Changes in protein conformation and surface hydrophobicity upon peroxidase-catalyzed cross-linking of apo-α-lactalbumin

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 38, 2014, Pages 9345-9352

  Saricay, Yunus ^a   Wierenga, Peter A ^a   De Vries, Renko ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Enzymatic cross linking; Horseradish peroxidase; Protein nanoparticles; Structural transition; Surface hydrophobicity; lactalbumin

Indexed keywords

CATALYSIS; HYDROPHOBICITY; PROTEINS;

CONFORMATIONAL CHANGE; HORSE-RADISH PEROXIDASE; MOLECULAR CONFORMATION; PROTEIN CONFORMATION; PROTEIN NANOPARTICLES; PROTEIN SURFACE HYDROPHOBICITIES; STRUCTURAL TRANSITIONS; SURFACE HYDROPHOBICITY;

CROSSLINKING;

ARMORACIA RUSTICANA;

APO-ALPHA-LACTALBUMIN; APOPROTEIN; HORSERADISH PEROXIDASE; LACTALBUMIN;

ANIMAL; BOVINAE; CATALYSIS; CHEMICAL PHENOMENA; CHEMISTRY; CIRCULAR DICHROISM; PROTEIN CONFORMATION;

ANIMALS; APOPROTEINS; CATALYSIS; CATTLE; CIRCULAR DICHROISM; HORSERADISH PEROXIDASE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LACTALBUMIN; PROTEIN CONFORMATION;

EID: 84924390285     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf502664q     Document Type: Article

References (58)

