AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Food Science and Human Wellness Article
PDF (2.3 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Nystose attenuates bone loss and promotes BMSCs differentiation to osteoblasts through BMP and Wnt/β-catenin pathway in ovariectomized mice

Qi Zhanga, Sijing Hua, Jianjun Wua, Peng Suna, Quanlong Zhanga, Yang Wangb, Qiming Zhaoa, Ting Hanc( ), Luping Qina,c ( ), Qiaoyan Zhanga,c( )
School of Pharmaceutical Sciences, Zhejiang Chinese Medical University, Hangzhou 310053, China
Zhejiang Traditional Chinese Medicine & Health Industry Group Co., Ltd. Hangzhou 310016, China
School of Pharmacy, Second Military Medical University, Shanghai 200433, China

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

Show Author Information

Abstract

Increasing the osteogenic differentiation ability and decreasing the adipogenic differentiation ability of bone marrow mesenchymal stem cells (BMSCs) is a potential strategy for the treatment of osteoporosis (OP). Naturally derived oligosaccharides have shown significant anti-osteoporotic effects. Nystose (NST), an oligosaccharide, was isolated from the roots of Morinda officinalis How. (MO). The aim of the present study was to investigate the effects of NST on bone loss in ovariectomized mice, and explore the underlying mechanism of NST in promoting differentiation of BMSCs to osteoblasts. Administration of NST (40, 80 and 160 mg/kg) and the positive control of estradiol valerate (0.2 mg/kg) for 8 weeks significantly prevented bone loss induced by ovariectomy (OVX), increased the bone mass density (BMD), improved the bone microarchitecture and reduced urine calcium and deoxypyridinoline (DPD) in ovariectomized mice, while inhibited the increase of body weight without significantly affecting the uterus weight. Furthermore, we found that NST increased osteogenic differentiation, inhibited adipogenic differentiation of BMSCs in vitro, and upregulated the expression of the key proteins of BMP and Wnt/β-catenin pathways. In addition, Noggin and Dickkopf-related protein-1 (DKK-1) reversed the effect of NST on osteogenic differentiation and expression of the key proteins in BMP and Wnt/β-catenin pathway. The luciferase activities and the molecular docking analysis further supported the mechanism of NST. In conclusion, these results indicating that NST can be clinically used as a potential alternative medicine for the prevention and treatment of postmenopausal osteoporosis.

Keywords

NystoseBone marrow mesenchymal stem cellOsteoblastAdipocyteBMP pathwayWnt/β-catenin pathway

References

[1]

M.H. Kim, H. Lee, I.J. Ha, et al., Zanthoxylum piperitum alleviates the bone loss in osteoporosis via inhibition of RANKL-induced c-fos/NFATc1/NF-κB pathway, Phytomedicine. 80 (2021) 153397. https://doi.org/10.1016/j.phymed.2020.153397.
Crossref Google Scholar
[2]

Y. Ukon, T. Makino, J. Kodama, et al., Molecular-based treatment strategies for osteoporosis: a literature review, Int. J. Mol. Sci. 20 (2019) 2557. https://doi.org/10.3390/ijms20102557.
Crossref Google Scholar
[3]

S. Chai, L. Wan, J.L. Wang, et al., Gushukang inhibits osteocyte apoptosis and enhances BMP-2/Smads signaling pathway in ovariectomized rats, Phytomedicine. 64 (2019) 153063. https://doi.org/10.1016/j.phymed.2019.153063.
Crossref Google Scholar
[4]

H. Zheng, B. He, T. Wu, et al., Extraction, purification and anti-osteoporotic activity of a polysaccharide from Epimedium brevicornum Maxim. in vitro, Int J Biol Macromol. 156 (2020) 1135-1145. https://doi.org/10.1016/j.ijbiomac.2019.11.145.
Crossref Google Scholar
[5]

