Anti-osteoporosis effects of mammalian lignans and their precursors from flaxseed and safflower seed using zebrafish model.

anti-osteoporosis flaxseed lignan mammalian lignan safflower seed

Journal

Journal of food science
ISSN: 1750-3841
Titre abrégé: J Food Sci
Pays: United States
ID NLM: 0014052

Informations de publication

Date de publication:
27 Oct 2023
Historique:
revised: 26 08 2023
received: 18 06 2023
accepted: 12 10 2023
medline: 27 10 2023
pubmed: 27 10 2023
entrez: 27 10 2023
Statut: aheadofprint

Résumé

Secoisolariciresinol diglucoside (SDG) and tracheloside (TCL) are the main lignan components of flaxseed cake and safflower seed cake, which are by-products of oil extraction. Both SDG and TCL are metabolized into mammalian lignan enterolactone (EL) with the involvement of intestinal bacteria. In this research, we evaluated the anti-osteoporosis effects of SDG and the in vivo metabolites EL and enterodiol (ED) prepared in our previous work, as well as the newly isolated chemical constituents from safflower seed, including TCL, the lactone ring opening product of TCL (OTCL) and two alkaloids on the alloxan-induced zebrafish model. All the compounds showed significant anti-osteoporosis effects at 80 µM, with p < 0.05 for EL and p < 0.001 for other compounds compared with the model. SDG and TCL showed the most significant and concentration-dependent effects, with p < 0.001 compared with model at 20 µM. The alkaloids, N-coumaroylserotonin glucoside and N-feruloylserotonin glucoside, also showed anti-osteoporosis at 20 µM with p < 0.01, whereas EL, ED, and OTCL showed no significant effects. Quantitative real-time polymerase chain reaction revealed that SDG and TCL upregulated the expression of osteogenic genes Runx2, SP7, OPG, Col1a1a, Alp, ON, OPN, and OCN in alloxan-treated zebrafish. The in vivo metabolite of lignans, EL, showed significant anti-inflammatory effect (p < 0.01) at 20 µM, which might also help to combat osteoporosis and other complications caused by excessive immune response in the body. The results provided scientific data for using the oil extraction by-products as sources of anti-osteoporosis compounds. PRACTICAL APPLICATION: This study found that lignans in flaxseed cake and safflower seed cake exhibited anti-osteoporosis effects by upregulating the expression of osteogenic genes, making the oil extraction by-products sources of anti-osteoporosis compounds.

Identifiants

pubmed: 37889085
doi: 10.1111/1750-3841.16816
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : The Science and Technology Program of Inner Mongolia Autonomous Region of China
ID : 2019GG247
Organisme : The autonomous project of Inner Mongolia University

Informations de copyright

© 2023 Institute of Food Technologists.

