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Transgenerational Susceptibility to Food Addiction-Like Behavior in Rats Associates to a Decrease of the Anti-Inflammatory IL-10 in Plasma

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Abstract

Maternal nutritional programming by energy-dense foods leads to the transgenerational heritance of addiction-like behavior. Exposure to energy-dense foods also activates systemic and central inflammation in the offspring. This study aimed to characterize pro- and anti-inflammatory cytokine profiles in blood and their correlation to the transgenerational heritance of the addiction-like behavior in rats. F1 offspring of male Wistar diagnosed with addiction-like behavior were mated with virgin females to generate the F2 and the F3 offspring, respectively. Diagnosis of addiction-like behavior was performed by the operant training schedule (FR1, FR5 and PR) and pro- and anti-inflammatory cytokine profiles in blood were measured by multiplex platform. Multiple linear models between behavior, fetal programming by diet and pro- and anti-inflammatory cytokine profiles were performed. We found that the addiction-like behavior found in the F1 male offspring exposed to energy-dense food (cafeteria, CAF) diet during fetal programing is transgenerational inherited to the F2 and F3 generations. Blood from addiction-like behavior subjects of F2 and F3 generations exposed to CAF diet during maternal programming showed decrease in the anti-inflammatory IL-10 in the plasma. Conversely, decreased levels of the pro-inflammatory MCP-1 was identified in non-addiction-like subjects. No changes were found in plasmatic TNF-α levels in the F2 and F3 offspring of non-addiction-like and addiction-like subjects. Finally, biological modeling between IL-10 or MCP-1 plasma levels and prenatal diet exposure on operant training responses confirmed an association of decreased IL-10 levels on addiction-like behavior in the F2 and F3 generations. Globally, we identified decreased anti-inflammatory IL-10 cytokine in the blood of F2 and F3 offspring subjects diagnosed with addiction-like behavior for food rewards.

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Acknowledgements

This work was supported by the National Council of Science and Technology in Mexico (CONACYT) (Grant number: 255317), 708452 CONACYT for L. J. Montalvo-Martínez, 855559 CONACYT for G. Cruz-Carrillo, 573686 CONACYT for R. Maldonado-Ruiz, 650620 CONACYT for M. Cárdenas-Tueme, 781759 CONACYT for L.A. Trujillo-Villarreal. and IBRO-LARC 2020 for Alberto Camacho-Morales.

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Authors and Affiliations

  1. Department of Biochemistry, College of Medicine, Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Monterrey, NL, Mexico

    Larisa Montalvo-Martínez, Gabriela Cruz-Carrillo, Roger Maldonado-Ruiz, Luis A. Trujillo-Villarreal & Alberto Camacho-Morales

  2. Neurometabolism Unit, Center for Research and Development in Health Sciences, Universidad Autónoma de Nuevo León, Monterrey, NL, Mexico

    Larisa Montalvo-Martínez, Gabriela Cruz-Carrillo, Roger Maldonado-Ruiz, Luis A. Trujillo-Villarreal & Alberto Camacho-Morales

  3. Institute for Obesity Research. Escuela de Medicina y Ciencias de la Salud, Instituto Tecnológico de Estudios Superiores Monterrey, Monterrey, NL, Mexico

    Marcela Cardenas-Tueme & Rocío Ortiz-López

  4. Centro de Investigaciones Biomédicas, Universidad Veracruzana, Xalapa, Mexico

    Rubí Viveros-Contreras

  5. Departamento de Bioquímica, Facultad de Medicina, Universidad Autonoma de Nuevo Leon, Madero y Dr. Aguirre Pequeño. Col. Mitras Centro, S/N, C.P. 64460, Monterrey, NL, Mexico

    Alberto Camacho-Morales

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  1. Larisa Montalvo-Martínez
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Montalvo-Martínez, L., Cruz-Carrillo, G., Maldonado-Ruiz, R. et al. Transgenerational Susceptibility to Food Addiction-Like Behavior in Rats Associates to a Decrease of the Anti-Inflammatory IL-10 in Plasma. Neurochem Res 47, 3093–3103 (2022). https://doi.org/10.1007/s11064-022-03660-7

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