Transcript profile of skeletal muscle lipid metabolism genes affected by diet in a piglet model of low birth weight


Autoři: Quentin L. Sciascia aff001;  Gürbüz Daş aff001;  Steffen Maak aff002;  Claudia Kalbe aff002;  Barbara U. Metzler-Zebeli aff003;  Cornelia C. Metges aff001
Působiště autorů: Institute of Nutritional Physiology, Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee, Dummerstorf, Germany aff001;  Institute of Muscle Biology and Growth, Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee, Dummerstorf, Germany aff002;  Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Austria aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224484

Souhrn

Dysregulated skeletal muscle metabolism (DSMM) is associated with increased inter- and intramuscular fat deposition in low birth weight (L) individuals. The mechanisms behind DSMM in L individuals are not completely understood but decreased muscle mass and shifts in lipid and carbohydrate utilisation may contribute. Previously, we observed lower fat oxidation in a porcine model of low birth weight. To elucidate the biological activities underpinning this difference microfluidic arrays were used to assess mRNA associated with lipid metabolism in longissimus dorsi (LD) and semitendinosus (ST) skeletal muscle samples from thirty-six female L and normal birth weight (N) pigs. Plasma samples were collected from a sub-population to measure metabolite concentrations. Following overnight fasting, skeletal muscle and plasma samples were collected and the association with birth weight, diet and age was assessed. Reduced dietary fat was associated with decreased LD intermuscular fat deposition and beta-oxidation associated mRNA, in both birth weight groups. Lipid uptake and intramuscular fat deposition associated mRNA was reduced in only L pigs. Abundance of ST mRNA associated with lipolysis, lipid synthesis and transport increased in both birth weight groups. Lipid uptake associated mRNA reduced in only L pigs. These changes were associated with decreased plasma L glucose and N triacylglycerol. Post-dietary fat reduction, LD mRNA associated with lipid synthesis and inter- and intramuscular fat deposition increased in L, whilst beta-oxidation associated mRNA remains elevated for longer in N. In the ST, mRNA associated with lipolysis and intramuscular fat deposition increased in both birth weight groups, however this increase was more significant in L pigs and associated with reduced beta-oxidation. Analysis of muscle lipid metabolism associated mRNA revealed that profile shifts are a consequence of birth weight. Whilst, many of the adaptions to diet and age appear to be similar in birth weight groups, the magnitude of response and individual changes underpin the previously observed lower fat oxidation in L pigs.

Klíčová slova:

Birth weight – Diet – Fats – Lipid metabolism – Lipids – Skeletal muscles – Swine – Lipolysis


Zdroje

1. Kelley DE. Skeletal muscle fat oxidation: timing and flexibility are everything. J Clin Invest. 2005;115(7):1699–702. Epub 2005/07/12. doi: 10.1172/JCI25758 16007246; PubMed Central PMCID: PMC1159159.

2. Xiao X, Zhang ZX, Li WH, Feng K, Sun Q, Cohen HJ, et al. Low birth weight is associated with components of the metabolic syndrome. Metabolism. 2010;59(9):1282–6. Epub 2010/01/05. doi: 10.1016/j.metabol.2009.12.001 20045533; PubMed Central PMCID: PMC2895955.

3. Williams PJ, Marten N, Wilson V, Litten-Brown JC, Corson AM, Clarke L, et al. Influence of birth weight on gene regulators of lipid metabolism and utilization in subcutaneous adipose tissue and skeletal muscle of neonatal pigs. Reproduction. 2009;138(3):609–17. Epub 2009/06/09. doi: 10.1530/REP-08-0445 19502453.

4. Rehfeldt C, Tuchscherer A, Hartung M, Kuhn G. A second look at the influence of birth weight on carcass and meat quality in pigs. Meat Sci. 2008;78(3):170–5. Epub 2008/03/01. doi: 10.1016/j.meatsci.2007.05.029 22062267.

5. Hausman GJ, Basu U, Du M, Fernyhough-Culver M, Dodson MV. Intermuscular and intramuscular adipose tissues: Bad vs. good adipose tissues. Adipocyte. 2014;3(4):242–55. Epub 2015/09/01. doi: 10.4161/adip.28546 26317048; PubMed Central PMCID: PMC4550684.

