Skip to main content Accessibility help

Restriction of dietary protein does not promote hepatic lipogenesis in lean or fatty pigs

  • Marta S. Madeira (a1), Virgínia M. R. Pires (a1), Cristina M. Alfaia (a1), Paula A. Lopes (a1), Susana V. Martins (a1), Rui M. A. Pinto (a2) and José A. M. Prates (a1)...


The influence of genotype (lean v. fatty) and dietary protein level (normal v. reduced) on plasma metabolites, hepatic fatty acid composition and mRNA levels of lipid-sensitive factors is reported for the first time, using the pig as an experimental model. The experiment was conducted on forty entire male pigs (twenty lean pigs of Large White×Landrace×Pietrain cross-breed and twenty fatty pigs of Alentejana purebreed) from 60 to 93 kg of live weight. Each pig genotype was divided into two subgroups, which were fed the following diets: a normal protein diet (NPD) equilibrated for lysine (17·5 % crude protein and 0·7 % lysine) and a reduced protein diet (RPD) not equilibrated for lysine (13·1 % crude protein and 0·4 % lysine). The majority of plasma metabolites were affected by genotype, with lean pigs having higher contents of lipids, whereas fatty pigs presented higher insulin, leptin and urea levels. RPD increased plasma TAG, free fatty acids and VLDL-cholesterol compared with NPD. Hepatic total lipids were higher in fatty pigs than in the lean genotype. RPD affected hepatic fatty acid composition but had a slight influence on gene expression levels in the liver. Sterol regulatory element-binding factor 1 was down-regulated by RPD, and fatty acid desaturase 1 (FADS1) and fatty acid binding protein 4 (FABP4) were affected by the interaction between genotype and diet. In pigs fed RPD, FADS1 was up-regulated in the lean genotype, whereas FABP4 increased in the fatty genotype. Although there is a genotype-specific effect of dietary protein restriction on hepatic lipid metabolism, lipogenesis is not promoted in the liver of lean or fatty pigs.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Restriction of dietary protein does not promote hepatic lipogenesis in lean or fatty pigs
      Available formats

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Restriction of dietary protein does not promote hepatic lipogenesis in lean or fatty pigs
      Available formats

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Restriction of dietary protein does not promote hepatic lipogenesis in lean or fatty pigs
      Available formats


Corresponding author

* Corresponding author: J. A. M. Prates, fax +351 213 652 895, email


Hide All

Both authors contributed equally to this work.



