An intake of nutrients is essential for maintaining
life, as they provide energy to the body, and also trigger other
important body functions. The interaction between ingested
foodstuffs and the gastrointestinal endocrine cells is a new
emerging concept (1,2). Understanding this interaction is not only
important for understanding the normal physiology and the role of
ingested nutrients in gastrointestinal disorders and diseases, but
also for managing certain gastrointestinal disorders (3–6).
New data on the interaction between ingested
nutrients and the gastrointestinal endocrine cells obtained from
basic science and clinical research have accumulated in the last
few years. The present review aimed to interpret the newly gained
knowledge so as to understand the role of this interaction.
The gastrointestinal endocrine cells are scattered
between the mucosal epithelial cells facing the intestinal lumen
(Fig. 1) (7,8). There are
≥10 types of endocrine cell, and they are found in the stomach and
the small and large intestines (8).
Different segments of the gastrointestinal tract contain several
different populations of gut endocrine cells (Fig. 2). Certain types of endocrine cells are
located only in specific areas of the gastrointestinal tract. For
example, serotonin- and somatostatin-secreting cells occur in the
stomach and small and large intestines, while those producing
ghrelin and gastrin are found only in the stomach, those producing
secretin, cholecystokinin, gastric inhibitory peptide (GIP) and
motilin are found only in the upper small intestine, and those
producing polypeptide YY (PYY), pancreatic polypeptide and
oxyntomodulin are located only in the lower small intestine and
large intestine (7,9–11). The
densities of these cells vary in different sections of the
gastrointestinal tract, with the density being highest in the
duodenum (12–16) (Fig. 3).
The gastrointestinal endocrine cells regulate gastrointestinal
motility, secretion, absorption, visceral sensitivity, local immune
defence, cell proliferation and appetite (7,17–31). These endocrine cells interact with each
other and also with the enteric nervous system, and the afferent
and efferent nerve fibers of the autonomic nervous system and the
central nervous system (CNS) (7,18,22,32).
Depletion of gastrointestinal endocrine cells as in congenital
malabsorptive diarrhea caused by mutant neurogenin-3 (33), or complete loss of these cells in
mutant mice with ablation of the transcript factor neurogenin-3
(34) show that the gastrointestinal
endocrine cells are essential for life.
Immunohistochemical studies have shown that two
hormones can be colocalized in the same endocrine cell type, such
as glucagon-like peptide-1 and GIP in the small intestine as well
as PYY and oxyntomodulin in the large intestine (34–38). Recent
studies have further found that mature intestinal endocrine cells
are capable of expressing several hormones (39,40).
The gastrointestinal endocrine cells have
specialized microvilli that project into the lumen and function as
sensors of the gut contents (mostly nutrients and/or bacteria
byproducts), and respond to luminal stimuli by releasing their
hormones into the lamina propria (41–63). The gut
intraluminal contents of carbohydrates, proteins and fats trigger
the release of different signaling substances (such as hormones)
from the gut endocrine cells (Table I)
(41–53).
The signaling substances (hormones) released from
the gastrointestinal endocrine cells may exert their actions
locally on nearby cells or neurons (paracrine mode) or by entering
the circulating blood and reaching distant targets (endocrine mode)
(64–67).
The gastrointestinal endocrine cells possess a basal
cytoplasmic process, which is believed to facilitate the paracrine
mode of action (Figs. 4 and 5) (68–72). This cytoplasmic process extends ≤70 µm,
compared with the base of the endocrine cells being only 10 µm in
diameter (70). This process has
certain similarities to neuronal axons, and has been named a
neuropod (70, 73–75). The neuropod has other axon-like
characteristics, such as containing neurofilaments, being escorted
by enteric glia cells, and expressing receptors for neurotrophins
(74). Furthermore, gut endocrine
cells have small clear synaptic vesicles, express several genes
encoding for presynaptic proteins (synapsin 1, piccolo, bassoon,
MUNC13B, regulating synaptic membrane exocytosis 2, latrophilin and
transsynaptic neurexin), and also express postsynaptic genes
(transsynaptic neuroligins 2 and 3, homer 3 and postsynaptic
density 95) (75). Based on these
data, it was concluded that the gut endocrine cells have the
necessary elements for afferent and efferent synaptic transmission
(75). Therefore, it appears that the
gastrointestinal endocrine cells exert their effects via three
modes of action: Endocrine, paracrine and synaptic (Fig. 6).
The recent findings of gastrointestinal endocrine
cells exhibiting endocrine and neuron-like characteristics support
and revive the old hypothesis on the evolution of the
neuroendocrine system of the gut (76). The observation that the mammalian
gastrointestinal hormonal peptides occur in the CNS, but not in the
gut of invertebrates (77–79), led to the hypothesis that the
gastrointestinal endocrine cells of vertebrates originated in the
nervous system of a common ancestor, and migrated during a later
stage of evolution into the gut as scattered endocrine cells
(76).
As aforementioned, the composition of the diet with
different proportions of carbohydrates, proteins and fats is a
trigger for the release of different gut hormones into the lamina
propria. Furthermore, the ingested foodstuffs act as prebiotics for
the intestinal microbiota, and the byproducts of the bacteria
trigger also the release of hormones from the gut endocrine
cells.
It has been shown recently that a change in diet is
accompanied by a change in the density of gastrointestinal cells
(3–6).
This could be due to an ingested foodstuff acting as a prebiotic
for the intestinal bacteria with the associated bacterial
byproducts. These bacterial byproducts may act on the stem cells
and/or differentiation progenitors, resulting in changes in the
stem cell clonogenic activity and/or differentiation progeny.
Alternatively, these bacterial byproducts could act on mature
gastrointestinal cells to favor the expression of specific hormones
(Fig. 7). Thus, the change in the
density of a certain endocrine cell type could be caused by
switching to the expression of a different hormone.
The diet is important for regulating the functions
of gastrointestinal endocrine cells. It not only regulates the
release of hormones from these cells, but also affects their
densities. The interaction between nutrients and gastrointestinal
endocrine cells could be useful for the clinical management of
several diseases, such as irritable bowel syndrome, obesity and
diabetes (17,80–85).
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