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Higher membrane fluidity mediates the increased subcutaneous fatty acid content in pigs fed reduced protein diets

Published online by Cambridge University Press:  17 October 2016

P. A. Lopes ,
A. P. Martins ,
S. V. Martins ,
M. S. Madeira ,
N. C. Santos ,
T. F. Moura ,
J. A. M. Prates  and
G. Soveral
P. A. Lopes*
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, 1300-477 Lisboa, Portugal
A. P. Martins
Affiliation:
Research Institute for Medicines (iMed.ULisboa), Faculdade de Farmácia, Universidade de Lisboa, 1649-003 Lisboa, Portugal
S. V. Martins
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, 1300-477 Lisboa, Portugal
M. S. Madeira
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, 1300-477 Lisboa, Portugal
N. C. Santos
Affiliation:
Instituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, 1649-028 Lisboa, Portugal
T. F. Moura
Affiliation:
Research Institute for Medicines (iMed.ULisboa), Faculdade de Farmácia, Universidade de Lisboa, 1649-003 Lisboa, Portugal
J. A. M. Prates
Affiliation:
CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, 1300-477 Lisboa, Portugal
G. Soveral
Affiliation:
Research Institute for Medicines (iMed.ULisboa), Faculdade de Farmácia, Universidade de Lisboa, 1649-003 Lisboa, Portugal Departamento Bioquímica e Biologia Humana, Faculdade de Farmácia, Universidade de Lisboa, 1649-003 Lisboa, Portugal
*
†E-mail: ampalopes@fmv.ulisboa.pt
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Abstract

The production of pork with moderate amounts of intramuscular fat (IMF) without an increase in subcutaneous fat is highly desirable for the meat industry. Several studies indicate that dietary protein reduction during the growing–finishing period of pigs enhances IMF content, but its consequence on carcass fat deposition is still contradictory. In this study, we hypothesized that the effects of reduced protein diets (RPD), corrected or not with the limiting amino acid lysine, on subcutaneous fat deposition from pigs with distinct genotypes are mediated by adipose membranes biophysical properties. In total, 36 crossbred (Large White×Landrace×Pietrain – a lean genotype) and purebred (Alentejana breed – a fatty genotype) male pigs were randomly assigned to the control group, the RPD group or the reduced protein diet equilibrated for lysine (RPDL) group, allowing a 2×3 factorial arrangement (n=6). Backfat thickness and total fatty acid content were higher in Alentejana relative to crossbred pigs. Although dietary treatments did not change backfat thickness, RPD and RPDL increased total fatty acids content of subcutaneous fat. In order to understand this effect, adipose tissue membranes isolated from pig’s subcutaneous fat were assayed for glycerol permeability and fluidity, using 1,6-diphenyl-1,3,5-hexatriene (DPH) and 1-(4-(trimethylamino)-phenyl)-6-phenyl-1,3,5-hexatriene (TMA-DPH) probes. The glycerol transport across adipose membranes was not mediated by aquaglyceroporins and remained unchanged across dietary groups. Regardless of lysine correction, RPD increased membrane fluidity at the hydrocarbon region (lower DPH fluorescence anisotropy) in both genotypes of pigs. This result was associated with a lower ratio between oleic acid and linoleic acid on membrane’s fatty acid composition. Adipose membrane’s cholesterol content was independent from genotype and diet. Taken together, the present study shows that dietary protein reduction is successful in maintaining backfat thickness, although a negative side effect was observed on total fatty acids in subcutaneous fat, which may be due to changes in the fluidity of adipose membranes.

Keywords

reduced protein dietssubcutaneous fatmembrane fluidityglycerol permeabilitypigs
Type
Research Article
Information
animal , Volume 11 , Issue 4 , April 2017 , pp. 713 - 719
Copyright
© The Animal Consortium 2016 

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Footnotes

a

These authors contributed equally to this article.

