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Maternal Plane of Nutrition During Late-Gestation and Weaning Age Alter Steer Calf Longissimus Muscle Adipogenic MicroRNA and Target Gene Expression

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Lipids

Abstract

The main objective was to evaluate if different planes of maternal nutrition during late gestation and weaning age alter microRNA (miRNA) and target gene expression in offspring longissimus muscle (LM). Early (EW) and normal weaned (NW) Angus × Simmental calves (n = 30) born to cows that were grazing endophyte-infected tall fescue and red clover pastures with no supplement [low plane of nutrition (LPN)], or supplemented with 2.3 and 9.1 kg of dried distiller’s grains with solubles and soy hulls [medium and high plane of nutrition (MPN, HPN), respectively] during the last 105 ± 11 days of gestation were used. Biopsies of LM were harvested at 78 (early weaning), 187 (normal weaning) and 354 days of age. Results indicate a role of pro-adipogenic miRNA in the control of adipogenesis in LM of NW-MPN steers between 78 and 187 days of age through upregulation of (1) miR-103 which inhibits CAV1, a protein that destabilizes INSR and leads to insulin resistance; (2) miR-143 which inhibits DLK1, a protein that inhibits adipocyte differentiation; and (3) miR-21 which impairs TGFBR2-induced inhibition of adipocyte differentiation. Among the studied anti-adipogenic miRNA, cow plane of nutrition resulted in downregulation of miR-34a expression in MPN steers compared with HPN and LPN at 78 days of age. Data for miR-34a provided a potential sign of epigenetic regulation of LM in beef offspring due to the cow plane of nutrition during late gestation.

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Abbreviations

ADIPOQ:

Adiponectin

ADG:

Average daily gain

CAV1:

Caveolin 1

C/EBPA:

CCAAT/enhancer binding protein (C/EBP), alpha

C/EBPB:

CCAAT/enhancer binding protein (C/EBP), beta

C/EBPD:

CCAAT/enhancer binding protein (C/EBP), delta

CREB:

cAMP response element binding protein

DLK1:

Delta-like 1 homolog

DM:

Dry matter

DMI:

Dry matter intake

ERK1/2:

Mitogen-activated protein kinase 3

EW:

Early wean(ed)

FABP4:

Fatty acid binding protein 4

G0S2:

G0/G1 switch 2

hASC:

Human adipose tissue-derived mesenchymal stem cells

HPN:

High plane of nutrition

IL-6:

Interleukin 6

INSR:

Insulin receptor

KLF5:

Kruppel-like factor 5

LM:

Longissimus muscle

LPN:

Low plane of nutrition

MAPK1:

Mitogen-activated protein kinase 1

miRNA:

MicroRNA

miR-16b:

MicroRNA 16a

miR-let-7a:

MicroRNA let7a

miR-181a:

MicroRNA 181a

miR-103:

MicroRNA 103

miR-143:

MicroRNA 143

miR-21-5p:

MicroRNA 21-5p

miR-378:

MicroRNA 378

miR-27a/b:

MicroRNA 27a/b

miR-130a:

MicroRNA 130a

miR-34a:

MicroRNA 34a

miR-369-5p:

MicroRNA 369-5p

miR-448:

MicroRNA 448

MPN:

Medium plane of nutrition

MSTN:

Myostatin

MTG1:

Mitochondrial ribosome-associated GTPase 1

NF-κB:

Nuclear factor of kappa light polypeptide gene enhancer in B-cells

NW:

Normal wean(ed)

PANK:

Pantothenate kinase

PDCD4:

Programmed cell death 4

PGC-1β:

Peroxisome proliferator-activated receptor gamma coactivator 1 beta

PPARG:

Peroxisome proliferator-activated receptor gamma

PTEN:

Phosphatase and tensin homolog

qPCR:

Quantitative RT-PCR

RPS15A:

Ribosomal protein S15a

SIRT1:

Sirtuin 1

SLC2A4:

Solute carrier family 2 (facilitated glucose transporter), member 4

SREBP:

Sterol responsive element binding protein

STAT3:

Signal transducer and activator of transcription 3

TGFBR2:

