Spectroscopic study of the physical properties making trehalose a stabilizing and shelf life extending compound in food industry
Main Article Content
Keywords
biotechnology, cereals quality, food quality, food safety, protein
Abstract
Introduction Trehalose, a glass-forming bioprotectant disaccharide, has been demonstrated to possess significant potential within the food industry. It does not interact with reactive molecules such as amino groups from peptides and proteins, preventing the degradation and aggregation due to Maillard reactions. Objective This paper aims to review at the molecular level the effects of trehalose on the structural and dynamical properties of water and on protein to highlight the stabilization and conservation properties on food products. Results and Conclusions The experimental findings presented show that water molecules are arranged in presence of trehalose in a particular configuration which avoids ice formation, so limiting damage due to freezing and cooling. On the other hand, homologous disaccharides, and trehalose to a greater extent, slow down the dynamics of water with a significant influence on the biological activity. These results imply thattrehalose has a greater ability to bind volatile substances and deliver superior bioprotective effectiveness. Furthermore trehalose is shown to be incapable of taking part in the denaturation process of lysozyme under thermal stress.
References
Angell C.A. (1997) Glassforming liquids with microscopic to macroscopic two-state complexity. Progress of Theoretical Physics,126, 1–7.
Angell C.A., Poole P.H., Shao J. (1994) Glassforming liquids, anomalous liquids and polyamorphism in liquids and biopolymers. II Nuovo Cimento D,16, 993–1025.
Branca C., Magazu`S., Maisano G., Migliardo P. (1999) Anomalous cryoprotective effectiveness of trehalose: Raman scattering evidences. Journal of Chemical Physics,111,281–287.
Cordone L., Cottone G., Giuffrida S., Palazzo G., Venturoli G., Viappiani C. (2005) Internal dynamics and protein-matrix coupling in trehalose coated proteins. Biochimica Biophysica Acta,1749, 252–281.
Cottone G., Cicciotti G., Cordone L. (2002) Protein-trehalose-water structures in trehalose coated carboxy-myoglobin. Journal of Chemical Physics,117, 9862–9866.
Crowe J.H. (1975) The physiology of cryptobiosis in tardigrades.In: R. Higgins (ed.) International symposium on tardigrades, Italy, June 17–19, 1974. Mem. Ist. Ital. Idrobiol. 32 (Suppl.),37–59.
Crowe J.H., Crowe L.M., Carpenter J.F., Wistrom C. (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochemical Journal, 242, 1–10.
Crowe J.H., Crowe L.M., Chapman D. (1984a) Infra-red spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Archives of Biochemical Biophysics, 232, 400–407.
Crowe J.H., Crowe L.M., Chapman D. (1984b) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science,223, 701–703.
Danielson M., Rollin S.T. (2004) USDA determines Cargill’sascend trehalose suitable for meat products. Report to Cargill, Cargill Health and Food Technologies (H&FT).
D’Arrigo G., Maisano G., Mallamace F., Migliardo P., Wanderlingh F. (1981) Raman scattering and structure of normal and supercooled water. Journal of Chemical Physics,75,4264–4271.
Duong T., Barrangou R., Michael Russell W., Klaenhammer T.R.(2006) Characterization of the tre locus and analysis of trehalose cryoprotection in Lactobacillus acidophilus NCFM. Applied and Environmental Microbiology,72, 1218–1225.
Gleeson M., Bishop N.C. (2000a) Studies on the potential use of trehalose as an ingredient of sports beverage; Study 1 the Glycaemic index of trehalose. Report to British Sugar, University of Birmingham, UK.
Gleeson M., Bishop N.C. (2000b) Studies on the potential use of trehalose as an ingredient of sports beverage; Study 2 effects of trehalose, glucose, or placebo ingestion on metabolic responses, perception of effort and endurance performance during constant load cycling to fatigue. Report to BritishSugar, University of Birmingham, UK.
Guo N., Puhlev I., Brown D.R., Mansbridge J., Levine F. (2000) Trehalose production confers desiccation tolerance on human cells. Nature Biotechnology,18, 168–171.