I. Macías, N. Alcorta-Sevillano, C.I. Rodríguez, et al., Osteoporosis and the potential of cell-based therapeutic strategies, Int. J. Mol. Sci. 21 (2020) 1653. https://doi.org/10.3390/ijms21051653.
Crossref Google Scholar
[6]

F. Karadeniz, J.H. Oh, J.I. Lee, et al., 3,5-Dicaffeoylepi-quinic acid from Atriplex gmelinii enhances the osteoblast differentiation of bone marrow-derived human mesenchymal stromal cells via Wnt/BMP signaling and suppresses adipocyte differentiation via AMPK activation, Phytomedicine. 71 (2020) 153225. https://doi.org/10.1016/j.phymed.2020.153225.
Crossref Google Scholar
[7]

J.H. Hong, E.S. Hwang, M.T. McManus, et al., TAZ, a transcriptional modulator of mesenchymal stem cell differentiation, Science 309 (2005) 1074-1078. https://doi.org/10.1126/science.1110955.
Crossref Google Scholar
[8]

N. Kamiya, Y. Mishina, New insights on the roles of BMP signaling in bone: A review of recent mouse genetic studies, Biofactors. 37 (2011) 75-82. https://doi.org/10.1002/biof.139.
Crossref Google Scholar
[9]

S. Manandhar, S.P. Kabekkodu, K. Pai, Aberrant canonical Wnt signaling: phytochemical based modulation, Phytomedicine. 76 (2020) 153243. https://doi.org/10.1016/j.phymed.2020.153243.
Crossref Google Scholar
[10]

P.Y. Chen, J.S. Sun, Y.H. Tsuang, et al., Simvastatin promotes osteoblast viability and differentiation via Ras/Smad/Erk/BMP-2 signaling pathway, Nutr. Res. 30 (2010) 191-199. https://doi.org/10.1016/j.nutres.2010.03.004.
Crossref Google Scholar
[11]

R. Apolinar-Valiente, P. Williams, T. Doco, Recent advances in the knowledge of wine oligosaccharides, Food Chem. 342 (2021) 128330. https://doi.org/10.1016/j.foodchem.2020.128330.
Crossref Google Scholar
[12]

J. Zhao, S. Wang, J. Bao, et al., Trehalose maintains bioactivity and promotes sustained release of BMP-2 from lyophilized CDHA scaffolds for enhanced osteogenesis in vitro and in vivo, PLoS ONE 8 (2013) e54645. https://doi.org/10.1371/journal.pone.0054645.
Crossref Google Scholar
[13]

G.J. Hong, L. Zhou, X.G. Shi, et al., Bajijiasu abrogates osteoclast differentiation via the suppression of RANKL signaling pathways through NF-κB and NFAT, Int J Mol Sci. 18 (2017) 203. https://doi.org/10.3390/ijms18010203.
Crossref Google Scholar
[14]

L. Wang, H.Y. Wang, N.Y. Fang, Algal oligosaccharides ameliorate osteoporosis via up-regulation of parathyroid hormone 1-84 and vascular endothelial growth factor, J Tradit Chin Med. 36 (2016) 332-339. https://doi.org/10.1016/S0254-6272(16)30046-2.
Crossref Google Scholar
[15]

C.Y. Yan, S.J. Zhang, C.S. Wang, et al., A fructooligosaccharide from Achyranthes bidentata inhibits osteoporosis by stimulating bone formation, Carbohydr Polym. 210 (2019) 110-118. https://doi.org/10.1016/j.carbpol.2019.01.026.
Crossref Google Scholar
[16]

T. Yodthong, U. Kedjarune-Leggat, C. Smythe, et al., Enhancing Activity of Pleurotus sajor-caju (Fr.) Sing β-1,3-Glucanoligosaccharide (Ps-GOS) on Proliferation, Differentiation, and Mineralization of MC3T3-E1 Cells through the involvement of BMP-2/Runx2/MAPK/Wnt/β-catenin signaling pathway, Biomolecules 10 (2020) 190. https://doi.org/10.3390/biom10020190.
Crossref Google Scholar
[17]

