Recent research on the physiological functions, applications, and biotechnological production of d-allose

  • Ziwei Chen
  • Jiajun Chen
  • Wenli Zhang
  • Tao Zhang
  • Cuie Guang
  • Wanmeng Mu
Mini-Review
  • 62 Downloads

Abstract

d-Allose is a rare monosaccharide, which rarely appears in the natural environment. d-Allose has an 80% sweetness relative to table sugar but is ultra-low calorie and non-toxic and is thus an ideal candidate to take the place of table sugar in food products. It displays unique health benefits and physiological functions in various fields, including food systems, clinical treatment, and the health care fields. However, it is difficult to produce chemically. The biotechnological production of d-allose has become a research hotspot in recent years. Therefore, an overview of recent studies on the physiological functions, applications, and biotechnological production of d-allose is presented. In this review, the physiological functions of d-allose are introduced in detail. In addition, the different types of d-allose-producing enzymes are compared for their enzymatic properties and for the biotechnological production of d-allose. To date, very little information is available on the molecular modification and food-grade expression of d-allose-producing enzymes, representing a very large research space yet to be explored.

Keywords

d-Allose Physiological function Application Biological production 

Notes

Acknowledgements

This work was supported by the Support Project of Jiangsu Province (No. 2015-SWYY-009).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