Hamaratoglu F., Eroglu A., Toner M., Sadler K.C. (2005) Cryopreservation of starfish oocytes. Cryobiology, 50, 38–47.
Hiashiyama T. (2002) Novel function and application of trehalose. Pure Applied Chemistry,74, 123–129.
Ivy J.L. (2001) The glycaemic index and performance enhancing capacity of trehalose. Report to Cargill, University of Texas, USA.
King S.M. (1999). Small angle neutron scattering.In Modern Techniques for Polymer Characterisationeds Pethrick R.A., Dawkins J.V. John Wiley and Sons, UK. pp. 171–232.
Lerbret A., Bordat P., Affouard F., Descamps M., Migliardo F.(2005) How homogeneous are the trehalose, maltose, and sucrose water solutions? An insight from molecular dynamics simulations. Journal of Physical Chemistry B,109,11046–11053.
Lindner P. (1991).Neutron, X-Ray and Light Scattering. Th.Zemb, The Netherlands.
Magazu`S., Maisano G., Migliardo F., Benedetto A. (2008a) Elastic incoherent neutron scattering on systems of biophysical interest: mean square displacement evaluation from self-distribution function. Journal of Physical Chemistry B,112,8936–8942.
Magazu`S., Maisano G., Migliardo F., Mondelli C. (2004) Mean square displacement relationship in bioprotectant systems by elastic neutron scattering. Biophysics Journal,86, 3241–3249.
Magazu`S., Migliardo F. (2007) Elastic, quasi elastic and inelastic neutron scattering studies on hydrogen-bonded systems of biophysical interest. Chemical Physics Research Journal,1,37–43.
Magazu`S., Migliardo F., Ramirez-Cuesta A.J. (2005) Inelastic neutron scattering study on bioprotectant systems. Journal of Royal Society Interface,2, 527–531.
Magazu`S., Migliardo F., Ramirez-Cuesta A.J. (2007) Changes in water vibrational modes induced by bioprotectant systems. Biophysical Chemistry,125, 138–142.
Magazu`S., Migliardo F., Telling M.T.F. (2006) a,a-trehalose/water solutions. VIII. Study of diffusive dynamics of water by high-resolution quasi elastic neutron scattering.Journal of Physical Chemistry B,110, 1020–1026.
Magazu`S., Migliardo F., Telling M.T.F. (2008b) Structural and dynamical properties of water in sugar mixtures. Food Chemistry,106, 1460–1467.
Murray I.A., Coupland K., Smith J.A., Ansell D., Long R.A. (2000) Intestinal trehalase in a UK population; establishing a normal range and the effect of disease. British Journal of Nutrition, 83,241–245.
Nie Y., de Pablo J.J., Palecek S.P. (2005) Platelet cryopreservation using a trehalose and phosphate formulation. Biotechnology Bioeng, 92, 79–90.
Oku T., Nakamura S. (2000) Estimation of intestinal trehalase activity from a laxative threshold of trehalose and lactulose on healthy female subjects. European Journal of Clinical Nutrition, 54, 783–788.
Pagnotta S.E., RicciM.A., BruniF., McLainS., Magazu` S. (2008) Water structure around trehalose.Chemical Physics, 345, 159–163.
Pakchung A.A.H., Simpson P.J.L., Codd R. (2006) Life on earth. Extremophiles continue to move the goal posts. Environmental Chemistry, 3, 77–93.
Patist A., Zoerb H. (2005) Preservation mechanisms of trehalose in food and biosystems. Colloids and Surfaces B: Biointerfaces, 40, 107–113.
Pollock G.E., Holmstrom C.D. (1951) The trehalose content and the quality of active dry yeast. Cereal Chemistry, 28, 498–505.
Richards A.B., Krakowka S., Dexter L.B., Schmid H., WolterbeekA.P.M., Waalkens-Berendsen D.H., Shigoyuki A., Kurimoto M.(2002) Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies. Food and Chemical Toxicology, 40, 871–898.
Robert H., Le Marrec C., Blanco C., Jebbar M. (2000) Glycinebetaine, carnitine, and choline enhance salinity tolerance and prevent the accumulation of sodium to a level inhibiting growth of Tetragenococcus halophila. Applied Environmental Microbogy, 66, 509–517.
