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

• Published in: Neurochemical research Vol. 47; no. 10; pp. 3093 - 3103
• Main Authors: Montalvo-Martínez, Larisa, Cruz-Carrillo, Gabriela, Maldonado-Ruiz, Roger, Trujillo-Villarreal, Luis A., Cardenas-Tueme, Marcela, Viveros-Contreras, Rubí, Ortiz-López, Rocío, Camacho-Morales, Alberto
• Format: Journal Article
• Language: English
• Published: New York Springer US 01.10.2022; Springer Nature B.V
• Subjects: Addictions; Biochemistry; Biomedical and Life Sciences; Biomedicine; Blood; Cell Biology; Cytokines; Diet; Energy; Exposure; Fetuses; Food; Inflammation; Interleukin 10; Males; Monocyte chemoattractant protein 1; Neurochemistry; Neurology; Neurosciences; Offspring; Operant conditioning; Original Paper; Plasma levels; Prenatal experience; Programming; Reinforcement; Training; Tumor necrosis factor-α; MCP-1; intergenerational heritance; Food addiction; Fetal programming; IL-10
• ISSN: 0364-3190; 1573-6903
• DOI: 10.1007/s11064-022-03660-7

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.