Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-24T13:57:11.555Z Has data issue: false hasContentIssue false

Expression of genes involved in adipogenesis and lipid metabolism in subcutaneous adipose tissue and longissimus muscle in low-marbled Pirenaica beef cattle

Published online by Cambridge University Press:  24 June 2016

B. Soret*
Affiliation:
Departamento de Producción Agraria, Universidad Pública de Navarra, Campus Arrosadia, 31006 Pamplona, Spain
J. A. Mendizabal
Affiliation:
Departamento de Producción Agraria, Universidad Pública de Navarra, Campus Arrosadia, 31006 Pamplona, Spain
A. Arana
Affiliation:
Departamento de Producción Agraria, Universidad Pública de Navarra, Campus Arrosadia, 31006 Pamplona, Spain
L. Alfonso
Affiliation:
Departamento de Producción Agraria, Universidad Pública de Navarra, Campus Arrosadia, 31006 Pamplona, Spain
*
Get access

Abstract

The ability to accumulate intramuscular fat (IMF) is a highly variable characteristic in beef cattle. In breeds with a low tendency to accumulate IMF, this can lead to compromised meat quality because of the contribution of fat to such organoleptic attributes as juiciness and taste. This study considered adiposity and gene expression of some of the main markers involved in adipogenesis and lipid metabolism in the subcutaneous (SC) adipose tissue (AT) and the longissimus thoracis muscle (LM) and investigated differences in adipogenic regulation between the tissues during growth and fattening under different conditions. Pirenaica beef cattle were chosen for the study due to the breed’s low tendency to accumulate IMF and the breed’s regional importance. The young Pirenaica bulls used (n=16) were allocated to four groups and slaughtered at 6, 12 and 18 months. From 12 months onwards the bulls slaughtered at 18 months were fed diets having different energy densities. Backfat thickness increased from 6 to 12 months (P<0.05) but then was unchanged, while other fattening parameters such as percentage chemical fat and marbling did not vary. The adipose cell size distribution displayed a bimodal distribution for SC adipocytes and a unimodal distribution for IMF cells, suggestive of tissue-specific hyperplasia. Gene expression of peroxisome proliferator-activated receptor γ (PPARG), CCAAT/enhancer-binding protein α (CEBPA), sterol regulatory element-binding transcription factor 1 (SREBF1), wingless-type MMTV integration site family 10B (WNT10B), fatty acid-binding protein 4 (FABP4), acetyl Co-A carboxylase α, lipoprotein lipase and fatty acid synthase (FASN) were determined by real-time quantitative PCR. Expression did not differ between the experimental groups within the tissues but did differ between the tissues: PPARG, FABP4 and FASN were upregulated in the SC AT, while CEBPA, WNT10B and SREBF1 were upregulated in the LM. Although age and diet energy density did not have a significant effect on increasing the amount of IMF, these factors could have influenced adipocyte development in this tissue differently than in the SC AT. This was evidenced by the different size distributions of the cells in the two tissues, and the differing expression patterns of certain markers in the SC AT and the LM, which may indicate a differential role of PPARG and WNT10B in triggering adipocyte proliferation and fat accumulation capacity.

