Nanoliposome-Mediated Encapsulation of Chlorella Oil for the Development of a Controlled-Release Lipid-Lowering Formulation
Abstract
:1. Introduction
2. Materials and Methods
2.1. Reagents
2.2. Preparation of CO-NLP
2.3. Analysis of Chlorella Oil Content
2.4. Analysis of the Fatty Acid Composition of Chlorella Oil
2.5. Encapsulation Efficiency
2.6. Determination of Particle Size, Zeta Potential, and Polydispersity Coefficient
2.7. Microscopic Morphological Analysis
2.8. Storage Stability of CO-NLP
2.9. In Vitro Release Experiments of CO-NLP
2.10. In Vitro Digestion Experiments
2.11. In Vitro Simulated Digestion Bioavailability Study
2.12. Calculation of the Particle Dimensions and Zeta Potential of Digestion Byproducts from CO-NLP
2.13. Assessment of Inhibitory Effects of CO-NLP on Porcine Pancreatic Cholesterol Esterase Activity
2.14. Assessment of the Hypolipidemic Impact of CO-NLP in the C. elegans Model
2.15. Statistical Analysis
3. Results and Discussion
3.1. Analysis of Chlorella Oil Content and Fatty Acid Composition
3.2. Characterization of the Physical and Chemical Attributes of CO-NLP
3.2.1. Particle Size and Zeta Potential of CO-NLP
3.2.2. Microscopic Morphological Observation
3.2.3. Analysis of the Storage Stability of CO-NLP
3.2.4. In Vitro Release Studies of Microalgal Nanoliposomes
3.2.5. Bioavailability of CO-NLP
3.2.6. Changes in Particle Size and Zeta Potential during Digestion of CO-NLP
3.3. Evaluation of the Lipid-Lowering Activity of CO-NLP
3.3.1. Inhibition Activities of CO-NLP on Cholesterol Esterase
3.3.2. Assessment of the Hypolipidemic Impact In Vivo of CO-NLP in C. elegans MODEL
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Salvia-Trujillo, L.; Qian, C.; Martín-Belloso, O.; McClements, D.J. Influence of particle size on lipid digestion and β-carotene bioaccessibility in emulsions and nanoemulsions. Food Chem. 2013, 141, 1472–1480. [Google Scholar] [CrossRef] [PubMed]
- Enamala, M.K.; Enamala, S.; Murthy, C.; Jagadish, D.; Rajasri, Y.; Bhulakshmi, K.; Tirumala, V.A.; Jeevitha, V.; Chandrasekhar, K. Production of biofuels from microalgae-a review on cultivation, harvesting, lipid extraction, and numerous applications of microalgae. Renew. Sustain. Energy Rev. 2018, 94, 49–68. [Google Scholar] [CrossRef]
- Sarabandi, K.; Seid, M.J.; Maryam, M.; Zahra, A.; Akram, P.; Maryam, K.H. Production of Reconstitutable Nanoliposomes Loaded with Flaxseed Protein Hydrolysates: Stability and Characterization. Food Hydrocoll. 2019, 96, 442–450. [Google Scholar] [CrossRef]
- Zhu, Y.; Zhou, Y.; Tian, T.; Wang, Z.; Qi, B.; Zhang, X.; Liu, J.; Li, Y.; Jiang, L.; Wang, Z. In vitro simulated digestion and microstructure of peppermint oil nanoemulsion. J. Oleo Sci. 2019, 68, 863–871. [Google Scholar] [CrossRef] [PubMed]
- Masoud, A.M.; Parastou, F.; Parisa, A.; Azam, A.; Mohammad, Y.; Marjan, G.; Seyede, M.H. Encapsulation of vitamins using nanoliposome: Recent advances and perspectives. Adv. Pharm. Bull. 2023, 13, 48–68. [Google Scholar]
- Wickramasinghe, A.S.D.; Attanayake, A.P.; Kalansuriya, P. Herbal extracts encapsulated nanoliposomes as potential glucose-lowering agents: An in vitro and in vivo approach using three herbal extracts. J. Pharm. Sci. 2023, 112, 2538–2551. [Google Scholar] [CrossRef]
- Darachai, P.; Limpawattana, M.; Hawangjoo, M.; Klaypradit, W. Effects of shrimp waste types and their cooking on properties of extracted astaxanthin and its characteristics in liposomes. J. Food Nutr. Res. 2019, 7, 530–536. [Google Scholar] [CrossRef]
