Skip to main content
SpringerLink
Log in

Differential growth inhibition of cancer cell lines and antioxidant activity of extracts of red, brown, and green marine algae

  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Abstract

As the use of various anticancer drugs is associated with many undesirable side effects, there is an urgent need for the discovery of new, better, and specific anticancer compounds. Antioxidant and antiproliferative activities as well as effects on cell morphology were investigated for methanol (M), chloroform (C), ethyl acetate (E), and aqueous (A) extracts of Caulerpa peltata, Gelidiella acerosa, Padina gymnospora, and Sargassum wightii using 2,2-diphenyl-1-picrylhydrazyl radical-scavenging, ferrous ion chelation, and resazurin-based growth inhibition (in A549, HCT-15, MG-63, and PC-3 cell lines) assays. A general trend was the greater extraction of phenols and flavonoids by chloroform and ethyl acetate, which showed higher activity in many assays. These non-polar C and E extracts showed higher DPPH radical-scavenging and growth inhibitory activities in A549, HCT-15, and PC-3 cells. However, higher ferrous ion chelation (A extracts) and growth inhibition in MG-63 cells (M and A extracts) were seen for the polar extracts. Furthermore, P. gymnospora and C. peltata emerged as promising sources for antiproliferative agents that could be explored for their own activity and as leads for the development of other compounds.

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

Figure 1.
Figure 2.
Figure 3.
Figure 4.

Similar content being viewed by others

References

  • Agardh JG (1848) Species genera et ordines algarum, seu descriptiones succinctae specierum, generum et ordinum, quibus algarum regnum constituitur. Algas fucoideas complectens 1–363. Lundae [Lund]: Gleerup CWK.

  • Anoopkumar-Dukie S.; Carey J. B.; Conere T.; O’ Suvllian E.; van Pelt F. N.; Allshire A. Resazurin assay of radiation response in cultured cells. Br. J. Radiol. 78: 945–947; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Awad N. E.; Selim M. A.; Metawe H. M.; Matloub A. A. Cytotoxic xenicane diterpenes from the brown alga Padina pavonia. Phytother. Res. 22: 1610–1613; 2008.

    Article  PubMed  CAS  Google Scholar 

  • Ayyad S. E.; Ezmirly S. T.; Basaif S. A.; Alarif W. M.; Badria A. F.; Badria F. A. Antioxidant, cytotoxic, antitumor and protective DNA damage metabolites from the Red Sea brown alga Sargassum sp. Pharmacogn. Res. 3: 160–165; 2011.

    Article  CAS  Google Scholar 

  • Bonni A.; Brunet A.; West A. E.; Datta S. R.; Takasu M. A.; Greenberg M. E. Cell survival promoted by the Ras-MAPK signalling pathway by transcription-dependent and -independent mechanisms. Science 286: 1358–1362; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Cancer facts & figures (2012) American Cancer Society, Atlanta. http://www.cancer.org. Cited 21 Sept 2012.

  • Cancer incidence and mortality worldwide (2008) GLOBOCAN. http://globocan.iarc.fr. Cited 27 Sept 2012.

  • Chung J. Y.; Huang C.; Meng X.; Dong Z.; Yang C. S. Inhibition of activator protein 1 activity and cell growth by purified green tea and black tea polyphenols in H-ras-transformed cells: structure–activity relationship and mechanisms involved. Cancer. Res. 59: 4610–4617; 1999.

    PubMed  CAS  Google Scholar 

  • de Sousa A. P. A.; Torres M. R.; Pessosa C.; de Moraes M. O.; Filho F. D. R.; Alves A. P. N. N.; Costa-Lotufo L. V. In vivo growth-inhibition of Sarcoma 180 tumor by alginates from brown seaweed Sargassum vulgare. Carbohydr. Polym. 69: 7–13; 2007.

