Maternal high-fat diet increases anhedonic behavior and modulates hippocampal Mash1 and BDNF expression in adult offspring

Curi, Haidar Tafner; Dias, Clarissa Tavares; Camargo, Maria Laura Monteiro da Luz; Gomez, Paula dos Santos; Gomes, Moisés Felipe Pereira; Beserra-Filho, José Ivo Araújo; Medeiros, Alessandra; Ribeiro, Alessandra Mussi; Simabuco, Fernando Moreira; Lambertucci, Rafael Herling; Mendes‐da‐Silva, Cristiano

doi:10.1016/j.neulet.2021.136239

Cited by 10 publications

(3 citation statements)

References 29 publications

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“…Sasaki et al [28,29] also found reduced anxiety in adolescent rats with perinatal HFD exposure, whereas adult rats exhibited increased anxiety. Curi et al [59] showed that maternal HFD increased anhedonic behaviour in male mice offspring, as indicated by decreased sucrose preference, and reduced anxiety-like behaviour in the EPM, compared to offspring born to chow dams. Thus, our data are in line with previous literature and suggest that maternal obesity tends to reduce anxiety in offspring, though effects may be sex-or age-dependent.…”

Section: Discussionmentioning

confidence: 99%

Male Rat Offspring Are More Impacted by Maternal Obesity Induced by Cafeteria Diet than Females—Additive Effect of Postweaning Diet

Tajaddini

Kendig

Prates

et al. 2022

IJMS

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Maternal obesity increases the risk of health complications in offspring, but whether these effects are exacerbated by offspring exposure to unhealthy diets warrants further investigation. Female Sprague-Dawley rats were fed either standard chow (n = 15) or ‘cafeteria’ (Caf, n = 21) diets across pre-pregnancy, gestation, and lactation. Male and female offspring were weaned onto chow or Caf diet (2–3/sex/litter), forming four groups; behavioural and metabolic parameters were assessed. At weaning, offspring from Caf dams were smaller and lighter, but had more retroperitoneal (RP) fat, with a larger effect in males. Maternal Caf diet significantly increased relative expression of ACACA and Fasn in male and female weanling liver, but not CPT-1, SREBP and PGC1; PPARα was increased in males from Caf dams. Maternal obesity enhanced the impact of postweaning Caf exposure on adult body weight, RP fat, liver mass, and plasma leptin in males but not females. Offspring from Caf dams appeared to exhibit reduced anxiety-like behaviour on the elevated plus maze. Hepatic CPT-1 expression was reduced only in adult males from Caf fed dams. Post weaning Caf diet consumption did not alter liver gene expression in the adult offspring. Maternal obesity exacerbated the obesogenic phenotype produced by postweaning Caf diet in male, but not female offspring. Thus, the impact of maternal obesity on adiposity and liver gene expression appeared more marked in males. Our data underline the sex-specific detrimental effects of maternal obesity on offspring.

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Section: Discussionmentioning

confidence: 99%

Male Rat Offspring Are More Impacted by Maternal Obesity Induced by Cafeteria Diet than Females—Additive Effect of Postweaning Diet

Tajaddini

Kendig

Prates

et al. 2022

IJMS

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show abstract

“… 88 , 89 Consistent with our findings, recent research has observed reduced BDNF levels in the offspring of obese HFD-fed mothers, suggesting that these changes may be due to a decrease in Serotonin (5HT1A), and with a possible impact on hippocampal neurogenesis. 20 These changes in BNDF and PSD95 could suggest an altered synaptic function in the hippocampus and possibly spatial learning, synaptic function, and cognitive function.…”

Section: Discussionmentioning

confidence: 99%

Preimplantation or gestation/lactation high-fat diet alters adult offspring metabolism and neurogenesis