- Pan, L.; Wang, H.; Gu, K. Nanoliposomes as vehicles for astaxanthin: Characterization, in vitro release evaluation and structure. Molecules 2018, 23, 2822. [Google Scholar] [CrossRef]
- Ojagh, S.M.; Hasani, S. Characteristics and oxidative stability of fish oil nano-liposomes and its application in functional bread. J. Food Meas. Charact. 2018, 12, 1084–1092. [Google Scholar] [CrossRef]
- Chen, Y.; Shuang, L.; Yuan, Y.J. Quality assessment of blended vegetable oil based on fatty acid index. J. Food Saf. Qual. 2021, 12, 2073–2079. [Google Scholar]
- Wang, J.L.; Dong, X.Y.; Wei, F.; Zhong, J.; Liu, B.; Yao, M.H.; Yang, M.; Zheng, C.; Quek, S.Y.; Chen, H. Preparation and characterization of novel lipid carriers containing microalgae oil for food applications. J. Food Sci. 2014, 79, 169–177. [Google Scholar] [CrossRef] [PubMed]
- Smith, M.C.; Crist, R.M.; Clogston, J.D.; McNeil, S.E. Zeta potential: A case study of cationic, anionic, and neutral liposomes. Anal. Bioanal. Chem. 2017, 409, 5779–5787. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Jiang, S.; Liu, L.; Zhao, Y.; Zeng, M. Encapsulation of oyster protein hydrolysates in nanoliposomes: Vesicle characteristics, storage stability, in vitro release, and gastrointestinal digestion. J. Food Sci. 2021, 86, 960–968. [Google Scholar] [CrossRef] [PubMed]
- Su, J.; Ma, C.; Yang, L.; Wang, H.; Gao, C.; Nie, R. Inhibition of pancreatic cholesterol esterase activities and cholesterol micelle of EGCG and quercetin. Sci. Technol. Food Ind. 2015, 36, 346–349. [Google Scholar]
- Lv, W.; Xu, D. Docosahexaenoic acid delivery systems, bioavailability, functionality, and applications: A review. Foods 2022, 11, 2685. [Google Scholar] [CrossRef] [PubMed]
- Li, T.; Nowell, C.J.; Cipolla, D.; Rades, T.; Boyd, B.J. Direct comparison of standard transmission electron microscopy and cryogenic-TEM in imaging nanocrystals inside liposomes. Mol. Pharm. 2019, 16, 1775–1781. [Google Scholar] [CrossRef] [PubMed]
- Rattanawongwiboon, T.; Soontaranon, S.; Hemvichian, K.; Lertsarawut, P.; Laksee, S.; Picha, R. Study on particle size and size distribution of gold nanoparticles by TEM and SAXS. Radiat. Phys. Chem. 2022, 191, 109842. [Google Scholar] [CrossRef]
- Safi, C.; Zebib, B.; Merah, O.; Pontalier, P.Y.; Vaca-Garcia, C. Morphology, composition, production, processing and applications of chlorella vulgaris: A review. Renew. Sustain. Energy Rev. 2014, 35, 265–278. [Google Scholar] [CrossRef]
- Wang, F.L.; Pu, C.F.; Liu, M.Y.; Li, R.S.; Yue, S.; Tang, W.T.; Sun, Q.J.; Qin, T. Fabrication and characterization of walnut peptides-loaded proliposomes with three lyoprotectants: Environmental stabilities and antioxidant/antibacterial activities. Food Chem. 2022, 366, 130643. [Google Scholar] [CrossRef]
- Xiao, X.X.; Xue, H.W.; Yu, Z.L.; He, J.H. Incorporation of the sterol from camellia oil deodorant distillate into vitamin C liposomes: Vesicle characteristics, stability, release, and bioavailability. Food Biophys. 2023, 18, 10–22. [Google Scholar] [CrossRef]
- Peschka, R.; Dennehy, C.; Szoka, J.F.C. A simple in vitro model to study the release kinetics of liposome encapsulated material. J. Control. Release 1998, 56, 41–51. [Google Scholar] [CrossRef]
- Tian, S.J.; Zhang, B.B.; Wang, L.; Chang, H.M. Study on stability and release performance of flaxseed oil precursor liposomes. J. Chin. Cereals Oils Assoc. 2019, 34, 92–106. [Google Scholar]
