Paternal line multigenerational passage of altered risk assessment behavior in female but not male rat offspring of mothers fed a low protein diet

Reyes-Castro, Luis A.; Rodríguez-González, Guadalupe L.; Chavira, Roberto; Ibáñez, Carlos A.; Lomas-Soria, Consuelo; Rodriguez, Jesse S.; Nathanielsz, Peter W.; Zambrano, Elena

doi:10.1016/j.physbeh.2014.12.017

Cited by 9 publications

(9 citation statements)

References 53 publications

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“…No studies have investigated F2, so inter-generational effects are entirely unstudied in NHPs. The importance of inter-generational studies is shown by the multiple reports of intergenerational and transgenerational epigenetic and non-epigenetic transfer in guinea pigs, 71 rodents, [72][73][74][75] and sheep. 76,77 Another major weakness in the literature to date is investigation of sex as a biological variable.…”

Section: Deficiencies In the Literature And Directions For Future Workmentioning

confidence: 99%

Strength of nonhuman primate studies of developmental programming: review of sample sizes, challenges, and steps for future work

Huber

Jenkins

et al. 2019

J Dev Orig Health Dis

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Nonhuman primate (NHP) studies are crucial to biomedical research. NHPs are the species most similar to humans in lifespan, body size, and hormonal profiles. Planning research requires statistical power evaluation, which is difficult to perform when lacking directly relevant preliminary data. This is especially true for NHP developmental programming studies, which are scarce. We review the sample sizes reported, challenges, areas needing further work, and goals of NHP maternal nutritional programming studies. The literature search included 27 keywords, for example, maternal obesity, intrauterine growth restriction, maternal high-fat diet, and maternal nutrient reduction. Only fetal and postnatal offspring studies involving tissue collection or imaging were included. Twenty-eight studies investigated maternal over-nutrition and 33 under-nutrition; 23 involved macaques and 38 baboons. Analysis by sex was performed in 19; minimum group size ranged from 1 to 8 (mean 4.7 ± 0.52, median 4, mode 3) and maximum group size from 3 to 16 (8.3 ± 0.93, 8, 8). Sexes were pooled in 42 studies; minimum group size ranged from 2 to 16 (mean 5.3 ± 0.35, median 6, mode 6) and maximum group size from 4 to 26 (10.2 ± 0.92, 8, 8). A typical study with sex-based analyses had group size minimum 4 and maximum 8 per sex. Among studies with sexes pooled, minimum group size averaged 6 and maximum 8. All studies reported some significant differences between groups. Therefore, studies with group sizes 3–8 can detect significance between groups. To address deficiencies in the literature, goals include increasing age range, more frequently considering sex as a biological variable, expanding topics, replicating studies, exploring intergenerational effects, and examining interventions.

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Section: Deficiencies In the Literature And Directions For Future Workmentioning

confidence: 99%

Strength of nonhuman primate studies of developmental programming: review of sample sizes, challenges, and steps for future work

Huber

Jenkins

et al. 2019

J Dev Orig Health Dis

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“…Hormone disruptions that cause epigenetic alterations may also play a role in the long term effects on progeny through multiple generations, not just first generation offspring of protein malnourished dams. Reyes-Castro et al investigated the paternal line multigenerational passage of altered risk assessment behavior, as a result of blunted corticosterone levels, in second generation female offspring of low protein diet fed dams [ 169 ]. First generation males of dams fed low protein gestational diets had lower corticosterone levels which can result in risk taking behaviors.…”

Section: Proposed Mechanisms Of Fetal Programming By Proteinsmentioning

confidence: 99%

“…There are several proposed mechanisms by which sex-specific transmission of phenotypes can occur including alterations in metabolic environment (transmaternal inheritance of obesity), gene expression mediated by developmental and epigenetic pathways (transpaternal inheritance of low body weight), or both (impaired glucose tolerance) [ 170 ]. Authors suggest that epigenetic modifications through the paternal lineage are manifested more robustly in second generation females [ 169 ]. However, there is no evidence indicating epigenetic traits as possible mechanism in current study.…”

