Tagatose as a Potential Nutraceutical: Production, Properties, Biological Roles, and Applications

Journal of Food Science

Volumn 83, Issue 11, 2018, Pages 2699-2709

  Roy, Sohini ^a   Chikkerur, Jayaram ^a   Roy, Sudhir Chandra ^b   Dhali, Arindam ^b   Kolte, Atul Puroshtam ^b   Sridhar, Manpal ^b   Samanta, Ashis Kumar ^b  

^a JAIN UNIVERSITY   (India)

^b ICAR NATIONAL INSTITUTE OF ANIMAL NUTRITION AND PHYSIOLOGY   (India)

Author keywords

antidiabetic; d tagatose; l arabinose isomerase; nutraceutical

Indexed keywords

ANTIDIABETIC AGENT; ANTIOBESITY AGENT; ANTIOXIDANT; HEXOSE; IRON CHELATING AGENT; ISOMERASE; L-ARABINOSE ISOMERASE; PREBIOTIC AGENT; TAGATOSE;

AGING; BACILLUS SUBTILIS; BIOSYNTHESIS; CHEMISTRY; CORYNEBACTERIUM GLUTAMICUM; DIETARY SUPPLEMENT; DRUG EFFECT; INTESTINE FLORA; LACTOCOCCUS LACTIS; METABOLISM;

AGING; ALDOSE-KETOSE ISOMERASES; ANTI-OBESITY AGENTS; ANTIOXIDANTS; BACILLUS SUBTILIS; CORYNEBACTERIUM GLUTAMICUM; DIETARY SUPPLEMENTS; GASTROINTESTINAL MICROBIOME; HEXOSES; HYPOGLYCEMIC AGENTS; IRON CHELATING AGENTS; LACTOCOCCUS LACTIS; PREBIOTICS;

EID: 85055212432     PISSN: 00221147     EISSN: 17503841     Source Type: Journal    
DOI: 10.1111/1750-3841.14358     Document Type: Review

References (120)

1. Adachi, S. (1958). Formation of lactulose and tagatose from lactose in strongly heated milk. Nature, 181(4612), 840–841. https://doi.org/10.1038/181840a0
2. Agius, L. (1998). The physiological role of glucokinase binding and translocation in hepatocytes. Advances in Enzyme Regulation, 38, 303–331. https://doi.org/10.1016/S0065-2571(97)00001-0
3. Al-Jobore, A. A. H., Guthrie, R. D., & Wells, R. D. (1971). A new route for the synthesis of D-tagatose. Carbohydrate Research, 16(2), 474–476. https://doi.org/10.1016/S0008-6215(00)81187-8
4. Armstrong, L. M., Luecke, K. J., & Bell, L. N. (2009). Consumer evaluation of bakery product flavor as affected by incorporating the prebiotic tagatose. International Journal of Food Science, 44(4), 815–819. https://doi.org/10.1111/j.1365-2621.2009.01909.x
5. Beadle, J. R., Saunders, J. P., & Wajda, T. J., inventors (1992). Process of manufacturing tagatose. U.S. Patent 5078796A. Retrieved from https://www.google.ch/patents/US5078796
6. Bertelsen, H., Jensen, B. B., & Buemann, B. (1999). D-tagatose: A novel low caloric sweetener with prebiotic properties. World Review of Nutrition Dietetics, 85, 98–109. Retrieved from https://doi.org/0.1159/000059685
7. Boesch, C., Ith, M., Jung, B., Bruegger, K., Erban, S., Diamantis, I., … Bar, A. (2001). Effect of oral D-tagatose on liver volume and hepatic glycogen accumulation in healthy male volunteers. Regulatory Toxicology and Pharmacology, 33(2), 257–267. https://doi.org/10.1006/rtph.2001.1470
8. Buemann, B., Toubro, S., & Astrup, A. (1999a). Human gastrointestinal tolerance to D-tagatose. Regulatory Toxicology and Pharmacology, 29(2 Pt 2), S71–S77. https://doi.org/10.1006/rtph.1998.1265
9. Buemann, B., Toubro, S., Raben, A., & Astrup, A. (1999b). Human tolerance to single, high dose of D-tagatose. Regulatory Toxicology and Pharmacology, 29(2), S66–S70. https://doi.org/10.1006/rtph.1998.1252
10. Buemann, B., Toubro, S., Raben, A., Blundell, J., & Astrup, A. (2000). The acute effect of D-tagatose on food intake in human subjects. British Journal of Nutrition, 84(2), 227–231. https://doi.org/10.1017/S000711450000146X
11. Bunn, H. F., & Higgins, P. J. (1981). Reactions of monosaccharaides with proteins: Possible evolutionary significance. Science, 213(4504), 222–224.https://doi.org/10.1126/science.12192669
12. Canani, R. B., Costanzo, M. D., Leone, L., Pedata, M., Meli, R., & Calignano, A. (2011). Potential beneficial effects of butyrate in intestinal and extra intestinal diseases. World Journal of Gastroenterology, 17(12), 1519–1528. https://doi.org/10.3748/wjg.v17.i12. 1519