- Zeng, L.; An, L.; Wu, X. Modeling drug-carrier interaction in the drug release from nanocarriers. J. Drug Deliv. 2011, 2011, 370308. [Google Scholar] [CrossRef] [PubMed]
- Charoensit, P.; Kawakami, S.; Higuchi, Y.; Yamashita, F.; Hashida, M. Enhanced Growth Inhibition of Metastatic Lung Tumors by Intravenous Injection of ATRA-cationic Liposome IL-12 PDNA Complexes in Mice. Cancer Gene Ther. 2010, 17, 512–522. [Google Scholar] [CrossRef] [PubMed]
- Shi, J.; Jun, S.; De, S.F.; Pei, Y.; Shao, K.C. Stimuli-responsive Hybrid Composites Based on CaCO3 Microparticles and Smart Polyelectrolytes for Controllable Drug Delivery. Polym. Bull. 2014, 71, 1857–1873. [Google Scholar] [CrossRef]
- Raj, S.; Khurana, S.; Choudhari, R.; Kesari, K.K.; Kamal, M.A.; Garg, N.; Ruokolainen, J.; Das, B.C.; Kumar, D. Specific targeting cancer cells with nanoparticles and drug delivery in cancer therapy. Semin. Cancer Biol. 2021, 69, 166–177. [Google Scholar] [CrossRef] [PubMed]
- Pan, Y.; Nitin, N. Real-time measurements to characterize dynamics of emulsion interface during simulated intestinal digestion. Colloids Surf. B Biointerfaces 2016, 141, 233–241. [Google Scholar] [CrossRef]
- Haas, G.H.D.; Sarda, L.; Roger, J. Positional specific hydrolysis of phospholipids by pancreatic lipase. BBA-Lipids Lipid Metab. 1965, 106, 638–640. [Google Scholar] [CrossRef]
- Howles, P.N.; Carter, C.P.; Hui, D.Y. Dietary free and esterified cholesterol absorption in cholesterol esterase (bile salt-stimulated lipase) gene-targeted mice. J. Biol. Chem. 1996, 271, 7196–7202. [Google Scholar] [CrossRef]
- He, S.; Gu, C.; Wang, D.; Xu, W.; Wang, R.; Ma, Y. The stability and in vitro digestion of curcumin emulsions containing Konjac glucomannan. LWT 2020, 117, 108672. [Google Scholar] [CrossRef]
- Kossena, G.A.; Boyd, B.J.; Porter, C.J.H.; Charman, W.N. 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. 2003, 92, 634–648. [Google Scholar] [CrossRef] [PubMed]
- O’Connor, C.J.; Wallace, R.G.; Iwamoto, K.; Taguchi, T.; Sunamoto, J. Bile salt damage of egg phosphatidylcholine liposomes. BBA-Biomembr. 1985, 817, 95–102. [Google Scholar] [CrossRef] [PubMed]
- Zou, L.; Zheng, B.; Liu, W.; Liu, C.; Xiao, H.; McClements, D.J. Enhancing nutraceutical bioavailability using excipient emulsions: Influence of lipid droplet size on solubility and bioaccessibility of powdered curcumin. J. Funct. Foods 2015, 15, 72–83. [Google Scholar] [CrossRef]
- Ahmed, K.; Li, Y.; McClements, D.J.; Xiao, H. Nanoemulsion- and emulsion-based delivery systems for curcumin: Encapsulation and release properties. Food Chem. 2012, 132, 799–807. [Google Scholar] [CrossRef]
- Makino, K.; Yamada, T.; Kimura, M.; Oka, T.; Ohshima, H.; Kondo, T. Temperature- and ionic strength-induced conformational changes in the lipid head group region of liposomes as suggested by zeta potential data. Biophys. Chem. 1991, 41, 175–183. [Google Scholar] [CrossRef] [PubMed]
- Koyande, A.K.; Chew, K.W.; Rambabu, K.; Tao, Y.; Chu, D.T.; Show, P.L. Microalgae: A potential alternative to health supplementation for humans. Food Sci. Hum. Wellness 2019, 8, 16–24. [Google Scholar] [CrossRef]
- Regueiras, A.; Huguet, Á.; Conde, T.; Couto, D.; Domingues, P.; Domingues, M.R.; Costa, A.M.; Silva, J.L.D.; Vasconcelos, V.; Urbatzka, R. Potential anti-obesity, anti-steatosis, and anti-inflammatory properties of extracts from the microalgae chlorella vulgaris and chlorococcum amblystomatis under different growth conditions. Mar. Drugs 2022, 20, 9. [Google Scholar] [CrossRef]
