Remarkable evolutionary relatedness among the enzymes and proteins from the α-amylase family

Cellular and Molecular Life Sciences

Volumn 73, Issue 14, 2016, Pages 2707-2725

  Janeček, Štefan ^a,b   Gabriško, Marek ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b UNIVERSITY OF SS CYRIL AND METHODIUS IN TRNAVA   (Slovakia)

Author keywords

Evolutionary relatedness; Family GH77 amylomaltases of borrelian origin; Heavy chains of rBAT and 4F2 proteins; Plant and archaeal amylases; Amylase family GH13

Indexed keywords

4ALPHA GLUCANOTRANSFERASE; ALPHA GLUCOSIDASE; AMYLASE;

AMINO ACID SEQUENCE; ARCHAEON; BORRELIA; ENZYME CONFORMATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENETIC TREE; PROTEIN FAMILY; REVIEW; ANIMAL; ENZYMOLOGY; GENETICS; MOLECULAR MODEL; MULTIGENE FAMILY; PLANT;

ALPHA-AMYLASES; AMINO ACID SEQUENCE; ANIMALS; ARCHAEA; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; MULTIGENE FAMILY; PLANTS;

EID: 84966425270     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-016-2246-6     Document Type: Review

References (230)

1. Janecek S, Svensson B, MacGregor EA (2014) α-Amylase—an enzyme specificity found in various families of glycoside hydrolases. Cell Mol Life Sci 71:1149–1170
2. MacGregor EA (1988) α-Amylase structure and activity. J Protein Chem 7:399–415
3. Vihinen M, Mäntsälä P (1989) Microbial amylolytic enzymes. Crit Rev Biochem Mol Biol 24:329–418
4. Pandey A, Nigam P, Soccol CR, Soccol VT, Singh D, Mohan R (2000) Advances in microbial amylases. Biotechnol Appl Biochem 31:135–152
5. Søgaard M, Ji Abe, Martin-Eauclaire MF, Svensson B (1993) α-Amylases: structure and function. Carbohydr Polym 21:137–146
6. Gupta R, Gigras P, Mohapatra H, Kumar Goswami V, Chauhan B (2003) Microbial α-amylases: a biotechnological perspective. Process Biochem 38:1599–1616
7. Svensson B (1988) Regional distant sequence homology between amylases, α-glucosidases and transglucanosylases. FEBS Lett 230:72–76
8. MacGregor EA, Svensson B (1989) A super-secondary structure predicted to be common to several α-1,4-D-glucan-cleaving enzymes. Biochem J 259:145–152
9. Jespersen HM, MacGregor EA, Sierks MR, Svensson B (1991) Comparison of the domain-level organization of starch hydrolases and related enzymes. Biochem J 280:51–55
10. Uitdehaag JC, Mosi R, Kalk KH, van der Veen BA, Dijkhuizen L, Withers SG, Dijkstra BW (1999) X-ray structures along the reaction pathway of cyclodextrin glycosyltransferase elucidate catalysis in the α-amylase family. Nat Struct Biol 6:432–436
11. Kimura K, Kataoka S, Ishii Y, Takano T, Yamane K (1987) Nucleotide sequence of the β-cyclodextrin glucanotransferase gene of alkalophilic Bacillus sp. strain 1011 and similarity of its amino acid sequence to those of α-amylases. J Bacteriol 169:4399–4402
12. Janecek S, Svensson B, MacGregor EA (1995) Characteristic differences in the primary structure allow discrimination of cyclodextrin glucanotransferases from α-amylases. Biochem J 305:685–686
13. Itkor P, Tsukagoshi N, Udaka S (1990) Nucleotide sequence of the raw-starch-digesting amylase gene from Bacillus sp. B1018 and its strong homology to the cyclodextrin glucanotransferase genes. Biochem Biophys Res Commun 166:630–636
14. Bahl H, Burchhardt G, Spreinat A, Haeckel K, Wienecke A, Schmidt B, Antranikian G (1991) α-Amylase of Clostridium thermosulfurogenes EM1: nucleotide sequence of the gene, processing of the enzyme, and comparison of other α-amylases. Appl Environ Microbiol 57:1554–1559
15. del-Rio G, Morett E, Soberon X (1997) Did cyclodextrin glycosyltransferases evolve from α-amylases? FEBS Lett 416:221–224
16. Tsukamoto A, Kimura K, Ishii Y, Takano T, Yamane K (1988) Nucleotide sequence of the maltohexaose-producing amylase gene from an alkalophilic Bacillus sp. #707 and structural similarity to liquefying type α-amylases. Biochem Biophys Res Commun 151:25–31
17. Imanaka T, Kuriki T (1989) Pattern of action of Bacillus stearothermophilus neopullulanase on pullulan. J Bacteriol 171:369–374
18. Kuriki T, Imanaka T (1989) Nucleotide sequence of the neopullulanase gene from Bacillus stearothermophilus. J Gen Microbiol 135:1521–1528
19. Kuriki T, Takata H, Okada S, Imanaka T (1991) Analysis of the active center of Bacillus stearothermophilus neopullulanase. J Bacteriol 173:6147–6152
20. Takata H, Kuriki T, Okada S, Takesada Y, Iizuka M, Minamiura N, Imanaka T (1992) Action of neopullulanase. Neopullulanase catalyzes both hydrolysis and transglycosylation at α-(1,4)- and α-(1,6)-glucosidic linkages. J Biol Chem 267:18447–18452
21. MacGregor EA (1993) Relationships between structure and activity in the α-amylase family of starch-metabolising enzymes. Starch/Staerke 45:232–237
22. 8-barrel domain and evolutionary relationship to other amylolytic enzymes. J Protein Chem 12:791–805
23. Janecek S (1994) Parallel β/α-barrels of α-amylase, cyclodextrin glycosyltransferase and oligo-1,6-glucosidase versus the barrel of β-amylase: evolutionary distance is a reflection of unrelated sequences. FEBS Lett 353:119–123
24. Svensson B (1994) Protein engineering in the α-amylase family: catalytic mechanism, substrate specificity, and stability. Plant Mol Biol 25:141–157
25. Aghajari N, Roth M, Haser R (2002) Crystallographic evidence of a transglycosylation reaction: ternary complexes of a psychrophilic α-amylase. Biochemistry 41:4273–4280
26. Nakajima R, Imanaka T, Aiba S (1986) Comparison of amino acid sequences of eleven different α-amylases. Appl Microbiol Biotechnol 23:355–360
27. 8-barrel domains. Biochem J 288:1069–1070
