Journal Home > Volume 12 , Issue 5
Food Science and Human Wellness 2023, 12(5): 1861-1871 https://doi.org/10.1016/j.fshw.2023.02.038
Research Article | Open Access | Issue | Published: 21 March 2023

Encapsulation of docosahexaenoic acid (DHA) using self-assembling food-derived proteins for efficient biological functions

Show Author's Information Yumeng Liua,b,  Kaixin Caoa,b,  Tong Lia,b,  Delun Mua,c,  Naiqi Zhanga,b,  Ying Wanga,b,  Rina Wua,b,c( ),  Junrui Wua,b,c( )
College of Food Science, Shenyang Agricultural University, Shenyang 110866, China
Liaoning Engineering Research Center of Food Fermentation Technology, Shenyang 110161, China
Shenyang Key Laboratory of Microbial Fermentation Technology Innovation, Shenyang 110866, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Keywords:
Stability, Micelle, Cellular uptake, Solubility, Docosahexaenoic acid
Cite this article:
Liu Y, Cao K, Li T, et al. Encapsulation of docosahexaenoic acid (DHA) using self-assembling food-derived proteins for efficient biological functions. Food Science and Human Wellness, 2023, 12(5): 1861-1871. https://doi.org/10.1016/j.fshw.2023.02.038
Download citation
EndNote(RIS)
BibTeX

335

Views

14

Downloads

Citations

4

Crossref

2

WoS

3

Scopus

0

CSCD

Abstract Full text About this article

Docosahexaenoic acid (DHA; 22n-6) possesses multiple biological functions, including antioxidant activity and ameliorating hypertriglyceridemia. However, the application of DHA has been limited due to poor aqueous solubility and susceptible to oxidation. Here, ovalbumin (O), myosin (M), 7S soy globulin (S), and β-lactoglobulin (β), hydrolyzed by chymotrypsin, self-assembled into micelles, respectively. Adding incremental DHA to micelles caused endogenous fluorescence quenching of O, M, S, and β micelles, implying successful incorporation of DHA into hydrophobic cores of micelles (O (DHA), M (DHA), S (DHA), and β (DHA)). The results showed that micelles provided spatial stability and improved solubility, and stability against thermal and ultraviolet (UV) light for DHA. The uptake of DHA from M (DHA), β (DHA), O (DHA), and S (DHA) was 3.27-, 3.91-, 2.7-, and 3.95-fold higher, respectively, than that of DHA by Caco-2 cells. Encapsulation in micelles increased DHA aqueous solubility and uptake, which enhanced cellular endogenous antioxidant defense. Meanwhile, increased uptake of DHA was verified by HepG2 cells, and O, M, S, and β micelles were proven to increase DHA uptake to reduce lipid deposition. Our findings strongly support the possibility that O, M, S, and β micelles can be regarded as a carrier for loading DHA.


menu
Abstract
Full text
Outline
About this article

Encapsulation of docosahexaenoic acid (DHA) using self-assembling food-derived proteins for efficient biological functions

Show Author's information Yumeng Liua,b, Kaixin Caoa,b, Tong Lia,b, Delun Mua,c, Naiqi Zhanga,b, Ying Wanga,b, Rina Wua,b,c( ), Junrui Wua,b,c( )
College of Food Science, Shenyang Agricultural University, Shenyang 110866, China
Liaoning Engineering Research Center of Food Fermentation Technology, Shenyang 110161, China
Shenyang Key Laboratory of Microbial Fermentation Technology Innovation, Shenyang 110866, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Docosahexaenoic acid (DHA; 22n-6) possesses multiple biological functions, including antioxidant activity and ameliorating hypertriglyceridemia. However, the application of DHA has been limited due to poor aqueous solubility and susceptible to oxidation. Here, ovalbumin (O), myosin (M), 7S soy globulin (S), and β-lactoglobulin (β), hydrolyzed by chymotrypsin, self-assembled into micelles, respectively. Adding incremental DHA to micelles caused endogenous fluorescence quenching of O, M, S, and β micelles, implying successful incorporation of DHA into hydrophobic cores of micelles (O (DHA), M (DHA), S (DHA), and β (DHA)). The results showed that micelles provided spatial stability and improved solubility, and stability against thermal and ultraviolet (UV) light for DHA. The uptake of DHA from M (DHA), β (DHA), O (DHA), and S (DHA) was 3.27-, 3.91-, 2.7-, and 3.95-fold higher, respectively, than that of DHA by Caco-2 cells. Encapsulation in micelles increased DHA aqueous solubility and uptake, which enhanced cellular endogenous antioxidant defense. Meanwhile, increased uptake of DHA was verified by HepG2 cells, and O, M, S, and β micelles were proven to increase DHA uptake to reduce lipid deposition. Our findings strongly support the possibility that O, M, S, and β micelles can be regarded as a carrier for loading DHA.