Transforming growth factor, beta receptor II

TNF:

Tumor necrosis alpha

TNF-α:

Tumor necrosis alpha

TP53:

Tumor protein p53

UTR:

Untranslated region

UXT:

Ubiquitously-expressed

References

  1. Wilkins JF (2005) Genomic imprinting and methylation: epigenetic canalization and conflict. Trends Genet 21:356–365

    Article  PubMed  CAS  Google Scholar 

  2. Munshi A, Shafi G, Aliya N, Jyothy A (2009) Histone modifications dictate specific biological readouts. J Genet Genom 36:75–88

    Article  CAS  Google Scholar 

  3. McKay JA, Mathers JC (2011) Diet induced epigenetic changes and their implications for health. Acta Physiol (Oxf) 202:103–118

    Article  CAS  Google Scholar 

  4. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Jin W, Grant JR, Stothard P, Moore SS, Guan LL (2009) Characterization of bovine miRNAs by sequencing and bioinformatics analysis. BMC Mol Biol 10:90

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Basu U, Romao JM, Guan LL (2012) Adipogenic transcriptome profiling using high throughput technologies. J Genom 1:22–28

    Article  Google Scholar 

  7. Erhuma A, Salter AM, Sculley DV, Langley-Evans SC, Bennett AJ (2007) Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol Endocrinol Metab 292:E1702–E1714

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Moisa SJ, Shike DW, Shoup L, Rodriguez-Zas SL, Loor JJ (2015) Maternal plane of nutrition during late gestation and weaning age alter Angus × Simmental offspring longissimus muscle transcriptome and intramuscular fat. PLoS One 10:e0131478

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Shoup LM, Wilson TB, González-Peña D, Ireland FA, Rodriguez-Zas S, Felix TL, Shike DW (2015) Beef cow prepartum supplement level and age at weaning: II. Effects of developmental programming on performance and carcass composition of steer progeny. J Anim Sci 93(10):4936–4947. doi:10.2527/jas2014-8565

    Article  PubMed  CAS  Google Scholar 

  10. Shoup LM, Kloth AC, Wilson TB, González-Peña D, Ireland FA, Rodriguez-Zas S, Felix TL, Shike DW (2015) Prepartum supplement level and age at weaning: I. Effects on pre- and postpartum beef cow performance and calf performance through weaning. J Anim Sci 93(10):4926-35. doi: 10.2527/jas2014-8564

  11. Raddatz J (2008) Measurement of adiponectin and insulin in lactating and non-lactating Holstein cows in Animal Sciences. North Carolina State University, Raleigh, p 79. http://repository.lib.ncsu.edu/ir/handle/1840.1816/1845

  12. Funston RN, Larson DM, Vonnahme KA (2010) Effects of maternal nutrition on conceptus growth and offspring performance: implications for beef cattle production. J Anim Sci 88:E205–E215

    Article  PubMed  CAS  Google Scholar 

  13. Bohnert DW, Stalker LA, Mills RR, Nyman A, Falck SJ, Cooke RF (2013) Late gestation supplementation of beef cows differing in body condition score: effects on cow and calf performance. J Anim Sci 91:5485–5491

    Article  PubMed  CAS  Google Scholar 

  14. Moisa SJ, Shike DW, Faulkner DB, Meteer WT, Keisler D, Loor JJ (2014) Central role of the PPARgamma gene network in coordinating beef cattle intramuscular adipogenesis in response to weaning age and nutrition. Gene Regul Syst Bio 8:17–32

    PubMed  PubMed Central  Google Scholar 

  15. Hoffstedt J, Arvidsson E, Sjolin E, Wahlen K, Arner P (2004) Adipose tissue adiponectin production and adiponectin serum concentration in human obesity and insulin resistance. J Clin Endocrinol Metab 89:1391–1396

    Article  PubMed  CAS  Google Scholar 

  16. Smith J, Al-Amri M, Sniderman A, Cianflone K (2006) Leptin and adiponectin in relation to body fat percentage, waist to hip ratio and the apoB/apoA1 ratio in Asian Indian and Caucasian men and women. Nutr Metab (Lond) 3:18