13. Castanon, J. I. R. (2007). History of the use of antibiotic as growth promoters in European poultry feeds. Poultry Science, 86(11), 2466–2471. https://doi.org/10.3382/ps.2007-00249
14. Cheetham, P. S. J., & Wootton, A. N. (1993). Bioconversion of D-galactose into D-tagatose. Enzyme and Microbial Technology, 15(2), 105–108. https://doi.org/10.1016/0141-0229(93)90032-W
15. Cheng, L., Mu, W., & Jiang, B. (2010a). Thermostable L-arabinose isomerase from Bacillus stearothermophilus IAM11001 for D-tagatose production: Gene cloning, purification and characterization. Journal of the Science of Food and Agriculture, 90(8), 1327–1333. https://doi.org/10.1002/jsfa.3938
16. Cheng, L., Mu, W., Zhang, T., & Jiang, B. (2010b). An L-arabinose isomerase from Acidothermus cellulolytics ATCC 43068: Cloning, expression, purification, and characterization. Applied Microbiology and Biotechnology, 86(4), 1089–1097. https://doi.org/10.1007/s00253-009-2322-z
17. Cheon, J., Kim, S. B., Park, S. W., Han, J. K., & Kim, P. (2009). Characterization of L-arabinose isomerase in Bacillus subtilis, A GRAS host, for the production of edible tagatose. Food Biotechnology, 23(1), 8–16. https://doi.org/10.1080/08905430802671873
18. Choi, J. M., Lee, Y. J., Cao, T. P., Shin, S. M., Park, M. K., Lee, H. S., … Lee, D. W. (2016). Structure of the thermophilic L-arabinose isomerase from Geobacillus kaustophilus reveals metal-mediated inter subunit interactions for activity and thermostability. Archives of Biochemistry and Biophysics, 596, 51–62. https://doi.org/10.1016/j.abb.2016.02.033
19. Chouayekh, H., Bejar, W., Rhimi, M., Jelleli, K., Mseddi, M., & Bejar, S. (2007). Characterization of an L-arabinose isomerase from the Lactobacillus plantarum NC8 strain showing pronounced stability at acidic pH. FEMS Microbiology Letters, 277(2), 260–267. https://doi.org/10.1111/j.1574-6968.2007.00961.x
20. De Muynck, C., Beauprez, J., Soetaert, W., & Vandamme, E. J. (2006). Boric acid as a mobile phase additive for high performance liquid chromatography separation of ribose, arabinose and ribulose. Journal of Chromatography A, 1101(1–2), 115–21. https://doi.org/10.1016/j.chroma.2005.09.068
21. Dobbs, C. M., & Bell, L. N. (2010). Storage stability of Tagatose in buffer solutions of various compositions. Food Research International, 43(1), 383–386. https://doi.org/10.1016/j.foodres.2009.10.010
22. Donner, T. W. (2006). The metabolic effects of dietary supplementation with D-tagatose in patients with type 2 diabetes. Diabetes, 55(Suppl.1), 461
23. Donner, T., Wilber, J., & Ostrowski, D. (1996). D-tagatose: A novel therapeutic adjunct for non-insulin-dependent diabetes. Diabetes, 45(Suppl. 2), 125A
24. Donner, T. W., Wilber, J. F., & Ostrowski, D. (1999). D-tagatose, a novel hexose: Acute effects on carbohydrate tolerance in subjects with and without type 2 diabetes. Diabetes, Obesity and Metabolism, 1(5), 285–291. https://doi.org/10.1046/j.1463-1326.1999.00039.x
25. Ensor, M., Williams, J., Smith, R., Banfield, A., & Lodder, R. A. (2014). Effects of three low-doses of D-tagatose on glycemic control over six months in subjects with mild type 2 diabetes mellitus under control with diet and exercise. Journal of Endocrinology, Diabetes & Obesity, 2(4), 1057
26. Ensor, M., Banfield, A. B., Smith, R. R., Williams, J., & Lodder, R. A. (2015). Safety and efficacy of D-tagatose in glycemic control in subjects with type 2 diabetes. Journal of Endocrinology, Diabetes & Obesity, 3(1), 1065
27. Ercan-Fang, N., Gannon, M. C., Rath, V. L., Treadway, J. L., Taylor, M. R., & Nuttall, F. Q. (2002). Integrated effects of multiple modulators on human liver glycogen phosphorylase α. American Journal of Physiology-Endocrinology and Metabolism, 283(1), E29–E37.https://doi.org/10.1152/ajpendo.00425.2001
28. 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. Journal of Molecular Catalysis B: Enzymatic, 102, 120–126. https://doi.org/10.1016/j.molcatb.2014.02.001