28. Janecek S (1994) Sequence similarities and evolutionary relationships of microbial, plant and animal α-amylases. Eur J Biochem 224:519–524
29. 8-barrel glycosyl hydrolases suggested by the similarity of their fifth conserved sequence region. FEBS Lett 377:6–8
30. Janecek S (1997) α-Amylase family: molecular biology and evolution. Prog Biophys Mol Biol 67:67–97
31. MacGregor EA, Janecek S, Svensson B (2001) Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochim Biophys Acta 1546:1–20
32. Janecek S (2002) How many conserved sequence regions are there in the α-amylase family? Biologia 57(Suppl 11):29–41
33. Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316
34. Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 293:781–788
35. Henrissat B, Bairoch A (1996) Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316:695–696
36. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The carbohydrate-active enZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37:D233–D238
37. Lombard V, Ramulu GH, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucl Acids Res 42:D490–D495
38. Henrissat B, Davies GJ (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637–644
39. MacGregor EA, Jespersen HM, Svensson B (1996) A circularly permuted α-amylase-type α/β-barrel structure in glucan-synthesizing glucosyltransferases. FEBS Lett 378:263–266
40. Vujicic-Zagar A, Pijning T, Kralj S, Lopez CA, Eeuwema W, Dijkhuizen L, Dijkstra BW (2010) Crystal structure of a 117 kDa glucansucrase fragment provides insight into evolution and product specificity of GH70 enzymes. Proc Natl Acad Sci USA 107:21406–21411
41. Kralj S, Grijpstra P, van Leeuwen SS, Leemhuis H, Dobruchowska JM, van der Kaaij RM, Malik A, Oetari A, Kamerling JP, Dijkhuizen L (2011) 4,6-α-Glucanotransferase, a novel enzyme that structurally and functionally provides an evolutionary link between glycoside hydrolase enzyme families 13 and 70. Appl Environ Microbiol 77:8154–8163
42. Takaha T, Yanase M, Okada S, Smith SM (1993) Disproportionating enzyme (4-α-glucanotransferase; EC 2.4.1.25) of potato. Purification, molecular cloning, and potential role in starch metabolism. J Biol Chem 268:1391–1396
43. Terada Y, Fujii K, Takaha T, Okada S (1999) Thermus aquaticus ATCC 33923 amylomaltase gene cloning and expression and enzyme characterization: production of cycloamylose. Appl Environ Microbiol 65:910–915
44. Przylas I, Tomoo K, Terada Y, Takaha T, Fujii K, Saenger W, 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
45. Oslancova A, Janecek S (2002) Oligo-1,6-glucosidase and neopullulanase enzyme subfamilies from the α-amylase family defined by the fifth conserved sequence region. Cell Mol Life Sci 59:1945–1959
46. Stam MR, Danchin EG, Rancurel C, Coutinho PM, Henrissat B (2006) Dividing the large glycoside hydrolase family 13 into subfamilies:towards improved functional annotations of α-amylase-related proteins. Protein Eng Des Sel 19:555–562
47. Lei Y, Peng H, Wang Y, Liu Y, Han F, Xiao Y, Gao Y (2012) Preferential and rapid degradation of raw rice starch by an α-amylase of glycoside hydrolase subfamily GH13_37. Appl Microbiol Biotechnol 94:1577–1584
48. Majzlova K, Pukajova Z, Janecek S (2013) Tracing the evolution of the α-amylase subfamily GH13_36 covering the amylolytic enzymes intermediate between oligo-1,6-glucosidases and neopullulanases. Carbohydr Res 367:48–57
49. Janecek S, Kuchtova A, Petrovicova S (2015) A novel GH13 subfamily of α-amylases with a pair of tryptophans in the helix α3 of the catalytic TIM-barrel, the LPDlx signature in the conserved sequence region V and a conserved aromatic motif at the C-terminus. Biologia 70:1284–1294
50. Gabrisko M, Janecek S (2009) Looking for the ancestry of the heavy-chain subunits of heteromeric amino acid transporters rBAT and 4F2hc within the GH13 α-amylase family. FEBS J 276:7265–7278
51. Dong G, Vieille C, Savchenko A, Zeikus JG (1997) Cloning, sequencing, and expression of the gene encoding extracellular α-amylase from Pyrococcus furiosus and biochemical characterization of the recombinant enzyme. Appl Environ Microbiol 63:3569–3576
52. Jorgensen S, Vorgias CE, Antranikian G (1997) Cloning, sequencing, characterization, and expression of an extracellular α-amylase from the hyperthermophilic archaeon Pyrococcus furiosus in Escherichia coli and Bacillus subtilis. J Biol Chem 272:16335–16342
53. Jones RA, Jermiin LS, Easteal S, Patel BK, Beacham IR (1999) Amylase and 16S rRNA genes from a hyperthermophilic archaebacterium. J Appl Microbiol 86:93–107
54. Frillingos S, Linden A, Niehaus F, Vargas C, Nieto JJ, Ventosa A, Antranikian G, Drainas C (2000) Cloning and expression of α-amylase from the hyperthermophilic archaeon Pyrococcus woesei in the moderately halophilic bacterium Halomonas elongata. J Appl Microbiol 88:495–503
55. Leveque E, Haye B, Belarbi A (2000) Cloning and expression of an α-amylase encoding gene from the hyperthermophilic archaebacterium Thermococcus hydrothermalis and biochemical characterisation of the recombinant enzyme. FEMS Microbiol Lett 186:67–71
56. Rogers JC, Milliman C (1983) Isolation and sequence analysis of a barley α-amylase cDNA clone. J Biol Chem 258:8169–8174
57. Rogers JC (1985) Two barley α-amylase gene families are regulated differently in aleurone cells. J Biol Chem 260:3731–3738
58. Baulcombe DC, Huttly AK, Martienssen RA, Barker RF, Jarvis MG (1987) A novel wheat α-amylase gene (α-Amy3). Mol Gen Genet 209:33–40
59. Huang N, Sutliff TD, Litts JC, Rodriguez RL (1990) Plant Mol Biol 14:655–668
