Skip to main content
Log in

Anticancer Activity of the Potential Pyropia yezoensis Galactan Fractionated in Human Prostate Cancer Cells

  • Research Paper
  • Published:
Biotechnology and Bioprocess Engineering Aims and scope Submit manuscript

Abstract

Galactan is a major sulfate polysaccharide in the red seaweed, Pyropia yezoensis. In the present study, the prebiotic potential and anticancer activities of three sulfate galactans with different molecular weights (GPYcrude, GPY300, and GPY10) were evaluated in vitro. Monosaccharide composition and structural analyses of these sulfate galactans showed that all polysaccharide fractions contained the same monosaccharides but had different molecular weights. All the polysaccharides tested displayed potential prebiotic activity, with GPY10 noticeably having the best potential compared to others, especially for Bifidobacterium spp., which highlights possible correlations between structural galactan features and prebiotic activity. Furthermore, all three sulfate galactans were cytotoxic to DU145 and PC-3 prostate cancer cells, with GPY10 exhibiting the greatest inhibition in DU145 cells. Moreover, GPY10 induced modulates the production of intracellular reactive oxygen species (ROS), with subsequent increased apoptosis of DU145 prostate cancer cell and modulating the PI3K/AKT/mTOR signaling pathway. GPY10 increased expression of Bax, executor caspase-3, and initiator caspases 8 and 9. Therefore, sulfate galactans from P. yezoensis could be applied as a novel prebiotic and anticancer compounds in prostate cancer cells.

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.

Similar content being viewed by others

References

  1. Cao, J., J. Wang, S. Wang, and X. Xu (2016) Porphyra species: a mini-review of its pharmacological and nutritional properties. J. Med. Food. 19: 111–119.

    Article  CAS  Google Scholar 

  2. Kim, G. H., K. H. Moon, J. Y. Kim, J. Shim, and T. A. Klochkova (2014) A revaluation of algal diseases in Korean Pyropia (Porphyra) sea farms and their economic impact. Algae. 29: 249–265.

    Article  Google Scholar 

  3. Kwon, M. J. and T. J. Nam (2007) Chromatographically purified porphyran from Porphyra yezoensis effectively inhibits proliferation of human cancer cells. Food Sci. Biotechnol. 16: 873–878.

    CAS  Google Scholar 

  4. Bhatia, S., A. Sharma, K. Sharma, M. Kavale, B. B. Chaugule, K. Dhalwal, A. G. Namdeo, and K. R. Mahadik (2008) Novel algal polysaccharides from marine source: Porphyran. Pharmacogn. Rev. 2: 271–276.

    Google Scholar 

  5. Isaka, S., K. Cho, S. Nakazono, R. Abu, M. Ueno, D. Kim, and T. Oda (2015) Antioxidant and anti-inflammatory activities of porphyran isolated from discolored nori (Porphyra yezoensis). Int. J. Biol. Macromol. 74: 68–75.

    Article  CAS  Google Scholar 

  6. Kato, T. and M. Sugimoto (2020) Quality of life in active surveillance for early prostate cancer. Int. J. Urol. 27: 296–306.

    Article  Google Scholar 

  7. Lee, S. J., D. G. Lee, S. H. Park, M. Kim, C. S. Kong, Y. Y. Kim, and S. H. Lee (2015) Comparison of biological activities in Sargassum siliquanstrum fermented by isolated lactic acid bacteria. Biotechnol. Bioprocess Eng. 20: 341–348.

    Article  CAS  Google Scholar 

  8. Seong, H., J. H. Bae, J. S. Seo, S. A. Kim, T. J. Kim, and N. S. Han (2019) Comparative analysis of prebiotic effects of seaweed polysaccharides laminaran, porphyran, and ulvan using in vitro human fecal fermentation. J. Funct. Foods. 57: 408–416.

