Na⁺ transport across rumen epithelium of hay‐fed sheep is acutely stimulated by the peptide IGF‐1 in vitro

Abstract

An energy-rich diet leads to enhanced ruminal Na(+) absorption, which is associated with elevated plasma insulin-like growth factor 1 (IGF-1) levels and an increased number of IGF-1 receptors in rumen papillae. This study examined the in vitro effect of IGF-1 on Na(+) transport across the rumen epithelium of hay-fed sheep, in which the IGF-1 concentration in plasma is lower than in concentrate-fed animals. At concentrations ranging from 20 to 100 μg l(-1), serosal LR3-IGF-1, a recombinant analogue of IGF-1, rapidly (within 30 min) stimulated the mucosal-to-serosal Na(+) flux (J(ms)Na) and consequently the net Na(+) flux (J(net)Na). Compared with controls, J(net)Na increased by about 60% (P < 0.05) following the serosal application of LR3-IGF-1 (20 μg l(-1)). The IGF-1-induced increment of J(ms)Na and J(net)Na was inhibited by mucosal amiloride (1 mmol l(-1)). Neither IGF-1 nor amiloride altered tissue conductance or the short-circuit current of the isolated rumen epithelium. These data support the assumption that the stimulating effect of serosally applied IGF-1 on Na(+) transport across the rumen epithelium is mediated by Na(+)-H(+) exchange (NHE). A further study was performed with cultured rumen epithelial cells and a fluorescent probe (BCECF) to estimate the rate of pH(i) recovery after acid loading. The pH(i) of isolated rumen epithelial cells was 6.43 ± 0.15 after butyrate loading and recovered by 0.26 ± 0.02 pH units (15 min)(-1). Application of LR3-IGF-1 (20 μg l(-1)) significantly increased the rate of pH(i) recovery to 0.33 ± 0.02 pH units (15 min)(-1). Amiloride administration reduced the recovery rate in both control and IGF-1-stimulated cells. These results show, for the first time, that an acute effect of IGF-1 on Na(+) absorption across rumen epithelium results from increased NHE activity. Insulin-like growth factor 1 is thus important for the fast functional adaptation of ruminal Na(+) transport via NHE.

Short-term adaptation of the ruminal epithelium involves abrupt changes in sodium and short-chain fatty acid transport

“…Several factors influence Na ϩ transport, including luminal osmolality (49), SCFA concentration (52), and, more recently, it has been demonstrated that IGF-1 acutely stimulates Na ϩ transport (53). However, in the current study, mRNA abundance of IGFBP5 was downregulated, and IGFBP3 was not affected by increasing days fed the moderate-grain diet.…”

“…However, in the current study, mRNA abundance of IGFBP5 was downregulated, and IGFBP3 was not affected by increasing days fed the moderate-grain diet. Although these receptors influence epithelial growth (18,54), IGF also acutely stimulates Na ϩ absorption in the rumen (53). This opposes results previously showing upregulation of IGFBP5 within 1 wk of abrupt grain adaptation in mature nonlactating dairy cows (55), and as early as 4 days after inducing a grain challenge in second-lactation dairy cows (56).…”

“…Maximal ruminal epithelial surface area has been shown to occur 4 to 6 wk after an increase in dietary fermentability for dairy cattle (7,16) and goats (53,61). The short timeframe imposed in the current study (maximum of 3 wk) allowed for evaluation of functional adaptation.…”

“…Sodium transport across the ruminal epithelium is well characterized (17,21,24,52,53) and is driven by the Na ϩ / K ϩ -ATPase located on the basolateral membrane (27). Several factors influence Na ϩ transport, including luminal osmolality (49), SCFA concentration (52), and, more recently, it has been demonstrated that IGF-1 acutely stimulates Na ϩ transport (53).…”

Review: Exogenous butyrate: implications for the functional development of ruminal epithelium and calf performance

“…Recent studies also point to the impact of butyrate on the activity of the endocrine system. The increase in the concentrations of gastrin, secretin, cholecystokinin, glucagon-like peptide 2, and IGF-1 in the blood and the increase in IGF-receptor 1 in the ruminal epithelial cells have been observed as a result of butyrate supplementation (Shen et al, 2005;Gorka et al, 2009;Guilloteau et al, 2010;Kato et al, 2011;Shen et al, 2012). All of these proteins and peptides are considered hormonal signals that regulate the nutrient absorption, metabolism and growth in mammalian tissues (Shen et al, 2004;Siddle, 2011;Connor et al, 2015).…”