References

Alves, SP and Bessa, RJ 2009. Comparison of two gas-liquid chromatograph columns for the analysis of fatty acids in ruminant meat. Journal of Chromatography A 1216, 5130–5139.Google Scholar
Bradford, MM 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Campos, E, Moura, TF, Oliva, A, Leandro, P and Soveral, G 2011. Lack of Aquaporin 3 in bovine erythrocyte membranes correlates with low glycerol permeation. Biochemical and Biophysical Research Communications 408, 477–481.Google Scholar
Christie, WW, Dobson, G and Adlof, RO 2007. A practical guide to the isolation, analysis and identification of conjugated linoleic acid. Lipids 42, 1073–1084.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.Google Scholar
D´Souza, DN, Pethick, DW, Dunshea, FR, Pluske, JR and Mullan, BP 2008. Reducing the lysine to energy content in the grower growth phase diet increases intramuscular fat and improves the eating quality of the longissimus thoracis muscle of gilts. Australian Journal of Experimental Agriculture 48, 1105–1109.Google Scholar
Folch, J, Lees, M and Sloane Stanley, GH 1957. A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497–509.Google Scholar
Garcia-Valverde, R, Barea, R, Lara, L, Nieto, R and Aguilera, J 2008. The effects of feeding level upon protein and fat deposition in Iberian heavy pigs. Livestock Science 114, 263–273.Google Scholar
Huff-Lonergan, E, Bass, TJ, Malek, M, Dekkers, JCM, Prusa, K and Rothschild, MF 2002. Correlations among selected pork quality traits. Journal of Animal Science 80, 617–627.Google Scholar
Jeremiah, LE, Gibson, JP, Gibsona, LL, Ballc, RO, Akerd, C and Fortin, A 1999. The influence of breed, gender, and PSS (Halothane) genotype on meat quality, cooking loss, and palatability of pork. Food Research International 32, 59–71.Google Scholar
Jung, J, Shim, Kwan, Na, C and Choe, H 2015. Studies on intramuscular fat percentage in live swine using real-time ultrasound to determine pork quality. Asian-Australasian Journal of Animal Sciences 28, 318–322.Google Scholar
Kishida, K, Kuriyama, H, Funahashi, T, Shimomura, I, Kihara, S, Ouchi, N, Nishida, M, Nishizawa, H, Matsuda, M, Takahashi, M, Hotta, K, Nakamura, T, Yamashita, S, Tochino, Y and Matsuzawa, Y 2000. Aquaporin adipose, a putative glycerol channel in adipocytes. Journal of Biological Chemistry 275, 20896–208902.Google Scholar
Kondo, H, Shimomura, I, Kishida, K, Kuriyama, H, Makino, Y, Nishizawa, H, Matsuda, M, Maeda, N, Nagaretani, H, Kihara, S, Kurachi, Y, Nakamura, T, Funahashi, T and Matsuzawa, Y 2002. Human aquaporin adipose (AQPap) gene. Genomic structure, promoter analysis and functional mutation. European Journal of Biochemistry 269, 1814–1826.CrossRefGoogle ScholarPubMed
Lebret, B 2008. Effects of feeding and rearing systems on growth, carcass composition and meat quality in pigs. Animal 2, 1548–1558.Google Scholar
Lee, AG 1985. Some principles of membrane structure. Proceedings of the Nutrition Society 44, 147–156.Google Scholar
Madeira, MS, Alfaia, CM, Costa, P, Lopes, PA, Lemos, JP, Bessa, RJ and Prates, JA 2014. The combination of arginine and leucine supplementation of reduced crude protein diets for boars increases eating quality of pork. Journal of Animal Science 92, 2030–2040.Google Scholar
Madeira, MS, Alfaia, CM, Costa, P, Lopes, PA, Martins, SV, Lemos, JP, Moreira, O, Santos-Silva, J, Bessa, RJ and Prates, JA 2015. Effect of betaine and arginine in lysine-deficient diets on growth, carcass traits and pork quality. Journal of Animal Science 93, 4721–4733.Google Scholar
