Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T04:24:58.680Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression of metabolic sensing receptors in adipose tissues of periparturient dairy cows with differing extent of negative energy balance

Published online by Cambridge University Press:  10 November 2015

P. Friedrichs ,
H. Sauerwein ,
K. Huber ,
L. F. Locher ,
J. Rehage ,
U. Meyer ,
S. Dänicke ,
B. Kuhla  and
M. Mielenz
P. Friedrichs
Affiliation:
Institute of Animal Science, Physiology & Hygiene Unit, University of Bonn, 53115 Bonn, Germany
H. Sauerwein
Affiliation:
Institute of Animal Science, Physiology & Hygiene Unit, University of Bonn, 53115 Bonn, Germany
K. Huber
Affiliation:
Department of Physiology, University of Veterinary Medicine Hannover, Foundation, 30171 Hannover, Germany
L. F. Locher
Affiliation:
Clinic for Cattle, University of Veterinary Medicine Hannover, Foundation, 30171 Hannover, Germany
J. Rehage
Affiliation:
Clinic for Cattle, University of Veterinary Medicine Hannover, Foundation, 30171 Hannover, Germany
U. Meyer
Affiliation:
Institute of Animal Nutrition, Friedrich-Loeffler-Institute (FLI), Federal Research Institute for Animal Health, 38116 Braunschweig, Germany
S. Dänicke
Affiliation:
Institute of Animal Nutrition, Friedrich-Loeffler-Institute (FLI), Federal Research Institute for Animal Health, 38116 Braunschweig, Germany
B. Kuhla
Affiliation:
Institute of Nutritional Physiology ‘Oskar Kellner’, Leibniz Institute for Farm Animal Biology (FBN), 18196 Dummerstorf, Germany
M. Mielenz*
Affiliation:
Institute of Animal Science, Physiology & Hygiene Unit, University of Bonn, 53115 Bonn, Germany
*
†E-mail: [email protected]
Get access

Abstract

We recently showed that the mRNA expression of genes encoding for specific nutrient sensing receptors, namely the free fatty acid receptors (FFAR) 1, 2, 3, and the hydroxycarboxylic acid receptor (HCAR) 2, undergo characteristic changes during the transition from late pregnancy to lactation in certain adipose tissues (AT) of dairy cows. We hypothesised that divergent energy intake achieved by feeding diets with either high or low portions of concentrate (60% v. 30% concentrate on a dry matter basis) will alter the mRNA expression of FFAR 1, 2, 3, as well as HCAR2 in subcutaneous (SCAT) and retroperitoneal AT (RPAT) of dairy cows in the first 3 weeks postpartum (p.p.). For this purpose, 20 multiparous German Holstein cows were allocated to either the high concentrate ration (HC, n=10) or the low concentrate ration (LC, n=10) from day 1 to 21 p.p. Serum samples and biopsies of SCAT (tail head) and RPAT (above the peritoneum) were obtained at day −21, 1 and 21 relative to parturition. The mRNA abundances were measured by quantitative PCR. The concentrations of short-chain fatty acid (SCFA) in serum were measured by gas chromatography-flame ionisation detector. The FFAR1 and FFAR2 mRNA abundance in RPAT was higher at day −21 compared to day 1. At day 21 p.p. the FFAR2 mRNA abundance was 2.5-fold higher in RPAT of the LC animals compared to the HC cows. The FFAR3 mRNA abundance tended to lower values in SCAT of the LC group at day 21. The HCAR2 mRNA abundance was neither affected by time nor by feeding in both AT. On day 21 p.p. the HC group had 1.7-fold greater serum concentrations of propionic acid and lower concentrations of acetic acid (trend: 1.2-fold lower) compared with the LC group. Positive correlations between the mRNA abundance of HCAR2 and peroxisome proliferator-activated receptor γ-2 (PPARG2) indicate a link between HCAR2 and PPARG2 in both AT. We observed an inverse regulation of FFAR2 and FFAR3 expression over time and both receptors also showed an inverse mRNA abundance as induced by different portions of concentrate. Thus, indicating divergent nutrient sensing of both receptors in AT during the transition period. We propose that the different manifestation of negative EB in both groups at day 21 after parturition affect at least FFAR2 expression in RPAT.

