Curcumin Stimulates the Overexpression of Virulence Factors in <i>Salmonella enterica</i> Serovar Typhimurium: In Vitro and Animal Model Studies

<i>Salmonella</i> spp. is one of the most common food poisoning pathogens and the main cause of diarrheal diseases in humans in developing countries. The increased <i>Salmonella</i> resistance to antimicrobials has led to the search for new alternatives, including natural com...

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Main Authors: Martin Zermeño-Ruiz, Itzia A. Rangel-Castañeda, Daniel Osmar Suárez-Rico, Leonardo Hernández-Hernández, Rafael Cortés-Zárate, José M. Hernández-Hernández, Gabriela Camargo-Hernández, Araceli Castillo-Romero
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Antibiotics
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Online Access:https://www.mdpi.com/2079-6382/11/9/1230
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author Martin Zermeño-Ruiz
Itzia A. Rangel-Castañeda
Daniel Osmar Suárez-Rico
Leonardo Hernández-Hernández
Rafael Cortés-Zárate
José M. Hernández-Hernández
Gabriela Camargo-Hernández
Araceli Castillo-Romero
author_facet Martin Zermeño-Ruiz
Itzia A. Rangel-Castañeda
Daniel Osmar Suárez-Rico
Leonardo Hernández-Hernández
Rafael Cortés-Zárate
José M. Hernández-Hernández
Gabriela Camargo-Hernández
Araceli Castillo-Romero
author_sort Martin Zermeño-Ruiz
collection DOAJ
description <i>Salmonella</i> spp. is one of the most common food poisoning pathogens and the main cause of diarrheal diseases in humans in developing countries. The increased <i>Salmonella</i> resistance to antimicrobials has led to the search for new alternatives, including natural compounds such as curcumin, which has already demonstrated a bactericidal effect; however, in Gram-negatives, there is much controversy about this effect, as it is highly variable. In this study, we aimed to verify the antibacterial activity of curcumin against the <i>Salmonella enterica</i> serovar Typhimurium growth rate, virulence, and pathogenicity. The strain was exposed to 110, 220 or 330 µg/mL curcumin, and by complementary methods (spectrophotometric, pour plate and MTT assays), we determined its antibacterial activity. To elucidate whether curcumin regulates the expression of virulence genes, <i>Salmonella</i> <i>invA</i>, <i>fliC</i> and <i>siiE</i> genes were investigated by quantitative real-time reverse transcription (qRT-PCR). Furthermore, to explore the effect of curcumin on the pathogenesis process in vivo, a <i>Caenorhabditis elegans</i> infection model was employed. No antibacterial activity was observed, even at higher concentrations of curcumin. All concentrations of curcumin caused overgrowth (35–69%) and increased the pathogenicity of the bacterial strain through the overexpression of virulence factors. The latter coincided with a significant reduction in both the lifespan and survival time of <i>C. elegans</i> when fed with curcumin-treated bacteria. Our data provide relevant information that may support the selective antibacterial effects of curcumin to reconsider the indiscriminate use of this phytochemical, especially in outbreaks of pathogenic Gram-negative bacteria.