29. Fan, C., Xu, W., Zhang, T., Zhou, L., Jiang, B., & Mu, W. (2015). Engineering of Alicyclobacillus hesperidum L-arabinose isomerase for improved catalytic activity and reduced pH optimum using random and site-directed mutagenesis. Applied Biochemistry and Biotechnology, 177(7), 1480–92. https://doi.org/10.1007/s12010-015-1828-3
30. Gibson, G. R., & Roberfroid, M. B. (1995). Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. Journal of Nutrition, 125(6), 1401–1412
31. Granstrom, T. B., Takata, G., Tokuda, M., & Izumori, K. (2004). Izumoring: A novel and complete strategy for bio-production of rare sugars. Journal of Bioscience and Bioengineering, 97(2), 89–94. https://doi.org/10.1016/S1389-1723(04)70173-5
32. Heath, E., Horecker, B., Smyrniotis, P., & Takagi, Y. (1958). Pentose fermentation by Lactobacillus plantarum II L-arabinose isomerase. Journal of Biological Chemistry, 231(2), 1031–1037
33. Hirst, E. L., Hough, L., & Jones, J. K. N. (1949a). Composition of the gum of Sterculiasetigera: Occurrence of D-tagatose in nature. Nature, 163(4135), 177. https://doi.org/10.1038/163177b0
34. Hirst, E. L., Hough, L., & Jones, J. K. N. (1949b). The structure of Sterculia setigera gum. Part I. An investigation by the method of paper partition chromatography of the products of hydrolysis of the gum. Journal of the Chemical Society, 3145–3151. https://doi.org/10.1039/JR9490003145
35. Hong, Y. H., Lee, D. W., Lee, S. J., Choe, E. A., Kim, S. B., Lee, Y. H., … Pyun, Y. R. (2007). Production of D-tagatose at high temperatures using immobilized Escherichia coli cells expressing L-arabinose isomerase from Thermotoga neapolitana. Biotechnology Letters, 29(4), 569–574.https://doi.org/10.1007/s10529-006-9277-2
36. Hudson, C. S., Wolfrom, M. L., & Cantor, S. M. (1952). Advances in carbohydrate chemistry. New York, USA: Academic Press, Inc
37. Hung, X. G., Tseng, W. C., Liu, S. M., Tzou, W. S., & Fang, T. Y. (2014). Characterization of a thermophilic l-arabinose isomerase from Thermoanaerobacterium saccharolyticum NTOU1. Biochemical Engineering Journal, 83, 121–128. https://doi.org/10.1016/j.bej.2013.04.026
38. Huwig, A., Emmel, S., Jakel, G., & Giffhorn, F. (1997). Enzymatic synthesis of l-tagatose from galactitol with galactitol dehydrogenase from Rhodobacter sphaeroides D. Carbohydrate Research, 305(3–4), 337–339. https://doi.org/10.1016/S0008-6215(97)00265-6
39. International Society of Rare Sugars. (2011). Kagawa University, Miki, Japan. Retrieved from https://sites.google.com/site/raresugars/activity
40. Izumori, K., Yamanaka, K., & Elbein, D. (1976). Pentose metabolism in Mycobacterium smegmatis: Specificity of induction of pentose isomerases. Journal of Bacteriology, 128(2), 587–591
41. Izumori, K., Ueda, Y., & Yamanaka, K. (1978). Pentose metabolism in Mycobacterium smegmatis: Comparison of L-arabinose isomerases induced by L-arabinose and D-galactose. Journal of Bacteriology, 133(1), 413–414
42. Izumori, K., Miyoshi, T., Tokuda, S., & Yamabe, K. (1984). Production of D-tagatose from dulcitol by Arthrobacter globiformis. Applied and Environmental Microbiology, 48(5), 1055–1057
43. Izumori, K., & Tsuzaki, K. (1988). Production of d-tagatose from d-galactitol by Mycobacterium smegmatis. Journal of Fermentation Technology, 66(2), 225–227. https://doi.org/10.1016/0385-6380(88)90052-0
44. Jagtap, S. S., Singh, R., Kang, Y. C., Zhao, H., & Lee, J. K. (2014). Cloning and characterization of a galactitol 2-dehydrogenase from Rhizobium legumenosarum and its application in D-tagatose production. Enzyme and Microbial Technology, 58–59, 44–51. https://doi.org/10.1016/j.enzmictec.2014.02.012
45. Jorgensen, F., Hansen, O. C., & Stougaard, P. (2004). Enzymatic conversion of D-galactose to D-tagatose: Heterologous expression and characterization of a thermostable L-arabinose isomerase from Thermoanaerobacter mathranii. Applied Microbiology and Biotechnology, 64(6), 816–822. https://doi.org/10.1007/s00253-004-1578-6