Keywords: Stability, Micelle, Cellular uptake, Solubility, Docosahexaenoic acid

References(53)

[1]

M.L. Baack, S.E. Puumala, S.E. Messier, et al., Daily enteral DHA supplementation alleviates deficiency in premature infants, Lipids 51(4) (2016) 423-433. http://doi.org/10.1007/s11745-016-4130-4.
DOI Google Scholar
[2]

D.E. Barre, The role of consumption of alpha-linolenic, eicosapentaenoic and docosahexaenoic acids in human metabolic syndrome and type 2 diabetes-a mini-review, J. Oleo Sci. 56(7) (2007) 319-325. http://doi.org/10.5650/jos.56.319.
DOI Google Scholar
[3]

L. De Salazar, A. Torregrosa-García, A.J. Luque-Rubia, et al., Oxidative stress in endurance cycling is reduced dose-dependently after one month of re-esterified DHA supplementation, Antioxidants 9(11) (2020) 1145. http://doi.org/10.3390/antiox9111145.
DOI Google Scholar
[4]

S. Klingel, A. Metherel, M. Irfan, et al., EPA and DHA have divergent effects on serum triglycerides and lipogenesis, but similar effects on lipoprotein lipase activity: a randomized controlled trial, Am. J. Clin. Nutr. 6 (2019) 6. http://doi.org/10.1093/ajcn/nqz234.
DOI Google Scholar
[5]

A. Ismail, G. Bannenberg, H.B. Rice, et al., Oxidation in EPA- and DHA-rich oils: an overview, Lipid Technol. 28 (3/4) (2016) 55-59. http://doi.org/10.1002/lite.201600013.
DOI Google Scholar
[6]

E. Arab-Tehrany, M. Jacquot, C. Gaiani, et al., Beneficial effects and oxidative stability of omega-3 long-chain polyunsaturated fatty acids, Trends Food Sci. Technol. 25(1) (2012) 24-33. http://doi.org/10.1016/j.tifs.2011.12.002.
DOI Google Scholar
[7]

A.F. Vikbjerg, T.L. Andresen, K. Jørgensen, et al., Oxidative stability of liposomes composed of docosahexaenoic acid-containing phospholipids, J. Am. Oil Chem. Soc. 84(7) (2007) 631-637. http://doi.org/10.1007/s11746-007-1086-9.
DOI Google Scholar
[8]

G. Yildiz, J. Ding, S. Gaur, et al., Microencapsulation of docosahexaenoic acid (DHA) with four wall materials including pea protein-modified starch complex, Int. J. Biol. Macromol. 114 (2018) 935-941. http://doi.org/10.1016/j.ijbiomac.2018.03.175.
DOI Google Scholar
[9]

J. Hussein, W. Rasheed, T. Ramzy, et al., Synthesis of docosahexaenoic acid–loaded silver nanoparticles for improving endothelial dysfunctions in experimental diabetes, Hum. Exp. Toxicol. (2019). http://doi.org/10.1177/0960327119843586.
DOI Google Scholar
[10]

E.J. Olloqui, A. Castañeda-Ovando, E. Contreras-López, et al., Encapsulation of fish oil into low-cost alginate beads and EPA-DHA release in a rumino-intestinal in vitro digestion model, Eur. J. Lipid Sci. Technol. (2018). http://doi.org/10.1002/ejlt.201800036
DOI Google Scholar
[11]

P.V. Subbaiah, K.J. Dammanahalli, P. Yang, et al., Enhanced incorporation of dietary DHA into lymph phospholipids by altering its molecular carrier, Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1861(8) (2016) 723-729. http://doi.org/10.1016/j.bbalip.2016.05.002.
DOI Google Scholar
[12]

