Skip to main content
Log in

Structure and antitumor activity of the extracellular polysaccharides from Aspergillus aculeatus via apoptosis and cell cycle arrest

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

Abstract

Two extracellular polysaccharides, designated as WPA and WPB, were isolated from the fungus Aspergillus aculeatus using Q-Sepharose fast flow and Sephacryl S-300 column chromatography. WPA composed of mannose and galactose in a molar ratio of 3.9:1.0, and WPB mainly contained mannose. The molecular weight of WPA and WPB was about 28.1 kDa and 21.0 kDa, respectively. On the basis of methylation and NMR analysis, the possible main chain of WPA was [→5)-β-D-Galf-(1 → 2,6)-α-D-Manp(1→], and WPB was mainly [→2,6)-α-D-Manp(1→], both with [α-D-Manp(1 → 2)-α-D-Manp(1 → 2)-α-D-Manp(1→] substituted at C-2 of [→2,6)-α-D-Manp(1→]. Meanwhile, WPA displayed a stronger anti-proliferative effect than WPB on HeLa, MCF-7 and MGC-803 cells in vitro. WPA and WPB could arrest HeLa cells in G2/M phase and induce HeLa cells apoptosis. Thus, our study provides evidence that WPA and WPB may be taken as potential candidates for treating cervical carcinoma.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  1. Seviour R.J., Stasinopoulos S.J., Auer D.P.F., Gibbs P.A.: Production of pullulan and other exopolysaccharides by filamentous fungi. Crit. Rev. Biotechnol. 12, 279–298 (1992)

    Article  CAS  Google Scholar 

  2. Bae J.S., Jang K.H., Jin H.K.: Effects of natural polysaccharides on the growth and peritoneal carcinomatosis of human gastric adenocatcinoma in a nude mouse model. Cancer Lett. 235, 60–68 (2006)

    Article  CAS  PubMed  Google Scholar 

  3. Chen G.C., Zhang P.Y., Huang T.T., Yu W.Q., Lin J., Li P., Chen K.S.: Polysaccharides from Rhizopus nigricans mycelia induced apoptosis and G2/M arrest in BGC-823 cells. Carbohydr. Polym. 97, 800–808 (2013)

    Article  CAS  PubMed  Google Scholar 

  4. Pei J.J., Wang Z.B., Ma H.L., Yan J.K.: Structural features and antitumor activity of a novel polysaccharide from alkaline extract of Phellinus linteus mycelia. Carbohydr. Polym. 115, 472–477 (2015)

    Article  CAS  PubMed  Google Scholar 

  5. Meng L., Sun S.S., Li R., Shen Z.P., Wang P., Jiang X.L.: Antioxidant activity of polysaccharides produced by Hirsutella sp. and relation with their chemical characteristics. Carbohyd. Polym. 117, 452–457 (2015)

    Article  CAS  Google Scholar 

  6. Zhang B.Z., Inngjerdingen K.T., Zou Y.F., Rise F., Michaelsen T.R., Yan P.S., Paulsenm B.S.: Characterization and immunomodulating activities of exo-polysaccharides from submerged cultivation of Hypsizigus marmoreus. Food Chem. 163, 120–128 (2014)

    Article  CAS  PubMed  Google Scholar 

  7. Sun Y., Sun T.W., Wang F., Zhang J., Li C., Chen X.N., Li Q., Sun S.B.: A polysaccharide from the fungi of Huaier exhibits anti-tumor potential and immunomodulatory effects. Carbohydr. Polym. 92, 577–582 (2013)

    Article  CAS  PubMed  Google Scholar 

  8. Gómez-Miranda, B, Prieto, A, Leal, J.A., Ahrazem, O, Jiménez-Barbero, J, Bernabé, M. Differences among the cell wall galactomannans from Aspergillus wentii and Chaetosartorya chrysella and that of Aspergillus fumigatus. Glycoconj. J. 20, 239–246(2004)

  9. Choma A., Wiater A., Komaniecka I., Paduch R., Pleszczyńska M., Szczodrak J.: Chemical characterization of a water insoluble (1 → 3)-α-D-glucan from an alkaline extract of Aspergillus wentii. Carbohydr. Polym. 91, 603–608 (2013)

    Article  CAS  PubMed  Google Scholar 

  10. Jin X.C., Zhao S.J.: Extraction optimization and bioactivities of an extracellular polysaccharide produced by Aspergillus fumigatus. Int. J. Biol. Macromol. 68, 13–17 (2014)

    Article  CAS  PubMed  Google Scholar 

  11. Sun H.H., Mao W.J., Chen Y., Guo S.D., Li H.Y., Qi X.H., Chen Y.L., Xu J.: Isolation, chemical characteristics and antioxidant properties of the polysaccharides from marine fungus Penicillium sp. F23–2. Carbohydr. Polym. 78, 117–124 (2009)