6. Wigmore PM, Stickland NC. Muscle development in large and small pig fetuses. J Anat. 1983;137 (Pt 2):235–45. Epub 1983/09/01. 6630038; PubMed Central PMCID: PMC1171817.

7. Gondret F, Lefaucheur L, Juin H, Louveau I, Lebret B. Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. J Anim Sci. 2006;84(1):93–103. Epub 2005/12/20. doi: 10.2527/2006.84193x 16361495.

8. Rehfeldt C. Prenatal events that determine the number of muscle fibres are important for lean growth and meat quality in pigs. Arch Anim Breed. 2005;48(Sp.Iss.):11–22.

9. Befroy DE, Petersen KF, Dufour S, Mason GF, de Graaf RA, Rothman DL, et al. Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes. 2007;56(5):1376–81. Epub 2007/02/09. doi: 10.2337/db06-0783 17287462; PubMed Central PMCID: PMC2995532.

10. Hu L, Han F, Chen L, Peng X, Chen D, Wu, et al. High nutrient intake during the early postnatal period accelerates skeletal muscle fiber growth and maturity in intrauterine growth-restricted pigs. Genes Nutr. 2018;13:23. Epub 2018/08/02. doi: 10.1186/s12263-018-0612-8 30065792; PubMed Central PMCID: PMC6062929.

11. Zhao X, Mo D, Li A, Gong W, Xiao S, Zhang Y, et al. Comparative analyses by sequencing of transcriptomes during skeletal muscle development between pig breeds differing in muscle growth rate and fatness. PLoS One. 2011;6(5):e19774. Epub 2011/06/04. doi: 10.1371/journal.pone.0019774 21637832; PubMed Central PMCID: PMC3102668.

12. Krueger R, Derno M, Goers S, Metzler-Zebeli BU, Nuernberg G, Martens K, et al. Higher body fatness in intrauterine growth retarded juvenile pigs is associated with lower fat and higher carbohydrate oxidation during ad libitum and restricted feeding. Eur J Nutr. 2014;53(2):583–97. Epub 2013/08/03. doi: 10.1007/s00394-013-0567-x 23907209; PubMed Central PMCID: PMC3925302.

13. Metges CC, Gors S, Martens K, Krueger R, Metzler-Zebeli BU, Nebendahl C, et al. Body composition and plasma lipid and stress hormone levels during 3 weeks of feed restriction and refeeding in low birth weight female pigs. J Anim Sci. 2015;93(3):999–1014. Epub 2015/05/29. doi: 10.2527/jas.2014-8616 26020878.

14. Chen FF, Wang YQ, Tang GR, Liu SG, Cai R, Gao Y, et al. Differences between porcine longissimus thoracis and semitendinosus intramuscular fat content and the regulation of their preadipocytes during adipogenic differentiation. Meat Sci. 2019;147:116–26. Epub 2018/09/17. doi: 10.1016/j.meatsci.2018.09.002 30219363.

15. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007;8(2):R19. Epub 2007/02/13. doi: 10.1186/gb-2007-8-2-r19 17291332; PubMed Central PMCID: PMC1852402.

16. Bustin SA. Why the need for qPCR publication guidelines?—The case for MIQE. Methods. 2010;50(4):217–26. Epub 2009/12/23. doi: 10.1016/j.ymeth.2009.12.006 20025972.

17. Beauchamp B, Ghosh S, Dysart MW, Kanaan GN, Chu A, Blais A, et al. Low birth weight is associated with adiposity, impaired skeletal muscle energetics and weight loss resistance in mice. Int J Obes (Lond). 2015;39(4):702–11. Epub 2014/08/06. doi: 10.1038/ijo.2014.120 25091727; PubMed Central PMCID: PMC4326251.

18. Kelstrup L, Hjort L, Houshmand-Oeregaard A, Clausen TD, Hansen NS, Broholm C, et al. Gene Expression and DNA Methylation of PPARGC1A in Muscle and Adipose Tissue From Adult Offspring of Women With Diabetes in Pregnancy. Diabetes. 2016;65(10):2900–10. Epub 2016/07/09. doi: 10.2337/db16-0227 27388218.

19. Brown LD, Hay WW Jr. Impact of placental insufficiency on fetal skeletal muscle growth. Mol Cell Endocrinol. 2016;435:69–77. Epub 2016/03/21. doi: 10.1016/j.mce.2016.03.017 26994511; PubMed Central PMCID: PMC5014698.

