1932

Abstract

Enzyme technologies can be used to create food dispersions with novel functional attributes using structural design principles. Enzymes that utilize food-grade proteins and/or polysaccharides as substrates have gained recent interest among food scientists. The utilization of enzymes for structuring foods is an ecologically and economically viable alternative to the utilization of chemical cross-linking and depolymerization agents. This review highlights recent progress in the use of enzymes to modify food structures, particularly the interfacial and/or bulk properties of food dispersions with special emphasis on commercially available enzymes. Cross-linking enzymes such as transglutaminase and laccase promote the formation of intra- and intermolecular bonds between biopolymers to improve stability and functionality, whereas various degrading enzymes such as proteases alter the native conformation of proteins, leading to self-assembly of hierarchically ordered colloids. Results of this bio-inspired approach show that rational use of structure-affecting enzymes may enable food manufacturers to produce food dispersions with improved physical, functional, textural, and optical properties.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-food-030216-025753
2017-02-28
2024-10-03
Loading full text...

Full text loading...

/deliver/fulltext/food/8/1/annurev-food-030216-025753.html?itemId=/content/journals/10.1146/annurev-food-030216-025753&mimeType=html&fmt=ahah

Literature Cited

  1. Adamcik J, Mezzenga R. 2012. Study of amyloid fibrils via atomic force microscopy. Curr. Opin. Colloid Interface Sci. 17:369–76 [Google Scholar]
  2. Agboola SO, Dalgleish DG. 1996. Enzymatic hydrolysis of milk proteins used for emulsion formation. 1. Kinetics of protein breakdown and storage stability of the emulsions. J. Agric. Food Chem. 44:3631–36 [Google Scholar]
  3. Aguilera JM. 2006. Seligman lecture 2005. Food product engineering: building the right structures. J. Sci. Food Agric. 86:1147–55 [Google Scholar]
  4. Agyare KK, Addo K, Xiong YL. 2009. Emulsifying and foaming properties of transglutaminase-treated wheat gluten hydrolysate as influenced by pH, temperature and salt. Food Hydrocoll. 23:72–81 [Google Scholar]
  5. Akkermans C, van der Goot AJ, Venema P, van der Linden E, Boom RM. 2008a. Formation of fibrillar whey protein aggregates: influence of heat and shear treatment, and resulting rheology. Food Hydrocoll. 22:1315–25 [Google Scholar]
  6. Akkermans C, Venema P, Goot A, Boom R, Linden E. 2008b. Enzyme-induced formation of β-lactoglobulin fibrils by AspN endoproteinase. Food Biophys 3:390–94 [Google Scholar]
  7. Autio K, Kruus K, Knaapila A, Gerber N, Flander L, Buchert J. 2005. Kinetics of transglutaminase-induced cross-linking of wheat proteins in dough. J. Agric. Food Chem. 53:1039–45 [Google Scholar]
  8. Azarikia F, Wu B-C, Abbasi S, McClements DJ. 2015. Stabilization of biopolymer microgels formed by electrostatic complexation: influence of enzyme (laccase) cross-linking on pH, thermal, and mechanical stability. Food Res. Int. 78:18–26 [Google Scholar]
  9. Bao SS, Hu XC, Zhang K, Xu XK, Zhang HM, Huang H. 2010. Characterization of spray-dried microalgal oil encapsulated in cross-linked sodium caseinate matrix induced by microbial transglutaminase. J. Food Sci. 76:E112–18 [Google Scholar]
  10. Beicht J, Zeeb B, Gibis M, Fischer L, Weiss J. 2013. Influence of layer thickness and composition of cross-linked multilayered oil-in-water emulsions on the release behavior of lutein. Food Funct 4:1457–67 [Google Scholar]
  11. Bourbonnais R, Paice MG. 1990. Oxidation of non-phenolic substrates: an expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102 [Google Scholar]