Références

Arooj, A., Rabail, R., Naeem, M., Goksen, G., Xu, B., & Aadil, R. M. (2023). A comprehensive review of the bioactive components of sesame seeds and their impact on bone health issues in postmenopausal women. Food and Function, 14, 4966-4980. https://doi.org/10.1039/d3fo00531c
Boldizsar, I., Kraszni, M., Toth, F., Noszal, B., & Molnar-Perl, I. (2010). Complementary fragmentation pattern analysis by gas chromatography-mass spectrometry and liquid chromatography tandem mass spectrometry confirmed the precious lignan content of Cirsium weeds. Journal of Chromatography A, 1217, 6281-6289. https://doi.org/10.1016/j.chroma.2010.08.018
Brown, J. P., Adachi, J. D., Schemitsch, E., Tarride, J. E., Brown, V., Bell, A., Reiner, M., Oliveira, T., Motsepe-Ditshego, P., Burke, N., & Slatkovska, L. (2021). Mortality in older adults following a fragility fracture: Real-world retrospective matched-cohort study in Ontario. BMC Musculoskeletal Disorders, 22, 105. https://doi.org/10.1186/s12891-021-03960-z
Caro, M., Iturria, I., Martinez-Santos, M., Pardo, M. A., Rainieri, S., Tueros, I., & Navarro, V. (2016). Zebrafish dives into food research: Effectiveness assessment of bioactive compounds. Food &Function, 7, 2615-2623. https://doi.org/10.1039/c6fo00046k
Chemat, F., Rombaut, N., Sicaire, A. G., Meullemiestre, A., Fabiano-Tixier, A. S., & Abert-Vian, M. (2017). Ultrasound assisted extraction of food and natural products. Mechanisms, techniques, combinations, protocols and applications. A review. Ultrasonics Sonochemistry, 34, 540-560. https://doi.org/10.1016/j.ultsonch.2016.06.035
Cui, X.-Y., Shan, C.-B., Zhang, D.-J., & Ma, C.-M. (2023). Investigation on the in vivo antithrombotic effects of typical plant phenolic compounds. Journal of Inner Mongolia University (Natural Science Edition), (Published online first). https://kns.cnki.net/kcms/detail//15.1052.N.20230119.1716.001.html
Dietrich, K., Fiedler, I. A. K., Kurzyukova, A., López-Delgado, A. C., McGowan, L. M., Geurtzen, K., Hammond, C. L., Busse, B., & Knopf, F. (2021). Skeletal biology and disease modeling in zebrafish. Journal of Bone and Mineral Research, 6, 436-458.
Dubale, N. M., Kapron, C. M., & West, S. L. (2022). Commentary: Zebrafish as a model for osteoporosis-An approach to accelerating progress in drug and exercise-based treatment. International Journal of Environental Research and Public Health, 19, 15866. https://doi.org/10.3390/ijerph192315866
Eeckhaut, E., Struijs, K., Possemiers, S., Vincken, J. P., De Keukeleire, D., & Verstraete, W. (2008). Metabolism of the lignan macromolecule into enterolignans in the gastrointestinal lumen as determined in the simulator of the human intestinal microbial ecosystem. Journal of Agricultural and Food Chemistry, 56, 4806-4812. https://doi.org/10.1021/jf800101s
Eggers, B., Wagenheim, A.-M., Jung, S., Kleinheinz, J., Nokhbehsaim, M., Kramer, F.-J., & Sielker, S. (2022). Effect of cold atmospheric plasma (CAP) on osteogenic differentiation potential of human osteoblasts. International Journal of Molecular Sciences, 23, 2503. https://doi.org/10.3390/ijms23052503
Gaya, P., Medina, M., Sánchez-Jiménez, A., & Landete, J. M. (2016). Phytoestrogen metabolism by adult human gut microbiota. Molecules (Basel, Switzerland), 21, 1034. https://doi.org/10.3390/molecules21081034
Hu, Y., Yuan, W., Cai, N., Jia, K., Meng, Y. L., Wang, F., Ge, Y. R., & Lu, H. Q. (2022). Exploring quercetin anti-osteoporosis pharmacological mechanisms with in silico and in vivo models. Life, 12, 980.
Jin, J. S., & Hattori, M. (2010). Human intestinal bacterium, strain END-2 is responsible for demethylation as well as lactonization during plant lignan metabolism. Biologial & Pharmaceutical Bulletin, 33, 1443-1447. https://doi.org/10.1248/bpb.33.1443
Jin, J. S., Tobo, T., Chung, M. H., Ma, C. M., & Hattori, M. (2012). Transformation of trachelogenin, an aglycone of tracheloside from safflower seeds, to phytoestrogenic (−)-enterolactone by human intestinal bacteria. Food Chemistry, 134, 74-80. https://doi.org/10.1016/j.foodchem.2012.02.060
