Characterization of amylomaltase from Thermus filiformis and the increase in alkaline and thermo-stability by E27R substitution

Process Biochemistry

Volumn 50, Issue 11, 2015, Pages 1814-1824

  Kaewpathomsri, Piriya ^a   Takahashi, Yui ^b   Nakamura, Shigeyoshi ^c   Kaulpiboon, Jarunee ^d   Kidokoro, Shun Ichi ^c   Murakami, Shuichiro ^b   Krusong, Kuakarun ^a   Pongsawasdi, Piamsook ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b MEIJI UNIVERSITY   (Japan)

^c NAGAOKA UNIVERSITY OF TECHNOLOGY   (Japan)

^d THAMMASAT UNIVERSITY   (Thailand)

Author keywords

Alkaline stability; Amylomaltase; Cyclization; Large ring cyclodextrin; Thermostability; Thermus filiformis

Indexed keywords

ALKALINITY; CLONING; CYCLODEXTRINS; DICHROISM; ENZYMES; ESCHERICHIA COLI; OLIGOSACCHARIDES;

AMYLOMALTASE; CIRCULAR DICHROISM SPECTRA; CONFORMATIONAL CHANGE; CYCLIZATION REACTIONS; GLYCOSIDE HYDROLASES; LARGE RINGS; THERMOSTABILITY; THERMUS;

CYCLIZATION;

EID: 84946496453     PISSN: 13595113     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.procbio.2015.08.006     Document Type: Article

References (63)