46. Jung, E. S., Kim, H. J., & Oh, D. K. (2005). Tagatose production by immobilized recombinant Escherichia coli cells containing Geobacillus stearothermophilus L-arabinose isomerase mutant in a packed-bed bioreactor. Biotechnology Progress, 21(4), 1335–1340. https://doi.org/10.1021/bp050078p
47. Karabinos, J. V. (1952). Psicose, sorbose and tagatose. Advances in Carbohydrate Chemistry, 7, 99–136. https://doi.org/10.1016/S0096-5332(08)60083-1
48. Kaveeshwar, S. A., & Cornwall, J. (2014). The current state of diabetes mellitus in India. Australasian Medical Journal, 7(1), 45–48.https://doi.org/10.4066/AMJ.2013.1979
49. Kim, P. (2004). Current studies on biological tagatose production using L-arabinose isomerase: A review and future perspective. Applied Microbiology and Biotechnology, 65(3), 243–249. https://doi.org/10.1007/s00253-004-1665-8
50. Kim, P., Yoon, S. H., Roh, H. J., & Choi, J. H. (2001a). High production of D-tagatose, a potential sugar substitute, using immobilized L-arabinose isomerase. Biotechnology Progress, 17(1), 208–210. https://doi.org/10.1021/bp000147u
51. Kim, P., Yoon, S. H., Seo, M. J., Oh, D. K., & Choi, J. H. (2001b). Improvement of tagatose conversion rate by genetic evolution of thermostable galactose isomerase. Biotechnology and Applied Biochemistry, 34(Pt2), 99–102. https://doi.org/10.1042/BA20010025
52. Kim, B. C., Lee, Y. H., Lee, H. S., Lee, D. W., Choe, E. A., & Pyun, Y. R. (2002). Cloning, expression and characterization of L-arabinose isomerase from Thermotoga neapolitana: Bioconversion of D-galactose to D-tagatose using the enzyme. FEMS Microbiology Letters, 212(1), 121–126. https://doi.org/10.1111/j.1574-6968.2002.tb11254.x
53. Kim, J. W., Kim, Y. W., Roh, H. J., Kim, H. Y., Cha, J. H., Park, K. H., & Park, C. S. (2003a). Production of tagatose by a recombinant thermostable L-arabinose isomerase from Thermus sp. IM6501. Biotechnology Letters, 25(12), 963–967. https://doi.org/10.1023/A:1024069813839
54. Kim, H. J., Ryu, S. A., Kim, P., & Oh, D. K. (2003b). A feasible enzymatic process for D-tagatose production by an immobilized thermostable L-arabinose isomerase in a packed-bed bioreactor. Biotechnology Progress, 19(2), 400–404. https://doi.org/10.1021/bp025675f
55. Kim, H. J., & Oh, D. K. (2005). Purification and characterization of an L-arabinose isomerase from an isolated strain of Geobacillus thermodenitrificans producing D-tagatose. Journal of Biotechnology, 120(2), 162–73. https://doi.org/10.1016/j.jbiotec.2005.06.004
56. Kim, H. J., Kim, J. H., Oh, H. J., & Oh, D. K. (2006). Characterization of a mutated Geobacillus stearothermophilus L-arabinose isomerase that increases the production rate of D-tagatose. Journal of Applied Microbiology, 101(1), 213–221. https://doi.org/10.1111/j.1365-2672.2006.02975.x
57. Kim, S. B., Lee, Y. M., Park, S. W., Kim, J. H., Song, S. H., & Lee, K. P., inventors (2012). Recombinant GRAS strains expressing thermophilic arabinose isomerase as an active form and method of preparing food grade tagatose by using the same. U.S. Patent 8137946B2. Retrieved from https://www.google.com/patents/US8137946
58. Kim, B. J., Hong, S. H., Shin, K. C., Jo, Y. S., & Oh, D. K. (2014a). Characterization of a F280N variant of L-arabinose isomerase from Geobacillus thermodenitrificans identified as a D-galactose isomerase. Applied Microbiology and Biotechnology, 98(22), 9271–9281. https://doi.org/10.1007/s00253-014-5827-z
59. Kim, S. B., Lee, Y. M., Park, S. W., Kim, J. H., Song, S. H., Lee, K. P., … Choi, H., inventors (2014b). Arabinose isomerase expressed from Corynebacterium genus and tagatose manufacturing method by using it. U.S. Patent 8802393B2
60. Kruger, C. L., Whittaker, M. H., Frankos, V. H., & Schroeder, R. E. (1999a). Developmental toxicity study of D-tagatose in rats. Regulatory Toxicology and Pharmacology, 29(2 Pt 2), S29–S35. https://doi.org/10.1006/rtph.1998.1261