Roser B.J. (1991a) Trehalose drying: a novel replacement for freeze-drying. Biopharmacy,5, 44–53.
Roser B.J. (1991b) Trehalose, a new approach to premium dried foods.Trends Food Science Technology, 2, 166–169.
Rothschild L.J., Mancinelli R.L. (2001) Life in extreme environments. Nature, 409, 1092–1101.
Salas-Mellado M.M., Chang Y.K. (2003) Effect of formulation on the quality of frozen bread dough. Brazilian Archives of Biology and Technology, 46, 461–468.
Schiraldi C., De Rosa M. (2002) The production of biocatalysts and biomolecules from extremophiles. Trends in Biotechnology, 20, 515–521.
Soper A.K. (2000) Probing the structure of water around biological molecules: concepts, constructs, and consequences. Physical B,276–278, 12–26.
Soper A.K., Luzar A. (1992) A neutron diffraction study of dimethyl sulphoxide–water mixtures. Journal of Chemical Physics, 97, 1320–1326.
Tanaka M., Machida Y., Niu S., Ikeda T., Jana N.R., Doi H., Kurosawa M., Nekooki M., Nukina N. (2004) Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nature Medicine,10, 148–154.
Unsworth L.D., van der Oost J., Koutsopoulos S. (2007) Hyperthermophilic enzymes – stability, activity and implementation strategies for high temperature applications. FEBS Journal,274, 4044–4056.
van den Burg B. (2003) Extremophiles as a source for novel enzymes. Current Opinion in Microbiology,6, 213–218.
Van Dijck P., Colavizza D., Smet P., Thevelein J.M. (1995)Differential importance of trehalose in stress resistance in fermenting and nonfermenting Saccharomyces cerevisiae cells. Applied Environmental Microbiology, 61, 109–115.
Varga B., Migliardo F., Takacs E., Vertessy B., Magazu`S., Mondelli C. (2008) Neutron scattering studies on dUTPase complex in presence of bioprotectant systems. Chemical Physics, 345,250–256.
Zhang X.B., Li K., Yau K.H., Tsang K.S., Fok T.F., Li C.K., LeeS.M., Yuen P.M. (2003) Trehalose ameliorates the cryopreservation of cord blood in a preclinical system and increases the recovery of CFUs, long-term culture-initiating cells, and nonobese diabetic-SCID repopulating cells. Transfusion,43, 265–272.
Zhou A., Benjakul S., Pan K., Gong J., Liu X. (2006)Cryoprotective effects of trehalose and sodium lactate on tilapia (Sarotherodon nilotica) surimi during frozen storage.Food Chemistry,96, 96–103.
Angell C.A., Poole P.H., Shao J. (1994) Glassforming liquids, anomalous liquids and polyamorphism in liquids and biopolymers. II Nuovo Cimento D,16, 993–1025.
Branca C., Magazu`S., Maisano G., Migliardo P. (1999) Anomalous cryoprotective effectiveness of trehalose: Raman scattering evidences. Journal of Chemical Physics,111,281–287.
Cordone L., Cottone G., Giuffrida S., Palazzo G., Venturoli G., Viappiani C. (2005) Internal dynamics and protein-matrix coupling in trehalose coated proteins. Biochimica Biophysica Acta,1749, 252–281.
Cottone G., Cicciotti G., Cordone L. (2002) Protein-trehalose-water structures in trehalose coated carboxy-myoglobin. Journal of Chemical Physics,117, 9862–9866.
Crowe J.H. (1975) The physiology of cryptobiosis in tardigrades.In: R. Higgins (ed.) International symposium on tardigrades, Italy, June 17–19, 1974. Mem. Ist. Ital. Idrobiol. 32 (Suppl.),37–59.
Crowe J.H., Crowe L.M., Carpenter J.F., Wistrom C. (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochemical Journal, 242, 1–10.
Crowe J.H., Crowe L.M., Chapman D. (1984a) Infra-red spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Archives of Biochemical Biophysics, 232, 400–407.
Crowe J.H., Crowe L.M., Chapman D. (1984b) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science,223, 701–703.
