The impact of selected xanthophylls on oil hydrolysis by pancreatic lipase: in silico and in vitro studies.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
01 Feb 2024
01 Feb 2024
Historique:
received:
02
08
2023
accepted:
30
01
2024
medline:
2
2
2024
pubmed:
2
2
2024
entrez:
1
2
2024
Statut:
epublish
Résumé
Lipase inhibition is one of the directions to control obesity. In vitro assays have confirmed the inhibitory effect of selected xanthophylls, including astaxanthin, fucoxanthinol, fucoxanthin, and neoxanthin. Similarly, an in-silico study also demonstrated the successful inhibition of pancreatic lipase by astaxanthin. Unfortunately, the efficacy of these protocols in the emulsion state typical of lipid digestion remains untested. To address this issue, the current study employed the pH-stat test, which mimics lipid digestion in the gastrointestinal tract, to evaluate native and prepared sea buckthorn and rapeseed oils with varying xanthophyll contents from 0 to 1400 mg/kg oil. Furthermore, a molecular docking of zeaxanthin and violaxanthin (commonly found in plant-based foods), astaxanthin (widely distributed in foods of marine origin) and orlistat (approved as a drug) was performed. The in-silico studies revealed comparable inhibitory potential of all tested xanthophylls (variation from - 8.0 to - 9.3 kcal/mol), surpassing that of orlistat (- 6.5 kcal/mol). Nonetheless, when tested in an emulsified state, the results of pH-stat digestion failed to establish the inhibitory effect of xanthophylls in the digested oils. In fact, lipolysis of native xanthophyll-rich sea buckthorn oil was approximately 22% higher than that of the xanthophyll-low preparation. The key insight derived from this study is that the amphiphilic properties of xanthophylls during the digestion of xanthophyll-rich lipids/meals facilitate emulsion formation, which leads to enhanced fat lipolysis.
Identifiants
pubmed: 38302772
doi: 10.1038/s41598-024-53312-9
pii: 10.1038/s41598-024-53312-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2731Subventions
Organisme : Narodowe Centrum Nauki
ID : 2018/31/B/NZ9/02433
Informations de copyright
© 2024. The Author(s).
Références
Lin, X. & Li, H. Obesity: Epidemiology, pathophysiology, and therapeutics. Front. Endocrinol. 12, 706978 (2021).
doi: 10.3389/fendo.2021.706978
Müller, T. D., Blüher, M., Tschöp, M. H. & DiMarchi, R. D. Anti-obesity drug discovery: Advances and challenges. Nat. Rev. Drug Discov. 21, 201–223 (2022).
doi: 10.1038/s41573-021-00337-8
pubmed: 34815532
Mamdooh, N. et al. Evaluation of selected commercial pharmacotherapeutic drugs as potential pancreatic lipase inhibitors and antiproliferative compounds. Drug Dev. Res. 80, 310–324 (2019).
doi: 10.1002/ddr.21499
pubmed: 30511444
Acevedo-Fani, A. & Singh, H. Biophysical insights into modulating lipid digestion in food emulsions. Prog. Lipid Res. 85, 101129 (2022).
doi: 10.1016/j.plipres.2021.101129
pubmed: 34710489
Bajes, H. R., Almasri, I. & Bustanji, Y. Plant products and their inhibitory activity against pancreatic lipase. Rev. Bras. Farmacogn. 30, 321–330 (2020).
doi: 10.1007/s43450-020-00055-z
Birari, R. B. & Bhutani, K. K. Pancreatic lipase inhibitors from natural sources: Unexplored potential. Drug Discov. Today 12, 879–889 (2007).
doi: 10.1016/j.drudis.2007.07.024
pubmed: 17933690
Podsędek, A., Redzynia, M., Klewicka, E. & Koziołkiewicz, M. Matrix effects on the stability and antioxidant activity of red cabbage anthocyanins under simulated gastrointestinal digestion. Biomed. Res. Int. 2014, 1–11 (2014).
doi: 10.1155/2014/365738
Du, X. et al. Inhibitory effect of astaxanthin on pancreatic lipase with inhibition kinetics integrating molecular docking simulation. J. Funct. Foods 48, 551–557 (2018).
doi: 10.1016/j.jff.2018.07.045
Matsumoto, M. et al. Suppressive effects of the marine carotenoids, fucoxanthin and fucoxanthinol on triglyceride absorption in lymph duct-cannulated rats. Eur. J. Nutr. 49, 243–249 (2010).
doi: 10.1007/s00394-009-0078-y
pubmed: 19888619
Wang, N., Manabe, Y., Sugawara, T., Paul, N. A. & Zhao, J. Identification and biological activities of carotenoids from the freshwater alga Oedogonium intermedium. Food Chem. 242, 247–255 (2018).
doi: 10.1016/j.foodchem.2017.09.075
pubmed: 29037686
Hitoe, S. & Shimoda, H. Seaweed fucoxanthin supplementation improves obesity parameters in mild obese Japanese subjects. FFHD 7, 246–262 (2017).
doi: 10.31989/ffhd.v7i4.333
Lopes, D. B., Fraga, L. P., Fleuri, L. F. & Macedo, G. A. Lipase and esterase—To what extent can this classification be applied accurately?. Food Sci. Technol. 31, 603–613 (2011).
doi: 10.1590/S0101-20612011000300009
Park, J.-Y., Ha, J., Choi, Y., Chang, P.-S. & Park, K.-M. Optimization of spectrophotometric and fluorometric assays using alternative substrates for the high-throughput screening of lipase activity. J. Chem. 2021, 1–10 (2021).