References

  1. Angyal SJ (1994) The composition of reducing sugars in dimethyl sulfoxide solution. Carbohydr Res 263(1):1–11CrossRefGoogle Scholar
  2. Bai W, Shen J, Zhu Y, Men Y, Sun Y, Ma Y (2015) Characteristics and kinetic properties of L-rhamnose isomerase from Bacillus subtilis by isothermal titration calorimetry for the production of D-allose. Food Sci Technol Res 21(1):13–22CrossRefGoogle Scholar
  3. Bernaerts MJ, Furnelle J, De LJ (1963) The preparation of some new disaccharides and D-allose from 3-ketoglycosides. Biochim Biophys Acta 69(2):322–330CrossRefPubMedGoogle Scholar
  4. Chari VM, Grayer-Barkmeijer RJ, Harborne JB, Österdahl B-G (1981) An acylated allose-containing 8-hydroxyflavone glycoside from Veronica filiformis. Phytochemistry 20(8):1977–1979CrossRefGoogle Scholar
  5. Chen Z, Xu W, Zhang W, Zhang T, Jiang B, Mu W (2017) Characterization of a thermostable recombinant L-rhamnose isomerase from Caldicellulosiruptor obsidiansis OB47 and its application for the production of L-fructose and L-rhamnulose. J Sci Food Agric.  https://doi.org/10.1002/jsfa.8703
  6. 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(5):719–724CrossRefPubMedGoogle Scholar
  7. 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 (Tokyo) 53(6):365–374CrossRefGoogle Scholar
  8. Gao D, Kawai N, Tamiya T (2011) The anti-inflammatory effects of D-allose contribute to attenuation of cerebral ischemia–reperfusion injury. Med Hypotheses 76(6):911–913CrossRefPubMedGoogle Scholar
  9. Harada M, Kondo E, Hayashi H, Suezawa C, Suguri S, Arai M (2012) D-Allose and D-psicose reinforce the action of metronidazole on trichomonad. Parasitol Res 110(4):1565–1567CrossRefPubMedGoogle Scholar
  10. Hayashi N, Iida T, Yamada T, Okuma K, Takehara I, Yamamoto T, Yamada K, Tokuda M (2010) Study on the postprandial blood glucose suppression effect of D-psicose in borderline diabetes and the safety of long-term ingestion by normal human subjects. Biosci Biotechnol Biochem 74(3):510–519CrossRefPubMedGoogle Scholar
  11. Herber RR, Maher GF, Arnold EC, Lorsbach TW (1995) Preparation of high purity D-allose from D-glucose. US Patent No. 5433793Google Scholar
  12. Hirata Y, Saito M, Tsukamoto I, Yamaguchi F, Sui L, Kamitori K, Dong Y, Uehara E, Konishi R, Janjua N (2009) Analysis of the inhibitory mechanism of D-allose on MOLT-4F leukemia cell proliferation. J Biosci Bioeng 107(5):562–568CrossRefPubMedGoogle Scholar
  13. Hoshikawa H, Indo K, Mori T, Mori N (2011) Enhancement of the radiation effects by D-allose in head and neck cancer cells. Cancer Lett 306(1):60–66CrossRefPubMedGoogle Scholar
  14. Hoshikawa H, Mori T, Mori N (2010) In vitro and in vivo effects of D-allose: up-regulation of thioredoxin-interacting protein in head and neck cancer cells. Ann Otol Rhinol Laryngol 119(8):567–571CrossRefPubMedGoogle Scholar
  15. Hossain M, 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 32:2021–2023CrossRefPubMedGoogle Scholar
  16. Huang T, Gao D, Hei Y, Zhang X, Chen X, Fei Z (2016) D-Allose protects the blood brain barrier through PPAR gamma-mediated anti-inflammatory pathway in the mice model of ischemia reperfusion injury. Brain Res 1642:478–486CrossRefPubMedGoogle Scholar
  17. Iga Y, Nakamichi K, Shirai Y, Matsuo T (2010) Acute and sub-chronic toxicity of D-allose in rats. Biosci Biotechnol Biochem 74(7):1476–1478CrossRefPubMedGoogle Scholar
  18. 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(5):2044–2050CrossRefPubMedGoogle Scholar
  19. Ishihara Y, Katayama K, Sakabe M, Kitamura M, Aizawa M, Takara M, Itoh K (2011) Antioxidant properties of rare sugar D-allose: effects on mitochondrial reactive oxygen species production in Neuro2A cells. J Biosci Bioeng 112(6):638–642CrossRefPubMedGoogle Scholar
  20. Izumori K (2002) Bioproduction strategies for rare hexose sugars. Naturwissenschaften 89(3):120–124CrossRefPubMedGoogle Scholar
  21. Izumori K (2006) Izumoring: a strategy for bioproduction of all hexoses. J Biotechnol 124(4):717–722CrossRefPubMedGoogle Scholar
  22. Jensen SR, Mikkelsen CB, Nielsen BJ (1981) Iridoid mono-and di-glycosides in Mentzelia. Phytochemistry 20(1):71–83CrossRefGoogle Scholar
