Maternal nutrition and developmental programming of offspring
Lawrence P. Reynolds A * , Wellison J. S. Diniz B , Matthew S. Crouse C , Joel S. Caton A , Carl R. Dahlen A , Pawel P. Borowicz A and Alison K. Ward AA Center for Nutrition and Pregnancy, and Department of Animal Sciences, North Dakota State University, Fargo, ND 58108-6050, USA.
B Department of Animal Sciences, Auburn University, Auburn, AL 36832, USA.
C Nutrition, Growth, and Physiology Research Unit, USDA/Agricultural Research Service, U.S. Meat Animal Research Center, Clay Center, NE 68933-0166, USA.
Reproduction, Fertility and Development 35(2) 19-26 https://doi.org/10.1071/RD22234
Published online: 1 November 2022
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the IETS. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Developmental programming is the concept that ‘stressors’ during development (i.e. pregnancy, the perinatal period and infancy) can cause long-term changes in gene expression, leading to altered organ structure and function. Such long-term changes are associated with an increased risk of a host of chronic pathologies, or non-communicable diseases including abnormal growth and body composition, behavioural or cognitive dysfunction, metabolic abnormalities, and cardiovascular, gastro-intestinal, immune, musculoskeletal and reproductive dysfunction. Maternal nutrition during the periconceptual period, pregnancy and postnatally can have profound influences on the developmental program. Animal models, including domestic livestock species, have been important for defining the mechanisms and consequences of developmental programming. One of the important observations is that maternal nutritional status and other maternal stressors (e.g. environmental temperature, high altitude, maternal age and breed, multiple fetuses, etc.) early in pregnancy and even periconceptually can affect not only embryonic/fetal development but also placental development. Indeed, altered placental function may underlie the effects of many maternal stressors on fetal growth and development. We suggest that future directions should focus on the consequences of developmental programming during the offspring’s life course and for subsequent generations. Other important future directions include evaluating interventions, such as strategic dietary supplementation, and also determining how we can take advantage of the positive, adaptive aspects of developmental programming.
Keywords: developmental programming, fetal programming, gene expression, maternal nutrition, organ function, organ structure, periconceptual, placental programming.
Introduction
Developmental programming, also known as fetal programming, is the concept that developmental stressors can alter gene expression in the developing fetus/neonate via epigenetic mechanisms. Such epigenetic alterations are thought to ‘program’ not only fetal and postnatal growth and development, but also to cause long-term changes in organ structure (e.g. altered number of nephrons in the kidney, altered pancreatic islet number or size, altered number of myofibres) and function (Barker 1990; Paneth and Susser 1995, 2004; Armitage et al. 2004; Wu et al. 2006; Caton and Hess 2010; Reynolds et al. 2010a, 2017, 2019, 2022; Reynolds and Caton 2012; Caton et al. 2019; Dahlen et al. 2021; Diniz et al. 2022). The consequences of developmental programming include preterm delivery, low birth weight and poor survival of newborns as well as a host of chronic pathologies in the offspring including abnormal growth and body composition, behavioural or cognitive dysfunction, metabolic abnormalities and cardiovascular, gastro-intestinal, immune, musculoskeletal and reproductive dysfunction (Barker 2004; Wu et al. 2006; Caton and Hess 2010; Reynolds et al. 2010a, 2017, 2019, 2022; Reynolds and Caton 2012; Reynolds and Vonnahme 2016; Caton et al. 2019; Cushman and Perry 2019; Dahlen et al. 2021). Additionally, chronically altered function of organ systems may contribute to aging and, importantly for livestock production, reduced longevity and production (Zambrano et al. 2014, 2015, 2020, 2021; Du et al. 2015; Franke et al. 2017; Kuo et al. 2017, 2018; Pankey et al. 2017; Yang et al. 2017; Broadhead et al. 2019; Cushman and Perry 2019; Wang et al. 2019).
The concept of developmental programming was first articulated by Dr. David Barker and colleagues. They used epidemiological evidence in humans to show a strong association between low birth weight, poor postnatal environment, or other developmental insults, and the subsequent risk of developing the range of pathologies noted above (Barker 1990, 2004). These studies suggested that an adverse intrauterine environment can lead to a greater incidence of non-communicable diseases in the offspring and that poor maternal nutrition was ‘.. an obvious suspect (Barker 1990, 2004).’ Subsequently, numerous epidemiological studies in humans, as well as many carefully controlled studies in various animal models, have confirmed the initial observations of Barker and colleagues, and some of the risk factors for developmental programming have been identified (Armitage et al. 2004; Wu et al. 2006; Caton and Hess 2010; Reynolds et al. 2010a, 2017, 2019, 2022; Reynolds and Caton 2012; Reynolds and Vonnahme 2017; Caton et al. 2019).
An additional, and important concept is that developmental programming must have entered and remained in the genome because of its adaptive advantages (Nettle et al. 2013; Bateson et al. 2014; Mueller et al. 2015). Whether we can take advantage of these adpatations to improve fitness and therefore productivity of the offspring is not known but should be kept in mind as we study various aspects of developmental programming (Reynolds et al. 2022).
