Abstract
Background and Aim
The importance of earthworm in treatment of various diseases has been proven in ancient literatures. Nowadays, with advances in biotechnology, earthworm is considered a rich natural source of many biomolecules that possesses antioxidant and antitumor activities. The present study aimed to evaluate the antitumor activity of earthworm powder (Lumbricus terrestris) against two cell lines, breast cancer cells (MCF-7) and prostate cancer cells (PC-3).
Methods
Fully matured earthworms (L. terrestris) were collected from soil in Baghdad, Iraq. To assess the cytotoxicity of earthworm powder, the MTT assay was conducted on cancerous (MCF-7 and PC-3 cells) and normal cell line (WRL68 cells) lines.
Results
It was revealed that earthworm powder exerts cytotoxic effects against two cancer cell lines. The viability of MCF-7 and PC-3 cells decreased with increasing the concentration. The IC50 values for PC-3 and MCF-7 cell lines were 265.5 and 965.9 μg/ml, respectively, while the earthworm powder exhibited no cytotoxicity against the WRL68 cells. According to the analysis of the results of the multiple cytotoxicity assay (HCS), the treatment of PC-3 cells with 100, 200, and 400 μg/ml of earthworm powder for 24 h at 37 °C led to cell death by changing the permeability of mitochondrial membrane resulting in cytochrome C release and inducing apoptosis.
Conclusion
The results of the present study contribute additional evidence for the antitumor activity of earthworm extracts. Therefore, further research should concentrate on isolating and identifying the earthworm’s active biomolecules that have antitumor activity by investigating the molecular mechanism, genetics, and pathways responsible for the antitumor activity of these biomolecules.
Similar content being viewed by others
References
Organization WH. Global Health estimates 2016: deaths by cause, age, sex, by country and by region, 2000–2016. Geneva: World Health Organization; 2018.
Obeyed HH, Ibrahim RHKM, Abdo-Alkareem RM, Hasan AH, Nasser LM, et al Annual report: Iraqi cancer registry 2015. Republic of Iraq/ Ministry of health/Iraqi Cancer Board; 2018.
Udensi UK, Tchounwou PB. Dual effect of oxidative stress on leukemia cancer induction and treatment. J Exp Clin Cancer Res. 2014;33:106.
Hong C, Takahashi S, Imamura M, Okutani E, Zhang Z-G, Chayama K, et al. Earthworm fibrinolytic enzyme: anti-tumor activity on human hepatoma cellsin vitroandin vivo. Chin Med J. 2007;120:898–904.
Augustine D, Rao RS, Anbu J, Murthy KC. Anticancer prospects of earthworm extracts: a systematic review of in vitro and in vivo studies. Pharmacogn Rev. 2018;12:46.
Zhang S, Tian Q, Wang K, Xu D. Radioenhancement effect of radiotherapy combined with earthworm capsule in the treatment of esophagus and lung carcinoma. Journal of the Fourth Military Medical University. 1992;13:165–8.
Zhang W, Li L, Mao H. The clinical observation of lymphoma and lung cancer treated with chemical drugs and 912. Chin J Clin Oncol. 1991;18:181–2.
Blakemore R An updated list of valid, invalid and synonymous names of Criodriloidea and Lumbricoidea (Annelida: Oligochaeta: Criodrilidae, Sparganophilidae, Ailoscolecidae, Hormogastridae, Lumbricidae, Lutodrilidae). A series of searchable texts on earthworm biodiversity, ecology and systematics from various regions of the world-supplemental. CD publication under ICZN (1999: Art. 8) also presented online http://www.annelida.net/earthworm/Accessed Oct 2012 2008.
Andleeb S, Ejaz M, Awan UA, Ali S, Kiyani A, Shafique I, et al. In vitro screening of mucus and solvent extracts of Eisenia foetida against human bacterial and fungal pathogens. Pak J Pharm Sci 2016,29.
Byrne F, Prina-Mello A, Whelan A, Mohamed BM, Davies A, Gun’ko YK, et al. High content analysis of the biocompatibility of nickel nanowires. J Magn Magn Mater. 2009;321:1341–5.
Augustine D, Rao RS, Anbu J, Murthy KC. In vitro antiproliferative effect of earthworm coelomic fluid of Eudrilus eugeniae, Eisenia foetida, and Perionyx excavatus on squamous cell carcinoma-9 cell line: a pilot study. Pharm Res. 2017;9:S61.
Augustine D, Rao RS, Jayaraman A, Murthy KC. Anti-proliferative activity of earthworm coelomic fluid using oral squamous carcinoma KB 3-1 cells: an in vitro study with serine protease analysis. Pharmacogn Mag. 2018;14:528.
Fiołka MJ, Czaplewska P, Macur K, Buchwald T, Kutkowska J, Paduch R, et al. Anti-Candida albicans effect of the protein-carbohydrate fraction obtained from the coelomic fluid of earthworm Dendrobaena veneta. PLoS One. 2019;14:e0212869.
Renz A, Berdel WE, Kreuter M, Belka C, Schulze-Osthoff K, Los M. Rapid extracellular release of cytochrome c is specific for apoptosis and marks cell death in vivo. Blood. 2001;98:1542–8.
Cooper EL, Balamurugan M, Huang C-Y, Tsao CR, Heredia J, Tommaseo-Ponzetta M, et al. Earthworms dilong: ancient, inexpensive, noncontroversial models may help clarify approaches to integrated medicine emphasizing neuroimmune systems. Evid Based Complement Alternat Med. 2012;2012:1–11.
MATEJKO S, POCHEĆ E, HOMA J. Earthworms as a source of bioactive molecules: antitumor properties of the earthworm proteins. KOSMOS. 2016;65:23–32.
Liu C, Chen X, Pan Y, Liang H, Song S, Ji A. Antitumor studies of earthworm fibrinolytic enzyme component a from Eisenia foetida on breast cancer cell line MCF-7. Indian J Pharm Sci. 2017;79:361–8.
Augustine D, Rao RS, Anbu J, Murthy KC. In vitro cytotoxic and apoptotic induction effect of earthworm coelomic fluid of Eudrilus eugeniae, Eisenia foetida, and Perionyx excavatus on human oral squamous cell carcinoma-9 cell line. Toxicol Rep. 2019;6:347–57.
Yang Y, Yang L, You Q-D, Nie F-F, Gu H-Y, Zhao L, et al. Differential apoptotic induction of gambogic acid, a novel anticancer natural product, on hepatoma cells and normal hepatocytes. Cancer Lett. 2007;256:259–66.
Tiwari M. The role of serratiopeptidase in the resolution of inflammation. Asian J Pharm Sci 2017;12:209–15.
Engelmann P, Kiss J, Csöngei V, Cooper E, Németh P. Earthworm leukocytes kill HeLa, HEp-2, PC-12 and PA317 cells in vitro. J Biochem Biophys Methods. 2004;61:215–27.
Acknowledgments
This study was supported by Department of Biology, College of Science, Mustansiriyah University, Baghdad, Iraq.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This study was ethically approved by the College of Science, Mustansiriyah University, Baghdad, Iraq.
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Shafi, F.A., Faleh, N. Anticancer Activity of Earthworm Powder (Lumbricus terrestris) Against MCF-7 and PC-3 Cancer Cell Lines. J Gastrointest Canc 50, 919–925 (2019). https://doi.org/10.1007/s12029-019-00268-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12029-019-00268-z