Plasticity in gastrointestinal morphology and enzyme activity in lactating striped hamsters (Cricetulus barabensis)

Abstract

In small mammals, marked phenotypic plasticity of digestive physiology has been shown to make it easier for them to cope with energetically stressful periods, such as lactation. It has been proposed that the capacity of the gut to digest and absorb food is not the limiting factor to sustained energy intake (SusEI) during peak lactation. In this study, plasticity in energy intake and gastrointestinal morphology was examined in striped hamsters at different stages of reproduction and when raising litters of different sizes. Mechanisms associated with digestive enzymes and neuroendocrine hormones underpinning the plasticity were also examined. Females significantly increased energy intake, digestibility, digestive tract mass and the activity of stomach pepsin and small intestine maltase, sucrase and aminopeptidase in peak lactation compared with the non-productive and post-lactating periods. Further, females raising large litters significantly increased energy intake, digestibility, gastrointestinal mass and activity of digestive enzymes, and weaned heavier offspring compared with those nursing small and medium litters, indicating that the significant plasticity of digestive physiology increased reproductive performance. Agouti-related protein (AgRP) mRNA expression in the hypothalamus was up-regulated significantly in females raising large litters relative to those raising small litters. Serum leptin levels, and mRNA expression of hypothalamus neuropeptide Y (NPY) and the anorexigenic neuropeptides proopiomelanocortin (POMC) and cocaine-and amphetamine-regulated transcript (CART) did not differ among females raising small, medium and large litters. Leptin levels in lactation may only reflect a state of energy balance rather than being the prime driver of hyperphagia. Some hypothalamic neuropeptides, such as NPY, POMC and CART, may be involved in the limits to the SusEI during lactation.

Compensatory changes in villus morphology of lactating Mus musculus in response to insufficient dietary protein

“…Much research on dietary plasticity has focused on aminopeptidase (e.g. Sabat et al, 1999;Naya et al, 2008a;Zhang et al, 2016), a protein-digesting enzyme found throughout the small intestine (Miura et al, 1983;Naya et al, 2008a). Our finding that protein deficiency localizes morphological flexibility to the proximal small intestine suggests that enterokinase, an enzyme expressed at highest levels in the most proximal part of the duodenum (Nordström and Dahlqvist, 1971;Yuan et al, 1998), may be an important actor in dietary flexibility.…”

Regulation of intestinal growth in response to variations in energy supply and demand

“…For example, in striped hamsters ( Cricetulus brabensis ), these changes are correlated with changes in food intake, digestive efficiency and gene expression of AgRP in the hypothalamus . However, in this situation, the levels of POMC and CART were unchanged despite the large differences in food intake, and trends in both NPY and leptin levels were not significant . Given the trends, however, this could be a power issue at the low sample size.…”

“…This energetic challenge provides further insight into the link between adipose tissue‐associated energy loss and intestinal growth. Notably, lactation involves large increases in energy intake and intestinal growth on a background of reduced adipose tissue mass and lowered leptin levels . At the hypothalamic level, lactation reduces the expression of POMC and increases the expression of AgRP and NPY in the ARC and increases the expression of NPY in the dorsomedial hypothalamus .…”

“…The tremendous growth of the intestine during lactation in the rat , mouse and other small rodents appears to serve to maintain the absorption efficiency relatively constant in the face of the increase in food intake (Table ), which may reach four to five times the intake of non‐breeding females . Although in general the changes in the alimentary tract seem to serve to sustain assimilation efficiency constant, in some situations, the energy absorption/assimilation efficiency has been reported to change significantly.…”

“…Modulations of the gastrointestinal tract during lactation in small rodents also vary in relation to the litter size . For example, in striped hamsters ( Cricetulus brabensis ), these changes are correlated with changes in food intake, digestive efficiency and gene expression of AgRP in the hypothalamus .…”