Isomerases for biotransformation of D-hexoses

Abstract

Monosaccharides are polyhydroxyl compounds containing several chiral carbons, giving rise to tens of isomeric forms. Only minority of them are natural carbohydrates existing in nature abundantly, and most of them are rarely in nature, called rare sugars. These rare sugars attract increasing attention because of their low-calorie property and promising beneficial effects. Izumoring strategy has been established for linking all monosaccharides by three types of enzymes including ketose 3-epimerases, polyol dehydrogenases, and aldose isomerases. Recently, more attention has been paid on the Izumoring of hexoses, especially the D-zone hexoses. So far, at least ten isomerases have been used for the isomerization reactions between D-aldohexoses and D-ketohexoses. In this article, the interconnections and potential physiological effects of D-ketohexoses and D-aldohexoses are summarized, the D-zone hexose Izumoring is shown by giving the exact biocatalysts, and importantly, the isomerases for D-hexose biotransformation are reviewed in detail.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Ahmed Z (2001) Production of natural and rare pentoses using microorganisms and their enzymes. Electron J Biotechnol l4:103–111

    Google Scholar 

  2. Allenza P, Morrell MJ, Detroy RW (1990) Conversion of mannose to fructose by immobilized mannose isomerase from Pseudomonas cepacia. Appl Biochem Biotechnol 24-25:171–182

    CAS  PubMed  Google Scholar 

  3. Anderson RL, Allison DP (1965) Purification and characterization of D-lyxose isomerase. J Biol Chem 240:2367–2372

    CAS  PubMed  Google Scholar 

  4. Armstrong LM, Luecke KJ, Bell LN (2009) Consumer evaluation of bakery product flavour as affected by incorporating the prebiotic tagatose. Int J Food Sci Technol 44:815–819

    CAS  Google Scholar 

  5. Beerens K, Desmet T, Soetaert W (2012) Enzymes for the biocatalytic productioin of rare sugars. J Ind Microbiol Biotechnol 39:823–834

    CAS  PubMed  Google Scholar 

  6. Bhosale SH, Rao MB, Deshpande VV (1996) Molecular and industrial aspects of glucose isomerase. Microbiol Rev 60:280–300

    CAS  PubMed Central  PubMed  Google Scholar 

  7. Bhuiyan SH, Itami Y, Izumori K (1997) Isolation of an L-rhamnose isomerase-constitutive mutant ofPseudomonas sp. strain LL172: purification and characterization of the enzyme. J Ferment Bioeng 84:319–323

    CAS  Google Scholar 

  8. Bhuiyan SH, Itami Y, Takada G, Izumori K (1999) Preparation of L-talose and D-gulose from L-tagatose and D-sorbose, respectively, using immobilized L-rhamnose isomerase. J Biosci Bioeng 88:567–570

    CAS  PubMed  Google Scholar 

  9. Brown SH, Sjoholm C, Kelly RM (1993) Purification and characterization of a highly thermostable glucose isomerase produced by the extremely thermophilic eubacterium, Thermotoga maritima. Biotechnol Bioeng 41:878–886

    CAS  PubMed  Google Scholar 

  10. Cheng L, Mu W, Jiang B (2010a) Thermostable L-arabinose isomerase from Bacillus stearothermophilus IAM 11001 for D-tagatose production: gene cloning, purification and characterisation. J Sci Food Agric 90:1327–1333

    CAS  PubMed  Google Scholar 

  11. Cheng L, Mu W, Zhang T, Jiang B (2010b) An L-arabinose isomerase from Acidothermus cellulolytics ATCC 43068: cloning, expression, purification, and characterization. Appl Microbiol Biotechnol 86:1089–1097

    CAS  PubMed  Google Scholar 

  12. Cho EA, Lee DW, Cha YH, Lee SJ, Jung HC, Pan JG, Pyun YR (2007) Characterization of a novel D-lyxose isomerase from Cohnella laevoribosii RI-39 sp. nov. J Bacteriol 189:1655–1663

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Choi JG, Hong SH, Kim YS, Kim KR, Oh DK (2012) Characterization of a recombinant thermostable D-lyxose isomerase from Dictyoglomus turgidum that produces D-lyxose from D-xylulose. Biotechnol Lett 34:1079–1085

    CAS  PubMed  Google Scholar 

  14. de Lonlay P, Seta N (2009) The clinical spectrum of phosphomannose isomerase deficiency, with an evaluation of mannose treatment for CDG-Ib. Biochim Biophys Acta Mol Basis Dis 1792:841–843