  23. Jeong RU, Lim S, Kim MO, Moon MH (2011) Effect of D-allose on prostate cancer cell lines: phospholipid profiling by nanoflow liquid chromatography-tandem mass spectrometry. Anal Bioanal Chem 401(2):689–698CrossRefPubMedGoogle Scholar
  24. Köpper S, Freimund S (2003) The composition of keto aldoses in aqueous solution as determined by NMR spectroscopy. Helv Chim Acta 86(3):827–843CrossRefGoogle Scholar
  25. Kannan RRR, Arumugam R, Anantharaman P (2012) Chemical composition and antibacterial activity of Indian seagrasses against urinary tract pathogens. Food Chem 135(4):2470–2473CrossRefGoogle Scholar
  26. Kano A, Fukumoto T, Ohtani K, Yoshihara A, Ohara T, Tajima S, Izumori K, Tanaka K, Ohkouchi T, Ishida Y, Nishizawa Y, Ichimura K, Tada Y, Gomi K, Akimitsu K (2013) The rare sugar D-allose acts as a triggering molecule of rice defence via ROS generation. J Exp Bot 64(16):4939–4951CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kashiwagi H, Asano E, Noguchi C, Sui L, Hossain A, Akamoto S, Okano K, Tokuda M, Suzuki Y (2016) Beneficial effect of D-allose for isolated islet culture prior to islet transplantation. J Hepatobiliary Pancreat Sci 23(1):37–42CrossRefPubMedGoogle Scholar
  28. 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(2):259–264CrossRefPubMedGoogle Scholar
  29. Kimura S, Zhang G-X, Nishiyama A, Nagai Y, Nakagawa T, Miyanaka H, Fujisawa Y, Miyatake A, Nagai T, Tokuda M (2005) D-Allose, an all-cis aldo-hexose, suppresses development of salt-induced hypertension in Dahl rats. J Hypertens 23(10):1887–1894CrossRefPubMedGoogle Scholar
  30. Kozakai T, Fukada K, Kuwatori R, Ishii T, Senoo T, Izumori K (2015) Aqueous phase behavior of the rare monosaccharide D-allose and X-ray crystallographic analysis of D-allose dihydrate. B Chem Soc Jpn 88(3):465–470CrossRefGoogle Scholar
  31. Leang K, Takada G, Fukai Y, Morimoto K, Granstrom TB, Izumori K (2004) Novel reactions of L-rhamnose isomerase from Pseudomonas stutzeri and its relation with D-xylose isomerase via substrate specificity. Biochim Biophys Acta 1674(1):68–77CrossRefPubMedGoogle Scholar
  32. Lin C-J, Tseng W-C, Lin T-H, Liu S-M, Tzou W-S, Fang T-Y (2010) Characterization of a thermophilic L-rhamnose isomerase from Thermoanaerobacterium saccharolyticum NTOU1. J Agric Food Chem 58(19):10431–10436CrossRefPubMedGoogle Scholar
  33. Lin CJ, Tseng WC, Fang TY (2011) Characterization of a thermophilic L-rhamnose isomerase from Caldicellulosiruptor saccharolyticus ATCC 43494. J Agric Food Chem 59(16):8702–8708CrossRefPubMedGoogle Scholar
  34. 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(1):31CrossRefPubMedPubMedCentralGoogle Scholar
  35. Matsuo T, Baba Y, Hashiguchi M, Takeshita K, Izumori K, Suzuki H (2001) Dietary D-psicose, a C-3 epimer of D-fructose, suppresses the activity of hepatic lipogenic enzymes in rats. Asia Pac J Clin Nutr 10(3):233–237CrossRefPubMedGoogle Scholar
  36. Menavuvu BT, Poonperm W, Leang K, Noguchi N, Okada H, Morimoto K, Granström TB, Takada G, Izumori K (2006) 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(4):340–345CrossRefPubMedGoogle Scholar
  37. Miyawaki Y, Ueki M, Ueno M, Asaga T, Tokuda M, Shirakami G (2012) D-Allose ameliorates cisplatin-induced nephrotoxicity in mice. Tohoku J Exp Med 228(3):215–221CrossRefPubMedGoogle Scholar
  38. Moller D, Berger J (2003) Role of PPARs in the regulation of obesity-related insulin sensitivity and inflammation. Int J Obes 27(S3):S17–S21CrossRefGoogle Scholar
  39. Mooradian AD, Smith M, Tokuda M (2017) The role of artificial and natural sweeteners in reducing the consumption of table sugar: a narrative review. Clin Nutr Espen 18:1–8CrossRefPubMedGoogle Scholar
  40. Morimoto K, Park C-S, Ozaki M, Takeshita K, Shimonishi T, Granström TB, Takata G, Tokuda M, Izumori K (2006) Large scale production of D-allose from D-psicose using continuous bioreactor and separation system. Enzym Microb Technol 38(6):855–859CrossRefGoogle Scholar
  41. Mu W, Zhang W, Feng Y, Jiang B, Zhou L (2012) Recent advances on applications and biotechnological production of D-psicose. Appl Microbiol Biotechnol 94(6):1461–1467CrossRefPubMedGoogle Scholar