60. Young TE, DeMason DA, Close TJ (1994) Cloning of an α-amylase cDNA from aleurone tissue of germinating maize seed. Plant Physiol 105:759–760
61. Kadziola A, Abe J, Svensson B, Haser R (1994) Crystal and molecular structure of barley α-amylase. J Mol Biol 239:104–121
62. Kadziola A, Søgaard M, Svensson B, Haser R (1998) Molecular structure of a barley α-amylase-inhibitor complex:implications for starch binding and catalysis. J Mol Biol 278:205–217
63. Matsuura Y, Kusunoki M, Harada W, Kakudo M (1984) Structure and possible catalytic residues of Taka-amylase A. J Biochem 95:697–702
64. Swift HJ, Brady L, Derewenda ZS, Dodson EJ, Dodson GG, Turkenburg JP, Wilkinson AJ (1991) Structure and molecular model refinement of Aspergillus oryzae (TAKA) α-amylase: an application of the simulated-annealing method. Acta Crystallogr B 47:535–544
65. Boel E, Brady L, Brzozowski AM, Derewenda Z, Dodson GG, Jensen VJ, Petersen SB, Swift H, Thim L, Woldike HF (1990) Calcium binding in α-amylases: an X-ray diffraction study at 2.1-Å resolution of two enzymes from Aspergillus. Biochemistry 29:6244–6249
66. Brady RL, Brzozowski AM, Derewenda ZS, Dodson EJ, Dodson GG (1991) Solution of the structure of Aspergillus niger acid α-amylase by combined molecular replacement and multiple isomorphous replacement methods. Acta Crystallogr B 47:527–535
67. Buisson G, Duee E, Haser R, Payan F (1987) Three dimensional structure of porcine pancreatic α-amylase at 2.9 Å resolution. Role of calcium in structure and activity. EMBO J 6:3909–3916
68. Qian M, Haser R, Payan F (1993) Structure and molecular model refinement of pig pancreatic α-amylase at 2.1 Å resolution. J Mol Biol 231:785–799
69. Robert X, Haser R, Gottschalk TE, Ratajczak F, Driguez H, Svensson B, Aghajari N (2003) The structure of barley α-amylase isozyme 1 reveals a novel role of domain C in substrate recognition and binding: a pair of sugar tongs. Structure 11:973–984
70. Robert X, Haser R, Mori H, Svensson B, Aghajari N (2005) Oligosaccharide binding to barley α-amylase 1. J Biol Chem 280:32968–32978
71. Ochiai A, Sugai H, Harada K, Tanaka S, Ishiyama Y, Ito K, Tanaka T, Uchiumi T, Taniguchi M, Mitsui T (2014) Crystal structure of α-amylase from Oryza sativa: molecular insights into enzyme activity and thermostability. Biosci Biotechnol Biochem 78:989–997
72. Linden A, Mayans O, Meyer-Klaucke W, Antranikian G, Wilmanns M (2003) Differential regulation of a hyperthermophilic α-amylase with a novel (Ca, Zn) two-metal center by zinc. J Biol Chem 278:9875–9884
73. 8 scaffold. Mol Biol Evol 18:38–54
74. Da Lage JL, Feller G, Janecek S (2004) Horizontal gene transfer from Eukarya to bacteria and domain shuffling: the α-amylase model. Cell Mol Life Sci 61:97–109
75. van der Kaaij RM, Janecek S, van der Maarel MJ, Dijkhuizen L (2007) Phylogenetic and biochemical characterization of a novel cluster of intracellular fungal α-amylase enzymes. Microbiology 153:4003–4015
76. Godany A, Majzlova K, Horvathova V, Vidova B, Janecek S (2010) Tyrosine 39 of GH13 α-amylase from Thermococcus hydrothermalis contributes to its thermostability. Biologia 65:408–415
77. Hostinova E, Janecek S, Gasperik J (2010) Gene sequence, bioinformatics and enzymatic characterization of α-amylase from Saccharomycopsis fibuligera KZ. Protein J 29:355–364
78. Puspasari F, Radjasa O, Noer A, Nurachman Z, Syah Y, van der Maarel M, Dijkhuizen L, Janecek S, Natalia D (2013) Raw starch degrading α-amylase from Bacillus aquimaris MKSC 6.2: isolation and expression of the gene, bioinformatics and biochemical characterization of the recombinant enzyme. J Appl Microbiol 114:108–120
79. Janecek S, Leveque E, Belarbi A, Haye B (1999) Close evolutionary relatedness of α-amylases from Archaea and plants. J Mol Evol 48:421–426
80. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
81. Li C, Du M, Cheng B, Wang L, Liu X, Ma C, Yang C, Xu P (2014) Close relationship of a novel Flavobacteriaceae α-amylase with archaeal α-amylases and good potentials for industrial applications. Biotechnol Biofuels 7:18
82. Linden A, Wilmanns M (2004) Adaptation of class-13 α-amylases to diverse living conditions. ChemBioChem 5:231–239
83. Lim JK, Lee HS, Kim YJ, Bae SS, Jeon JH, Kang SG, Lee JH (2007) Critical factors to high thermostability of an α-amylase from hyperthermophilic archaeon Thermococcus onnurineus NA1. J Microbiol Biotechnol 17:1242–1248
84. Kobayashi T, Kanai H, Hayashi T, Akiba T, Akaboshi R, Horikoshi K (1992) Haloalkaliphilic maltotriose-forming α-amylase from the archaebacterium Natronococcus sp. strain Ah-36. J Bacteriol 174:3439–3444
85. Kobayashi T, Kanai H, Aono R, Horikoshi K, Kudo T (1994) Cloning, expression, and nucleotide sequence of the α-amylase gene from the haloalkaliphilic archaeon Natronococcus sp. strain Ah-36. J Bacteriol 176:5131–5134
86. Onodera M, Yatsunami R, Tsukimura W, Fukui T, Nakasone K, Takashina T, Nakamura S (2013) Gene analysis, expression, and characterization of an intracellular α-amylase from the extremely halophilic archaeon Haloarcula japonica. Biosci Biotechnol Biochem 77:281–288
87. Zorgani MA, Patron K, Desvaux M (2014) New insight in the structural features of haloadaptation in α-amylases from halophilic Archaea following homology modeling strategy: folded and stable conformation maintained through low hydrophobicity and highly negative charged surface. J Comput Aided Mol Des 28:721–734
88. Hutcheon GW, Vasisht N, Bolhuis A (2005) Characterisation of a highly stable α-amylase from the halophilic archaeon Haloarcula hispanica. Extremophiles 9:487–495
89. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371
