Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene

Beste Bayramoğlu

doi:10.31015/jaefs.2022.3.18

EN

Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene

Abstract

It was aimed to investigate the structural changes taking place in duodenal mixed micelles (MM) at fasted state with the incorporation of fatty acids (FA) and the morphological transformations in these MMs upon solubilization of β-carotene (BCR) through coarse-grained (CG) molecular dynamics (MD) simulations. All simulations were performed with GROMACS 2019 simulation package using the Martini force field. Lauric acid (LA), stearic acid (SA) and linoleic acid (LNA) were used to explore the effects of FA chain length and unsaturation. Micelle swelling was observed with the incorporation of all FAs. The increase in size was in line with increasing FA chain length and unsaturation. MMs incorporating LA and SA were ellipsoidal in shape, while polyunsaturated LNA resulted in a worm-like MM. Upon solubilization of BCRs, swelling was observed only in the MMs with long-chain SA and LNA. No micelle growth was observed in the plain and LA MMs despite their smaller sizes. This was attributed to their low-density hydrophobic cores, which allowed a condensation effect induced by the interactions between BCRs and POPC tails. It is inferred that when the micelle is large enough to solubilize BCRs, whether or not swelling will take place depends on the core density. The increase in micelle size was very small in the MM incorporating LNA compared to that in the MM with SA, which was accompanied by an elliptical-to-cylindrical shape transformation. This was due to the fluid nature of the worm-like LNA micelle, which readily allowed the solubilization of 3 BCRs within its core. By resolving the internal structures of BCR incorporated MMs, this study gives valuable insight into the effects of FA chain length and unsaturation on the solubilization behavior of dietary MMs. The results are expected to give direction to the development of rational design strategies for effective BCR delivery systems.

Keywords

Molecular dynamics simulation, β-carotene, dietary mixed micelle, bioaccessibility, nutraceutical delivery system

Supporting Institution

TÜBİTAK

Project Number

118O378

Thanks

This study was supported by The Scientific and Technological Research Council of Turkey (TUBITAK) (grant number:118O378). Computing sources were provided by the National Center for High Performance Computing of Turkey (UHEM) under grant number 5004012016.

References

Abraham, M.J., Murtola, T., Schulz, R., Páll, S., Smith, J.C., Hess, B., Lindah, E. (2015). Gromacs: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
Berendsen, H.J.C., Postma, J.P.M., Gunsteren, W.F. Van, Dinola, A., Haak, J.R. (1984). Molecular dynamics with coupling to an external bath. J. Chem. Phys. 3684. https://doi.org/10.1063/1.448118
Birru, W.A., Warren, D.B., Ibrahim, A., Williams, H.D., Benameur, H., Porter, C.J.H., Chalmers, D.K., Pouton, C.W. (2014). Digestion of phospholipids after secretion of bile into the duodenum changes the phase behavior of bile components. Mol. Pharm. 11, 2825–2834. https://doi.org/10.1021/mp500193g
Bogusz, S., Venable, R.M., Pastor, R.W. (2000). Molecular Dynamics Simulations of Octyl Glucoside Micelles: Structural Properties. J. Phys. Chem. B 104, 5462–5470. https://doi.org/10.1021/jp000159y
Bustos, A.Y., Raya, R., de Valdez, G.F., Taranto, M.P. (2011). Efflux of bile acids in Lactobacillus reuteri is mediated by ATP. Biotechnol. Lett. 33, 2265–2269. https://doi.org/10.1007/s10529-011-0696-3
Cheng, X., Jo, S., Lee, H.S., Klauda, J.B., Im, W. (2013). CHARMM-GUI micelle builder for pure/mixed micelle and protein/micelle complex systems. J. Chem. Inf. Model. https://doi.org/10.1021/ci4002684
Clulow, A.J., Parrow, A., Hawley, A., Khan, J., Pham, A.C., Larsson, P., Bergström, C.A.S., Boyd, B.J. (2017). Characterization of Solubilizing Nanoaggregates Present in Different Versions of Simulated Intestinal Fluid. J. Phys. Chem. B 121, 10869–10881. https://doi.org/10.1021/acs.jpcb.7b08622
Cohen, D.E., Thurston, G.M., Chamberlin, R.A., Benedek, G.B., Carey, M.C. (1998). Laser light scattering evidence for a common wormlike growth structure of mixed micelles in bile salt- and straight-chain detergent- phosphatidylcholine aqueous systems: Relevance to the micellar structure of bile. Biochemistry 37, 14798–14814. https://doi.org/10.1021/bi980182y
de Jong, D.H., Liguori, N., van den Berg, T., Arnarez, C., Periole, X., Marrink, S.J. (2015). Atomistic and Coarse Grain Topologies for the Cofactors Associated with the Photosystem II Core Complex. J. Phys. Chem. B 119, 7791–7803. https://doi.org/10.1021/acs.jpcb.5b00809
El Aoud, A., Reboul, E., Dupont, A., Mériadec, C., Artzner, F., Marze, S. (2021). In vitro solubilization of fat-soluble vitamins in structurally defined mixed intestinal assemblies. J. Colloid Interface Sci. 589, 229–241. https://doi.org/10.1016/j.jcis.2021.01.002

