Analysis of the thermally induced structural changes of bovine lactoferrin

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 9, 2013, Pages 2234-2243

  Stǎnciuc, Nicoleta ^a   Aprodu, Iuliana ^a   Raîpeanu, Gabriela ^a   Van Der Plancken, Iesel ^b   Bahrim, Gabriela ^a   Hendrickx, Marc ^b  

^a DUNAREA DE JOS UNIVERSITY OF GALATI   (Romania)

^b LEUVEN FOOD SCIENCE AND NUTRITION RESEARCH CENTRE LFORCE   (Belgium)

Author keywords

conformational changes; enzymatic hydrolysis; fluorescence spectroscopy; lactoferrin; molecular modeling

Indexed keywords

BOVINE LACTOFERRIN; CONFORMATIONAL CHANGE; FLEXIBLE CONFORMATION; HYDROPHOBIC RESIDUES; LACTOFERRIN; STRUCTURAL CHANGE; TEMPERATURE-INDUCED; THERMALLY INDUCED;

CONFORMATIONS; DAIRY PRODUCTS; ENZYMATIC HYDROLYSIS; FLUORESCENCE SPECTROSCOPY; MAMMALS; PHASE DIAGRAMS;

MOLECULAR MODELING;

LACTOFERRIN; THERMOLYSIN;

ANIMAL; ARTICLE; CATTLE; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; HEAT; HYDROLYSIS; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN CONFORMATION; SOLUTION AND SOLUBILITY; SPECTROFLUOROMETRY;

ANIMALS; CATTLE; HOT TEMPERATURE; HYDROLYSIS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LACTOFERRIN; MODELS, MOLECULAR; PROTEIN CONFORMATION; SOLUTIONS; SPECTROMETRY, FLUORESCENCE; THERMOLYSIN;

EID: 84874908349     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf305178s     Document Type: Article

References (54)