    Article  CAS  Google Scholar 

  9. Muraoka, T., K. Ishihara, C. Oyamada, H. Kunitake, I. Hirayama, and T. Kimura (2008) Fermentation properties of low-quality red alga susabinori Porphyra yezoensis by intestinal bacteria. Biosci. Biotechnol. Biochem. 72: 1731–1739.

    Article  CAS  Google Scholar 

  10. Pierre, G., V. Sopena, C. Juin, A. Mastouri, M. Graber, and T. Maugard (2011) Antibacterial activity of a sulfated galactan extracted from the marine alga Chaetomorpha aerea against Staphylococcus aureus. Biotechnol. Bioprocess Eng. 16: 937–945.

    Article  CAS  Google Scholar 

  11. Nishiguchi, T., K. Cho, S. Isaka, M. Ueno, J. O. Jin, K. Yamaguchi, D. Kim, and T. Oda (2016) Protective effect of porphyran isolated from discolored nori (Porphyra yezoensis) on lipopolysaccharide-induced endotoxin shock in mice. Int. J. Biol. Macromol. 93: 1273–1278.

    Article  CAS  Google Scholar 

  12. He, D., S. Wu, L. Yan, J. Zuo, Y. Cheng, H. Wang, J. Liu, X. Zhang, M. Wu, J. I. Choi, and H. Tong (2019) Antitumor bioactivity of porphyran extracted from Pyropia yezoensis Chonsoo2 on human cancer cell lines. J. Sci. Food Agric. 99: 6722–6730.

    Article  CAS  Google Scholar 

  13. Park, J. H. and J. G. Koo (2008) A simple purification method and chemical properties of porphyran from Porphyra yezoensis. J. Kor. Fish Soc. 41: 409–413.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  15. Cesaretti, M., E. Luppi, F. Maccari, and N. Volpi (2003) A 96-well assay for uronic acid carbazole reaction. Carbohydr. Polym. 54: 59–61.

    Article  CAS  Google Scholar 

  16. Dodgson, K. and R. G. Price (1962) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem. J. 84: 106–110.

    Article  CAS  Google Scholar 

  17. Le, B., J. A. Shin, M. G. Kang, S. Sun, S. H. Yang, and G. Chung (2018) Enhanced growth rate and ulvan yield of Ulva pertusa using light-emitting diodes (LEDs). Aquacult. Int. 26: 937–946.

    Article  Google Scholar 

  18. Zhang, G., D. A. Mills, and D. E. Block (2009) Development of chemically defined media supporting high-cell-density growth of lactococci, enterococci, and streptococci. Appl. Environ. Microbiol. 75: 1080–1087.

    Article  CAS  Google Scholar 

  19. Livak, K. J. and T. D. Schmittgen (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25: 402–408.

    Article  CAS  Google Scholar 

  20. Zou, P., X. Lu, C. Jing, Y. Yuan, Y. Lu, C. Zhang, L. Meng, H. Zhao, and Y. Li (2018) Low-molecular-weightt polysaccharides from Pyropia yezoensis enhance tolerance of wheat seedlings (Triticum aestivum L.) to salt stress. Front. Plant Sci. 9: 427.

    Article  Google Scholar 

  21. Barbosa, A. I., A. J. Coutinho, S. A. Costa Lima, and S. Reis (2019) Marine polysaccharides in pharmaceutical applications: fucoidan and chitosan as key players in the drug delivery match field. Mar. Drugs. 17: 654.

    Article  CAS  Google Scholar 

  22. Yu, X., C. Zhou, H. Yang, X. Huang, H. Ma, X. Qin, and J. Hu (2015) Effect of ultrasonic treatment on the degradation and inhibition cancer cell lines of polysaccharides from Porphyra yezoensis. Carbohydr. Polym. 117: 650–656.

    Article  CAS  Google Scholar 

  23. Wen, Z. S., X. W. Xiang, H. X. Jin, X. Y. Guo, L. J. Liu, Y. N. Huang, X. K. OuYang, and Y. L. Qu (2016) Composition and anti-inflammatory effect of polysaccharides from Sargassum horneri in RAW264.7 macrophages. Int. J. Biol. Macromol. 88: 403–413.