61. Kruger, C. L., Whittaker, M. H., Frankos, V. H., & Trimmer, G. W. (1999b). 90-Day oral toxicity study of D-tagatose in rats. Regulatory Toxicology and Pharmacology, 29(2 Pt 2), S1–S10. https://doi.org/10.1006/rtph.1998.1262
62. Laerke, H. N., & Jensen, B. B. (1999). D-Tagatose has low small intestinal digestibility but high large intestinal fermentability in pigs. Journal of Nutrition, 129(5), 1002–1009
63. Laerke, H. N., Jensen, B. B., & Hojsgaard, S. (2000). In vitro fermentation pattern of D-tagatose is affected by adaptation of microbiota from gastrointestinal tract of pigs. Journal of Nutrition, 130(7), 1772–1779
64. Lee, D. W., Jang, H. J., Choe, E. A., Kim, B. C., Lee, S. J., Kim, S. B., … Pyun, Y. R. (2004). Characterization of a thermostable L-arabinose (D-galactose) isomerase from the hyperthermophiliceubacterium Thermotoga maritima. Applied and Environmental Microbiology, 70(3), 1397–1404. https://doi.org/10.1128/AEM.70.3.1397-1404.2004
65. Lee, D. W., Choe, E. A., Kim, S. B., Eom, S. H., Hong, Y. H., Lee, S. J., … Pyun, Y. R. (2005a). Distinct metal dependence for catalytic and structural functions in the L-arabinose isomerases from the mesophilic Bacillus halodurans and the thermophilic Geobacillus stearothermophilus. Archives of Biochemistry and Biophysics, 434(2), 333–343. https://doi.org/10.1016/j.abb.2004.11.004
66. Lee, S. J., Lee, D. W., Choe, E. A., Hong, Y. H., Kim, S. B., Kim, B. C., & Pyun, Y. R. (2005b). Characterization of a thermoacidophilic L-arabinose isomerase from Alicyclobacillus acidocaldarius: Role of Lys-269 in pH optimum. Applied and Environmental Microbiology, 71(12), 7888–7896.https://doi.org/10.1128/AEM.71.12.7888-7896.2005
67. Levin, G. V., Zehner, L. R., Saunders, J. P., & Beadle, J. R. (1995). Sugar substitutes: Their energy values, bulk characteristics, and potential health benefits. The American Journal of Clinical Nutrition, 62(5 Suppl), 1161S–1168S
68. Levin, G. V., inventor (2001). Increased fertility and improved fetal development drug. U.S. Patent 6225452 B1. Retrieved from https://www.google.co.in/patents/US6225452
69. Levin, G. V., inventor (2006). Use of tagatose to enhance key blood factors. European Patent 1173 186B1. Retrieved from https://data.epo.org/publication-server/rest/v1.0/publication-dates/20060614/patents/EP1173186NWB1/document.pdf
70. Li, Y., Zhu, Y., Liu, A., & Sun, Y. (2011). Identification and characterization of a novel L-arabinose isomerase from Anoxybacillus flavithermus useful in D-tagatose production. Extremophiles, 15(3), 441–450. https://doi.org/10.1007/s00792-011-0375-2
71. Li, G., Xu, Z., Li, S., & Xu, H. (2012). Probing the essential catalytic residues and substrate affinity in thermophilic L-arabinose isomerase by homology modeling and site-directed mutagenesis. Chinese Journal of Catalysis, 33(10), 1717–1723. https://doi.org/10.3724/SP.J.1088.2012.20606
72. Liang, M., Chen, M., Liu, X., Zhai, Y., Liu, X., Zhang, H., … Wang, P. (2012). Bioconversion of D-galactose to D-tagatose: Continuous packed bed reaction with an immobilized thermostable L-arabinose isomerase and efficient purification by selective microbial degradation. Applied Microbiology and Biotechnology, 93(4), 1469–1474. https://doi.org/10.1007/s00253-011-3638-z
73. Lim, B. C., Kim, H. J., & Oh, D. K. (2007). High production of D-tagatose by the addition of boric acid. Biotechnology Progress, 23(4), 824–828. https://doi.org/10.1021/bp070056y
74. Lim, B. C., Kim, H. J., & Oh, D. K. (2008). Tagatose production with pH control in a stirred tank reactor containing immobilized L-arabinose isomerase from Thermotoga neapolitana. Applied Biochemistry and Biotechnology, 149(3), 245–253.https://doi.org/10.1007/s12010-007-8095-x
75. Lindberg, B. (1955). Studies on the chemistry of lichens. VIII. Investigation of a Dermatocarpon and some Roccella species. Acta Chemica Scandinavica, 9(6), 917–919
