Role of N-linked glycosylation in the secretion and enzymatic properties of Rhizopus chinensis lipase expressed in Pichia pastoris

Microbial Cell Factories

Volumn 14, Issue 1, 2015, Pages

  Yang, Min ^a   Yu, Xiao Wei ^a   Zheng, Haiyan ^b   Sha, Chong ^a   Zhao, Caifeng ^b   Qian, Meiqian ^b   Xu, Yan ^a  

^a JIANGNAN UNIVERSITY   (China)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Enzyme activity; LC MS MS; N glycosylation; Pichia pastoris; Rhizopus chinensis lipase; Secretion; Thermostability

Indexed keywords

ASPARAGINE; FUNGAL ENZYME; GLYCAN; MESSENGER RNA; RHIZOPUS CHINENSIS LIPASE; UNCLASSIFIED DRUG; TRIACYLGLYCEROL LIPASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME RELEASE; GLYCOSYLATION; KOMAGATAELLA PASTORIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THERMOSTABILITY; ENZYMOLOGY; METABOLISM; PICHIA; PROTEIN ENGINEERING; RHIZOPUS;

PICHIA PASTORIS; RHIZOPUS MICROSPORUS VAR. CHINENSIS;

GLYCOSYLATION; LIPASE; PICHIA; PROTEIN ENGINEERING; RHIZOPUS;

EID: 84928793234     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-015-0225-5     Document Type: Article

References (59)