Danielson M., Rollin S.T. (2004) USDA determines Cargill’sascend trehalose suitable for meat products. Report to Cargill, Cargill Health and Food Technologies (H&FT).
D’Arrigo G., Maisano G., Mallamace F., Migliardo P., Wanderlingh F. (1981) Raman scattering and structure of normal and supercooled water. Journal of Chemical Physics,75,4264–4271.
Duong T., Barrangou R., Michael Russell W., Klaenhammer T.R.(2006) Characterization of the tre locus and analysis of trehalose cryoprotection in Lactobacillus acidophilus NCFM. Applied and Environmental Microbiology,72, 1218–1225.
Gleeson M., Bishop N.C. (2000a) Studies on the potential use of trehalose as an ingredient of sports beverage; Study 1 the Glycaemic index of trehalose. Report to British Sugar, University of Birmingham, UK.
Gleeson M., Bishop N.C. (2000b) Studies on the potential use of trehalose as an ingredient of sports beverage; Study 2 effects of trehalose, glucose, or placebo ingestion on metabolic responses, perception of effort and endurance performance during constant load cycling to fatigue. Report to BritishSugar, University of Birmingham, UK.
Guo N., Puhlev I., Brown D.R., Mansbridge J., Levine F. (2000) Trehalose production confers desiccation tolerance on human cells. Nature Biotechnology,18, 168–171.
Hamaratoglu F., Eroglu A., Toner M., Sadler K.C. (2005) Cryopreservation of starfish oocytes. Cryobiology, 50, 38–47.
Hiashiyama T. (2002) Novel function and application of trehalose. Pure Applied Chemistry,74, 123–129.
Ivy J.L. (2001) The glycaemic index and performance enhancing capacity of trehalose. Report to Cargill, University of Texas, USA.
King S.M. (1999). Small angle neutron scattering.In Modern Techniques for Polymer Characterisationeds Pethrick R.A., Dawkins J.V. John Wiley and Sons, UK. pp. 171–232.
Lerbret A., Bordat P., Affouard F., Descamps M., Migliardo F.(2005) How homogeneous are the trehalose, maltose, and sucrose water solutions? An insight from molecular dynamics simulations. Journal of Physical Chemistry B,109,11046–11053.
Lindner P. (1991).Neutron, X-Ray and Light Scattering. Th.Zemb, The Netherlands.
Magazu`S., Maisano G., Migliardo F., Benedetto A. (2008a) Elastic incoherent neutron scattering on systems of biophysical interest: mean square displacement evaluation from self-distribution function. Journal of Physical Chemistry B,112,8936–8942.
Magazu`S., Maisano G., Migliardo F., Mondelli C. (2004) Mean square displacement relationship in bioprotectant systems by elastic neutron scattering. Biophysics Journal,86, 3241–3249.
Magazu`S., Migliardo F. (2007) Elastic, quasi elastic and inelastic neutron scattering studies on hydrogen-bonded systems of biophysical interest. Chemical Physics Research Journal,1,37–43.
Magazu`S., Migliardo F., Ramirez-Cuesta A.J. (2005) Inelastic neutron scattering study on bioprotectant systems. Journal of Royal Society Interface,2, 527–531.
Magazu`S., Migliardo F., Ramirez-Cuesta A.J. (2007) Changes in water vibrational modes induced by bioprotectant systems. Biophysical Chemistry,125, 138–142.
Magazu`S., Migliardo F., Telling M.T.F. (2006) a,a-trehalose/water solutions. VIII. Study of diffusive dynamics of water by high-resolution quasi elastic neutron scattering.Journal of Physical Chemistry B,110, 1020–1026.
Magazu`S., Migliardo F., Telling M.T.F. (2008b) Structural and dynamical properties of water in sugar mixtures. Food Chemistry,106, 1460–1467.
Murray I.A., Coupland K., Smith J.A., Ansell D., Long R.A. (2000) Intestinal trehalase in a UK population; establishing a normal range and the effect of disease. British Journal of Nutrition, 83,241–245.
Nie Y., de Pablo J.J., Palecek S.P. (2005) Platelet cryopreservation using a trehalose and phosphate formulation. Biotechnology Bioeng, 92, 79–90.