    Article  CAS  Google Scholar 

  17. Kabara E, Sordillo LM, Holcombe S, Contreras GA (2014) Adiponectin links adipose tissue function and monocyte inflammatory responses during bovine metabolic stress. Comp Immunol Microbiol Infect Dis 37:49–58

    Article  PubMed  Google Scholar 

  18. Ji P, Drackley JK, Khan MJ, Loor JJ (2014) Overfeeding energy upregulates peroxisome proliferator-activated receptor (PPAR)gamma-controlled adipogenic and lipolytic gene networks but does not affect proinflammatory markers in visceral and subcutaneous adipose depots of Holstein cows. J Dairy Sci 97:3431–3440

    Article  PubMed  CAS  Google Scholar 

  19. Ji P, Drackley JK, Khan MJ, Loor JJ (2014) Inflammation- and lipid metabolism-related gene network expression in visceral and subcutaneous adipose depots of Holstein cows. J Dairy Sci 97:3441–3448

    Article  PubMed  CAS  Google Scholar 

  20. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y (2012) Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. 1999. Biochem Biophys Res Commun 425:560–564

    Article  PubMed  CAS  Google Scholar 

  21. Ohtani Y, Takahashi T, Sato K, Ardiyanti A, Song SH, Sato R, Onda K, Wada Y, Obara Y, Suzuki K, Hagino A, Roh SG, Katoh K (2012) Changes in circulating adiponectin and metabolic hormone concentrations during periparturient and lactation periods in Holstein dairy cows. Anim Sci J 83:788–795

    Article  PubMed  CAS  Google Scholar 

  22. Xie H, Lim B, Lodish HF (2009) MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes 58:1050–1057

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Sarr O, Thompson JA, Zhao L, Lee TY, Regnault TR (2014) Low birth weight male guinea pig offspring display increased visceral adiposity in early adulthood. PLoS One 9:e98433

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Polster BJ, Westaway SK, Nguyen TM, Yoon MY, Hayflick SJ (2010) Discordant expression of miR-103/7 and pantothenate kinase host genes in mouse. Mol Genet Metab 101:292–295

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Wilfred BR, Wang WX, Nelson PT (2007) Energizing miRNA research: a review of the role of miRNAs in lipid metabolism, with a prediction that miR-103/107 regulates human metabolic pathways. Mol Genet Metab 91:209–217

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Ragaller V, Lebzien P, Sudekum KH, Huther L, Flachowsky G (2011) Pantothenic acid in ruminant nutrition: a review. J Anim Physiol Anim Nutr (Berl) 95:6–16

    Article  CAS  Google Scholar 

  27. Rottiers V, Naar AM (2012) MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 13:239–250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Trajkovski M, Hausser J, Soutschek J, Bhat B, Akin A, Zavolan M, Heim MH, Stoffel M (2011) MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 474:649–653

    Article  PubMed  CAS  Google Scholar 

  29. Wang H, Xiao S, Wang M, Kim NH, Li H, Wang G (2015) In silico identification of conserved microRNAs and their targets in bovine fat tissue. Gene 559(2):119–128

    Article  PubMed  CAS  Google Scholar 

  30. Li H, Zhang Z, Zhou X, Wang Z, Wang G, Han Z (2011) Effects of microRNA-143 in the differentiation and proliferation of bovine intramuscular preadipocytes. Mol Biol Rep 38:4273–4280

    Article  PubMed  CAS  Google Scholar 

  31. Zhu L, Shi C, Ji C, Xu G, Chen L, Yang L, Fu Z, Cui X, Lu Y, Guo X (2013) FFAs and adipokine-mediated regulation of hsa-miR-143 expression in human adipocytes. Mol Biol Rep 40:5669–5675

    Article  PubMed  CAS  Google Scholar 

  32. Kim YJ, Min TS, Seo KS, Kim SH (2015) Expression of pref-1/dlk-1 is regulated by microRNA-143 in 3T3-L1 cells. Mol Biol Rep 42:617–624