- Yang, Y.; Ge, S.; Chen, Q.; Lin, S.; Zeng, S.; Tan, B.K.; Hu, J. Chlorella unsaturated fatty acids suppress high-fat diet-induced obesity in C57/BL6J mice. J. Food Sci. 2022, 87, 3644–3658. [Google Scholar] [CrossRef]
- Zhang, H.; Wu, Q.; Wei, X.; Qin, X. Pancreatic lipase and cholesterol esterase inhibitory effect of Camellia nitidissima Chi flower extracts in vitro and in vivo. Food Biosci. 2020, 37, 100682. [Google Scholar] [CrossRef]
Tube | Cholesterol Esterase Solution (μL) | CO-NLP (μL) | PNPB (μL) | Buffer (mL) |
---|---|---|---|---|
Blank 1 (A1) | 50 | - | 10 | 1 |
Blank control 2 (A2) | - | - | 10 | 1 |
Sample 3 (A3) | 50 | 25 | 10 | 1 |
Sample control 4 (A4) | - | 25 | 10 | 1 |
Composition | Relative Content | |
---|---|---|
Octanoic acid | C8:0 | 0.01 ± 0.00% |
Carpic acid | C10:0 | 0.03 ± 0.01% |
Hendecanoic acid | C11:0 | 10.50 ± 0.27% |
Lauric acid | C12:0 | 0.15 ± 0.05% |
Tridecanoic acid | C13:0 | 0.02 ± 0.00% |
Myristic acid | C14:0 | 11.50 ± 0.15% |
Myristoleic acid | C14:1 | 0.02 ± 0.01% |
Pentadecanoic acid | C15:0 | 1.25 ± 0.11% |
Pentadecanoic acid | C15:1 | 0.04 ± 0.01% |
Palmitic acid | C16:0 | 25.02 ± 0.74% |
Palmitoleic acid | C16:1 | 11.34 ± 0.91% |
cis-10-heptadecenoic acid | C17:0 | 6.81 ± 0.96% |
Heptadecanoic acid | C17:1 | 0.13 ± 0.02% |
Stearic acid | C18:0 | 1.02 ± 0.19% |
Oleic acid | C18:1n9c | 2.51 ± 0.48% |
Linolelaidic acid | C18:2n6t | 1.71 ± 0.12% |
Linoleic acid | C18:2n6c | 1.71 ± 0.11% |
gamma linolenic acid | C18:3n6 | 0.84 ± 0.04% |
arachidic acid | C20:0 | 0.31 ± 0.02% |
11-Eicosenoic acid | C20:1n9 | 0.02 ± 0.00% |
11,14-Eicosadienoicacid | C20:2 | 0.01 ± 0.00% |
cis-8,11,14-Eicosatrienoic | C20:3n6 | 0.20 ± 0.03% |
Arachidonic acid | C20:4n6 | 1.46 ± 0.08% |
cis-11,14,17-Eicosatrienoic acid | C20:3n3 | 0.02 ± 0.00% |
Eicosapentaenoic acid (EPA) | C20:5 | 12.52 ± 0.19% |
Heneicosanoic acid | C21:0 | 0.02 ± 0.00% |
Docosanoic acid | C22:0 | 0.12 ± 0.02% |
Erucic acid | C22:1n9 | 0.07 ± 0.01% |
cis-13,16-Docosadienoic acid | C22:2 | 0.01 ± 0.00% |
Docosahexaenoic acid (DHA) | C22:6n3 | 9.10 ± 0.13% |
Tricosanoic acid | C23:0 | 0.01 ± 0.00% |
Tricosanoic acid | C24:0 | 0.59 ± 0.31% |
Nervonic acid | C24:1n9 | 0.94 ± 0.17% |
Fitted Equation | Fitted Results | R2 |
---|---|---|
Zero-level kinetic equation [22] | Q = 1.4402t + 22.5620 | 0.7764 |
The first-level kinetic equation [23] | Q = 82.6282(1 − exp(−0.0897t)) | 0.9911 |
Higuchi plane diffusion equation [24] | Q = 12.6950t1/2 + 1.9597 | 0.9351 |
Retger-Peppas equation [25] | Q = 15.20t0.452 | 0.9438 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tu, L.; Zeng, J.; Bai, X.; Wu, Z.; Wu, J.; Xu, S. Nanoliposome-Mediated Encapsulation of Chlorella Oil for the Development of a Controlled-Release Lipid-Lowering Formulation. Foods 2024, 13, 158. https://doi.org/10.3390/foods13010158
Tu L, Zeng J, Bai X, Wu Z, Wu J, Xu S. Nanoliposome-Mediated Encapsulation of Chlorella Oil for the Development of a Controlled-Release Lipid-Lowering Formulation. Foods. 2024; 13(1):158. https://doi.org/10.3390/foods13010158
Chicago/Turabian StyleTu, Lanlan, Jihao Zeng, Xue Bai, Ziyun Wu, Jinhong Wu, and Shannan Xu. 2024. "Nanoliposome-Mediated Encapsulation of Chlorella Oil for the Development of a Controlled-Release Lipid-Lowering Formulation" Foods 13, no. 1: 158. https://doi.org/10.3390/foods13010158