Skip to main content

Advertisement

SpringerLink
Log in

A novel acid polysaccharide from Boletus edulis: extraction, characteristics and antitumor activities in vitro

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

Abstract

A novel cold-water-soluble polysaccharide (BEP), with a molecular weight of 6.0 × 106 Da, was isolated from Boletus edulis. BEP consists of galactose, glucose, xylose, mannose, glucuronic, and galacturonic acid in a ratio of 0.34:0.28:0.28:2.57:1.00:0.44. The IR results showed that BEP was an acid polysaccharide, containing α-type and β-type glucoside bonds. MTT assay showed BEP could inhibit cell proliferation significantly. Morphological observation demonstrated that BEP-treated MDA-MB-231 and Ca761 cells exhibited typical apoptotic morphological features. Flow cytometry analysis revealed that BEP caused mitochondrial membrane potential collapse. Annexin V-FITC/PI staining indicated that BEP induced apoptosis of MDA-MB-231 and Ca761 cells through cell block in S phase and G0/G1 phase, respectively. Western blot results showed that BEP could increase the Bax/Bcl-2 ratios, promote the release of cytochrome C, and activate the expression of caspase-3 and caspase-9 in MDA-MB-231 and Ca761 cells. In conclusion, our results demonstrated that BEP could inhibit the proliferation of breast cancer cells and induce apoptosis through mitochondrial pathways.

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. Monnot, G.C., Romero, P.: Rationale for immunological approaches to breast cancer therapy. Breast. 37, 187–195 (2018). https://doi.org/10.1016/j.breast.2017.06.009

    Article  PubMed  Google Scholar 

  2. Wang, X., Yang, Y., An, Y., Fang, G.: The mechanism of anticancer action and potential clinical use of kaempferol in the treatment of breast cancer. Biomed. Pharmacother. 117, 109086 (2019). https://doi.org/10.1016/j.biopha.2019.109086

    Article  CAS  PubMed  Google Scholar 

  3. Goldhirsch, A., Winer, E.P., Coates, A.S., Gelber, R.D., Piccart-Gebhart, M., Thurlimann, B., Senn, H.J.: Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann. Oncol. 24(9), 2206–2223 (2013). https://doi.org/10.1093/annonc/mdt303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bernier, J., Poortmans, P.M.: Surgery and radiation therapy of triple-negative breast cancers: from biology to clinics. Breast. 28, 148–155 (2016). https://doi.org/10.1016/j.breast.2016.05.014

    Article  PubMed  Google Scholar 

  5. Bauer, K.R., Brown, M., Cress, R.D., Parise, C.A., Caggiano, V.: Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer registry. Cancer. 109(9), 1721–1728 (2007). https://doi.org/10.1002/cncr.22618

    Article  PubMed  Google Scholar 

  6. Meshkat, B., Prichard, R.S., Al-Hilli, Z., Bass, G.A., Quinn, C., O’Doherty, A., Rothwell, J., Geraghty, J., Evoy, D., McDermott, E.W.: A comparison of clinical-pathological characteristics between symptomatic and interval breast cancer. Breast. 24(3), 278–282 (2015). https://doi.org/10.1016/j.breast.2015.02.032

  7. Moran, M.S., Yang, Q., Harris, L.N., Jones, B., Tuck, D.P., Haffty, B.G.: Long-term outcomes and clinicopathologic differences of African-American versus white patients treated with breast conservation therapy for early-stage breast cancer. Cancer. 113(9), 2565–2574 (2008). https://doi.org/10.1002/cncr.23881

    Article  PubMed  Google Scholar 

  8. Tajbakhsh, A., Rivandi, M., Abedini, S., Pasdar, A., Sahebkar, A.: Regulators and mechanisms of anoikis in triple-negative breast cancer (TNBC): a review. Crit. Rev. Oncol. Hematol. 140, 17–27 (2019). https://doi.org/10.1016/j.critrevonc.2019.05.009