    Google Scholar 

  15. De Muynck C, Beauprez J, Soetaert W, Vandamme EJ (2006) Boric acid as a mobile phase additive for high performance liquid chromatography separation of ribose, arabinose and ribulose. J Chromatogr A 1101:115–121

    PubMed  Google Scholar 

  16. Edwards TE, Abramov AB, Smith ER, Baydo RO, Leonard JT, Leibly DJ, Thompkins KB, Clifton MC, Gardberg AS, Staker BL, Van Voorhis WC, Myler PJ, Stewart LJ (2011) Structural characterization of a ribose-5-phosphate isomerase B from the pathogenic fungus Coccidioides immitis. BMC Struct Biol 11:39

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Elliott SS, Keim NL, Stern JS, Teff K, Havel PJ (2002) Fructose, weight gain, and the insulin resistance syndrome. Am J Clin Nutr 76:911–922

    CAS  PubMed  Google Scholar 

  18. Fan C, Liu K, Zhang T, Zhou L, Xue D, Jiang B, Mu W (2014) Biochemical characterization of a thermostable l-arabinose isomerase from a thermoacidophilic bacterium, Alicyclobacillus hesperidum URH17-3-68. J Mol Catal B Enzym 102:120–126

    CAS  Google Scholar 

  19. Feng Z, Mu W, Jiang B (2013) Characterization of ribose-5-phosphate isomerase converting D-psicose to D-allose from Thermotoga lettingae TMO. Biotechnol Lett 35:719–724

    CAS  PubMed  Google Scholar 

  20. Friedman M (1996) Food browning and its prevention: an overview. J Agric Food Chem 44:631–653

    CAS  Google Scholar 

  21. Gao D, Kawai N, Nakamura T, Lu F, Fei Z, Tamiya T (2013) Anti-inflammatory effect of D-allose in cerebral ischemia/reperfusion injury in rats. Neurol Med Chir 53:365–374

    Google Scholar 

  22. Granstrom TB, Takata G, Tokuda M, Izumori K (2004) Izumoring: a novel and complete strategy for bioproduction of rare sugars. J Biosci Bioeng 97:89–94

    PubMed  Google Scholar 

  23. Hajer BH, Dorra ZA, Monia M, Samir B, Nushin A (2014) Probing the role of helixα1 in the acid-tolerance and thermal stability of the Streptomyces sp SK glucose isomerase by site-directed mutagenesis. J Biotechnol 173:1–6

    CAS  PubMed  Google Scholar 

  24. Hanover LM, White JS (1993) Manufacturing, composition, and applications of fructose. Am J Clin Nutr 58:724S–732S

    CAS  PubMed  Google Scholar 

  25. Hey-Ferguson A, Elbein AD (1970) Purification of a D-mannose isomerase from Mycobacterium smegmatis. J Bacteriol 101:777–780

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Hirose J, Maeda K, Yokoi H, Takasaki Y (2001) Purification and characterization of mannose isomerase from Agrobacterium radiobacter M-1. Biosci Biotechnol Biochem 65:658–661

    CAS  PubMed  Google Scholar 

  27. Hirose J, Kinoshita Y, Fukuyama S, Hayashi S, Yokoi H, Takasaki Y (2003) Continuous isomerization of D-fructose to D-mannose by immobilized Agrobacterium radiobacter cells. Biotechnol Lett 25:349–352

    CAS  PubMed  Google Scholar 

  28. Hossain MA, Wakabayashi H, Goda F, Kobayashi S, Maeba T, Maeta H (2000) Effect of the immunosuppressants FK506 and D-allose on allogenic orthotopic liver transplantation in rats. Transplant Proc 32:2021–2023

    CAS  PubMed  Google Scholar 

  29. Iida T, Kishimoto Y, Yoshikawa Y, Hayashi N, Okuma K, Tohi M, Yagi K, Matsuo T, Izumori K (2008) Acute D-psicose administration decreases the glycemic responses to an oral maltodextrin tolerance test in normal adults. J Nutr Sci Vitaminol (Tokyo) 54:511–514

    CAS  Google Scholar 

  30. Indo K, Hoshikawa H, Kamitori K, Yamaguchi F, Mori T, Tokuda M, Mori N (2014) Effects of D-allose in combination with docetaxel in human head and neck cancer cells. Int J Oncol 45:2044–2050