    Article  PubMed  CAS  Google Scholar 

  33. Kavalkova P, Touskova V, Roubicek T, Trachta P, Urbanova M, Drapalova J, Haluzikova D, Mraz M, Novak D, Matoulek M, Lacinova Z, Haluzik M (2013) Serum preadipocyte factor-1 concentrations in females with obesity and type 2 diabetes mellitus: the influence of very low calorie diet, acute hyperinsulinemia, and fenofibrate treatment. Horm Metab Res 45:820–826

    Article  PubMed  CAS  Google Scholar 

  34. Keller P, Gburcik V, Petrovic N, Gallagher IJ, Nedergaard J, Cannon B, Timmons JA (2011) Gene-chip studies of adipogenesis-regulated microRNAs in mouse primary adipocytes and human obesity. BMC Endocr Disord 11:7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Kim YJ, Hwang SJ, Bae YC, Jung JS (2009) MiR-21 regulates adipogenic differentiation through the modulation of TGF-beta signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells 27:3093–3102

    PubMed  CAS  Google Scholar 

  36. Kim YJ, Hwang SH, Cho HH, Shin KK, Bae YC, Jung JS (2012) MicroRNA 21 regulates the proliferation of human adipose tissue-derived mesenchymal stem cells and high-fat diet-induced obesity alters microRNA 21 expression in white adipose tissues. J Cell Physiol 227:183–193

    Article  PubMed  CAS  Google Scholar 

  37. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH (2008) Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 283:1026–1033

    Article  PubMed  CAS  Google Scholar 

  38. Subedi A, Kim MJ, Nepal S, Lee ES, Kim JA, Sohn DH, Song K, Lee SH, Park WS, Jeong BS, Park PH (2013) Globular adiponectin modulates expression of programmed cell death 4 and miR-21 in RAW 264.7 macrophages through the MAPK/NF-kappaB pathway. FEBS Lett 587:1556–1561

    Article  PubMed  CAS  Google Scholar 

  39. Kang M, Yan LM, Zhang WY, Li YM, Tang AZ, Ou HS (2013) Role of microRNA-21 in regulating 3T3-L1 adipocyte differentiation and adiponectin expression. Mol Biol Rep 40:5027–5034

    Article  PubMed  CAS  Google Scholar 

  40. Eichner LJ, Perry MC, Dufour CR, Bertos N, Park M, St-Pierre J, Giguere V (2010) miR-378(*) mediates metabolic shift in breast cancer cells via the PGC-1beta/ERRgamma transcriptional pathway. Cell Metab 12:352–361

    Article  PubMed  CAS  Google Scholar 

  41. Romao JM, Jin W, He M, McAllister T, le Guan L (2014) MicroRNAs in bovine adipogenesis: genomic context, expression and function. BMC Genom 15:137

    Article  CAS  Google Scholar 

  42. Jin W, Dodson MV, Moore SS, Basarab JA, Guan LL (2010) Characterization of microRNA expression in bovine adipose tissues: a potential regulatory mechanism of subcutaneous adipose tissue development. BMC Mol Biol 11:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Ganesan J, Ramanujam D, Sassi Y, Ahles A, Jentzsch C, Werfel S, Leierseder S, Loyer X, Giacca M, Zentilin L, Thum T, Laggerbauer B, Engelhardt S (2013) MiR-378 controls cardiac hypertrophy by combined repression of mitogen-activated protein kinase pathway factors. Circulation 127:2097–2106

    Article  PubMed  CAS  Google Scholar 

  44. Liu SY, Zhang YY, Gao Y, Zhang LJ, Chen HY, Zhou Q, Chai ML, Li QY, Jiang H, Yuan B, Dai LS, Zhang JB (2015) MiR-378 Plays an Important Role in the Differentiation of Bovine Preadipocytes. Cell Physiol Biochem 36:1552–1562

    Article  PubMed  CAS  Google Scholar 

  45. Ishida M, Shimabukuro M, Yagi S, Nishimoto S, Kozuka C, Fukuda D, Soeki T, Masuzaki H, Tsutsui M, Sata M (2014) MicroRNA-378 regulates adiponectin expression in adipose tissue: a new plausible mechanism. PLoS One 9:e111537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Gerin I, Bommer GT, McCoin CS, Sousa KM, Krishnan V, MacDougald OA (2010) Roles for miRNA-378/378* in adipocyte gene expression and lipogenesis. Am J Physiol Endocrinol Metab 299:E198–E206

