Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-28T18:07:31.972Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of starter diet supplementation on rumen epithelial morphology and expression of genes involved in cell proliferation and metabolism in pre-weaned lambs

Published online by Cambridge University Press:  26 February 2018

D. M. Sun ,
S.Y. Mao ,
W.Y. Zhu  and
J.H. Liu
D. M. Sun
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China
S.Y. Mao
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China
W.Y. Zhu
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China
J.H. Liu*
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China
*
†E-mail: liujunhua0011@163.com
Get access

Abstract

Starter feeding is usually used in lamb production to improve rumen development and to facilitate the weaning process, but molecular mechanism of which is not well understood. Therefore, the objective of this study is to investigate the effect of starter feeding on the expression of ruminal epithelial genes involved in cell proliferation, apoptosis and metabolism in pre-weaned lambs. We selected eight pairs of 10-day-old lamb twins. One twin was fed ewe milk (M, n=8), while the other was fed ewe milk plus starter (M+S, n=8). The lambs were sacrificed at 56 days age. Results showed that the lambs fed M+S had lower pH in the rumen and a higher concentration of acetate, propionate, butyrate and total volatile fatty acid (VFA). Compared with the M group, the concentration of β-hydroxybutyric acid in plasma had an increased trend, and the concentration of IGF-1 in plasma had an decreased trend in the M+S group. The length, width and surface of rumen papillae increased in the M+S group compared with the M group; this was associated with increased cell layers in the stratum corneum, stratum granulosum and total epithelia. Messenger RNA (mRNA) expression of proliferative genes of cyclin A, cyclin D1 and cyclin-dependent kinase 2 in the ruminal epithelia of M+S lambs was increased compared with M only lambs. The mRNA expression of apoptosis genes of caspase-3, caspase-8, B-cell lymphoma-2 (Bcl-2) and Bcl-2-associated X protein (Bax) in the M+S group was decreased compared with M group, but the ratio of Bcl-2 to Bax were not changed between the two groups. Expression of IGF-1 mRNA was decreased, but the mRNA expression of IGF-1 receptor was higher in ruminal epithelia in the M+S group. Furthermore, the mRNA expression of VFA absorption and metabolism genes of β-hydroxybutyrate dehydrogenase isoforms 1 and 3-hydroxy-3-methylglutaryl-CoA lyase had an increased trend in the M+S group than in the M group, but the mRNA expression of 3-hydroxy-3-methylglutaryl-CoA synthase isoform 1, monocarboxylate transporter isoform 1 and putative anion transporter isoform 1 had a decreased trend in the M+S group than in the M group. These results suggest that starter feeding increased proliferation and inhibited apoptosis of ruminal epithelial cells, and may promote the VFA metabolism in ruminal epithelium in pre-weaned lambs. These findings provide new insights into improving rumen development by nutritional intervention strategies in pre-weaned lambs.

