A Novel Strategy for Thermostability Improvement of Trypsin Based on N-Glycosylation within the Ω-Loop Region |
Guo, Chao
(Department of Biochemical Engineering, School of Chemical Engineering and Technology, Tianjin University)
Liu, Ye (Department of Biochemical Engineering, School of Chemical Engineering and Technology, Tianjin University) Yu, Haoran (Department of Biochemical Engineering, School of Chemical Engineering and Technology, Tianjin University) Du, Kun (Department of Biochemical Engineering, School of Chemical Engineering and Technology, Tianjin University) Gan, Yiru (Department of Biochemical Engineering, School of Chemical Engineering and Technology, Tianjin University) Huang, He (Department of Biochemical Engineering, School of Chemical Engineering and Technology, Tianjin University) |
1 | Badieyan S, Bevan DR, Zhang C. 2012. Study and design of stability in GH5 cellulases. Biotechnol. Bioeng. 109: 31-44. DOI |
2 | Bai Y, Sosnick TR, Mayne L, Englander SW. 1995. Protein folding intermediates: native-state hydrogen exchange. Science 269: 192-197. DOI |
3 | Çelik E, Çalik P. 2012. Production of recombinant proteins by yeast cells. Biotechnol. Adv. 30: 1108-1118. DOI |
4 | Chen Y, Chen X, Guo TL, Zhou P. 2015. Improving the thermostability of β-lactoglobulin via glycation: the effect of sugar structures. Food Res. Int. 69: 106-113. DOI |
5 | Daly R, Hearn MT. 2005. Expression of heterologous proteins in Pichia pastoris: a useful experimental tool in protein engineering and production. J. Mol. Recognit. 18: 119-138. DOI |
6 | Deng Z, Yang H, Shin H-D, Li J, Liu L. 2014. Structure-based rational design and introduction of arginines on the surface of an alkaline α-amylase from Alkalimonas amylolytica for improved thermostability. Appl. Microbiol. Biotechnol. 98: 8937-8945. DOI |
7 | Fang Z, Zhou P, Chang F, Yin Q, Fang W, Yuan J, et al. 2014. Structure-based rational design to enhance the solubility and thermostability of a bacterial laccase Lac15. PLoS One 9: 1-6. DOI |
8 | Fatima A, Husain Q. 2007. A role of glycosyl moieties in the stabilization of bitter gourd (Momordica charantia) peroxidase. Int. J. Biol. Macromol. 41: 56-63. DOI |
9 | Fei B, Xu H, Cao Y, Ma S, Guo H, Song T, et al. 2013. A multi-factors rational design strategy for enhancing the thermostability of Escherichia coli AppA phytase. J. Ind. Microbiol. Biotechnol. 40: 457-464. DOI |
10 | Fetrow JS. 1995. Omega loops: nonregular secondary structures significant in protein function and stability. FASEB J. 9: 708-717. DOI |
11 | Finehout EJ, Cantor JR, Lee KH. 2005. Kinetic characterization of sequencing grade modified trypsin. Proteomics 5: 2319-2321. DOI |
12 | Gizurarson JG, Filippusson H. 2015. Conjugation of ᴅ-glucosamine to bovine trypsin increases thermal stability and alters functional properties. Enzyme Microb. Technol. 75-76: 1-9. DOI |
13 | Han M, Wang W, Jiang G, Wang X, Liu X, Cao H, et al. 2014. Enhanced expression of recombinant elastase in Pichia pastoris through addition of N-glycosylation sites to the propeptide. Biotechnol. Lett. 36: 2467-2471. DOI |
14 | Han M, Wang X, Yan G, Wang W, Tao Y, Liu X, et al. 2014. Modification of recombinant elastase expressed in Pichia pastoris by introduction of N-glycosylation sites. J. Biotechnol. 171: 3-7. DOI |
15 | Hoedemaeker FJ, van Eijsden RR, Díaz CL, de Pater BS, Kijne JW. 1993. Destabilization of pea lectin by substitution of a single amino acid in a surface loop. Plant Mol. Biol. 22: 1039-1046. DOI |
16 | Hoshida H, Fujita T, Cha-aim K, Akada R. 2013. N-Glycosylation deficiency enhanced heterologous production of a Bacillus licheniformis thermostable α-amylase in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 97: 5473-5482. DOI |
17 | Hossler P, Khattak SF, Li ZJ. 2009. Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology 19: 936-949. DOI |
