20040992280-A2, 2004.
40. Himmel, M. E.; Adney, W. S.; Fox, J. W.; Mitchell, D. J.; Baker, J. O. Isolation and characterization of two forms of beta-D-glucosidase from Aspergillus niger. Appl. Biochem. Biotechnol. 1993, 39-40, 213-25.
41. Langston, J.; Sheehy, N.; Xu, F. Substrate specificity of Aspergillus oryzae family 3 β-glucosidase. Biochim. Biophys. Acta 2006, 1764, 972-978.
42. Graff, M. D.; Van Veen, I. C.; Van der Meulen-Muileman, I. H.; Gerritsen, W. R.; Pinedo, H. M.; Haisma, H. J. Cloning and characterization of human liver cytosolic β-glycosidase. Biochem. J. 2001, 356, 907-910.
43. McKeon, T. A. Activity stain for polygalacturonase. J. Chromatogr., A 1988, 455, 376-381.
44. Saloheimo, M.; Kuja-Panula, J.; Ylö smä ki, E.; Ward, M.; Penttilä, M. Enzymatic properties and intracellular localization of the novel Trichoderma reesei β-glucosidase BGLII (Cel1A). Appl. Environ. Microbiol. 2002, 68, 4546-4553.
45. Nierman, W. C.; Pain, A.; Anderson, M. J.; Wortman, J. R.; Kim, H. S.; Arroyo, J.; Berriman, M.; Abe, K.; Archer, D. B.; Bermejo, C.; Bennett, J.; Bowyer, P.; Chen, D.; Collins, M.; Coulsen, R.; Davies, R.; Dyer, P. S.; Farman, M.; Fedorova, N.; Fedorova, N.; Feldblyum, T. V.; Fischer, R., Fosker; N. ; Fraser, A.; Garcia, J. L.; Garcia, M. J.; Goble, A.; Goldman, G. H.; Gomi, K.; Griffith-Jones, S.; Gwilliam, R.; Haas, B.; Haas, H.; Harris, D.; Horiuchi, H.; Huang, J. Q.; Humphray, S.; Jimenez, J.; Keller, N.; Khouri, H.; Kitamoto, K.; Kobayashi, T.; Konzack, S.; Kulkarni, R.; Kumagai, T.; Lafon, A.; Latge, J. P.; Li, W. X.; Lord, A.; Lu, C.; Majores, W. H.; May, G. S.; Miller, B. L.; Mohamoud, Y.; Molina, M.; Monod, M.; Mouyna, I.; Mulligan, S.; Murphy, L.; O'Neil, S.; Paulsen, I.; Penalva, M. A.; Pertea, M.; Price, C.; Pritchard, B. L.; Quail, M. A.; Rabbinowitsch, E.; Rawlins, N.; Rajandream, M. A.; Reichard, U.; Renauld, H.; Robson, G. D.; de-Cordoba, S. R.; Rodriguez-Pena, J. M.; Ronning, C. M.; Rutter, S.; Salzberg, S. L.; Sanchez, M.; Sanchez-Ferrero, J. C.; Saunders, D.; Seeger, K.; Squares, R.; Squares, S.; Takeuchi, M.; Tekaia, F.; Turner, G.; de-Aldana, C. R. V.; Weidman, J.; White, O.; Woodward, J.; Yu, J. H.; Fraser, C.; Galagan, J. E.; Asai, K.; Machida, M.; Hall, N.; Barrell, B.; Denning, D. W. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005, 438, 1151-1156; erratum Nature 2006, 439 (7075), 502.
46. Bernard, K. R.; Jonscher, K. R.; Resing, K. A.; Ahn, N. G. Methods in functional proteomics: two-dimensional Polyacrylamide gel electrophoresis with immobilized pH gradients, in-gel digestion and identification of proteins by mass spectrometry. Methods Mol. Biol. 2004, 250, 263-282.
47. Lewis, T. S.; Hunt, J. B.; Aveline, L. D.; Jonscher, K. R.; Louie, D. F.; Yeh, J. M.; Nahreini, T. S.; Resing, K. A.; Ahn, N. G. Identification of novel MAP kinase pathway signaling targets by functional proteomics and mass spectrometry. Mol. Cell 2000, 6 (6), 1343-1454.
48. Kawaguchi, T.; Enoki, T.; Tsurumaki. ; Sumitani, J.-i.; Ueda, M.; Ooi, T.; Arai, M. Cloning and sequencing of the cDNA encoding β-glucosidase 1 from Aspergillus aculeatus. Gene 1996, 173 (2), 287-288.
49. Parry, N. J.; Beever, D. E.; Owen, E.; Vandenberghe, I.; Van Beeumen, J.; Bhat, M. K. Biochemical characterization and mechanism of action of a thermostable β-glucosidase purified from Thermoascus aurantiacus. Biochem. J. 2001, 353, 117-127.
50. Hou, W.-C.; Lin, Y.-H. Activity staining of pectinesterase on Polyacrylamide gels after acidic or sodium dodecyl sulfate electrophoresis. Electrophoresis 1998, 19, 692-694.
51. Park, S. G.; Kho, C. W.; Cho, S.; Lee, D. H.; Kim, S. H.; Park, B. C. A functional proteomic analysis of secreted enzymes from Bacillus subtilis 168 using a combined method of two-dimensional gel electrophoresis and zymography. Proteomics 2002, 2, 206-211.
52. Kaino, S.; Furui, T.; Hatano, S.; Kaino, M.; Okita, K.; Nakamura, K. Two-dimensional zymography for analysis of proteolytic enzymes in human pure pancreatic juice. Electrophoresis 1998, 19, 782-787.
53. Feinstein, R. N.; Howard, J. B.; Savol, R. Heat and urea stability of blood catalase of catalase-mutant mouse strains. Experientia 1971, 27 (10), 1152-3115.
54. Pearce, R. J. Heat stability in concentrated and non-concentrated milks - the effect of urea and beta-lactoglobulin levels and the influence of preheating. J. Dairy Res. 1979, 46 (2), 385-386.
55. Graves, P. R.; Kwiek, J. J.; Fadden, P.; Ray, R.; Hardeman, K.; Coley, A. M.; Foley, M.; Haystead, T. A. J. Discovery of novel targets of quinoline drugs in the human purine binding proteome. Mol. Pharmacol. 2002, 62 (6), 1364-1372.