    CAS  PubMed  Google Scholar 

  31. Ishikawa K, Matsui I, Payan F, Cambillau C, Ishida H, Kawarabayasi Y, Kikuchi H, Roussel A (2002) A hyperthermostable D-ribose-5-phosphate isomerase from Pyrococcus horikoshii characterization and three-dimensional structure. Structure 10:877–886

    CAS  PubMed  Google Scholar 

  32. Itoh H, Okaya H, Khan AR, Tajima S, Hayakawa S, Izumori K (1994) Purification and characterization of D-tagatose 3-epimerase from Pseudomonas sp. ST-24. Biosci Biotechnol Biochem 58:2168–2171

    CAS  Google Scholar 

  33. Itoh T, Mikami B, Hashimoto W, Murata K (2008) Crystal structure of YihS in complex with D-mannose: structural annotation of Escherichia coli and Salmonella enterica yihS-encoded proteins to an aldose-ketose isomerase. J Mol Biol 377:1443–1459

    CAS  PubMed  Google Scholar 

  34. Izumori K (2002) Bioproduction strategies for rare hexose sugars. Naturwissenschaften 89:120–124

    CAS  PubMed  Google Scholar 

  35. Izumori K (2006) Izumoring: a strategy for bioproduction of all hexoses. J Biotechnol 124:717–722

    CAS  PubMed  Google Scholar 

  36. Jia M, Mu W, Chu F, Zhang X, Jiang B, Zhou LL, Zhang T (2014) A D-psicose 3-epimerase with neutral pH optimum from Clostridium bolteae for D-psicose production: cloning, expression, purification, and characterization. Appl Microbiol Biotechnol 98:717–725

    CAS  PubMed  Google Scholar 

  37. Ju YH, Oh DK (2010) Characterization of a recombinant L-fucose isomerase from Caldicellulosiruptor saccharolyticus that isomerizes L-fucose, D-arabinose, D-altrose, and L-galactose. Biotechnol Lett 32:299–304

    CAS  PubMed  Google Scholar 

  38. Jung WS, Singh RK, Lee JK, Pan CH (2013) Crystal structure and substrate specificity of D-galactose-6-phosphate isomerase complexed with substrates. PLoS One 8, e72902

    CAS  PubMed Central  PubMed  Google Scholar 

  39. Karaoglu H, Yanmis D, Sal FA, Celik A, Canakci S, Belduz AO (2013) Biochemical characterization of a novel glucose isomerase from Anoxybacillus gonensis G2(T) that displays a high level of activity and thermal stability. J Mol Catal B Enzym 97:215–224

    CAS  Google Scholar 

  40. Kasumi T, Mori S, Kaneko S, Matsumoto H, Kobayashi Y, Koyama Y (2014) Characterization of mannose isomerase from a cellulolytic Actinobacteria Thermobifida fusca MBL10003. J Appl Glycosci 61:21–25

    CAS  Google Scholar 

  41. Kim P (2004) Current studies on biological tagatose production using L-arabinose isomerase: a review and future perspective. Appl Microbiol Biotechnol 65:243–249

    CAS  PubMed  Google Scholar 

  42. Kim P, Yoon SH, Seo MJ, Oh DK, Choi JH (2001) Improvement of tagatose conversion rate by genetic evolution of thermostable galactose isomerase. Biotechnol Appl Biochem 34:99–102

    CAS  PubMed  Google Scholar 

  43. Kim BC, Lee YH, Lee HS, Lee DW, Choe EA, Pyun YR (2002) Cloning, expression and characterization of L-arabinose isomerase from Thermotoga neapolitana: bioconversion of D-galactose to D-tagatose using the enzyme. FEMS Microbiol Lett 212:121–126

    CAS  PubMed  Google Scholar 

  44. Kim HJ, Kim JH, Oh HJ, Oh DK (2006) Characterization of a mutated Geobacillus stearothermophilus L-arabinose isomerase that increases the production rate of D-tagatose. J Appl Microbiol 101:213–221

    CAS  PubMed  Google Scholar 

  45. Kim YS, Shin KC, Lim YR, Oh DK (2013) Characterization of a recombinant L-rhamnose isomerase from Dictyoglomus turgidum and its application for L-rhamnulose production. Biotechnol Lett 35:259–264

    CAS  PubMed  Google Scholar 

  46. Kim BJ, Hong SH, Shin KC, Jo YS, Oh DK (2014) Characterization of a F280N variant of L-arabinose isomerase from Geobacillus thermodenitrificans identified as a D-galactose isomerase. Appl Microbiol Biotechnol 98:9271–9281