Fatouros, D.G., Bergenstahl, B., Mullertz, A. (2007). Morphological observations on a lipid-based drug delivery system during in vitro digestion. Eur. J. Pharm. Sci. 31, 85–94. https://doi.org/10.1016/j.ejps.2007.02.009
Fatouros, D.G., Walrand, I., Bergenstahl, B., Mullertz, A. (2009). Physicochemical characterization of simulated intestinal fed-state fluids containing lyso-phosphatidylcholine and cholesterol. Dissolution Technol. 16, 47–50. https://doi.org/10.14227/DT160309P47
Gleize, B., Tourniaire, F., Depezay, L., Bott, R., Nowicki, M., Albino, L., Lairon, D., Kesse-Guyot, E., Galan, P., Hercberg, S., Borel, P. (2013). Effect of type of TAG fatty acids on lutein and zeaxanthin bioavailability. Br. J. Nutr. 110, 1–10. https://doi.org/10.1017/S0007114512004813
Hess, B., Bekker, H., Berendsen, H.J.C., Fraaije, J.G.E.M. (1997). LINCS: A linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
Hjelm, R.P., Alkan, M.H., Thiyagarajan, P. (1990). Small-Angle Neutron Scattering Studies of Mixed Bile Salt-Lecithin Colloids. Mol. Cryst. Liq. Cryst. Inc. Nonlinear Opt. 180, 155–164. https://doi.org/10.1080/00268949008025796
Hjelm, R.P., Thiyagarajan, P., Önyüksel, H. (1992). Organization of phosphatidylcholine and bile salt in rodlike mixed micelles. J. Phyical Chem. 96, 8653–8661. https://doi.org/10.1021/j100200a080
Humphrey, W., Dalke, A., Schulten, K. (1996). VMD: Visual molecular dynamics. J. Mol. Graph. 14, 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
Huo, T., Ferruzzi, M.G., Schwartz, S.J., Failla, M.L. (2007). Impact of fatty acyl composition and quantity of triglycerides on bioaccessibility of dietary carotenoids. J. Agric. Food Chem. 55, 8950–8957. https://doi.org/10.1021/jf071687a
Jemioła-Rzemińska, M., Pasenkiewicz-Gierula, M., Strzałka, K. (2005). The behaviour of β-carotene in the phosphatidylcholine bilayer as revealed by a molecular simulation study. Chem. Phys. Lipids 135, 27–37. https://doi.org/10.1016/j.chemphyslip.2005.01.006
Jójárt, B., Poša, M., Fiser, B., Szori, M., Farkaš, Z., Viskolcz, B. (2014). Mixed micelles of sodium cholate and sodium dodecylsulphate 1:1 binary mixture at different temperatures - Experimental and theoretical investigations. PLoS One 9, 1–9. https://doi.org/10.1371/journal.pone.0102114
Khoshakhlagh, P., Johnson, R., Nawroth, T., Langguth, P., Schmueser, L., Hellmann, N., Decker, H., Szekely, N.K. (2014). Nanoparticle structure development in the gastro-intestinal model fluid FaSSIF mod6.5 from several phospholipids at various water content relevant for oral drug administration. Eur. J. Lipid Sci. Technol. 116, 1155–1166. https://doi.org/10.1002/ejlt.201400066
Kossena, G.A., Boyd, B.J., Porter, C.J.H., Charman, W.N. (2003). Separation and characterization of the colloidal phases produced on digestion of common formulation lipids and assessment of their impact on the apparent solubility of selected poorly water-soluble drugs. J. Pharm. Sci. 92, 634–648. https://doi.org/10.1002/jps.10329
Madenci, D., Salonen, A., Schurtenberger, P., Pedersen, J.S., Egelhaaf, S.U. (2011). Simple model for the growth behaviour of mixed lecithin-bile salt micelles. Phys. Chem. Chem. Phys. 13, 3171–3178. https://doi.org/10.1039/c0cp01700k
Marrink, S. J. (2004). Molecular dynamics simulation of cholesterol nucleation in mixed micelles modelling human bile. In G. Adler, M. Fuchs, HE. Blum, & EF. Stange (Eds.), GALLSTONES: PATHOGENESIS AND TREATMENT (pp. 98-105 - 13). (FALK SYMPOSIUM; Vol. 139). Kluwer Academic Publishers.
Marrink, S.J., Mark, A.E. (2002). Molecular Dynamics Simulations of Mixed Micelles Modeling Human Bile. Biochemistry 41, 17, 5375–5382. https://doi.org/10.1021/bi015613i
Marrink, S.J., Risselada, H.J., Yefimov, S., Tieleman, D.P., De Vries, A.H. (2007). The MARTINI force field: Coarse grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812–7824. https://doi.org/10.1021/jp071097f
Marrink, S.J., Tieleman, D.P. (2013). Perspective on the Martini model. Chem. Soc. Rev. 42, 6801. https://doi.org/10.1039/c3cs60093a
Martini General Purpose Coarse-Grained Force Field (2022, August 10). Force field parameters. Retrieved from http://cgmartini.nl/index.php/force-field-parameters
Mashurabad, P.C., Palika, R., Jyrwa, Y.W., Bhaskarachary, K., Pullakhandam, R. (2017). Dietary fat composition, food matrix and relative polarity modulate the micellarization and intestinal uptake of carotenoids from vegetables and fruits. J. Food Sci. Technol. 54, 333–341. https://doi.org/10.1007/s13197-016-2466-7