76. Liu, Y., Li, S., Xu, H., Wu, L., Xu, Z., Liu, J., & Feng, X. (2014). Efficient Production of D-tagatose using a food-grade surface display system. Journal of Agriculture and Food Chemistry, 62(28), 6756–6762. https://doi.org/10.1021/jf501937j
77. Lobry de Bruyn, C. A., & Alberda van Ekenstein, W. (1897). Action des alcalis sur les sucres. V: Transformation dela galactose. Les tagatoses, et la galtose. Recueil des Travaux Chimiques des Pays-Bas, 16(9), 262–273.https://doi.org/10.1002/recl.18970160902
78. Lu, Y., Levin, G. V., & Donner, T. W. (2008). Tagatose, a new antidiabetic and obesity control drug. Diabetes Obesity and Metabolism, 10(2), 109–134. https://doi.org/10.1111/j.1463-1326.2007.00799.x
79. Manjasetty, B. A., & Chance, M. R. (2006). Crystal structure of Escherichia coli L-arabinose isomerase (ECAI), the putative target of biological tagatose production. Journal of Molecular Biology, 360, 297–309
80. Manzoni, M., Rollini, M., & Bergomi, S. (2001). Biotransformation of D-galactitol to tagatose by acetic acid bacteria. Process Biochemistry, 36(10), 971–977. https://doi.org/10.1016/S0032-9592(01)00137-6
81. Martinez, P., Carrascosa, J. M., & Nunez de Castro, I. (1987). Ketose induced respiratory inhibition in isolated hepatocytes. Revista Espanola De Fisiologia, 43(2), 163–171
82. Masoro, E. J. (1992). Aging and proliferative homeostasis: Modulation by food restriction in rodents. Laboratory Animal Science, 42(2), 132–137
83. Masoro, E. J. (1993). Dietary restriction and aging. Journal of the American Geriatrics Society, 41(9), 994–999. https://doi.org/10.1111/j.1532-5415.1993.tb06767.x
84. Mei, W., Wang, L., Zang, Y., Zheng, Z., & Ouyang, J. (2016). Characterization of an L-arabinose isomerase from Bacillus coagulans NL01 and its application for D-tagatose production. BMC Biotechnology, 16(1), 55. https://doi.org/10.1186/s12896-016-0286-5
85. Men, Y., Zhu, Y., Zhang, L., Kang, Z., Izumori, K., Sun, Y., & Ma, Y. (2014). Enzymatic conversion of D-galactose to D-tagatose: Cloning, over expression and characterization of L-arabinose isomerase from Pediococcus pentosaceus PC-5. Microbiological Research, 169(2–3), 171–178. https://doi.org/10.1016/j.micres.2013.07.001
86. Muniruzzaman, S., Tokunaga, H., & Izumori, K. (1994). Isolation of Enterobacter agglomerans strain 221e from soil, a potent D-tagatose producer from galactitol. Journal of Fermentation and Bioengineering, 78(2), 145–148. https://doi.org/10.1016/0922-338X(94)90253-4
87. Nakazawa, H., Genka, C., & Fujishima, M. (1996). Pathological aspects of active oxygen-free radicals. The Japanese Journal of Physiology, 46(1), 15–32. https://doi.org/10.2170/jjphysiol.46.15
88. Oh, H. J., Kim, H. J., & Oh, D. K. (2006). Increase in D-tagatose production rate by site-directed mutagenesis of L-arabinose isomerase from Geobacillus thermodenitrificans. Biotechnology Letters, 28(3), 145–149. https://doi.org/10.1007/s10529-005-5327-4
89. Patel, M. J., Akhani, R. C., Patel, A. T., Dedania, S. R., & Patel, D. H. (2017). A single and two step isomerization process for D-tagatose and L-ribose bio-production using L-arabinose isomerase and D-lyxose isomerase. Enzyme and Microbial Technology, 97, 27–33. https://doi.org/10.1016/j.enzmictec.2016.11.001
90. Paterna, J. C., Boess, F., Staubli, A., & Boelsterli, U. A. (1998). Antioxidant and cytoprotective properties of D-tagatose in cultured murine hepatocytes. Toxicology and Applied Pharmacology, 148(1), 117–125. https://doi.org/10.1006/taap.1997.8315
91. Rao, D., Gullapalli, P., Yoshihara, A., Jenkinson, S. F., Morimoto, K., Takata, G., … Izumori, K. (2008). Direct production of L-tagatose from L-psicose by Enterobacter aerogenes 230S. Journal of Bioscience and Bioengineering, 106(5), 473–480. https://doi.org/10.1263/jbb.106.473