20. Hansen NS, Hjort L, Broholm C, Gillberg L, Schrolkamp M, Schultz HS, et al. Metabolic and Transcriptional Changes in Cultured Muscle Stem Cells from Low Birth Weight Subjects. J Clin Endocrinol Metab. 2016;101(5):2254–64. Epub 2016/03/24. doi: 10.1210/jc.2015-4214 27003303.

21. Weinstock PH, Levak-Frank S, Hudgins LC, Radner H, Friedman JM, Zechner R, et al. Lipoprotein lipase controls fatty acid entry into adipose tissue, but fat mass is preserved by endogenous synthesis in mice deficient in adipose tissue lipoprotein lipase. Proc Natl Acad Sci U S A. 1997;94(19):10261–6. Epub 1997/09/18. doi: 10.1073/pnas.94.19.10261 9294198; PubMed Central PMCID: PMC23350.

22. Walton RG, Zhu B, Unal R, Spencer M, Sunkara M, Morris AJ, et al. Increasing adipocyte lipoprotein lipase improves glucose metabolism in high fat diet-induced obesity. J Biol Chem. 2015;290(18):11547–56. Epub 2015/03/19. doi: 10.1074/jbc.M114.628487 25784555; PubMed Central PMCID: PMC4416858.

23. Wang H, Eckel RH. Lipoprotein lipase: from gene to obesity. Am J Physiol Endocrinol Metab. 2009;297(2):E271–88. Epub 2009/03/26. doi: 10.1152/ajpendo.90920.2008 19318514.

24. Itabe H, Yamaguchi T, Nimura S, Sasabe N. Perilipins: a diversity of intracellular lipid droplet proteins. Lipids Health Dis. 2017;16(1):83. Epub 2017/04/30. doi: 10.1186/s12944-017-0473-y 28454542; PubMed Central PMCID: PMC5410086.

25. Morales PE, Bucarey JL, Espinosa A. Muscle Lipid Metabolism: Role of Lipid Droplets and Perilipins. J Diabetes Res. 2017;2017:1789395. Epub 2017/07/06. doi: 10.1155/2017/1789395 28676863; PubMed Central PMCID: PMC5476901.

26. Li B, Weng Q, Dong C, Zhang Z, Li R, Liu J, et al. A Key Gene, PLIN1, Can Affect Porcine Intramuscular Fat Content Based on Transcriptome Analysis. Genes (Basel). 2018;9(4). Epub 2018/04/05. doi: 10.3390/genes9040194 29617344; PubMed Central PMCID: PMC5924536.

27. Gandolfi G, Mazzoni M, Zambonelli P, Lalatta-Costerbosa G, Tronca A, Russo V, et al. Perilipin 1 and perilipin 2 protein localization and gene expression study in skeletal muscles of European cross-breed pigs with different intramuscular fat contents. Meat Sci. 2011;88(4):631–7. Epub 2011/03/23. doi: 10.1016/j.meatsci.2011.02.020 21420243.

28. Miyazaki M, Ntambi JM. Role of stearoyl-coenzyme A desaturase in lipid metabolism. Prostaglandins Leukot Essent Fatty Acids. 2003;68(2):113–21. Epub 2003/01/23. doi: 10.1016/s0952-3278(02)00261-2 12538075.

29. Yu K, Shu G, Yuan F, Zhu X, Gao P, Wang S, et al. Fatty acid and transcriptome profiling of longissimus dorsi muscles between pig breeds differing in meat quality. Int J Biol Sci. 2013;9(1):108–18. Epub 2013/01/29. doi: 10.7150/ijbs.5306 23355796; PubMed Central PMCID: PMC3555150.

30. Matsui H, Yokoyama T, Sekiguchi K, Iijima D, Sunaga H, Maniwa M, et al. Stearoyl-CoA desaturase-1 (SCD1) augments saturated fatty acid-induced lipid accumulation and inhibits apoptosis in cardiac myocytes. PLoS One. 2012;7(3):e33283. Epub 2012/03/14. doi: 10.1371/journal.pone.0033283 22413010; PubMed Central PMCID: PMC3297642.

31. Hulver MW, Berggren JR, Carper MJ, Miyazaki M, Ntambi JM, Hoffman EP, et al. Elevated stearoyl-CoA desaturase-1 expression in skeletal muscle contributes to abnormal fatty acid partitioning in obese humans. Cell Metab. 2005;2(4):251–61. Epub 2005/10/11. doi: 10.1016/j.cmet.2005.09.002 16213227; PubMed Central PMCID: PMC4285571.

