Glycoconjugate Journal

, Volume 33, Issue 6, pp 975–984 | Cite as

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

  • Hongyan Li
  • Xin Liu
  • Yan Xu
  • Xiaoke Wang
  • Huajie Zhu
Original Article


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.


Aspergillus aculeatus Extracellular polysaccharide Structure Antitumor activity 



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).

Compliance with ethical standards

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.

Supplementary material

10719_2016_9717_MOESM1_ESM.pdf (314 kb)
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)
10719_2016_9717_MOESM2_ESM.pdf (28 kb)
Supplementary Fig. S2 Cell cycle synchronization of HeLa cells with or without 10 % FBS for 24 h. (PDF 27 kb)


  1. 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)CrossRefGoogle Scholar
  2. 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)CrossRefPubMedGoogle Scholar
  3. 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)CrossRefPubMedGoogle Scholar
  4. 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)CrossRefPubMedGoogle Scholar
  5. 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)CrossRefGoogle Scholar
  6. 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)CrossRefPubMedGoogle Scholar
  7. 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)CrossRefPubMedGoogle Scholar
  8. 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)Google Scholar
  9. 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)CrossRefPubMedGoogle Scholar
  10. 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)CrossRefPubMedGoogle Scholar
  11. 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)CrossRefGoogle Scholar
  12. 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)CrossRefGoogle Scholar
  13. 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)CrossRefGoogle Scholar
  14. 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)CrossRefGoogle Scholar
  15. 15.
    Bitter T., Muir H.M.: A modified uronic acid carbazole reaction. Anal. Biochem. 4, 330–334 (1962)CrossRefPubMedGoogle Scholar
  16. 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)CrossRefPubMedGoogle Scholar
  17. 17.
    Hakomori S.: A rapid permethylation of glycolipid, and polysaccharide catalyzed by methylsulfinyl carbanion in dimethyl sulfoxide. J. Biochem. 55, 205–208 (1964)PubMedGoogle Scholar
  18. 18.
    Mosman T.: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65, 55–63 (1983)CrossRefGoogle Scholar
  19. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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)CrossRefPubMedGoogle Scholar
  21. 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)CrossRefPubMedGoogle Scholar
  22. 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)Google Scholar
  23. 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)CrossRefPubMedGoogle Scholar
  24. 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)CrossRefGoogle Scholar
  25. 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)Google Scholar
  26. 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)CrossRefPubMedGoogle Scholar
  27. 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)CrossRefGoogle Scholar
  28. 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)CrossRefPubMedGoogle Scholar
  29. 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)CrossRefPubMedGoogle Scholar
  30. 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)CrossRefPubMedGoogle Scholar
  31. 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)CrossRefGoogle Scholar
  32. 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)CrossRefPubMedGoogle Scholar
  33. 33.
    Ren L., Perera C., Hemar Y.: Antitumor activity of mushroom polysaccharides: A review. Food Funct. 3, 1118–1130 (2012)CrossRefPubMedGoogle Scholar
  34. 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)CrossRefGoogle Scholar
  35. 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)CrossRefPubMedGoogle Scholar
  36. 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)CrossRefGoogle Scholar
  37. 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)CrossRefPubMedGoogle Scholar
  38. 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)CrossRefPubMedGoogle Scholar
  39. 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)CrossRefGoogle Scholar
  40. 40.
    Jin X.C., Ning Y.: Extraction optimization and bioactivity of polysaccharides from Aspergillus fumigatus AF1. Carbohydr. Polym. 96, 411–416 (2013)CrossRefPubMedGoogle Scholar
  41. 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)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Key Laboratory of Medicinal Chemistry and Molecular Diagnosis, Ministry of EducationBaodingChina
  2. 2.College of Chemistry and Environment ScienceHebei UniversityBaodingChina
  3. 3.College of Pharmaceutical ScienceHebei UniversityBaodingChina
  4. 4.Biology Institute of Shandong Academy of Sciences/Key Laboratory for Biosensors of Shandong ProvinceJinanChina

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