Skip to main content
SpringerLink
Log in

The preparation of a cold-water soluble polysaccharide from Grifola frondosa and its inhibitory effects on MKN-45 cells

  • Original Article
  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

In this study, a novel water soluble polysaccharide (named GFP-4) was extracted from Grifola frondosa at 4 oC, and its preliminary structure and inhibitory effects on human gastric carcinoma MKN-45 cells through the Fas/FasL death receptor apoptosis pathway were investigated. High-performance gel permeation chromatography (HPGPC), fourier-transform infrared spectroscopy (FT-IR), and ion chromatography (IC) results showed that GFP-4 was a 1.09 × 106 Da neutral hetero polysaccharide with pyranose rings, and α- and β-type glycosidic linkages that contained galactose, glucose, and mannose at a molar ratio of 1.00:3.45:1.19. MTT results indicated that GFP-4 significantly inhibited the proliferation of MKN-45 cells in a concentration-dependent manner. The H&E staining and Hoechst 33342/PI double staining results showed that GFP-4-treated MKN-45 cells were subjected to underwent typical apoptotic morphologic changes such as nuclear pyknosis, chromatin condensation, and an increase of membrane permeability. Annexin V-FITC/PI double staining, cell cycle analysis, and western blot results revealed the GFP-4 induced MKN-45 cells apoptosis through the Fas/FasL-mediated death receptor pathway with cells arrested at the G0/G1 phase. These data indicate that GFP-4 is a promising candidate for treating gastric cancer and provide a theoretical basis for the future development and utilization of G. frondosa clinically.

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

  1. Sun, Q., Lu, N.N., Feng, L.: Apigetrin inhibits gastric cancer progression through inducing apoptosis and regulating ROS-modulated STAT3/JAK2 pathway. Biochem. Biophys. Res. Commun. 498:164–170 (2018)

    CAS  PubMed  Google Scholar 

  2. Wenjun, X., Zhenxuan, D., Yuxin, T., Zhenwei, D., Mingsong, L.: Downregulation of KMT2D suppresses proliferation and induces apoptosis of gastric cancer. Biochem. Biophys. Res. Commun. S0006291 × 18318370 (2018)

  3. Zhou, Q., Wu, X., Wen, C., Wang, H., Wang, H., Liu, H., Peng, J.: Toosendanin induces caspase-dependent apoptosis through the p38 MAPK pathway in human gastric cancer cells. Biochem. Biophys. Res. Commun. 505, 261–266 (2018)

    CAS  PubMed  Google Scholar 

  4. Strong, V.E., Ai-Wen, W., Selby, L.V., Mithat, G., Meier, H., Kyo Young, S., Cho Hyun, P., Coit, D.G., Jia-Fu, J., Brennan, M.F.: Differences in gastric cancer survival between the U.S. and China. J. Surg. Oncol. 112, 31–37 (2015)

  5. Dong, J., Zheng, N., Wang, X., Tang, C., Yan, P., Zhou, H.B., Huang, J.: A novel HDAC6 inhibitor exerts an anti-cancer effect by triggering cell cycle arrest and apoptosis in gastric cancer. Eur. J. Pharmacol. 828, 67 (2018)

    CAS  PubMed  Google Scholar 

  6. Yu, J., Ji, H., Dong, X., Feng, Y., Liu, A.: Apoptosis of human gastric carcinoma MGC-803 cells induced by a novel Astragalus membranaceus polysaccharide via intrinsic mitochondrial pathways. Int. J. Biol. Macromol. 126, 811–819 (2019)

    CAS  PubMed  Google Scholar 

  7. Kang, B., Sun, X.H.: Regulation of cancer stem cells by RING finger ubiquitin ligases. Stem Cell Investig. 1, 5 (2014)

  8. Zheng, G.Q., Ji, H.Y., Zhang, S.J., Yu, J., Liu, A.J.: Selenious-β-lactoglobulin induces the apoptosis of human lung cancer A549 cells via an intrinsic mitochondrial pathway. Cytotechnology 70, 1551–1563 (2018)

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Carles, G.: Caspase-8 activation independent of CD95/CD95-L interaction during paclitaxel-induced apoptosis in human colon cancer cells (HT29-D4). Biochem. Pharmacol. 60, 1579–1584 (2000)

    PubMed  Google Scholar 

  10. Han, F., Jin, F., Li, Y., Li, Z., Liu, Z., Luo, Y.: Seawater induces apoptosis in alveolar epithelial cells via the Fas/FasL-mediated pathway. Respir. Physiol. Neuro. 182, 71–80 (2012)