Matsuoka, K., Maeda, M., Moroi, Y. (2004). Characteristics of conjugate bile salt–phosphatidylcholine–cholesterol–water systems. Colloids Surfaces B Biointerfaces 33, 101–109. https://doi.org/10.1016/j.colsurfb.2003.09.002
Mazer, N.A., Benedek, G.B., Carey, M.C. (1980). Quasielastic Light-Scattering Studies of Aqueous Biliary Lipid Systems. Mixed Micelle Formation in Bile Salt-Lecithin Solutions. Biochemistry 19, 601–615. https://doi.org/10.1021/bi00545a001
Mostofian, B., Johnson, Q.R., Smith, J.C., Cheng, X. (2020). Carotenoids promote lateral packing and condensation of lipid membranes. Phys. Chem. Chem. Phys. 22, 12281–12293. https://doi.org/10.1039/D0CP01031F
Nagao, A., Kotake-Nara, E., Hase, M. (2013). Effects of fats and oils on the bioaccessibility of carotenoids and vitamin E in vegetables. Biosci. Biotechnol. Biochem. 77, 1055–60. https://doi.org/10.1271/bbb.130025
Parrow, A., Larsson, P., Augustijns, P., Bergström, C.A.S. (2020). Molecular Dynamics Simulations on Interindividual Variability of Intestinal Fluids: Impact on Drug Solubilization. Mol. Pharm. 17, 3837–3844. https://doi.org/10.1021/acs.molpharmaceut.0c00588
Phan, S., Salentinig, S., Gilbert, E., Darwish, T.A., Hawley, A., Nixon-Luke, R., Bryant, G., Boyd, B.J. (2015). Disposition and crystallization of saturated fatty acid in mixed micelles of relevance to lipid digestion. J. Colloid Interface Sci. 449, 160–166. https://doi.org/10.1016/j.jcis.2014.11.026
Qian, C., Decker, E.A., Xiao, H., McClements, D.J. (2012). Nanoemulsion delivery systems: Influence of carrier oil on β-carotene bioaccessibility. Food Chem. 135, 1440–1447. https://doi.org/10.1016/j.foodchem.2012.06.047
Sayyed-Ahmad, A., Lichtenberger, L.M., Gorfe, A.A. (2010). Structure and dynamics of cholic acid and dodecylphosphocholine-cholic acid aggregates. Langmuir 26, 13407–13414. https://doi.org/10.1021/la102106t
Schurtenberger, P., Mazer, N., Känzig, W. (1985). Micelle to vesicle transition in aqueous solutions of bile salt and lecithin. J. Phys. Chem. 89, 1042–1049. https://doi.org/10.1021/j100252a031
Suys, E.J.A., Warren, D.B., Porter, C.J.H., Benameur, H., Pouton, C.W., Chalmers, D.K. (2017). Computational Models of the Intestinal Environment. 3. the Impact of Cholesterol Content and pH on Mixed Micelle Colloids. Mol. Pharm. 14, 3684–3697. https://doi.org/10.1021/acs.molpharmaceut.7b00446
Tande, B.M., Wagner, N.J., Mackay, M.E., Hawker, C.J., Jeong, M. (2001). Viscosimetric, hydrodynamic, and conformational properties of dendrimers and dendrons. Macromolecules 34, 8580–8585. https://doi.org/10.1021/ma011265g
Tuncer, E., Bayramoglu, B. (2019). Characterization of the self-assembly and size dependent structural properties of dietary mixed micelles by molecular dynamics simulations. Biophys. Chem. 248, 16–27. https://doi.org/10.1016/j.bpc.2019.02.001
Tunçer, E., Bayramoğlu, B. (2022). Molecular dynamics simulations of duodenal self assembly in the presence of different fatty acids. Colloids Surfaces A Physicochem. Eng. Asp. 644. https://doi.org/10.1016/j.colsurfa.2022.128866
Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A.E., Berendsen, H.J.C. (2005). GROMACS: Fast, flexible, and free. J. Comput. Chem. 26, 1701–1718. https://doi.org/10.1002/jcc.20291
Wilson, M.D., Rudel, L.L. (1994). Review of cholesterol absorption with emphasis on dietary and biliary cholesterol. J. Lipid Res. 35, 943–955. https://doi.org/10.1016/S0022-2275(20)40109-9
Wright, A.J., Pietrangelo, C., MacNaughton, A. (2008). Influence of simulated upper intestinal parameters on the efficiency of beta carotene micellarisation using an in vitro model of digestion. Food Chem. 107, 1253–1260. https://doi.org/10.1016/j.foodchem.2007.09.063
Yao, K., Mcclements, D.J., Xiao, H., Liu, X. (2019). Improvement of carotenoid bioaccessibility from spinach by co-ingesting with excipient nanoemulsions: impact of the oil phase composition. Food Funct. 10, 5302–5311. https://doi.org/10.1039/c9fo01328h
Yuan, X., Liu, X., Mcclements, D.J., Cao, Y., Xiao, H. (2018). Enhancement of phytochemical bioaccessibility from plant-based foods using excipient emulsions : impact of lipid type on carotenoid solubilization. Food Funct. 9, 4352–4365. https://doi.org/10.1039/c8fo01118d