1. Daly R, Hearn MT. Expression of heterologous proteins in Pichia pastoris: a useful experimental tool in protein engineering and production. J Mol Rec. 2005;18:119-38.
2. Sørensen HP. Towards universal systems for recombinant gene expression. Microb Cell Fact. 2010;9:27.
3. Pratap J, Rajamohan G, Dikshit K. Characteristics of glycosylated streptokinase secreted from Pichia pastoris: enhanced resistance of SK to proteolysis by glycosylation. Appl Microbiol Biotechnol. 2000;53:469-75.
4. Parodi AJ. Reglucosylation of glycoproteins and quality control of glycoprotein folding in the endoplasmic reticulum of yeast cells. Biochem Biophy Acta. 1999;1426:287-95.
5. Helenius A, Aebi M. Intracellular functions of N-linked glycans. Science. 2001;291:2364-9.
6. Ito K, Seri A, Kimura F, Matsudomi N. Site-specific glycosylation at Asn-292 in ovalbumin is essential to efficient secretion in yeast. J Biochem. 2007;141:193-9.
7. Kazenwadel C, Klebensberger J, Richter S, Pfannstiel J, Gerken U, Pickel B, et al. Optimized expression of the dirigent protein AtDIR6 in Pichia pastoris and impact of glycosylation on protein structure and function. Appl Microbiol Biotechnol. 2013;97:7215-27.
8. Wei W, Chen L, Zou G, Wang Q, Yan X, Zhang J, et al. N-glycosylation affects the proper folding, enzymatic characteristics and production of a fungal β-glucosidase. Biochem Bioeng. 2013;110:3075-84.
9. Winiarska B, Dwornik A, Dȩbski J, Grzelak K, Bystranowska D, Zalewska M, et al. N-linked glycosylation of G mellonella juvenile hormone binding protein-comparison of recombinant mutants expressed in P pastoris cells with native protein. Biochim Biophys Acta. 2011;1814:610-21.
10. Borman S. Glycosylation engineering. Chem Eng News. 2006;84:13-22.
11. Solá RJ, Griebenow K. Chemical glycosylation: new insights on the interrelation between protein structural mobility, thermodynamic stability, and catalysis. FEBS Lett. 2006;580:1685-90.
12. Hang HC, Bertozzi CR. Chemoselective approaches to glycoprotein assembly. Acc Chem Res. 2001;34:727-36.
13. Dwek RA. Glycobiology-more functions for oligosaccharides. Science. 1995;269:1234-5.
14. Solá R, Rodriguez-Martinez J, Griebenow K. Modulation of protein biophysical properties by chemical glycosylation: biochemical insights and biomedical implications. Cell Mol Life Sci. 2007;64:2133-52.
15. Sharma R, Chisti Y, Banerjee UC. Production, purification, characterization, and applications of lipases. Biotechnol Adv. 2001;19:627-62.
16. Soumanou MM, Pérignon M, Villeneuve P. Lipase-catalyzed interesterification reactions for human milk fat substitutes production: a review. Eur J Lipid Sci Technol. 2013;115:270-85.
17. Peng Q, Wang X, Shang M, Huang J, Guan G, Li Y, et al. Isolation of a novel alkaline-stable lipase from a metagenomic library and its specific application for milkfat flavor production. Microb Cell Fact. 2014;13:1-9.
18. Hama S, Kondo A. Enzymatic biodiesel production: an overview of potential feedstocks and process development. Bioresour Technol. 2013;135:386-95.
19. Mounguengui RWM, Brunschwig C, Baréa B, Villeneuve P, Blin J. Are plant lipases a promising alternative to catalyze transesterification for biodiesel production? Progr Energy Combust Sci. 2013;39:441-56.
20. Hwang HT, Qi F, Yuan C, Zhao X, Ramkrishna D, Liu D, et al. Lipase catalyzed process for biodiesel production: Protein engineering and lipase production. Biotechnol Bioeng. 2014;111:639-53.
21. Di Lorenzo M, Hidalgo A, Haas M, Bornscheuer UT. Heterologous production of functional forms of Rhizopus oryzae lipase in Escherichia coli. Appl Enviro Microbiol. 2005;71:8974-7.
22. Ueda M, Takahashi S, Washida M, Shiraga S, Tanaka A. Expression of Rhizopus oryzae lipase gene in Saccharomyces cerevisiae. J Mol Catal B-Enzym. 2002;17:113-24.
23. Takahashi S, Ueda M, Atomi H, Beer H, Bornscheuer U, Schmid R, et al. Extracellular production of active Rhizopus oryzae lipase by Saccharomyces cerevisiae. J Ferment Bioeng. 1998;86:164-8.
24. Resina D, Serrano A, Valero F, Ferrer P. Expression of a Rhizopus oryzae lipase in Pichia pastoris under control of the nitrogen source-regulated formaldehyde dehydrogenase promoter. J Biotechnol. 2004;109:103-13.
25. Minning S, Schmidt-Dannert C, Schmid R. Functional expression of Rhizopus oryzae lipase in Pichia pastoris: high-level production and some properties. J Biotechnol. 1998;66:147.
26. Minning S, Serrano A, Ferrer P, Sola C, Schmid RD, Valero F. Optimization of the high-level production of Rhizopus oryzae lipase in Pichia pastoris. J Biotechnol. 2001;86:59-70.
27. Liu Y, Xie W, Yu H. Enhanced activity of Rhizomucor miehei lipase by deglycosylation of its propeptide in Pichia pastoris. Curr Microbio. 2014;68:186-91.
28. Takahashi S, Ueda M, Tanaka A. Independent production of two molecular forms of a recombinant Rhizopus oryzae lipase by KEX2-engineered strains of Saccharomyces cerevisiae. Appl Microbiol Biotechnol. 1999;52:534-40.
29. Zhu J, Liu H, Zhang J, Wang P, Liu S, Liu G, et al. Effects of Asn-33 glycosylation on the thermostability of Thermomyces lanuginosus lipase. J Appl Microbiol. 2014;117:1-8.