Keywords

starter feedingrumen developmentvolatile fatty acidketogenesislamb
Type
Research Article
Information
animal , Volume 12 , Issue 11 , November 2018 , pp. 2274 - 2283
Copyright
© The Animal Consortium 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abecia, L, Ramos-Morales, E, Martinez-Fernandez, G, Arco, A, Martin-Garcia, AI, Newbold, CJ and Yanez-Ruiz, DR 2014. Feeding management in early life influences microbial colonisation and fermentation in the rumen of newborn goat kids. Animal Production Science 54, 1449–1454.Google Scholar
Aschenbach, JR, Penner, GB, Stumpff, F and Gabel, G 2011. Ruminant nutrition symposium: role of fermentation acid absorption in the regulation of ruminal pH. Journal of Animal Science 89, 1092–1107.Google Scholar
Baldwin, R, McLeod, K, Klotz, J and Heitmann, R 2004. Rumen development, intestinal growth and hepatic metabolism in the pre-and postweaning ruminant. Journal of Dairy Science 87, E55–E65.Google Scholar
Chomczynski, P and Sacchi, N 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.Google Scholar
Cory, S and Adams, JM 2002. The Bcl2 family: regulators of the cellular life-or-death switch. Nature Reviews Cancer 2, 647–656.Google Scholar
Faulkner, A 1999. Changes in plasma and milk concentrations of glucose and IGF-1 in response to exogenous growth hormone in lactating goats. Journal of Dairy Research 66, 207–214.Google Scholar
Filmus, J, Robles, AI, Shi, W, Wong, MJ, Colombo, LL and Conti, CJ 1994. Induction of cyclin D1 overexpression by activated ras. Oncogene 9, 3627–3633.Google Scholar
Gorka, P, Kowalski, ZM, Pietrzak, P, Kotunia, A, Jagusiak, W, Holst, JJ, Guilloteau, R and Zabielski, R 2011. Effect of method of delivery of sodium butyrate on rumen development in newborn calves. Journal of Dairy Science 94, 5578–5588.Google Scholar
Heinrichs, AJ and Heinrichs, BS 2011. A prospective study of calf factors affecting first-lactation and lifetime milk production and age of cows when removed from the herd. Journal of Dairy Science 94, 336–341.Google Scholar
Korsmeyer, SJ, Shutter, JR, Veis, DJ, Merry, DE and Oltvai, ZN 1993. Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Seminars in Cancer Biology 4, 327–332.Google Scholar
Laarman, AH and Oba, M 2011. Short communication: effect of calf starter on rumen pH of Holstein dairy calves at weaning. Journal of Dairy Science 94, 5661–5664.Google Scholar
Laarman, AH, Ruiz-Sanchez, AL, Sugino, T, Guan, LL and Oba, M 2012. Effects of feeding a calf starter on molecular adaptations in the ruminal epithelium and liver of Holstein dairy calves. Journal of Dairy Science 95, 2585–2594.Google Scholar
Lane, MA, Baldwin, RLt and Jesse, BW 2000. Sheep rumen metabolic development in response to age and dietary treatments. Journal of Animal Science 78, 1990–1996.Google Scholar
Lesmeister, KE and Heinrichs, AJ 2005. Effects of adding extra molasses to a texturized calf starter on rumen development, growth characteristics, and blood parameters in neonatal dairy calves. Journal of Dairy Science 88, 411–418.Google Scholar
Liu, J, Bian, G, Sun, D, Zhu, W and Mao, S 2017. Starter feeding supplementation alters colonic mucosal bacterial communities and modulates mucosal immune homeostasis in newborn lambs. Frontiers In Microbiology 8, 429.Google Scholar
Lu, J, Zhao, H, Xu, J, Zhang, L, Yan, L and Shen, Z 2013. Elevated cyclin D1 expression is governed by plasma IGF-1 through Ras/Raf/MEK/ERK pathway in rumen epithelium of goats supplying a high metabolizable energy diet. Journal of Animal Physiology and Animal Nutrition 97, 1170–1178.Google Scholar
Malhi, M, Gui, H, Yao, L, Aschenbach, JR, Gabel, G and Shen, Z 2013. 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. Journal of Dairy Science 96, 7603–7616.Google Scholar
Meale, SJ, Chaucheyras-Durand, F, Berends, H, Guan, LL and Steele, MA 2017. From pre- to postweaning: transformation of the young calf’s gastrointestinal tract. Journal of Dairy Science 100, 5894–5995.Google Scholar
Mentschel, J, Leiser, R, Mulling, C, Pfarrer, C and Claus, R 2001. Butyric acid stimulates rumen mucosa development in the calf mainly by a reduction of apoptosis. Archives of Animal Nutrition (Archiv Fur Tierernahrung) 55, 85–102.Google Scholar
Naeem, A, Drackley, JK, Stamey, J and Loor, JJ 2012. Role of metabolic and cellular proliferation genes in ruminal development in response to enhanced plane of nutrition in neonatal Holstein calves. Journal of Dairy Science 95, 1807–1820.Google Scholar
Norbury, C and Nurse, P 1992. Animal cell cycles and their control. Annual Review of Biochemistry 61, 441–470.Google Scholar
Odongo, NE, Alzahal, O, Lindinger, MI, Duffield, TF, Valdes, EV, Terrell, SP and McBride, BW 2006. Effects of mild heat stress and grain challenge on acid-base balance and rumen tissue histology in lambs. Journal of Animal Science 84, 447–455.Google Scholar
Penner, GB, Steele, MA, Aschenbach, JR and McBride, BW 2011. Ruminant nutrition symposium: molecular adaptation of ruminal epithelia to highly fermentable diets. Journal of Animal Science 89, 1108–1119.Google Scholar
Schlau, N, Guan, LL and Oba, M 2012. The relationship between rumen acidosis resistance and expression of genes involved in regulation of intracellular pH and butyrate metabolism of ruminal epithelial cells in steers. Journal of Dairy Science 95, 5866–5875.Google Scholar
Schwab, M, Reynders, V, Ulrich, S, Zahn, N, Stein, J and Schroder, O 2006. PPAR gamma is a key target of butyrate-induced caspase-3 activation in the colorectal cancer cell line Caco-2. Apoptosis 11, 1801–1811.Google Scholar
Sevi, A, Napolitano, F, Casamassima, D, Annicchiarico, G, Quarantelli, T and De Paola, R 1999. Effect of gradual transition from maternal to reconstituted milk on behavioural, endocrine and immune responses of lambs. Applied Animal Behaviour Science 64, 249–259.Google Scholar
Steele, MA, Vandervoort, G, AlZahal, O, Hook, SE, Matthews, JC and McBride, BW 2011a. Rumen epithelial adaptation to high-grain diets involves the coordinated regulation of genes involved in cholesterol homeostasis. Physiological Genomics 43, 308–316.Google Scholar
Sugino, T, Hasegawa, Y, Kurose, Y, Kojima, M, Kangawa, K and Terashima, Y 2004. Effects of ghrelin on food intake and neuroendocrine function in sheep. Animal Reproduction Science 82–83, 183–194.Google Scholar
Wardrop, I 1961. Some preliminary observations on the histological development of the fore-stomachs of the lamb II. The effects of diet on the histological development of the fore-stomachs of the lamb during post-natal life. The Journal of Agricultural Science 57, 343–346.Google Scholar
Supplementary material: File

Sun et al. supplementary material 1

Sun et al. supplementary material

Download Sun et al. supplementary material 1(File)
File 34.4 KB