    CAS  PubMed  Google Scholar 

  47. Kimura S, Zhang GX, Nishiyama A, Nagai Y, Nakagawa T, Miyanaka H, Fujisawa Y, Miyatake A, Nagai T, Tokuda M, Abe Y (2005) D-allose, an all-cis aldo-hexose, suppresses development of salt-induced hypertension in Dahl rats. J Hypertens 23:1887–1894

    CAS  PubMed  Google Scholar 

  48. Kluskens LD, Zeilstra J, Geerling ACM, de Vos WM, van der Oost J (2010) Molecular characterization of the glucose isomerase from the thermophilic bacterium Fervidobacterium gondwanense. Environ Technol 31:1083–1090

    CAS  PubMed  Google Scholar 

  49. Konak L, Kolcuoglu Y, Ozbek E, Colak A, Ergenoglu B (2014) Purification and characterization of an extremely stable glucose isomerase from Geobacillus thermodenitrificans TH2. Appl Biochem Microbiol 50:25–29

    CAS  Google Scholar 

  50. Korndorfer IP, Fessner WD, Matthews BW (2000) The structure of rhamnose isomerase from Escherichia coli and its relation with xylose isomerase illustrates a change between inter and intra-subunit complementation during evolution. J Mol Biol 300:917–933

    CAS  PubMed  Google Scholar 

  51. Korneeva OS, Cheremushkina IV, Glushchenko AS, Mikhailova NA, Baturo AP, Romanenko EE, Zlygostev SA (2012) Prebiotic properties of mannose and its effect on specific resistance. Zhurnal Mikrobiologii Eepidemiologii IImmunobiologii 5:67–70

    Google Scholar 

  52. Kwak JH, Kim MS, Lee JH, Yang YJ, Lee KH, Kim OY, Lee JH (2013) Beneficial effect of tagatose consumption on postprandial hyperglycemia in Koreans: a double-blind crossover designed study. Food Funct 4:1223–1228

    CAS  PubMed  Google Scholar 

  53. Kwon HJ, Yeom SJ, Park CS, Oh DK (2010) Substrate specificity of a recombinant D-lyxose isomerase from Providencia stuartii for monosaccharides. J Biosci Bioeng 110:26–31

    CAS  PubMed  Google Scholar 

  54. Leang K, Takada G, Fukai Y, Morimoto K, Granstrom TB, Izumori K (2004a) Novel reactions of L-rhamnose isomerase from Pseudomonas stutzeri and its relation with D-xylose isomerase via substrate specificity. Biochim Biophys Acta 1674:68–77

    CAS  PubMed  Google Scholar 

  55. Leang K, Takada G, Ishimura A, Okita M, Izumori K (2004b) Cloning, nucleotide sequence, and overexpression of the L-rhamnose isomerase gene from Pseudomonas stutzeri in Escherichia coli. Appl Environ Microbiol 70:3298–3304

    CAS  PubMed Central  PubMed  Google Scholar 

  56. Lee DW, Jang HJ, Choe EA, Kim BC, Lee SJ, Kim SB, Hong YH, Pyun YR (2004) Characterization of a thermostable L-arabinose (D-galactose) isomerase from the hyperthermophilic eubacterium Thermotoga maritima. Appl Environ Microbiol 70:1397–1404

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Lee YJ, Lee SJ, Kim SB, Lee SJ, Lee SH, Lee DW (2014) Structural insights into conserved L-arabinose metabolic enzymes reveal the substrate binding site of a thermophilic L-arabinose isomerase. FEBS Lett 588:1064–1070

    CAS  PubMed  Google Scholar 

  58. Lim YR, Oh DK (2011) Microbial metabolism and biotechnological production of D-allose. Appl Microbiol Biotechnol 91:229–235

    CAS  PubMed  Google Scholar 

  59. Lim BC, Kim HJ, Oh DK (2007) High production of D-tagatose by the addition of boric acid. Biotechnol Prog 23:824–828

    CAS  PubMed  Google Scholar 

  60. Lin CJ, Tseng WC, Lin TH, Liu SM, Tzou WS, Fang TY (2010) Characterization of a thermophilic L-rhamnose isomerase from Thermoanaerobacterium saccharolyticum NTOU1. J Agric Food Chem 58:10431–10436