Type
Research Article
Copyright
© The Animal Consortium 2016 

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

Alfonso, L and Mendizabal, JA 2016. Characterizing adipocyte size distribution for adipose tissue studies in animal production. ITEA 112, 147–161.Google Scholar
Bennet, CN, Ross, SE, Longo, KA, Bajnok, L, Hemati, N, Johnson, KW, Harrison, SD and MacDougald, OA 2002. Regulation of Wnt signaling during adipogenesis. The Journal of Biological Chemistry 277, 3099831004.CrossRefGoogle Scholar
Chung, KY, Lunt, DK, Kawachi, H, Yano, H and Smith, SB 2007. Lipogenesis and stearoyl-CoA desaturase gene expression and enzyme activity in adipose tissue of short- and long-fed Angus and Wagyu steers fed corn- or hay-based diets. Journal of Animal Science 85, 380387.Google Scholar
Cristancho, AG and Lazar, MA 2011. Forming functional fat: a growing understanding of adipocyte differentiation. Nature Reviews Molecular Cell Biology 28, 722734.Google Scholar
Duarte, MS, Gionbelli, MP, Paulino, PVR, Serão, NVL, Nascimento, CS, Botelho, ME, Martins, TS, Filho, SCV, Dodson, MV, Guimarães, SEF and Du, M 2014. Maternal overnutrition enhances mRNA expression of adipogenic markers and collagen deposition in skeletal muscle of beef cattle fetuses. Journal of Animal Science 92, 38463854.Google Scholar
EU 2009. Council Regulation (EC) No. 1099/2009 of 24 September 2009 on the protection of animals at the time of killing. Official Journal of the European Union L303, 130.Google Scholar
EU 2010. Directive No. 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Official Journal of the European Union L276, 3379.Google Scholar
Fajas, L, Fruchart, JC and Auwers, J 1998. Transcriptional control of adipogenesis. Current Opinion in Cell Biology 10, 165173.Google Scholar
Gilbert, CD, Lunt, DK, Miller, RK and Smith, SB 2003. Carcass, sensory, and adipose tissue traits of Brangus steers fed casein-formaldehyde-protected starch and/or canola lipid. Journal of Animal Science 81, 24572468.Google Scholar
Gotoh, T, Albrecht, E, Teuscher, F, Kawabata, K, Sakashita, K, Iwamoto, H and Wegner, J 2009. Differences in muscle and fat accretion in Japanese Black and European cattle. Meat Science 82, 300308.CrossRefGoogle ScholarPubMed
Hartigan, JA and Hartigan, PM 1985. The dip test of unimodality. The Annals of Statistics 13, 7084.Google Scholar
Hausman, GJ, Dodson, MV, Ajuwon, K, Azain, M, Barnes, KM, Guan, LL, Jiang, Z, Poulos, SP, Sainz, RD, Smith, S, Spurlock, M, Novakofski, J, Fernyhough, ME and Bergen, WG 2009. Board-invited review: the biology and regulation of preadipocytes and adipocytes in meat animals. Journal of Animal Science 87, 12181246.Google Scholar
Hausman, GJ and Poulos, S 2004. Recruitment and differentiation of intramuscular preadipocytes in stromal-vascular cell cultures derived from neonatal pig semitendinosus muscles. Journal of Animal Science 82, 429437.Google Scholar
Jeong, JY, Kim, JS, Nguyen, TH, Lee, H-J and Baik, M 2013. Wnt/b-catenin signaling and adipogenic genes are associated with intramuscular fat content in the longissimus dorsi muscle of Korean cattle. Animal Genetics 44, 627635.Google Scholar
Jo, J, Shreif, Z and Periwal, V 2012. Quantitative dynamics of adipose cells. Adipocyte 1, 8088.Google Scholar
Key, CN, Perkins, SD, Bratcher, CL, Kriese-Anderson, LA and Brandebourg, TD 2013. Grain feeding coordinately alters expression patterns of transcription factor and metabolic genes in subcutaneous adipose tissue of crossbred heifers. Journal of Animal Science 91, 26162627.Google Scholar
Kim, JB, Wright, HM, Wright, M and Spiegleman, BM 1998. ADD1/SREBP1 activates PPARG through the production of endogenous ligand. Proceedings of the National Academy of Sciences of the United States of America 95, 43334337.Google Scholar
Maltin, C, Balcerzak, D, Tilley, R and Delday, M 2003. Determinants of meat quality: tenderness. Proceedings of the Nutrition Society 62, 337347.Google Scholar