Keywords

transition periodbovine adipose tissuemetabolic sensing
Type
Research Article
Information
animal , Volume 10 , Supplement 4 , April 2016 , pp. 623 - 632
Copyright
© The Animal Consortium 2015 

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

Bergman, EN 1990. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567–590.Google Scholar
Brown, AJ, Jupe, S and Briscoe, CP 2005. A family of fatty acid binding receptors. DNA and Cell Biology 24, 54–61.Google Scholar
Carretta, MD, Conejeros, I, Hidalgo, MA and Burgos, RA 2013. Propionate induces the release of granules from bovine neutrophils. Journal of Dairy Science 96, 2507–2520.Google Scholar
Dewulf, EM, Ge, Q, Bindels, LB, Sohet, FM, Cani, PD, Brichard, SM and Delzenne, NM 2013. Evaluation of the relationship between GPR43 and adiposity in human. Nutrition & Metabolism 10, 11.Google Scholar
Drackley, JK 1999. ADSA Foundation Scholar Award. Biology of dairy cows during the transition period: the final frontier? Journal of Dairy Science 82, 2259–2273.Google Scholar
Friedrichs, P, Saremi, B, Winand, S, Rehage, J, Dänicke, S, Sauerwein, H and Mielenz, M 2014. Energy and metabolic sensing G protein-coupled receptors during lactation-induced changes in energy balance. Domestic Animal Endocrinology 48, 33–41.Google Scholar
GfE 2001. Empfehlungen zur Energie- und Nährstoffaufnahme der Milchkühe und Aufzuchtrinder [Recommended energy and nutrient supply for dairy cows and growing cattle]. DLG Verlag, Frankfurt am Main.Google Scholar
Hammarstedt, A, Andersson, CX, Rotter Sopasakis, V and Smith, U 2005. The effect of PPARgamma ligands on the adipose tissue in insulin resistance. Prostaglandins, Leukotrienes, and Essential Fatty Acids 73, 65–75.CrossRefGoogle ScholarPubMed
Harmon, DL 1992. Impact of nutrition on pancreatic exocrine and endocrine secretion in ruminants: a review. Journal of Animal Science 70, 1290–1301.Google Scholar
Hong, YH, Nishimura, Y, Hishikawa, D, Tsuzuki, H, Miyahara, H, Gotoh, C, Choi, KC, Feng, DD, Chen, C, Lee, HG, Katoh, K, Roh, SG and Sasaki, S 2005. Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology 146, 5092–5099.CrossRefGoogle ScholarPubMed
Hosseini, A, Behrendt, C, Regenhard, P, Sauerwein, H and Mielenz, M 2012. Differential effects of propionate or beta-hydroxybutyrate on genes related to energy balance and insulin sensitivity in bovine white adipose tissue explants from a subcutaneous and a visceral depot. Journal of Animal Physiology and Animal Nutrition 96, 570–580.Google Scholar
Hudson, BD, Christiansen, E, Tikhonova, IG, Grundmann, M, Kostenis, E, Adams, DR, Ulven, T and Milligan, G 2012. Chemically engineering ligand selectivity at the free fatty acid receptor 2 based on pharmacological variation between species orthologs. FASEB Journal 26, 4951–4965.Google Scholar
Isken, F, Klaus, S, Osterhoff, M, Pfeiffer, AF and Weickert, MO 2010. Effects of long-term soluble vs. insoluble dietary fiber intake on high-fat diet-induced obesity in C57BL/6J mice. Journal of Nutritional Biochemistry 21, 278–284.Google Scholar
Itoh, Y, Kawamata, Y, Harada, M, Kobayashi, M, Fujii, R, Fukusumi, S, Ogi, K, Hosoya, M, Tanaka, Y, Uejima, H, Tanaka, H, Maruyama, M, Satoh, R, Okubo, S, Kizawa, H, Komatsu, H, Matsumura, F, Noguchi, Y, Shinohara, T, Hinuma, S, Fujisawa, Y and Fujino, M 2003. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422, 173–176.CrossRefGoogle ScholarPubMed
Kebede, M, Ferdaoussi, M, Mancini, A, Alquier, T, Kulkarni, RN, Walker, MD and Poitout, V 2012. Glucose activates free fatty acid receptor 1 gene transcription via phosphatidylinositol-3-kinase-dependent O-GlcNAcylation of pancreas-duodenum homeobox-1. Proceedings of the National Academy of Sciences 109, 2376–2381.CrossRefGoogle ScholarPubMed
Kenéz, A, Locher, L, Rehage, J, Dänicke, S and Huber, K 2014. Agonists of the G protein-coupled receptor 109A-mediated pathway promote antilipolysis by reducing serine residue 563 phosphorylation of hormone-sensitive lipase in bovine adipose tissue explants. Journal of Dairy Science 97, 3626–3634.Google Scholar
Kenéz, Á, Locher, L, Rizk, A, Dänicke, S, Rehage, J and Huber, K 2013. Lipolytic capacity of visceral adipose tissue in the dairy cow. In Energy and protein metabolism and nutrition in sustainable animal production (ed. J Oltjen, E Kebreab and H Lapierre), pp. 459–461. Wageningen Academic Publishers, Wageningen, The Netherlands.CrossRefGoogle Scholar