1. T. Takaha, and S.M. Smith The functions of 4-alpha-glucanotransferases and their use for the production of cyclic glucans Biotechnol. Genet. Eng. Rev. 16 1999 257 280
2. B. Henrissat A classification of glycosyl hydrolases based on amino acid sequence similarities Biochem. J. 280 1991 309 316
3. Y. Bourne, and B. Henrissat Glycoside hydrolases and glycosyltransferases: families and functional modules Curr. Opin. Struct. Biol. 11 2011 593 600
4. H. Taira, H. Nagase, T. Endo, and H. Ueda Isolation, purification and characterization of large-ring cyclodextrins (CD36∼CD39) J. Incl. Phenom. Macrocycl. Chem. 56 2006 23 28
5. K.L. Larsen Large cyclodextrins J. Incl. Phenom. Macrocycl. Chem. 43 2002 1 13
6. M.G. Gotsev, and P.M. Ivanov Large-ring cyclodextrins. A molecular dynamics study of the conformational dynamics and energetics of CD10, CD14 and CD26 Arkivoc 13 2007 67 89
7. T. Endo Large-ring cyclodextrins Trends Glycosci. Glycotechnol. 23 2011 79 92
8. K. Tomono, A. Mugishima, T. Suzuki, H. Goto, H. Ueda, T. Nagai, and J. Watanabe Interaction between cycloamylose and various drugs J. Incl. Phenom. Macrocycl. Chem. 44 2002 267 270
9. S. Machida, S. Ogawa, S. Xiaohua, T. Takaha, K. Fujii, and K. Hayashi Cycloamylose as an efficient artificial chaperone for protein refolding FEBS Lett. 486 2000 131 135
10. H.-S. Lee, J.-H. Auh, H.-G. Yoon, M.-J. Kim, J.-H. Park, S.-S. Hong, M.-H. Kang, T.-J. Kim, T.-W. Moon, J.-W. Kim, and K.-H. Park Cooperative action of α-glucanotransferase and maltogenic amylase for an improved process of isomaltooligosaccharide (IMO) production J. Agric. Food Chem. 50 2002 2812 2817
11. S. Saehu, W. Srisimarat, M.H. Prousoontorn, and P. Pongsawasdi Transglucosylation reaction of amylomaltase for the synthesis of anticariogenic oligosaccharides J. Mol. Catal. B: Enzym. 88 2013 77 83
12. T. Kaper, B. Talik, T.J. Ettema, H. Bos, M.J.E.C. van der Maarel, and L. Dijkhuizen Amylomaltase of Pyrobaculum aerophilum IM2 produces thermoreversible starch gels Appl. Environ. Microbiol. 71 2005 5098 5106
13. S.K. Goda, O. Eissa, M. Akhtar, and N.P. Minton Molecular analysis of a Clostridium butyricum NCIMB 7423 gene encoding 4-α-glucanotransferase and characterization of the recombinant enzyme produced in Escherichia coli Microbiology 143 1997 3287 3294
14. W. Liebl, R. Feil, J. Gabelsberger, J. Kellermann, and K.-H. Schleifer Purification and characterization of a novel thermostable 4-α-glucanotransferase of Thermotoga maritima cloned in Escherichia coli Eur. J. Biochem. 207 1992 81 88
15. S.H. Bhuiyan, M. Kitaoka, and K. Hayashi A cycloamylose-forming hyperthermostable 4-α-glucanotransferase of Aquifex aeolicus expressed in Escherichia coli J. Mol. Catal. B: Enzym. 22 2003 45 53
16. Y. Terada, K. Fujii, T. Takaha, and S. Okada Thermus aquaticus ATCC 33923 amylomaltase gene cloning and expression and enzyme characterization: production of cycloamylose Appl. Environ. Microbiol. 65 1999 910 915
17. M.J.E.C. van der Maarel, G.J.W. Euverink, D.J. Binnema, H.T.P. Bos, and J. Bergsma Amylomaltase from the hyperthermophilic bacterium Thermus thermophilus: enzyme characteristics and application in the starch industry Med. Fac. Landbouww Univ. Gent. 65/3a 2000 231 234
18. B.Y. Bang, H.J. Kim, H.Y. Kim, M.Y. Baik, S.C. Ahn, C.H. Kim, and C.S. Park Cloning and overexpression of 4-α-glucanotransferase from Thermus brockianus (TBGT) in E. coli J. Microbiol. Biotechnol. 16 2006 1809 1813
19. N.-S. Seo, S.-A. Roh, J.-H. Auh, J.-H. Park, Y.-R. Kim, and K.-H. Park Structural characterization of rice starch in rice cake modified by Thermus scotoductus 4-α-glucanotransferase (TSαGTase) J. Food Sci. 72 2007 C331 C336
20. W. Srisimarat, A. Powviriyakul, J. Kaulpiboon, K. Krusong, W. Zimmermann, and P. Pongsawasdi A novel amylomaltase from Corynebacterium glutamicum and analysis of the large-ring cyclodextrin products J. Incl. Phenom. Macrocycl. Chem. 70 2011 369 375