90. Suvd D, Fujimoto Z, Takase K, Matsumura M, Mizuno H (2001) Crystal structure of Bacillus stearothermophilus α-amylase: possible factors determining the thermostability. J Biochem 129:461–468
91. Wells RG, Hediger MA (1992) Cloning of a rat kidney cDNA that stimulates dibasic and neutral amino acid transport and has sequence similarity to glucosidases. Proc Natl Acad Sci USA 89:5596–5600
92. Bertran J, Werner A, Moore ML, Stange G, Markovich D, Biber J, Testar X, Zorzano A, Palacin M, Murer H (1992) Expression cloning of a cDNA from rabbit kidney cortex that induces a single transport system for cystine and dibasic and neutrl amino acids. Proc Natl Acad Sci USA 89:5601–5605
93. Kuriki T, Imanaka T (1999) The concept of the α-amylase family: structural similarity and common catalytic mechanism. J Biosci Bioeng 87:557–565
94. Kuriki T, Takata H, Yanase M, Ohdan K, Fujii K, Terada Y, Takaha T, Hondoh H, Matsuura Y, Imanaka T (2006) The concept of the α-amylase family: a rational tool for interconverting glucanohydrolases/glucanotransferases, and their specificities. J Appl Glycosci 53:155–161
95. Janecek S, Svensson B, Henrissat B (1997) Domain evolution in the α-amylase family. J Mol Evol 45:322–331
96. Watanabe K, Hata Y, Kizaki H, Katsube Y, Suzuki Y (1997) The refined crystal structure of Bacillus cereus oligo-1,6-glucosidase at 2.0 Å resolution: structural characterization of proline-substitution sites for protein thermostabilization. J Mol Biol 269:142–153
97. Zhang D, Li N, Lok SM, Zhang LH, Swaminathan K (2003) Isomaltulose synthase (PalI) of Klebsiella sp. LX3. Crystal structure and implication of mechanism. J Biol Chem 278:35428–35434
98. Hondoh H, Saburi W, Mori H, Okuyama M, Nakada T, Matsuura Y, Kimura A (2008) Substrate recognition mechanism of α-1,6-glucosidic linkage hydrolyzing enzyme, dextran glucosidase from Streptococcus mutans. J Mol Biol 378:913–922
99. Shirai T, Hung VS, Morinaka K, Kobayashi T, Ito S (2008) Crystal structure of GH13 α-glucosidase GSJ from one of the deepest sea bacteria. Proteins 73:126–133
100. Kim JS, Cha SS, Kim HJ, Kim TJ, Ha NC, Oh ST, Cho HS, Cho MJ, Kim MJ, Lee HS, Kim JW, Choi KY, Park KH, Oh BH (1999) Crystal structure of a maltogenic amylase provides insights into a catalytic versatility. J Biol Chem 274:26279–26286
101. Lee HS, Kim MS, Cho HS, Kim JI, Kim TJ, Choi JH, Park C, Lee HS, Oh BH, Park KH (2002) Cyclomaltodextrinase, neopullulanase, and maltogenic amylase are nearly indistinguishable from each other. J Biol Chem 277:21891–21897
102. Hondoh H, Kuriki T, Matsuura Y (2003) Three-dimensional structure and substrate binding of Bacillus stearothermophilus neopullulanase. J Mol Biol 326:177–188
103. Fort J, de la Ballina LR, Burghardt HE, Ferrer-Costa C, Turnay J, Ferrer-Orta C, Uson I, Zorzano A, Fernandez-Recio J, Orozco M, Lizarbe MA, Fita I, Palacin M (2007) The structure of human 4F2hc ectodomain provides a model for homodimerization and electrostatic interaction with plasma membrane. J Biol Chem 282:31444–31452
104. Janecek S (2000) Proteins without enzymatic function with sequence relatedness to the α-amylase family. Trends Glycosci Glycotechnol 12:363–371
105. Broer S, Wagner CA (2002) Structure-function relationships of heterodimeric amino acid transporters. Cell Biochem Biophys 36:155–168
106. Hediger MA, Romero MF, Peng JB, Rolfs A, Takanaga H, Bruford EA (2004) The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteins. Pflug Arch 447:465–468
107. Palacin M, Nunes V, Font-Llitjos M, Jimenez-Vidal M, Fort J, Gasol E, Pineda M, Feliubadalo L, Chillaron J, Zorzano A (2005) The genetics of heteromeric amino acid transporters. Physiology 20:112–124
108. Chillaron J, Roca R, Valencia A, Zorzano A, Palacin M (2001) Heteromeric amino acid transporters: biochemistry, genetics, and physiology. Am J Physiol Renal Physiol 281:995–1018
109. Chillaron J, Font-Llitjos M, Fort J, Zorzano A, Goldfarb DS, Nunes V, Palacin M (2010) Pathophysiology and treatment of cystinuria. Nat Rev Nephrol 6:424–434
110. Bertran J, Werner A, Chillaron J, Nunes V, Biber J, Testar X, Zorzano A, Estivill X, Murer H, Palacin M (1993) Expression cloning of a human renal cDNA that induces high affinity transport of L-cystine shared with dibasic amino acids in Xenopus oocytes. J Biol Chem 268:14842–14849
111. Lee WS, Wells RG, Sabbag RV, Mohandas TK, Hediger MA (1993) Cloning and chromosomal localization of a human kidney cDNA involved in cystine, dibasic, and neutral amino acid transport. J Clin Invest 91:1959–1963
112. Reig N, Chillaron J, Bartoccioni P, Fernandez E, Bendahan A, Zorzano A, Kanner B, Palacin M, Bertran J (2002) The light subunit of system b0, + is fully functional in the absence of the heavy subunit. EMBO J 21:4906–4914
113. Fernandez E, Jimenez-Vidal M, Calvo M, Zorzano A, Tebar F, Palacin M, Chillaron J (2006) The structural and functional units of heteromeric amino acid transporters. The heavy subunit rBAT dictates oligomerization of the heteromeric amino acid transporters. J Biol Chem 281:26552–26556
114. Rosell A, Meury M, Alvarez-Marimon E, Costa M, Perez-Cano L, Zorzano A, Fernandez-Recio J, Palacin M, Fotiadis D (2014) Structural bases for the interaction and stabilization of the human amino acid transporter LAT2 with its ancillary protein 4F2hc. Proc Natl Acad Sci USA 111:2966–2971
115. Park KH, Kim TJ, Cheong TK, Kim JW, Oh BH, Svensson B (2000) Structure, specificity and function of cyclomaltodextrinase, a multispecific enzyme of the α-amylase family. Biochim Biophys Acta 1478:165–185
