High level production of the Magnaporthe grisea fructose 1,6-bisphosphate aldolase enzyme in Escherichia coli using a small volume bench-top fermentor

Protein Expression and Purification

Volumn 51, Issue 1, 2007, Pages 110-119

  Labbé, Geneviève ^a   Bezaire, Jeremy ^a   Groot, Sarah de ^a   How, Christine ^a   Rasmusson, Tim ^a   Yaeck, Jason ^a   Jervis, Eric ^a   Dmitrienko, Gary I ^a   Guy Guillemette, J ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Fed batch fermentation; Fructose 1,6 bisphosphate aldolase; Magnaporthe grisea; Recombinant enzymes; Zinc metalloenzyme

Indexed keywords

FRUCTOSE BISPHOSPHATE ALDOLASE; ZINC;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; BIOREACTOR; BIOSYNTHESIS; CHEMISTRY; DIMERIZATION; ENZYMOLOGY; ESCHERICHIA COLI; FERMENTATION; GENE EXPRESSION; KINETICS; MAGNAPORTHE; METABOLISM; METHODOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; MOLECULAR WEIGHT; PH; PROTEIN QUATERNARY STRUCTURE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BINDING SITES; BIOREACTORS; CLONING, MOLECULAR; DIMERIZATION; ESCHERICHIA COLI; FERMENTATION; FRUCTOSE-BISPHOSPHATE ALDOLASE; GENE EXPRESSION; HYDROGEN-ION CONCENTRATION; KINETICS; MAGNAPORTHE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PROTEIN STRUCTURE, QUATERNARY; SEQUENCE ALIGNMENT; ZINC;

ESCHERICHIA COLI; MAGNAPORTHE GRISEA;

EID: 33751400230     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2006.06.020     Document Type: Article

References (54)