    CAS  PubMed  Google Scholar 

  61. Lin CJ, Tseng WC, Fang TY (2011) Characterization of a thermophilic L-rhamnose isomerase from Caldicellulosiruptor saccharolyticus ATCC 43494. J Agric Food Chem 59:8702–8708

    CAS  PubMed  Google Scholar 

  62. Lu Y, Levin GV, Donner TW (2008) Tagatose, a new antidiabetic and obesity control drug. Diabetes Obes Metab 10:109–134

    CAS  PubMed  Google Scholar 

  63. Malm SW, Hanke NT, Gill A, Carbajal L, Baker AF (2015) The anti-tumor efficacy of 2-deoxyglucose and D-allose are enhanced with p38 inhibition in pancreatic and ovarian cell lines. J Exp Clin Cancer Res 34:31

    PubMed Central  PubMed  Google Scholar 

  64. Manjasetty BA, Chance MR (2006) Crystal structure of Escherichia coli L-arabinose isomerase (ECAI), the putative target of biological tagatose production. J Mol Biol 360:297–309

    CAS  PubMed  Google Scholar 

  65. Marles-Wright J, Lewis RJ (2011) The structure of a D-lyxose isomerase from the sigmaB regulon of Bacillus subtilis. Proteins 79:2015–2019

    CAS  PubMed  Google Scholar 

  66. Menavuvu BT, Poonperm W, Leang K, Noguchi N, Okada H, Morimoto K, Granstrom TB, Takada G, Izumori K (2006a) Efficient biosynthesis of D-allose from D-psicose by cross-linked recombinant L-rhamnose isomerase: separation of product by ethanol crystallization. J Biosci Bioeng 101:340–345

    CAS  PubMed  Google Scholar 

  67. Menavuvu BT, Poonperm W, Takeda K, Morimoto K, Granstrom TB, Takada G, Izumori K (2006b) Novel substrate specificity of D-arabinose isomerase from Klebsiella pneumoniae and its application to production of D-altrose from D-asicose. J Biosci Bioeng 102:436–441

    CAS  PubMed  Google Scholar 

  68. Moralejo P, Egan SM, Hidalgo E, Aguilar J (1993) Sequencing and characterization of a gene cluster encoding the enzymes for L-rhamnose metabolism in Escherichia coli. J Bacteriol 175:5585–5594

    CAS  PubMed Central  PubMed  Google Scholar 

  69. Mu W, Chu F, Xing Q, Yu S, Zhou L, Jiang B (2011) Cloning, expression, and characterization of a D-psicose 3-epimerase from Clostridium cellulolyticum H10. J Agric Food Chem 59:7785–7792

    CAS  PubMed  Google Scholar 

  70. Mu W, Wang X, Xue Q, Jiang B, Zhang T, Miao M (2012a) Characterization of a thermostable glucose isomerase with an acidic pH optimum from Acidothermus cellulolyticus. Food Res Int 47:364–367

    CAS  Google Scholar 

  71. Mu W, Zhang W, Feng Y, Jiang B, Zhou L (2012b) Recent advances on applications and biotechnological production of D-psicose. Appl Microbiol Biotechnol 94:1461–1467

    CAS  PubMed  Google Scholar 

  72. Mu W, Zhang W, Fang D, Zhou L, Jiang B, Zhang T (2013) Characterization of a D-psicose-producing enzyme, D-psicose 3-epimerase, from Clostridium sp. Biotechnol Lett 35:1481–1486

    CAS  PubMed  Google Scholar 

  73. Muniruzzaman S, Kobayashi H, Izumori K (1994) Production of D-talitol from D-tagatose by aureobasidium-pullulans strain 113B. J Ferment Bioeng 78:346–350

    CAS  Google Scholar 

  74. Nakamura T, Tanaka S, Hirooka K, Toyoshima T, Kawai N, Tamiya T, Shiraga F, Tokuda M, Keep RF, Itano T, Miyamoto O (2011) Anti-oxidative effects of D-allose, a rare sugar, on ischemia-reperfusion damage following focal cerebral ischemia in rat. Neurosci Lett 487:103–106

    CAS  PubMed  Google Scholar 

  75. Ochiai M, Onishi K, Yamada T, Iida T, Matsuo T (2014) D-Psicose increases energy expenditure and decreases body fat accumulation in rats fed a high-sucrose diet. Int J Food Sci Nutr 65:245–250