Maternal nutrition
Maternal nutrition has a profound effect on fetal growth, as reflected by fetal weights in late pregnancy (Reynolds et al. 2019, 2022). For example, adolescent sheep that are overfed throughout pregnancy exhibit reduced fetal and placental weights similar to those of heat-stressed adult mothers. In this experimental paradigm, not only is placental vascular development reduced, but gravid uterine (maternal placental) and umbilical (fetal placental) blood flows are profoundly reduced, similar to that seen in heat-stressed pregnancies (Reynolds et al. 2019, 2022). Reduced placental blood flows are associated with altered placental vascular growth and development (Reynolds et al. 2006, 2010a, 2010b, 2019, 2022).
These observations are not surprising, as soon after implantation the placenta becomes the sole organ of exchange between the fetal and maternal systems. In other words, very early in pregnancy, the exchange of nutrients, oxygen and metabolic wastes between the maternal and fetal systems occurs solely via the placenta (Mayhew et al. 2004; Redmer et al. 2005, 2009; Vonnahme et al. 2007; Mayhew 2009; Reynolds et al. 2010b). Because it is primarily an organ of transport, the placenta also develops an extensive blood supply (i.e. it becomes highly vascular), which causes gravid uterine and umbilical blood flows (that represent the blood supplies to the maternal and fetal sides of the placenta, respectively) to increase exponentially throughout pregnancy. In fact, the increase in umbilical blood flow keeps pace with the exponential growth of the fetus (Reynolds and Redmer 1995; Reynolds et al. 2010b).
Many studies in livestock have shown that placental development and function are altered late in pregnancy in a variety of models of developmental programming, including maternal dietary intake (overfed or underfed), environmental heat stress, multiple pregnancies (singletons vs twins or triplets), maternal age (adolescent vs adult pregnancies), and maternal breed (Reynolds et al. 2019, 2022). These observations agree with those in other species, including humans (Mayhew et al. 2004; Reynolds et al. 2006; Mayhew 2009). In addition, defects in placental growth, including vascular defects, normally precede altered fetal growth and development (Reynolds et al. 2017, 2019).
We have shown in nutritionally-compromised pregnancies that placental vascular development is reduced very early in gestation (Grazul-Bilska et al. 2013, 2014; Vonnahme et al. 2013; Reynolds et al. 2014, 2019, 2022; Bairagi et al. 2016; McLean et al. 2017). Not only is placental vascular development altered by maternal nutrition during early pregnancy, but other aspects of placental function are affected as well. For example, placental expression of nutrient transporters and angiogenic factors is reduced in nutrient-restricted heifers during early pregnancy (Table 1). Similarly, maternal dietary restriction during early pregnancy profoundly affects gene expression in fetal liver, muscle and cerebrum (Table 1).
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Because placental vascular growth and development are critical for normal placental function (Reynolds and Redmer 1995; Reynolds et al. 2010b, 2013, 2014; Bairagi et al. 2016), the observations described in the preceding paragraph have led to the concept of placental programming; i.e. that defects in placental growth and development underpin the altered fetal growth and organ development that is seen with developmental programming by maternal nutrition, and perhaps other ‘stressors’ such as in vitro production of embryos (see the next section of the manuscript; Reynolds et al. 2006; Vonnahme et al. 2013; Bairagi et al. 2016; Reynolds and Vonnahme 2017). Thus, despite the low metabolic demands of the conceptus in early pregnancy, these studies have confirmed that poor maternal diet can ‘program’ placental, and consequently fetal, development during their earliest stages (Diniz et al. 2021a, 2021b). In addition, maternal nutritional restriction is associated with effects, either directly or indirectly (e.g. via altered placental development and function) on gene expression in fetal organs (Table 1). Importantly, we also have shown that nutritional interventions (e.g. vitamin–mineral, energy and/or one-carbon metabolite supplementation; Table 1) can ‘rescue’ placental vascular development.
An additional time during which maternal nutrition seems to be important is the periconceptual period; that is, immediately before and after conception. Perhaps one of the most dramatic examples of developmental programming involves maternal nutrient restriction of ewes for 60 days before until 30 days after mating, which results in delivery an average of 7 days early compared with normally fed ewes and results in ‘… all preterm lambs [dying] soon after birth’ (Fig. 1; Bloomfield et al. 2003; Kumarasamy et al. 2005). Similarly, overfeeding or underfeeding of ewes for 8 weeks before collecting their oocytes results in poor rates of in vitro fertilisation and poor development of embryos in vitro (Fig. 2; Grazul-Bilska et al. 2012). These studies emphasise the importance of maternal nutritional status not only during early pregnancy but also during the periconceptual period.