1. Guo, M.; Zhang, L. Y.; Lü, W. J.; Cao, H. R. Analysis of the spectroscopic characteristics on the binding interaction between tosufloxacin and bovine lactoferrin J. Lumin. 2011, 131, 768-775
2. Spik, G.; Coddeville, B.; Montreuil, J. Comparative study of the primary structures of sero-, lacto- and ovotransferrin glycans from different species Biochimie 1988, 70, 1459-1469
3. Nisar, S.; Kazmi, S. A. Spectrofluorometric study of iron removal from bovine lactoferrin by ethylenediamminetetraacetic acid Spectrochim. Acta Part A: Mol. Biomol. Spectrosc. 2010, 77, 933-937
4. Baker, E. N. Structure and reactivity of transferrins Adv. Inorg. Chem. 1994, 41, 389-463
5. Steijns, J. M.; van Hooijdonk, A. C. M. Occurrence, structure, biochemical properties and technological characteristics of lactoferrin Br. J. Nutr. 2000, 84 (Suppl. 1) S11-S17
6. Brock, J. H. The physiology of lactoferrin Biochem. Cell Biol. 2002, 80, 1-6
7. Wakabayashi, H.; Takase, M.; Tomita, M. Lactoferricin derived from milk protein lactoferrin Curr. Pharm. Design 2003, 9, 1277-1287
8. Van der Kraan, M. I. A.; Groenink, J.; Nazmi, K.; Veerman, E. C. I.; Bolscher, J. G. M.; Nieuw Amerongen, A. V. Lactoferrampin: A novel antimicrobial peptide in the N1-domain of bovine lactoferrin Peptides 2004, 25, 177-183
9. Fox, P. F.; Kelly, A. L. Developments in the chemistry and technology of milk proteins. Minor milk proteins Food Australia 2003, 55, 231-234
10. Sui, Q.; Roginski, H.; Williams, R. P. W.; Versteeg, C.; Wan, J. Effect of pulsed electric field and thermal treatment on the physicochemical properties of lactoferrin with different iron saturation levels Int. Dairy J. 2010, 20, 707-714
11. Abe, H.; Saito, H.; Miyakawa, H.; Tamura, Y.; Shimamura, S.; Nagao, E. Heat stability of bovine lactoferrin at acidic pH J. Dairy Sci. 1991, 74, 65-71
12. Sreedhara, A.; Flengsrud, R.; Prakash, V.; Krowarsch, D.; Langsrud, T.; Kaul, P.; Devold, T. G.; Vegarud, G. E. A comparison of effects of pH on the thermal stability and conformation of caprine and bovine lactoferrin Int. Dairy J. 2010, 20, 487-494
13. Polverino de Laureto, P.; Scaramella, E.; Frigo, M.; Gefter Wondrich, F.; De Filippis, V.; Zambonin, M.; Fontana, A. Limited proteolysis of bovine α-lactalbumin: Isolation and characterization of protein domains Protein Sci. 1999, 8, 2290-2303
14. Dodson, G. G.; Lane, D. P.; Verma, C. S. Molecular simulations of protein dynamics: New windows on mechanisms in biology EMBO Rep. 2008, 9, 144-150
15. Van Gunsteren, W. F.; Dolenc, J.; Mark, A. E. Molecular simulation as an aid to experimentalists Curr. Opin. Struct. Biol. 2008, 18, 149-153
16. Royer, C. A. Probing protein folding and conformational transitions with fluorescence Chem. Rev. 2006, 106, 1769-1784
17. Bushmarina, N. A.; Kuznetsova, I. M.; Biktashev, A. G.; Turoverov, K. K.; Uversky, V. N. Partially folded conformations in the folding pathway of bovine carbonic anhydrase II: A fluorescence spectroscopic analysis ChemBioChem 2001, 2, 813-821
18. Kuznetsova, M.; Turoverov, K. K.; Uversky, V. N. Use of the phase diagram method to analyze the protein unfolding-refolding reactions: Fishing out the "invisible" intermediates J. Proteome Res. 2004, 3, 485-494
19. Moore, S. A.; Anderson, B. F.; Groom, C. R.; Haridas, M.; Baker, E. N. Three-dimensional structure of diferric bovine lactoferrin at 2.8 Å resolution J. Mol. Biol. 1997, 274, 222-236
20. Laskowski, R A. PDBsum new things Nucleic Acids Res. 2009, 37, D355-D359
21. Church, F. C.; Swaisgood, H. E.; Porter, D. H.; Catignani, G. L. Spectrophotometric assay using o -phtaldialdehyde for determination of proteolysis in milk and isolated milk proteins J. Dairy Sci. 1983, 66, 1219-1227
22. González-Chávez, S. A.; Arévalo-Gallegos, S.; Rascón-Cruz, Q. Lactoferrin: Structure, function and applications Int. J. Antimicrob. Agents 2009, 33, 301.e1-301.e8
23. Williams, R.; Sui, Q.; Roginski, H.; Wooster, T.; Versteeg, C.; Wan, J. Effect of ionic strength of pulsed electric field treatment medium on the physicochemical and structural characteristics of lactoferrin J. Agric. Food Chem. 2010, 58, 11725-11731
24. Sánchez, L.; Peiró, J. M.; Castillo, H.; Pérez, M. D.; Ena, J. M.; Calvo, M. Kinetic Parameters for Denaturation of Bovine Milk Lactoferrin J. Food Sci. 1992, 57, 873-879
25. Kawakami, H.; Tanaka, M.; Tatsumi, K.; Dosako, S. Effects of ionic strength and pH on the thermostability of lactoferrin Int. Dairy J. 1992, 2, 287-298
26. Mata, L.; Sánchez, L.; Headon, D.; Calvo, M. Thermal denaturation of human lactoferrin and its effect on the ability to bind iron J. Agric. Food Chem. 1998, 46, 3964-3970
27. Stǎnciuc, N.; Raîpeanu, G.; Bahrim, G.; Aprodu, I. pH and heat-induced structural changes of bovine apo-α-lactalbumin Food Chem. 2012, 131, 956-963