    CAS  PubMed  Google Scholar 

  76. Oh DK (2007) Tagatose: properties, applications, and biotechnological processes. Appl Microbiol Biotechnol 76:1–8

    CAS  PubMed  Google Scholar 

  77. Oyofo BA, Deloach JR, Corrier DE, Norman JO, Zippin RL, Mollenhauer HH (1989) Prevention of Salmonella typhimuriumcolonization of broilers with D-mannose. Poultry Sci 68:1357–1360

    CAS  Google Scholar 

  78. Palleroni NJ, Doudoroff M (1956) Mannose isomerase of Pseudomonas saccharophila. J Biol Chem 218:535–548

    CAS  PubMed  Google Scholar 

  79. Park CS (2014) Characterization of a recombinant L-rhamnose isomerase from Bacillus subtilis and its application on production of L-lyxose and L-mannose. Biotechnol Bioprocess Eng 19:18–25

    CAS  Google Scholar 

  80. Park CS, Yeom SJ, Kim HJ, Lee SH, Lee JK, Kim SW, Oh DK (2007a) Characterization of ribose-5-phosphate isomerase of Clostridium thermocellum producing D-allose from D-psicose. Biotechnol Lett 29:1387–1391

    CAS  PubMed  Google Scholar 

  81. Park HY, Park CS, Kim HJ, Oh DK (2007b) Substrate specificity of a galactose 6-phosphate isomerase from Lactococcus lactis that produces D-allose from D-psicose. J Biotechnol 132:88–95

    CAS  PubMed  Google Scholar 

  82. Park CS, Kwon HJ, Yeom SJ, Oh DK (2010a) Mannose production from fructose by free and immobilized D-lyxose isomerases from Providencia stuartii. Biotechnol Lett 32:1305–1309

    CAS  PubMed  Google Scholar 

  83. Park CS, Yeom SJ, Lim YR, Kim YS, Oh DK (2010b) Characterization of a recombinant thermostable L-rhamnose isomerase from Thermotoga maritima ATCC 43589 and its application in the production of L-lyxose and L-mannose. Biotechnol Lett 32:1947–1953

    CAS  PubMed  Google Scholar 

  84. Park CS, Yeom SJ, Lim YR, Kim YS, Oh DK (2010c) Substrate specificity of a recombinant D-lyxose isomerase from Serratia proteamaculans that produces D-lyxose and D-mannose. Lett Appl Microbiol 51:343–350

    CAS  PubMed  Google Scholar 

  85. Patel DH, Wi SG, Lee SG, Lee DS, Song YH, Bae HJ, Patel DH, Wi SG, Lee SG, Lee DS, Song YH, Bae HJ (2011) Substrate specificity of the Bacilluslicheniformis lyxose isomerase YdaE and its application in in vitro catalysis for bioproduction of lyxose and glucose by two-step isomerization. Appl Environ Microbiol 77:3343–3350

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Poonperm W, Takata G, Okada H, Morimoto K, Granstrom TB, Izumori K (2007) Cloning, sequencing, overexpression and characterization of L-rhamnose isomerase from Bacillus pallidus Y25 for rare sugar production. Appl Microbiol Biotechnol 76:1297–1307

    CAS  PubMed  Google Scholar 

  87. Prabhu P, Doan TN, Tiwari M, Singh R, Kim SC, Hong MK, Kang YC, Kang LW, Lee JK (2014) Structure-based studies on the metal binding of two-metal-dependent sugar isomerases. FEBS J 281:3446–3459

    CAS  PubMed  Google Scholar 

  88. Ryu SA, Kim CS, Kim HJ, Baek DH, Oh DK (2003) Continuous D-tagatose production by immobilized thermostable L-arabinose isomerase in a packed-bed bioreactor. Biotechnol Prog 19:1643–1647

    CAS  PubMed  Google Scholar 

  89. Sasahara H, Mine M, Izumori K (1998) Production of D-talitol from D-psicose by Candida famata R28. J Ferment Bioeng 85:84–88

    CAS  Google Scholar 

  90. Seemann JE, Schulz GE (1997) Structure and mechanism of L-fucose isomerase from Escherichia coli. J Mol Biol 273:256–268

    CAS  PubMed  Google Scholar 

  91. Sriprapundh D, Vieille C, Zeikus JG (2003) Directed evolution of Thermotoga neapolitana xylose isomerase: high activity on glucose at low temperature and low pH. Protein Eng 16:683–690

    CAS  PubMed  Google Scholar 

  92. Stevens F, Stevens P, Hovis J, Wu T (1981) Some properties of D-mannose isomerase from Escherichiacoli K12. J Gen Microbiol 124:219–223