116. Jin X, Aimanova K, Ross LS, Gill SS (2003) Identification, functional characterization and expression of a LAT type amino acid transporter from the mosquito Aedes aegypti. Insect Biochem Mol Biol 33:815–827
117. Reynolds B, Roversi P, Laynes R, Kazi S, Boyd CA, Goberdhan DC (2009) Drosophila expresses a CD98 transporter with an evolutionarily conserved structure and amino acid-transport properties. Biochem J 420:363–372
118. Veljkovic E, Stasiuk S, Skelly PJ, Shoemaker CB, Verrey F (2004) Functional characterization of Caenorhabditis elegans heteromeric amino acid transporters. J Biol Chem 279:7655–7662
119. Krautz-Peterson G, Camargo S, Huggel K, Verrey F, Shoemaker CB, Skelly PJ (2007) Amino acid transport in schistosomes: characterization of the permease heavy chain SPRM1hc. J Biol Chem 282:21767–21775
120. Gabrisko M (2013) Evolutionary history of eukaryotic α-glucosidases from the α-amylase family. J Mol Evol 76:129–145
121. Verrey F, Jack DL, Paulsen IT, Saier MH Jr, Pfeiffer R (1999) New glycoprotein-associated amino acid transporters. J Membr Biol 172:181–192
122. Kuchtova A, Janecek S (2015) In silico analysis of family GH77 with focus on amylomaltases from borreliae and disproportionating enzymes DPE2 from plants and bacteria. Biochim Biophys Acta 1854:1260–1268
123. Smith AM, Zeeman SC, Thorneycroft D, Smith SM (2003) Starch mobilization in leaves. J Exp Bot 54:577–583
124. Kaper T, van der Maarel MJ, Euverink GJ, Dijkhuizen L (2004) Exploring and exploiting starch-modifying amylomaltases from thermophiles. Biochem Soc Trans 32:279–282
125. Pugsley AP, Dubreuil C (1988) Molecular characterization of malQ, the structural gene for the Escherichia coli enzyme amylomaltase. Mol Microbiol 2:473–479
126. Goda SK, Eissa O, Akhtar M, Minton NP (1997) Molecular analysis of a Clostridium butyricum NCIMB 7423 gene encoding 4-α-glucanotransferase and characterization of the recombinant enzyme produced in Escherichia coli. Microbiology 143:3287–3294
127. Bhuiyan SH, Kitaoka M, Hayashi K (2003) A cycloamylose-forming hyperthermostable 4-α-glucanotransferase of Aquifex aeolicus expressed in Escherichia coli. J Mol Catal B Enzym 22:45–53
128. Kaper T, Talik B, Ettema TJ, Bos H, van der Maarel MJ, Dijkhuizen L (2005) Amylomaltase of Pyrobaculum aerophilum IM2 produces thermoreversible starch gels. Appl Environ Microbiol 71:5098–5106
129. Godany A, Vidova B, Janecek S (2008) The unique glycoside hydrolase family 77 amylomaltase from Borrelia burgdorferi with only catalytic triad conserved. FEMS Microbiol Lett 284:84–91
130. Lee BH, Oh DK, Yoo SH (2009) Characterization of 4-α-glucanotransferase from Synechocystis sp. PCC 6803 and its application to various corn starches. N Biotechnol 26:29–36
131. Srisimarat W, Powviriyakul A, Kaulpiboon J, Krusong K, Zimmermann W, Pongsawasdi P (2011) A novel amylomaltase from Corynebacterium glutamicum and analysis of the large-ring cyclodextrin products. J Incl Phenom Macrocycl Chem 70:369–375
132. Hwang S, Choi KH, Kim J, Cha J (2013) Biochemical characterization of 4-α-glucanotransferase from Saccharophagus degradans 2-40 and its potential role in glycogen degradation. FEMS Microbiol Lett 344:145–151
133. Sawasdee S, Rudeekulthamrong P, Zimmermann W, Murakami S, Pongsawasdi P, Kaulpiboo J (2014) Direct cloning of gene encoding a novel amylomaltase from soil bacterial DNA for large-ring cyclodextrin production. Appl Biochem Microbiol 50:17–24
134. Wattebled F, Ral JP, Dauvillee D, Myers AM, James MG, Schlichting R, Giersch C, Ball SG, D’Hulst C (2003) STA11, a Chlamydomonas reinhardtii locus required for normal starch granule biogenesis, encodes disproportionating enzyme. Further evidence for a function of α-1,4 glucanotransferases during starch granule biosynthesis in green algae. Plant Physiol 132:137–145
135. Bresolin NS, Li Z, Kosar-Hashemi B, Tetlow IJ, Chatterjee M, Rahman S, Morell MK, Howitt CA (2006) Characterisation of disproportionating enzyme from wheat endosperm. Planta 224:20–31
136. van der Maarel MJ, van der Veen B, Uitdehaag JC, Leemhuis H, Dijkhuizen L (2002) Properties and applications of starch-converting enzymes of the α-amylase family. J Biotechnol 94:137–155
137. van der Maarel MJ, Leemhuis H (2013) Starch modification with microbial α-glucanotransferase enzymes. Carbohydr Polym 93:116–121
138. Ahmad N, Mehboob S, Rashid N (2015) Starch-processing enzymes– emphasis on thermostable 4-α-glucanotransferases. Biologia 70:709–725
139. Przylas I, Terada Y, Fujii K, Takaha T, Saenger W, 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
140. Barends TR, Bultema JB, Kaper T, van der Maarel MJ, Dijkhuizen L, Dijkstra BW (2007) Three-way stabilization of the covalent intermediate in amylomaltase, an α-amylase-like transglycosylase. J Biol Chem 282:17242–17249
141. Jung JH, Jung TY, Seo DH, Yoon SM, Choi HC, Park BC, Park CS, Woo EJ (2011) Structural and functional analysis of substrate recognition by the 250s loop in amylomaltase from Thermus brockianus. Proteins 79:633–644
142. Weiss SC, Skerra A, Schiefner A (2015) Structural basis for the interconversion of maltodextrins by MalQ, the amylomaltase of Escherichia coli. J Biol Chem 290:21352–21364
143. O’Neill EC, Stevenson CE, Tantanarat K, Latousakis D, Donaldson MI, Rejzek M, Nepogodiev SA, Limpaseni T, Field RA, Lawson DM (2015) Structural dissection of the maltodextrin disproportionation cycle of the Arabidopsis plastidial enzyme DPE1. J Biol Chem 290:29834–29853
144. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK, Gwinn M, Dougherty B, Tomb JF, Fleischmann RD, Richardson D, Peterson J, Kerlavage AR, Quackenbush J, Salzberg S, Hanson M, van Vugt R, Palmer N, Adams MD, Gocayne J, Weidman J, Utterback T, Watthey L, McDonald L, Artiach P, Bowman C, Garland S, Fuji C, Cotton MD, Horst K, Roberts K, Hatch B, Smith HO, Venter JC (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580–586
145. Machovic M, Janecek S (2003) The invariant residues in the α-amylase family: just the catalytic triad. Biologia 58:1127–1132
146. Hoon-Hanks LL, Morton EA, Lybecker MC, Battisti JM, Samuels DS, Drecktrah D (2012) Borrelia burgdorferi malQ mutants utilize disaccharides and traverse the enzootic cycle. FEMS Immunol Med Microbiol 66:157–165
147. Lloyd JR, Blennow A, Burhenne K, Kossmann J (2004) Repression of a novel isoform of disproportionating enzyme (stDPE2) in potato leads to inhibition of starch degradation in leaves but not tubers stored at low temperature. Plant Physiol 134:1347–1354
148. Lütken H, Lloyd JR, Glaring MA, Baunsgaard L, Laursen KH, Haldrup A, Kossmann J, Blennow A (2010) Repression of both isoforms of disproportionating enzyme leads to higher malto-oligosaccharide content and reduced growth in potato. Planta 232:1127–1139
149. Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37:853–863
150. Lu Y, Sharkey TD (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218:466–473
151. Steichen JM, Petty RV, Sharkey TD (2008) Domain characterization of a 4-α-glucanotransferase essential for maltose metabolism in photosynthetic leaves. J Biol Chem 283:20797–20804
152. Ruzanski C, Smirnova J, Rejzek M, Cockburn D, Pedersen HL, Pike M, Willats WG, Svensson B, Steup M, Ebenhöh O, Smith AM, Field RA (2013) A bacterial glucanotransferase can replace the complex maltose metabolism required for starch to sucrose conversion in leaves at night. J Biol Chem 288:28581–28598
153. Srisimarat W, Murakami S, Pongsawasdi P, Krusong K (2013) Crystallization and preliminary X-ray crystallographic analysis of the amylomaltase from Corynebacterium glutamicum. Acta Crystallogr, Sect F: Struct Biol Cryst Commun 69:1004–1006
154. Srisimarat W, Kaulpiboon J, Krusong K, Zimmermann W, Pongsawasdi P (2012) Altered large-ring cyclodextrin product profile due to a mutation at Tyr-172 in the amylomaltase of Corynebacterium glutamicum. Appl Environ Microbiol 78:7223–7228
155. Rachadech W, Nimpiboon P, Naumthong W, Nakapong S, Krusong K, Pongsawasdi P (2015) Identification of essential tryptophan in amylomaltase from Corynebacterium glutamicum. Int J Biol Macromol 76:230–235
156. D’Amico S, Gerday C, Feller G (2000) Structural similarities and evolutionary relationships in chloride-dependent α-amylases. Gene 253:95–105
157. Da Lage JL, Danchin EG, Casane D (2007) Where do animal α-amylases come from? An interkingdom trip. FEBS Lett 581:3927–3935
158. Sivakumar N, Li N, Tang JW, Patel BK, Swaminathan K (2006) Crystal structure of AmyA lacks acidic surface and provide insights into protein stability at poly-extreme condition. FEBS Lett 580:2646–2652
159. Møller MS, Fredslund F, Majumder A, Nakai H, Poulsen JC, Lo Leggio L, Svensson B, Abou Hachem M (2012) Enzymology and structure of the GH13_31 glucan 1,6-α-glucosidase that confers isomaltooligosaccharide utilization in the probiotic Lactobacillus acidophilus NCFM. J Bacteriol 194:4249–4259
160. Kobayashi M, Saburi W, Nakatsuka D, Hondoh H, Kato K, Okuyama M, Mori H, Kimura A, Yao M (2015) Structural insights into the catalytic reaction that is involved in the reorientation of Trp238 at the substrate-binding site in GH13 dextran glucosidase. FEBS Lett 589:484–489
161. Saburi W, Rachi-Otsuka H, Hondoh H, Okuyama M, Mori H, Kimura A (2015) Structural elements responsible for the glucosidic linkage-selectivity of a glycoside hydrolase family 13 exo-glucosidase. FEBS Lett 589:865–869
162. Møller MS, Henriksen A, Svensson B (2016) Structure and function of α-glucan debranching enzymes. Cell Mol Life Sci. doi:10.1007/s00018-016-2241-y
163. Okuyama M, Saburi W, Mori H, Kimura A (2016) α-Glucosidases and α-1,4-glucan lyases: structures, functions, and physiological actions. Cell Mol Life Sci. doi:10.1007/s00018-016-2247-5
164. Janecek S, Blesak K (2011) Sequence-structural features and evolutionary relationships of family GH57 α-amylases and their putative α-amylase-like homologues. Protein J 30:429–435
165. Blesak K, Janecek S (2012) Sequence fingerprints of enzyme specificities from the glycoside hydrolase family GH57. Extremophiles 16:497–506
166. Blesak K, Janecek S (2013) Two potentially novel amylolytic enzyme specificities in the prokaryotic glycoside hydrolase α-amylase family GH57. Microbiology 159:2584–2593
167. Janecek S, Kuchtova A (2012) In silico identification of catalytic residues and domain fold of the family GH119 sharing the catalytic machinery with the α-amylase family GH57. FEBS Lett 586:3360–3366
168. Passerini D, Vuillemin M, Ufarte L, Morel S, Loux V, Fontagné-Faucher C, Monsan P, Remaud-Simeon M, Moulis C (2015) Inventory of the GH70 enzymes encoded by Leuconostoc citreum NRRL B-1299—identification of three novel α-transglucosylases. FEBS J 282:2115–2130
169. Moulis C, André I, Remaud-Simeon M (2016) GH13 amylosucrases and GH70 branching sucrases, atypical enzymes in their respective families. Cell Mol Life Sci. doi:10.1007/s00018-016-2244-8
170. Meng X, Gangoiti J, Bai Y, Pijning T, Van Leeuwen SS, Dijkhuizen L (2016) Structure-function relationships of family GH70 glucansucrase and 4,6-α-glucanotransferase enzymes, and their evolutionary relationships with family GH13 enzymes. Cell Mol Life Sci. doi:10.1007/s00018-016-2245-7