Hide All
1. Dodson, MV, Hausman, GJ, Guan, L, et al. (2010) Lipid metabolism, adipocyte depot physiology and utilization of meat animals as experimental models for metabolic research. Int J Biol Sci 6, 691699.
2. DeVol, DL, McKeith, FK, Bechtel, PJ, et al. (1988) Variation in composition and palatability traits and relationships between muscle characteristics and palatability in a random sample of pork carcasses. J Anim Sci 66, 385395.
3. Doran, O, Moule, SK, Teye, GA, et al. (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. Br J Nutr 95, 609617.
4. D’Souza, DN, Pethick, DW, Dunshea, FR, et al. (2008) Reducing the lysine to energy content in the grower growth phase diet increases intramuscular fat and improves the eating quality of the 563 longissimus thoracis muscle of gilts. Aust J Exp Agric 48, 11051109.
5. Madeira, MS, Pires, VMR, Alfaia, CM, et al. (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. Br J Nutr 110, 216229.
6. Witte, DP, Ellis, M, Mckeith, FK, et al. (2000) Effect of dietary lysine level and environmental temperature during the finishing phase on the intramuscular fat content of pork. J Anim Sci 78, 12721276.
7. Horton, JD, Golstein, JL & Brown, MS (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109, 11251131.
8. Schadinger, SE, Bucher, NLR, Schreiber, BM, et al. (2005) PPARgamma2 regulated lipogenesis and lipid accumulation in steatotic hepatocytes. Am J Physiol Endocrinol Metab 288, 11951205.
9. Corominas, J, Ramayo-Caldas, Y, Puig-Oliveras, A, et al. (2013) Analysis of porcine adipose tissue transcriptome reveals differenced in the novo fatty acid synthesis in pigs with divergent muscle fatty acid composition. BMC Genomics 14, 843.
10. Nafikov, RA & Beitz, DC (2007) Carbohydrate and lipid metabolism in farm animals. J Nutr 137, 702705.
11. Vallim, T & Salter, AM (2010) Regulation of hepatic gene expression by saturated fatty acids. Prostaglandins Leukot Essent Fatty Acids 82, 211218.
12. Nakamura, MT & Nara, TY (2004) Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Ann Rev Nutr 24, 345376.
13. Zhao, S, Wang, J, Song, X, et al. (2010) Impact of dietary protein on lipid metabolism-related gene expression in porcine adipose tissue. Nutr Metab 7, 6.
14. Denechaud, PD, Bossard, P & Lobaccaro, JM (2008) ChREBP, but not LXRs, is required for the induction of glucose-regulated genes in mouse liver. J Clin Invest 118, 956964.
15. Hocquette, JF, Gondret, F, Baéza, E, et al. (2010) Intramuscular fat content in meat-producing animals: development, genetic and nutritional control and identification of putative markers. Animal 4, 303319.
16. Garcia-Vaverde, R, Barea, R, Lara, L, et al. (2008) The effects of feeding level upon protein and fat deposition in Iberian heavy pigs. Livest Sci 114, 264273.
17. Ramalho, F (2007) Apectos de produção do porco de Raça Alentejana (Production aspects of the Alentejana pig breed). Suinicultura 75, 6869.
18. Association of Official Analytical Chemists (2000) Official Methods of Analysis, 17th ed. Arlington, VA: AOAC.
19. Clegg, KM (1956) The application of the anthrone reagent to the estimation of starch in cereals. J Sci Food Agric 70, 4044.
20. Sukhija, PS & Palmquist, DL (1988) Rapid method for determination of total fatty acid content and composition of feedstuffs and feces. J Agric Food Chem 36, 12021206.
21. Association of Official Analytical Chemists (2005) Amino acid analysis using Zorbax Eclipse-AAA columns and the Agilent 1100 HPLC. In Official Methods of Analysis of the Association of Official Analytical Chemists International, 18th ed., p. 473 [GW Latimer and W Horwitz, editors]. Gaithersburg, MD: AOAC International.
22. Henderson, JW, Ricker, RD, Bidlingmeyer, BA, et al. (2000) Rapid, Accurate, Sensitive and Reproducible Analysis of Amino Acids. Palo Alto, CA: Agilent Technologies.
23. Friedewald, WT, Levy, RI & Fredrickson, DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18, 499502.
24. Covaci, A, Voorspoels, S, Thomsen, C, et al. (2006) Evaluation of total lipids using enzymatic methods for the normalization of persistent organic pollutant levels in serum. Sci Total Environ 366, 361366.
25. Matthews, DR, Hosker, JP, Rudenski, AS, et al. (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412419.
26. Folch, J, Lees, M & Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497509.
27. Carlson, LA (1985) Extraction of lipids from human whole serum and lipoproteins and from rat liver tissue with methylene chloride-methanol: a comparison with extraction chloroform-methanol. Clin Chim Acta 149, 8993.
28. Raes, K, De Smet, SD & Demeyer, D (2001) Effect of double-muscling in Belgian Blue young bulls on the intramuscular fatty acid composition with emphasis on conjugated linoleic acid and polyunsaturated fatty acids. Anim Sci 73, 253260.
29. Alves, SP & Bessa, RJB (2009) Comparison of two gas–liquid chromatograph columns for the analysis of fatty acids in ruminant meat. J Chromatogr A 1216, 51305139.
30. Vandesompele, J, De Preter, K & Pattyn, F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, 7.
31. Andersen, CL, Jensen, JL & Orntoft, TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64, 52455250.
32. Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta C(T)) Method. Methods 25, 402408.
33. Fleige, S, Walf, V & Huch, S (2006) Comparison of relative mRNA quantification models and the impact of RNA integrity in quantitative real-time RT-PCR. Biotechnol Lett 28, 16011613.