    CAS  PubMed  Google Scholar 

  93. Sui L, Nomura R, Dong Y, Yamaguchi F, Izumori K, Tokuda M (2007) Cryoprotective effects of D-allose on mammalian cells. Cryobiology 55:87–92

    CAS  PubMed  Google Scholar 

  94. Suna S, Yamaguchi F, Kimura S, Tokuda M, Jitsunari F (2007) Preventive effect of D-psicose, one of rare ketohexoses, on di-(2-ethylhexyl) phthalate (DEHP)-induced testicular injury in rat. Toxicol Lett 173:107–117

    CAS  PubMed  Google Scholar 

  95. Takasaki Y (1967) Kinetic and equilibrium studies on D-mannose-D-fructose isomerization catalyzed by mannose isomerase from Streptomyces aerocolorigenes. Agric Biol Chem 31:435–440

    CAS  Google Scholar 

  96. Takasaki Y, Takano S (1964) Studies on the isomerization of sugars by bacteria. Agric Biol Chem 28:605–609

    CAS  Google Scholar 

  97. Takasaki Y, Hinoki K, Kataoka Y, Fukuyama S, Nishimura N, Hayashi S, Imada K (1993) Enzymatic production of D-mannose from D-fructose by mannose isomerase. J Ferment Bioeng 76:237–239

    CAS  Google Scholar 

  98. Takata MK, Yamaguchi F, Nakanose K, Watanabe Y, Hatano N, Tsukamoto I, Nagata M, Izumori K, Tokuda M (2005) Neuroprotective effect of D-psicose on 6-hydroxydopamine-induced apoptosis in rat pheochromocytoma (PC12) cells. J Biosci Bioeng 100:511–516

    CAS  PubMed  Google Scholar 

  99. Takata G, Uechi K, Taniguchi E, Kanbara Y, Yoshihara A, Morimoto K, Izumori K (2011) Characterization of Mesorhizobiumloti L-rhamnose isomerase and its application to L-talose production. Biosci Biotechnol Biochem 75:1006–1009

    CAS  PubMed  Google Scholar 

  100. Takeda K, Yoshida H, Izumori K, Kamitori S (2010) X-ray structures of Bacillus pallidus D-arabinose isomerase and its complex with L-fucitol. Biochim Biophys Acta 1804:1359–1368

    CAS  PubMed  Google Scholar 

  101. Uechi K, Takata G, Fukai Y, Yoshihara A, Morimoto K (2013) Gene cloning and characterization of L-ribulose 3-epimerase from Mesorhizobium loti and its application to rare sugar production. Biosci Biotechnol Biochem 77:511–515

    CAS  PubMed  Google Scholar 

  102. van Staalduinen LM, Park CS, Yeom SJ, Adams-Cioaba MA, Oh DK, Jia Z (2010) Structure-based annotation of a novel sugar isomerase from the pathogenic E. coli O157:H7. J Mol Biol 401:866–881

    PubMed  Google Scholar 

  103. Xu Z, Li S, Feng X, Liang J, Xu H (2014a) L-Arabinose isomerase and its use for biotechnological production of rare sugars. Appl Microbiol Biotechnol 98:8869–8878

    CAS  PubMed  Google Scholar 

  104. Xu Z, Li S, Feng XH, Zhan YJ, Xu H (2014b) Function of aspartic acid residues in optimum pH control of L-arabinose isomerase from Lactobacillus fermentum. Appl Microbiol Biotechnol 98:3987–3996

    CAS  PubMed  Google Scholar 

  105. Yamada T, Hayashi N, Iida T, Takamine S, Okuma K, Matsuo T (2014) Dietary D-sorbose decreases serum insulin levels in growing sprague-dawley rats. J Nutr Sci Vitaminol 60:297–299

    CAS  PubMed  Google Scholar 

  106. Yeom SJ, Ji JH, Kim NH, Park CS, Oh DK (2009a) Substrate specificity of a mannose-6-phosphate isomerase from Bacillus subtilis and its application in the production of L-ribose. ApplEnviron Microbiol 75:4705–4710

    CAS  Google Scholar 

  107. Yeom SJ, Kim NH, Yoon RY, Kwon HJ, Park CS, Oh DK (2009b) Characterization of a mannose-6-phosphate isomerase from Geobacillus thermodenitrificans that converts monosaccharides. Biotechnol Lett 31:1273–1278