K. Tanabe, S. Nakamura, M. Moriyama-Hashiguchi, et al., Dietary fructooligosaccharide and glucomannan alter gut microbiota and improve bone metabolism in senescence-accelerated mouse, J Agric Food Chem. 67 (2019) 867-874. https://doi.org/10.1021/acs.jafc.8b05164.
Crossref Google Scholar
[18]

J.H. Zhang, H.L. Xin, Y.M. Xu, et al., Morinda officinalis How. - A comprehensive review of traditional uses, phytochemistry and pharmacology, J. Ethnopharmacol. 213 (2018) 230-255. https://doi.org/10.1016/j.jep.2017.10.028.
Crossref Google Scholar
[19]

X. Sun, B. Wei, Z.H. Peng, et al., A polysaccharide from the dried rhizome of Drynaria fortunei (Kunze) J. Sm. prevents ovariectomized (OVX)-induced osteoporosis in rats, J Cell Mol Med. 24 (2020) 3692-3700. https://doi.org/10.1111/jcmm.15072.
Crossref Google Scholar
[20]
National Pharmacopoeia Committee, Pharmacopoeia of the People’s Republic of China. Chin. Med. Sci. Tech. Press. Beijing, 2020.
[21]

L.L.C. Schrödinger, The PyMOL Molecular Graphics System, version 1.2r3pre, Schrödinger, LLC: New York, NY, USA. 2017.
[22]

H. Okada, E. Fukushi, A. Yamamori, et al., Novel fructopyranose oligosaccharides isolated from fermented beverage of plant extract, Carbohydr. Res. 345 (2010) 414-418. https://doi.org/10.1016/j.carres.2009.12.003.
Crossref Google Scholar
[23]

J. Liu, A.L. Waterhouse, N.J. Chatterton, Proton and carbon NMR chemical-shift assignments for [β-D-Fruf-(2 → 1)]3-(2 ↔ 1)-α-D-Glcp (nystose) and [β-D-Fruf-(2 → 1)]4-(2 ↔ 1)-α-D-Glcp (1,1,1-kestopentaose) from two-dimensional NMR spectral measurements, Carbohydr. Res. 245 (1993) 11-19. https://doi.org/10.1016/0008-6215(93)80056-k.
Crossref Google Scholar
[24]

L. Ruiz-Aceituno, M.L. Sanz, B. de Las Rivas, et al., Enzymatic synthesis and structural characterization of theanderose through transfructosylation reaction catalyzed by levansucrase from bacillus subtilis CECT 39, J Agric Food Chem. 65 (2017) 10505-10513. https://doi.org/10.1021/acs.jafc.7b03092.
Crossref Google Scholar
[25]

A.C. Apolinário, E.M.D. Carvalho, B.P.G.D.L. Damasceno, et al., Extraction, isolation and characterization of inulin from Agave sisalana boles, Ind Crops Prod. 108 (2017) 355-362. https://doi.org/10.1016/j.indcrop.2017.06.045.
Crossref Google Scholar
[26]

J.W. Timmermans, P.D. Waard, H. Tournois, Leeflang, et al., NMR spectroscopy of nystose, Carbohydr Res. 243 (1993) 379-384. https://doi.org/10.1016/0008-6215(93)87041-p.
Crossref Google Scholar
[27]

H.D. Wang, Z. Chen, I. Inoue, et al., Effects of electroacupuncture at GB points on markers of osteoporosis and bodyweight in ovariectomized rats, Acupunct Med. 33 (2015) 465-471. https://doi.org/10.1136/acupmed-2014-010743.
Crossref Google Scholar
[28]

H. Li, J. Qu, H.H. Zhu, et al., CGRP regulates the age-related switch between osteoblast and adipocyte differentiation, Front Cell Dev Biol. 26 (2021) 675503. https://doi.org/10.3389/fcell.2021.675503.
Crossref Google Scholar
[29]