    PubMed  PubMed Central  CAS  Google Scholar 

  47. Jiang X, Xue M, Fu Z, Ji C, Guo X, Zhu L, Xu L, Pang L, Xu M, Qu H (2014) Insight into the effects of adipose tissue inflammation factors on miR-378 expression and the underlying mechanism. Cell Physiol Biochem 33:1778–1788

    Article  PubMed  CAS  Google Scholar 

  48. Zhu Y, Zhang X, Ding X, Wang H, Chen X, Zhao H, Jia Y, Liu S, Liu Y (2014) miR-27 inhibits adipocyte differentiation via suppressing CREB expression. Acta Biochim Biophys Sin (Shanghai) 46:590–596

    Article  CAS  Google Scholar 

  49. Qin L, Chen Y, Niu Y, Chen W, Wang Q, Xiao S, Li A, Xie Y, Li J, Zhao X, He Z, Mo D (2010) A deep investigation into the adipogenesis mechanism: profile of microRNAs regulating adipogenesis by modulating the canonical Wnt/beta-catenin signaling pathway. BMC Genom 11:320

    Article  CAS  Google Scholar 

  50. Zhao JX, Hu J, Zhu MJ, Du M (2011) Trenbolone enhances myogenic differentiation by enhancing beta-catenin signaling in muscle-derived stem cells of cattle. Domest Anim Endocrinol 40:222–229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Miretti S, Martignani E, Accornero P, Baratta M (2013) Functional effect of mir-27b on myostatin expression: a relationship in Piedmontese cattle with double-muscled phenotype. BMC Genom 14:194

    Article  CAS  Google Scholar 

  52. McFarlane C, Vajjala A, Arigela H, Lokireddy S, Ge X, Bonala S, Manickam R, Kambadur R, Sharma M (2014) Negative auto-regulation of myostatin expression is mediated by Smad3 and microRNA-27. PLoS One 9:e87687

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Guilherme A, Virbasius JV, Puri V, Czech MP (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 9:367–377

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Kim C, Lee H, Cho YM, Kwon OJ, Kim W, Lee EK (2013) TNFalpha-induced miR-130 resulted in adipocyte dysfunction during obesity-related inflammation. FEBS Lett 587:3853–3858

    Article  PubMed  CAS  Google Scholar 

  55. Ortega FJ, Moreno-Navarrete JM, Pardo G, Sabater M, Hummel M, Ferrer A, Rodriguez-Hermosa JI, Ruiz B, Ricart W, Peral B, Fernandez-Real JM (2010) MiRNA expression profile of human subcutaneous adipose and during adipocyte differentiation. PLoS One 5:e9022

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Chen F, Hu SJ (2012) Effect of microRNA-34a in cell cycle, differentiation, and apoptosis: a review. J Biochem Mol Toxicol 26:79–86

    Article  PubMed  CAS  Google Scholar 

  57. Yamakuchi M, Lowenstein CJ (2009) MiR-34, SIRT1 and p53: the feedback loop. Cell Cycle 8:712–715

    Article  PubMed  CAS  Google Scholar 

  58. Yamakuchi M, Ferlito M, Lowenstein CJ (2008) miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci USA 105:13421–13426

    Article  PubMed  PubMed Central  Google Scholar 

  59. Bork S, Horn P, Castoldi M, Hellwig I, Ho AD, Wagner W (2011) Adipogenic differentiation of human mesenchymal stromal cells is down-regulated by microRNA-369-5p and up-regulated by microRNA-371. J Cell Physiol 226:2226–2234

    Article  PubMed  CAS  Google Scholar 

  60. Oishi Y, Manabe I, Tobe K, Tsushima K, Shindo T, Fujiu K, Nishimura G, Maemura K, Yamauchi T, Kubota N, Suzuki R, Kitamura T, Akira S, Kadowaki T, Nagai R (2005) Kruppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation. Cell Metab 1:27–39