Marques, BG, Hausman, DB and Martin, RJ 1998. Association of fat cell size and paracrine growth factors in development of hyperplastic obesity. American Journal of Physiology 275, R1898R1908.Google Scholar
McLaughlin, T, Sherman, A, Tsao, P, Gonzalez, O, Yee, G, Lamendola, C, Reaven, GM and Cushman, SW 2007. Enhanced proportion of small adipose cells in insulin resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis. Diabetologia 50, 17071715.CrossRefGoogle ScholarPubMed
Mendizabal, JA, Purroy, A, Indurain, G and Insausti, K 2005. Medida del grado de veteado de la carne mediante análisis de imagen. In Estandarización de las metodologías para evaluar la calidad del producto (animal vivo, canal, carne y grasa) en los rumiantes (ed. V Cañeque and C Sañudo), pp. 251256. INIA, Serie Ganadera 3, Madrid, Spain.Google Scholar
Mendizabal, JA, Soret, B, Purroy, A, Arana, A and Horcada, A 1997. Influence of sex on celullarity and lipogenic enzymes of Spanish lamb breeds (Lacha and Rasa Aragonesa). Animal Science 64, 283289.Google Scholar
Miller, ME, Cross, HR, Lunt, DK and Smith, SB 1991. Lipogenesis in acute and 48-hour cultures of bovine intramuscular and subcutaneous adipose tissue explants. Journal of Animal Science 69, 162170.Google Scholar
Moisá, SJ, Shike, WW, Faulkner, DB, Meteer, WT, Keisler, D and Loor, JJ 2014. Central role of the PPARG network in coordinating beef cattle intramuscular adipogenesis in response to weaning age and nutrition. Gene Regulation and Systems Biology 8, 1732.CrossRefGoogle ScholarPubMed
Moura, J, Jin, W, He, M, McAllister, T and Guan, LL 2013. Elucidation of molecular mechanisms of physiological variations between subcutaneous and visceral fat depots under different nutritional regimes. PLoS One 8, e83211.Google Scholar
Pickworth, CL, Loerch, SC, Velleman, SG, Pate, JL, Poole, DH and Fluharty, FL 2011. Adipogenic differentiation state-specific gene expression as related to bovine carcass adiposity. Journal of Animal Science 89, 355366.Google Scholar
Rodbell, M 1964. Metabolism of isolated fat cells. Journal of Biological Chemistry 239, 375380.CrossRefGoogle ScholarPubMed
Rosen, DE and Spiegelman, BM 2006. Adipocytes as energy balance regulators and glucose homeostasis. Nature 444, 847853.Google Scholar
Savell, JW and Cross, HR 1988. The role of fat in the palatability of beef, pork, and lamb. In Designing foods: animal product options in the marketplace (ed. DL Call), pp. 345355. National Research Council, Washington, DC, USA.Google Scholar
Smith, SB and Crouse, JD 1984. Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. Journal of Nutrition 114, 792800.CrossRefGoogle ScholarPubMed
Soula, HA, Julienne, H, Soulage, CO and Géloen, A 2013. Modelling adipocytes size distribution. Journal of Theoretical Biology 332, 8995.Google Scholar
Steibel, JP, Poletto, R, Coussens, PM and Rosa, GJM 2009. A powerful and flexible linear mixed model framework for the analysis of relative quantification RT-PCR data. Genomics 94, 146152.Google Scholar
Tchoukalova, YD, Sarr, MG and Jensen, MD 2004. Measuring committed preadipocytes in human adipose tissue from severely obese patients by using adipocyte fatty acid binding protein. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 287, R1132R1140.Google Scholar
Vernon, RG 1986. The growth and metabolism of adipocytes. In Control and manipulation of animal growth (ed. PJ Buttery, NB Haynes and DB Lindsay), pp. 6783. Butterworths, London, UK.Google Scholar
Yamada, T and Nakanishi, N 2012. Effects of the roughage/concentrate ratio on the expression of angiogenic growth factors in adipose tissue of fattening Wagyu steers. Meat Science 90, 807813.CrossRefGoogle ScholarPubMed
Supplementary material: File

Soret supplementary material

Tables S1-S6

Download Soret supplementary material(File)
File 44.8 KB