E. Abe, M. Yamamoto, Y. Taguchi, et al., Essential requirement of BMPs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by noggin, J Bone Miner Res. 15 (2000) 663-673. https://doi.org/10.1359/jbmr.2000.15.4.663.
Crossref Google Scholar
[30]

M. Chen, H. Han, S.Q. Zhou, et al., Morusin induces osteogenic differentiation of bone marrow mesenchymal stem cells by canonical Wnt/β-catenin pathway and prevents bone loss in an ovariectomized rat model, Stem Cell Res Ther. 12 (2021) 173. https://doi.org/10.1186/s13287-021-02239-3.
Crossref Google Scholar
[31]

Schrödinger. Maestro, version 11.0, Schrödinger LLC: New York, NY, USA, 2017.
[32]

F. Stauffer, S.W. Cowan-Jacob, C. Scheufler, et al., Identification of a 5-[3-phenyl-(2-cyclic-ether)-methylether]-4-aminopyrrolo [2,3-d] pyrimidine series of IGF-1R inhibitors, Bioorg Med. Chem. Lett. 26 (2016) 2065-2067. https://doi.org/10.1016/j.bmcl.2016.02.074.
Crossref Google Scholar
[33]

S.P. Singh, J.S. Jadaun, L.K. Narnoliya, et al., Prebiotic oligosaccharides: special focus on fructooligosaccharides, its biosynthesis and bioactivity, Appl. Biochem. Biotech. 183 (2017) 613-635. https://doi.org/10.1007/s12010-017-2605-2.
Crossref Google Scholar
[34]

V. Bali, P.S. Panesar, M.B. Bera, et al., Fructo-oligosaccharides: production, purification and potential applications, Crit. Rev. Food Sci. 55 (2015) 1475-1490. https://doi.org/10.1080/10408398.2012.694084.
Crossref Google Scholar
[35]

L. Mira-Pascual, C. Patlaka, S. Desai, et al., A novel sandwich ELISA for tartrate-resistant acid phosphatase 5a and 5b protein reveals that both isoforms are secreted by differentiating osteoclasts and correlate to the type Ⅰ collagen degradation marker CTX-I in vivo and in vitro, Calcified Tissue In. 106 (2020) 194-207. https://doi.org/10.1007/s00223-019-00618-w.
Crossref Google Scholar
[36]

C. Niramitchainon, S. Mongkornkarn, C. Sritara, et al., Trabecular bone score, a new bone quality index, is associated with severe periodontitis, J Periodontol. 91 (2020) 1264-1273. https://doi.org/10.1002/JPER.19-0580.
Crossref Google Scholar
[37]

D. Kim, M. Thangavelu, S. Cheolui, et al., Effect of different concentration of demineralized bone powder with gellan gum porous scaffold for the application of bone tissue regeneration, Int. J. Biol. Macromol. 134 (2019) 749-758. https://doi.org/10.1016/j.ijbiomac.2019.04.184.
Crossref Google Scholar
[38]

L.F. Hu, C. Yin, F. Zhao, et al., Mesenchymal stem cells: cell fate decision to osteoblast or adipocyte and application in osteoporosis treatment, Int. J. Mol. Sci. 19 (2018) 360. https://doi.org/10.3390/ijms19020360.
Crossref Google Scholar
[39]

C. Yan, D. Huang, X. Shen, et al., Identification and characterization of a polysaccharide from the roots of Morinda officinalis, as an inducer of bone formation by up-regulation of target gene expression, Int. J. Biol. Macromol. 133 (2019) 446-456. https://doi.org/10.1016/j.ijbiomac.2019.04.084.
Crossref Google Scholar
[40]