30. Yu XW, Wang LL, Yan X. Rhizopus chinensis lipase: gene cloning, expression in Pichia pastoris and properties. J Mol Catal B-Enzym. 2009;57:304-11.
31. Yu XW, Sha C, Guo YL, Xiao R, Xu Y. High-level expression and characterization of a chimeric lipase from Rhizopus oryzae for biodiesel production. Biotechnol Biofuels. 2013;6:29.
32. Rudd PM, Scragg IG, Coghill E, Dwek RA. Separation and analysis of the glycoform populations of ribonuclease B using capillary electrophoresis. Glycoconjugate J. 1992;9:86-91.
33. Petrescu AJ, Milac AL, Petrescu SM, Dwek RA, Wormald MR. Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology. 2004;14:103-14.
34. Fryksdale BG, Jedrzejewski PT, Wong DL, Gaertner AL, Miller BS. Impact of deglycosylation methods on two-dimensional gel electrophoresis and matrix assisted laser desorption/ionization-time of flight-mass spectrometry for proteomic analysis. Electrophoresis. 2002;23:2184-93.
35. Maley F, Trimble RB, Tarentino AL, Plummer Jr TH. Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal Biochem. 1989;180:195-204.
36. Durchschlag H, Christl R, Jaenicke R. Comparative determination of the particle weight of glycoproteins by SDS-PAGE and analytical ultracentrifugation. In Progress in Analytical Ultracentrifugation. Progr Colloid Polym Sci. 1991: 41-56
37. Brakch N, Allemandou F, Keller I, Nussberger J. The renin prosequence enhances constitutive secretion of renin and optimizes renin activity. Curr Neurovasc Res. 2011;8:121-30.
38. Han M, Wang X, Ding H, Jin M, Yu L, Wang J, et al. The role of N-glycosylation sites in the activity, stability, and expression of the recombinant elastase expressed by Pichia pastoris. Enzym Micro Technol. 2014;54:32-7.
39. Miller GC, Long CJ, Bojilova ED, Marchadier D, Badellino KO, Blanchard N, et al. Role of N-linked glycosylation in the secretion and activity of endothelial lipase. J Lipid Res. 2004;45:2080-7.
40. Desko MM, Gross DA, Kohler JJ. Effects of N-glycosylation on the activity and localization of GlcNAc-6-sulfotransferase 1. Glycobiology. 2009;19:1068-77.
41. Shinde U, Inouye M. Intramolecular chaperones and protein folding. Trends Biochem Sci. 1993;18:442-6.
42. Shinde U, Li Y, Chatterjee S, Inouye M. Folding pathway mediated by an intramolecular chaperone. Proc Natl Acad Sci U S A. 1993;90:6924-8.
43. Baker D, Sohl JL, Agard DA. A protein-folding reaction under kinetic control. Nature. 1992;356:263-5.
44. Mitra J, Tang X-j, Almo S, Shields D. Temperature-induced conformational changes in prosomatostatin-II: implications for processing. Biochem J. 1998;334:275-82.
45. Andersson E, Hellman L, Gullberg U, Olsson I. The role of the propeptide for processing and sorting of human myeloperoxidase. J Biolo Chemi. 1998;273:4747-53.
46. Imperiali B, O'Connor S. Effect of N-linked glycosylation on glycopeptide and glycoprotein structure. Curr Opin Chem Biol. 1999;3:643.
47. Muller-Steffner H, Kuhn I, Argentini M, Schuber F. Identification of the N-glycosylation sites on recombinant bovine CD38 expressed in Pichia pastoris: Their impact on enzyme stability and catalytic activity. Protein Expr Purif. 2010;70:151-7.
48. Mitsutaka Kohno ME, Rie T, Wataru K. Thermal stability of Rhizopus niveus lipase expressed in a Kex2 mutant yeast. J Biotechnol. 2000;81:141-50.
49. Fonseca-Maldonado R, Vieira DS, Alponti JS, Bonneil E, Thibault P, Ward RJ. Engineering the pattern of protein glycosylation modulates the thermostability of a GH11 xylanase. J Biolo Chemi. 2013;288:25522-34.
50. Rudd PM, Joao HC, Coghill E, Fiten P, Saunders MR, Opdenakker G, et al. Glycoforms modify the dynamic stability and functional activity of an enzyme. Biochem. 1994;33:17-22.
51. Lige B, Ma S, van Huystee R. The effects of the site-directed removal of N-glycosylation from cationic peanut peroxidase on its function. Arch Biochem Biophys. 2001;386:17-24.
52. Sugihara A, Ueshima M, Shimada Y, Tsunasawa S, Tominaga Y. Purification and characterization of a novel thermostable lipase from Pseudomonas cepacia. J Biochem. 1992;112:598-603.
53. Zou S, Huang S, Kaleem I, Li C. N-Glycosylation enhances functional and structural stability of recombinant β-glucuronidase expressed in Pichia pastoris. J Biotechnol. 2013;164:75-81.
54. Zhu SS, Yu XW, Xu Y. Constitutive expression of lipase in Pichia pastoris and the high throughput screening method. Microbiol China. 2012;39:873-81.
55. Hananan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983;166:557-80.
56. Kordel M, Hofmann B, Schomburg D, Schmid R. Extracellular lipase of Pseudomonas sp. strain ATCC 21808: purification, characterization, crystallization, and preliminary X-ray diffraction data. J Bacteriol. 1991;173:4836-41.
57. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-5.
58. Burdette RA, Quinn D. Interfacial reaction dynamics and acyl-enzyme mechanism for lipoprotein lipase-catalyzed hydrolysis of lipid p-nitrophenyl esters. J Biolo Chemi. 1986;261:12016-21.
59. Hernández-Rodríguez B, Córdova J, Bárzana E, Favela-Torres E. Effects of organic solvents on activity and stability of lipases produced by thermotolerant fungi in solid-state fermentation. J Mol Catal B-Enzym. 2009;61:136-42.