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As we have already mentioned, developmental programming must have entered and remained in the genome because of its adaptive advantages (Nettle et al. 2013; Bateson et al. 2014; Mueller et al. 2015), and taking advantage of these may improve fitness and therefore productivity of the offspring (Reynolds et al. 2022). For example, our studies of maternal nutritional status during the first 50 days of pregnancy in cattle showed that the vast majority of genes in fetal liver, muscle, and brain were upregulated in fetuses from nutrient-restricted dams (Table 1). Based on these observations, we have suggested that the upregulation of genes may represent an adaptive response to the maternal nutrient restriction (Crouse et al. 2019; Reynolds et al. 2022). This suggestion seems likely, as cattle under an extensive, pasture-based system, which is very common in regions with large areas of grassland such as the western region of the U.S., are often under nutritional stress during early pregnancy, which is typically in the fall, because of the declining yield and quality of pastures (Krysl et al. 1987; Wu et al. 2006; NASEM 2016; Caton et al. 2019, 2020). Thus, the adaptive response to limited maternal nutrient intake seems to involve upregulation of genes and even ‘rewiring’ of gene networks at the systems level (Caton et al. 2020; Diniz et al. 2021b).
In vitro production (IVP) of embryos
An instructive paradigm that is likely related to the nutritional, or perhaps more appropriately the environmental, status of the embryo during fertilisation and early development is that of in vitro production (IVP) of embryos. As shown by Loi et al. (2006) and subsequently many others, IVP by in vitro fertilisation or cloning results in a relatively low percentage (10–40%) of embryos surviving to term (Palmieri et al. 2008; Reynolds et al. 2013, 2014, 2019, 2022). Associated with the high rate of embryonic loss and poor pregnancy outcomes is poor embryonic and placental development very early in pregnancy (approximately 0.15, or 15%, of gestation; Arnold et al. 2006; Palmieri et al. 2007, 2008; Grazul-Bilska et al. 2013, 2014; Fidanza et al. 2014; Reynolds et al. 2014).
As shown in Table 2, poor embryonic and placental development after assisted reproductive technologies (ART) includes reduced fetal and placental growth; reduced placental vascularisation; reduced placental expression of a host of angiogenic factors, gap junctional connexins, and DNA methyl transferases; increased conceptus DNA methylation; and altered placental expression of oestrogen and progesterone receptors. All of these alterations would be expected to dramatically affect embryonic and placental growth and development and likely contribute to placental programming.
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Observations in other mammalian species, including humans, have shown similar results after ART, including poor embryonic/fetal and placental development, poor pregnancy outcomes, and developmental programming of the offspring (Beaujean et al. 2004; Farin et al. 2006; Loi et al. 2006; Palmieri et al. 2007, 2008; Canovas et al. 2017; Coy et al. 2022). A promising approach to at least partially overcome the embryonic/fetal and placental defects seen with ART is the inclusion of oviductal or other reproductive fluids in the culture media. Inclusion of oviductal and other reproductive fluids improves the success of IVP and subsequent pregnancy rates and also reduces the effects of IVP on embryonic/fetal gene expression and DNA methylation status (Coy and Yanagimachi 2015; Canovas et al. 2017; Coy et al. 2022).
Conclusions and future directions
As discussed in this review, maternal nutritional status, ART, and a host of other maternal ‘stressors’ can profoundly affect embryonic/fetal development and survival, and often result in ‘programming’ of gene expression and subsequently altered growth and development. Recent data have shown that programming of placental growth and development very early in pregnancy may underlie many of the defects in embryonic/fetal growth and development that lead to poor outcomes during pregnancy and postnatally. In addition, maternal nutrition during the periconceptual period, that is, before and immediately after mating, also appears to program conceptus development.
Whether such early programming has long-lasting effects is unclear, but certainly epigenetic alterations occur, and there is every reason to believe they affect organ structure and function and will have lasting consequences throughout an individual’s life. Nevertheless, an important direction for future research is investigating the consequences of early programming both for health and productivity of the offspring and subsequent generations.
Another important area of future research focus should be whether interventions, including some of those discussed in this review, such as strategic dietary supplementation or culture of embryos with reproductive fluids, can mitigate some of the negative consequences of developmental programming, or even enhance the fitness of the offspring and future generations. That is, whether some of the strategies currently being evaluated for their ability to overcome the negative consequences of developmental programming can actually take advantage of the positive effects of developmental programming. This is especially apropos since, as we have already mentioned, it seems clear that we need a much better understanding of whether changes in expression of fetal and placental genes are adaptive, and therefore positive, or maladaptive, and therefore detrimental in both the short and long term.
Data availability
Any data from our research programs that are described in this review article will be shared upon reasonable request to the corresponding author.
Conflicts of interest
The authors declare no conflicts of interest.
Declaration of funding
Funding that supported the work from our research programs described in this manuscript came primarily from the Agriculture and Food Research Initiative (National Institute of Food and Agriculture, U.S. Department of Agriculture), the National Institutes of Health (U.S. Public Health Service), the North Dakota Agricultural Experiment Station, and the North Dakota State Board of Agricultural Research and Education.
Acknowledgements
The authors wish to acknowledge the many colleagues and collaborators, postdoctoral fellows, graduate and undergraduate students, and support staff who have made invaluable contributions to our work described in this manuscript.
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