Structural dissection of the maltodextrin disproportionation cycle of the Arabidopsis plastidial disproportionating enzyme 1 (DPE1)

Journal of Biological Chemistry

Volumn 290, Issue 50, 2015, Pages 29834-29853

  O'Neill, Ellis C ^a   Stevenson, Clare E M ^a   Tantanarat, Krit ^b,c   Latousakis, Dimitrios ^a   Donaldson, Matthew I ^a   Rejzek, Martin ^a   Nepogodiev, Sergey A ^a   Limpaseni, Tipaporn ^b   Field, Robert A ^a   Lawson, David M ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b CHULALONGKORN UNIVERSITY   (Thailand)

^c NARESUAN UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

POLYSACCHARIDES; SUBSTRATES;

ACTIVE SITE; ACTIVE SITE RESIDUES; ARABIDOPSIS; DISPROPORTIONATIONS; MALTODEXTRINS; MOLECULAR LEVELS; STARCH DEGRADATION;

ENZYMES;

DISPROPORTIONATING ENZYME 1; HOMODIMER; MALTODEXTRIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ENZYME; POLYSACCHARIDE;

ARABIDOPSIS THALIANA; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ASSAY; ENZYME BINDING; ENZYME SUBSTRATE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; RESIDUE ANALYSIS; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; ARABIDOPSIS; CHEMISTRY; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; PLASTID; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ARABIDOPSIS; CRYSTALLOGRAPHY, X-RAY; ENZYMES; MOLECULAR SEQUENCE DATA; PLASTIDS; POLYSACCHARIDES; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84949636198     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.682245     Document Type: Article

References (63)