doi: 10.1155/2021/3688124
Damerau, A. et al. Food fortification using spray-dried emulsions of fish oil produced with maltodextrin, plant and whey proteins—Effect on sensory perception, volatiles and storage stability. Molecules 27, 3553 (2022).
doi: 10.3390/molecules27113553
pubmed: 35684490
pmcid: 9182505
Dąbrowski, G. et al. Composition of flesh lipids and oleosome yield optimization of selected sea buckthorn (Hippophae rhamnoides L.) cultivars grown in Poland. Food Chem. 369, 130921 (2022).
doi: 10.1016/j.foodchem.2021.130921
pubmed: 34461512
Pop, R. M. et al. Carotenoid composition of berries and leaves from six Romanian sea buckthorn (Hippophae rhamnoides L.) varieties. Food Chem. 147, 1–9 (2014).
doi: 10.1016/j.foodchem.2013.09.083
pubmed: 24206678
Andersson, S. C., Olsson, M. E., Johansson, E. & Rumpunen, K. Carotenoids in sea buckthorn (Hippophae rhamnoides L.) berries during ripening and use of pheophytin a as a maturity marker. J. Agric. Food Chem. 57, 250–258 (2009).
doi: 10.1021/jf802599f
pubmed: 19125686
Tkacz, K., Wojdyło, A., Turkiewicz, I. P., Bobak, Ł & Nowicka, P. Anti-oxidant and anti-enzymatic activities of sea buckthorn (Hippophaë rhamnoides L.) fruits modulated by chemical components. Antioxidants 8, 618 (2019).
doi: 10.3390/antiox8120618
pubmed: 31817215
pmcid: 6943611
Ahmed, B., Ali Ashfaq, U. & Usman, Mirza M. Medicinal plant phytochemicals and their inhibitory activities against pancreatic lipase: Molecular docking combined with molecular dynamics simulation approach. Nat. Prod. Res. 32, 1123–1129 (2018).
doi: 10.1080/14786419.2017.1320786
pubmed: 28446025
Molinspiration. Molinspiration Cheminformatics, https://www.molinspiration.com (2023).
Sahu, V. K., Singh, R. K. & Singh, P. P. Extended rule of five and prediction of biological activity of peptidic HIV-1-PR inhibitors. Trends J. Sci. Res. 1, 20–42 (2022).
doi: 10.31586/ujpp.2022.403
Naqvi, A. A. T., Mohammad, T., Hasan, G. M. & Hassan, Md. I. Advancements in docking and molecular dynamics simulations towards ligand-receptor interactions and structure–function relationships. Curr. Top. Med. Chem. 18, 1755–1768 (2018).
doi: 10.2174/1568026618666181025114157
pubmed: 30360721
Shamarao, N. & Chethankumar, M. Antiobesity drug-likeness properties and pancreatic lipase inhibition of a novel low molecular weight lutein oxidized product, LOP6. Food Funct. 13, 6036–6055 (2022).
doi: 10.1039/D1FO04064B
pubmed: 35615990
Pereira, A. G. et al. Xanthophylls from the sea: Algae as source of bioactive carotenoids. Mar. Drugs 19, 188 (2021).
doi: 10.3390/md19040188
pubmed: 33801636
pmcid: 8067268
Grudzinski, W. et al. Localization and orientation of xanthophylls in a lipid bilayer. Sci. Rep. 7, 9619 (2017).
doi: 10.1038/s41598-017-10183-7
pubmed: 28852075
pmcid: 5575131
Shibata, A., Kiba, Y., Akati, N., Fukuzawa, K. & Terada, H. Molecular characteristics of astaxanthin and β-carotene in the phospholipid monolayer and their distributions in the phospholipid bilayer. Chem. Phys. Lipids 113, 11–22 (2001).
doi: 10.1016/S0009-3084(01)00136-0
pubmed: 11687223
Khan, F. I. et al. The lid domain in lipases: Structural and functional determinant of enzymatic properties. Front. Bioeng. Biotechnol. 5, 16 (2017).
doi: 10.3389/fbioe.2017.00016
pubmed: 28337436
pmcid: 5343024
Carpen, A., Bonomi, F., Iametti, S. & Marengo, M. Effects of starch addition on the activity and specificity of food-grade lipases. Biotechnol. Appl. Biochem. 66, 607–616 (2019).
doi: 10.1002/bab.1761
pubmed: 31056790
Ye, Z. et al. Fatty acid profiles of typical dietary lipids after gastrointestinal digestion and absorbtion: A combination study between in-vitro and in-vivo. Food Chem. 280, 34–44 (2019).
doi: 10.1016/j.foodchem.2018.12.032
pubmed: 30642504
Armand, M. et al. Digestion and absorption of 2 fat emulsions with different droplet sizes in the human digestive tract. Am. J. Clin. Nutr. 70, 1096–1106 (1999).
doi: 10.1093/ajcn/70.6.1096
pubmed: 10584056
Chetima, A., Wahabou, A., Zomegni, G., Ntieche Rahman, A. & Bup Nde, D. Bleaching of neutral cotton seed oil using organic activated carbon in a batch system: Kinetics and adsorption isotherms. Processes 6, 22 (2018).
doi: 10.3390/pr6030022
PubChem. PubChem Database; https://pubchem.ncbi.nlm.nih.gov (2023).
Korkus, E. et al. Evaluation of the anti-diabetic activity of sea buckthorn pulp oils prepared with different extraction methods in human islet EndoC-betaH1 cells. NFS J. 27, 54–66 (2022).
doi: 10.1016/j.nfs.2022.05.002
Czaplicki, S., Tańska, M. & Konopka, I. Sea-buckthorn oil in vegetable oils stabilisation. Ital. J. Food Sci. 28, 412–425 (2016).