    Article  PubMed  Google Scholar 

  9. Shamsaei, S., Getso, M., Ahmadikia, K., Yarahmadi, M., Farahani, H.E., Aslani, R., Mohammadzade, A.S., Raissi, V., Soleimani, A., Arghavan, B., Karami, S., Mohseni, M., Mohseni, M.S., Raiesi, O.: Recent findings on the role of fungal products in the treatment of cancer. Clin. Transl. Oncol. (2020). https://doi.org/10.1007/s12094-020-02428-1

    Article  PubMed  Google Scholar 

  10. MacFarlane, M., Williams, A.C.: Apoptosis and disease: a life or death decision. EMBO Rep. 5(7), 674–678 (2004). https://doi.org/10.1038/sj.embor.7400191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tang, X., Tang, J., Liu, X., Zeng, L., Cheng, C., Luo, Y., Li, L., Qin, S.L., Sang, Y., Deng, L.M., Lv, X.B.: Downregulation of miR-129-2 by promoter hypermethylation regulates breast cancer cell proliferation and apoptosis. Oncol. Rep. 35(5), 2963–2969 (2016). https://doi.org/10.3892/or.2016.4647

    Article  CAS  PubMed  Google Scholar 

  12. von Schwarzenberg, K., Vollmar, A.M.: Targeting apoptosis pathways by natural compounds in cancer: marine compounds as lead structures and chemical tools for cancer therapy. Cancer Lett. 332(2), 295–303 (2013). https://doi.org/10.1016/j.canlet.2010.07.004

    Article  CAS  Google Scholar 

  13. Nicholson, D.W., Thornberry, N.A.: Caspases: killer proteases. Trends Biochem. Sci. 22(8), 299–306 (1997). https://doi.org/10.1016/S0968-0004(97)01085-2

    Article  CAS  PubMed  Google Scholar 

  14. Duprez, L., Wirawan, E., Vanden Berghe, T., Vandenabeele, P.: Major cell death pathways at a glance. Microbes Infect. 11(13), 1050–1062 (2009). https://doi.org/10.1016/j.micinf.2009.08.013

    Article  CAS  PubMed  Google Scholar 

  15. Levine, B., Sinha, S.C., Kroemer, G.J.A.: Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy. 4(5), 600–606 (2008). https://doi.org/10.4161/auto.6260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Yan, X., Wang, L., Yang, X., Qiu, Y., Tian, X., Lv, Y., Tian, F., Song, G., Wang, T.: Fluoride induces apoptosis in H9c2 cardiomyocytes via the mitochondrial pathway. Chemosphere. 182, 159–165 (2017). https://doi.org/10.1016/j.chemosphere.2017.05.002

    Article  CAS  PubMed  Google Scholar 

  17. Cui, L., Bu, W., Song, J., Feng, L., Xu, T., Liu, D., Ding, W., Wang, J., Li, C., Ma, B., Luo, Y., Jiang, Z., Wang, C., Chen, J., Hou, J., Yan, H., Yang, L., Jia, X.: Apoptosis induction by alantolactone in breast cancer MDA-MB-231 cells through reactive oxygen species-mediated mitochondrion-dependent pathway. Arch Pharm Res. 41(3), 299–313 (2018). https://doi.org/10.1007/s12272-017-0990-2

    Article  CAS  PubMed  Google Scholar 

  18. Manzi, P., Gambelli, L., Marconi, S., Vivanti, V., Pizzoferrato, L.: Nutrients in edible mushrooms: an inter-species comparative study. Food Chem. 65(4), 477–482 (1999). https://doi.org/10.1016/S0308-8146(98)00212-X

    Article  CAS  Google Scholar 

  19. Kalač, P.: Chemical composition and nutritional value of European species of wild grow-ing mushrooms: a review. Food Chem. 113(1), 9–16 (2009). https://doi.org/10.1016/j.foodchem.2008.07.077

    Article  CAS  Google Scholar 

  20. Ruthes, A.C., Smiderle, F.R., Iacomini, M.: d-Glucans from edible mushrooms: A review on the extraction, purification and chemical characterization approaches. Carbohydr. Polym. 117, 753–761 (2015). https://doi.org/10.1016/j.carbpol.2014.10.051