32. Kraemer FB, Shen WJ. Hormone-sensitive lipase: control of intracellular tri-(di-)acylglycerol and cholesteryl ester hydrolysis. J Lipid Res. 2002;43(10):1585–94. Epub 2002/10/05. doi: 10.1194/jlr.r200009-jlr200 12364542.

33. Pawlak M, Lefebvre P, Staels B. Molecular mechanism of PPARalpha action and its impact on lipid metabolism, inflammation and fibrosis in non-alcoholic fatty liver disease. J Hepatol. 2015;62(3):720–33. Epub 2014/12/03. doi: 10.1016/j.jhep.2014.10.039 25450203.

34. Goldberg IJ, Eckel RH, Abumrad NA. Regulation of fatty acid uptake into tissues: lipoprotein lipase- and CD36-mediated pathways. J Lipid Res. 2009;50 Suppl:S86-90. Epub 2008/11/27. doi: 10.1194/jlr.R800085-JLR200 19033209; PubMed Central PMCID: PMC2674753.

35. Paton CM, Ntambi JM. Biochemical and physiological function of stearoyl-CoA desaturase. Am J Physiol Endocrinol Metab. 2009;297(1):E28–37. Epub 2008/12/11. doi: 10.1152/ajpendo.90897.2008 19066317; PubMed Central PMCID: PMC2711665.

36. Fischer H, Gustafsson T, Sundberg CJ, Norrbom J, Ekman M, Johansson O, et al. Fatty acid binding protein 4 in human skeletal muscle. Biochem Biophys Res Commun. 2006;346(1):125–30. Epub 2006/06/06. doi: 10.1016/j.bbrc.2006.05.083 16750515.

37. Furuhashi M, Hotamisligil GS. Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov. 2008;7(6):489–503. Epub 2008/05/31. doi: 10.1038/nrd2589 18511927; PubMed Central PMCID: PMC2821027.

38. Kusudo T, Kontani Y, Kataoka N, Ando F, Shimokata H, Yamashita H. Fatty acid-binding protein 3 stimulates glucose uptake by facilitating AS160 phosphorylation in mouse muscle cells. Genes Cells. 2011;16(6):681–91. Epub 2011/04/20. doi: 10.1111/j.1365-2443.2011.01517.x 21501347.

39. Modica S, Straub LG, Balaz M, Sun W, Varga L, Stefanicka P, et al. Bmp4 Promotes a Brown to White-like Adipocyte Shift. Cell Rep. 2016;16(8):2243–58. Epub 2016/08/16. doi: 10.1016/j.celrep.2016.07.048 27524617.

40. Mello T, Materozzi M, Galli A. PPARs and Mitochondrial Metabolism: From NAFLD to HCC. PPAR Res. 2016;2016:7403230. Epub 2017/01/25. doi: 10.1155/2016/7403230 PubMed Central PMCID: PMC5223052. 28115925

41. Henique C, Mansouri A, Fumey G, Lenoir V, Girard J, Bouillaud F, et al. Increased mitochondrial fatty acid oxidation is sufficient to protect skeletal muscle cells from palmitate-induced apoptosis. J Biol Chem. 2010;285(47):36818–27. Epub 2010/09/15. doi: 10.1074/jbc.M110.170431 PubMed Central PMCID: PMC2978610. 20837491

42. Timmers S, Nabben M, Bosma M, van Bree B, Lenaers E, van Beurden D, et al. Augmenting muscle diacylglycerol and triacylglycerol content by blocking fatty acid oxidation does not impede insulin sensitivity. Proc Natl Acad Sci U S A. 2012;109(29):11711–6. Epub 2012/07/04. doi: 10.1073/pnas.1206868109 PubMed Central PMCID: PMC3406830. 22753483

43. Wicks SE, Vandanmagsar B, Haynie KR, Fuller SE, Warfel JD, Stephens JM, et al. Impaired mitochondrial fat oxidation induces adaptive remodeling of muscle metabolism. Proc Natl Acad Sci U S A. 2015;112(25):E3300–9. Epub 2015/06/10. doi: 10.1073/pnas.1418560112 PubMed Central PMCID: PMC4485116. 26056297

44. Perreault L, Newsom SA, Strauss A, Kerege A, Kahn DE, Harrison KA, et al. Intracellular localization of diacylglycerols and sphingolipids influences insulin sensitivity and mitochondrial function in human skeletal muscle. JCI Insight. 2018;3(3). Epub 2018/02/09. doi: 10.1172/jci.insight.96805 29415895; PubMed Central PMCID: PMC5821197.

