Gene overexpression and biochemical characterization of the biotechnologically relevant chlorogenic acid hydrolase from Aspergillus niger

Applied and Environmental Microbiology

Volumn 73, Issue 17, 2007, Pages 5624-5632

  Benoit, Isabelle ^a   Asther, Michèle ^a   Bourne, Yves ^b   Navarro, David ^a   Canaan, Stéphane ^c   Lesage Meessen, Laurence ^a   Herweijer, Marga ^d   Coutinho, Pedro M ^b   Asther, Marcel ^a   Record, Eric ^a  

^a Centre International de Ressources Microbiennes Champignons Filamenteux   (France)

^b Centre National de la Recherche Scientifique   (France)

^c Centre National de la Recherche Scientifique   (France)

^d DSM FOOD SPECIALTIES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ASPERGILLUS NIGER; BIOCHEMICAL CHARACTERIZATION; CAFFEIC ACID; CHLOROGENIC ACID HYDROLASE;

AMINO ACIDS; CATALYSIS; CLONING; GENE EXPRESSION; GLYCOSYLATION; MASS SPECTROMETRY; THERMODYNAMIC STABILITY;

YEAST;

ACID HYDROLASE; AMINO ACID; CAFFEIC ACID; CHLOROGENIC ACID; CHLOROGENIC ACID HYDROLASE; HISTIDINE; UNCLASSIFIED DRUG;

AMINO ACID; BIOTECHNOLOGY; CHROMATOGRAPHY; COFFEE; ENZYME; FUNGUS; GENE EXPRESSION; PH; POLYMERASE CHAIN REACTION; PROTEIN; TEMPERATURE EFFECT;

APPLE; ARTICLE; ASPERGILLUS NIGER; CATALYSIS; COFFEE; ENZYME ANALYSIS; ENZYME STABILITY; GENE OVEREXPRESSION; GENOME; GLYCOSYLATION; MASS SPECTROMETRY; MOLECULAR CLONING; MOLECULAR SIZE; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; POLYMERASE CHAIN REACTION; THERMOSTABILITY;

AMINO ACID SEQUENCE; ASPERGILLUS NIGER; BIOTECHNOLOGY; CHLOROGENIC ACID; CLONING, MOLECULAR; FUNGAL PROTEINS; HYDROLASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; TRANSFORMATION, GENETIC; UP-REGULATION;

ASPERGILLUS NIGER; MALUS X DOMESTICA;

EID: 34548508191     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00374-07     Document Type: Article

