Advertisement

Lipids

, Volume 51, Issue 1, pp 123–138 | Cite as

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

  • Sonia J. Moisá
  • Daniel W. Shike
  • Lindsay Shoup
  • Juan J. Loor
Original Article

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.

Keywords

Nutrition Epigenetics Fetal programming Marbling 

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

Notes

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).

Compliance with Ethical Standards

Competing interests

Author(s) disclose no potential conflicts of interest.

Supplementary material

11745_2015_4092_MOESM1_ESM.docx (101 kb)
Supplementary material 1 (DOCX 100 kb)

References

  1. 1.
    Wilkins JF (2005) Genomic imprinting and methylation: epigenetic canalization and conflict. Trends Genet 21:356–365PubMedCrossRefGoogle Scholar
  2. 2.
    Munshi A, Shafi G, Aliya N, Jyothy A (2009) Histone modifications dictate specific biological readouts. J Genet Genom 36:75–88CrossRefGoogle Scholar
  3. 3.
    McKay JA, Mathers JC (2011) Diet induced epigenetic changes and their implications for health. Acta Physiol (Oxf) 202:103–118CrossRefGoogle Scholar
  4. 4.
    Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Jin W, Grant JR, Stothard P, Moore SS, Guan LL (2009) Characterization of bovine miRNAs by sequencing and bioinformatics analysis. BMC Mol Biol 10:90PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Basu U, Romao JM, Guan LL (2012) Adipogenic transcriptome profiling using high throughput technologies. J Genom 1:22–28CrossRefGoogle Scholar
  7. 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–E1714PubMedPubMedCentralCrossRefGoogle Scholar
  8. 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:e0131478PubMedPubMedCentralCrossRefGoogle Scholar
  9. 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 PubMedCrossRefGoogle Scholar
  10. 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. 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. 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–E215PubMedCrossRefGoogle Scholar
  13. 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 91:5485–5491PubMedCrossRefGoogle Scholar
  14. 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 8:17–32PubMedPubMedCentralGoogle Scholar
  15. 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 89:1391–1396PubMedCrossRefGoogle Scholar
  16. 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) 3:18CrossRefGoogle Scholar
  17. 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 37:49–58PubMedCrossRefGoogle Scholar
  18. 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 97:3431–3440PubMedCrossRefGoogle Scholar
  19. 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 97:3441–3448PubMedCrossRefGoogle Scholar
  20. 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 425:560–564PubMedCrossRefGoogle Scholar
  21. 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 83:788–795PubMedCrossRefGoogle Scholar
  22. 22.
    Xie H, Lim B, Lodish HF (2009) MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes 58:1050–1057PubMedPubMedCentralCrossRefGoogle Scholar
  23. 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:e98433PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 101:292–295PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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 91:209–217PubMedPubMedCentralCrossRefGoogle Scholar
  26. 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) 95:6–16CrossRefGoogle Scholar
  27. 27.
    Rottiers V, Naar AM (2012) MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 13:239–250PubMedPubMedCentralCrossRefGoogle Scholar
  28. 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 474:649–653PubMedCrossRefGoogle Scholar
  29. 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):119–128PubMedCrossRefGoogle Scholar
  30. 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 38:4273–4280PubMedCrossRefGoogle Scholar
  31. 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 40:5669–5675PubMedCrossRefGoogle Scholar
  32. 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 42:617–624PubMedCrossRefGoogle Scholar
  33. 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 45:820–826PubMedCrossRefGoogle Scholar
  34. 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 11:7PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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 27:3093–3102PubMedGoogle Scholar
  36. 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 227:183–193PubMedCrossRefGoogle Scholar
  37. 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 283:1026–1033PubMedCrossRefGoogle Scholar
  38. 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 587:1556–1561PubMedCrossRefGoogle Scholar