28. Stǎnciuc, N.; Aprodu, I.; Raîpeanu, G.; Bahrim, G. Fluorescence spectroscopy and molecular modeling investigations on the thermally induced structural changes of bovine β-lactoglobulin Innovative Food Sci. Emerging Technol. 2012, 15, 50-56
29. Nosoh, Y.; Sekiguchi, T. Protein Stability and Stabilization through Protein Engineering; Ellis Harwood: New York, 1991.
30. Bengoechea, C.; Peinado, I.; McClements, D. J. Formation of protein nanoparticles by controlled heat treatment of lactoferrin: Factors affecting particle characteristics Food Hydrocolloids 2011, 25, 1354-1360
31. Paulsson, M. A.; Svensson, U.; Kishore, A. R.; Naidu, A. S. Thermal behavior of bovine lactoferrin in water and its relation to bacterial interaction and antibacterial activity J. Dairy Sci. 1993, 76, 3711-3720
32. Engelhard, M.; Evans, P. H. Kinetics of interaction of partially folded proteins with a hydrophobic dye: Evidence that molten globule character is maximal in early folding intermediates Protein Sci. 1995, 4, 1553-1562
33. Uversky, V. N. Natively unfolded proteins: A point where biology waits for physics Protein Sci. 2002, 11, 739-756
34. Permyakov, E. A.; Yarmolenko, V. V.; Emelyanenko, V. I.; Burstein, E. A.; Gerday, C.; Closset, J. Fluorescence Studies of the Calcium Binding to Whiting (Gadus merlangus) Parvalbumin Eur. J. Biochem. 1980, 109, 307-315
35. Yang, F., Jr.; Zhang, M.; Zhou, B. R.; Chen, J.; Liang, Y. Structural changes of α-lactalbumin induced by low pH and oleic acid Biochem. Biophys. Acta 2006, 1764, 1389-1396
36. Jiao, M.; Zhou, Y. L.; Li, H. T.; Zhang, D. L.; Chen, J.; Liang, Y. Structural and functional alterations of two multidomain oxidoreductases induced by guanidine hydrochloride Biochem. Biophys. Acta 2010, 42, 30-38
37. Kussendrager, K. D. Effects of heat treatment on structure and iron-binding capacity of bovine lactoferrin. In IDF Bulletin: Indigenous Antimicrobial Agents of Milk: Recent Developments; Brussels, Belgium, 1994; S.I. 9404, pp 133-146.
38. Indyk, H. E.; McGrail, I. J.; Watene, G. A.; Filonzi, E. L. Optical biosensor analysis of the heat denaturation of bovine lactoferrin Food Chem. 2007, 101, 838-844
39. Laurence, L. S.; Middaugh, C. R. Fundamental structures and behaviors of proteins. In Aggregation of Therapeutic Proteins,; Wnag, W., Roberts, C. J., Eds.; John Wiley & Sons, Inc.: Hoboken, NJ, p 14.
40. Halle, B. Flexibility and packing in proteins Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 1274-1279
41. Richardson, J. S. The anatomy and taxonomy of protein structure Adv. Protein Chem. 1981, 34, 167-339
42. Schwarcz, W. D.; Carnelocce, L.; Silva, J. L.; Oliveira, A. C.; Gonçalves, R. B. Conformational changes in bovine lactoferrin induced by slow or fast temperature increases Biol. Chem. 2008, 389, 1137-1142
43. Pawar, S. A.; Deshpande, V. V. Characterization of acid-induced unfolding intermediates of glucose/xylose isomerase Eur. J. Biochem. 2000, 267, 6331-6338
44. Chadborn, N.; Bryant, J.; Bain, A. J.; O'Shea, P. Ligand-dependent conformational equilibria of serum albumin revealed by tryptophan fluorescence quenching Biophys. J. 1999, 76, 2198-2207
45. Guo, M. R.; Fox, P. F.; Flynn, A.; Kindstedt, P. S. Susceptibility of β-lactoglobulin and sodium caseinate to proteolysis by pepsin and trypsin J. Dairy Sci. 1995, 78, 2336-2344
46. Wu, L. C.; Grandori, R.; Carey, J. Autonomous subdomains in protein folding Protein Sci. 1994, 3, 369-371
47. Fontana, A.; Polverino de Laureto, P.; De Filippis, V.; Scaramella, E.; Zambonin, M. Limited proteolysis in the study of protein conformation. In Proteolytic Enzymes: Tools and Targets; Sterchi, E. E.; Stöcker, W., Eds.; Springer: Heidelberg, Germany, 1999; pp 253-280.
48. Hubbard, S. J. The structural aspects of limited proteolysis of native proteins Biochem. Biophys. Acta. 1998, 1382, 191-206
49. Nik, A. M.; Wright, A. J.; Corredig, M. Surface adsorption alters the susceptibility of whey proteins to pepsin-digestion J. Colloid Interface Sci. 2010, 344, 372-381
50. N'Negue, M.-A.; Miclo, L.; Girardet, J.-M.; Campagna, S.; Molle, D.; Gaillard, J.-L. Proteolysis of bovine α-lactalbumin by thermolysin during thermal denaturation Inter. Dairy J. 2006, 16, 1157-1167
51. nd ed.; Thomson Brooks/Cole: Belmont, CA, USA, 2007; p 1100.
52. Gasteiger, E.; Hoogland, C.; Gattiker, A.; Duvaud, S.; Wilkins, M. R.; Appel, R. D.; Bairoch, A. Protein Identification and Analysis Tools on the ExPASy Server. In The Proteomics Protocols Handbook; Walker, J. M., Ed.; Humana Press: Totowa, NJ, 2005; pp 571-607.
53. Keil, B. Specificity of Proteolysis; Springer-Verlag: NewYork, 1992; p 335.
54. Cheison, S. C.; Schmitt, M.; Leeb, E.; Letzel, T.; Kulozik, U. Influence of the temperature and the degree of hydrolysis on the peptide composition of trypsin hydrolysates of β-lactoglobulin: analysis by LC-ESI-TOF/MS Food Chem. 2010, 121, 457-467