21. B.-S. Jeon, H. Taguchi, H. Sakai, T. Ohshima, T. Wakagi, and H. Matsuzawa 4-α-glucanotransferase from the hyperthermophilic archaeon Thermococcus litoralis Eur. J. Biochem. 248 1997 171 178
22. A. Godany, B. Vidova, and S. Janecek The unique glycoside hydrolase family 77 amylomaltase from Borrelia burgdorferi with only catalytic triad conserved FEMS Microbiol. Lett. 284 2008 84 91
23. T. Takaha, M. Yanase, S. Okada, and S.M. Smith Disproportionating enzyme (4-alpha-glucanotransferase; EC 2.4.1.25) of potato. Purification, molecular cloning, and potential role in starch metabolism J. Biol. Chem. 268 1993 1391 1396
24. N. Yoshio, I. Maeda, H. Taniguchi, and M. Nakamura Purification and properties of D-enzyme from malted barley J. Jpn. Soc. Starch Sci. 33 1986 244 252
25. K. Tantanarat, E.C. O'Neill, M. Rejzek, R.A. Field, and T. Limpaseni Expression and characterization of 4-α-glucanotransferase genes from Manihot esculenta Crantz and Arabidopsis thaliana and their use for the production of cycloamyloses Process Biochem. 49 2014 84 89
26. I. Przylas, K. Tomoo, Y. Terada, T. Takaha, K. Fujii, W. Saenger, and N. Sträter Crystal structure of amylomaltase from Thermus aquaticus, a glycosyltransferase catalysing the production of large cyclic glucans J. Mol. Biol. 296 2000 873 886
27. T. Kaper, H. Leemhuis, J.C.M. Uitdehaag, B.A. van der Veen, B.W. Dijkstra, M.J.E.C. van der Maarel, and L. Dijkhuizen Identification of acceptor substrate binding subsites + 2 and +3 in the amylomaltase from Thermus thermophilus HB8 Biochemistry 46 2007 5261 5269
28. J.-H. Jung, T.-Y. Jung, D.-H. Seo, S.-M. Yoon, H.-C. Choi, B.C. Park, and E.J. Woo Structural and functional analysis of substrate recognition by the 250s loop in amylomaltase from Thermus brockianus Proteins Struct. Funct. Bioinform. 79 2011 633 644
29. A. Roujeinikova, C. Raasch, S. Sedelnikova, W. Liebl, and D.W. Rice Crystal structure of Thermotoga maritima 4-α-glucanotransferase and its acarbose complex: implications for substrate specificity and catalysis J. Mol. Biol. 321 2002 149 162
30. H. Imamura, S. Fushinobu, M. Yamamoto, T. Kumasaka, B.-S. Jeon, T. Wakagi, and H. Matsuzawa Crystal structures of 4-α-glucanotransferase from Thermococcus litoralis and its complex with an inhibitor J. Biol. Chem. 278 2003 19378 19386
31. J.A. Hudson, H.W. Morgan, and R.M. Daniel Thermus filiformis sp. nov., a filamentous caldoactive bacterium Int. J. Syst. Bacteriol. 37 1987 431 436
32. M.R. Green, and J. Sambrook Molecular Cloning: A Laboratory Manual 4th ed. 2012 Cold Spring Harbor Cold Spring Harbor Laboratory Press New York 44 46
33. F. Sanger, S. Nicklen, and A.R. Coulson DNA sequencing with chain-terminating inhibitors Proc. Natl. Acad. Sci. U. S. A. 74 1977 5463 5467
34. M. Wei, J. Deng, K. Feng, B. Yu, and Y. Chen Universal method facilitating the amplification of extremely GC-rich DNA fragments from genomic DNA Anal. Chem. 82 2010 6303 6307
35. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins Clustal w and clustal x version 2.0 Bioinformatics 23 2007 2947 2948
36. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar MEGA6: molecular evolutionary genetics analysis version 6.0 Mol. Biol. Evol. 30 2013 2725 2729
37. R.M. Bennett-Lovsey, A.D. Herbert, M.J.E. Sternberg, and L.A. Kelley Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre Proteins Struct. Funct. Bioinform. 70 2008 611 625
38. N. Guex, and M.C. Peitsch SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18 1997 2714 2723
39. M. Johansson, V. Zoete, O. Michielin, and N. Guex Defining and searching for structural motifs using DeepView/Swiss-PdbViewer BMC Bioinform. 13 2012 173
40. D.M. Bollag, and S.J. Edelstein Protein Methods 1991 Wiley-Liss 107 154
41. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
42. A. Sols, and G. De La Fuente Glucose oxidase as an analytic reagent Rev. Esp. Fisiol. 13 1957 231 245