    CAS  Google Scholar 

  11. He, X., Wu, J., Yuan, L., Lin, F., Yi, J., Li, J., Yuan, H., Shi, J., Yuan, T., Zhang, S.: Lead induces apoptosis in mouse TM3 Leydig cells through the Fas/FasL death receptor pathway. Environ. Toxicol. Pharmacol. 56, 99–105 (2017)

    CAS  PubMed  Google Scholar 

  12. Yajima, T., Hoshino, K., Muranushi, R., Mogi, A., Onozato, R., Yamaki, E., Kosaka, T., Tanaka, S., Shirabe, K., Yoshikai, Y., Kuwano, H.: Fas/FasL signaling is critical for the survival of exhausted antigen-specific CD8 + T cells during tumor immune response. Mol. Immunol. 107, 97–105 (2019)

    CAS  PubMed  Google Scholar 

  13. Wang, D., Chen, P., Chen, L., Zeng, F., Zang, R., Liu, H., Lu, C.: Betulinic acid protects the neuronal damage in new born rats from isoflurane-induced apoptosis in the developing brain by blocking FASL-FAS signaling pathway. Biomed. Pharmacother. 95, 1631–1635 (2017)

    CAS  PubMed  Google Scholar 

  14. Shih, I.L., Chou, B.W., Chen, C.C., Wu, J.Y., Hsieh, C.: Study of mycelial growth and bioactive polysaccharide production in batch and fed-batch culture of Grifola frondosa. Bioresour. Technol. 99, 785–793 (2008)

    CAS  PubMed  Google Scholar 

  15. Cui, F.J., Li, Y., Xu, Y.Y., Liu, Z.Q., Huang, D.M., Zhang, Z.C., Tao, W.Y.: Induction of apoptosis in SGC-7901 cells by polysaccharide-peptide GFPS1b from the cultured mycelia of Grifola frondosa GF9801. Toxicol. Vitro 21, 417–427 (2007)

    CAS  Google Scholar 

  16. Ji, H.Y., Yu, J., Chen, X.Y., Liu, A.J.: Extraction, optimization and bioactivities of alcohol-soluble polysaccharide from Grifola frondosa. J. Food Meas. Charact. 13, 1645–1651 (2019)

    Google Scholar 

  17. Mao, G., Zou, Y., Feng, W., Wang, W., Zhao, T., Ye, C., Zhu, Y., Wu, X., Yang, L., Wu, X.: Extraction, preliminary characterization and antioxidant activity of Se-enriched Maitake polysaccharide. Carbohydr. Polym. 101, 213–219 (2014)

    CAS  PubMed  Google Scholar 

  18. Mao, G.H., Ren, Y., Feng, W.W., Li, Q., Wu, H.Y., Jin, D., Zhao, T., Xu, C.Q., Yang, L.Q., Wu, X.Y.: Antitumor and immunomodulatory activity of a water-soluble polysaccharide from Grifola frondosa. Carbohydr. Polym. 134, 406–412 (2015)

    CAS  PubMed  Google Scholar 

  19. Zhao, C., Gao, L., Wang, C., Liu, B., Jin, Y., Xing, Z.: Structural characterization and antiviral activity of a novel heteropolysaccharide isolated from Grifola frondosa against enterovirus 71. Carbohydr. Polym. 144, 382–389 (2016)

    CAS  PubMed  Google Scholar 

  20. Chen, Y., Liu, Y., Sarker, M.M.R., Yan, X., Yang, C., Zhao, L., Lv, X., Liu, B., Zhao, C.: Structural characterization and antidiabetic potential of a novel heteropolysaccharide from Grifola frondosa via IRS1/PI3K-JNK signaling pathways. Carbohydr. Polym. 198, 452–461 (2018)

    PubMed  Google Scholar 

  21. Chen, R.Z., Tan, L., Jin, C.G., Lu, J., Tian, L., Chang, Q.Q., Wang, K.: Extraction, isolation, characterization and antioxidant activity of polysaccharides from Astragalus membranaceus. Ind. Crops Prod. 77, 434–443 (2015)

    CAS  Google Scholar 

  22. Hromádková, Z., Ebringerová, A., Valachovic, P.: Ultrasound-assisted extraction of water-soluble polysaccharides from the roots of valerian (Valeriana officinalis L.). Ultrason. Sonochem. 9, 37–44 (2002)

    PubMed  Google Scholar 

  23. Ji, H.Y., Chen, P., Yu, J., Feng, Y.Y., Liu, A.J.: Effects of Heat Treatment on the Structural Characteristics and Antitumor Activity of Polysaccharides from Grifola frondosa. Appl. Biochem. Biotechnol. 188, 481–490 (2019)