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spelling doaj.art-b58589c2af5d4cda903203237bd322b12023-11-23T14:45:15ZengMDPI AGAntibiotics2079-63822022-09-01119123010.3390/antibiotics11091230Curcumin Stimulates the Overexpression of Virulence Factors in <i>Salmonella enterica</i> Serovar Typhimurium: In Vitro and Animal Model StudiesMartin Zermeño-Ruiz0Itzia A. Rangel-Castañeda1Daniel Osmar Suárez-Rico2Leonardo Hernández-Hernández3Rafael Cortés-Zárate4José M. Hernández-Hernández5Gabriela Camargo-Hernández6Araceli Castillo-Romero7Departamento de Microbiología y Patología, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Calle Sierra Mojada 950, Independencia Oriente, Guadalajara 44100, MexicoCentro de Investigación y Estudios Avanzados del Instituto Politécnico Nacional, Ciudad de México 07360, MexicoDepartamento de Fisiología, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Calle Sierra Mojada 950, Independencia Oriente, Guadalajara 44100, MexicoDepartamento de Fisiología, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Calle Sierra Mojada 950, Independencia Oriente, Guadalajara 44100, MexicoDepartamento de Microbiología y Patología, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Calle Sierra Mojada 950, Independencia Oriente, Guadalajara 44100, MexicoCentro de Investigación y Estudios Avanzados del Instituto Politécnico Nacional, Ciudad de México 07360, MexicoDepartamento de Ciencias de la Salud, Centro Universitario de los Altos, Universidad de Guadalajara, Av. Rafael Casillas Aceves No. 1200, Tepatitlán de Morelos 44100, MexicoDepartamento de Microbiología y Patología, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Calle Sierra Mojada 950, Independencia Oriente, Guadalajara 44100, Mexico<i>Salmonella</i> spp. is one of the most common food poisoning pathogens and the main cause of diarrheal diseases in humans in developing countries. The increased <i>Salmonella</i> resistance to antimicrobials has led to the search for new alternatives, including natural compounds such as curcumin, which has already demonstrated a bactericidal effect; however, in Gram-negatives, there is much controversy about this effect, as it is highly variable. In this study, we aimed to verify the antibacterial activity of curcumin against the <i>Salmonella enterica</i> serovar Typhimurium growth rate, virulence, and pathogenicity. The strain was exposed to 110, 220 or 330 µg/mL curcumin, and by complementary methods (spectrophotometric, pour plate and MTT assays), we determined its antibacterial activity. To elucidate whether curcumin regulates the expression of virulence genes, <i>Salmonella</i> <i>invA</i>, <i>fliC</i> and <i>siiE</i> genes were investigated by quantitative real-time reverse transcription (qRT-PCR). Furthermore, to explore the effect of curcumin on the pathogenesis process in vivo, a <i>Caenorhabditis elegans</i> infection model was employed. No antibacterial activity was observed, even at higher concentrations of curcumin. All concentrations of curcumin caused overgrowth (35–69%) and increased the pathogenicity of the bacterial strain through the overexpression of virulence factors. The latter coincided with a significant reduction in both the lifespan and survival time of <i>C. elegans</i> when fed with curcumin-treated bacteria. Our data provide relevant information that may support the selective antibacterial effects of curcumin to reconsider the indiscriminate use of this phytochemical, especially in outbreaks of pathogenic Gram-negative bacteria.https://www.mdpi.com/2079-6382/11/9/1230<i>Salmonella enterica</i> serovar Typhimuriumcurcuminantibacterial activitypathogenicity<i>C. elegans</i>
spellingShingle Martin Zermeño-Ruiz
Itzia A. Rangel-Castañeda
Daniel Osmar Suárez-Rico
Leonardo Hernández-Hernández
Rafael Cortés-Zárate
José M. Hernández-Hernández
Gabriela Camargo-Hernández
Araceli Castillo-Romero
Curcumin Stimulates the Overexpression of Virulence Factors in <i>Salmonella enterica</i> Serovar Typhimurium: In Vitro and Animal Model Studies
Antibiotics
<i>Salmonella enterica</i> serovar Typhimurium
curcumin
antibacterial activity
pathogenicity
<i>C. elegans</i>
title Curcumin Stimulates the Overexpression of Virulence Factors in <i>Salmonella enterica</i> Serovar Typhimurium: In Vitro and Animal Model Studies
title_full Curcumin Stimulates the Overexpression of Virulence Factors in <i>Salmonella enterica</i> Serovar Typhimurium: In Vitro and Animal Model Studies
title_fullStr Curcumin Stimulates the Overexpression of Virulence Factors in <i>Salmonella enterica</i> Serovar Typhimurium: In Vitro and Animal Model Studies
title_full_unstemmed Curcumin Stimulates the Overexpression of Virulence Factors in <i>Salmonella enterica</i> Serovar Typhimurium: In Vitro and Animal Model Studies
title_short Curcumin Stimulates the Overexpression of Virulence Factors in <i>Salmonella enterica</i> Serovar Typhimurium: In Vitro and Animal Model Studies
title_sort curcumin stimulates the overexpression of virulence factors in i salmonella enterica i serovar typhimurium in vitro and animal model studies
topic <i>Salmonella enterica</i> serovar Typhimurium
curcumin
antibacterial activity
pathogenicity
<i>C. elegans</i>
url https://www.mdpi.com/2079-6382/11/9/1230
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