  12. Buchert J, Cura DE, Ma H, Gasparetti C, Monogioudi E. et al. 2010. Crosslinking food proteins for improved functionality. Annu. Rev. Food Sci. Technol. 1:113–38 [Google Scholar]
  13. Burke MD, Park JO, Srinivasarao M, Khan SA. 2005. A novel enzymatic technique for limiting drug mobility in a hydrogel matrix. J. Controlled Release 104:141–53 [Google Scholar]
  14. Chang C, Tu S, Ghosh S, Nickerson MT. 2015. Effect of pH on the inter-relationships between the physicochemical, interfacial and emulsifying properties for pea, soy, lentil and canola protein isolates. Food Res. Int. 77:360–67 [Google Scholar]
  15. Chen B, McClements DJ, Gray DA, Decker EA. 2010. Stabilization of soybean oil bodies by enzyme (laccase) cross-linking of adsorbed beet pectin coatings. J. Agric. Food Chem. 58:9259–65 [Google Scholar]
  16. Clare DA, Daubert CR. 2011. Expanded functionality of modified whey protein dispersions after transglutaminase catalysis. J. Food Sci. 76:C576–84 [Google Scholar]
  17. Claus H. 2004. Laccases: structure, reactions, distribution. Micron 35:93–96 [Google Scholar]
  18. De Jong GAH, Koppelman SJ. 2002. Transglutaminase catalyzed reactions: impact on food applications. J. Food Sci. 67:2798–806 [Google Scholar]
  19. Dickinson E. 1997. Enzymatic crosslinking as a tool for food colloid rheology control and interfacial stabilization. Trends Food Sci. Technol. 8:334–39 [Google Scholar]
  20. Dickinson E. 2012. Emulsion gels: the structuring of soft solids with protein-stabilized oil droplets. Food Hydrocoll. 28:224–41 [Google Scholar]
  21. Dickinson E. 2015. Colloids in food: ingredients, structure, and stability. Annu. Rev. Food Sci. Technol. 6:211–33 [Google Scholar]
  22. Dickinson E, Yamamoto Y. 1996. Rheology of milk protein gels and protein-stabilized emulsion gels cross-linked with transglutaminase. J. Agric. Food Chem. 44:1371–77 [Google Scholar]
  23. Doucet D, Foegeding EA. 2005. Gel formation of peptides produced by extensive enzymatic hydrolysis of β-lactoglobulin. Biomacromolecules 6:1140–48 [Google Scholar]
  24. Doucet D, Gauthier SF, Foegeding EA. 2001. Rheological characterization of a gel formed during extensive enzymatic hydrolysis. J. Food Sci. 66:711–15 [Google Scholar]
  25. Doucet D, Gauthier SF, Otter DE, Foegeding EA. 2003a. Enzyme-induced gelation of extensively hydrolyzed whey proteins by alcalase: comparison with the plastein reaction and characterization of interactions. J. Agric. Food Chem. 51:6036–42 [Google Scholar]
  26. Doucet D, Otter DE, Gauthier SF, Foegeding EA. 2003b. Enzyme-induced gelation of extensively hydrolyzed whey proteins by alcalase: peptide identification and determination of enzyme specificity. J. Agric. Food Chem. 51:6300–8 [Google Scholar]
  27. Færgemand M, Murray BS, Dickinson E. 1997. Cross-linking of milk proteins with transglutaminase at the oil-water interface. J. Agric. Food Chem. 45:2514–19 [Google Scholar]
  28. Flanagan J, Gunning Y, FitzGerald RJ. 2003. Effect of cross-linking with transglutaminase on the heat stability and some functional characteristics of sodium caseinate. Food Res. Int. 36:267–74 [Google Scholar]
  29. Folk JE, Finlayson JS. 1977. The epsilon-(gamma-glutamyl)lysine crosslink and the catalytic role of transglutaminases. Adv. Protein Chem. 31:1–133 [Google Scholar]
  30. Forneris F, Mattevi A. 2008. Enzymes without borders: mobilizing substrates, delivering products. Science 321:213–16 [Google Scholar]
  31. Gerrard JA. 2002. Protein-protein crosslinking in food: methods, consequences, applications. Trends Food Sci. Technol. 13:391–99 [Google Scholar]
  32. Giosafatto CVL, Rigby NM, Wellner N, Ridout M, Husband F, Mackie AR. 2012. Microbial transglutaminase-mediated modification of ovalbumin. Food Hydrocoll. 26:261–67 [Google Scholar]