    Article  CAS  Google Scholar 

  12. Wang C.Y., Mao W.J., Chen Z.Q., Zhu W.M., Chen Y.L., Zhao C.Q., Li N., Yan M.X., Liu X., Guo T.T.: Purification, structural characterization and antioxidant property of an extracellular polysaccharide from Aspergillus terreus. Process Biochem. 48, 1395–1401 (2013)

    Article  CAS  Google Scholar 

  13. Matthaei J.H., Jones O.W., Martin R.G., Nirenberg M.W.: Characteristics and composition of RNA coding units. P. Natl. Acad. Sci USA. 48, 666–667 (1962)

    Article  CAS  Google Scholar 

  14. Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F.: Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–356 (1956)

    Article  CAS  Google Scholar 

  15. Bitter T., Muir H.M.: A modified uronic acid carbazole reaction. Anal. Biochem. 4, 330–334 (1962)

    Article  CAS  PubMed  Google Scholar 

  16. Bradford M.M.: A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976)

    Article  CAS  PubMed  Google Scholar 

  17. Hakomori S.: A rapid permethylation of glycolipid, and polysaccharide catalyzed by methylsulfinyl carbanion in dimethyl sulfoxide. J. Biochem. 55, 205–208 (1964)

    CAS  PubMed  Google Scholar 

  18. Mosman T.: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65, 55–63 (1983)

    Article  Google Scholar 

  19. Ikuta K., Shibata N., Blake J.S., Dahl M.V., Nelson R.D., Hisamichi K., Kobayashi H., Suzuki S., Okawa Y.: NMR study of the galactomannans of Trichophyton mentagrophytes and Trichophyton rubrum. Biochem. J. 323, 297–305 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ahrazem O., Prieto A., Leal J.A., Jiménez-Barbero J., Bernabé M.: Fungal cell-wall galactomannans isolated from Geotrichum spp. and their teleomorphs, Dipodascus and Galactomyces. Carbohydr. Res. 337, 2347–2351 (2002)

    Article  CAS  PubMed  Google Scholar 

  21. Bernabé M., Salvachúa D., Jiménez-Barbero J., Leal J.A., Prieto A.: Structures of wall heterogalactomannans isolated from three genera of entomopathogenic fungi. Fungal Biol. 115, 862–870 (2011)

    Article  PubMed  Google Scholar 

  22. Prieto, A., Leal, J.A., Povera, A., Jiménez-Barbero, J., Gόmez-Miranda, B., Domenech, K., A hrazem, O., Bernabé, M. Structure of complex cell wall polysaccharides isolated from Trichoderma and Hypocrea species. Carbohyd. Res. 304, 281–291 (1997)

  23. Giménez-Abián M.I., Bernabé M., Leal J.A., Jiménez-Barbero J., Prieto A.: Structure of a galactomannan isolated from the cell wall of the fungus Lineolata rhizophorae. Carbohydr. Res. 342, 2599–2603 (2007)

    Article  PubMed  Google Scholar 

  24. Domenech J., Prieto A., Gómez-Miranda B., Leal J.A., Ahrazem O., Jiménez-Barbero J., Bernabé M.: Structure of fungal polysaccharides isolated from the cell-wall of three strains of Verticillium fungicola. Carbohydr. Polym. 50, 209–212 (2002)

    Article  CAS  Google Scholar 

  25. Chen, Y, Mao W.J., Wang, B.F., Zhou, L.N., Gu, Q.Q., Chen, Y.L., Zhao, C.Q., Li, N, Wang, C.Y., Shan, J.M., Yan, M.X., Lin, C. Preparation and characterization of an extracellular polysaccharide produced by the deep-sea fungus Penicillium griseofulvum. Bioresour. Technol. 132, 178–181 (2013)

  26. Omarsdottir S., Petersen B.O., Paulsen B.S., Togola A., Duus J.D., Olafsdottir E.S.: Structural characterisation of novel lichen heteroglycans by NMR spectroscopy and methylation analysis. Carbohydr. Res. 341, 2449–2455 (2006)

    Article  CAS  PubMed  Google Scholar 

  27. He M.W., Yang X.B., Jiao Y.B., Tiao L.M., Zhao Y.: Characterization of antioxidant and antiproliferative acidic polysaccharides from Chinese wolfberry fruits. Food Chem. 133, 978–989 (2012)

    Article  CAS  Google Scholar 

  28. Xie J.H., Liu X., Shen M.Y., Nie S.P., Zhang H., Li C., Gong D.M., Xie M.Y.: Purification, physicochemical characterisation and anticancer activity of a polysaccharide from Cyclocarya paliurus leaves. Food Chem. 136, 1453–1460 (2013)

    Article  CAS  PubMed  Google Scholar 

  29. Zhu Q.Q., Jiang Y.M., Lin S., Wen L.R., Wu D., Zhao M.M., Chen F., Jia Y.X., Yang B.: Structural identification of (1 → 6)-α-D-Glucan, a key responsible for the health benefits of Longan, and evaluation of antitumor activity. Biomacromolecules. 14, 1999–2003 (2013)