1. Jones, O. G.; McClements, D. J. Functional biopolymer particles: Design, fabrication, and applications. Compr. Rev. Food Sci. Food Saf. 2010, 9, 374-397.
2. Panyam, D.; Kilara, A. Enhancing the functionality of food proteins by enzymatic modification. Trends Food Sci. Technol. 1996, 7, 120-125.
3. Foegeding, E. A.; Davis, J. P. Food protein functionality: A comprehensive approach. Food Hydrocolloids 2011, 25, 1853-1864.
4. Kluger, R.; Alagic, A. Chemical cross-linking and protein-protein interactions-A review with illustrative protocols. Bioorg. Chem. 2004, 32, 451-472.
5. Considine, T.; Patel, H. A.; Anema, S. G.; Singh, H.; Creamer, L. K. Interactions of milk proteins during heat and high hydrostatic pressure treatments-A review. Innov. Food Sci. Emerg. Technol. 2007, 8, 1-23.
6. Fass, D. Disulfide bonding in protein biophysics. Annu. Rev. Biophys. 2012, 41, 63-79.
7. Shimada, K.; Cheftel, J. C. Sulfhydryl-group disulfide bond interchange reactions during heat-induced gelation of whey-protein isolate. J. Agric. Food Chem. 1989, 37, 161-168.
8. Liu, X. M.; Powers, J. R.; Swanson, B. G.; Hill, H. H.; Clark, S. Modification of whey protein concentrate hydrophobicity by high hydrostatic pressure. Innov. Food Sci. Emerg. Technol. 2005, 6, 310-317.
9. Nicolai, T.; Britten, M.; Schmitt, C. β-Lactoglobulin and WPI aggregates: Formation, structure and applications. Food Hydrocolloids 2011, 25, 1945-1962.
10. Alting, A. C.; Hamer, R. J.; de Kruif, C. G.; Paques, M.; Visschers, R. W. Number of thiol groups rather than the size of the aggregates determines the hardness of cold set whey protein gels. Food Hydrocolloids 2003, 17, 469-479.
11. Huebner, F. R.; Bietz, J. A.; Wall, J. S. Disulfide bonds: Key to wheat protein functionality. Adv. Exp. Med. Biol. 1977, 86A, 67-88.
12. s1-casein as a model. J. Agric. Food Chem. 1990, 38, 1303-1306.
13. Foegeding, E. A.; Davis, J. P.; Doucet, D.; McGuffey, M. K. Advances in modifying and understanding whey protein functionality. Trends Food Sci. Technol. 2002, 13, 151-159.
14. Schmitt, C.; Moitzi, C.; Bovay, C.; Rouvet, M.; Bovetto, L.; Donato, L.; Leser, M. E.; Schurtenberger, P.; Stradner, A. Internal structure and colloidal behaviour of covalent whey protein microgels obtained by heat treatment. Soft Matter 2010, 6, 4876-4884.
15. Miller, A. G.; Meade, S. J.; Gerrard, J. A. New insights into protein crosslinking via the maillard reaction: Structural requirements, the effect on enzyme function, and predicted efficacy of crosslinking inhibitors as anti-ageing therapeutics. Bioorg. Med. Chem. 2003, 11, 843-852.
16. Oliver, C. M.; Melton, L. D.; Stanley, R. A. Creating proteins with novel functionality via the Maillard reaction: A review. Crit. Rev. Food Sci. Nutr. 2006, 46, 337-350.
17. Liu, J.; Ru, Q.; Ding, Y. Glycation a promising method for food protein modification: Physicochemical properties and structure, a review. Food Res. Int. 2012, 49, 170-183.
18. De Goes-Favoni, S. P.; Bueno, F. R. Microbial transglutaminase: General characteristics and performance in food processing technology. Food Biotechnol. 2014, 28, 1-24.
19. Partanen, R.; Forssell, P.; Mackie, A.; Blomberg, E. Interfacial cross-linking of β-casein changes the structure of the adsorbed layer. Food Hydrocolloids 2013, 32, 271-277.
20. Truong, V. D.; Clare, D. A.; Catignani, G. L.; Swaisgood, H. E. Cross-linking and rheological changes of whey proteins treated with microbial transglutaminase. J. Agric. Food Chem. 2004, 52, 1170-1176.
21. Ozrenk, E. The use of transglutaminase in dairy products. Int. J. Dairy Technol. 2006, 59, 1-7.
22. Jaros, D.; Partschefeld, C.; Henle, T.; Rohm, H. Transglutaminase in dairy products: Chemistry, physics, applications. J. Texture Stud. 2006, 37, 113-155.
23. Nieuwenhuizen, W. F.; Dekker, H. L.; Gröneveld, T.; de Koster, C. G.; de Jong, G. A. H. Transglutaminase-mediated modification of glutamine and lysine residues in native bovine β-lactoglobulin. Biotechnol. Bioeng. 2004, 85, 248-258.
24. Eissa, A. S.; Puhl, C.; Kadla, J. F.; Khan, S. A. Enzymatic crosslinking of β-lactoglobulin: Conformational properties using FTIR spectroscopy. Biomacromolecules 2006, 7, 1707-1713.
25. Agyare, K. K.; Damodaran, S. pH-stability and thermal properties of microbial transglutaminase-treated whey protein isolate. J. Agric. Food Chem. 2010, 58, 1946-1953.
26. 2+-independent microbial transglutaminase from Streptomyces lydicus. Food Hydrocolloids 1997, 11, 19-25.
27. Burke, M. D.; Ha, S. Y.; Pysz, M. A.; Khan, S. A. Rheology of protein gels synthesized through a combined enzymatic and heat treatment method. Int. J. Biol. Macromol. 2002, 31, 37-44.
28. Buchert, J.; Cura, D. E.; Ma, H.; Gasparetti, C.; Monogioudi, E.; Faccio, G.; Mattinen, M.; Boer, H.; Partanen, R.; Selinheimo, E.; Lantto, R.; Kruus, K. Crosslinking food proteins for improved functionality. Annu. Rev. Food Sci. Technol. 2010, 1, 113-38.
29. Thalmann, C. R.; Lotzbeyer, T. Enzymatic cross-linking of proteins with tyrosinase. Eur. Food Res. Technol. 2002, 214, 276-281.
30. Faergemand, M.; Otte, J.; Qvist, K. B. Cross-linking of whey proteins by enzymatic oxidation. J. Agric. Food Chem. 1998, 46, 1326-1333.