Kopp, C, Hosseini, A, Singh, SP, Regenhard, P, Khalilvandi-Behroozyar, H, Sauerwein, H and Mielenz, M 2014. Nicotinic acid increases adiponectin secretion from differentiated bovine preadipocytes through G-protein coupled receptor signaling. International Journal of Molecular Sciences 15, 21401–21418.CrossRefGoogle ScholarPubMed
Kristensen, NB 2000. Quantification of whole blood short-chain fatty acids by gas chromatographic determination of plasma 2-chloroethyl derivatives and correction for dilution space in erythrocytes. Acta Agriculturae Scandinavica A 50, 231–236.Google Scholar
Lemor, A, Hosseini, A, Sauerwein, H and Mielenz, M 2009. Transition period-related changes in the abundance of the mRNAs of adiponectin and its receptors, of visfatin, and of fatty acid binding receptors in adipose tissue of high-yielding dairy cows. Domestic Animal Endocrinology 37, 37–44.Google Scholar
Li, CJ, Li, RW, Wang, YH and Elsasser, TH 2007. Pathway analysis identifies perturbation of genetic networks induced by butyrate in a bovine kidney epithelial cell line. Functional & Integrative Genomics 7, 193–205.Google Scholar
Locher, LF, Meyer, N, Weber, EM, Rehage, J, Meyer, U, Dänicke, S and Huber, K 2011. Hormone-sensitive lipase protein expression and extent of phosphorylation in subcutaneous and retroperitoneal adipose tissues in the periparturient dairy cow. Journal of Dairy Science 94, 4514–4523.Google Scholar
Offermanns, S, Colletti, SL, Lovenberg, TW, Semple, G, Wise, A and Ijzerman, AP 2011. International Union of Basic and Clinical Pharmacology. LXXXII: nomenclature and classification of hydroxy-carboxylic acid receptors (GPR81, GPR109A, and GPR109B). Pharmacological Reviews 63, 269–290.CrossRefGoogle ScholarPubMed
Rabelo, E, Rezende, RL, Bertics, SJ and Grummer, RR 2003. Effects of transition diets varying in dietary energy density on lactation performance and ruminal parameters of dairy cows. Journal of Dairy Science 86, 916–925.Google Scholar
Saremi, B, Sauerwein, H, Dänicke, S and Mielenz, M 2012. Technical note: identification of reference genes for gene expression studies in different bovine tissues focusing on different fat depots. Journal of Dairy Science 95, 3131–3138.Google Scholar
Saremi, B, Winand, S, Friedrichs, P, Kinoshita, A, Rehage, J, Dänicke, S, Häussler, S, Breves, G, Mielenz, M and Sauerwein, H 2014. Longitudinal profiling of the tissue-specific expression of genes related with insulin sensitivity in dairy cows during lactation focusing on different fat depots. PLoS One 9, e86211.Google Scholar
Stoddart, LA, Smith, NJ and Milligan, G 2008. International Union of Pharmacology. LXXI. Free fatty acid receptors FFA1, -2, and -3: pharmacology and pathophysiological functions. Pharmacological Reviews 60, 405–417.Google Scholar
Sundvold, H, Brzozowska, A and Lien, S 1997. Characterisation of bovine peroxisome proliferator-activated receptors gamma 1 and gamma 2: genetic mapping and differential expression of the two isoforms. Biochemical and Biophysical Research Communications 239, 857–861.Google Scholar
Titgemeyer, EC, Mamedova, LK, Spivey, KS, Farney, JK and Bradford, BJ 2011. An unusual distribution of the niacin receptor in cattle. Journal of Dairy Science 94, 4962–4967.Google Scholar
Tyagi, S, Gupta, P, Saini, AS, Kaushal, C and Sharma, S 2011. The peroxisome proliferator-activated receptor: a family of nuclear receptors role in various diseases. Journal of Advanced Pharmaceutical Technology and Research 2, 236–240.Google Scholar
Wanders, AJ, Brouwer, IA, Siebelink, E and Katan, MB 2010. Effect of a high intake of conjugated linoleic acid on lipoprotein levels in healthy human subjects. PLoS One 5, e9000.Google Scholar
Wanders, D, Graff, EC and Judd, RL 2012. Effects of high fat diet on GPR109A and GPR81 gene expression. Biochemical and Biophysical Research Communications 425, 278–283.Google Scholar
Xiong, Y, Miyamoto, N, Shibata, K, Valasek, MA, Motoike, T, Kedzierski, RM and Yanagisawa, M 2004. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proceedings of the National Academy of Sciences 101, 1045–1050.Google Scholar
Supplementary material: File

Friedrichs supplementary material

Table S1

Download Friedrichs supplementary material(File)
File 18 KB