    CAS  PubMed  Google Scholar 

  24. Chen, Q.L., Chen, Y.J., Zhou, S.S., Yip, K.M., Xu, J., Chen, H.B., Zhao, Z.Z.: Laser microdissection hyphenated with high performance gel permeation chromatography-charged aerosol detector and ultra performance liquid chromatography-triple quadrupole mass spectrometry for histochemical analysis of polysaccharides in herbal medicine. Int. J. Biol. Macromol. 107, 332–342 (2017)

    PubMed  Google Scholar 

  25. Yu, J., Ji, H., Yang, Z., Liu, A.: Relationship between structural properties and antitumor activity of Astragalus polysaccharides extracted with different temperatures. Int. J. Biol. Macromol. 124, 469–477 (2019)

    CAS  PubMed  Google Scholar 

  26. Liu, A.J., Yu, J., Ji, H.Y., Zhang, H.C., Zhang, Y., Liu, H.P.: Extraction of a Novel Cold-Water-Soluble Polysaccharide from Astragalus membranaceus and Its Antitumor and Immunological Activities. Molecules 23, 62-. (2017)

    PubMed Central  Google Scholar 

  27. Feng, Y., Ji, H., Dong, X., Liu, A.: An alcohol-soluble polysaccharide from Atractylodes macrocephala Koidz induces apoptosis of Eca-109 cells. Carbohydr. Polym. 226, 115136 (2019)

    CAS  PubMed  Google Scholar 

  28. Zhang, A., Deng, J., Yu, S., Zhang, F., Linhardt, R.J., Sun, P.: Purification and structural elucidation of a water-soluble polysaccharide from the fruiting bodies of the Grifola frondosa. Int. J. Biol. Macromol. 115, 221–226 (2018)

    CAS  PubMed  Google Scholar 

  29. Meng, M., Cheng, D., Han, L., Chen, Y., Wang, C.: Isolation, purification, structural analysis and immunostimulatory activity of water-soluble polysaccharides from Grifola Frondosa fruiting body. Carbohydr. Polym. 157, 1134–1143 (2017)

    CAS  PubMed  Google Scholar 

  30. Li, Q., Zhang, F., Chen, G., Chen, Y., Zhang, W., Mao, G., Zhao, T., Zhang, M., Yang, L., Wu, X.: Purification, characterization and immunomodulatory activity of a novel polysaccharide from Grifola frondosa. Int. J. Biol. Macromol. 111, 1293–1303 (2018)

    CAS  PubMed  Google Scholar 

  31. Cao, W., Li, X.Q., Wang, X., Fan, H.T., Zhang, X.N., Hou, Y., Liu, S.B., Mei, Q.B.: A novel polysaccharide, isolated from Angelica sinensis (Oliv.) Diels induces the apoptosis of cervical cancer HeLa cells through an intrinsic apoptotic pathway. Phytomedicine 17, 598–605 (2010)

    CAS  PubMed  Google Scholar 

  32. Cui, F.J., Tao, W.Y., Xu, Z.H., Guo, W.J., Xu, H.Y., Ao, Z.H., Jin, J., Wei, Y.Q.: Structural analysis of anti-tumor heteropolysaccharide GFPS1b from the cultured mycelia of Grifola frondosa GF9801. Bioresour. Technol. 98, 395–401 (2007)

    CAS  PubMed  Google Scholar 

  33. Mao, G.-H., Zhang, Z.-H., Fei, F., Ding, Y.-Y., Zhang, W.-J., Chen, H., Ali, S.S., Zhao, T., Feng, W.-W., Wu, X.-Y., Yang, L.-Q.: Effect of Grifola frondosa polysaccharide on anti-tumor activity in combination with 5-Fu in Heps-bearing mice. Int. J. Biol. Macromol. 121, 930–935 (2019)

    CAS  PubMed  Google Scholar 

  34. Li, T., Zhu, J., Guo, L., Shi, X., Liu, Y., Yang, X.: Differential effects of polyphenols-enriched extracts from hawthorn fruit peels and fleshes on cell cycle and apoptosis in human MCF-7 breast carcinoma cells. Food Chem. 141, 1008–1018 (2013)

    CAS  PubMed  Google Scholar 

  35. Doonan, F., Cotter, T.G.: Morphological assessment of apoptosis. Methods 44, 200–204 (2008)

    CAS  PubMed  Google Scholar 

  36. Eisenberg-Lerner, A., Bialik, S., H-U, S., Kimchi, A.: Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell. Death Differ. 16, 966 (2009)

    CAS  PubMed  Google Scholar 

  37. Jin, M., Zhao, K., Huang, Q., Shang, P.: Structural features and biological activities of the polysaccharides from Astragalus membranaceus. Int. J. Biol. Macromol. 64, 257–266 (2014)

    CAS  PubMed  Google Scholar 

  38. Van, E.M., Fcs, R., Cpm, S.B.R., Ljw, N.: Annexin V-affinity assay: A review on an apoptosis detection system based on phosphatidylserine exposure [Review]. Cytometry 31, 1–9 (2015)