References (46)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Asther, M., M. I. Estrada Alvarado, M. Haon, D. Navarro, M. Asther, L. Lesage-Meessen, and E. Record. 2005. Purification and characterization of a chlorogenic acid hydrolase from Aspergillus niger catalysing the hydrolysis of chlorogenic acid. J. Biotechnol. 115:47-56.
3. Barbe, C., and D. Dubourdieu. 1998. Characterization and purification of a cinnamate esterase from Aspergillus niger industrial pectinase preparation. J. Sci. Food Agric. 78:471-478.
4. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
5. Benoit, I., M. Asther, G. Sulzenbacher, E. Record, L. Marmuse, G. Parsiegla, I. Gimbert, M. Asther, and C. Bignon. 2006. Respective importance of protein folding and glycosylation in the thermal stability of recombinant feruloyl esterase. FEBS Lett. 580:5815-5821.
6. Benoit, I., D. Navarro, N. Marnet, N. Rakotomanomana, L. Lesage-Meessen, J.-C. Sigoillot, M. Asther, and M. Asther. 2006. Feruloyl esterase as a tool for the release of phenolic compounds from agro-industrial by-products. Carbohydr. Res. 341:1820-1827.
7. Bourne, Y., A. A. Hasper, H. Chahinian, M. Juin, L. H. de Graaff, and P. Marchot. 2004. Aspergillus niger protein EstA defines a new class of fungal esterases within the alpha/beta hydrolase fold superfamily of proteins. Structure 12:677-687.
8. Chahinian, H., L. Nini, E. Boitard, J. P. Dubes, L. Sarda, and L. C. Comeau. 2000. Kinetic properties of Penicillium cyclopium lipases studied with vinyl esters. Lipids 35:919-925.
9. Chen, J. H., and C. T. Ho. 1997. Antioxidant activities of caffeic acid and its related hydroxycinnamic acid compounds. J. Agric. Food Chem. 45:2374-2378.
10. Chu, F. K., R. B. Trimble, and F. Maley. 1978. The effect of carbohydrate depletion on the properties of yeast external invcrtase. J. Biol. Chem. 253: 8691-8693.
11. Clifford, M. N. 1999. Chlorogenic acids and other cinnamates - nature, occurrence and dietary burden. J. Sci. Food Agric. 79:362-372.
12. Clifford, M. N. 2000. Chlorogenic acids and other cinnamates - nature, occurrence, dietary burden, absorption and metabolism. J. Sci. Food Agric. 80:1033-1043.
13. Colquhoun, I. J., M.-C. Ralet, J.-F. Thibault, C. B. Faulds, and G. Williamson. 1994. Structure identification of feruloylated oligosaccharides from sugar-beet pulp by NMR spectroscopy. Carbohydr. Res. 263:243-256.
14. Conesa, A., P. J. Punt, N. van Luijk, and C. A. van den Hondel. 2001. The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genet. Biol. 33:155-171.
15. Couteau, D., A. L. McCartney, G. R. Gibson, G. Williamson, and C. B. Faulds. 2001. Isolation and characterization of human bacteria able to hydrolyse chlorogenic acid. J. Appl. Microbiol. 90:873-881.
16. Crepin, V. F., C. B. Faulds, and I. F. Connerton. 2004. Functional classification of the microbial feruloyl esterases. Appl. Microbiol. Biotechnol. 63: 647-652.
17. Crepin, V. F., C. B. Faulds, and I. F. Connerton. 2003. A non-modular type B feruloyl esterase from Neurospora crassa exhibits concentration-dependent substrate inhibition. Biochem. J. 370:417-427.
18. de Vries, R. P., B. Michelsen, C. H. Poulsen, P. A. Kroon, R. H. H. van den Heuvel, C. B. Faulds, G. Williamson, J. P. T. W. van den Homberg, and J. Visser. 1997. The faeA genes from Aspergillus niger and Aspergillus tubingensis encode ferulic acid esterases involved in degradation of complex cell wall polysaccharides. Appl. Environ. Microbiol. 63:4638-4644.
19. de Vries, R. P., P. A. VanKuyk, H. C. M. Kester, and J. Visser. 2002. The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds. Biochem. J. 363:377-386.
20. Faulds, C. B., and G. Williamson. 1994. Purification and characterization of a ferulic acid esterase (FAE-III) from Aspergillus niger specificity for the phenolic moiety and binding to microcrystalline cellulose. Microbiology 140: 779-787.
21. Garcia, R., J. A. Cremata, O. Quintero, R. Montesino, K. Benkestock, and J. Stahlberg. 2001. Characterization of protein glycoforms with N-linked neutral and phosphoryiated oligosaccharides: studies on the glycosylation of endoglucanase 1 (Cc17B) from Trichodenna recsei. Biotechnol. Appl. Biochem. 33:141-152.
22. Hata, Y., K. Tsuchiya, K. Kitamoto, K. Gomi, C. Kumagai, G. Tamura, and S. Hara. 1991. Nucleotide sequence and expression of the glucoamylase-encoding gene (glaA) horn Aspergillus oryzae. Gene 108:145-150.
23. Juge, N., G. Williamson, A. Puigserver, N. J. Cummings, I. F. Connerton, and C. B. Faulds. 2001. High-level production of recombinant Aspergillus niger cinnamoyl esterase (FAEA) in the methylotrophic yeast Pichia pastoris. FEMS Yeast Res. 1:127-132.
24. Kroon, P. A., C. B. Faulds, and G. Williamson. 1996. Purification and characterization of a novel esterase induced by growth of Aspergillus niger on sugar-beet pulp. Biotechnol. Appl. Biochem. 23:255-262.
25. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Levasseur, A., I. Benoit, M. Asther, M. Asther, and E. Record. 2004. Homologous expression of the feruloyl esterase B gene from Aspergillus niger and characterization of the recombinant enzyme. Protein Expr. Purif. 37: 126-133.
27. Mateos, R., L. Goya, and L. Bravo. 2006. Uptake and metabolism of hydroxycinnamic acids (chlorogenic, caffeic, ferulic acids) by HepG2 cells as a model of the human liver. J. Agric. Food Chem. 54:8724-8732.
28. Okamura, S., and M. Watanabe. 1982. Purification and properties of hydroxycinnamic ester hydrolase from Aspergillus japonicus. Agric. Biol. Chem. 46:1839-1848.
29. Pel, H. J., J. H. de Winde, D. B. Archer, P. S. Dyer, G. Hofmann, P. J. Schaap, G. Turner, R. P. de Vries, R. Albang, K. Albermann, M. R. Andersen, J. D. Bendtsen, J. A. E. Benen, M. van den Berg, S. Breestraat, M. X. Caddick, R. Contreras, M. Cornell, P. M. Coutinho, E. G. J. Danchin, A. J. M. Debets, P. Dekker, P. W. M. van Dijck, A. van Dijk, L. Dijkhuizen, A. J. M. Driessen, C. d'Enfert, S. Geysens, C. Goosen, G. S. P. Groot, P. W. J. de Groot, T. Guillemette, B. Henrissat, M. Herweijer, J. P. T. W. van den Hombergh, C. A. M. J. J. van den Hondel, R. T. J. M. van der Heijden, R. M. van der Kaaij, F. M. Klis, H. J. Kools, C. P. Kubicek, P. A. van Kuyk, J. Lauber, X. Lu, M. J. E. C. van der Maarel, R. Meulenberg, H. Menke, A. M. Mortimer, J. Nielsen, S. G. Oliver, M. Olsthoorn, K. Pal, N. N. M. E. van Peij, A. F. J. Ram, U. Rinas, J. A. Roubos, C. M. J. Sagt, M. Schmoll, J. Sun, D. Ussery, J. Varga, W. Vervecken, P. J. I. van de Vondervoort, H. Wedler, H. A. B. Wösten, A.-P. Zeng, A. J. J. van Ooyen, J. Visser, and H. Stam. 2007. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat. Biotechnol. 25:221-231.
30. Punt, P. J., M. A. Dingemanse, B. J. M. Jacobs-Meijsing, P. H. Pouwels, and C. A. M. J. J. van den Hondel. 1988. Isolation and characterization of the glyceraldehyde-3-phosphate dehydrogenase gene of Aspergillus nidulans. Gene 69:49-57.
31. Punt, P. J., N. van Biezen, A. Conesa, A. Albers, J. Mangnus, and C. van den Hondel. 2002. Filamentous fungi as cell factories for heterologous protein production. Trends Biotechnol. 20:200-206.
32. Punt, P. J., and C. A. van den Hondel. 1992. Transformation of filamentous fungi based on hygromycin B and phleomycin resistance markers. Methods Enzymol. 216:447-457.
33. Punt, P. J., I. A. van Gemeren, J. Drint-Kuijvenhoven, J. G. Hessing, G. M. van Muijlwijk-Harteveld, A. Beijersbergen, C. T. Verrips, and C. A. van den Hondel. 1998. Analysis of the role of the gene bipA, encoding the major endoplasmic reticulum chaperone protein in the secretion of homologous and heterologous proteins in black Aspergilli. Appl. Microbiol. Biotechnol. 50:447-454.
34. Ralet, M. C., C. B. Faulds, G. Williamson, and J. F. Thibault. 1994. Degradation of feruloylated oligosaccharides from sugar-beet pulp and wheat bran by ferulic acid esterases from Aspergillus niger. Carbohydr. Res. 263: 257-269.
35. Record, E., M. Asther, C. Sigoillot, S. Pagès, P. J. Punt, M. Delattre, M. Haon, C. A. M. J. J. van den Hondel, J. C. Sigoillot, L. Lesage-Meessen, and M. Asther. 2003. Overproduction of the Aspergillus niger feruloyl esterase for pulp bleaching application. Appl. Microbiol. Biotechnol. 62:349-355.
36. Rice-Evans, C. A., N. J. Miller, and G. Paganga. 1996. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 20:933-956.
37. Rumlova, M., J. Benedikova, R. Cubinkova, I. Pichova, and T. Ruml. 2001. Comparison of classical and affinity purification techniques of Mason-Pfizer monkey virus capsid protein: the alteration of the product by an affinity tag. Protein Expr. Purif. 23:75-83.
38. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, p. 7.43-7.45. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Saulnier, L., C. Marot, M. Elgorriaga, E. Bonnin, and J. F. Thibault. 2001. Thermal and enzymatic treatments for the release of free ferulic acid from maize bran. Carbohydr. Polym. 45:269-275.
40. Schöbel, B., and W. Pollmann. 1980. Isolation and characterization of a chlorogenic acid esterase from Aspergillus niger. Z. Naturforsch. 35c:209-212.
41. Schöbel, B., and W. Pollmann. 1980. Further characterization of a chlorogenic acid hydrolase from Aspergillus niger. Z. Naturforsch. 35c:699-701.
42. Small, G. J., and J. Hemingway. 2000. Differential glycosylation produces heterogeneity in elevated esterases associated with insecticide resistance in the brown planthopper Nilaparvata lugens Stal. Insect Biochem. Mol. Biol. 30:443-453.
43. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
44. van Hartingsveldt, W., I. E. Mattern, C. M. van Zeijl, P. H. Pouwells, and C. A. van den Hondel. 1987. Development of a homologous transformation system for Aspergillus niger based on the pyrG gene. Mol. Gen. Genet. 206:71-75.
45. Wong, D. W. 2006. Feruloyl esterase: a key enzyme in biomass degradation. Appl. Biochem. Biotechnol. 133:87-112.
46. Wyss, D. F., and G. Wagner. 1996. The structural role of sugars in glycoproteins. Curr. Opin. Biotechnol. 7:409-416.