Details

Primary Language

English

Subjects

Food Engineering

Journal Section

Research Article

Authors

Beste Bayramoğlu ^*
0000-0002-3958-9241
Türkiye

Publication Date

September 23, 2022

Submission Date

August 11, 2022

Acceptance Date

September 16, 2022

Published in Issue

Year 2022 Volume: 6 Number: 3

DOI

https://doi.org/10.31015/jaefs.2022.3.18

IZ

https://izlik.org/JA86FY68YP

APA

Bayramoğlu, B. (2022). Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene. International Journal of Agriculture Environment and Food Sciences, 6(3), 480-493. https://doi.org/10.31015/jaefs.2022.3.18

AMA

1.Bayramoğlu B. Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene. int. j. agric. environ. food sci. 2022;6(3):480-493. doi:10.31015/jaefs.2022.3.18

Chicago

Bayramoğlu, Beste. 2022. “Structural Changes in Fasted State Dietary Mixed Micelles Upon Solubilization of Beta-Carotene”. International Journal of Agriculture Environment and Food Sciences 6 (3): 480-93. https://doi.org/10.31015/jaefs.2022.3.18.

EndNote

Bayramoğlu B (September 1, 2022) Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene. International Journal of Agriculture Environment and Food Sciences 6 3 480–493.

IEEE

[1]B. Bayramoğlu, “Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene”, int. j. agric. environ. food sci., vol. 6, no. 3, pp. 480–493, Sept. 2022, doi: 10.31015/jaefs.2022.3.18.

ISNAD

Bayramoğlu, Beste. “Structural Changes in Fasted State Dietary Mixed Micelles Upon Solubilization of Beta-Carotene”. International Journal of Agriculture Environment and Food Sciences 6/3 (September 1, 2022): 480-493. https://doi.org/10.31015/jaefs.2022.3.18.

JAMA

1.Bayramoğlu B. Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene. int. j. agric. environ. food sci. 2022;6:480–493.

MLA

Bayramoğlu, Beste. “Structural Changes in Fasted State Dietary Mixed Micelles Upon Solubilization of Beta-Carotene”. International Journal of Agriculture Environment and Food Sciences, vol. 6, no. 3, Sept. 2022, pp. 480-93, doi:10.31015/jaefs.2022.3.18.

Vancouver

1.Beste Bayramoğlu. Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene. int. j. agric. environ. food sci. 2022 Sep. 1;6(3):480-93. doi:10.31015/jaefs.2022.3.18

Abstracting & Indexing Services

Google Scholar | Crossref DOI Registry

All content published in this journal is licensed under the Creative Commons Attribution 4.0 International License (CC BY 4.0).
Authors retain copyright of their work and grant the journal a non-exclusive right to publish, reproduce, and distribute the articles within an open-access framework.

Web: dergipark.org.tr/jaefs E-mail: editorialoffice@jaefs.com Phone / WhatsApp: +90 850 309 59 27

Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene

Abstract

Structural changes in fasted state dietary mixed micelles upon solubilization of beta-carotene

Abstract

Keywords

Supporting Institution

Project Number

Thanks

References

Details

Primary Language

Subjects

Journal Section

Authors

Publication Date

Submission Date

Acceptance Date

Published in Issue

DOI

IZ

Cite

Abstracting & Indexing Services

© International Journal of Agriculture, Environment and Food Sciences