18 | Macauley-Patrick S, Fazenda ML, McNeil B, Harvey LM. 2005. Heterologous protein production using the Pichia pastoris expression system. Yeast 22: 249-270. DOI |
19 | Kemmler W, Peterson JD, Steiner DF. 1971. Studies on the conversion of proinsulin to insulin I. Conversion in vitro with trypsin and carboxypeptidase B. J. Biol. Chem. 246: 6786-6791. |
20 | Kostova Z, Wolf DH. 2003. For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin–proteasome connection. EMBO J. 22: 2309-2317. DOI |
21 | Meldgaard M. 1994. Different effects of N-glycosylation on the thermostability of highly homologous bacterial (1, 3-1, 4)-β-glucanases secreted from yeast. Microbiology 140: 159-166. DOI |
22 | Miyazaki T, Yashiro H, Nishikawa A, Tonozuka T. 2014. The side chain of a glycosylated asparagine residue is important for the stability of isopullulanase. J. Biochem. 157: 225-234. DOI |
23 | Obuchi M, Kawahara K, Motooka D, Nakamura S, Yamanaka M, Takeda T, et al. 2009. Hyperstability and crystal structure of cytochrome c555 from hyperthermophilic Aquifex aeolicus. Acta Crystallogr. D Biol. Crystallogr. 65: 804-813. DOI |
24 | Parge HE, Hallewell RA, Tainer JA. 1992. Atomic structures of wild-type and thermostable mutant recombinant human Cu,Zn superoxide dismutase. Proc. Natl. Acad. Sci. USA 89: 6109-6113. DOI |
25 | Pham VT, Ewing E, Kaplan H, Choma C, Hefford MA. 2008. Glycation improves the thermostability of trypsin and chymotrypsin. Biotechnol. Bioeng. 101: 452-459. DOI |
26 | Samoudi M, Tabandeh F, Minuchehr Z, Cohan RA, Inanlou DN, Khodabandeh M, Anvar MS. 2015. Rational design of hyper-glycosylated interferon beta analogs: a computational strategy for glycoengineering. J. Mol. Graph. Model. 56: 31-42. DOI |
27 | Skropeta D. 2009. The effect of individual N-glycans on enzyme activity. Bioorg. Med. Chem. 17: 2645-2653. DOI |
28 | Schweiker KL, Makhatadze GI. 2009. Protein stabilization by the rational design of surface charge–charge interactions. Methods Mol. Biol. 490: 261-283. |
29 | Scott WR, Hünenberger PH, Tironi IG, Mark AE, Billeter SR, Fennen J, et al. 1999. The GROMOS biomolecular simulation program package. J. Phys. Chem. A 103: 3596-3607. DOI |
30 | Shental-Bechor D, Levy Y. 2009. Folding of glycoproteins: toward understanding the biophysics of the glycosylation code. Curr. Opin. Struct. Biol. 19: 524-533. DOI |
31 | Thangudu RR, Vinayagam A, Pugalenthi G, Manonmani A, Offmann B, Sowdhamini R. 2005. Native and modeled disulfide bonds in proteins: knowledge-based approaches toward structure prediction of disulfide-rich polypeptides. Proteins 58: 866-879. DOI |
32 | Tull D, Gottschalk TE, Svendsen I, Kramhøft B, Phillipson BA, Bisgård-Frantzen H, et al. 2001. Extensive N-glycosylation reduces the thermal stability of a recombinant alkalophilic Bacillus α-amylase produced in Pichia pastoris. Protein Expr. Purif. 21: 13-23. DOI |
33 | Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ. 2005. GROMACS: fast, flexible, and free. J. Comput. Chem. 26: 1701-1718. DOI |
34 | Wildt S, Gerngross TU. 2005. The humanization of N-glycosylation pathways in yeast. Nat. Rev. Microbiol. 3: 119-128. DOI |
35 | Xi H, Tian Y, Zhou N, Zhou Z, Shen W. 2015. Characterization of an N-glycosylated Bacillus subtilis leucine aminopeptidase expressed in Pichia pastoris. J. Basic Microbiol. 55: 236-246. DOI |
36 | Zheng L, Baumann U, Reymond J-L. 2004. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32: e115. DOI |
37 | Yu H, Huang H. 2014. Engineering proteins for thermostability through rigidifying flexible sites. Biotechnol. Adv. 32: 308-315. DOI |
38 | Yu H, Zhao Y, Guo C, Gan Y, Huang H. 2015. The role of proline substitutions within flexible regions on thermostability of luciferase. Biochim. Biophys. Acta 1854: 65-72. DOI |