  39. 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 40:5027–5034PubMedCrossRefGoogle Scholar
  40. 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 12:352–361PubMedCrossRefGoogle Scholar
  41. 41.
    Romao JM, Jin W, He M, McAllister T, le Guan L (2014) MicroRNAs in bovine adipogenesis: genomic context, expression and function. BMC Genom 15:137CrossRefGoogle Scholar
  42. 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 11:29PubMedPubMedCentralCrossRefGoogle Scholar
  43. 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 127:2097–2106PubMedCrossRefGoogle Scholar
  44. 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 36:1552–1562PubMedCrossRefGoogle Scholar
  45. 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:e111537PubMedPubMedCentralCrossRefGoogle Scholar
  46. 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–E206PubMedPubMedCentralGoogle Scholar
  47. 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 33:1778–1788PubMedCrossRefGoogle Scholar
  48. 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) 46:590–596CrossRefGoogle Scholar
  49. 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 11:320CrossRefGoogle Scholar
  50. 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 40:222–229PubMedPubMedCentralCrossRefGoogle Scholar
  51. 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 14:194CrossRefGoogle Scholar
  52. 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:e87687PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 9:367–377PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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 587:3853–3858PubMedCrossRefGoogle Scholar
  55. 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:e9022PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Chen F, Hu SJ (2012) Effect of microRNA-34a in cell cycle, differentiation, and apoptosis: a review. J Biochem Mol Toxicol 26:79–86PubMedCrossRefGoogle Scholar
  57. 57.
    Yamakuchi M, Lowenstein CJ (2009) MiR-34, SIRT1 and p53: the feedback loop. Cell Cycle 8:712–715PubMedCrossRefGoogle Scholar
  58. 58.
    Yamakuchi M, Ferlito M, Lowenstein CJ (2008) miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci USA 105:13421–13426PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 226:2226–2234PubMedCrossRefGoogle Scholar
  60. 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 1:27–39PubMedCrossRefGoogle Scholar
  61. 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 24:1978–1987PubMedCrossRefGoogle Scholar
  62. 62.
    Farmer SR (2006) Transcriptional control of adipocyte formation. Cell Metab 4:263–273PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Pratt SL, Burns TA, Curry E, Duckett SK (2010) Expression of microRNA during bovine adipogenesis. J Nucleic Acids Investig 1:12CrossRefGoogle Scholar
  64. 64.
    Hulsmans M, De Keyzer D, Holvoet P (2011) MicroRNAs regulating oxidative stress and inflammation in relation to obesity and atherosclerosis. FASEB J 25:2515–2527PubMedCrossRefGoogle Scholar
  65. 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 12:5267–5277PubMedCrossRefGoogle Scholar
  66. 66.
    McGregor RA, Choi MS (2011) microRNAs in the regulation of adipogenesis and obesity. Curr Mol Med 11:304–316PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Romao JM, Jin W, Dodson MV, Hausman GJ, Moore SS, le Guan L (2011) MicroRNA regulation in mammalian adipogenesis. Exp Biol Med (Maywood) 236:997–1004CrossRefGoogle Scholar
  68. 68.
    Lin Q, Gao Z, Alarcon RM, Ye J, Yun Z (2009) A role of miR-27 in the regulation of adipogenesis. FEBS J 276:2348–2358PubMedCrossRefGoogle Scholar
  69. 69.
    Sacco J, Adeli K (2012) MicroRNAs: emerging roles in lipid and lipoprotein metabolism. Curr Opin Lipidol 23:220–225PubMedCrossRefGoogle Scholar
  70. 70.
    Lee J, Kemper JK (2010) Controlling SIRT1 expression by microRNAs in health and metabolic disease. Aging (Albany NY) 2:527–534Google Scholar
  71. 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 40:4446–4460PubMedPubMedCentralCrossRefGoogle Scholar
  72. 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 279:52361–52365PubMedCrossRefGoogle Scholar
  73. 73.
    Kajimoto K, Naraba H, Iwai N (2006) MicroRNA and 3T3-L1 pre-adipocyte differentiation. RNA 12:1626–1632PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© AOCS 2015

Authors and Affiliations

  • Sonia J. Moisá
    • 1
  • Daniel W. Shike
    • 2
  • Lindsay Shoup
    • 2
  • Juan J. Loor
    • 1
    • 2
    • 3
  1. 1.Mammalian NutriPhysioGenomics, Department of Animal SciencesUniversity of IllinoisUrbanaUSA
  2. 2.Department of Animal SciencesUniversity of IllinoisUrbanaUSA
  3. 3.Division of Nutritional Sciences, Illinois Informatics InstituteUniversity of IllinoisUrbanaUSA

Personalised recommendations