Skip to main content
SpringerLink
Log in

Sialoglycoprotein from Gadous morhua eggs improve high bone turnover activity via down-regulating BMP-2/Smads and Wnt/β-catenin signal pathways

  • Published:
Food Science and Biotechnology Aims and scope Submit manuscript

Abstract

The effect of sialoglycoprotein isolated from Gadous morhua eggs (Gm-SGP) on ovariectomized (OVX) induced osteoporosis, which is characterized by high bone turnover activity was investigated. Results revealed that Gm-SGP significantly increased bone mineral density, enhanced bone biomechanical properties and repaired the microstructure of the trabecular bone. Also, the treatment with Gm-SGP remarkably decreased biochemical marker contents or activities, such as serum BALP, PICP, BMP-2, TrACP, Cath-K, urine Ca and P, leading to the reduction in bone turnover. The elevation in the rate of bone formative process contributed in the increase of bone turnover. Both BMP-2/Smads and Wnt/β-catenin signaling pathways played an important role in osteogenesis. Gm-SGP suppressed the key factors expression in these two pathways such as BMP-2, Smad1, Smad4, Lrp-5b, Runx2, Osx, ALP, Col1, OCN and β-catenin. These findings might provide some theoretical basis for the application of Gm-SGP as a potential anti-osteoporotic drug or as functional food.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • An J, Yang H, Zhang Q, Liu C, Zhao J, Zhang L, Chen B. Natural products for treatment of osteoporosis: the effects and mechanisms on promoting osteoblast-mediated bone formation. Life Sci. 147: 46–58 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Babij P, Zhao WG, Small C, Kharode Y, Yaworsky PJ, Bouxsein ML, Reddy PS, Bodine PVN, Robinson JA, Bhat B, Marzolf J, Moran RA, Bex F. High bone mass in mice expressing a mutant LRP5 gene. J. Bone Miner. Res. 18: 960–974 (2003)

    Article  CAS  PubMed  Google Scholar 

  • Baron R, Rawadi G. Minireview: targeting the Wnt/beta-catenin pathway to regulate bone formation in the adult skeleton. Endocrinology. 148: 2635–2643 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Brewer L, Williams D, Moore A. Current and future treatment options in osteoporosis. Eur. J. Clin. Pharmacol. 67: 321–331 (2011)

    Article  CAS  PubMed  Google Scholar 

  • Cao PC, Xiao WX, Yan YB, Zhao X, Liu S, Feng J, Zhang W, Wang J, Feng YF, Lei W. Preventive effect of crocin on osteoporosis in an ovariectomized rat model. Evid. Based Complement. Altern. Med. 2014: 825181 (2014)

    Google Scholar 

  • Chung SL, Leung KS, Cheung WH. Low-magnitude high-frequency vibration enhances gene expression related to callus formation, mineralization and remodeling during osteoporotic fracture healing in rats. J. Orthop. Res. 32: 1572–1579 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Day TF, Guo X, Garrett-Beal L, Yang Y. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell. 8: 739–750 (2005)

    Article  CAS  PubMed  Google Scholar 

  • Genant HK, Engelke K, Bolognese MA, Mautalen C, Brown JP, Recknor C, Goemaere S, Fuerst T, Yang YC, Grauer A, Libanati C. Effects of romosozumab compared with teriparatide on bone density and mass at the spine and hip in postmenopausal women with low bone mass. J. Bone Miner. Res. 32: 181–187 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Gerstenfeld LC, Uporova T, Schmidt J, Strauss PG, Shih SD, Huang LF, Gundberg C, Mizuno S, Glowacki J. Osteogenic potential of murine osteosarcoma cells: comparison of bone-specific gene expression in in vitro and in vivo conditions. Lab. Investig. 74: 895–906 (1996)

    CAS  PubMed  Google Scholar 

  • Herrero S, Pico Y. Treatments for post-menopausal osteoporotic women, What’s new? How can we manage long-term treatment? Eur. J. Pharmacol. 779: 8–21 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Hu HL, Hilton MJ, Tu XL, Yu K, Ornitz DM, Long F. Sequential roles of hedgehog and Wnt signaling in osteoblast development. Development. 132: 49–60 (2005)

    Article  CAS  PubMed  Google Scholar 

  • Hu SW, Xia GH, Wang JF, Wang YM, Li ZJ, Xue CH. Fucoidan from sea cucumber protects against high-fat high-sucrose diet-induced hyperglycaemia and insulin resistance in mice. J. Funct. Foods. 10: 128–138 (2014)

    Article  CAS  Google Scholar 

  • Inoue S, Inoue Y. Fish glycoproteins. New Compr. Biochem. 29: 143–161 (1997)

    Article  Google Scholar 

  • Jian J, Sun L, Cheng X, Hu X, Liang J, Chen Y. Calycosin-7-O-beta-d-glucopyranoside stimulates osteoblast differentiation through regulating the BMP/WNT signaling pathways. Acta Pharm. Sin. B. 5: 454–60 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Kato M, Patel MS, Levasseur R, Lobov I, Chang BHJ, Glass DA, Hartmann C, Li L, Hwang TH, Brayton CF, Lang RA, Karsenty G, Chan L. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J. Cell Biol. 157: 303–314 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keen RW. Burden of osteoporosis and fractures. Curr. Osteoporos Rep. 1: 66–70 (2003)