    Article  CAS  PubMed  Google Scholar 

  30. Khammanit R., Chantakru S., Kitiyanant Y., Saikhun J.: Effect of serum starvation and chemical inhibitors on cell cycle synchronization of canine dermal fibroblasts. Theriogenology. 70, 27–34 (2008)

    Article  CAS  PubMed  Google Scholar 

  31. Zhang E.M., Li X.L., Zhang S.F., Chen L.Q., Zheng X.X.: Cell cycle synchronization of embryonic stem cells: Effect of serum deprivation on the differentiation of embryonic bodies in vitro. Biochem. Bioph. Res. Co. 333, 1171–1177 (2005)

    Article  CAS  Google Scholar 

  32. Zong A.Z., Cao H.Z., Wang F.S.: Antitumor polysaccharides from natural resources: A review of recent research. Carbohydr. Polym. 90, 1395–1410 (2012)

    Article  CAS  PubMed  Google Scholar 

  33. Ren L., Perera C., Hemar Y.: Antitumor activity of mushroom polysaccharides: A review. Food Funct. 3, 1118–1130 (2012)

    Article  CAS  PubMed  Google Scholar 

  34. Nie S.P., Zhang H., Li W.J., Xie M.Y.: Current development of polysaccharides from Ganoderma: isolation, structure and bioactivities. Bioactive carbohydrates and Dietary Fibre. 1, 10–20 (2013)

    Article  CAS  Google Scholar 

  35. Mei Y.X., Zhu H., Hu Q.M., Liu Y.Y., Zhao S.M., Peng N., Liang Y.X.: A novel polysaccharide from mycelia of cultured Phellinus linteus displays antitumor activity through apoptosis. Carbohydr. Polym. 124, 90–97 (2015)

    Article  CAS  PubMed  Google Scholar 

  36. Li J.E., Cui S.W., Nie S.P., Xie M.Y.: Structure and biological activities of a pectic polysaccharide from Mosla chinensis Maxim. cv. Jiangxiangru. Carbohyd. Polym. 105, 276–284 (2014)

    Article  CAS  Google Scholar 

  37. Zhu Z.Y., Pang W., Li Y.Y., Ge X.R., Chen L.J., Liu X.C., Lv Q., Dong G.L., Liu A.J., Zhang Y.M.: Effect of ultrasonic treatment on structure and antitumor activity of mycelial polysaccharides from Cordyceps gunnii. Carbohydr. Polym. 114, 12–20 (2014)

    Article  CAS  PubMed  Google Scholar 

  38. Yu J., Sun R.L., Zhao Z.Q., Wang Y.Y.: Auricularia polytricha polysaccharides induce cell cycle arrest and apoptosis in human lung cancer A549 cell. Int. J. Biol. Macromol. 68, 67–71 (2014)

    Article  CAS  PubMed  Google Scholar 

  39. Zhang M., Cheung P.C.K., Chiu L.C.M., Wong E.Y.L., Ooi V.E.C.: Cell-cycle arrest and apoptosis induction in human breast carcinoma MCF-7 cells by carboxymethylated β-glucan from the mushroom sclerotia of Pleurotus tuber-regium. Carbohydr. Polym. 66, 455–462 (2006)

    Article  CAS  Google Scholar 

  40. Jin X.C., Ning Y.: Extraction optimization and bioactivity of polysaccharides from Aspergillus fumigatus AF1. Carbohydr. Polym. 96, 411–416 (2013)

    Article  CAS  PubMed  Google Scholar 

  41. Li X., Jiao L.L., Zhang X., Tian W.M., Chen S., Zhang L.P.: Structure of polysaccharides from mycelium and culture medium of Phellinus nigricans using submerged fermentation. Sci. China Ser. C Life Sci. 51, 513–519 (2008)

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by financial support from Hebei University, Natural Science Foundation of Hebei province in China (B2015201069), Youth Fund Project of Hebei Education Department (QN2014131), and Bureau of Baoding city science and technology project (14ZF083).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hongyan Li or Huajie Zhu.

Ethics declarations

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.

Electronic supplementary material

Supplementary Fig. S1

NMR spectra of WPA and WPB. (a) 1H-1H COSY spectrum, (b) 1H-13C HMQC spectrum, (c) 1H-1H NOESY spectrum and (d) 1H-13C HMBC spectrum. A: [→2)-α-D-Manp(1→], B: [→2)-α-D-Manp(1→], C: [→2,6)-α-D-Manp(1→], D: [α-D-Manp(1→], E: [→5)-β-D-Galf(1→] (PDF 313 kb)

Supplementary Fig. S2

Cell cycle synchronization of HeLa cells with or without 10 % FBS for 24 h. (PDF 27 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, H., Liu, X., Xu, Y. et al. Structure and antitumor activity of the extracellular polysaccharides from Aspergillus aculeatus via apoptosis and cell cycle arrest. Glycoconj J 33, 975–984 (2016). https://doi.org/10.1007/s10719-016-9717-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-016-9717-8

Keywords

Navigation