    Article  CAS  Google Scholar 

  24. Ye, H., K. Wang, C. Zhou, J. Liu, and X. Zeng (2008) Purification, antitumor and antioxidant activities in vitro of polysaccharides from the brown seaweed Sargassum pallidum. Food Chem. 111:428–432.

    Article  CAS  Google Scholar 

  25. Shao, P., X. Chen, and P. Sun (2013) In vitro antioxidant and antitumor activities of different sulfated polysaccharides isolated from three algae. Int. J. Biol. Macromol. 62: 155–161.

    Article  CAS  Google Scholar 

  26. Hwang, H. J., S. Y. Lee, S. M. Kim, and S. B. Lee (2011) Fermentation of seaweed sugars by Lactobacillus species and the potential of seaweed as a biomass feedstock. Biotechnol. Bioprocess Eng. 16: 1231–1239.

    Article  CAS  Google Scholar 

  27. Brausi, M., P. Hoskin, E. Andritsch, I. Banks, M. Beishon, H. Boyle, M. Colecchia, R. Delgado-Bolton, M. Höckel, K. Leonard, J. Lövey, P. Maroto, K. Mastris, R. Medeiros, P. Naredi, R. Oyen, T. de Reijke, P. Selby, T. Saarto, R. Valdagni, A. Costa, and P. Poortmans (2020) ECCO essential requirements for quality cancer care: prostate cancer. Crit. Rev. Oncol. Hematol. 148: 102861.

    Article  Google Scholar 

  28. Jemal, A., R. Siegel, E. Ward, Y. Hao, J. Xu, and M. J. Thun (2009) Cancer statistics, 2009. CA Cancer J. Clin. 59: 225–249.

    Article  Google Scholar 

  29. Cairns, R. A., I. S. Harris, and T. W. Mak (2011) Regulation of cancer cell metabolism. Nat. Rev. Cancer. 11: 85–95.

    Article  CAS  Google Scholar 

  30. Jia, Y., Y. Sun, L. Weng, Y. Li, Q. Zhang, H. Zhou, and B. Yang (2016) Low molecular weight fucoidan protects renal tubular cells from injury induced by albumin overload. Sci. Rep. 6: 31759.

    Article  CAS  Google Scholar 

  31. Vaikundamoorthy, R., V. Krishnamoorthy, R. Vilwanathan, and R. Rajendran (2018) Structural characterization and anticancer activity (MCF7 and MDA-MB-231) of polysaccharides fractionated from brown seaweed Sargassum wightii. Int. J. Biol. Macromol. 111: 1229–1237.

    Article  CAS  Google Scholar 

  32. McIlwain, D. R., T. Berger, and T. W. Mak (2013) Caspase functions in cell death and disease. Cold Spring Harb. Perspect. Biol. 5: a008656.

    Article  Google Scholar 

  33. Morgensztern, D. and H. L. McLeod (2005) PI3K/Akt/mTOR pathway as a target for cancer therapy. Anticancer Drugs. 16: 797–803.

    Article  CAS  Google Scholar 

Download references

Acknowledgment

This research was financially supported by the Ministry of Small and Medium-sized Enterprises (SMEs) and Startups (MSS), Korea, under the “Regional Specialized Industry Development Plus Program (R&D, S3005783)” supervised by the Korea Institute for Advancement of Technology (KIAT).

The authors declare no conflict of interest.

Neither ethical approval nor informed consent was required for this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seung Hwan Yang.

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

Pham, T.N.A., Le, B. & Yang, S.H. Anticancer Activity of the Potential Pyropia yezoensis Galactan Fractionated in Human Prostate Cancer Cells. Biotechnol Bioproc E 26, 63–70 (2021). https://doi.org/10.1007/s12257-020-0157-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12257-020-0157-8

Keywords

Navigation