    Article  PubMed  Google Scholar 

  • Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 89: 755–764 (1997)

    Article  CAS  PubMed  Google Scholar 

  • Leboime A, Confavreux CB, Mehsen N, Paccou J, David C, Roux C. Osteoporosis and mortality. Joint Bone Spine. 77: S107-12 (2010)

    Article  PubMed  Google Scholar 

  • Lian JB, Stein GS, Javed A, van Wijnen AJ, Stein JL, Montecino M, Hassan MQ, Gaur T, Lengner CJ, Young DW. Networks and hubs for the transcriptional control of osteoblastogenesis. Rev. Endocr. Metab. Disord. 7: 1–16 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Liu JP, Xia Y. Chinese herbal medicines for treating osteoporosis. Cochrane Database Syst. Rev. CD005467 (2014)

  • Ma J, Granton PV, Holdsworth DW, Turley EA. Oral administration of hyaluronan reduces bone turnover in ovariectomized rats. J. Agric. Food Chem. 61: 339–345 (2013)

    Article  CAS  PubMed  Google Scholar 

  • Ma YL, Liao EY, Dai RC, Sheng ZF. Longitudinal changes of bone microstructure and biomechanical properties of vertebral trabeculae in OVX rats. Chin. J. Osteoporos. Bone Miner. Res. 43: S99–S100 (2009)

    Google Scholar 

  • Nakashima K, Zhou X, Kunkel G, Zhang ZP, Deng JM, Behringer RR, de Crombrugghe B. The novel zinc finger-containing transcription factor Osterix is required for osteoblast differentiation and bone formation. Cell. 108: 17–29 (2002)

    Article  CAS  PubMed  Google Scholar 

  • Pacifici R. Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J. Bone Miner. Res. 11: 1043–1051 (1996)

    Article  CAS  PubMed  Google Scholar 

  • Riggs BL, Khosla S, Melton LJ, 3rd. Sex steroids and the construction and conservation of the adult skeleton. Endocr. Rev. 23: 279–302 (2002)

    Article  CAS  PubMed  Google Scholar 

  • Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J. writing group for the women’s health initiative I. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the women’s health initiative randomized controlled trial. JAMA. 288: 321–333 (2002)

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Wang Y, Zhao Y, Zhan Q, Yu P, Wang J, Xue C. Sialoglycoprotein isolated from eggs of Carassius auratus ameliorates osteoporosis: an effect associated with regulation of the Wnt/beta-catenin pathway in rodents. J. Agric. Food Chem. 64: 2875–2882 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Xue CH, Li ZJ, Xu J. Phosphatidylcholine levels and their fatty acid compositions in squid egg: a comparison study with pollack roe and sturgeon caviar. J. Food Lipids. 15: 222–230 (2008)

    Article  CAS  Google Scholar 

  • Wirries A, Schubert AK, Zimmermann R, Jabari S, Ruchholtz S, El-Najjar N. Thymoquinone accelerates osteoblast differentiation and activates bone morphogenetic protein-2 and ERK pathway. Int. Immunopharmacol. 15: 381–386 (2013)

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Adeeb S, Doschak MR. Using micro-CT derived bone microarchitecture to analyze bone stiffness—a case study on osteoporosis rat bone. Front. Endocrinol. 6: 80 (2015)

    Article  Google Scholar 

  • Xia G, Wang J, Sun S, Zhao Y, Wang Y, Yu Z, Wang S, Xue C. Sialoglycoproteins prepared from the eggs of Carassius auratus prevent bone loss by inhibiting the NF-kappaB pathway in ovariectomized rats. Food Funct. 7: 704–712 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Xia G, Zhao Y, Yu Z, Tian Y, Wang Y, Wang S, Wang J, Xue C. Phosphorylated peptides from antarctic krill (Euphausia superba) prevent estrogen deficiency induced osteoporosis by inhibiting bone resorption in ovariectomized rats. J. Agric. Food Chem. 63: 9550–9557 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Huo H, Xiu CY, Song M, Han YF, Li YF, Zhu YZ. Inhibition of osteoblast differentiation by aluminum trichloride exposure is associated with inhibition of BMP-2/Smad pathway component expression. Food Chem. Toxicol. 97: 120–126 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Zhan Q, Gui X, Wang F, Yu P, Zhao M, Wang J, Xue C. Sialoglycoprotein isolated from the eggs of Gadus morhua enhances fracture healing in osteoporotic mice. Food Funct. 8: 1094–1104 (2017)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by National Natural Science Foundation of China (No. 31371876) and National Primary Research & Developement Plan. (No. 2017YFF0207805).

Author information

Authors and Affiliations

  1. College of Food Science and Engineering, Ocean University of China, Qingdao, 266003, Shandong Province, China

    Kai Wang, Lihua Han, Na Wang, Yiming Wang & Jingfeng Wang

Authors
  1. Kai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lihua Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Na Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yiming Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jingfeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jingfeng Wang.

Ethics declarations

Conflict interests

The authors declare no competing financial interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, K., Han, L., Wang, N. et al. Sialoglycoprotein from Gadous morhua eggs improve high bone turnover activity via down-regulating BMP-2/Smads and Wnt/β-catenin signal pathways. Food Sci Biotechnol 27, 1455–1465 (2018). https://doi.org/10.1007/s10068-018-0379-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-018-0379-0

Keywords

Search

Navigation