1. Rutter W.J. Evolution of aldolase. Fed. Proc. 23 (1964) 1248-1257
2. Siebers B., Brinkmann H., Dorr C., Tjaden B., Lilie H., van der O.J., and Verhees C.H. Archaeal fructose-1,6-bisphosphate aldolases constitute a new family of archaeal type class I aldolase. J. Biol. Chem. 276 (2001) 28710-28718
3. Sanchez L., Horner D., Moore D., Henze K., Embley T., and Muller M. Fructose-1,6-bisphosphate aldolases in amitochondriate protists constitute a single protein subfamily with eubacterial relationships. Gene 295 (2002) 51-59
4. Kroth P.G., Schroers Y., and Kilian O. The peculiar distribution of class I and class II aldolases in diatoms and in red algae. Curr. Genet. (2005) 1-12
5. Sauve V., and Sygusch J. Molecular cloning, expression, purification, and characterization of fructose-1,6-bisphosphate aldolase from Thermus aquaticus. Protein Expr. Purif. 21 (2001) 293-302
6. Lewis D.J., and Lowe G. Phosphoglycollohydroxamic acid: an inhibitor of class I and II aldolases and triosephosphate isomerase. A potential antibacterial and antifungal agent. J.C.S. Chem. Commun. (1973) 713-715
7. Blom N.S., Tetreault S., Coulombe R., and Sygusch J. Novel active site in Escherichia coli fructose 1,6-bisphosphate aldolase. Nat. Struct. Biol. 3 (1996) 856-862
8. Giaever G., Chu A.M., Ni L., Connelly C., Riles L., Veronneau S., Dow S., Lucau-Danila A., Anderson K., Andre B., Arkin A.P., Astromoff A., El Bakkoury M., Bangham R., Benito R., Brachat S., Campanaro S., Curtiss M., Davis K., Deutschbauer A., Entian K.D., Flaherty P., Foury F., Garfinkel D.J., Gerstein M., Gotte D., Guldener U., Hegemann J.H., Hempel S., Herman Z., Jaramillo D.F., Kelly D.E., Kelly S.L., Kotter P., LaBonte D., Lamb D.C., Lan N., Liang H., Liao H., Liu L., Luo C., Lussier M., Mao R., Menard P., Ooi S.L., Revuelta J.L., Roberts C.J., Rose M., Ross-Macdonald P., Scherens B., Schimmack G., Shafer B., Shoemaker D.D., Sookhai-Mahadeo S., Storms R.K., Strathern J.N., Valle G., Voet M., Volckaert G., Wang C.Y., Ward T.R., Wilhelmy J., Winzeler E.A., Yang Y., Yen G., Youngman E., Yu K., Bussey H., Boeke J.D., Snyder M., Philippsen P., Davis R.W., and Johnston M. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418 (2002) 387-391
9. Gerdes S.Y., Scholle M.D., Campbell J.W., Balazsi G., Ravasz E., Daugherty M.D., Somera A.L., Kyrpides N.C., Anderson I., Gelfand M.S., Bhattacharya A., Kapatral V., D'Souza M., Baev M.V., Grechkin Y., Mseeh F., Fonstein M.Y., Overbeek R., Barabasi A.L., Oltvai Z.N., and Osterman A.L. Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J. Bacteriol. 185 (2003) 5673-5684
10. Kobayashi K., Ehrlich S.D., Albertini A., Amati G., Andersen K.K., Arnaud M., Asai K., Ashikaga S., Aymerich S., Bessieres P., Boland F., Brignell S.C., Bron S., Bunai K., Chapuis J., Christiansen L.C., Danchin A., Debarbouille M., Dervyn E., Deuerling E., Devine K., Devine S.K., Dreesen O., Errington J., Fillinger S., Foster S.J., Fujita Y., Galizzi A., Gardan R., Eschevins C., Fukushima T., Haga K., Harwood C.R., Hecker M., Hosoya D., Hullo M.F., Kakeshita H., Karamata D., Kasahara Y., Kawamura F., Koga K., Koski P., Kuwana R., Imamura D., Ishimaru M., Ishikawa S., Ishio I., Le Coq D., Masson A., Mauel C., Meima R., Mellado R.P., Moir A., Moriya S., Nagakawa E., Nanamiya H., Nakai S., Nygaard P., Ogura M., Ohanan T., O'Reilly M., O'Rourke M., Pragai Z., Pooley H.M., Rapoport G., Rawlins J.P., Rivas L.A., Rivolta C., Sadaie A., Sadaie Y., Sarvas M., Sato T., Saxild H.H., Scanlan E., Schumann W., Seegers J.F.M.L., Sekiguchi J., Sekowska A., Seror S.J., Simon M., Stragier P., Studer R., Takamatsu H., Tanaka T., Takeuchi M., Thomaides H.B., Vagner V., van Dijl J.M., Watabe K., Wipat A., Yamamoto H., Yamamoto M., Yamamoto Y., Yamane K., Yata K., Yoshida K., Yoshikawa H., Zuber U., and Ogasawara N. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100 (2003) 4678-4683
11. Wehmeier U.F. Molecular cloning, nucleotide sequence and structural analysis of the Streptomyces galbus DSM40480 fda gene: the S. galbus fructose-1,6-bisphosphate aldolase is a member of the class II aldolases. FEMS Microbiol. Lett. 197 (2001) 53-58