  42. Murata A, Sekiya K, Watanabe Y, Yamaguchi F, Hatano N, Izumori K, Tokuda M (2003) A novel inhibitory effect of D-allose on production of reactive oxygen species from neutrophils. J Biosci Bioeng 96(1):89–91CrossRefPubMedGoogle Scholar
  43. Naha N, Lee HY, Jo MJ, Chung BC, Kim SH, Kim MO (2008) Rare sugar D-allose induces programmed cell death in hormone refractory prostate cancer cells. Apoptosis 13(9):1121–1134CrossRefPubMedGoogle Scholar
  44. Nakamura T, Tanaka S, Hirooka K, Toyoshima T, Kawai N, Tamiya T, Shiraga F, Tokuda M, Keep RF, Itano T (2011) Anti-oxidative effects of D-allose, a rare sugar, on ischemia–reperfusion damage following focal cerebral ischemia in rat. Neurosci Lett 487(1):103–106CrossRefPubMedGoogle Scholar
  45. Noguchi C, Kamitori K, Hossain A, Hoshikawa H, Katagi A, Dong Y, Sui L, Tokuda M, Yamaguchi F (2016) D-Allose inhibits cancer cell growth by reducing GLUT1 expression. Tohoku J Exp Med 238(2):131–141CrossRefPubMedGoogle Scholar
  46. Noguchi C, Yamada K, Yamaguchi F, Kamitori K, Dong Y, Hirata Y, Hossein A, Tsukamoto I, Tokuda M (2013) Rare sugar D-allose strongly induces thioredoxin interacting protein (TXNIP) expression and inhibits osteoclast differentiation. J Physiol Sci 63:S250–S250Google Scholar
  47. O’Neil M, Heckelman P, Koch C, Roman K (2006) The Merck index: an encyclopedia of chemicals, drugs, and biologicals, 14th edn. Whitehouse Station, NJ: Merck & Co. Inc 46(7069): 78Google Scholar
  48. Panghal A, Janghu S, Virkar K, Gat Y, Kumar V, Chhikara N (2017) Potential non-dairy probiotic products—a healthy approach. Food Biosci 21:80–89.  https://doi.org/10.1016/j.fbio.2017.12.003 CrossRefGoogle Scholar
  49. Park C-S, Yeom S-J, Kim H-J, Lee S-H, Lee J-K, Kim S-W, Oh D-K (2007a) Characterization of ribose-5-phosphate isomerase of Clostridium thermocellum producing D-allose from D-psicose. Biotechnol Lett 29(9):1387–1391CrossRefPubMedGoogle Scholar
  50. Park C-S, Yeom S-J, Lim Y-R, Kim Y-S, Oh D-K (2010) 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(12):1947–1953CrossRefPubMedGoogle Scholar
  51. Park H-Y, Park C-S, Kim H-J, Oh D-K (2007b) Substrate specificity of a galactose 6-phosphate isomerase from Lactococcus lactis that produces D-allose from D-psicose. J Biotechnol 132(1):88–95CrossRefPubMedGoogle Scholar
  52. Perold GW, Beylis P, Howard AS (1973) Metabolites of proteaceae. Part VIII. The occurrence of (+)-D-allose in nature: rubropilosin and pilorubrosin from Protea rubropilosa beard. J Chem Soc Perkin Trans 1:643–649CrossRefGoogle Scholar
  53. Phelps FP, Bates F (1934) Preparation of crystalline β-D-allose. J Am Chem Soc 56(5):1250–1250CrossRefGoogle Scholar
  54. 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(6):1297–1307CrossRefPubMedGoogle Scholar
  55. Sakoguchi H, Yoshihara A, Izumori K, Sato M (2016) Screening of biologically active monosaccharides: growth inhibitory effects of D-allose, D-talose, and L-idose against the nematode Caenorhabditis elegans. Biosci Biotechnol Biochem 80(6):1058–1061CrossRefPubMedGoogle Scholar
  56. Seo M-J, Choi J-H, Kang S-H, Shin K-C, Oh D-K (2017) Characterization of L-rhamnose isomerase from Clostridium stercorarium and its application to the production of D-allose from D-allulose (D-psicose). Biotechnol Lett 40:325–334.  https://doi.org/10.1007/s10529-017-2468-1 CrossRefPubMedGoogle Scholar
  57. Shinohara N, Nakamura T, Abe Y, Hifumi T, Kawakita K, Shinomiya A, Tamiya T, Tokuda M, Keep RF, Yamamoto T, Kuroda Y (2016) D-Allose attenuates overexpression of inflammatory cytokines after cerebral ischemia/reperfusion injury in gerbil. J Stroke Cerebrovasc Dis 25(9):2184–2188CrossRefPubMedGoogle Scholar
  58. Sithara R, Selvakumar P, Arun C, Anandan S, Sivashanmugam P (2017) Economical synthesis of silver nanoparticles using leaf extract of Acalypha hispida and its application in the detection of Mn(II) ions. J Adv Res 8(6):561–568CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sui L, Dong Y, Watanabe Y, Yamaguchi F, Hatano N, Izumori K, Tokuda M (2005a) Growth inhibitory effect of D-allose on human ovarian carcinoma cells in vitro. Anticancer Res 25(4):2639–2644PubMedGoogle Scholar