1. Zeeman, S. C., Kossmann, J., and Smith, A. M. (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol. 61, 209-234
2. Smith, A. M. (2012) Starch in the Arabidopsis plant. Starch 64, 421-434
3. Smirnova, J., Fernie, A. R., and Steup, M. (2015) in Starch: Metabolism and Structure (Nakamura, Y., ed) pp. 239-290, Springer Publishing, Tokyo
4. Smith, A. M., Zeeman, S. C., and Smith, S. M. (2005) Starch degradation. Annu. Rev. Plant Biol. 56, 73-98
5. Delatte, T., Umhang, M., Trevisan, M., Eicke, S., Thorneycroft, D., Smith, S. M., and Zeeman, S. C. (2006) Evidence for distinct mechanisms of starch granule breakdown in plants. J. Biol. Chem. 281, 12050-12059
6. O'Neill, E. C., Rashid, A. M., Stevenson, C. E. M., Hetru, A.-C., Gunning, A. P., Rejzek, M., Nepogodiev, S. A., Bornemann, S., Lawson, D. M., and Field, R. A. (2014) Sugar-coated sensor chip and nanoparticle surfaces for the in vitro enzymatic synthesis of starch-like materials. Chem. Sci. 5, 341-350
7. Fulton, D. C., Stettler, M., Mettler, T., Vaughan, C. K., Li, J., Francisco, P., Gil, M., Reinhold, H., Eicke, S., Messerli, G., Dorken, G., Halliday, K., Smith, A. M., Smith, S. M., and Zeeman, S. C. (2008) β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell 20, 1040-1058
8. Critchley, J. H., Zeeman, S. C., Takaha, T., Smith, A. M., and Smith, S. M. (2001) A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant J. 26, 89-100
9. Lin, T. P., and Preiss, J. (1988) Characterization of D-enzyme (4-α-glucanotransferase) in Arabidopsis leaf. Plant Physiol. 86, 260-265
10. Kakefuda, G., and Duke, S. H. (1989) Characterization of pea chloroplast D-enzyme (4-α-D-glucanotransferase). Plant Physiol. 91, 136-143
11. Tantanarat, K., O'Neill, E., Rejzek, M., Field, R. A., and Limpaseni, T. (2014) 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, 84-89
12. Bresolin, N. S., Li, Z., Kosar-Hashemi, B., Tetlow, I. J., Chatterjee, M., Rahman, S., Morell, M. K., and Howitt, C. A. (2006) Characterisation of disproportionating enzyme from wheat endosperm. Planta 224, 20-31
13. Dippel, R., and Boos, W. (2005) The maltodextrin system of Escherichia coli: metabolism and transport. J. Bacteriol. 187, 8322-8331
14. Takaha, T., Yanase, M., Takata, H., Okada, S., and Smith, S. M. (1996) Potato D-enzyme catalyzes the cyclization of amylose to produce cycloamylose, a novel cyclic glucan. J. Biol. Chem. 271, 2902-2908
15. Fujii, H., Shin-Ya, M., Takeda, S., Hashimoto, Y., Mukai, S. A., Sawada, S., Adachi, T., Akiyoshi, K., Miki, T., and Mazda, O. (2014) Cycloamylosenanogel drug delivery system-mediated intratumor silencing of the vascular endothelial growth factor regulates neovascularization in tumor microenvironment. Cancer Sci. 105, 1616-1625
16. Toita, S., Morimoto, N., and Akiyoshi, K. (2010) Functional cycloamylose as a polysaccharide-based biomaterial: application in a gene delivery system. Biomacromolecules 11, 397-401
17. Machida, S., Ogawa, S., Xiaohua, S., Takaha, T., Fujii, K., and Hayashi, K. (2000) Cycloamylose as an efficient artificial chaperone for protein refolding. FEBS Lett. 486, 131-135
18. Tantanarat, K., Rejzek, M., O'Neill, E., Ruzanski, C., Hill, L., Fairhurst, S. A., Limpaseni, T., and Field, R. A. (2012) An expedient enzymatic route to isomeric 2-, 3-and 6-monodeoxy-monofluoro-maltose derivatives. Carbohydr. Res. 358, 12-18
19. Tagami, T., Tanaka, Y., Mori, H., Okuyama, M., and Kimura, A. (2013) Enzymatic synthesis of acarviosyl-maltooligosaccharides using disproportionating enzyme 1. Biosci. Biotechnol. Biochem. 77, 312-319
20. Kaper, T., Talik, B., Ettema, T. J., Bos, H., van der Maarel, M. J., and Dijkhuizen, L. (2005) Amylomaltase of Pyrobaculum aerophilum IM2 produces thermoreversible starch gels. Appl. Environ. Microbiol. 71, 5098-5106
21. Kaur, B., Ariffin, F., Bhat, R., and Karim, A. A. (2012) Progress in starch modification in the last decade. Food Hydrocolloids 26, 398-404
22. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
23. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., and Henrissat, B. (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490-D495
24. MacGregor, E. A. (2005) An overview of clan GH-H and distantly-related families. Biologia 60, 5-12
25. Przylas, I., Terada, Y., Fujii, K., Takaha, T., Saenger, W., and Sträter, N. (2000) X-ray structure of acarbose bound to amylomaltase from Thermus aquaticus: implications for the synthesis of large cyclic glucans. Eur. J. Biochem. 267, 6903-6913
26. Przylas, I., Tomoo, K., Terada, Y., Takaha, T., Fujii, K., Saenger, W., and Sträter, N. (2000) Crystal structure of amylomaltase from Thermus aquaticus, a glycosyltransferase catalysing the production of large cyclic glucans. J. Mol. Biol. 296, 873-886
27. Barends, T. R., Bultema, J. B., Kaper, T., van der Maarel, M. J., Dijkhuizen, L., and Dijkstra, B. W. (2007) Three-way stabilization of the covalent intermediate in amylomaltase, an α-amylase-like transglycosylase. J. Biol. Chem. 282, 17242-17249
28. Jung, J. H., Jung, T. Y., Seo, D. H., Yoon, S. M., Choi, H. C., Park, B. C., Park, C. S., and Woo, E. J. (2011) Structural and functional analysis of substrate recognition by the 250s loop in amylomaltase from Thermus brockianus. Proteins 79, 633-644
29. Weiss, S. C., Skerra, A., and Schiefner, A. (2015) Structural basis for the interconversion of maltodextrins by MalQ, the amylomaltase of Escherichia coli. J. Biol. Chem. 290, 21352-21364
30. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) in The Proteomics Protocols Handbook (Walker, J. M., ed) pp. 571-607, Humana Press, New York