L. Gayoso, D. Ansorena, I. Astiasarán, DHA rich algae oil delivered by O/W or gelled emulsions: strategies to increase its bioaccessibility, J. Sci. Food Agric. (2018). http://doi.org/10.1002/jsfa.9420.
DOI Google Scholar
[13]

S. Gonzalez-Toledo, J. Wu, Encapsulation of long-chain n-3 polyunsaturated fatty acids using egg yolk, J. Am. Oil Chem. Soc. (2019). https://doi.org/10.1002/aocs.12299.
DOI Google Scholar
[14]

S. Alven, B.A. Aderibigbe, Efficacy of polymer-based nanocarriers for co-delivery of curcumin and selected anticancer drugs, Nanomaterials 10(8) (2020) 1556. https://doi.org/10.3390/nano10081556.
DOI Google Scholar
[15]

C. He, S. Wu, D. Liu, et al., Glycopeptide self-assembly modulated by glycan stereochemistry through glycan–aromatic interactions, J. Am. Chem. Soc. 142(40) (2020) 17015-17023. https://doi.org/10.1021/jacs.0c06360
DOI Google Scholar
[16]

H. Ma, J. Hao, Ordered patterns and structures via interfacial self-assembly: superlattices, honeycomb structures and coffee rings, Chem. Soc. Rev. 40(11) (2011) 5457. https://doi.org/10.1039/C1CS15059F.
DOI Google Scholar
[17]

Y. Du, C. Bao, J. Huang, et al., Improved stability, epithelial permeability and cellular antioxidant activity of β-carotene via encapsulation by self-assembled α-lactalbumin micelles, Food Chem. 271 (2019) 707-714. https://doi.org/10.1016/j.foodchem.2018.07.216.
DOI Google Scholar
[18]

N. Hanafy, M. El-Kemary, S. Leporatti, Micelles structure development as a strategy to improve smart cancer therapy, Cancers 10(7) (2018) 238. https://doi.org/10.3390/cancers10070238.
DOI Google Scholar
[19]

A. Bose, D.R. Burman, B. Sikdar, et al., Nanomicelles: types, properties and applications in drug delivery, IET Nanobiotechnol. (2021). https://doi.org/10.1049/nbt2.12018.
DOI Google Scholar
[20]

P. Jiang, J. Huang, C. Bao, et al., Enzymatically partial hydrolyzed α-lactalbumin peptides for self-assembled micelles formation and their application for co-encapsulation of multiple anti-oxidants, J. Agric. Food Chem. (2018). https://doi.org/10.1021/acs.jafc.8b03798.
DOI Google Scholar
[21]

Y. Tian, C. Shi, X. Zhang, et al., Nanomicelle based peroral delivery system for enhanced absorption and sustained release of 10-hydrocamptothecin, J. Biomed. Nanotechnol. 11(2) (2015) 262-273. https://doi.org/10.1166/jbn.2015.1909.
DOI Google Scholar
[22]

C. Qian, E.A. Decker, H. Xiao, et al., Physical and chemical stability of β-carotene-enriched nanoemulsions: influence of pH, ionic strength, temperature, and emulsifier type, Food Chem. 132(3) (2012) 1221-1229. https://doi.org/10.1016/j.foodchem.2011.11.091.
DOI Google Scholar
[23]

P. Hou, F. Pu, H. Zou, et al., Whey protein stabilized nanoemulsion: a potential delivery system for ginsenoside Rg3 whey protein stabilized nanoemulsion: potential Rg3 delivery system, Food Biosci. (2019). https://doi.org/10.1016/j.fbio.2019.100427.
DOI Google Scholar
[24]

M. Fathi, F. Donsi, D.J. McClements, Protein-based delivery systems for the nanoencapsulation of food ingredients, Compr. Rev. Food Sci. Food Saf. 17(4) (2018) 920-936. https://doi.org/10.1111/1541-4337.12360.
DOI Google Scholar
[25]

A. Abaee, M. Mohammadian, S.M. Jafari, Whey and soy protein-based hydrogels and nano-hydrogels as bioactive delivery systems, Trends Food Sci. Technol. 70 (2017) 69-81. https://doi.org/10.1016/j.tifs.2017.10.011.
DOI Google Scholar
[26]

