Heteroprotein Complex Formation of Bovine Lactoferrin and Pea Protein Isolate: A Multiscale Structural Analysis

Biomacromolecules

Volumn 18, Issue 2, 2017, Pages 625-635

  Adal, Eda ^a,b   Sadeghpour, Amin ^a   Connell, Simon ^a   Rappolt, Michael ^a   Ibanoglu, Esra ^b   Sarkar, Anwesha ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b GAZIANTEP UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

ASPECT RATIO; ATOMIC FORCE MICROSCOPY; ELECTROSTATICS; LIGHT SCATTERING; MIXTURES; SIZE DISTRIBUTION; TURBIDITY; X RAY SCATTERING;

CHAINLIKE STRUCTURE; COMPLEMENTARY TECHNIQUES; COMPLEX FORMATIONS; DIFFERENT LENGTH SCALE; ELECTROSTATIC COMPLEXES; PEA PROTEIN ISOLATES; STRUCTURAL ASPECTS; TURBIDITY MEASUREMENTS;

PROTEINS;

AVENIN; CONVICILIN; GLOBULAR PROTEIN; LACTOFERRIN; PEA PROTEIN ISOLATE; PLANT PROTEIN; UNCLASSIFIED DRUG; VICILIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BOVINE; COACERVATION; COMPLEX FORMATION; IMAGE ANALYSIS; NONHUMAN; PHOTON CORRELATION SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; STATIC ELECTRICITY; TURBIDITY; X RAY CRYSTALLOGRAPHY; ZETA POTENTIAL; ANIMAL; CHEMISTRY; METABOLISM; PEA; PH; SMALL ANGLE SCATTERING; X RAY DIFFRACTION;

ANIMALS; CATTLE; HYDROGEN-ION CONCENTRATION; LACTOFERRIN; MICROSCOPY, ATOMIC FORCE; PEAS; PLANT PROTEINS; SCATTERING, SMALL ANGLE; STATIC ELECTRICITY; X-RAY DIFFRACTION;

EID: 85012272807     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/acs.biomac.6b01857     Document Type: Article

References (39)