  33. Grossmann L, Zeeb B, Weiss J. 2016. Diffusion behavior of microbial transglutaminase to induce protein crosslinking in oil-in-water emulsions. J. Dispers. Sci. Technol. 37:1745–50 [Google Scholar]
  34. Grossmann L, Wefers D, Bunzel M, Weiss J, Zeeb B. 2017. Accessibility of transglutaminase to induce protein crosslinking in gelled food matrices: influence of network structure. LWT Food Sci. Technol. 75:271–78 [Google Scholar]
  35. Gübitz GM, Paulo AC. 2003. New substrates for reliable enzymes: enzymatic modification of polymers. Curr. Opin. Biotechnol. 14:577–82 [Google Scholar]
  36. Hinz K, Huppertz T, Kulozik U, Kelly AL. 2007. Influence of enzymatic cross-linking on milk fat globules and emulsifying properties of milk proteins. Int. Dairy J. 17:289–93 [Google Scholar]
  37. Hu X, Zhao M, Sun W, Zhao G, Ren J. 2011. Effects of microfluidization treatment and transglutaminase cross-linking on physicochemical, functional, and conformational properties of peanut protein isolate. J. Agric. Food Chem. 59:8886–94 [Google Scholar]
  38. Joye IJ, McClements DJ. 2013. Production of nanoparticles by anti-solvent precipitation for use in food systems. Trends Food Sci. Technol. 34:2109–23 [Google Scholar]
  39. Joye IJ, McClements DJ. 2014. Biopolymer-based nanoparticles and microparticles: fabrication, characterization, and application. Curr. Opin. Colloid Interface Sci. 19:5417–27 [Google Scholar]
  40. Ju ZY, Kilara A. 1998. Gelation of hydrolysates of a whey protein isolate induced by heat, protease, salts and acid. Int. Dairy J. 8:303–9 [Google Scholar]
  41. Jung J, Wicker L. 2012a. Laccase mediated conjugation of heat treated β-lactoglobulin and sugar beet pectin. Carbohydr. Polym. 89:1244–49 [Google Scholar]
  42. Jung J, Wicker L. 2012b. Laccase mediated conjugation of sugar beet pectin and the effect on emulsion stability. Food Hydrocoll. 28:168–73 [Google Scholar]
  43. Kellerby SS, Yeun SG, McClements DJ, Decker EA. 2006. Lipid oxidation in a menhaden oil-in-water emulsion stabilized by sodium caseinate cross-linked with transglutaminase. J. Agric. Food Chem. 54:10222–27 [Google Scholar]
  44. Kilara A, Panyam D. 2003. Peptides from milk proteins and their properties. Crit. Rev. Food Sci. Nutr. 43:607–33 [Google Scholar]
  45. Kroes-Nijboer A, Venema P, Bouman J, Van Der Linden E. 2011. Influence of protein hydrolysis on the growth kinetics of β-lg fibrils. Langmuir 27:5753–61 [Google Scholar]
  46. Kudanga T, Nyanhongo GS, Guebitz GM, Burton S. 2011. Potential applications of laccase-mediated coupling and grafting reactions: a review. Enzyme Microb. Technol. 48:195–208 [Google Scholar]
  47. Kuraishi C, Yamazaki K, Susa Y. 2001. Transglutaminase: its utilization in the food industry. Food Rev. Int. 17:221–46 [Google Scholar]
  48. Kurth L, Rogers PJ. 1984. Transglutaminase catalyzed cross-linking of myosin to soya protein, casein and gluten. J. Food Sci. 49:573–76 [Google Scholar]
  49. Littoz F, McClements DJ. 2008. Bio-mimetic approach to improving emulsion stability: cross-linking adsorbed beet pectin layers using laccase. Food Hydrocoll. 22:1203–11 [Google Scholar]
  50. Ma H, Forssell P, Kylli P, Lampi AM, Buchert J. et al. 2012. Transglutaminase catalyzed cross-linking of sodium caseinate improves oxidative stability of flaxseed oil emulsion. J. Agric. Food Chem. 60:6223–29 [Google Scholar]
  51. Ma H, Forssell P, Partanen R, Buchert J, Boer H. 2011. Improving laccase catalyzed cross-linking of whey protein isolate and their application as emulsifiers. J. Agric. Food Chem. 59:1406–14 [Google Scholar]
  52. Macierzanka A, Bordron F, Rigby NM, Mills ENC, Lille M. et al. 2011. Transglutaminase cross-linking kinetics of sodium caseinate is changed after emulsification. Food Hydrocoll. 25:843–50 [Google Scholar]