    Google Scholar 

  39. Ranganathan, S., Halagowder, D., Sivasithambaram, N.D.: Quercetin Suppresses Twist to Induce Apoptosis in MCF-7 Breast Cancer Cells. Plos One 10, e0141370 (2015)

    PubMed  PubMed Central  Google Scholar 

  40. Vermes, I., Haanen, C., Steffens-Nakken, H., Reutellingsperger, C.: A novel assay for apoptosis Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods 184, 39–51 (1995)

    CAS  PubMed  Google Scholar 

  41. Wang, J., Zhang, Y.-S., Thakur, K., Hussain, S.S., Zhang, J.-G., Xiao, G.-R., Wei, Z.-J.: Licochalcone A from licorice root, an inhibitor of human hepatoma cell growth via induction of cell apoptosis and cell cycle arrest. Food Chem. Toxicol. 120, 407–417 (2018)

    CAS  PubMed  Google Scholar 

  42. Yong, X., Qian, L., Yongxia, Z., Tinghong, Y., Ningyu, W., Guobo, L., Xuanhong, S., Yantong, L., Bin, S., Tao, Y.: SKLB316, a novel small-molecule inhibitor of cell-cycle progression, induces G2/M phase arrest and apoptosis in vitro and inhibits tumor growth in vivo. Cancer Lett. 355, 297–309 (2014)

    Google Scholar 

  43. Shirjang, S., Mansoori, B., Asghari, S., Duijf, P.H.G., Mohammadi, A., Gjerstorff, M., Baradaran, B.: MicroRNAs in cancer cell death pathways: Apoptosis and necroptosis. Free Radic. Biol. Med. 139, 1–15 (2019)

    CAS  PubMed  Google Scholar 

  44. Parvesh, C., Radhika, S., Patel, F.D., Sarala, G., Siddhartha, M.: Serum soluble Fas levels and prediction of response to platinum-based chemotherapy in epithelial ovarian cancer. Int. J. Cancer 122, 1716–1721 (2010)

    Google Scholar 

  45. Través, P.G., López-Fontal, R., Cuadrado, I., Luque, A., Boscá, L., Heras, B., De Las, S., Hortelano: Critical role of the death receptor pathway in the antitumoral effects induced by hispanolone derivatives. Oncogene 32, 259–268 (2013)

    PubMed  Google Scholar 

  46. Zhang, X.J., Wei, C., He, L.J., An, J., Pharmacy, S.O.: Xanthotoxin induces apoptosis in SGC-7901 cells through death receptor pathway. Chin. Herb. Med. 4, 437–444 (2018)

    Google Scholar 

  47. Nallapalle, S.R., Daripally, S., Prasad, V.T.S.V.J.T.B.: Promoter polymorphism of FASL confers protection against female-specific cancers and those of FAS impact the cancers divergently. Tumor Biol. 36, 2709–2724 (2015)

    CAS  Google Scholar 

  48. Fegan, C., Pepper, C.: Apoptosis Deregulation in CLL. Adv. Exp. Med. Biol. 792, 151–171 (2013)

    CAS  PubMed  Google Scholar 

  49. Soriano, M.E., Scorrano, L.: The Interplay between BCL-2 Family Proteins and Mitochondrial Morphology in the Regulation of Apoptosis, Oxygen Transport to Tissue XXXIII, 687, (2010), pp. 97–114

  50. Thorburn, A.: Death receptor-induced cell killing. Cell. Signal 16, 139–144 (2004)

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The study received no financial support.

Author information

Authors and Affiliations

  1. State Key Laboratory of Food Nutrition and Safety, Ministry of Education, College of Food Engineering and Biotechnology, Tianjin University of Science and Technology, No. 29, 13th Street, TEDA, 300457, Tianjin, People’s Republic of China

    Chao Liu, Hai-yu Ji, Peng Wu, Juan Yu & An-jun Liu

  2. QingYunTang Biotech (Beijing) Co., Ltd, Beijing Economic-Technological Development Area, No. 14, Zhonghe Street, 100176, Beijing, China

    Chao Liu, Hai-yu Ji, Peng Wu & Juan Yu

Authors
  1. Chao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hai-yu Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. An-jun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hai-yu Ji or An-jun Liu.

Ethics declarations

None of the authors of this study has any financial interest or conflict with industries or parties.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, C., Ji, Hy., Wu, P. et al. The preparation of a cold-water soluble polysaccharide from Grifola frondosa and its inhibitory effects on MKN-45 cells. Glycoconj J 37, 413–422 (2020). https://doi.org/10.1007/s10719-020-09932-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-020-09932-0

Keywords

Search

Navigation