    CAS  PubMed  Google Scholar 

  108. Yeom SJ, Kim BN, Park CS, Oh DK (2010) Substrate specificity of ribose-5-phosphate isomerases from Clostridium difficile and Thermotoga maritima. Biotechnol Lett 32:829–835

    CAS  PubMed  Google Scholar 

  109. Yeom SJ, Seo ES, Kim YS, Oh DK (2011) Increased D-allose production by the R132E mutant of ribose-5-phosphate isomerase from Clostridium thermocellum. Appl Microbiol Biotechnol 89:1859–1866

    CAS  PubMed  Google Scholar 

  110. Yoon RY, Yeom SJ, Kim HJ, Oh DK (2009) Novel substrates of a ribose-5-phosphate isomerase from Clostridium thermocellum. J Biotechnol 139:26–32

    CAS  PubMed  Google Scholar 

  111. Yoshida H, Yamada M, Ohyama Y, Takada G, Izumori K, Kamitori S (2007) The structures of L-rhamnose isomerase from Pseudomonas stutzeri in complexes with L-rhamnose and D-allose provide insights into broad substrate specificity. J Mol Biol 365:1505–1516

    CAS  PubMed  Google Scholar 

  112. Yoshihara K, Shinohara Y, Hirotsu T, Izumori K (2006) Bioconversion of D-psicose to D-tagatose and D-talitol by Mucoraceae fungi. J Biosci Bioeng 101:219–222

    CAS  PubMed  Google Scholar 

  113. Zhang R, Andersson CE, Savchenko A, Skarina T, Evdokimova E, Beasley S, Arrowsmith CH, Edwards AM, Joachimiak A, Mowbray SL (2003) Structure of Escherichia coli ribose-5-phosphate isomerase: a ubiquitous enzyme of the pentose phosphate pathway and the Calvin cycle. Struct 11:31–42

    CAS  Google Scholar 

  114. Zhang L, Mu W, Jiang B, Zhang T (2009) Characterization of D-tagatose-3-epimerase from Rhodobacter sphaeroides that converts D-fructose into D-psicose. Biotechnol Lett 31:857–862

    CAS  PubMed  Google Scholar 

  115. Zhang W, Fang D, Xing Q, Zhou L, Jiang B, Mu W (2013a) Characterization of a novel metal-dependent D-psicose 3-epimerase from Clostridium scindens 35704. PLoS ONE 8, e62987

    CAS  PubMed Central  PubMed  Google Scholar 

  116. Zhang W, Fang D, Zhang T, Zhou L, Jiang B, Mu W (2013b) Characterization of a metal-dependent d-psicose 3-epimerase from a novel strain, Desmospora sp. 8437. J Agric Food Chem 61:11468–11476

    CAS  PubMed  Google Scholar 

  117. Zhang W, Zhang T, Jiang B, Mu W (2015) Biochemical characterization of a D-psicose 3-epimerase from Treponema primitia ZAS-1 and its application on enzymatic production of D-psicose. J Sci Food AgricDOI:. doi:10.1002/jsfa.7187

    Google Scholar 

  118. Zhou H, Cheng JS, Wang BL, Fink GR, Stephanopoulos G (2012) Xylose isomerase overexpression along with engineering of the pentose phosphate pathway and evolutionary engineering enable rapid xylose utilization and ethanol production by Saccharomyces cerevisiae. MetabEng 14:611–622

    CAS  Google Scholar 

  119. Zhu Y, Men Y, Bai W, Li X, Zhang L, Sun Y, Ma Y (2012) Overexpression of D-psicose 3-epimerase from Ruminococcus sp. in Escherichia coli and its potential application in D-psicose production. Biotechnol Lett 34:1901–1906

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the NSFC Project (Nos. 21276001 and 31171705), the 863 Project (No. 2013AA102102), the Fundamental Research Funds for the Central Universities (No. JUSRP51304A), and the Support Project of Jiangsu Province (No. BK20130001).

Conflict of interest

The authors declare that they have no conflict of interest.

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Wanmeng Mu.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mu, W., Yu, L., Zhang, W. et al. Isomerases for biotransformation of D-hexoses. Appl Microbiol Biotechnol 99, 6571–6584 (2015). https://doi.org/10.1007/s00253-015-6788-6

Download citation

Keywords

  • Aldose isomerase
  • Biotransformation
  • Hexose
  • Monosaccharide
  • Rare sugar