    Article  Google Scholar 

  • Devi K. P.; Natarajan S.; Periyanaina K.; Shanmughaiahthevar K. P. Bioprotective properties of seaweeds: in vitro evaluation of antioxidant activity and antimicrobial activity against food borne bacteria in relation to polyphenolic content. BMC Complement. Altern. Med. 8: 1–11; 2008.

    Article  Google Scholar 

  • Dias P. F.; Siuyeira J. M.; Vendruscolo L. F.; de Jesus N. T.; Gaqliardi A. R.; Maraschin M.; Ribeiro-do-Valle R. M. Antiangiogenic and antitumoral properties of a polysaccharide isolated from the seaweed Sargassum stenophyllum. Cancer. Chemother. Pharmacol. 56: 436–446; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Ermakova S.; Sokolova R.; Kim S. M.; Um B. H.; Isakov V.; Zvyagintseva T. Fucoidans from brown seaweeds Sargassum hornery, Eclonia cava, Costaria costata: structural characteristics and anticancer activity. Appl. Biochem. Biotechnol. 164: 841–850; 2011.

    Article  PubMed  CAS  Google Scholar 

  • Feldmann J.; Hamel G. Observations sur quelques Gélidiacées. Rev. Gén. Bot. 46: 528–549; 1934.

    Google Scholar 

  • Fischel J. L.; Lemee R.; Formento P.; Caldani C.; Moll J. L.; Pesando D.; Meinesz A.; Grelier P.; Pietra P.; Guerriero A. Cell growth inhibitory effects of caulerpenyne, a sesquiterpenoid from the marine algae Caulerpa taxifolia. Anticancer. Res. 15: 2155–2160; 1995.

    PubMed  CAS  Google Scholar 

  • Fitton J. H. Brown marine algae—a survey of therapeutic potentials. Alternat. Complement. Ther. 9: 29–33; 2003.

    Article  Google Scholar 

  • Folmer F.; Japars M.; Dictato M.; Diederich M. Photosynthetic marine organisms as a source of anticancer compounds. Phytochem. Rev. 9: 557–579; 2010.

    Article  CAS  Google Scholar 

  • Fuller R. W.; Cardellina J. H.; Kato Y.; Brinen L. S.; Clardy J.; Snader K. M.; Boyd M. R. A pentahalogenated monoterpene from the red alga Portieria hornemannii produces a novel cytotoxicity profile against a diverse panel of human tumor cell lines. J. Med. Chem. 35: 3007–3011; 1992.

    Article  PubMed  CAS  Google Scholar 

  • Funahashi H.; Imai T.; Mase T.; Sekiya M.; Yokoi K.; Hayashi H.; Shibata A.; Hayashi T.; Nishikawa M.; Suda N.; Hibi Y.; Mizuno Y.; Tsukamura K.; Hayakawa A.; Tanuma S. Seaweed prevents breast cancer? Cancer. Sci. 92: 483–487; 2001.

    Article  CAS  Google Scholar 

  • Green K. C.; Reed J. C. Mitochondria and apoptosis. Science 281: 1309–1312; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Heffeter P.; Jungwirth U.; Jakupec M.; Hartinger C.; Galanski M.; Elbling L.; Micksche M.; Keppler B.; Berger W. Resistance against novel anticancer metal compounds: differences and similarities. Drug Resist. Updat. 11: 1–16; 2008.

    Article  PubMed  CAS  Google Scholar 

  • Jaganathan SK, Mandal M (2009) Antiproliferative effects of honey and of its polyphenols: a review. J. Biomed. Biotechnol. 13 pages.

  • Jaswir I.; Noviendri D.; Salleh H. M.; Taher M.; Miyashita K. Isolation of fucoxanthin and fatty acids analysis of Padina australis and cytotoxic effect of fucoxanthin on human lung cancer (H1299) cell lines. Afr. J. Biotechnol. 10: 18855–18862; 2011.

    CAS  Google Scholar 

  • Jha R. K.; Zi-rong X. Biomedical compounds from marine organisms. Mar Drugs 2: 123–146; 2004.