34. SAS Institute Inc (2009) SAS/STAT 9.2 User’s Guide, 2nd ed. Cary, NC: SAS Institute Inc.
35. Milliken, GA & Johnson, DE (2002) Analysis of Messy Data, Volume III: Analysis of Covariance. London: Chapman and Hall/CRC.
36. Teye, GA, Sheard, PR, Whittington, FM, et al. (2006) Influence of dietary oils and protein level on pork quality. 1. Effects on muscle fatty acid composition, carcass, meat and eating quality. Meat Sci 73, 157165.
37. O’Connell, MK, Lynch, PB & O’Doherty, JV (2006) The effect of dietary lysine restriction during the grower phase and subsequent dietary lysine concentration during the realimentation phase on the performance, carcass characteristics and nitrogen balance of growing-finishing pigs. Livest Sci 101, 169179.
38. Madeira, MS, Costa, P, Alfaia, CM, et al. (2013) The increased intramuscular fat promoted by dietary lysine restriction in lean but not in fatty pig genotypes improves pork sensory attributes. J Anim Sci 91, 31773187.
39. O’Hea, EK & Leveille, GA (1969) Lipid biosynthesis and transport in the domestic chick (Gallus domesticus). Comp Biochem Physiol 30, 149159.
40. Jackson, PGG & Cockcroft, PD (2002) Laboratory reference values: biochemistry. In Clinical Examination of Farm Animals, Appendix 3, pp. 303305. Oxford: Blackwell Science.
41. Patterson, E, Wall, R, Fitzgerald, GF, et al. (2012) Health implications of high dietary omega-6 polyunsaturated fatty acids. J Nutr Metab 2012, 539426.
42. Atinmo, T, Baldijao, C, Pond, WG, et al. (1976) Maternal protein malnutrition during gestation alone and its effects on plasma insulin levels of the pregnant pigs, its foetuses and the developing offspring. J Nutr 106, 16471653.
43. Caperna, TJ, Steele, NC, Komarck, DR, et al. (1990) Influence of dietary protein and recombinant porcine somatotropin administration in young pigs: growth, body composition and hormone status. J Anim Sci 68, 4243.
44. Blat, S, Morise, A, Sauret, A, et al. (2012) The protein level of isoenergetic formulae does not modulate postprandial insulin secretion in piglets and has no consequences on later glucose tolerance. Br J Nutr 108, 102112.
45. Wilcox, G (2005) Insulin and insulin resistance. Clin Biochem Rev 26, 1939.
46. Savage, DB & O’Rahilly, S (2002) Leptin: a novel therapeutic role in lipodystrophy. J Clin Invest 109, 12851286.
47. Gan, L, Liu, Z, Cao, W, et al. (2015) FABP4 reversed the regulation of leptin on mitochondrial fatty acid oxidation in mice adipocytes. Sci Rep 5, 13588.
48. Herrero, MC, Remesar, X, Arola, L, et al. (1994) Splanchnic ammonia management in genetic and dietary obesity in the rat. Int J Obes Relat Metab Disord 18, 255261.
49. Matthews, JO, Southern, LL, Pontif, JE, et al. (1998) Interative effects of betaine, crude protein and net energy in finishing pigs. J Anim Sci 76, 24442455.
50. Gomez, RS, Lewis, AJ, Miller, PS, et al. (2002) Growth performance, diet apparent digestibility, and plasma metabolite concentrations of barrows fed corn-soybean meal diets or low-protein, amino acid-supplemented diets at different feeding level. J Anim Sci 80, 644653.
51. Ntawubizi, M, Raes, K, Buys, N, et al. (2009) Effect of sire and sex on the intramuscular fatty acid profile and indices for enzyme activities in pigs. Livest Sci 122, 264270.
52. Kersten, S, Seydoux, J, Peters, JM, et al. (1999) Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest 103, 14891498.
53. Mcneel, RL, Ding, ST, Smith, EO, et al. (2000) Effect of feed restriction on adipose tissue transcript concentrations in genetically lean and obese pigs. J Anim Sci 78, 934942.
54. Cheng, PT & Mukherjee, R (2005) PPARs as targets for metabolic and cardiovascular diseases. Mini Rev Med Chem 5, 741753.
55. Lim, S, Oh, TJ & Koh, KK (2015) Mechanisms link between nonalcoholic fatty liver disease and cardiometabolic disorders. Int J Cardiol 201, 408414.
56. Kirpich, IA, Marsano, LS & McClain, CJ (2015) Gut-liver axis, nutrition, and non-alcoholic fatty liver disease. Clin Biochem 48, 923930.
57. Ntambi, JM (1999) Regulation of stearoyl-CoA desaturase by polyunsaturated fatty acids and cholesterol. J Lipid Res 40, 15491558.
58. Dannenberger, D, Nuernberg, K & Nuernberg, G (2014) Impact of dietary protein level and source of polyunsaturated fatty acids on lipid metabolism-related protein expression and fatty acid concentrations in porcine tissues. J Agric Food Chem 62, 1245312461.
59. Guillon, H, Martin, PGP & Pineau, T (2008) Transcriptional regulation of hepatic fatty acid metabolism. In Lipids in Health and Disease, Chapter 1, pp. 3–47 [PJ Quinn and X Wang, editors]. London: Springer Science+Business Media B.V.
60. Osborne, TF (2000) Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J Biol Chem 275, 3237932382.
61. Wang, X, Sato, R, Brown, MS, et al. (1994) SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 77, 5362.
62. Flowers, MT & Ntambi, JM (2008) Role of stearoyl-coenzyme A desaturase in regulating lipid metabolism. Curr Opin Lipidol 9, 248256.


Related content

Powered by UNSILO

Restriction of dietary protein does not promote hepatic lipogenesis in lean or fatty pigs

  • Marta S. Madeira (a1), Virgínia M. R. Pires (a1), Cristina M. Alfaia (a1), Paula A. Lopes (a1), Susana V. Martins (a1), Rui M. A. Pinto (a2) and José A. M. Prates (a1)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.