Jing, Y., Wen, C. T., Duan, Y. Q., Deng, Q. C., Peng, D. F., Zhang, H. H., & Ma, L. (2021). The composition, extraction, analysis, bioactivities, bioavailability and applications in food system of flaxseed (Linum usitatissimum L.) oil: A review. Trends in Food Science & Technology, 118, 252-260. https://doi.org/10.1016/j.tifs.2021.09.025
Jo, A. R., Han, H. S., Seo, S., Shin, J. S., Lee, J. Y., Kim, H. J., & Lee, K. T. (2017). Inhibitory effect of moschamine isolated from Carthamus tinctorius on LPS-induced inflammatory mediators via AP-1 and STAT1/3 inactivation in RAW 264.7 macrophages. Bioorganic & Medicinal Chemistry Letters, 27, 5245-5251. https://doi.org/10.1016/j.bmcl.2017.10.035
Khalid, N., Khan, R. S., Hussain, M. I., Farooq, M., Ahmad, A., & Ahmed, I. (2017). A comprehensive characterisation of safflower oil for its potential applications as a bioactive food ingredient-A review. Trends in Food Science & Technology, 66, 176-186. https://doi.org/10.1016/j.tifs.2017.06.009
Kim, D. H., Lee, J. H., Ahn, E. M., Lee, Y. H., Baek, N. I., & Kim, I. H. (2006). Phenolic glycosides isolated from safflower (Carthamus tinctorius L.) seeds increase the alkaline phosphatase (ALP) activity of human osteoblast-like cells. Food Science and Biotechnology, 15, 781-785.
Kim, H. J., Bae, Y. C., Park, R. W., Choi, S. W., Cho, S. H., Choi, Y. S., & Lee, W. J. (2002). Bone-protecting effect of safflower seeds in ovariectomized rats. Calcified Tissue International, 71, 88-94. https://doi.org/10.1007/s00223-001-1080-4
Kim, J. M., Lin, C., Stavre, Z., Greenblatt, M. B., & Shim, J.-H. (2020). Osteoblast-osteoclast communication and bone homeostasis. Cells, 9, 2073. https://doi.org/10.3390/cells9092073
Li, C., Luo, X. T., Ji, S. Y., Xie, T. Y., Li, J., Lin, C. S., Li, B. X., Huang, N. G., Yang, F. C., & Liu, Y. (2021). Research on the progress of inflammatory factors in the pathogenesis of osteoporosis. Chinese Journal of Osteoporosis, 27, 1512-1516. https://doi.org/10.3969/j.issn.1006-7108.2021.10.022
Li, L. S., Zhou, J., Xu, Y. P., Huang, Z. S., Zhang, N., Qiu, X. M., & Wang, L. (2021). C-C chemokine receptor type 6 modulates the biological function of osteoblastogenesis by altering the expression levels of Osterix and OPG/RANKL. BioScience Trends, 15, 240-248. https://doi.org/10.5582/bst.2021.01199
Luo, D., Liu, Y. F., Zhou, Y., Chen, Z. W., Yang, L., Liu, Y., Xu, Q. Y., Xu, H., Kuang, H. B., Huang, Q. R., He, M., & Peng, W. J. (2015). Association between dietary phytoestrogen intake and bone mineral density varied with estrogen receptor alpha gene polymorphisms in southern Chinese postmenopausal women. Food and Function, 6, 1977-1983. https://doi.org/10.1039/c5fo00295h
Maira, D. C. D., Leticia, R. P., Costa, L. R. D., Boueri, B. F. D., Carolina, R. P., Pereira, A. D., Ribeiro, D. C., da Silva, E. M., da Costa, C. A. S., & Gilson, T. B. (2018). Flaxseed (Linum usitatissimum) flour contributes to bone health in adult male rats. Nutrition (Burbank, Los Angeles County, Calif.), 49, 48-50. https://doi.org/10.1016/j.nut.2017.11.025
Michalak, B., Filipek, A., Chomicki, P., Pyza, M., Woźniak, M., Żyżyńska-Granica, B., Piwowarski, J. P., Kicel, A., Olszewska, M. A., & Kiss, A. K. (2018). Lignans from Forsythia × Intermedia leaves and flowers attenuate the pro-inflammatory function of leukocytes and their interaction with endothelial cells. Frontiers in Pharmacology, 9, 401. https://doi.org/10.3389/fphar.2018.00401
Mundy, G. R. (2007). Osteoporosis and inflammation. Nutrition Reviews, 65, S147-S151. https://doi.org/10.1301/nr.2007.dec.S147-S151
Peng, C.-H., Lin, W.-Y., Li, C.-Y., Dharini, K. K., Chang, C.-Y., Hong, J.-T., & Lin, M.-D. (2022). Gu Sui Bu (Drynaria fortunei J. Sm.) antagonizes glucocorticoid-induced mineralization reduction in zebrafish larvae by modulating the activity of osteoblasts and osteoclasts. Journal of Ethnopharmacology, 297, 115565. https://doi.org/10.1016/j.jep.2022.115565
Peng, W., Zhang, W. J., & Xue, Y. (2019). Research progress of zebrafish models of bone diseases. Acta Laboratorium Animalis Scientia Sinica, 27, 248-253. https://doi.org/10.3969/j.issn.1005-4847.2019.02.019
