Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-19T06:01:31.634Z Has data issue: false hasContentIssue false
  • English
  • Français

Contrasting cellularity on fat deposition in the subcutaneous adipose tissue and longissimus lumborum muscle from lean and fat pigs under dietary protein reduction

Published online by Cambridge University Press:  18 March 2014

P. A. Lopes ,
A. S. H. Costa ,
P. Costa ,
V. M. R. Pires ,
M. S. Madeira ,
F. Achega ,
R. M. A. Pinto  and
J. A. M. Prates
P. A. Lopes*
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, Pólo Universitário do Alto da Ajuda, 1300-477 Lisboa, Portugal
A. S. H. Costa
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, Pólo Universitário do Alto da Ajuda, 1300-477 Lisboa, Portugal
P. Costa
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, Pólo Universitário do Alto da Ajuda, 1300-477 Lisboa, Portugal
V. M. R. Pires
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, Pólo Universitário do Alto da Ajuda, 1300-477 Lisboa, Portugal
M. S. Madeira
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, Pólo Universitário do Alto da Ajuda, 1300-477 Lisboa, Portugal
F. Achega
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, Pólo Universitário do Alto da Ajuda, 1300-477 Lisboa, Portugal
R. M. A. Pinto
Affiliation:
iMed.UL, Faculdade de Farmácia, Universidade de Lisboa, Avenida Professor Gama Pinto, 1649-003 Lisboa, Portugal
J. A. M. Prates*
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, Pólo Universitário do Alto da Ajuda, 1300-477 Lisboa, Portugal
*
†E-mail: [email protected]; [email protected]
†E-mail: [email protected]; [email protected]
Get access

Abstract

The production of pork with high amounts of intramuscular fat (IMF) without an increase in subcutaneous fat is highly desirable for the pig industry and consumers. Herein, we question the impact of dietary protein reduction (18% v. 13%) on fat deposition in the subcutaneous adipose tissue (SAT) and longissimus lumborum (LL) muscle using genetically diverse pigs for body fatness (lean v. fat). A clear effect of genotype was observed on plasma insulin (P=0.004) and leptin (P<0.001), as well as on backfat thickness (P<0.001), with the fat pigs having higher values. Accordingly, IMF was higher in the fat pigs, when compared with their lean counterparts (P=0.003), which was supported by enlarged adipocytes (P<0.001). The area of lipid droplets within the LL fibres (P=0.039) and extramyocellular lipids number (P=0.017) were increased in pigs fed reduced protein diets, regardless of genotype, which is consistent with higher levels of plasma triacylglycerols (P=0.002). The gene-expression pattern of lipogenic factors in the SAT was distinct from the LL muscle. In the SAT, PPARG expression was similar among genotypes (P>0.05), whereas in the LL muscle it was higher in the lean pigs (P=0.023), especially when fed on low protein diet (P=0.057). The CEBPA and FABP4 mRNA levels were increased in the SAT of fat pigs (P<0.001), without changes in the LL muscle (P>0.05). The influence of diet on FABP4 expression in the SAT was dependent on pig’s genetic background (P=0.005). In conclusion, fat deposition was clearly influenced by genotype and, to a lesser extent, by dietary protein level, the SAT being more sensitive than the LL muscle. One can speculate that the pathways involved in lipid metabolism are downregulated in intramuscular adipocytes when compared with SAT fat cells. This result might be a direct consequence of the relatively low proportion of adipocytes found in the LL muscle.

Keywords

pigreduced protein dietsfat depositionsubcutaneous adipose tissue and longissimus lumborum musclegene expression
Type
Full Paper
Information
animal , Volume 8 , Issue 4 , April 2014 , pp. 629 - 637
Copyright
© The Animal Consortium 2014 