Oku T., Nakamura S. (2000) Estimation of intestinal trehalase activity from a laxative threshold of trehalose and lactulose on healthy female subjects. European Journal of Clinical Nutrition, 54, 783–788.
Pagnotta S.E., RicciM.A., BruniF., McLainS., Magazu` S. (2008) Water structure around trehalose.Chemical Physics, 345, 159–163.
Pakchung A.A.H., Simpson P.J.L., Codd R. (2006) Life on earth. Extremophiles continue to move the goal posts. Environmental Chemistry, 3, 77–93.
Patist A., Zoerb H. (2005) Preservation mechanisms of trehalose in food and biosystems. Colloids and Surfaces B: Biointerfaces, 40, 107–113.
Pollock G.E., Holmstrom C.D. (1951) The trehalose content and the quality of active dry yeast. Cereal Chemistry, 28, 498–505.
Richards A.B., Krakowka S., Dexter L.B., Schmid H., WolterbeekA.P.M., Waalkens-Berendsen D.H., Shigoyuki A., Kurimoto M.(2002) Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies. Food and Chemical Toxicology, 40, 871–898.
Robert H., Le Marrec C., Blanco C., Jebbar M. (2000) Glycinebetaine, carnitine, and choline enhance salinity tolerance and prevent the accumulation of sodium to a level inhibiting growth of Tetragenococcus halophila. Applied Environmental Microbogy, 66, 509–517.
Roser B.J. (1991a) Trehalose drying: a novel replacement for freeze-drying. Biopharmacy,5, 44–53.
Roser B.J. (1991b) Trehalose, a new approach to premium dried foods.Trends Food Science Technology, 2, 166–169.
Rothschild L.J., Mancinelli R.L. (2001) Life in extreme environments. Nature, 409, 1092–1101.
Salas-Mellado M.M., Chang Y.K. (2003) Effect of formulation on the quality of frozen bread dough. Brazilian Archives of Biology and Technology, 46, 461–468.
Schiraldi C., De Rosa M. (2002) The production of biocatalysts and biomolecules from extremophiles. Trends in Biotechnology, 20, 515–521.
Soper A.K. (2000) Probing the structure of water around biological molecules: concepts, constructs, and consequences. Physical B,276–278, 12–26.
Soper A.K., Luzar A. (1992) A neutron diffraction study of dimethyl sulphoxide–water mixtures. Journal of Chemical Physics, 97, 1320–1326.
Tanaka M., Machida Y., Niu S., Ikeda T., Jana N.R., Doi H., Kurosawa M., Nekooki M., Nukina N. (2004) Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nature Medicine,10, 148–154.
Unsworth L.D., van der Oost J., Koutsopoulos S. (2007) Hyperthermophilic enzymes – stability, activity and implementation strategies for high temperature applications. FEBS Journal,274, 4044–4056.
van den Burg B. (2003) Extremophiles as a source for novel enzymes. Current Opinion in Microbiology,6, 213–218.
Van Dijck P., Colavizza D., Smet P., Thevelein J.M. (1995)Differential importance of trehalose in stress resistance in fermenting and nonfermenting Saccharomyces cerevisiae cells. Applied Environmental Microbiology, 61, 109–115.
Varga B., Migliardo F., Takacs E., Vertessy B., Magazu`S., Mondelli C. (2008) Neutron scattering studies on dUTPase complex in presence of bioprotectant systems. Chemical Physics, 345,250–256.
Zhang X.B., Li K., Yau K.H., Tsang K.S., Fok T.F., Li C.K., LeeS.M., Yuen P.M. (2003) Trehalose ameliorates the cryopreservation of cord blood in a preclinical system and increases the recovery of CFUs, long-term culture-initiating cells, and nonobese diabetic-SCID repopulating cells. Transfusion,43, 265–272.
Zhou A., Benjakul S., Pan K., Gong J., Liu X. (2006)Cryoprotective effects of trehalose and sodium lactate on tilapia (Sarotherodon nilotica) surimi during frozen storage.Food Chemistry,96, 96–103.
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Jun 30, 2010
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