Peptide transport and animal growth: the fish paradigm

Abstract

Physiology Opinion piecePeptide transport and animal growth: the fish paradigm Protein digestion products are transported from the intestinal lumen into the enterocyte both in the form of free amino acids (AAs), by a large variety of brush border membrane AA transporters, and in the form of di/tripeptides, by a single brush border membrane transporter known as PEPtide Transporter 1 (PEPT1). Recent data indicate that, at least in teleost fish, PEPT1 plays a significant role in animal growth by operating, at the gastrointestinal level, as part of an integrated response network to food availability that directly supports body weight. Notably, PEPT1 responds to both fasting and refeeding and is involved in a phenomenon known as compensatory growth (a phase of accelerated growth when food levels are restored after a period of growth depression). In particular, PEPT1 expression decreases during fasting and increases during refeeding, which is the opposite of what observed so far in mammals and birds. These findings in teleost fish document, to our knowledge, for the first time in a vertebrate model, a direct correlation between the expression of an intestinal transporter, such as PEPT1, primarily involved in the uptake of dietary protein degradation products and animal growth.Keywords: di/tripeptides; PEPtide Transporter 1; teleost fish; growth; fasting/refeeding INTRODUCTIONThe modern mode of thinking that digested protein is transported from the intestinal lumen into enterocytes and then into the circulation both as amino acids (AAs) and di/tripeptides dates back to the mid-1970s. Today, we know that di/tripeptides are taken up by a single transporter known as PEPtide Transporter 1 (PEPT1). However, some questions remain unanswered. For instance, although PEPT1 knock-out models have been generated [1,2], it is not clear whether the intestinal peptide transporter plays a role in the up-or downregulation of animal growth. Indeed, by deleting the intestinal peptide transporter pept1 (previously known as pep-2) body size is reduced in an invertebrate animal model, such as the nematode Caenorhabditis elegans [1,3], whereas PepT1 null mice grow to normal size, body weight and organ weight [2].In recent years, interest in piscine PEPT1 has grown rapidly [4,5]. This is owing to the recurring observation that fish can efficiently use dietary di/tripeptides to sustain development, growth and metabolism [6][7][8][9][10][11][12][13][14]. MAJOR, SPECIFIC ASPECTS OF FISH GROWTHIn most fish, growth is indeterminate and the majority of absorbed nutrients are invested in accreting muscle tissue [15]. Muscle growth in juvenile fish increases both the size (hypertrophia) and number of muscle fibres (hyperplasia). By contrast, the increase in the number of fibres in mammals and birds is arrested shortly after embryonic development has been completed [16], and further muscle growth is mainly caused by hypertrophy of existing fibres. Skeletal muscle forms 40 -60% of the body mass in most adult fish. In muscle, all of the synthesized prot...

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“…Studies in several teleost species have revealed that intestinal expression levels of PepT1 respond to fasting and refeeding, with expression levels rising in some species after short-term fasting, followed by a decline in long-term fasting/starvation. Re-feeding stimulates upregulation of PepT1 above pre-fasted levels, indicating sensitive responsiveness to food availability and a potential role for the transporter in the phenomenon known as compensatory growth [51]–[54]. Aquaculture researchers are keenly interested in use of PepT1 as an indicator of protein uptake and as a direct predictor of animal growth [51], [55].…”

“…Re-feeding stimulates upregulation of PepT1 above pre-fasted levels, indicating sensitive responsiveness to food availability and a potential role for the transporter in the phenomenon known as compensatory growth [51]–[54]. Aquaculture researchers are keenly interested in use of PepT1 as an indicator of protein uptake and as a direct predictor of animal growth [51], [55]. PepT1 may also serve as another bridge between nutritional and immune regulation, given its roles in binding bacterial peptides and stimulation of gut innate immune activation and inflammation [56].…”

Dietary nitrogen and fish welfare

“…gradient on an abundant high-capacity, low-specificity peptide transporter (PepT1) or through endocytosis. Intestinal peptide transport is of major nutritional significance in that the intraluminal products of protein digestion are predominantly di-and tripeptides (up to 85% of the digesta in mammals) and not AA as previously believed (Taylor et al 2011;Verri et al 2011). In addition, many AA are more rapidly and efficiently absorbed in peptide form (for a review see Gilbert et al 2008).…”

“…(asterisk) indicates significantly different means from controls, for each time point tested (P \ 0.05). This figure has been adapted from Terova et al (2009) addition, PepT1 gene expression is up-regulated with refeeding and correlates with fish compensatory growth (Verri et al 2011). Moreover, Bakke et al (2010) have shown that dietary protein hydrolysates and free AA affect the expression of PepT1 along the digestive tract of Atlantic cod (Gadus morhua), indicating an adaptive response to keep a maximal efficiency of protein absorption at the intestinal level.…”

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“…; Verri et al . , ). Peptide absorption has also aroused the interest of scientists working on the larval and juvenile stages of fish (see e.g.…”