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Moringa oleifera extract promotes apoptosis-like death in Toxoplasma gondii tachyzoites in vitro

Published online by Cambridge University Press:  30 June 2021

Letícia Nishi Open the ORCID record for Letícia Nishi [Opens in a new window] ,
Raquel Arruda da Silva Sanfelice Open the ORCID record for Raquel Arruda da Silva Sanfelice [Opens in a new window] ,
Bruna Taciane da Silva Bortoleti ,
Fernanda Tomiotto-Pellissier Open the ORCID record for Fernanda Tomiotto-Pellissier [Opens in a new window] ,
Taylon Felipe Silva ,
Fernanda Ferreira Evangelista Open the ORCID record for Fernanda Ferreira Evangelista [Opens in a new window] ,
Danielle Lazarin-Bidóia ,
Idessania Nazareth Costa Open the ORCID record for Idessania Nazareth Costa [Opens in a new window] ,
Wander Rogério Pavanelli  and
Ivete Conchon Costa
...Show all authors
Letícia Nishi
Affiliation:
Graduate Program in Health Science, State University of Maringá, Colombo Avenue, 5790, Zip Code 87020-900, Maringá, Paraná, Brazil
Raquel Arruda da Silva Sanfelice
Affiliation:
Department of Pathological Sciences, Laboratory of Immunoparasitology of Neglected Diseases and Cancer – LIDNC, Center of Biological Sciences, State University of Londrina, Rodovia Celso Garcia Cid Campus, Zip Code 86057-970, Postal box 10.011, Londrina, Paraná, Brazil
Bruna Taciane da Silva Bortoleti
Affiliation:
Department of Pathological Sciences, Laboratory of Immunoparasitology of Neglected Diseases and Cancer – LIDNC, Center of Biological Sciences, State University of Londrina, Rodovia Celso Garcia Cid Campus, Zip Code 86057-970, Postal box 10.011, Londrina, Paraná, Brazil Biosciences and Biotechnology Postgraduate Program, Carlos Chagas Institute (ICC/Fiocruz-PR), Curitiba, Paraná, Brazil
Fernanda Tomiotto-Pellissier
Affiliation:
Department of Pathological Sciences, Laboratory of Immunoparasitology of Neglected Diseases and Cancer – LIDNC, Center of Biological Sciences, State University of Londrina, Rodovia Celso Garcia Cid Campus, Zip Code 86057-970, Postal box 10.011, Londrina, Paraná, Brazil Biosciences and Biotechnology Postgraduate Program, Carlos Chagas Institute (ICC/Fiocruz-PR), Curitiba, Paraná, Brazil
Taylon Felipe Silva
Affiliation:
Department of Pathological Sciences, Laboratory of Immunoparasitology of Neglected Diseases and Cancer – LIDNC, Center of Biological Sciences, State University of Londrina, Rodovia Celso Garcia Cid Campus, Zip Code 86057-970, Postal box 10.011, Londrina, Paraná, Brazil
Fernanda Ferreira Evangelista
Affiliation:
Graduate Program in Health Science, State University of Maringá, Colombo Avenue, 5790, Zip Code 87020-900, Maringá, Paraná, Brazil
Danielle Lazarin-Bidóia
Affiliation:
Department of Pathological Sciences, Laboratory of Immunoparasitology of Neglected Diseases and Cancer – LIDNC, Center of Biological Sciences, State University of Londrina, Rodovia Celso Garcia Cid Campus, Zip Code 86057-970, Postal box 10.011, Londrina, Paraná, Brazil
Idessania Nazareth Costa
Affiliation:
Department of Pathological Sciences, Laboratory of Immunoparasitology of Neglected Diseases and Cancer – LIDNC, Center of Biological Sciences, State University of Londrina, Rodovia Celso Garcia Cid Campus, Zip Code 86057-970, Postal box 10.011, Londrina, Paraná, Brazil
Wander Rogério Pavanelli
Affiliation:
Department of Pathological Sciences, Laboratory of Immunoparasitology of Neglected Diseases and Cancer – LIDNC, Center of Biological Sciences, State University of Londrina, Rodovia Celso Garcia Cid Campus, Zip Code 86057-970, Postal box 10.011, Londrina, Paraná, Brazil
Ivete Conchon Costa
Affiliation:
Department of Pathological Sciences, Laboratory of Immunoparasitology of Neglected Diseases and Cancer – LIDNC, Center of Biological Sciences, State University of Londrina, Rodovia Celso Garcia Cid Campus, Zip Code 86057-970, Postal box 10.011, Londrina, Paraná, Brazil
Aline Takaoka Alves Baptista
Affiliation:
Departament of Food and Chemical Engineering, Federal University of Technology – Paraná – UTFPR, Câmpus Campo Mourão, Via Rosalina Maria Dos Santos, 1233, Zip Code 87301-899, Campo Mourão, Paraná, Brazil
Rosângela Bergamasco
Affiliation:
Department of Chemical Engineering, State University of Maringa, Colombo Avenue, 5790, Zip Code 87020-900, Maringá, Paraná, Brazil
Ana Lúcia Falavigna-Guilherme*
Affiliation:
Graduate Program in Health Science, State University of Maringá, Colombo Avenue, 5790, Zip Code 87020-900, Maringá, Paraná, Brazil
*
Author for correspondence: Ana Lúcia Falavigna-Guilherme, E-mail: [email protected]
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Abstract

Toxoplasma gondii is the causative agent of toxoplasmosis, and an important problem of public health. The current treatment for toxoplasmosis is the combination of pyrimethamine and sulphadiazine, which do not act in the chronic phase of toxoplasmosis and have several side-effects. This study evaluated the anti-T. gondii activity and potential mechanism of Moringa oleifera seeds’ aqueous extract in vitro. The concentration of M. oleifera extract in HeLa cells was determined by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide cell viability assays. The presence of T. gondii was assessed by quantitative polymerase chain reaction and toluidine blue staining. Pyrimethamine and sulphadiazine were used as drug controls. Modifications in T. gondii morphology and ultrastructure were observed by electron microscopy. In vitro, the M. oleifera extract had no toxic effect on HeLa cells at concentrations below 50 μg mL−1. Moringa oleifera extract inhibits T. gondii invasion and intracellular proliferation with similar results for sulphadiazine + pyrimethamine, and also shows cellular nitric oxide production at a concentration of 30 μg mL−1. Electron microscopy analyses indicated structural and ultrastructural modifications in tachyzoites after treatment. We also observed an increase in reactive oxygen species production and a loss of mitochondrial membrane integrity. Nile Red staining assays demonstrated a lipid accumulation. Annexin V–fluorescein isothiocyanate and propidium iodide staining demonstrated that the main action of M. oleifera extract in T. gondii tachyzoites was compatible with late apoptosis. In conclusion, M. oleifera extract has anti-T. gondii activity in vitro and might be a promising substance for the development of a new anti-T. gondii drug.

Keywords

HeLa cellsmechanism of actionplant extracttoxoplasmosis
Type
Research Article
Information
Parasitology , Volume 148 , Issue 12 , October 2021 , pp. 1447 - 1457
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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