1. Salvatore, D.; Croguennec, T.; Bouhallab, S.; Forge, V.; Nicolai, T. Kinetics and structure during self-assembly of oppositely charged proteins in aqueous solution Biomacromolecules 2011, 12 ( 5 ) 1920-1926 10.1021/bm200264m
2. Hwang, D. S.; Zeng, H.; Srivastava, A.; Krogstad, D. V.; Tirrell, M.; Israelachvili, J. N.; Waite, J. H. Viscosity and interfacial properties in a mussel-inspired adhesive coacervate Soft Matter 2010, 6 ( 14 ) 3232-3236 10.1039/c002632h
3. Toh, Y.-C.; Ho, S. T.; Zhou, Y.; Hutmacher, D. W.; Yu, H. Application of a polyelectrolyte complex coacervation method to improve seeding efficiency of bone marrow stromal cells in a 3D culture system Biomaterials 2005, 26 ( 19 ) 4149-4160 10.1016/j.biomaterials.2004.10.033
4. Jin, K.-M.; Kim, Y.-H. Injectable, thermo-reversible and complex coacervate combination gels for protein drug delivery J. Controlled Release 2008, 127 ( 3 ) 249-256 10.1016/j.jconrel.2008.01.015
5. Wu, B.-c.; Degner, B.; McClements, D. J. Soft matter strategies for controlling food texture: formation of hydrogel particles by biopolymer complex coacervation J. Phys.: Condens. Matter 2014, 26 ( 46 ) 464104 10.1088/0953-8984/26/46/464104
6. Schmitt, C.; Sanchez, C.; Desobry-Banon, S.; Hardy, J. Structure and technofunctional properties of protein-polysaccharide complexes: A review Crit. Rev. Food Sci. Nutr. 1998, 38 ( 8 ) 689-753 10.1080/10408699891274354
7. Chapeau, A.-L.; Tavares, G. M.; Hamon, P.; Croguennec, T.; Poncelet, D.; Bouhallab, S. Spontaneous co-assembly of lactoferrin and β-lactoglobulin as a promising biocarrier for vitamin B9 Food Hydrocolloids 2016, 57, 280-290 10.1016/j.foodhyd.2016.02.003
8. Tavares, G. M.; Croguennec, T.; Hamon, P.; Carvalho, A. F.; Bouhallab, S. Selective coacervation between lactoferrin and the two isoforms of β-lactoglobulin Food Hydrocolloids 2015, 48, 238-247 10.1016/j.foodhyd.2015.02.027
9. Yan, Y.; Kizilay, E.; Seeman, D.; Flanagan, S.; Dubin, P. L.; Bovetto, L.; Donato, L.; Schmitt, C. Heteroprotein complex coacervation: Bovine β-lactoglobulin and lactoferrin Langmuir 2013, 29 ( 50 ) 15614-15623 10.1021/la4027464
10. Flanagan, S. E.; Malanowski, A. J.; Kizilay, E.; Seeman, D.; Dubin, P. L.; Donato-Capel, L.; Bovetto, L.; Schmitt, C. Complex equilibria, speciation, and heteroprotein coacervation of lactoferrin and β-lactoglobulin Langmuir 2015, 31 ( 5 ) 1776-1783 10.1021/la504020e
11. Kizilay, E.; Seeman, D.; Yan, Y.; Du, X.; Dubin, P. L.; Donato-Capel, L.; Bovetto, L.; Schmitt, C. Structure of bovine β-lactoglobulin-lactoferrin coacervates Soft Matter 2014, 10 ( 37 ) 7262-7268 10.1039/C4SM01333F
12. Peixoto, P. D. S.; Tavares, G. M.; Croguennec, T.; Nicolas, A.; Hamon, P.; Roiland, C.; Bouhallab, S. Structure and dynamics of heteroprotein coacervates Langmuir 2016, 32 ( 31 ) 7821-7828 10.1021/acs.langmuir.6b01015
13. Du, X.; Seeman, D.; Dubin, P. L.; Hoagland, D. A. Nonfreezing water structuration in heteroprotein coacervates Langmuir 2015, 31 ( 31 ) 8661-8666 10.1021/acs.langmuir.5b01647
14. Anema, S. G.; de Kruif, C. G. Phase separation and composition of coacervates of lactoferrin and caseins Food Hydrocolloids 2016, 52, 670-677 10.1016/j.foodhyd.2015.08.011
15. Anema, S. G.; de Kruif, C. G. Interaction of lactoferrin and lysozyme with casein micelles Biomacromolecules 2011, 12 ( 11 ) 3970-3976 10.1021/bm200978k
16. Anema, S. G.; de Kruif, C. G. Complex coacervates of lactotransferrin and beta-lactoglobulin J. Colloid Interface Sci. 2014, 430, 214-220 10.1016/j.jcis.2014.05.036
17. Nigen, M.; Croguennec, T.; Madec, M.-N.; Bouhallab, S. Apo α-lactalbumin and lysozyme are colocalized in their subsequently formed spherical supramolecular assembly FEBS J. 2007, 274 ( 23 ) 6085-6093 10.1111/j.1742-4658.2007.06130.x
18. Nigen, M.; Croguennec, T.; Renard, D.; Bouhallab, S. Temperature affects the supramolecular structures resulting from α-lactalbumin-lysozyme interaction Biochemistry 2007, 46 ( 5 ) 1248-1255 10.1021/bi062129c
19. AOAC. Officialmethods of analysis of Association of Official Analytical ChemistsIn Washington, DC, USA, ( 1995.
20. Patil-Sen, Y.; Sadeghpour, A.; Rappolt, M.; Kulkarni, C. V. Facile preparation of internally self-assembled lipid particles stabilized by carbon nanotubes J. Visualized Exp. 2016 ) 108, e53489 10.3791/53489