92. Rhimi, M., & Bejar, S. (2006). Cloning, purification and biochemical characterization of metallic-ions independent and thermoactive L-arabinose isomerase from the Bacillus stearothermophilus US100 strain. Biochimica et Biophysica Acta, 1760(2), 191–199. https://doi.org/10.1016/j.bbagen.2005.11.007
93. Rhimi, M., Aghajari, N., Juy, M., Chouayekh, H., Maguin, E., Haser, R., & Bejar, S. (2009). Rational design of Bacillus stearothermophilus US100 L-arabinose isomerase: Potential applications for D-tagatose production. Biochimie, 91(5), 650–653. https://doi.org/10.1016/j.biochi.2009.01.014
94. Rhimi, M., Ihammami, R., Bajic, G., Boudebbouze, S., Maguin, E., Haser, R., & Aghajari, N. (2010). The acid tolerant L-arabinose isomerase from the food grade Lactobacillus sakei 23K is an attractive D-tagatose producer. Bioresource Technology, 101(23), 9171–9177. https://doi.org/10.1016/j.biortech.2010.07.036
95. Rhimi, M., Bajic, G., Ilhammami, R., Boudebbouze, S., Maguin, E., Haser, R., & Aghajari, N. (2011a). The acid-tolerant L-arabinose isomerase from the mesophilic Shewanella sp. ANA-3 is highly active at low temperatures. Microbial Cell Factories, 10, 96. https://doi.org/10.1186/1475-2859-10-96
96. Rhimi, M., Chouayekh, H., Gouillouard, I., Maguin, E., & Bejar, S. (2011b). Production of D-tagatose, a low caloric sweetener during milk fermentation using L-arabinose isomerase. Bioresource Technology, 102(3), 3309–3315. https://doi.org/10.1016/j.biortech.2010.10.078
97. Rhimi, M., Bermudez-Humaran, L. G., Huang, Y., Boudebbouze, S., Gaci, N., Garnier, A., … Maguin, E. (2015). The secreted L-arabinose isomerase displays anti-hyperglycemic effects in mice. Microbial Cell Factories, 14, 204. https://doi.org/10.1186/s12934-015-0391-5
98. Ryu, S. A., Kim, C. S., Kim, H. J., Baek, D. H., & Oh, D. K. (2003). Continuous D-tagatose production by immobilized thermostable L-arabinose isomerase in a packed-bed bioreactor. Biotechnology Progress, 19(6), 1643–1647. https://doi.org/10.1021/bp0340739
99. Salonen, N., Salonen, K., Leisola, M., & Nyyssola, A. (2013). D-Tagatose production in the presence of borate by resting Lactococcus lactis cells harboring Bifidobacterium longum L-arabinose isomerase. Bioprocess and Biosystems Engineering, 36(4), 489–497. https://doi.org/10.1007/s00449-012-0805-2
100. Samanta, A. K., Jayapal, N., Jayaram, C., Roy, S., Kolte, A. P., Senani, S., & Sridhar, M. (2015). Xylooligosaccharides as prebiotics from agricultural by-products: Production and applications. Bioactive Carbohydrate and Dietary Fibre, 5(1), 62–71. https://doi.org/10.1016/j.bcdf.2014.12.003
101. Saunders, J. P., Zehner, L. R., & Levin, G. V. (1999a). Disposition of D-[U-14C]-tagatose in the rat. Regulatory Toxicology and Pharmacology, 29(2), S46–S56. https://doi.org/10.1006/rtph.1998.1251
102. Saunders, J. P., Donner, T. W., Sadler, J. H., Levin, G. V., & Makris, N. G. (1999b). Effects of acute and repeated oral doses of D-tagatose on plasma uric acid in normal and diabetic humans. Regulatory Toxicology and Pharmacology, 29(2 Pt 2), S57–S65.https://doi.org/10.1006/rtph.1998.1264
103. Seo, M. J. (2013). Characterization of an L-arabinose isomerase from Bacillus thermoglucosidasius for D-tagatose production. Bioscience, Biotechnology, and Biochemistry, 77(2), 385–388. https://doi.org/10.1271/bbb.120723
104. Seoane, J., Gomez-Foix, A. M., O'Doherty, R. M., Gomez-Ara, C., Newgard, C. B., & Guinovart, J. J. (1996). Glucose 6-phosphate produced by glucokinase, but not hexokinase I, promotes the activation of hepatic glycogen synthase. Journal of Biological Chemistry, 271(39), 23756–23760. https://doi.org/10.1074/jbc.271.39.23756
105. Shaw, D. R. D. (1956). Polyol dehydrogenases. 3. Galactitol dehydrogenase and D-iditoldehydrognease. Biochemical Journal, 64(3), 316–322
106. Shimonishi, T., Okumura, Y., & Izumori, K. (1995). Production of L-tagatose from galactitol by Klebsiella pneumonia strain 40b. Journal of Fermentation and Bioengineering, 79(6), 620–622. https://doi.org/10.1016/0922-338X(95)94759-K
