Skip to main content

Advertisement

SpringerLink
Log in

Antioxidant and antiproliferative effects of different solvent fractions from Terminalia belerica Roxb. fruit on various cancer cells

  • Original Article
  • Published:
Cytotechnology Aims and scope Submit manuscript

Abstract

Terminalia belerica Roxb. fruits have been previously reported against diabetes, ulcer, microbial problems and hepatotoxicity. The present study was aimed to investigate antioxidant and anticancer potential of sequentially fractionated hexane (TBHE), chloroform (TBCE), ethyl acetate (TBEE), butanol (TBBE) and water (TBWE) extracts from the 70% methanolic extract of T. belerica fruits. TBCE, TBEE, TBBE and TBWE showed excellent ROS (reactive oxygen species) and RNS (reactive nitrogen species) scavenging activities which was investigated using 11 different assays for various free radicals. Among 5 fractions, TBHE and TBCE remained nontoxic to any of the malignant cell lines including normal cells (WI-38). TBBE and TBWE inhibited the proliferation of breast (MCF-7), cervical (HeLa) and brain (U87) cancer cells by inducing G2/M arrest while TBEE caused apoptosis. However, these fractions did not inhibit the proliferation of lung (A549) and liver (HepG2) cancer cells. BrdU incorporation study also suggested the efficient anticancer potential of TBEE, TBBE and TBWE. Moreover, TBBE and TBWE treated MCF-7, HeLa and U87 cells showed upregulation of p53 and p21 proteins. Phytochemical analysis reflected the presence of adequate quantities of different phytochemicals. Moreover, HPLC analysis show peaks of purpurin, catechin, tannic acid, reserpine, ellagic acid, methyl gallate, aconitine and rutin in TBBE, TBWE and TBEE. Hence these polar extracts of T. belerica can be used to develop drug against different types of cancer.

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
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Agarwal ML, Agarwal A, Taylor WR et al (1998) A p53-dependent S-phase checkpoint helps to protect cells from DNA damage in response to starvation for pyrimidine nucleotides. Proc Natl Acad Sci USA 95:14775–14778

    Article  CAS  Google Scholar 

  • Anand KK, Singh B, Saxena AK et al (1997) 3, 4, 5-trihydroxy benzoic acid (Gallic acid), the hepatoprotective principle in the fruits of Terminalia bellerica bioassay guided activity. Pharmacol Res 36:315–321

    Article  CAS  Google Scholar 

  • Aruoma OI, Halliwell B, Hoey BM et al (1989) The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Rad Biol Med 6:593–597

    Article  CAS  Google Scholar 

  • Buxton EJ, Meanwell CA, Hilton C et al (1989) Combination bleomycin, ifosfamide, and cisplatin chemotherapy in cervical cancer. J Natl Cancer Inst 81:359–361

    Article  CAS  Google Scholar 

  • Chao JI, Kuo PC, Hsu TS (2004) Down-regulation of survivin in nitric oxide induced cell growth inhibition and apoptosis of the human lung carcinoma cells. J Biol Chem 279:20267–20276

    Article  CAS  Google Scholar 

  • Christiansen S, Autschbach R (2006) Doxorubicin in experimental and clinical heart failure. Eur J Cardiothorac Surg 30:611–616

    Article  Google Scholar 

  • Cook NC, Samman S (1996) Flavonoids-chemistry, metabolism, cardioprotective effects, and dietary sources. Nutr Biochem 7:66–76

    Article  CAS  Google Scholar 

  • Das A, Chaudhuri D, Mandal N et al (2012) Study of antioxidant and reactive oxygen species scavenging activity of the edible tuber of “greater yam” (Dioscorea alata L.) from north-east India. Asian J Pharm Clin Res 5:74–84

    CAS  Google Scholar 

  • Elizabeth KM (2005) Antimicrobial activity of Terminalia bellerica. Indian J Clin Biochem 20:150–153

    Article  CAS  Google Scholar 

  • Fragkos M, Jurvansuu J, Beard P (2009) H2AX is required for cell cycle arrest via the p53/p21 pathway. Mol Cell Biol 29:2828–2840