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

Alonso, V, Campo, M del, M, Provincial, L, Roncalés, P and Beltrán, JA 2010. Effect of protein level in commercial diets on pork meat quality. Meat Science 85, 7–14.CrossRefGoogle ScholarPubMed
AOAC 2000. Official methods of analysis (ed. W Horwitz). 17th edition. AOAC, Gaithersburg, MD, USA.Google Scholar
Berryman, DE, List, EO, Sackman-Sala, L, Lubbers, E, Munn, R and Kopchick, JJ 2011. Growth hormone and adipose tissue: beyond the adipocyte. Growth Hormone & IGF Research 21, 113–123.CrossRefGoogle ScholarPubMed
Cánovas, A, Quintanilla, R, Amills, M and Pena, RN 2010. Muscle transcriptomic profiles in pigs with divergent phenotypes for fatness traits. BMC Genomics 11, 372–386.CrossRefGoogle ScholarPubMed
Cho, ES, Kwon, SG, Kim, JH, Park, DH, Kim, TW, Nam, J, Jang, IS, Choi, J-S, Bang, WY and Kim, CW 2011. Study for the expression of adiponectin, fatty acid binding protein (FABP)4, stearoyl-CoA desaturase (SCD) genes and the methylation of SCD promoter in porcine muscle and fat tissues. African Journal of Agricultural Research 6, 6425–6431.Google Scholar
Corino, C, Di Giancamillo, A, Rossi, R and Domeneghini, C 2005. Dietary conjugated linoleic acid affects morphofunctional and chemical aspects of subcutaneous adipose tissue in heavy pigs. The Journal of Nutrition 135, 1444–1450.CrossRefGoogle ScholarPubMed
Corino, C, Musella, M, Pastorelli, G, Rossi, R, Paolone, K, Costanza, L, Manchisi, A and Maiorano, G 2008. Influences of dietary conjugated linoleic acid (CLA) and total lysine content on growth, carcass characteristics and meat quality of heavy pigs. Meat Science 79, 307–316.CrossRefGoogle ScholarPubMed
Da Costa, N, Mcgillivray, C, Bai, Q, Wood, JD, Evans, G and Chang, KC 2004. Restriction of dietary energy and protein induces molecular changes in young porcine skeletal muscles. The Journal of Nutrition 134, 2191–2199.CrossRefGoogle ScholarPubMed
Damon, M, Louveau, I, Lefaucheur, L, Lebret, B, Vincent, A, Leroy, P, Sanchez, MP, Herpinand, P and Gondret, F 2006. Number of intramuscular adipocytes and fatty acid binding protein-4 content are significant indicators of intramuscular fat level in crossbred Large White×Duroc pigs. Journal of Animal Science 84, 1083–1092.CrossRefGoogle Scholar
Doran, O, Moule, SK, Teye, GA, Whittington, FM, Hallett, KG and Wood, JD 2006. A reduced protein diet induces stearoyl-CoA desaturase protein expression in pig muscle but not in subcutaneous adipose tissue: relationship with intramuscular lipid formation. British Journal of Nutrition 95, 609–617.CrossRefGoogle Scholar
Furuhashi, M and Hotamisligil, GS 2008. Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nature Reviews Drug Discovery 7, 489–503.CrossRefGoogle ScholarPubMed
Gondret, F and Lebret, B 2002. Feeding intensity and dietary protein level affect adipocyte cellularity and lipogenic capacity of muscle homogenates in growing pigs, without modification of the expression of sterol regulatory element binding protein. Journal of Animal Science 80, 3184–3193.CrossRefGoogle ScholarPubMed
Gregoire, FM, Smas, CM and Sul, HS 1998. Understanding adipocyte differentiation. Physiological Reviews 78, 783–809.CrossRefGoogle ScholarPubMed
Guillerm-Regost, C, Louveau, I, Sébert, SP, Damon, M, Champ, MM and Gondret, F 2006. Cellular and biochemical features of skeletal muscle in obese Yucatan minipigs. Obesity 14, 1700–1707.CrossRefGoogle ScholarPubMed
Guo, X, Tang, R, Wang, W, Liu, D and Wang, K 2011. Effects of dietary protein/carbohydrate ratio on fat deposition and gene expression of peroxisome proliferator activated receptor γ and heart fatty acid-binding protein of finishing pigs. Livestock Science 140, 111–116.CrossRefGoogle Scholar
Guo, Z 2007. Intramyocellular lipid kinetics and insulin resistance. Lipids in Health and Disease 6, 18–25.CrossRefGoogle ScholarPubMed
Hocquette, JF, Gondret, F, Baeza, E, Medale, F, Jurie, C and Pethick, EW 2010. Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, and identification of putative markers. Animal 4, 303–319.CrossRefGoogle ScholarPubMed