107. Torres, P. R., Manzo, R. M., Rubiolo, A. C., Batista-Vieraa, F. D., & Mammarella, E. J. (2014). Purification of an L-arabinose isomerase from Enterococcus faecium DBFIQ E36 employing a biospecific affinity strategy. Journal of Molecular Catalysis B: Enzymatic, 102, 99–105. https://doi.org/10.1016/j.molcatb.2014.01.023
108. Totton, E. L., & Lardy, H. A. (1949). The synthesis of D-tagatose by biochemical oxidation and by improved chemical method. Journal of the American Chemical Society, 71(9), 3076–3078. https://doi.org/10.1021/ja01177a037
109. USFDA. (2010). GRAS exemption claim for D-tagatose as an ingredient in foods. U.S. Food and Drug Administration. Retrieved from https://www.fda.gov/downloads/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm269560.pdf (Accessed on 7th February, 2018)
110. Valeri, F., Boess, F., Wolf, A., Goldlin, C., & Boelsterli, U. A. (1997). Fructose and tagatose protect against oxidative cell injury by iron chelation. Free Radical Biology and Medicine, 22(1–2), 257–268. https://doi.org/10.1016/S0891-5849(96)00331-0
111. Wanarska, M., & Kur, J. (2012). A method for the production of D-tagatose using a recombinant Pichia pastoris strain secreting β-D-galactosidase from Arthrobacter chlorophenolicus and a recombinant L-arabinose isomerase from Arthrobacter sp 22c. Microbial Cell Factories, 11, 113. https://doi.org/10.1186/1475-2859-11-113
112. World Health Organization. (2004). Evaluation of certain food additives and contaminants. Sixty first report of the Joint FAO/WHO expert committee on food additives. WHO Technical Report Series 922. Retrieved from https://apps.who.int/iris/bitstream/10665/42849/1/WHO_TRS_922
113. Xu, Z., Qing, Y. J., Li, S., Feng, X. H., Xu, H., & Ouyang, P. K. (2011). A novel L-arabinose isomerase from Lactobacillus fermentum CGMCC2921 for D-tagatose production: Gene cloning, purification and characterization. Journal of Molecular Catalysis B: Enzymatic, 70(1–2), 1–7. https://doi.org/10.1016/j.molcatb.2011.01.010
114. Xu, Z., Li, S., Fu, F. G., Li, G. X., Feng, X., Xu, H., & Ouyang, P. K. (2012). Production of D-tagatose, a functional sweetener, utilizing alginate immobilized Lactobacillus fermentum CGMCC2921 cells. Applied Biochemistry and Biotechnology, 166(4), 961–973. https://doi.org/10.1007/s12010-011-9484-8
115. Xu, Z., Li, S., Feng, X., Liang, J., & Xu, H. (2014a). L-Arabinose isomerase and its use for biotechnological production of rare sugars. Applied Microbiology and Biotechnology, 98(21), 8869–8878. https://doi.org/10.1007/s00253-014-6073-0
116. Xu, Z., Li, S., Feng, X., Zhan, Y., & Xu, H. (2014b). Function of aspartic acid residues in optimum pH control of L-arabinose isomerase from Lactobacillus fermentum. Applied Microbiology and Biotechnology, 98, 3987–3996. https://doi.org/10.1007/s00253-013-5342-7
117. Xu, Z., Li, S., Liang, J., Feng, X., & Xu, H. (2015). Protein purification, crystallization and preliminary X-ray diffraction analysis of L-arabinose isomerase from Lactobacillus fermentum CGMCC2921. Acta Crystallographica Section F, 71, 28–33. https://doi.org/10.1107/S2053230X14025321
118. Yoon, S. H., Kim, P., & Oh, D. K. (2003). Properties of L-arabinose isomerase from Escherichia coli as biocatalyst for tagatose production. World Journal of Microbiology and Biotechnology, 19(1), 47–51. https://doi.org/10.1023/A:1022575601492
119. Yoshihara, K., Shinohara, Y., Hirotsu, T., & Izumori, K. (2006). Bioconversion of D-psicose to D-tagatose and D-talitol by Mucoraceae Fungi. Journal of Bioscience and Bioengineering, 101(3), 219–222. https://doi.org/10.1263/jbb.101.219
120. Yu, P. L., Hodge, R. A., & Li, X. P. (1990). In vitro expression of Lac-PTS and tagatose 1,6-bisphosphate aldolase genes from Lactococcus lactis subsp cremoris plasmid pDI-21. Applied Microbiology and Biotechnology, 33(6), 677–679.https://doi.org/10.1007/BF00604936