12. Marino M., Hoffmann T., Schmid R., Mobitz H., and Jahn D. Changes in protein synthesis during the adaptation of Bacillus subtilis to anaerobic growth conditions. Microbiology 146 (2000) 97-105
13. Schmid R., Uhlemann E.M., Nolden L., Wersch G., Hecker R., Hermann T., Marx A., and Burkovski A. Response to nitrogen starvation in Corynebacterium glutamicum. FEMS Microbiol. Lett. 187 (2000) 83-88
14. Wilkins J.C., Homer K.A., and Beighton D. Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions. Appl. Environ. Microbiol. 68 (2002) 2382-2390
15. Rosenkrands I., Slayden R.A., Crawford J., Aagaard C., Barry B.E., and Andersen P. Hypoxic response of Mycobacterium tuberculosis studied by metabolic labeling and proteome analysis of cellular and extracellular proteins. J. Bacteriol. 184 (2002) 3485-3491
16. Tomas C.A., Beamish J., and Papoutsakis E.T. Transcriptional analysis of butanol stress and tolerance in Clostridium acetobutylicum. J. Bacteriol. 186 (2004) 2006-2018
17. Jakobsen O.M., Benichou A., Flickinger M.C., Valla S., Ellingsen T.E., and Brautaset T. Upregulated transcription of plasmid and chromosomal ribulose monophosphate pathway genes is critical for methanol assimilation rate and methanol tolerance in the methylotrophic bacterium Bacillus methanolicus. J. Bacteriol. 188 (2006) 3063-3072
18. Soanes D.M., Skinner W., Keon J., Hargreaves J., and Talbot N.J. Genomics of phytopathogenic fungi and the development of bioinformatic resources. Mol. Plant Microbe Interact. 15 (2002) 421-427
19. Ebbole D.J., Jin Y., Thon M., Pan H.Q., Bhattarai E., Thomas T., and Dean R. Gene discovery and gene expression in the rice blast fungus, Magnaporthe grisea: analysis of expressed sequence tags. Mol. Plant Microbe Interact. 17 (2004) 1337-1347
20. Dean R.A., Talbot N.J., Ebbole D.J., Farman M.L., Mitchell T.K., Orbach M.J., Thon M., Kulkarni R., Xu J.R., Pan H.Q., Read N.D., Lee Y.H., Carbone I., Brown D., Oh Y.Y., Donofrio N., Jeong J.S., Soanes D.M., Djonovic S., Kolomiets E., Rehmeyer C., Li W.X., Harding M., Kim S., Lebrun M.H., Bohnert H., Coughlan S., Butler J., Calvo S., Ma L.J., Nicol R., Purcell S., Nusbaum C., Galagan J.E., and Birren B.W. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434 (2005) 980-986
21. Henderson I., Garcia-Junceda E., Liu K.K., Chen Y.L., Shen G.J., and Wong C.H. Cloning, overexpression and isolation of the type II FDP aldolase from E. coli for specificity study and synthetic application. Bioorg. Med. Chem. 2 (1994) 837-843
22. Hu S.Y., Wu J.L., and Huang J.H. Production of tilapia insulin-like growth factor-2 in high cell density cultures of recombinant Escherichia coli. J. Biotechnol. 107 (2004) 161-171
23. Lee S.Y. High cell-density culture of Escherichia coli. Trends Biotechnol. 14 (1996) 98-105
24. Chen W., Graham C., and Ciccarelli R.B. Automated fed-batch fermentation with feed-back controls based on dissolved oxygen (DO) and pH for production of DNA vaccines. J. Ind. Microbiol. Biotechnol. 18 (1997) 43-48
25. Oh G., Moo-Young M., and Chisti Y. Automated fed-batch culture of recombinant Saccharomyces cerevisiae based on on-line monitored maximum substrate uptake rate. Biochem. Eng. J. 1 (1998) 211-217
26. Ramsaywak P.C., Labbe G., Siemann S., Dmitrienko G.I., and Guillemette J.G. Molecular cloning, expression, purification, and characterization of fructose 1,6-bisphosphate aldolase from Mycobacterium tuberculosis-a novel Class II A tetramer. Protein Expr. Purif. 37 (2004) 220-228
27. Tabor S., and Richardson C.C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA 82 (1985) 1074-1078
28. Berry A., and Marshall K.E. Identification of zinc-binding ligands in the class II fructose-1,6-bisphosphate aldolase of Escherichia coli. FEBS Lett. 318 (1993) 11-16
29. Laemmli U.K. Cleavage of structural proteins during assembly of head of bacteriophage T4. Nature 227 (1970) 680-685
30. Bradford M.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
31. Cornish-Bowden A. Analysis of Enzyme Kinetic Data (1995), Oxford University Press, Oxford, UK
32. Onishi H. In: Winefordner J.D., and Kolthoff I.M. (Eds). Chemical Analysis 3IIB (1989), Wiley, New York
33. Siemann S., Brewer D., Clarke A.J., Dmitrienko G.I., Lajoie G., and Viswanatha T. IMP-1 metallo-beta-lactamase: effect of chelators and assessment of metal requirement by electrospray mass spectrometry. Biochim. Biophys. Acta 1571 (2002) 190-200