    Article  CAS  Google Scholar 

  • Ghate NB, Chaudhuri D, Sarkar R et al (2013) An antioxidant extract of tropical lichen, Parmotrema reticulatum, induces cell cycle arrest and apoptosis in breast carcinoma cell line MCF-7. PLoS ONE 8:e82293. doi:10.1371/journal.pone.0082293

    Article  Google Scholar 

  • Ghate NB, Hazra B, Sarkar R et al (2014a) In vitro anticancer activity of Spondias pinnata bark on human lung and breast carcinoma. Cytotechnology 66:209–218

    Article  Google Scholar 

  • Ghate NB, Hazra B, Sarkar R et al (2014b) Alteration of Bax/Bcl-2 ratio contributes to Terminalia belerica induced apoptosis in human lung and breast carcinoma. In Vitro Cell Dev Biol Anim 50:527–537

    Article  CAS  Google Scholar 

  • Giaccone G, Herbst RS, Manegold C et al (2004) Gefitinib in combination with gemcitabine and cisplatin in advanced non–small-cell lung cancer: a phase III trial—INTACT 1. J Clin Oncol 2:777–784

    Article  Google Scholar 

  • Gokhale SB, Kokate CK, Purohit AP (2003) Pharmacognosy. Nirali Prakashan, Pune

    Google Scholar 

  • Halliwell B (1991) Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am J Med 91:S14–S22

    Article  Google Scholar 

  • Han YH, Park WH (2009) Growth inhibition in antimycin A treated-lung cancer Calu-6 cells via inducing a G1 phase arrest and apoptosis. Lung Cancer 65:150–160

    Article  Google Scholar 

  • Harbornen JB, Baxter H (1995) Phytochemical dictionary: a handbook of bioactive compounds from plants. Taylor and Francis, London

    Google Scholar 

  • Hazra B, Biswas S, Mandal N (2008) Antioxidant and free radical scavenging activity of Spondias pinnata. BMC Complement Altern Med 8:63. doi:10.1186/1472-6882-8-63

    Article  Google Scholar 

  • Hazra B, Sarkar R, Biswas S et al (2010) Comparative study of the antioxidant and reactive oxygen species scavenging properties in the extracts of the fruits of Terminalia chebula, Terminalia belerica and Emblica officinalis. BMC Complement Altern Med 10:20. doi:10.1186/1472-6882-10-20

    Article  Google Scholar 

  • Kang KH, Kim WH, Choi KH (1999) p21 promotes ceramide-induced apoptosis and antagonizes the antideath effect of Bcl-2 in human hepatocarcinoma cells. Exp Cell Res 253:403–412

    Article  CAS  Google Scholar 

  • Kao GD, McKenna WG, Yen TJ (2001) Detection of repair activity during the DNA damage-induced G2 delay in human cancer cells. Oncogene 20:3486–3496

    Article  CAS  Google Scholar 

  • Kochevar EI, Redmond WR (2000) Photosensitized production of singlet oxygen. Methods Enzymol 319:20–28

    Article  CAS  Google Scholar 

  • Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30:620–650

    Article  CAS  Google Scholar 

  • Kumudhavalli MV, Vyas M, Jayakar B (2010) Phytochemical and pharmacological evaluation of the plant fruit of Terminalia belerica Roxb. Int J Pharm Life Sci 1:1–11

    CAS  Google Scholar 

  • Lakin ND, Jackson SP (1999) Regulation of p53 in response to DNA damage. Oncogene 18:7644–7655

    Article  CAS  Google Scholar 

  • Levine A (1997) p53 the cellular gatekeeper for growth and division. Cell 88:323–331

    Article  CAS  Google Scholar 

  • Lin YJ, Liu YS, Yeh HH et al (2012) Selfassembled poly (e-caprolactone)-g-chondroitin sulfate copolymers as an intracellular doxorubicin delivery carrier against lung cancer cells. Int J Nanomed 7:4169–4183