45. McGarry JD, Woeltje KF, Kuwajima M, Foster DW. Regulation of ketogenesis and the renaissance of carnitine palmitoyltransferase. Diabetes Metab Rev. 1989;5(3):271–84. Epub 1989/05/01. 2656156.

46. Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A. Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J Lipid Res. 2009;50(1):3–21. Epub 2008/10/28. doi: 10.1194/jlr.R800031-JLR200 18952573.

47. Ishizawa M, Kagechika H, Makishima M. NR4A nuclear receptors mediate carnitine palmitoyltransferase 1A gene expression by the rexinoid HX600. Biochem Biophys Res Commun. 2012;418(4):780–5. Epub 2012/02/09. doi: 10.1016/j.bbrc.2012.01.102 22310716.

48. Hall AM, Soufi N, Chambers KT, Chen Z, Schweitzer GG, McCommis KS, et al. Abrogating monoacylglycerol acyltransferase activity in liver improves glucose tolerance and hepatic insulin signaling in obese mice. Diabetes. 2014;63(7):2284–96. Epub 2014/03/07. doi: 10.2337/db13-1502 24595352; PubMed Central PMCID: PMC4066334.

49. Abel ED. Free fatty acid oxidation in insulin resistance and obesity. Heart Metab. 2010;48:5–10. Epub 2010/09/01. 23646039; PubMed Central PMCID: PMC3643515.

50. Sugden MC, Bulmer K, Gibbons GF, Knight BL, Holness MJ. Peroxisome-proliferator-activated receptor-alpha (PPARalpha) deficiency leads to dysregulation of hepatic lipid and carbohydrate metabolism by fatty acids and insulin. Biochem J. 2002;364(Pt 2):361–8. Epub 2002/05/25. doi: 10.1042/BJ20011699 12023878; PubMed Central PMCID: PMC1222580.

51. Sankella S, Garg A, Agarwal AK. Characterization of the Mouse and Human Monoacylglycerol O-Acyltransferase 1 (Mogat1) Promoter in Human Kidney Proximal Tubule and Rat Liver Cells. PLoS One. 2016;11(9):e0162504. Epub 2016/09/10. doi: 10.1371/journal.pone.0162504 27611931; PubMed Central PMCID: PMC5017789 report.

52. Muoio DM, Way JM, Tanner CJ, Winegar DA, Kliewer SA, Houmard JA, et al. Peroxisome proliferator-activated receptor-alpha regulates fatty acid utilization in primary human skeletal muscle cells. Diabetes. 2002;51(4):901–9. Epub 2002/03/28. doi: 10.2337/diabetes.51.4.901 11916905.

53. Jensen CB, Storgaard H, Madsbad S, Richter EA, Vaag AA. Altered skeletal muscle fiber composition and size precede whole-body insulin resistance in young men with low birth weight. J Clin Endocrinol Metab. 2007;92(4):1530–4. Epub 2007/02/08. doi: 10.1210/jc.2006-2360 17284623.

54. Handel SE, Stickland NC. The growth and differentiation of porcine skeletal muscle fibre types and the influence of birthweight. J Anat. 1987;152:107–19. Epub 1987/06/01. 2958439; PubMed Central PMCID: PMC1261750.

55. Reichmann H, De Vivo DC. Coordinate enzymatic activity of beta-oxidation and purine nucleotide cycle in a diversity of muscle and other organs of rat. Comp Biochem Physiol B. 1991;98(2–3):327–31. Epub 1991/01/01. doi: 10.1016/0305-0491(91)90186-h 1678689.

56. Bauer R, Gedrange T, Bauer K, Walter B. Intrauterine growth restriction induces increased capillary density and accelerated type I fiber maturation in newborn pig skeletal muscles. J Perinat Med. 2006;34(3):235–42. Epub 2006/04/11. doi: 10.1515/JPM.2006.042 16602845.


Článek vyšel v časopise

PLOS One


2019 Číslo 10