21. Barac, M.; Cabrilo, S.; Pesic, M.; Stanojevic, S.; Zilic, S.; Macej, O.; Ristic, N. Profile and functional properties of seed proteins from six pea (Pisum sativum) genotypes Int. J. Mol. Sci. 2010, 11 ( 12 ) 4973-4990 10.3390/ijms11124973
22. Mertens, C.; Dehon, L.; Bourgeois, A.; Verhaeghe-Cartrysse, C.; Blecker, C. Agronomical factors influencing the legumin/vicilin ratio in pea (Pisum sativum L.) seeds J. Sci. Food Agric. 2012, 92 ( 8 ) 1591-1596 10.1002/jsfa.4738
23. Liu, S.; Low, N. H.; Nickerson, M. T. Effect of pH, salt, and biopolymer ratio on the formation of pea protein isolate-gum arabic complexes J. Agric. Food Chem. 2009, 57 ( 4 ) 1521-1526 10.1021/jf802643n
24. Qazvini, N. T.; Bolisetty, S.; Adamcik, J.; Mezzenga, R. Self-healing fish gelatin/sodium montmorillonite biohybrid coacervates: Structural and rheological characterization Biomacromolecules 2012, 13 ( 7 ) 2136-2147 10.1021/bm3005319
25. Kizilay, E.; Kayitmazer, A. B.; Dubin, P. L. Complexation and coacervation of polyelectrolytes with oppositely charged colloids Adv. Colloid Interface Sci. 2011, 167 ( 1-2 ) 24-37 10.1016/j.cis.2011.06.006
26. Gharsallaoui, A.; Cases, E.; Chambin, O.; Saurel, R. Interfacial and emulsifying characteristics of acid-treated pea protein Food Biophys 2009, 4 ( 4 ) 273-280 10.1007/s11483-009-9125-8
27. Croguennec, T.; Tavares, G. M.; Bouhallab, S. Heteroprotein complex coacervation: A generic process Adv. Colloid Interface Sci. 2016, 10.1016/j.cis.2016.06.009
28. Dubin, P. L.; Gao, J.; Mattison, K. Protein-Purification by Selective Phase-Separation with Polyelectrolytes Sep. Purif. Methods 1994, 23 ( 1 ) 1-16 10.1080/03602549408001288
29. Bergmann, A.; Fritz, G.; Glatter, O. Solving the generalized indirect Fourier transformation (GIFT) by Boltzmann simplex simulated annealing (BSSA) J. Appl. Crystallogr. 2000, 33 ( 5 ) 1212-1216 10.1107/S0021889800008372
30. Anderson, B. F.; Baker, H. M.; Dodson, E. J.; Norris, G. E.; Rumball, S. V.; Waters, J. M.; Baker, E. N. Structure of human lactoferrin at 3.2-A resolution Proc. Natl. Acad. Sci. U. S. A. 1987, 84 ( 7 ) 1769-1773 10.1073/pnas.84.7.1769
31. Grossmann, J. G.; Neu, M.; Pantos, E.; Schwab, F. J.; Evans, R. W.; Townes-Andrews, E.; Lindley, P. F.; Appel, H.; Thies, W.-G.; Hasnain, S. S. X-ray solution scattering reveals conformational changes upon iron uptake in lactoferrin, serum and ovo-transferrins J. Mol. Biol. 1992, 225 ( 3 ) 811-819 10.1016/0022-2836(92)90402-6
32. Welland, M. E.; Miles, M. J.; Lambert, N.; Morris, V. J.; Coombs, J. H.; Pethica, J. B. Structure of the globular protein vicilin revealed by scanning tunnelling microscopy Int. J. Biol. Macromol. 1989, 11 ( 1 ) 29-32 10.1016/0141-8130(89)90036-6
33. Mession, J.-L.; Sok, N.; Assifaoui, A.; Saurel, R. Thermal denaturation of pea globulins (Pisum sativum L.)-Molecular interactions leading to heat-induced protein aggregation J. Agric. Food Chem. 2013, 61 ( 6 ) 1196-1204 10.1021/jf303739n
34. Plietz, P.; Zirwer, D.; Schlesier, B.; Gast, K.; Damaschun, G. Shape, symmetry, hydration and secondary structure of the legumin from Vicia faba in solution Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1984, 784 ( 2 ) 140-146 10.1016/0167-4838(84)90120-1
35. I’Anson, K. J.; Miles, M. J.; Bacon, J. R.; Carr, H. J.; Lambert, N.; Morris, V. J.; Wright, D. J. Structure of the 7S globulin (vicilin) from pea (Pisum sativum) Int. J. Biol. Macromol. 1988, 10 ( 5 ) 311-317 10.1016/0141-8130(88)90010-4
36. Svergun, D. I.; Koch, M. H. J. Small-angle scattering studies of biological macromolecules in solution Rep. Prog. Phys. 2003, 66 ( 10 ) 1735 10.1088/0034-4885/66/10/R05
37. Pastré, D.; Piétrement, O.; Fusil, S.; Landousy, F.; Jeusset, J.; David, M.-O.; Hamon, L.; Le Cam, E.; Zozime, A. Adsorption of DNA to mica mediated by divalent counterions: A theoretical and experimental study Biophys. J. 2003, 85 ( 4 ) 2507-2518 10.1016/S0006-3495(03)74673-6
38. Kaibara, K.; Okazaki, T.; Bohidar, H. B.; Dubin, P. L. pH-Induced coacervation in complexes of bovine serum albumin and cationic polyelectrolytes Biomacromolecules 2000, 1 ( 1 ) 100-107 10.1021/bm990006k
39. Liberatore, M. W.; Wyatt, N. B.; Henry, M.; Dubin, P. L.; Foun, E. Shear-induced phase separation in polyelectrolyte/mixed micelle coacervates Langmuir 2009, 25 ( 23 ) 13376-13383 10.1021/la903260r