Ojeda

Hutton

Hopkins

et al. 2023

Brain Communications

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Poor maternal nutrition during pregnancy is known to impair fetal development. Moreover, the preimplantation period is vulnerable to adverse programming of disease. Here, we investigated the effect of mouse maternal high-fat diet in healthy non-obese dams during preimplantation or throughout pregnancy and lactation on metabolism-related parameters and hippocampal neurogenesis in adult offspring. Female mice were fed from conception either a normal fat diet (Normal Fat Diet group) or high-fat diet throughout gestation and lactation (High-Fat Diet group), or high-fat diet only during preimplantation (Embryonic High-Fat Diet group, high-fat diet up to E3.5, normal fat diet thereafter). Maternal high-fat diet caused changes in the offspring, including increased systolic blood pressure, diurnal activity, respiratory quotient, and energy expenditure in High-Fat Diet females, and increased systolic blood pressure and respiratory quotient but decreased energy expenditure in High-Fat Diet males. High-Fat Diet males had a higher density of newborn neurons and a lower density of mature neurons in the dentate gyrus, indicating that exposure to a maternal high-fat diet may regulate adult neurogenesis. Maternal high-fat diet also increased the density of astrocytes and microglia in the hippocampus of High-Fat Diet males and females. Generally, a graded response (Normal Fat Diet < Embryonic High-Fat < High-Fat Diet) was observed, with only 3 days of high-fat diet exposure altering offspring energy metabolism and hippocampal cell density. Thus, early maternal exposure to a fatty diet, well before neural differentiation begins and independently of maternal obesity, is sufficient to perturb offspring energy metabolism and brain physiology with lifetime consequences.

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“…Maternal overfeeding during pregnancy and/or lactation greatly impacts adult neurogenesis in offspring (Niculescu and Lupu, 2009;Tozuka et al, 2009;Lépinay et al, 2015;Xavier et al, 2021). In this sense, consumption of a HFD during pregnancy leads to longterm effects in the central nervous system of the offspring, affecting neurogenesis-related pathways (Mash1 and BDNF) which correlated with the development of anhedonic-like behavior in the adulthood (Curi et al, 2021). Furthermore, perinatal exposure to HFD sensitizes the offspring to the adverse effects of postnatal highfat intake on hippocampal function.…”

Section: Effect Of Maternal Diet On Offspring Ahnmentioning

confidence: 99%

Nutrition and adult neurogenesis in the hippocampus: Does what you eat help you remember?

et al. 2023

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Neurogenesis is a complex process by which neural progenitor cells (NPCs)/neural stem cells (NSCs) proliferate and differentiate into new neurons and other brain cells. In adulthood, the hippocampus is one of the areas with more neurogenesis activity, which is involved in the modulation of both emotional and cognitive hippocampal functions. This complex process is affected by many intrinsic and extrinsic factors, including nutrition. In this regard, preclinical studies performed in rats and mice demonstrate that high fats and/or sugars diets have a negative effect on adult hippocampal neurogenesis (AHN). In contrast, diets enriched with bioactive compounds, such as polyunsaturated fatty acids and polyphenols, as well as intermittent fasting or caloric restriction, can induce AHN. Interestingly, there is also growing evidence demonstrating that offspring AHN can be affected by maternal nutrition in the perinatal period. Therefore, nutritional interventions from early stages and throughout life are a promising perspective to alleviate neurodegenerative diseases by stimulating neurogenesis. The underlying mechanisms by which nutrients and dietary factors affect AHN are still being studied. Interestingly, recent evidence suggests that additional peripheral mediators may be involved. In this sense, the microbiota-gut-brain axis mediates bidirectional communication between the gut and the brain and could act as a link between nutritional factors and AHN. The aim of this mini-review is to summarize, the most recent findings related to the influence of nutrition and diet in the modulation of AHN. The importance of maternal nutrition in the AHN of the offspring and the role of the microbiota-gut-brain axis in the nutrition-neurogenesis relationship have also been included.

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Maternal high-fat diet increases anhedonic behavior and modulates hippocampal Mash1 and BDNF expression in adult offspring

Cited by 10 publications

References 29 publications

Male Rat Offspring Are More Impacted by Maternal Obesity Induced by Cafeteria Diet than Females—Additive Effect of Postweaning Diet

Male Rat Offspring Are More Impacted by Maternal Obesity Induced by Cafeteria Diet than Females—Additive Effect of Postweaning Diet

Preimplantation or gestation/lactation high-fat diet alters adult offspring metabolism and neurogenesis

Nutrition and adult neurogenesis in the hippocampus: Does what you eat help you remember?

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