Houseknecht, KL, Baile, CA, Matteri, RL and Spurlock, ME 1998. The biology of leptin: a review. Journal of Animal Science 76, 1405–1420.CrossRefGoogle ScholarPubMed
Kelley, DE and Goodpaster, BH 2001. Skeletal muscle triglyceride – an aspect of regional adiposity and insulin resistance. Diabetes Care 24, 933–941.CrossRefGoogle ScholarPubMed
Koopman, R, Schaart, G and Hesselink, MKC 2001. Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochemistry and Cell Biology 116, 63–68.CrossRefGoogle ScholarPubMed
Koranyi, LI, Bourey, RE, Vuorinen-Markkola, H, Koivisto, VA, Mueckler, M, Permutt, MA and Yki-Jiirvinen, H 1991. Level of skeletal muscle glucose transporter protein correlates with insulin-stimulated whole body glucose disposal in man. Diabetologia 34, 763–765.CrossRefGoogle ScholarPubMed
Le Lay, S and Dugail, I 2009. Connecting lipid droplet biology and the metabolic syndrome. Progress in Lipid Research 48, 191–195.CrossRefGoogle ScholarPubMed
Lebret, B, Noblet, Juin H and Bonneau, M 2001. The effects of two methods of increasing age at slaughter on carcass and muscle traits and meat sensory quality in pigs. Animal Science 72, 87–194.CrossRefGoogle Scholar
Liu, Y, Wang, Z, Yin, W, Li, Q, Cai, M, Zhang, C, Xiao, J, Hou, J, Li, H and Zu, X 2007. Severe insulin resistance and moderate glumerulosclerosis in a minipig model induced by high-fat/high-sucrose/high-cholesterol diet. Experimental Animals 56, 11–20.CrossRefGoogle Scholar
Madeira, MS, Pires, VR, Alfaia, CM, Costa, ASH, Luxton, R, Doran, O, Bessa, RJB and Prates, JAM 2013. Differential effects of reduced protein diets on fatty acid composition and gene expression in muscle and subcutaneous adipose tissue of Alentejana purebred and Large White×Landrace×Pietrain crossbred pigs. British Journal of Nutrition 110, 216–229.CrossRefGoogle Scholar
Matthews, DR, Hosker, JP, Rudenski, AS, Naylor, BA, Treacher, DF and Turner, RC 1985. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419.CrossRefGoogle ScholarPubMed
Michal, JJ, Zhang, ZW, Gaskins, CT and Jiang, Z 2006. The bovine fatty acid binding protein 4 gene is significantly associated with marbling and subcutaneous fat depth in Wagyu×Limousin F2 crosses. Animal Genetics 37, 400–402.CrossRefGoogle Scholar
Ronti, T, Lupattelli, G and Mannarino, E 2006. The endocrine function of adipose tissue: an update. Clinical Endocrinology 64, 355–365.CrossRefGoogle ScholarPubMed
Sturges, HA 1926. The choice of a class-interval. Journal of the American Statistical Association 21, 65–66.CrossRefGoogle Scholar
Tontonoz, P and Spiegelman, BM 2008. Fat and beyond: the diverse biology of PPARgamma. Annual Review of Biochemistry 77, 289–312.CrossRefGoogle ScholarPubMed
Witte, DP, Ellis, M, McKeith, FK and Wilson, ER 2000. Effect of dietary lysine level and environmental temperature during the finishing phase on the intramuscular fat content of pork. Journal of Animal Science 78, 1272–1276.CrossRefGoogle ScholarPubMed
Wood, JD, Nute, GR, Richardson, RI, Whittington, FM, Southwood, O, Plastow, G, Mansbridge, R, Da Costa, N and Chang, KC 2004. Effects of breed, diet and muscle on fat deposition and eating quality in pigs. Meat Science 67, 651–667.CrossRefGoogle ScholarPubMed
Zhou, G, Wang, S, Wang, Z, Zhu, X, Shu, G, Liao, W, Yu, K, Gao, P, Xi, Q, Wang, X, Zhang, Y, Yuan, L and Jiang, Q 2010. Global comparison of gene expression profiles between intramuscular and subcutaneous adipocytes of neonatal landrace pig using microarray. Meat Science 86, 440–450.CrossRefGoogle ScholarPubMed
Zhou, J, Zhao, RQ, Wei, XH, Xia, D, Xu, QF and Chen, J 2004. Developmental patterns of serum leptin levels, leptin gene expression in adipose tissue and Ob-Rb gene expression in hypothalamus of Erhualian and Large White pigs. Science in China Series C: Life Sciences 47, 190–196.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Lopez supplementary material

Lopez supplementary material

Download Lopez supplementary material(PDF)
PDF 179.3 KB