Section: Proposed Mechanisms Of Fetal Programming By Proteinsmentioning

confidence: 99%

“…However, there is no evidence indicating epigenetic traits as possible mechanism in current study. Authors also suggested that protein restrictive diets can have impact on the hormone regulation of multiple generations [ 169 ]. This study supports the notion that the transmission of transgenerational outcomes can be specific to either maternal or paternal route and it can influence the phenotype of the second generation in a sex-dependent manner.…”

Section: Proposed Mechanisms Of Fetal Programming By Proteinsmentioning

confidence: 99%

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The Role of Maternal Dietary Proteins in Development of Metabolic Syndrome in Offspring

et al. 2015

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The prevalence of metabolic syndrome and obesity has been increasing. Pre-natal environment has been suggested as a factor influencing the risk of metabolic syndrome in adulthood. Both observational and experimental studies showed that maternal diet is a major modifier of the development of regulatory systems in the offspring in utero and post-natally. Both protein content and source in maternal diet influence pre- and early post-natal development. High and low protein dams’ diets have detrimental effect on body weight, blood pressure191 and metabolic and intake regulatory systems in the offspring. Moreover, the role of the source of protein in a nutritionally adequate maternal diet in programming of food intake regulatory system, body weight, glucose metabolism and blood pressure in offspring is studied. However, underlying mechanisms are still elusive. The purpose of this review is to examine the current literature related to the role of proteins in maternal diets in development of characteristics of the metabolic syndrome in offspring.

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“…In contrast male offspring of these programmed males were unaffected (Reyes‐Castro et al . ). As discussed above, changes in maternal physiology often contribute to long‐term outcomes that may impact on the pregnancy and also lactation in the early postnatal period (Siebel et al .…”

Section: Introductionmentioning

confidence: 97%

Programming of maternal and offspring disease: impact of growth restriction, fetal sex and transmission across generations

Cheong

Wlodek

Moritz

et al. 2016

The Journal of Physiology

125

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partly attributed to different placenta-regulated growth strategies of the male and female fetus. Pregnancy is known to be a major risk factor for unmasking a number of conditions and can be considered a 'second hit' for women who were born small. As such, female offspring often develop impairments of physiology for the first time during pregnancy that present as pregnancy complications. Numerous maternal stressors can further increase the risk of developing a maternal complication during pregnancy. Importantly, these maternal complications can have long-term consequences for both the mother after pregnancy and the developing fetus. Conditions such as preeclampsia, gestational diabetes and hypertension as well as thyroid, liver and kidney diseases are all conditions that can complicate pregnancy and have long-term consequences for maternal and offspring health. Babies born to mothers who develop these conditions are often at a greater risk of developing disease in adulthood. This has implications as a mechanism for transmission of disease across generations. In this review, we discuss the evidence surrounding long-term intergenerational implications of being born small and/or experiencing stress during pregnancy on programming outcomes. Abstract figure legend Sex-specific fetal programming and the transgenerational transmission of diseases. Perturbations of the fetal environment during critical periods of development can have many consequences in postnatal life. This is primarily regulated by the placenta, which is known to respond to stressful stimuli in a sex-specific manner. Individuals exposed to suboptimal conditions in utero are programmed for various diseases including cardiovascular and metabolic diseases. Females programmed during fetal life have increased risk of developing pregnancy complications. The germ cells of exposed individuals may also be compromised. Together, they contribute to an adverse fetal environment and places the next generation of offspring at risk of adverse health. Importantly, stress is known to exacerbate these programmed outcomes during fetal and postnatal life.

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Paternal line multigenerational passage of altered risk assessment behavior in female but not male rat offspring of mothers fed a low protein diet

Cited by 9 publications

References 53 publications

Strength of nonhuman primate studies of developmental programming: review of sample sizes, challenges, and steps for future work

Strength of nonhuman primate studies of developmental programming: review of sample sizes, challenges, and steps for future work

The Role of Maternal Dietary Proteins in Development of Metabolic Syndrome in Offspring

Programming of maternal and offspring disease: impact of growth restriction, fetal sex and transmission across generations

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