A.O. Elzoghby, W.M. Samy, N.A. Elgindy, Albumin-based nanoparticles as potential controlled release drug delivery systems, J. Control. Release 157(2) (2012) 168-182. https://doi.org/10.1016/j.jconrel.
DOI Google Scholar
[27]

S., Rao, G. Xu, X. Lu, et al., Characterization of ovalbumin-carvacrol inclusion complexes as delivery systems with antibacterial application, Food Hydrocoll. 105(3) (2020) 105753. https://doi.org/10.1016/j.foodhyd.2020.105753.
DOI Google Scholar
[28]

T. Shi, Z. Xiong, H. Liu, et al., Ameliorative effects of L-arginine on heat-induced phase separation of aristichthys nobilis myosin are associated with the absence of ordered secondary structures of myosin, Food Res. Int. 141(10) (2021) 110154. https://doi.org/10.1016/j.foodres.2021.110154.
DOI Google Scholar
[29]

L. Zhu, Q. Xu, X. Liu, et al., Soy glycinin-soyasaponin mixtures at oil–water interface: interfacial behavior and O/W emulsion stability, Food Chem. (2020) 127062. https://doi.org/10.1016/j.foodchem.2020.127062.
DOI Google Scholar
[30]

X. Du, Z. Miao, D. Zhang, et al., Facile synthesis of β-lactoglobulin-functionalized multi-wall carbon nanotubes and gold nanoparticles on glassy carbon electrode for electrochemical sensing, Biosens. Bioelectron. 62 (2014) 73-78. https://doi.org/10.1016/j.bios.2014.06.030.
DOI Google Scholar
[31]

Y. Liu, Y. Fan, L. Gao, et al., Enhanced pH and thermal stability, solubility and antioxidant activity of resveratrol by nanocomplexation with α-lactalbumin, Food Funct. (2018). https://doi.org/10.1039/c8fo01172a.
DOI Google Scholar
[32]

R. Gao, Q. Yu, Y. Shen, et al., Production, bioactive properties, and potential applications of fish protein hydrolysates: developments and challenges, Trends Food Sci. Technol. 110 (2021) 687-699. https://doi.org/10.1016/j.tifs.2021.02.031.
DOI Google Scholar
[33]

C. Lavigueur, J.G. García, L. Hendriks, et al., Thermoresponsive giant biohybrid amphiphiles, Polym. Chem. 2(2) (2011) 333-340. https://doi.org/10.1039/C0PY00229A.
DOI Google Scholar
[34]

T. Nagano, M. Hirotsuka, H. Mori, et al., Dynamic viscoelastic study on the gelation of 7S globulin from soybeans, J. Agric. Food Chem. 40(6) (1992). https://doi.org/10.1021/jf00018a004.
DOI Google Scholar
[35]

M. van de Weert, Fluorescence quenching to study protein-ligand binding: common errors, J. Fluoresc. 20(2) (2009) 625-629. https://doi.org/10.1007/s10895-009-0572-x.
DOI Google Scholar
[36]

P. Hudáky, Kaslik, Gyula, et al., The differential specificity of chymotrypsin A and B is determined by amino acid 226, Eur. J. Biochem. 259(1/2) (1999) 528-533. https://doi.org/10.1046/j.1432-1327.1999.00075.x.
DOI Google Scholar
[37]

A. Barhoum, M.L. García-Betancourt, H. Rahier, et al., Physicochemical characterization of nanomaterials: polymorph, composition, wettability, and thermal stability, Emerging Applications of Nanoparticles and Architecture Nanostructures (2018) 255-278. https://doi.org/10.1016/B978-0-323-51254-1.00009-9.
DOI Google Scholar
[38]

E.B. Haghighi, N. Nikkam, M. Saleemi, et al., Shelf stability of nanofluids and its effect on thermal conductivity and viscosity, Meas. Sci. Technol. 24(10) (2013) 105301. https://doi.org/10.1088/0957-0233/24/10/105301.
DOI Google Scholar
[39]

S. Honary, F. Zahir, Effect of zeta potential on the properties of nano-drug delivery systems - a review (Part 1), Trop. J. Pharm. Res. 12(2) (2013). https://doi.org/10.4314/tjpr.v12i2.19.
DOI Google Scholar
[40]