Pessanha, C. R., Boueri, B. F. D., da Costa, L. R., Ferreira, M. R., de Abreu, M. D. C., Pessoa, L. R., Pereira, A. D., Ribeiro, D. C., da Silva, E. M., da Costa, C. A. S., & Boaventura, G. T. (2016). Flaxseed flour, compared to flaxseed oil, contributes to femoral structure in male rats subjected to early weaning. Food & Function, 7, 1296-1300. https://doi.org/10.1039/c6fo00021e
Renshaw, S. A., & Trede, N. S. (2012). A model 450 million years in the making: Zebrafish and vertebrate immunity. Disease Models & Mechanisms, 5, 38-47. https://doi.org/10.1242/dmm.007138
Shi, Z. Y., Liang, X. F., Zhao, Y. Q., Liu, W., & Martyniuk, C. J. (2022). Neurotoxic effects of synthetic phenolic antioxidants on dopaminergic, serotoninergic, and GABAergic signaling in larval zebrafish (Danio rerio). Science of the Total Environment, 830, 154688. https://doi.org/10.1016/j.scitotenv.2022.154688
Su, J., Chen, T. R., Liao, D. Y., Wang, Y., Su, Y. C., Liu, S. J., Chen, X. T., Qian, R. F., Jiang, L. L., & Liu, Z. Y. (2022). Novel peptides extracted from Muraenesox cinereus bone promote calcium transport, osteoblast differentiation, and calcium absorption. Journal of Functional Foods, 95, 105157. https://doi.org/10.1016/j.jff.2022.105157
Tauzin, S., Starnes, T. W., Becker, F. B., Lam, P. Y., & Huttenlocher, A. (2014). Redox and Src family kinase signaling control leukocyte wound attraction and neutrophil reverse migration. Journal of Cell Biology, 207, 589-598. https://doi.org/10.1083/jcb.201408090
Tu, Y. B., Yang, Y., Li, Y. F., & He, C. W. (2021). Naturally occurring coumestans from plants, their biological activities and therapeutic effects on human diseases. Pharmacological Research, 169, 105615-105615.
Wang, N., Xu, P. C., Wang, X. P., Yao, W. X., Wang, B. J., Wu, Y. Z., & Shou, D. (2020). Timosaponin AIII attenuates inflammatory injury in AGEs-induced osteoblast and alloxan-induced diabetic osteoporosis zebrafish by modulating the RAGE/MAPK signaling pathways. Phytomedicine, 75, 153247. https://doi.org/10.1016/j.phymed.2020.153247
Wu, Y. Y., Ye, Q. Q., Zhang, L., Cheng, Z. X., Xiao, K. J., Zhu, L., Yin, Y. R., & Dong, H. (2022). Evaluation on antiosteoporosis of collagen peptides prepared by immobilized protease with eggshell membrane. Journal of Food Science, 87, 2391-2404. https://doi.org/10.1111/1750-3841.16172
Yang, J. Y., Kim, G. R., Chae, J. S., Kan, H., Kim, S. S., Hwang, K.-S., Lee, B. H., Yu, S., Moon, S., Park, B., Bae, M. A., & Shin, D.-S. (2019). Antioxidant and anti-inflammatory effects of an ethanol fraction from the Schisandra chinensis baillon hot water extract fermented using Lactobacilius paracasei subsp. tolerans. Food Science and Biotechnology, 28, 1759-1767. https://doi.org/10.1007/s10068-019-00626-4
Yu, H. L., Chen, Y. X., & Zhu, J. J. (2022). Osteogenic activities of four calcium-chelating microalgae peptides. Journal of the Science of Food and Agriculture, 102, 6643-6649. https://doi.org/10.1002/jsfa.12031
Yue, H., Bo, Y. Y., Tian, Y. Y., Mao, L., Xue, C. H., Dong, P., & Wang, J. F. (2022). Docosahexaenoic acid-enriched phosphatidylcholine exerted superior effects to triglyceride in ameliorating obesity-induced osteoporosis through up-regulating the Wnt/β-catenin pathway. Journal of Agricultural & Food Chemistry, 70, 13904-13912. https://doi.org/10.1021/acs.jafc.2c06081
Zhang, H. L., Nagatsu, A., Watanabe, T., Sakakibara, J., & Okuyama, H. (1997). Antioxidative compounds isolated from safflower (Carthamus tinctorius L.) oil cake. Chemical & Pharmaceutical Bulletin, 45, 1910-1914.
Zhuang, C.-C., Feng, X., Xu, H.-Y., Zhang, L., Liu, L., Zhang, G., Zheng, Z., & Ma, C.-M. (2021). Technical note: Quantification of lignans in the urine, milk, and plasma of flaxseed cake-fed dairy sheep. Journal of Dairy Science, 104, 391-396. https://doi.org/10.3168/jds.2020-18470

Auteurs

Xin-Yue Yang (XY)

School of Life Sciences, Inner Mongolia University, Hohhot, P. R. China.

Dan-Dan Wu (DD)

School of Life Sciences, Inner Mongolia University, Hohhot, P. R. China.

Cong-Cong Zhuang (CC)

School of Life Sciences, Inner Mongolia University, Hohhot, P. R. China.

Chao-Mei Ma (CM)

School of Life Sciences, Inner Mongolia University, Hohhot, P. R. China.

Classifications MeSH