Madeira, MS, Costa, P, Alfaia, CM, Lopes, PA, Bessa, RJ, Lemos, JP and Prates, JA 2013. The increased intramuscular fat promoted by dietary lysine restriction in lean but not in fatty pig genotypes improves pork sensory attributes. Journal of Animal Science 91, 3177–3187.Google Scholar
Marsh, D 2009. Cholesterol-induced fluid membrane domains: a compendium of lipid-raft ternary phase diagrams. Biochimica et Biophysica Acta 1788, 2114–2123.CrossRefGoogle ScholarPubMed
Martins, AP, Lopes, PA, Costa, AS, Martins, SV, Santos, NC, Prates, JA, Moura, TF and Soveral, G 2011. Differential mesenteric fat deposition in bovines fed on silage or concentrate is independent of glycerol membrane permeability. Animal 5, 1949–1956.Google Scholar
Martins, AP, Lopes, PA, Martins, SV, Madeira, A, Santos, NC, Prates, JA, Moura, TF and Soveral, G 2010. Conjugated linoleic acid reduces permeability and fluidity of adipose plasma membranes from obese Zucker rats. Biochemical and Biophysical Research Communications 398, 199–204.Google Scholar
Nieto, R, Miranda, A, Garcia, MA and Aguilera, JF 2002. The effect of dietary protein content and feeding level on the rate of protein deposition and energy utilization in growing Iberian pigs from 15 to 50 kg body weight. British Journal of Nutrition 88, 39–49.Google Scholar
Pebay-Peyroula, E, Dufourc, EJ and Szabo, AG 1994. Location of diphenyl-hexatriene and trimethylammonium-diphenyl-hexatriene in dipalmitoylphosphatidylcholine bilayers by neutron diffraction. Biophysical Chemistry 53, 45–56.CrossRefGoogle ScholarPubMed
Raes, K, Fievez, V, Chow, TT, Ansorena, D, Demeyer, D and De Smet, S 2004. Effect of diet and dietary fatty acids on the transformation and incorporation of C18 fatty acids in double-muscled Belgian Blue young bulls. Journal of Agricultural and Food Chemistry 52, 6035–6041.Google Scholar
Ramalho, F 2007. Aspectos de produção do porco de Raça Alentejana. Suinicultura 75, 68–69.Google Scholar
Schwenk, RW, Holloway, GP, Luiken, JJ, Bonen, A and Glatz, JF 2010. Fatty acid transport across the cell membrane: regulation by fatty acid transporters. Prostaglandins Leukotrienes and Essential Fatty Acids 82, 149–154.CrossRefGoogle ScholarPubMed
Soveral, G, Macey, RI and Moura, TF 1997. Mechanical properties of brush border membrane vesicles from kidney proximal tubule. Journal of Membrane Biology 158, 209–217.Google Scholar
Suárez-Belloch, J, Guada, JA and Latorre, MA 2015. Effects of sex and dietary lysine on performances and serum and meat traits in finisher pigs. Animal 9, 1731–1739.Google Scholar
Teye, GA, Sheard, PR, Whittington, FM, Nute, GR, Stewart, A and Wood, JD 2006. Influence of dietary oils and protein level on pork quality. 1. Effects on muscle fatty acid composition, carcass, meat and eating quality. Meat Science 73, 157–165.Google Scholar
Van Barneveld, RJ 2003. Modern pork production – balancing efficient growth and feed conversion with product quality requirements and consumer demands. Asia Pacific Journal of Clinical Nutrition 12 (suppl.), S31.Google Scholar
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.Google Scholar
Wood, JD, Enser, M, Fisher, AV, Nute, GR, Sheard, PR, Richardson, RI, Hughes, SI and Whittington, FM 2008. Fat deposition, fatty acid composition and meat quality: a review. Meat Science 78, 343–358.Google Scholar
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.Google Scholar
York, DA 1985. Alterations in membrane function, organization and composition in the obese ob/ob mouse. Proceedings of the Nutrition Society 44, 189–200.Google Scholar