31. Heck, T.; Faccio, G.; Richter, M.; Thony-Meyer, L. Enzymecatalyzed protein crosslinking. Appl. Microbiol. Biotechnol. 2013, 97, 461-475.
32. Mattinen, M. L.; Hellman, M.; Permi, P.; Autio, K.; Kalkkinen, N.; Buchert, J. Effect of protein structure on laccase-catalyzed protein oligomerization. J. Agric. Food Chem. 2006, 54, 8883-8890.
33. Elliott, K. A. Oxidations catalysed by horseradish- and milkperoxidases. Biochem. J. 1932, 26, 1281-1290.
34. Steffensen, C. L.; Andersen, M. L.; Degn, P. E.; Nielsen, J. H. Cross-Linking proteins by laccase-catalyzed oxidation: Importance relative to other modifications. J. Agric. Food Chem. 2008, 56, 12002-12010.
35. Lantto, R.; Puolanne, E.; Katina, K.; Niemisto, M.; Buchert, J.; Autio, K. Effect of laccase and transglutaminase on the textural and water-binding properties of cooked chicken breast meat gels. Eur. Food Res. Technol. 2007, 225, 75-83.
36. Lantto, R.; Puolanne, E.; Kalkkinen, N.; Buchert, J.; Autio, K. Enzyme-aided modification of chicken-breast myofibril proteins: Effect of laccase and transglutaminase on gelation and thermal stability. J. Agric. Food Chem. 2005, 53, 9231-9237.
37. Ma, H.; Forssell, P.; Partanen, R.; Buchert, J.; Boer, H. Improving laccase catalyzed cross-linking of whey protein isolate and their application as emulsifiers. J. Agric. Food Chem. 2011, 59, 1406-1414.
38. Cura, D. E.; Lantto, R.; Lille, M.; Andberg, M.; Kruus, K.; Buchert, J. Laccase-aided protein modification: Effects on the structural properties of acidified sodium caseinate gels. Int. Dairy J. 2009, 19, 737-745.
39. Dhayal, S. K.; Gruppen, H.; de Vries, R.; Wierenga, P. A. Controlled formation of protein nanoparticles by enzymatic crosslinking of α-lactalbumin with horseradish peroxidase. Food Hydrocolloids 2014, 36, 53-59.
40. Saricay, Y.; Wierenga, P.; de Vries, R. Nanostructure development during peroxidase catalysed cross-linking of α-lactalbumin. Food Hydrocolloids 2013, 33, 280-288.
41. Heijnis, W. H.; Wierenga, P. A.; van Berkel, W. J. H.; Gruppen, H. Directing the oligomer size distribution of peroxidase-mediated cross-linked bovine α-lactalbumin. J. Agric. Food Chem. 2010, 58, 5692-5697.
42. Heijnis, W. H.; Dekker, H. L.; de Koning, L. J.; Wierenga, P. A.; Westphal, A. H.; de Koster, C. G.; Gruppen, H.; van Berkel, W. J. H. Identification of the peroxidase-generated intermolecular dityrosine cross-link in bovine α-lactalbumin. J. Agric. Food Chem. 2011, 59, 444-449.
43. Kronman, M. J.; Andreotti, R. E. Inter- and intramolecular interactions of α-lactalbumin. I. Apparent heterogeneity at acid pH. Biochemistry 1964, 3, 1145-1151.
44. Ohlsson, P. I.; Paul, K. G. Molar absorptivity of horseradishperoxidase. Acta Chem. Scand. B 1976, 30, 373-375.
45. Noble, R. W.; Gibson, Q. H. Reaction of ferrous horseradish peroxidase with hydrogen peroxide. J. Biol. Chem. 1970, 245, 2409-2413.
46. Provencher, S. W.; Glockner, J. Estimation of globular protein secondary structure from circular-dichroism. Biochemistry 1981, 20, 33-37.
47. Whitmore, L.; Wallace, B. A. Dichroweb, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 2004, 32, W668-W673.
48. Whitmore, L.; Wallace, B. A. Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases. Biopolymers 2008, 89, 392-400.
49. Chang, J. Y.; Li, L. The structure of denatured α-lactalbumin elucidated by the technique of disulfide scrambling-Fractionation of conformational isomers of α-lactalbumin. J. Biol. Chem. 2001, 276, 9705-9712.
50. Wierenga, P. A.; Meinders, M. B. J.; Egmond, M. R.; Voragen, F.; de Jongh, H. H. J. Protein exposed hydrophobicity reduces the kinetic barrier for adsorption of ovalbumin to the air-water interface. Langmuir 2003, 19, 8964-8970.
51. Yutani, K.; Ogasahara, K.; Kuwajima, K. Absence of the thermal transition in apo-α-lactalbumin in the molten globule state: A study by differential scanning microcalorimetry. J. Mol. Biol. 1992, 228, 347-350.
52. Harms, G.; Pauls, S.; Hedstrom, J.; Johnson, C. Fluorescence and rotational dynamics of dityrosine. J. Fluoresc. 1997, 7, 283-292.
53. Davies, K. J. A.; Delsignore, M. E. Protein damage and degradation by oxygen radicals. 3. Modification of secondary and tertiary structure. J. Biol. Chem. 1987, 262, 9908-9913.
54. Davies, K. J. A.; Lin, S. W.; Pacifici, R. E. Protein damage and degradation by oxygen radicals. 4. Degradation of denatured protein. J. Biol. Chem. 1987, 262, 9914-9920.
55. Kanwar, R.; Balasubramanian, D. Structural studies on some dityrosine-cross-linked globular proteins: Stability is weakened, but activity is not abolished. Biochemistry 2000, 39, 14976-14983.
56. Kanwar, R.; Balasubramanian, D. Structure and stability of the dityrosine-linked dimer of γB-crystallin. Exp. Eye Res. 1999, 68, 773-784.
57. Dalsgaard, T. K.; Otzen, D.; Nielsen, J. H.; Larsen, L. B. Changes in structures of milk proteins upon photo-oxidation. J. Agric. Food Chem. 2007, 55, 10968-10976.
58. Svensson, M.; Fast, J.; Mossberg, A. K.; Duringer, C.; Gustafsson, L.; Hallgren, O.; Brooks, C. L.; Berliner, L.; Linse, S.; Svanborg, C. α-Lactalbumin unfolding is not sufficient to cause apoptosis, but is required for the conversion to HAMLET (human α- lactalbumin made lethal to tumor cells). Protein Sci. 2003, 12, 2794-2804.