171. Gangoiti J, Pijning T, Dijkhuizen L (2016) Biochemical characterization of the Exiguobacterium sibiricum 255-15 GtfC enzyme representing a novel glycoside hydrolase 70 subfamily of 4,6-α-glucanotransferase enzymes. Appl Environ Microbiol 82:756–766
172. Gangoiti J, van Leeuwen SS, Vafiadi C, Dijkhuizen L (2016) The Gram-negative bacterium Azotobacter chroococcum NCIMB 8003 employs a new glycoside hydrolase family 70 4,6-α-glucanotransferase enzyme (GtfD) to synthesize a reuteran like polymer from maltodextrins and starch. Biochim Biophys Acta 1860:1224–1236
173. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781
174. Machovic M, Janecek S (2006) Starch-binding domains in the post-genome era. Cell Mol Life Sci 63:2710–2724
175. Carvalho CC, Phan NN, Chen Y, Reilly PJ (2015) Carbohydrate-binding module tribes. Biopolymers 103:203–214
176. Christiansen C, Abou Hachem M, Janecek S, Viksø-Nielsen A, Blennow A, Svensson B (2009) The carbohydrate-binding module family 20—diversity, structure, and function. FEBS J 276:5006–5029
177. Janecek S, Svensson B, MacGregor EA (2011) Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals. Enzyme Microb Technol 49:429–440
178. Majzlova K, Janecek S (2014) Two structurally related starch-binding domain families CBM25 and CBM26. Biologia 69:1087–1096
179. Koropatkin NM, Smith TJ (2010) SusG: a unique cell-membrane-associated α-amylase from a prominent human gut symbiont targets complex starch molecules. Structure 18:200–215
180. Cameron EA, Maynard MA, Smith CJ, Smith TJ, Koropatkin NM, Martens EC (2012) Multidomain carbohydrate-binding proteins involved in Bacteroides thetaiotaomicron starch metabolism. J Biol Chem 287:34614–34625
181. Peng H, Zheng Y, Chen M, Wang Y, Xiao Y, Gao Y (2014) A starch-binding domain identified in α-amylase (AmyP) represents a new family of carbohydrate-binding modules that contribute to enzymatic hydrolysis of soluble starch. FEBS Lett 588:1161–1167
182. Xu J, Ren F, Huang CH, Zheng Y, Zhen J, Sun H, Ko TP, He M, Chen CC, Chan HC, Guo RT, Song H, Ma Y (2014) Functional and structural studies of pullulanase from Anoxybacillus sp. LM18-11. Proteins 82:1685–1693
183. Ze X, Ben David Y, Laverde-Gomez JA, Dassa B, Sheridan PO, Duncan SH, Louis P, Henrissat B, Juge N, Koropatkin NM, Bayer EA, Flint HJ (2015) Unique organization of extracellular amylases into amylosomes in the resistant starch-utilizing human colonic Firmicutes bacterium Ruminococcus bromii. MBio 6:e01058–e01115
184. Foley MH, Cockburn DW, Koropatkin NM (2016) The Sus operon: a model system for starch uptake by the human gut Bacteroidetes. Cell Mol Life Sci. doi:10.1007/s00018-016-2242-x
185. Pfister B, Zeeman SC (2016) Formation of starch in plant cells. Cell Mol Life Sci. doi:10.1007/s00018-016-2250-x
186. Niittyla T, Comparot-Moss S, Lue WL, Messerli G, Trevisan M, Seymour MD, Gatehouse JA, Villadsen D, Smith SM, Chen J, Zeeman SC, Smith AM (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J Biol Chem 281:11815–11818
187. Minassian BA, Ianzano L, Meloche M, Andermann E, Rouleau GA, Delgado-Escueta AV, Scherer SW (2000) Mutation spectrum and predicted function of laforin in Lafora’s progressive myoclonus epilepsy. Neurology 55:341–346
188. Ganesh S, Tsurutani N, Suzuki T, Hoshii Y, Ishihara T, Delgado-Escueta AV, Yamakawa K (2004) The carbohydrate-binding domain of Lafora disease protein targets Lafora polyglucosan bodies. Biochem Biophys Res Commun 313:1101–1109
189. Gentry MS, Dixon JE, Worby CA (2009) Lafora disease: insights into neurodegeneration from plant metabolism. Trends Biochem Sci 34:628–639
190. Gentry MS, Dowen RH 3rd, Worby CA, Mattoo S, Ecker JR, Dixon JE (2007) The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. J Cell Biol 178:477–488
191. Tagliabracci VS, Turnbull J, Wang W, Girard JM, Zhao X, Skurat AV, Delgado-Escueta AV, Minassian BA, Depaoli-Roach AA, Roach PJ (2007) Laforin is a glycogen phosphatase, deficiency of which leads to elevated phosphorylation of glycogen in vivo. Proc Natl Acad Sci USA 104:19262–19266
192. Gentry MS, Roma-Mateo C, Sanz P (2013) Laforin, a protein with many faces: glucan phosphatase, adapter protein, et alii. FEBS J 280:525–537
193. Raththagala M, Brewer MK, Parker MW, Sherwood AR, Wong BK, Hsu S, Bridges TM, Paasch BC, Hellman LM, Husodo S, Meekins DA, Taylor AO, Turner BD, Auger KD, Dukhande VV, Chakravarthy S, Sanz P, Woods VL Jr, Li S, Vander Kooi CW, Gentry MS (2015) Structural mechanism of laforin function in glycogen dephosphorylation and lafora disease. Mol Cell 57:261–272
194. Sankhala RS, Koksal AC, Ho L, Nitschke F, Minassian BA, Cingolani G (2015) Dimeric quaternary structure of human laforin. J Biol Chem 290:4552–4559
195. Kötting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, Chen J, Smith AM, Steup M, Ritte G, Zeeman SC (2009) STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21:334–346
196. Vander Kooi CW, Taylor AO, Pace RM, Meekins DA, Guo HF, Kim Y, Gentry MS (2010) Structural basis for the glucan phosphatase activity of starch excess4. Proc Natl Acad Sci USA 107:15379–15384
197. Emanuelle S, Brewer MK, Meekins DA, Gentry MS (2016) Unique carbohydrate binding platforms employed by the glucan phosphatases. Cell Mol Life Sci. doi:10.1007/s00018-016-2249-3
198. Hudson ER, Pan DA, James J, Lucocq JM, Hawley SA, Green KA, Baba O, Terashima T, Hardie DG (2003) A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr Biol 13:861–866