34. Balbas P. Understanding the art of producing protein and nonprotein molecules in Escherichia coli. Mol. Biotechnol. 19 (2001) 251-267
35. Han K., Lim H., and Hong J. Acetic acid formation in E. coli fermentations. Biotechnol. Bioeng. 39 (1992) 663-671
36. Hall D.R., Leonard G.A., Reed C.D., Watt C.I., Berry A., and Hunter W.N. The crystal structure of Escherichia coli class II fructose-1, 6-bisphosphate aldolase in complex with phosphoglycolohydroxamate reveals details of mechanism and specificity. J. Mol. Biol. 287 (1999) 383-394
37. Harris C.E., Kobes R.D., Teller D.C., and Rutter W.J. The molecular characteristics of yeast aldolase. Biochemistry 8 (1969) 2442-2454
38. Scamuffa M.D., and Caprioli R.M. Comparison of the mechanisms of two distinct aldolases from Escherichia coli grown on gluconeogenic substrates. Biochim. Biophys. Acta 614 (1980) 583-590
39. Belasco J.G., and Knowles J.R. Polarization of substrate carbonyl groups by yeast aldolase: investigation by Fourier transform infrared spectroscopy. Biochemistry 22 (1983) 122-129
40. Pelzer-Reith B., Wiegand S., and Schnarrenberger C. Plastid class I and cytosol class II aldolase of Euglena gracilis (Purification and characterization). Plant Physiol. 106 (1994) 1137-1144
41. Zgiby S.M., Thomson G.J., Qamar S., and Berry A. Exploring substrate binding and discrimination in fructose 1,6-bisphosphate and tagatose 1,6-bisphosphate aldolases. Eur. J. Biochem. 267 (2000) 1858-1868
42. Schwede T., Kopp J., Guex N., and Peitsch M.C. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31 (2003) 3381-3385
43. Izard T., and Sygusch J. Induced fit movements and metal cofactor selectivity of class II aldolases: structure of Thermus aquaticus fructose-1,6-bisphosphate aldolase. J. Biol. Chem. 279 (2004) 11825-11833
44. Babul J., Clifton D., Kretschmer M., and Fraenkel D.G. Glucose metabolism in Escherichia coli and the effect of increased amount of aldolase. Biochemistry 32 (1993) 4685-4692
45. Boles E., and Zimmermann F.K. Saccharomyces cerevisiae phosphoglucose isomerase and fructose bisphosphate aldolase can be replaced functionally by the corresponding enzymes of Escherichia coli and Drosophila melanogaster. Curr. Genet. 23 (1993) 187-191
46. Rogers M., and Keeling P.J. Lateral transfer and recompartmentalization of Calvin cycle enzymes of plants and algae. J. Mol. Evol. 58 (2004) 367-375
47. Marsh J.J., and Lebherz H.G. Fructose-bisphosphate aldolases: an evolutionary history. Trends Biochem. 17 (1992) 110-113
48. Fernandez-Arenas E., Molero G., Nombela C., Diez-Orejas R., and Gil C. Contribution of the antibodies response induced by a low virulent Candida albicans strain in protection against systemic candidiasis. Proteomics 4 (2004) 1204-1215
49. Fernandez-Arenas E., Molero G., Nombela C., Diez-Orejas R., and Gil C. Low virulent strains of Candida albicans: unravelling the antigens for a future vaccine. Proteomics 4 (2004) 3007-3020
50. da Fonseca C.A., Jesuino R.S., Felipe M.S., Cunha D.A., Brito W.A., and Soares C.M. Two-dimensional electrophoresis and characterization of antigens from Paracoccidioides brasiliensis. Microbes Infect. 3 (2001) 535-542
51. Carneiro L.C., de Faria F.P., Felipe M.S., Pereira M., and Almeida Soares C.M. Paracoccidioides brasiliensis presents two different cDNAs encoding homologues of the fructose 1,6-biphosphate aldolase: protein isolation, cloning of the cDNAs and genes, structural, phylogenetic, and expression analysis. Fungal Genet. Biol. 42 (2005) 51-60
52. Yano A., Suzuki K., Uchimiya H., and Shinshi H. Induction of hypersensitive cell death by a fungal protein in cultures of tobacco cells. Mol. Plant Microbe Interact. 11 (1998) 115-123
53. Peng J.-L., Dong H.-S., Dong H.-P., Delaney T.P., Bonasera J.M., and Beer S.V. Harpin-elicited hypersensitive cell death and pathogen resistance requires the NDR1 and EDS1 genes. Physiol. Mol. Plant Pathol. 62 (2003) 317-326
54. Zhang H.K., Zhang X., Mao B.Z., Li Q., and He Z.H. Alpha-picolinic acid, a fungal toxin and mammal apoptosis-inducing agent, elicits hypersensitive-like response and enhances disease resistance in rice. Cell Res. 14 (2004) 27-33