Increased papillae growth and enhanced short-chain fatty acid absorption in the rumen of goats are associated with transient increases in cyclin D1 expression after ruminal butyrate infusion

Abstract

We tested the hypothesis that the proliferative effects of intraruminal butyrate infusions on the ruminal epithelium are linked to upregulation in cyclin D1 (CCND1), the cyclin-dependent kinase 4 (CDK4), and their possible association with enhanced absorption of short-chain fatty acids (SCFA). Goats (n=23) in 2 experiments (Exp.) were fed 200 g/d concentrate and hay ad libitum. In Exp. 1, goats received an intraruminal infusion of sodium butyrate at 0.3 (group B, n=8) or 0 (group C, n=7) g/kg of body weight (BW) per day before morning feeding for 28 d and were slaughtered 8 h after the butyrate infusion. In Exp. 2, goats (n=8) received butyrate infusion and feeding as in Exp. 1. On d 28, epithelial samples were biopsied from the antrium ruminis at 0, 3, and 7 h after the last butyrate infusion. In Exp. 1, the ruminal molar proportional concentration of butyrate increased in group B by about 110% after butyrate infusion and remained elevated for 1.5 h; thereafter, it gradually returned to the baseline (preinfusion) level. In group C, the molar proportional concentration of butyrate was unchanged over the time points. The length and width of papillae increased in B compared with C; this was associated with increased numbers of cells and cell layers in the epithelial strata and an increase in the surface area of 82%. The mRNA expression of CCND1 increased transiently at 3 h but returned to the preinfusion level at 7 h following butyrate infusion in Exp. 2. However, it did not differ between B and C in Exp. 1, in which the ruminal epithelium was sampled at 8 h after butyrate infusion. The mRNA expression of the monocarboxylate transporter MCT4, but not MCT1, was stably upregulated in B compared with C. The estimated absorption rate of total SCFA (%/h) increased in B compared with C. We conclude that transient increases in cyclin D1 transcription contribute to butyrate-induced papillae growth and subsequently to the increased absorption of SCFA in the ruminal epithelium of goats.

Relative contribution of ruminal buffering systems to pH regulation in feedlot cattle fed either low- or high-forage diets

“…Gäbel et al (1987) attributed this increase in absorption rates to a 200% to 400% increase in the surface area of papillae that was potentially induced by changes in the ruminal profile of SCFA, particularly, butyrate. This finding is supported by Malhi et al (2013), who documented an increase in the absorptive surface area (82%; papillae size and density) and the rate (%/h) of SCFA absorption following ruminal infusion of butyrate an hour before feeding in goats.…”

“…Conversely, the buffering capacity arising from SCFA absorption is predicted to be greater in low-forage (LF) than high-forage (HF)-fed cattle due to the SCFA-induced growth and proliferation of ruminal papillae (Malhi et al, 2013) and an upregulation of SCFA transporter activity (Gäbel et al, 1991). However, information on the relative importance of passive and protein-mediated transport of SCFA to pH regulation when ruminal fermentable CHO supply is altered remains scarce .…”

“…Besides the importance of morphological surface enlargement as the ruminal supply of rapidly fermentable CHO increases (Gäbel et al, 1987;Malhi et al, 2013), there is increasing evidence suggesting that functional adaptation in ruminal epithelial cells, which is characterized by changes in ion transport systems, also plays a critical role in pH regulation (Gäbel et al, 1991;Aschenbach et al, 2009 and. Our study focused on the SCFA − /HCO 3 − exchanger because an SCFA-induced upregulation of this system in concentrate-compared with hay-fed sheep was reported to elevate ruminal pH by increasing both the luminal appearance of HCO 3 − and disappearance of SCFA (Gäbel et al, 1991).…”

Short-chain fatty acids and acidic pH upregulate UT-B, GPR41, and GPR4 in rumen epithelial cells of goats

“…In our previous study, infusion of butyrate into the rumen has led to enhanced expression of the cell cycle-regulating protein, cyclin D1, and monocarboxylate transporter 4, in the rumen epithelium of goats (38). In cattle with grain-induced subacute ruminal acidosis (51), the expression of rumen epithelial genes, which act in cell proliferation, ketogenesis, and cholesterol homeostasis, have been largely altered, and these changes are related to the enhanced ruminal concentrations of SCFA and reduced pH.…”

“…Accumulating evidence indicates that SCFA in the gut affect mucosal homeostasis (42,44), epithelial absorption (38), immune responses, gene expression (36,44), and the activation of G proteincoupled receptors (GPRs) (64). SCFA and acidic pH also affect the growth and function of rumen epithelial cells (38,44,51,62).…”