43. K. Koizumi, H. Sanbe, Y. Kubota, Y. Terada, and T. Takaha Isolation and characterization of cyclic alpha-(1→4)-glucans having degrees of polymerization 9-31 and their quantitative analysis by high-performance anion-exchange chromatography with pulsed amperometric detection J. Chromatogr. A 852 1999 407 416
44. W. Srisimarat, J. Kaulpiboon, K. Krusong, W. Zimmermann, and P. Pongsawasdi Mutation at Tyr-172 in the amylomaltase from Corynebacterium glutamicum leads to a change in large-ring cyclodextrin products profile Appl. Environ. Microbiol. 78 2012 7223 7228
45. G.L. Miller Use of dinitrosalicylic acid reagent for determination of reducing sugar Anal. Chem. 31 1959 426 428
46. M. Sinner, and J. Puls Non-corrosive dye reagent for detection of reducing sugars in borate complex ion-exchange chromatography J. Chromatogr. A 156 1978 197 204
47. M.M. Islam, S. Sohya, K. Noguchi, S. Kidokoro, M. Yohda, and Y. Kuroda Thermodynamic and structural analysis of highly stabilized BPTIs by single and double mutations Proteins Struct. Funct. Bioinform. 77 2009 962 970
48. C. Aston, B. Mishra, and D.C. Schwartz Optical mapping and its potential for large-scale sequencing projects Trends Biotechnol. 17 1999 297 302
49. W. Rachadech, P. Nimpiboon, W. Naumthong, S. Nakapong, K. Krusong, and P. Pongsawasdi Identification of essential tryptophan in amylomaltase from Corynebacterium glutamicum Int. J. Biol. Macromol. 76 2015 230 235
50. K. Fujii, H. Minagawa, Y. Terada, T. Takaha, T. Kuriki, J. Shimada, and H. Kaneko Function of second glucan binding site including tyrosines 54 and 101 in Thermus aquaticus amylomaltase J. Biosci. Bioeng. 103 2007 167 173
51. M.S. da Costa, M.F. Nobre, and F.A. Rainey Genus I. Thrmus D.R. Boone, R.W. Castenholz, G.M. Garrity, Bergey's Manual of Systematic Bacteriology 2nd ed. 2001 New York Springer 404 414
52. A. Kuchtova, and S. Janecek In silico analysis of family GH77 with focus on amylomaltases from borreliae and disproportionating enzymes DPE2 from plants and bacteria Biochim. Biophys. Acta 2015 10.1016/j.bbapap.2015.05.009
53. E. Gasteiger, A. Gattiker, C. Hoogland, I. Ivanyi, R.D. Appel, and A. Bairoch ExPASy: the proteomics server for in-depth protein knowledge and analysis Nucleic Acids Res. 31 2003 3784 3788
54. T. Takaha, M. Yanase, H. Takata, S. Okada, and S.M. Smith Potato D-enzyme catalyzes the cyclization of amylose to produce cycloamylose, a novel cyclic glucan J. Biol. Chem. 271 1996 2902 2908
55. D. Shao-Wei, and L. Da-Nian Kinetics of the thermal inactivation of Bacillus subtilis α-amylase and its application on the desizing of cotton fabrics J. Appl. Polym. Sci. 109 2008 3733 3738
56. G. Vogt, S. Woell, and P. Argos Protein thermal stability, hydrogen bonds, and ion pairs J. Mol. Biol. 269 1997 631 643
57. F. Alam, and A. Hasnain Studies on swelling and solubility of modified starch from taro (Colocasia esculenta): effect of pH and temperature Agric. Conspec. Sci. ACS 74 2009 45 50
58. S. Kumar, C.-J. Tsai, and R. Nussinov Factors enhancing protein thermostability Protein Eng. 13 2000 179 191
59. A. Masui, N. Fujiwara, and T. Imanaka Stabilization and rational design of serine protease AprM under highly alkaline and high-temperature conditions Appl. Environ. Microbiol. 60 1994 3579 3584
60. S. Sokalingam, G. Raghunathan, N. Soundrarajan, and S.-G. Lee A study on the effect of surface lysine to arginine mutagenesis on protein stability and structure using green fluorescent protein PLoS ONE 7 2012 e40410
61. C. Zhou, M. Zhang, Y. Wang, W. Guo, Z. Liu, Y. Wang, and W. Wang Enhancement of the thermo-alkali-stability of xylanase II from Aspergillus usamii E001 by site-directed mutagenesis Afr. J. Microbiol. Res. 7 2013 1535 1542
62. Z. Deng, H. Yang, H. Shin, J. Li, and L. Liu 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 2014 8937 8945
63. J. Wen, K. Arthur, L. Chemmalil, S. Muzammil, J. Gabrielson, and Y. Jiang Applications of differential scanning calorimetry for thermal stability analysis of proteins: qualification of DSC J. Pharm. Sci. 101 2012 955 964