  53. Maier C, Oechsle AM, Weiss J. 2015. Cross-linking oppositely charged oil-in-water emulsions to enhance heteroaggregate stability. Colloids Surf. B 135:525–32 [Google Scholar]
  54. Maier C, Zeeb B, Weiss J. 2014. Investigations into aggregate formation with oppositely charged oil-in-water emulsions at different pH values. Colloids Surf. B 117:368–75 [Google Scholar]
  55. Mattinen M-L, Hellman M, Permi P, Autio K, Kalkkinen N, Buchert J. 2006. Effect of protein structure on laccase-catalyzed protein oligomerization. J. Agric. Food Chem. 54:8883–90 [Google Scholar]
  56. McClements DJ, Decker EA, Park Y, Weiss J. 2009. Structural design principles for delivery of bioactive components in nutraceuticals and functional foods. Crit. Rev. Food Sci. Nutr. 49:577–606 [Google Scholar]
  57. McClements DJ, Gumus CE. 2016. Natural emulsifiers—biosurfactants, phospholipids, biopolymers, and colloidal particles: molecular and physicochemical basis of functional performance. Adv. Colloid Interface Sci. 234:3–26 [Google Scholar]
  58. Minussi RC, Pastore GM, Durán N. 2002. Potential applications of laccase in the food industry. Trends Food Sci. Technol. 13:205–16 [Google Scholar]
  59. Mokoonlall A, Pfannstiel J, Struch M, Berger RG, Hinrichs J. 2015. Structure modification of stirred fermented milk gel due to laccase-catalysed protein crosslinking in a post-processing step. Innov. Food Sci. Emerg. Technol. 33:563–70 [Google Scholar]
  60. Moreira IP, Sasselli IR, Cannon DA, Hughes M, Lamprou DA. et al. 2016. Enzymatically activated emulsions stabilised by interfacial nanofibre networks. Soft Matter 12:2623–31 [Google Scholar]
  61. Motoki M, Seguro K. 1998. Transglutaminase and its use for food processing. Trends Food Sci. Technol. 9:204–10 [Google Scholar]
  62. Paananen A, Ercili-Cura D, Saloheimo M, Lantto R, Linder MB. 2013. Directing enzymatic cross-linking activity to the air-water interface by a fusion protein approach. Soft Matter 9:1612–19 [Google Scholar]
  63. Partanen R, Forssell P, Mackie A, Blomberg E. 2013. Interfacial cross-linking of β-casein changes the structure of the adsorbed layer. Food Hydrocoll. 32:271–77 [Google Scholar]
  64. Pezzella C, Guarino L, Piscitelli A. 2015. How to enjoy laccases. Cell. Mol. Life Sci. 72:923–40 [Google Scholar]
  65. Raikos V. 2014. Enzymatic hydrolysis of milk proteins as a tool for modification of functional properties at interfaces of emulsions and foams: a review. Curr. Nutr. Food Sci. 10:134–40 [Google Scholar]
  66. Rodríguez Couto S, Toca Herrera JL. 2006. Industrial and biotechnological applications of laccases: a review. Biotechnol. Adv. 24:500–13 [Google Scholar]
  67. Saricay Y, Dhayal SK, Wierenga PA, De Vries R. 2012. Protein cluster formation during enzymatic cross-linking of globular proteins. Faraday Discuss. 158:51–63 [Google Scholar]
  68. Scholten E, Moschakis T, Biliaderis CG. 2014. Biopolymer composites for engineering food structures to control product functionality. Food Struct. 1:39–54 [Google Scholar]
  69. Sharma R, Zakora M, Qvist KB. 2002. Characteristics of oil-water emulsions stabilised by an industrial α-lactalbumin concentrate, cross-linked before and after emulsification, by a microbial transglutaminase. Food Chem. 79:493–500 [Google Scholar]
  70. Steffensen CL, Andersen ML, Degn PE, Nielsen JH. 2008. Cross-linking proteins by laccase-catalyzed oxidation: importance relative to other modifications. J. Agric. Food Chem. 56:12002–10 [Google Scholar]
  71. Tang CH, Chen L, Foegeding EA. 2011. Mechanical and water-holding properties and microstructures of soy protein isolate emulsion gels induced by CaCl2, glucono-δ-lactone (GDL), and transglutaminase: influence of thermal treatments before and/or after emulsification. J. Agric. Food Chem. 59:4071–77 [Google Scholar]