31. Leslie, A. G. (2006) The integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 62, 48-57
32. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
33. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
34. Evans, P. R., and Murshudov, G. N. (2013)Howgood are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214
35. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
36. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
37. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
38. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
39. McNicholas, S., Potterton, E., Wilson, K. S., and Noble, M. E. (2011) Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr. D Biol. Crystallogr. 67, 386-394
40. McCranie, E. K., and Bachmann, B. O. (2014) Bioactive oligosaccharide natural products. Nat. Prod. Rep. 31, 1026-1042
41. Geng, P., Meng, X., Bai, G., and Luo, G. (2008) Profiling of acarviostatin family secondary metabolites secreted by Streptomyces coelicoflavus ZG0656 using ultraperformance liquid chromatography coupled with electrospray ionization mass spectrometry. Anal. Chem. 80, 7554-7561
42. Wierenga, R. K. (2001) The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Lett. 492, 193-198
43. Krissinel, E., and Henrick, K. (2005) in Computational Life Sciences (Berthold, M. R., Glen, R. C., Diederichs, K., Kohlbacher, O., and Fischer, I., eds) pp. 163-174, Springer-Verlag, Berlin
44. Syson, K., Stevenson, C. E., Rejzek, M., Fairhurst, S. A., Nair, A., Bruton, C. J., Field, R. A., Chater, K. F., Lawson, D. M., and Bornemann, S. (2011) Structure of Streptomyces maltosyltransferase GlgE, a homologue of a genetically validated anti-tuberculosis target. J. Biol. Chem. 286, 38298-38310
45. Hancock, R. D., and Tarbet, B. J. (2000) The other double helix: the fascinating chemistry of starch. J. Chem. Educ. 77, 988-992
46. Brzozowski, A. M., Lawson, D. M., Turkenburg, J. P., Bisgaard-Frantzen, H., Svendsen, A., Borchert, T. V., Dauter, Z., Wilson, K. S., and Davies, G. J. (2000) Structural analysis of a chimeric bacterial α-amylase: high-resolution analysis of native and ligand complexes. Biochemistry 39, 9099-9107
47. Tan, T. C., Mijts, B. N., Swaminathan, K., Patel, B. K., and Divne, C. (2008) Crystal structure of the polyextremophilic α-amylase AmyB from Halothermothrix orenii: details of a productive enzyme-substrate complex and an N domain with a role in binding raw starch. J. Mol. Biol. 378, 852-870
48. Mok, S. C., Teh, A. H., Saito, J. A., Najimudin, N., and Alam, M. (2013) Crystal structure of a compact α-amylase from Geobacillus thermoleovorans. Enzyme Microb. Technol. 53, 46-54
49. Davies, G. J., Brzozowski, A. M., Dauter, Z., Rasmussen, M. D., Borchert, T. V., and Wilson, K. S. (2005) Structure of a Bacillus halmapalus family 13α-amylase, BHA, in complex with an acarbose-derived nonasaccharide at 2.1 Å resolution. Acta Crystallogr. D Biol. Crystallogr. 61, 190-193
50. Lyhne-Iversen, L., Hobley, T. J., Kaasgaard, S. G., and Harris, P. (2006) Structure of Bacillus halmapalus α-amylase crystallized with and without the substrate analogue acarbose and maltose. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62, 849-854
51. Maurus, R., Begum, A., Williams, L. K., Fredriksen, J. R., Zhang, R., Withers, S. G., and Brayer, G. D. (2008) Alternative catalytic anions differentially modulate human α-amylase activity and specificity. Biochemistry 47, 3332-3344
52. Li, C., Begum, A., Numao, S., Park, K. H., Withers, S. G., and Brayer, G. D. (2005) Acarbose rearrangement mechanism implied by the kinetic and structural analysis of human pancreatic α-amylase in complex with analogues and their elongated counterparts. Biochemistry 44, 3347-3357
53. Uitdehaag, J. C., Mosi, R., Kalk, K. H., van der Veen, B. A., Dijkhuizen, L., Withers, S. G., and Dijkstra, B. W. (1999) X-ray structures along the reaction pathway of cyclodextrin glycosyltransferase elucidate catalysis in the α-amylase family. Nat. Struct. Biol. 6, 432-436
54. Cleland, W. W., Frey, P. A., and Gerlt, J. A. (1998) The low barrier hydrogen bond in enzymatic catalysis. J. Biol. Chem. 273, 25529-25532
55. Davies, G. J., Ducros, V. M., Varrot, A., and Zechel, D. L. (2003) Mapping the conformational itinerary of β-glycosidases by x-ray crystallography. Biochem. Soc. Trans. 31, 523-527
56. Withers, S. G., Rupitz, K., and Street, I. P. (1988) 2-Deoxy-2-fluoro-Dglycosyl fluorides. A new class of specific mechanism-based glycosidase inhibitors. J. Biol. Chem. 263, 7929-7932
57. Rempel, B. P., and Withers, S. G. (2008) Covalent inhibitors of glycosidases and their applications in biochemistry and biology. Glycobiology 18, 570-586
58. Syson, K., Stevenson, C. E., Rashid, A. M., Saalbach, G., Tang, M., Tuukkanen, A., Svergun, D. I., Withers, S. G., Lawson, D. M., and Bornemann, S. (2014) Structural insight into how Streptomyces coelicolor maltosyl transferase GlgE binds α-maltose 1-phosphate and forms a maltosyl-enzyme intermediate. Biochemistry 53, 2494-2504
59. Geng, P., Qiu, F., Zhu, Y., and Bai, G. (2008) Four acarviosin-containing oligosaccharides identified from Streptomyces coelicoflavus ZG0656 are potent inhibitors of α-amylase. Carbohydr. Res. 343, 882-892
60. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268
61. Robert, X., and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320-W324
62. Holm, L., and Sander, C. (1995) DALI: a network tool for protein structure comparison. Trends Biochem. Sci. 20, 478-480
63. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797