    Article  CAS  PubMed  Google Scholar 

  21. Zhang, H., Pu, D., Sun, B., Ren, F., Zhang, Y., Chen, H.: Characterization and comparison of key aroma compounds in raw and dry porcini mushroom (Boletus edulis) by aroma extract dilution analysis, quantitation and aroma recombination experiments. Food Chem. 258, 260–268 (2018). https://doi.org/10.1016/j.foodchem.2018.03.056

    Article  CAS  PubMed  Google Scholar 

  22. Dentinger, B.T., Ammirati, J.F., Both, E.E., Desjardin, D.E., Halling, R.E., Henkel, T.W., Moreau, P.A., Nagasawa, E., Soytong, K., Taylor, A.F., Watling, R., Moncalvo, J.M., McLaughlin, D.J.: Molecular phylogenetics of porcini mushrooms (Boletus section Boletus). Mol. Phylogenet. Evol. 57(3), 1276–1292 (2010). https://doi.org/10.1016/j.ympev.2010.10.004

    Article  CAS  PubMed  Google Scholar 

  23. Chen, W., Wang, W.P., Zhang, H.S., Huang, Q.: Optimization of ultrasonic-assisted extraction of water-soluble polysaccharides from Boletus edulis mycelia using response surface methodology. Carbohydr. Polym. 87(1), 614–619 (2012). https://doi.org/10.1016/j.carbpol.2011.08.029

    Article  CAS  Google Scholar 

  24. Zhang, A.Q., Liu, Y., Xiao, N.N., Zhang, Y., Sun, P.L.: Structural investigation of a novel heteropolysaccharide from the fruiting bodies of Boletus edulis. Food Chem. 146, 334–338 (2014). https://doi.org/10.1016/j.foodchem.2013.09.073

    Article  CAS  PubMed  Google Scholar 

  25. Zhang, A., Xiao, N., He, P., Sun, P.: Chemical analysis and antioxidant activity in vitro of polysaccharides extracted from Boletus edulis. Int. J. Biol. Macromol. 49(5), 1092–1095 (2011). https://doi.org/10.1016/j.ijbiomac.2011.09.005

    Article  CAS  PubMed  Google Scholar 

  26. Lemieszek, M.K., Cardoso, C., Ferreira Milheiro Nunes, F.H., Ramos Novo Amorim de Barros, A.I., Marques, G., Pozarowski, P., Rzeski, W.: Boletus edulis biologically active biopolymers induce cell cycle arrest in human colon adenocarcinoma cells. Food Funct. 4(4), 575–585 (2013). https://doi.org/10.1039/c2fo30324h

    Article  CAS  PubMed  Google Scholar 

  27. Wang, D., Sun, S.Q., Wu, W.Z., Yang, S.L., Tan, J.M.: Characterization of a water-soluble polysaccharide from Boletus edulis and its antitumor and immunomodulatory activities on renal cancer in mice. Carbohydr. Polym. 105, 127–134 (2014). https://doi.org/10.1016/j.carbpol.2013.12.085

    Article  CAS  PubMed  Google Scholar 

  28. Zhang, L., Zhang, Q., Zheng, Y., He, Z., Guan, P., He, X., Hui, L., Dai, Y.: Study of Schiff base formation between dialdehyde cellulose and proteins, and its application for the deproteinization of crude polysaccharide extracts. Ind. Crop. Prod. 112, 532–540 (2018). https://doi.org/10.1016/j.indcrop.2017.12.056

    Article  CAS  Google Scholar 

  29. Dubois, M., Gilles, H.A., Hamilton, J.K., Rebers, P.A., Smith, F.: Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 22–25 (1956). https://doi.org/10.1021/ac60111a017

    Article  Google Scholar 

  30. Barbosa, H., Slater, N.K., Marcos, J.C.: Protein quantification in the presence of poly(ethylene glycol) and dextran using the Bradford method. Anal. Biochem. 395(1), 108–110 (2009). https://doi.org/10.1016/j.ab.2009.07.045

    Article  CAS  PubMed  Google Scholar 

  31. Bitter, T., Muir, H.M.: A modified uronic acid carbazole reaction. Anal. Biochem. 4(4), 330–334 (1962). https://doi.org/10.1016/0003-2697(62)90095-7