B.M. Abdallah, E.M. Ali, 5'-Hydroxy Auraptene stimulates osteoblast differentiation of bone marrow-derived mesenchymal stem cells via a BMP-dependent mechanism, J. Biomed. Sci. 26 (2019) 51. https://doi.org/10.1186/s12929-019-0544-7.
Crossref Google Scholar
[41]

A.X. Yu, M.L. Xu, P. Yao, et al., Corylin, a flavonoid derived from Psoralea Fructus, induces osteoblastic differentiation via estrogen and Wnt/β-catenin signaling pathways, FASEB J. 34 (2020) 4311-4328. https://doi.org/10.1096/fj.201902319RRR.
Crossref Google Scholar
[42]

T. Zhou, Y. Yan, C. Zhao, et al., Resveratrol improves osteogenic differentiation of senescent bone mesenchymal stem cells through inhibiting endogenous reactive oxygen species production via AMPK activation, Redox. Rep. 24 (2019) 62-69. https://doi.org/10.1080/13510002.2019.1658376.
Crossref Google Scholar
[43]

J.W. Seok, D. Kim, B.K. Yoon, et al., Dexras1 plays a pivotal role in maintaining the equilibrium between adipogenesis and osteogenesis, Metabolism. 108 (2020) 154250. https://doi.org/10.1016/j.metabol.2020.154250.
Crossref Google Scholar
[44]

S. Parida, S. Siddharth, D. Sharma, Adiponectin, obesity, and cancer: clash of the bigwigs in health and disease, Int. J. Mol. Sci. 20 (2019) 2519. https://doi.org/10.3390/ijms20102519.
Crossref Google Scholar
[45]

A. Qadir, S. Liang, Z. Wu, et al., Senile osteoporosis: the involvement of differentiation and senescence of bone marrow stromal cells, Int. J. Mol.Sci. 21 (2020) 349. https://doi.org/10.3390/ijms21010349.
Crossref Google Scholar
[46]

X. Yang, D.L. Chen, J. Yang, et al., Effects of oligosaccharides from Morinda officinalis on gut microbiota and metabolome of APP/PS1 transgenic mice, Front Neurol. 9 (2018) 412. https://doi.org/10.3389/fneur.2018.00412.
Crossref Google Scholar
[47]

X. Yang, D.L. Chen, J. Yang, et al., Isolation and quantitative determination of inulin-type oligosaccharides in roots of Morinda officinalis, Carbohydr. Polym. 83 (2011) 1997-2004. https://doi.org/10.1016/j.carbpol.2019.03.016.
Crossref Google Scholar
[48]

X.X. Cha, S.N. Han, J. Yu, et al., Inulin with a low degree of polymerization protects human umbilical vein endothelial cells from hypoxia/reoxygenation-induced injury, Carbohydr. Polym. 216 (2019) 97-106. https://doi.org/10.1016/j.carbpol.2019.03.016.
Crossref Google Scholar
[49]

L. Chi, I. Khan, Z. Lin, et al., Fructo-oligosaccharides from Morinda officinalis remodeled gut microbiota and alleviated depression features in a stress rat model, Phytomedicine 67 (2020) 153157. https://doi.org/10.1016/j.phymed.2019.153157.
Crossref Google Scholar
Food Science and Human Wellness
Volume 12 Issue 2,
March 2023
Pages 634-646
DOI: 10.1016/j.fshw.2022.07.066
Cite this article:
Zhang Q, Hu S, Wu J, et al. Nystose attenuates bone loss and promotes BMSCs differentiation to osteoblasts through BMP and Wnt/β-catenin pathway in ovariectomized mice. Food Science and Human Wellness, 2023, 12(2): 634-646. https://doi.org/10.1016/j.fshw.2022.07.066

797

Views

56

Downloads

5

Crossref

5

Web of Science

5

Scopus

0

CSCD

Altmetrics
Received: 11 July 2021
Revised: 06 August 2021
Accepted: 28 September 2021
Published: 07 September 2022
© 2023 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

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