    Article  PubMed  CAS  Google Scholar 

  61. Kinoshita M, Ono K, Horie T, Nagao K, Nishi H, Kuwabara Y, Takanabe-Mori R, Hasegawa K, Kita T, Kimura T (2010) Regulation of adipocyte differentiation by activation of serotonin (5-HT) receptors 5-HT2AR and 5-HT2CR and involvement of microRNA-448-mediated repression of KLF5. Mol Endocrinol 24:1978–1987

    Article  PubMed  CAS  Google Scholar 

  62. Farmer SR (2006) Transcriptional control of adipocyte formation. Cell Metab 4:263–273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Pratt SL, Burns TA, Curry E, Duckett SK (2010) Expression of microRNA during bovine adipogenesis. J Nucleic Acids Investig 1:12

    Article  CAS  Google Scholar 

  64. Hulsmans M, De Keyzer D, Holvoet P (2011) MicroRNAs regulating oxidative stress and inflammation in relation to obesity and atherosclerosis. FASEB J 25:2515–2527

    Article  PubMed  CAS  Google Scholar 

  65. Kang M, Yan LM, Li YM, Zhang WY, Wang H, Tang AZ, Ou HS (2013) Inhibitory effect of microRNA-24 on fatty acid-binding protein expression on 3T3-L1 adipocyte differentiation. Genet Mol Res 12:5267–5277

    Article  PubMed  CAS  Google Scholar 

  66. McGregor RA, Choi MS (2011) microRNAs in the regulation of adipogenesis and obesity. Curr Mol Med 11:304–316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Romao JM, Jin W, Dodson MV, Hausman GJ, Moore SS, le Guan L (2011) MicroRNA regulation in mammalian adipogenesis. Exp Biol Med (Maywood) 236:997–1004

    Article  CAS  Google Scholar 

  68. Lin Q, Gao Z, Alarcon RM, Ye J, Yun Z (2009) A role of miR-27 in the regulation of adipogenesis. FEBS J 276:2348–2358

    Article  PubMed  CAS  Google Scholar 

  69. Sacco J, Adeli K (2012) MicroRNAs: emerging roles in lipid and lipoprotein metabolism. Curr Opin Lipidol 23:220–225

    Article  PubMed  CAS  Google Scholar 

  70. Lee J, Kemper JK (2010) Controlling SIRT1 expression by microRNAs in health and metabolic disease. Aging (Albany NY) 2:527–534

    CAS  Google Scholar 

  71. John E, Wienecke-Baldacchino A, Liivrand M, Heinaniemi M, Carlberg C, Sinkkonen L (2012) Dataset integration identifies transcriptional regulation of microRNA genes by PPARgamma in differentiating mouse 3T3-L1 adipocytes. Nucleic Acids Res 40:4446–4460

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Esau C, Kang X, Peralta E, Hanson E, Marcusson EG, Ravichandran LV, Sun Y, Koo S, Perera RJ, Jain R, Dean NM, Freier SM, Bennett CF, Lollo B, Griffey R (2004) MicroRNA-143 regulates adipocyte differentiation. J Biol Chem 279:52361–52365

    Article  PubMed  CAS  Google Scholar 

  73. Kajimoto K, Naraba H, Iwai N (2006) MicroRNA and 3T3-L1 pre-adipocyte differentiation. RNA 12:1626–1632

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge the help from J. Segers, T. B. Wilson and L. Shoup at the time of collecting tissue samples, as well as the rest of the staff at the University of Illinois Beef and Sheep Field Laboratory for animal handling and care. Supported in part by a competitive grant from the “Division of Nutritional Sciences: Vision 20/20’’ (University of Illinois, Urbana-Champaign) interdisciplinary nutrition-related research program. Project # ILLU-971-352 (National Institute of Food and Agriculture, USA).

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Moisá, S.J., Shike, D.W., Shoup, L. et al. Maternal Plane of Nutrition During Late-Gestation and Weaning Age Alter Steer Calf Longissimus Muscle Adipogenic MicroRNA and Target Gene Expression. Lipids 51, 123–138 (2016). https://doi.org/10.1007/s11745-015-4092-y

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