    Article  CAS  PubMed  Google Scholar 

  32. Yu, J., Ji, H.Y., Liu, A.J.: Alcohol-soluble polysaccharide from Astragalus membranaceus: Preparation, characteristics and antitumor activity. Int. J. Biol. Macromol. 118(Pt B), 2057–2064 (2018). https://doi.org/10.1016/j.ijbiomac.2018.07.073

    Article  CAS  PubMed  Google Scholar 

  33. 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). https://doi.org/10.1016/j.ijbiomac.2018.12.268

    Article  CAS  PubMed  Google Scholar 

  34. 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). https://doi.org/10.1016/j.ijbiomac.2018.11.156

    Article  CAS  PubMed  Google Scholar 

  35. Wang, Y., Li, Y., Liu, Y., Chen, X., Wei, X.: Extraction, characterization and antioxidant activities of se-enriched tea polysaccharides. Int. J. Biol. Macromol. 77, 76–84 (2015). https://doi.org/10.1016/j.ijbiomac.2015.02.052

    Article  CAS  PubMed  Google Scholar 

  36. Zhao, Y., Liu, Y., Wang, W., Wu, D., Shi, J., Liu, A.: Apoptosis and autophagy induction of Seleno-β-lactoglobulin (Se-β-Lg) on hepatocellular carcinoma cells lines. J. Funct. Foods 49, 412–423 (2018). https://doi.org/10.1016/j.jff.2018.09.011

    Article  CAS  Google Scholar 

  37. Zhang, L., Li, X., Deng, H., Jing, Y., Fu, Q.: Enhanced thermal conductivity and electrical insulation properties of polymer composites via constructing Pglass/CNTs confined hybrid fillers. Compos. A: Appl. Sci. Manuf. 115, 1–7 (2018). https://doi.org/10.1016/j.compositesa.2018.09.009

    Article  CAS  Google Scholar 

  38. Kong, L., Yu, L., Feng, T., Yin, X., Liu, T., Dong, L.: Physicochemical characterization of the polysaccharide from Bletilla striata: effect of drying method. Carbohydr. Polym. 125, 1–8 (2015). https://doi.org/10.1016/j.carbpol.2015.02.042

    Article  CAS  PubMed  Google Scholar 

  39. Jose, G.M., Raghavankutty, M., Kurup, G.M.: Sulfated polysaccharides from Padina tetrastromatica induce apoptosis in HeLa cells through ROS triggered mitochondrial pathway. Process Biochem. 68, 197–204 (2018). https://doi.org/10.1016/j.procbio.2018.02.014

    Article  CAS  Google Scholar 

  40. Chen, D., Sun, S., Cai, D., Kong, G.: Induction of mitochondrial-dependent apoptosis in T24 cells by a selenium (Se)-containing polysaccharide from Ginkgo biloba L. leaves. Int. J. Biol. Macromol. 101, 126–130 (2017). https://doi.org/10.1016/j.ijbiomac.2017.03.033

    Article  CAS  PubMed  Google Scholar 

  41. Cui, H., Wang, C., Wang, Y., Li, Z., Zhang, Y., Chen, M., Li, F.: Pleurotus nebrodensis polysaccharide induces apoptosis in human non-small cell lung cancer A549 cells. Carbohydr. Polym. 104, 246–252 (2014). https://doi.org/10.1016/j.carbpol.2014.01.001

    Article  CAS  PubMed  Google Scholar 

  42. Azzopardi, M., Farrugia, G., Balzan, R.: Cell-cycle involvement in autophagy and apoptosis in yeast. Mech. Ageing Dev. 161(Pt B), 211–224 (2017). https://doi.org/10.1016/j.mad.2016.07.006

    Article  CAS  PubMed  Google Scholar 

  43. Wang, Y., Huo, T., Feng, C., Zeng, Y., Yang, J., Zhang, X., Dong, F., Deng, J.: Chrysotile asbestos induces apoptosis via activation of the p53-regulated mitochondrial pathway mediated by ROS in A549 cells. Appl. Clay Sci. 182, 105245 (2019). https://doi.org/10.1016/j.clay.2019.105245