J.E. Brinkman, B. Dorius, S. Sharma, Physiology, Body Fluids, Treasure Island (FL): StatPearls (2021).
[41]

M.A. Crawford, C. Leigh Broadhurst, M. Guest, et al., A quantum theory for the irreplaceable role of docosahexaenoic acid in neural cell signalling throughout evolution, Prostaglandins Leukot. Essent. Fatty Acids 88(1) (2013) 5-13. https://doi.org/ 10.1016/j.plefa.2012.08.005.
DOI Google Scholar
[42]

B.H. Wong, J.P. Chan, A. Cazenave-Gassiot, et al., Mfsd2a is a transporter for the essential ω-3 fatty acid docosahexaenoic acid (DHA) in eye and is important for photoreceptor cell development, J. Biol. Chem. 291(20) (2016) 10501-10514. https://doi.org/10.1074/jbc.M116.721340.
DOI Google Scholar
[43]

M. Simionescu, A. Gafencu, F. Antohe, Transcytosis of plasma macromolecules in endothelial cells: a cell biological survey, Microsc. Res. Tech. 57(5) (2002) 269-288. https://doi.org/10.1002/jemt.10086.
DOI Google Scholar
[44]

S.W. Ryter, K. Mizumura, A.M.K. Choi, The impact of autophagy on cell death modalities, Int. J. Cell Biol. (2014) 1-12. https://doi.org/10.1155/2014/502676.
DOI Google Scholar
[45]

M. Valko, D. Leibfritz, J. Moncol, et al., Free radicals and antioxidants in normal physiological functions and human disease, Int. J. Biochem. Cell Biol. 39 (1) (2007) 44–84.
DOI Google Scholar
[46]

C. Zca, C. Rta, E. Zsacd, et al., Role of oxidative stress in the pathogenesis of nonalcoholic fatty liver disease, Free Radic. Biol. Med. 152 (2020) 116-141. https://doi.org/10.1016/j.freeradbiomed.2020.02.025.
DOI Google Scholar
[47]

R. Stefanatos, A. Sanz, The role of mitochondrial ROS in the aging brain, FEBS Lett. 592(5) (2017) 743-758. https://doi.org/10.1002/1873-3468.12902.
DOI Google Scholar
[48]

M. Brentnall, L. Rodriguez-Menocal, R. de Guevara, et al., Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis, BMC Cell Biol. 14(1) (2013) 32. https://doi.org/10.1186/1471-2121-14-32.
DOI Google Scholar
[49]

S. Mazumder, D. Plesca, A. Almasan, Caspase-3 activation is a critical determinant of genotoxic stress-induced apoptosis, Methods Mol. Biol. (2008) 13-21. https://doi.org/10.1007/978-1-4939-1661-0_1.
DOI Google Scholar
[50]

I. Gasnereau, O. Ganier, F. Bourgain, et al., Flow cytometry to sort mammalian cells in cytokinesis, Cytometry A 71(1) (2007) 1-7. https://doi.org/ 10.1002/cyto.a.20352.
DOI Google Scholar
[51]

M. Delgado, A. Kothari, W.N. Hittelman, et al., Preparation of primary acute lymphoblastic leukemia cells in different cell cycle phases by centrifugal elutriation, J. Vis. Exp. 129 (2017). https://doi.org/10.3791/56418.
DOI Google Scholar
[52]

Y. Liu, X. Chen, J. Ding, et al., Improved solubility and bioactivity of camptothecin family antitumor drugs with supramolecular encapsulation by water-soluble pillar[6]arene, ACS Omega 2(8) (2017) 5283-5288. https://doi.org/10.1021/acsomega.7b01032.
DOI Google Scholar
[53]

Y. Xiong, Y. Zou, L. Chen, et al., Development and in vivo evaluation of ziyuglycoside I–loaded self-microemulsifying formulation for activity of increasing leukocyte, AAPS PharmSciTech 20(3) (2019). https://doi.org/10.1208/s12249-019-1313-3.
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 10 February 2022
Revised: 08 April 2022
Accepted: 30 April 2022
Published: 21 March 2023
Issue date: September 2023

Copyright

© 2023 Beijing Academy of Food Sciences.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31871831), Shenyang Science and technology innovation platform project (21-103-0-14, 21-104-0-28).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return