    Article  CAS  Google Scholar 

  • Ji H.; Shao H.; Zhang C.; Hong P.; Xiong H. Separation of the polysaccharides in Caulerpa racemosa and their chemical composition and antitumor activity. J. Appl. Polym. Sci. 110: 1435–1440; 2008.

    Article  CAS  Google Scholar 

  • Khanavi M.; Gheidarloo R.; Sadati N.; Ardekani M. R. S.; Nabavi S. M. B.; Tavajohi S.; Ostad S. N. Cytotoxicity of fucosterol containing fraction of marine algae against breast and colon carcinoma cell line. Pharmacogn. Mag. 8: 60–64; 2012.

    Article  PubMed  Google Scholar 

  • Kim K. N.; Ham Y. M.; Moon J. Y.; Kim M. J.; Kim D. S.; Lee W. J.; Lee N. H.; Hyun C. G. In vitro cytotoxic activity of Sargassum thunbergii and Dictyopteris divaricata (Jeju seaweeds) on the HL-60 tumour cell line. Int. J. Pharmacol. 5: 298–306; 2009.

    Article  CAS  Google Scholar 

  • Kumar M.; Kumari P.; Trivedi N.; Shukla M. K.; Gupta V.; Reddy C. R. K.; Jha B. Minerals, PUFAs and antioxidant properties of some tropical seaweeds from Saurashtra coast of India. J. Appl. Phycol. 23: 797–810; 2011.

    Article  CAS  Google Scholar 

  • Lamouroux J. V. F. Observations sur la physiologie des algues marines, et description de cinq nouveaux genres de cette famille. Nouv. Bull. Sci. Soc. Philom. Paris. 1: 330–333; 1809.

    Google Scholar 

  • Logothetis C. J.; Lin S. H. Osteoblasts in prostate cancer metastasis to bone. Nat. Rev. Cancer 5: 21–28; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Masaldan S.; Iyer V. V. Antioxidant and antiproliferative activities of methanolic extract of Aloe vera leaves in human cancer cell lines. J. Pharm. Res. 4: 2791–2796; 2011.

    CAS  Google Scholar 

  • Masuda M.; Suzui M.; Weinstein I. B. Effects of epigallocatechin-3-gallate on growth, epidermal growth factor receptor signalling pathways, gene expression, and chemosensitivity in human head and neck squamous cell carcinoma cell lines. Clin. Cancer Res. 7: 4220–4229; 2001.

    PubMed  CAS  Google Scholar 

  • Meyers P. A.; Gorlick R. Osteosarcoma. Pediatr. Clin. N. Am. 44: 973–989; 1997.

    Article  CAS  Google Scholar 

  • Mohamed S.; Hasim S. N.; Rahman H. A. Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci. Technol. 23: 83–96; 2012.

    Article  CAS  Google Scholar 

  • Murugan K.; Iyer V. V. Antioxidant and antiproliferative activities of marine algae, Gracilaria edulis and Enteromorpha lingulata, from Chennai coast. Int. J. Cancer Res. 8: 15–26; 2012.

    Article  Google Scholar 

  • Nobili S.; Lippi D.; Witort E.; Donnini M.; Bausi L.; Mini E.; Capaccioli S. Natural compounds for cancer treatment and prevention. Pharmacol. Res. 59: 365–378; 2009.

    Article  PubMed  CAS  Google Scholar 

  • Rice-Evans C. A.; Miller N. J.; Paganga G. Structure–antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 20: 933–956; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Rotilio G.; Rossi L.; de Martino A. Free radicals, metal ions and oxidative stress: chemical mechanisms of damage and protection in living systems. J. Braz. Chem. Soc. 6: 221–227; 1995.

    Article  Google Scholar 

  • Sastry V. M. V. S.; Rao G. R. K. Dioctyl phthalate, and antibacterial compound from the marine brown alga—Sargassum wightii. J. App. Phycol. 7: 185–186; 1995.