199. Polekhina G, Gupta A, Michell BJ, van Denderen B, Murthy S, Feil SC, Jennings IG, Campbell DJ, Witters LA, Parker MW, Kemp BE, Stapleton D (2003) AMPK β subunit targets metabolic stress sensing to glycogen. Curr Biol 13:867–871
200. Polekhina G, Gupta A, van Denderen BJ, Feil SC, Kemp BE, Stapleton D, Parker MW (2005) Structural basis for glycogen recognition by AMP-activated protein kinase. Structure 13:1453–1462
201. Emanuelle S, Hossain MI, Moller IE, Pedersen HL, van de Meene AM, Doblin MS, Koay A, Oakhill JS, Scott JW, Willats WG, Kemp BE, Bacic A, Gooley PR, Stapleton DI (2015) SnRK1 from Arabidopsis thaliana is an atypical AMPK. Plant J 82:183–192
202. Janecek S (2002) A motif of a microbial starch-binding domain found in human genethonin. Bioinformatics 18:1534–1537
203. Jiang S, Heller B, Tagliabracci VS, Zhai L, Irimia JM, DePaoli-Roach AA, Wells CD, Skurat AV, Roach PJ (2010) Starch binding domain-containing protein 1/genethonin 1 is a novel participant in glycogen metabolism. J Biol Chem 285:34960–34971
204. Palopoli N, Busi MV, Fornasari MS, Gomez-Casati D, Ugalde R, Parisi G (2006) Starch-synthase III family encodes a tandem of three starch-binding domains. Proteins 65:27–31
205. Gomez-Casati DF, Martín M, Busi MV (2013) Polysaccharide-synthesizing glycosyltransferases and carbohydrate binding modules: the case of starch synthase III. Protein Pept Lett 20:856–863
206. Barchiesi J, Hedin N, Gomez-Casati DF, Ballicora MA, Busi MV (2015) Functional demonstrations of starch binding domains present in Ostreococcus tauri starch synthases isoforms. BMC Res Notes 8:613
207. Mikkelsen R, Suszkiewicz K, Blennow A (2006) A novel type carbohydrate-binding module identified in α-glucan, water dikinases is specific for regulated plastidial starch metabolism. Biochemistry 45:4674–4682
208. Glaring MA, Baumann MJ, Abou Hachem M, Nakai H, Nakai N, Santelia D, Sigurskjold BW, Zeeman SC, Blennow A, Svensson B (2011) Starch-binding domains in the CBM45 family—low-affinity domains from glucan, water dikinase and α-amylase involved in plastidial starch metabolism. FEBS J 278:1175–1185
209. Hejazi M, Steup M, Fettke J (2012) The plastidial glucan, water dikinase (GWD) catalyses multiple phosphotransfer reactions. FEBS J 279:1953–1966
210. Orzechowski S, Grabowska A, Sitnicka D, Siminska J, Felus M, Dudkiewicz M, Fudali S, Sobczak M (2013) Analysis of the expression, subcellular and tissue localisation of phosphoglucan, water dikinase (PWD/GWD3) in Solanum tuberosum L.: a bioinformatics approach for the comparative analysis of two α-glucan, water dikinases (GWDs) from Solanum tuberosum L. Acta Physiol Plant 35:483–500
211. Mahlow S, Orzechowski S, Fettke J (2016) Starch phosphorylation: insights and perspectives. Cell Mol Life Sci. doi:10.1007/s00018-016-2248-4
212. Vu VV, Beeson WT, Span EA, Farquhar ER, Marletta MA (2014) A family of starch-active polysaccharide monooxygenases. Proc Natl Acad Sci USA 111:13822–13827
213. Lo Leggio L, Simmons TJ, Poulsen JC, Frandsen KE, Hemsworth GR, Stringer MA, von Freiesleben P, Tovborg M, Johansen KS, De Maria L, Harris PV, Soong CL, Dupree P, Tryfona T, Lenfant N, Henrissat B, Davies GJ, Walton PH (2015) Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase. Nat Commun 6:5961
214. Vu VV, Marletta MA (2016) Starch-degrading polysaccharide monooxygenases. Cell Mol Life Sci. doi:10.1007/s00018-016-2251-9
215. Cuyvers S, Dornez E, Delcour JA, Courtin CM (2012) Occurrence and functional significance of secondary carbohydrate binding sites in glycoside hydrolases. Crit Rev Biotechnol 32:93–107
216. Cockburn D, Wilkens C, Ruzanski C, Andersen S, Willum Nielsen J, Smith AM, Field RA, Willemoës M, Abou Hachem M, Svensson B (2014) Analysis of surface binding sites (SBSs) in carbohydrate active enzymes with focus on glycoside hydrolase families 13 and 77—a mini-review. Biologia 69:705–712
217. Ragunath C, Manuel SG, Venkataraman V, Sait HB, Kasinathan C, Ramasubbu N (2008) Probing the role of aromatic residues at the secondary saccharide-binding sites of human salivary α-amylase in substrate hydrolysis and bacterial binding. J Mol Biol 384:1232–1248
218. Cockburn D, Nielsen MM, Christiansen C, Andersen JM, Rannes JB, Blennow A, Svensson B (2015) Surface binding sites in amylase have distinct roles in recognition of starch structure motifs and degradation. Int J Biol Macromol 75:338–345
219. Suzuki E, Suzuki R (2016) Distribution of glucan-branching enzymes among prokaryotes. Cell Mol Life Sci. doi:10.1007/s00018-016-2243-9
220. Coutinho PM, Henrissat B (1999) Life with no sugars? J Mol Microbiol Biotechnol 1:307–308
221. UniProt Consortium (2015) UniProt: a hub for protein information. Nucleic Acids Res 43:D204–D212
222. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
223. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
224. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128
225. Deshpande N, Addess KJ, Bluhm WF, Merino-Ott JC, Townsend-Merino W, Zhang Q, Knezevich C, Xie L, Chen L, Feng Z, Green RK, Flippen-Anderson JL, Westbrook J, Berman HM, Bourne PE (2005) The RCSB Protein Data Bank: a redesigned query system and relational database based on the mmCIF schema. Nucl Acids Res 3:D233–D237
226. The PyMOL Molecular Graphics System, Version 1.7.4 Schrödinger, LLC
227. Shatsky M, Nussinov R, Wolfson HJ (2004) A method for simultaneous alignment of multiple protein structures. Proteins 56:143–156
228. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201
229. Davies GJ, Wilson KS, Henrissat B (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem J 321:557–559
230. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539