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Synbiotic VSL#3 and yacon-based product modulate the intestinal microbiota and prevent the development of pre-neoplastic lesions in a colorectal carcinogenesis model

  • Genomics, transcriptomics, proteomics
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Abstract

Colorectal cancer is a public health problem, with dysbiosis being one of the risk factors due to its role in intestinal inflammation. Probiotics and synbiotics have been used in order to restore the microbiota balance and to prevent colorectal carcinogenesis. We aimed to investigate the effects of the probiotic VSL#3® alone or in combination with a yacon-based prebiotic concentrate on the microbiota modulation and its influence on colorectal carcinogenesis in an animal model. C57BL/6J mice were divided into three groups: control (control diet), probiotic (control diet + VSL#3®), and synbiotic (yacon diet + VSL#3®). The diets were provided for 13 weeks and, from the third one, all animals were subjected to induction of colorectal cancer precursor lesions. Stool samples were collected to evaluate organic acids, feces pH, β-glucuronidase activity, and microbiota composition. The colon was used to count pre-neoplastic lesions and to determine the cytokines. The microbiota composition was influenced by the use of probiotic and synbiotic. Modifications were also observed in the abundance of bacterial genera with respect to the control group, which confirms the interference of carcinogenesis in the microbiota. Pre-neoplastic lesions were reduced by the use of the synbiotic, but not with the probiotic. The protection provided by the synbiotic can be attributed to the modulation of the intestinal inflammatory response, to the inhibition of a pro-carcinogenic enzyme, and to the production of organic acids. The modulation of the composition and activity of the microbiota contributed to beneficial changes in the intestinal microenvironment, which led to a reduction in carcinogenesis.

Key points

• Synbiotic reduces the incidence of colorectal cancer precursor lesions.

• Synbiotic modulates the composition and activity of intestinal microbiota.

• Synbiotic increases the abundance of butyrate-producing bacteria.

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Acknowledgments

Our work was supported by the National Council of Technological and Scientific Development (CNPq), Coordination for the Improvement of Higher Education Personnel (CAPES), and Foundation for the Support to the Researches in Minas Gerais (Fapemig).

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Authors and Affiliations

  1. Nutritional Biochemistry Laboratory, Department of Nutrition and Health, Universidade Federal de Viçosa, Avenida P. H. Rolfs, Campus Universitário S/N, Viçosa, Minas Gerais, CEP: 36570-900, Brazil

    Bruna Cristina dos Santos Cruz & Maria do Carmo Gouveia Peluzio

  2. Department of Agronomy, Food, Natural Resources, Animals and Environment (DAFNAE), University of Padova, Legnaro, Italy

    Vinícius da Silva Duarte, Alessio Giacomini & Viviana Corich

  3. Immunovirology Laboratory, Department of Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil

    Sérgio Oliveira de Paula

  4. Biochemical Analysis Laboratory, Department of Biochemistry and Molecular Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil

    Lilian da Silva Fialho

  5. Biochemical Analysis Laboratory, Department of Biochemistry and Molecular Biology, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil

    Valéria Monteze Guimarães

  6. Institute of Biotechnology Applied to Agriculture & Livestock (Bioagro), Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil

    Célia Lúcia de Luces Fortes Ferreira

Authors
  1. Bruna Cristina dos Santos Cruz
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  2. Vinícius da Silva Duarte
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  3. Alessio Giacomini
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  4. Viviana Corich
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  5. Sérgio Oliveira de Paula
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  6. Lilian da Silva Fialho
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  7. Valéria Monteze Guimarães
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  8. Célia Lúcia de Luces Fortes Ferreira
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  9. Maria do Carmo Gouveia Peluzio
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Contributions

BCSC, MCGP, and CLLFF conceived and designed the research. BCSC, VSD, and LSF conducted the experiments. AG, VC, VMG, SOP, and MCGP contributed new reagents or analytical tools. BCSC, VSD, and LSF analyzed data. BCSC wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Bruna Cristina dos Santos Cruz.

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Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All experimental protocols were approved by the Ethics Committee in Animal Experimentation of the Federal University of Viçosa (n° 08/2017, date of approval: May 09, 2017), under the guidelines of the European Community (Directive 2010/63/EU).

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dos Santos Cruz, B.C., da Silva Duarte, V., Giacomini, A. et al. Synbiotic VSL#3 and yacon-based product modulate the intestinal microbiota and prevent the development of pre-neoplastic lesions in a colorectal carcinogenesis model. Appl Microbiol Biotechnol 104, 8837–8857 (2020). https://doi.org/10.1007/s00253-020-10863-x

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