    Article  CAS  Google Scholar 

  • Selvaraju M.; Makicka Gnanambigai D.; Tamil Mozhi S.; Muthuvel A.; Thangavel B. Total flavanoid and in vitro antioxidant activity of two seaweeds of Rameshwaram coast. Glob. J. Pharmacol. 3: 59–62; 2009.

    Google Scholar 

  • Sonder O. W. Die algen des tropischen Australiens. Abh. Nat. Ver. Hamburg. 5: 33–74; 1871.

    Google Scholar 

  • Stapleton A. E.; Walbot V. Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiol. 105: 881–889; 1994.

    Article  PubMed  CAS  Google Scholar 

  • Tripoli E.; La Guardia M.; Giammanco M. Citrus flavonoids: molecular structure, biological activity and nutritional properties: a review. Food Chem. 104: 466–479; 2007.

    Article  CAS  Google Scholar 

  • Valko M.; Leibfritz D.; Moncol J.; Cronin M. T.; Mazur M.; Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39: 44–84; 2007.

    Article  PubMed  CAS  Google Scholar 

  • Vergote D.; Cren-Olive C.; Chopin V.; Toillon R. A.; Rolando H.; Hondermarck H.; Le B. X. (−)-Epigallocatechin (EGC) of green tea induces apoptosis of human breast cancer cells but not of their normal counterparts. Breast Cancer Res. Treat. 76: 195–201; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Vinayak R. C.; Sabu A. S.; Chatterji A. Bio-prospecting of a few brown seaweeds for their cytotoxic and antioxidant activities. Evid. Based Complement. Alternat. Med. 21: 1–9; 2011a.

    Article  Google Scholar 

  • Vinayak R. C.; Sabu A. S.; Chatterji A. Bio-screening of a few green seaweeds from India for their cytotoxic and antioxidant potential. J. Sci. Food Agric. 91: 2471–2476; 2011b.

    Article  PubMed  CAS  Google Scholar 

  • Wang T.; Jónsdóttir R.; Ólafsdóttir G. Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem. 116: 240–248; 2009.

    Article  CAS  Google Scholar 

  • Williams R.; Spencer J. P. E.; Rice-Evans C. Flavonoids: antioxidants or signaling molecules? Free Radic. Biol. Med. 36: 838–849; 2004.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zubia M.; Fabre M. S.; Kerjean V.; Lann K. L.; Stiger-Pouvreau V.; Fauchon M.; Deslandes E. Antioxidant and antitumoral activities of some Phaeophyta from Brittany coasts. Food Chem. 116: 693–701; 2009.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors appreciate the technical assistance from S. Gowthami with some of the experiments. Financial support was provided from the funding by the Department of Science and Technology (DST), India, for the establishment of the Centre for Bio-Separation Technology (CBST), VIT University, where this project was carried out. The authors also appreciate the help from Mr. Ramalingam (former CMFRI employee, Mandapam) in authentication, from SNAP Natural and Alginate Products in generously providing S. wightii, and from Mr. Raju in the collection of the remaining algal samples.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

  1. Kavitha Murugan & Vidhya V. Iyer

    Present address: School of Bio Sciences and Technology, VIT University, Vellore, 632014, Tamil Nadu, India

Authors and Affiliations

  1. Centre for Bio-Separation Technology, VIT University, Vellore, 632014, Tamil Nadu, India

    Kavitha Murugan & Vidhya V. Iyer

Authors
  1. Kavitha Murugan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vidhya V. Iyer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vidhya V. Iyer.

Additional information

Editor: T. Okamoto

Rights and permissions

Reprints and permissions

About this article

Cite this article

Murugan, K., Iyer, V.V. Differential growth inhibition of cancer cell lines and antioxidant activity of extracts of red, brown, and green marine algae. In Vitro Cell.Dev.Biol.-Animal 49, 324–334 (2013). https://doi.org/10.1007/s11626-013-9603-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11626-013-9603-7

Keywords

Search

Navigation