    Article  CAS  Google Scholar 

  44. Chen, G., Zhang, P., Huang, T., Yu, W., Lin, J., Li, P., Chen, K.: Polysaccharides from Rhizopus nigricans mycelia induced apoptosis and G2/M arrest in BGC-823 cells. Carbohydr. Polym. 97(2), 800–808 (2013). https://doi.org/10.1016/j.carbpol.2013.05.068

    Article  CAS  PubMed  Google Scholar 

  45. Wang, A., Si, Z., Xue, P., Li, X., Liu, J.: Tacrolimus protects hippocampal neurons of rats with status epilepticus through suppressing oxidative stress and inhibiting mitochondrial pathway of apoptosis. Brain Res. 1715, 176–181 (2019). https://doi.org/10.1016/j.brainres.2019.02.031

    Article  CAS  PubMed  Google Scholar 

  46. Gross, A.: BCL-2 family proteins as regulators of mitochondria metabolism. Biochim. Biophys. Acta 1857(8), 1243–1246 (2016). https://doi.org/10.1016/j.bbabio.2016.01.017

    Article  CAS  PubMed  Google Scholar 

  47. Du, L., Fei, Z., Song, S., Wei, N.: Antitumor activity of Lobaplatin against esophageal squamous cell carcinoma through caspase-dependent apoptosis and increasing the Bax/Bcl-2 ratio. Biomed. Pharmacother. 95, 447–452 (2017). https://doi.org/10.1016/j.biopha.2017.08.119

    Article  CAS  PubMed  Google Scholar 

  48. Vucicevic, K., Jakovljevic, V., Colovic, N., Tosic, N., Kostic, T., Glumac, I., Pavlovic, S., Karan-Djurasevic, T., Colovic, M.: Association of Bax expression and Bcl2/Bax ratio with clinical and molecular prognostic markers in chronic lymphocytic leukemia. J. Med. Biochem. 35(2), 150–157 (2016). https://doi.org/10.1515/jomb-2015-0017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Yao, W., Lin, Z., Shi, P., Chen, B., Wang, G., Huang, J., Sui, Y., Liu, Q., Li, S., Lin, X., Yao, H.: Delicaflavone induces ROS-mediated apoptosis and inhibits PI3K/AKT/mTOR and Ras/MEK/Erk signaling pathways in colorectal cancer cells. Biochem. Pharmacol. 171, 113680 (2019). https://doi.org/10.1016/j.bcp.2019.113680

    Article  CAS  PubMed  Google Scholar 

  50. Zhong, Y., Jin, C., Gan, J., Wang, X., Shi, Z., Xia, X., Peng, X.: Apigenin attenuates patulin-induced apoptosis in HEK293 cells by modulating ROS-mediated mitochondrial dysfunction and caspase signal pathway. Toxicon. 137, 106–113 (2017). https://doi.org/10.1016/j.toxicon.2017.07.018

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Thanks to the College of Food Science and Engineering, Tianjin University of Science and Technology for supporting my research.

Author information

Authors and Affiliations

  1. State Key Laboratory of Food Nutrition and Safety, Tianjin University of Science and Technology, No. 29, 13th street, TEDA, Tianjin, 300457, People’s Republic of China

    Ting Meng, Sha-sha Yu, Hai-yu Ji, Xiao-meng Xu & An-jun Liu

  2. College of Food Science and Engineering, Tianjin University of Science and Technology, Tianjin, 300457, China

    Ting Meng, Sha-sha Yu, Hai-yu Ji, Xiao-meng Xu & An-jun Liu

  3. QingYunTang Biotech (Beijing) Co., Ltd., Beijing, 100176, China

    Hai-yu Ji

Authors
  1. Ting Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sha-sha Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hai-yu Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiao-meng Xu
    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 author

Correspondence to An-jun Liu.

Ethics declarations

Conflict 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

Meng, T., Yu, Ss., Ji, Hy. et al. A novel acid polysaccharide from Boletus edulis: extraction, characteristics and antitumor activities in vitro. Glycoconj J 38, 13–24 (2021). https://doi.org/10.1007/s10719-021-09972-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-021-09972-0

Keywords

Search

Navigation