    CAS  Google Scholar 

  • Lissi EA, Modak B, Torres R et al (1999) Total antioxidant potential of resinous exudates from Heliotropium species, and a comparison of the ABTS and DPPH methods. Free Rad Res 30:471–477

    Article  CAS  Google Scholar 

  • Lukas J, Lukas C, Bartek J (2004) Mammalian cell cycle checkpoints: signaling pathways and their organization in space and time. DNA Repair 3:997–1007

    Article  CAS  Google Scholar 

  • Moldovan GL, Pfander B, Jentsch S (2007) PCNA, the maestro of the replication fork. Cell 129:665–679

    Article  CAS  Google Scholar 

  • O’Loughlin C, Heenan M, Coyle S et al (2000) Altered cell cycle response of drug-resistant lung carcinoma cells to doxorubicin. Eur J Can 36:1149–1160

    Article  Google Scholar 

  • Rice-Evans CA, Miller NJ, Bolwell PG et al (1995) The relative antioxidant activities of plant-derived polyphenolic flavonoids. Free Rad Res 22:375–383

    Article  CAS  Google Scholar 

  • Roninson IB (2002) Oncogenic functions of tumour suppressor p21Waf1/Cip1/Sdi1: association with cell senescence and tumour-promoting activities of stromal fibroblasts. Cancer Lett 179:1–14

    Article  CAS  Google Scholar 

  • Saroya AS (2011) Herbalism phytochemistry and ethanopharmacology. Science Publishers, Enfield, pp 357–361

    Book  Google Scholar 

  • Stief TW (2003) The physiology and pharmacology of single oxygen. Med Hypotheses 60:567–572

    Article  CAS  Google Scholar 

  • Su D, Cheng Y, Liu M et al (2013) Comparision of piceid and resveratrol in antioxidation and antiproliferation activities in vitro. PLoS ONE 8:e54505. doi:10.1371/journal.pone.0054505

    Article  CAS  Google Scholar 

  • Tam K (2013) The roles of doxorubicin in hepatocellular carcinoma. ADMET DMPK 1:29–44

    Google Scholar 

  • Tyagi AK, Singh RP, Agarwal C et al (2002) Silibinin strongly synergizes human prostate carcinoma DU145 cells to doxorubicin-induced growth Inhibition, G2-M arrest, and apoptosis. Clin Can Res 8:3512–3519

    CAS  Google Scholar 

  • Tylor BS, Kion YM, Wang QI et al (1997) Nitric oxide down-regulates hepatocyte-inducible nitric oxide synthase gene expression. Arch Surg 132:1177–1183

    Article  Google Scholar 

  • Von Hoff DD, Layard MW, Basa P et al (1979) Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med 91:710–717

    Article  Google Scholar 

  • Yildirim A, Mavi A, Kara AA (2001) Determination of antioxidant and antimicrobial activities of Rumex crispus L. extracts. J Agric Food Chem 49:4083–4089

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to Mr. Ranjit Kumar Das, Mr. Pradip Kumar Mallik and Mr. Ranjan Dutta for their technical assistance.

Author information

Author notes

    Authors and Affiliations

    1. Division of Molecular Medicine, Bose Institute, P 1/12, C. I. T. Road, Scheme - VIIM, Kolkata, West Bengal, 700054, India

      Tapasree Basu, Sourav Panja, Nikhil Baban Ghate, Dipankar Chaudhuri & Nripendranath Mandal

    Authors
    1. Tapasree Basu
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Sourav Panja
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Nikhil Baban Ghate
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Dipankar Chaudhuri
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Nripendranath Mandal
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Nripendranath Mandal.

    Ethics declarations

    Conflict of interest

    Authors declared no conflict of interest.

    Additional information

    Tapasree Basu and Sourav Panja have contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Basu, T., Panja, S., Ghate, N.B. et al. Antioxidant and antiproliferative effects of different solvent fractions from Terminalia belerica Roxb. fruit on various cancer cells. Cytotechnology 69, 201–216 (2017). https://doi.org/10.1007/s10616-016-0051-6

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10616-016-0051-6

    Keywords

    Search

    Navigation