  60. Sui L, Dong Y, Watanabe Y, Yamaguchi F, Hatano N, Tsukamoto I, Izumori K, Tokuda M (2005b) The inhibitory effect and possible mechanisms of D-allose on cancer cell proliferation. Int J Oncol 27(4):907–912PubMedGoogle Scholar
  61. Sui L, Nomura R, Dong Y, Yamaguchi F, Izumori K, Tokuda M (2007) Cryoprotective effects of D-allose on mammalian cells. Cryobiology 55(2):87–92CrossRefPubMedGoogle Scholar
  62. Sun Y, Hayakawa S, Puangmanee S, Izumori K (2006) Chemical properties and antioxidative activity of glycated α-lactalbumin with a rare sugar, D-allose, by Maillard reaction. Food Chem 95(3):509–517CrossRefGoogle Scholar
  63. Takata G, Uechi K, Taniguchi E, Kanbara Y, Yoshihara A, Morimoto K, Izumori K (2011) Characterization of Mesorhizobium loti L-rhamnose isomerase and its application to L-talose production. Biosci Biotechnol Biochem 75(5):1006–1009CrossRefPubMedGoogle Scholar
  64. Tanaka S, Sakamoto H (2011) Effects of D-allose on the endocytic activity of dendritic cells and the subsequent stimulation of T cells. Cell Immunol 271(1):141–146CrossRefPubMedGoogle Scholar
  65. Weckwerth W, Loureiro ME, Wenzel K, Fiehn O (2004) Differential metabolic networks unravel the effects of silent plant phenotypes. P Natl Acad Sci the USA 101(20):7809–7814CrossRefGoogle Scholar
  66. Xu W, Zhang W, Tian Y, Zhang T, Jiang B, Mu W (2017) Characterization of a novel thermostable L-rhamnose isomerase from Thermobacillus composti KWC4 and its application for production of D-allose. Process Biochem 53:153–161CrossRefGoogle Scholar
  67. Xu W, Zhang WL, Zhang T, Jiang B, Mu WM (2016) L-Rhamnose isomerase and its use for biotechnological production of rare sugars. Appl Microbiol Biotechnol 100(7):2985–2992CrossRefPubMedGoogle Scholar
  68. Yamaguchi F, Takata M, Kamitori K, Nonaka M, Dong Y, Sui L, Tokuda M (2008) Rare sugar D-allose induces specific up-regulation of TXNIP and subsequent G1 cell cycle arrest in hepatocellular carcinoma cells by stabilization of p27kip1. Int J Oncol 32(2):377–385PubMedGoogle Scholar
  69. Yamamoto R, Iida A, Tankawa K, Shiratsuchi H, Tokuda M, Matsui T, Nakamura T (2017) Dietary D-allose ameliorates hepatic inflammation in mice with non-alcoholic steatohepatitis. Food Sci Technol Res 23(2):319–327CrossRefGoogle Scholar
  70. Yeom S-J, Ji J-H, Kim N-H, Park C-S, Oh D-K (2009) Substrate specificity of a mannose-6-phosphate isomerase from Bacillus subtilis and its application in the production of L-ribose. Appl Environ Microbiol 75(14):4705–4710CrossRefPubMedPubMedCentralGoogle Scholar
  71. Yeom S-J, Kim B-N, Park C-S, Oh D-K (2010) Substrate specificity of ribose-5-phosphate isomerases from Clostridium difficile and Thermotoga maritima. Biotechnol Lett 32(6):829–835CrossRefPubMedGoogle Scholar
  72. 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(6):1859–1866CrossRefPubMedGoogle Scholar
  73. Yokohira M, Hosokawa K, Yamakawa K, Saoo K, Matsuda Y, Zeng Y, Kuno T, Imaida K (2008) Potential inhibitory effects of D-allose, a rare sugar, on liver preneoplastic lesion development in F344 rat medium-term bioassay. J Biosci Bioeng 105(5):545–553CrossRefPubMedGoogle Scholar
  74. Yoon RY, Yeom SJ, Park CS, Oh DK (2009) Substrate specificity of a glucose-6-phosphate isomerase from Pyrococcus furiosus for monosaccharides. Appl Microbiol Biotechnol 83(2):295–303CrossRefPubMedGoogle Scholar
  75. Yue Z, Lingqia S, Jing W (2016) Optimization of trehalose synthase fermentation conditions from recombinant Escherichia coli. J Food Sci Biotechnol 35(9):913–919Google Scholar
  76. Zhang R-g, 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. Structure 11(1):31–42CrossRefPubMedPubMedCentralGoogle Scholar
  77. Zhang WL, Yu SH, Zhang T, Jiang B, Mu WM (2016) Recent advances in D-allulose: physiological functionalities, applications, and biological production. Trends Food Sci Technol 54:127–137CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ziwei Chen
    • 1
  • Jiajun Chen
    • 1
  • Wenli Zhang
    • 1
  • Tao Zhang
    • 1
    • 2
  • Cuie Guang
    • 1
  • Wanmeng Mu
    • 1
    • 2
  1. 1.State Key Laboratory of Food Science and TechnologyJiangnan UniversityWuxiChina
  2. 2.International Joint Laboratory on Food SafetyJiangnan UniversityWuxiChina

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