  72. Tarhan O, Spotti MJ, Schaffter S, Corvalan CM, Campanella OH. 2016. Rheological and structural characterization of whey protein gelation induced by enzymatic hydrolysis. Food Hydrocoll. 61:211–20 [Google Scholar]
  73. Thurston CF. 1994. The structure and function of fungal laccases. Microbiology 140:19–26 [Google Scholar]
  74. Turgeon SL, Laneuville SI, Stefan K, Ian TN, Johan BU. 2009. Protein + polysaccharide coacervates and complexes: from scientific background to their application as functional ingredients in food products. Modern Biopolymer Science S Kasapis, IT Norton, JB Ubbink 327–63 San Diego: Academic Press [Google Scholar]
  75. Ubbink J. 2012. Soft matter approaches to structured foods: from “cook-and-look” to rational food design?. Faraday Discuss 158:9–35 [Google Scholar]
  76. Varjonen S, Laaksonen P, Paananen A, Valo H, Hähl H. et al. 2011. Self-assembly of cellulose nanofibrils by genetically engineered fusion proteins. Soft Matter 7:2402–11 [Google Scholar]
  77. Xu X, Liu W, Liu C, Luo L, Chen J. et al. 2016. Effect of limited enzymatic hydrolysis on structure and emulsifying properties of rice glutelin. Food Hydrocoll. 61:251–60 [Google Scholar]
  78. Yang M, Liu F, Tang CH. 2011. Properties and microstructure of transglutaminase-set soy protein-stabilized emulsion gels. Food Res. Int. 52:409–18 [Google Scholar]
  79. Zeeb B, Beicht J, Eisele T, Gibis M, Fischer L, Weiss J. 2013a. Transglutaminase-induced crosslinking of sodium caseinate stabilized oil droplets in oil-in-water emulsions. Food Res. Int. 54:1712–21 [Google Scholar]
  80. Zeeb B, Fischer L, Weiss J. 2011. Cross-linking of interfacial layers affects the salt and temperature stability of multilayered emulsions consisting of fish gelatin and sugar beet pectin. J. Agric. Food Chem. 59:10546–55 [Google Scholar]
  81. Zeeb B, Fischer L, Weiss J. 2014. Stabilization of food dispersions by enzymes. Food Funct 5:198–213 [Google Scholar]
  82. Zeeb B, Gibis M, Fischer L, Weiss J. 2012a. Crosslinking of interfacial layers in multilayered oil-in-water emulsions using laccase: characterization and pH-stability. Food Hydrocoll. 27:126–36 [Google Scholar]
  83. Zeeb B, Gibis M, Fischer L, Weiss J. 2012b. Influence of interfacial properties on Ostwald ripening in crosslinked multilayered oil-in-water emulsions. J. Colloid Interface Sci. 387:65–73 [Google Scholar]
  84. Zeeb B, Grossmann L, Weiss J. 2016. Accessibility of transglutaminase to induce protein crosslinking in gelled food matrices: impact of membrane structure. Food Biophys 11:176–83 [Google Scholar]
  85. Zeeb B, Lopez-Pena CL, Weiss J, McClements DJ. 2015a. Controlling lipid digestion using enzyme-induced crosslinking of biopolymer interfacial layers in multilayer emulsions. Food Hydrocoll. 46:125–33 [Google Scholar]
  86. Zeeb B, Salminen H, Fischer L, Weiss J. 2013b. Impact of heat and laccase on the pH and freeze-thaw stability of oil-in-water emulsions stabilized by adsorbed biopolymer nanoparticles. Food Biophys 9:125–37 [Google Scholar]
  87. Zeeb B, Weiss J, McClements DJ. 2015b. Electrostatic modulation and enzymatic cross-linking of interfacial layers impacts gastrointestinal fate of multilayer emulsions. Food Chem 180:257–64 [Google Scholar]
  88. Zhu Y, Rinzema A, Tramper J, Bol J. 1995. Microbial transglutaminase: a review of its production and application in food processing. Appl. Microbiol. Biotechnol. 44:277–82 [Google Scholar]
  89. Zhu Y, Tramper J. 2008. Novel applications for microbial transglutaminase beyond food processing. Trends Biotechnol 26:559–65 [Google Scholar]
/content/journals/10.1146/annurev-food-030216-025753
Loading
/content/journals/10.1146/annurev-food-030216-025753
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error