期刊论文详细信息
BMC Genomics
Dynamics of mRNA and polysomal abundance in early 3T3-L1 adipogenesis
Bernhard G Baumgartner4  Tim Beissbarth2  Gabriela Salinas-Riester3  Carolin Fromm-Dornieden1  Silvia von der Heyde2 
[1] Institute for Research in Operative Medicine (IFOM), Witten/Herdecke University, Ostmerheimer Straße 200, 51109 Cologne, Germany;Department of Medical Statistics, Statistical Bioinformatics, University Medical Center Göttingen, Humboldtallee 32, 37073 Göttingen, Germany;Department of Developmental Biochemistry, DNA Microarray and Deep-Sequencing Facility Göttingen, University of Göttingen, Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany;Department of Internal Medicine, Metabolic Diseases and Medical Molecular Biology, Paracelsus Private Medical University Salzburg, Müllner Hauptstr 48, 5020 Salzburg, Austria
关键词: TOP motif;    Differential expression;    Gene enrichment;    Gene ontology;    3T3-L1 pre-adipocytes;    Translation;    Transcription;    Adipogenesis;   
Others  :  1217220
DOI  :  10.1186/1471-2164-15-381
 received in 2013-12-20, accepted in 2014-05-07,  发布年份 2014
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【 摘 要 】

Background

Adipogenesis is a complex process, in which immature pre-adipocytes change morphology, micro-anatomy and physiology to become mature adipocytes. These store and accumulate fat and release diverse hormones. Massive changes in protein content and protein composition of the transforming cell take place within a short time-frame.

In a previous study we analyzed changes in the abundance of free and polysomal, i.e. ribosome bound, RNAs in the first hours of adipogenesis in the murine cell line 3T3-L1. Here we analyze changes of mRNA levels and their potential contribution to the changing protein pool by determination of mRNA levels and ribosome binding to mRNAs in 3T3-L1 cells stimulated for adipogenesis. We grouped mRNA species into categories with respect to up- or down-regulated transcription and translation and analyzed the groups regarding specific functionalities based on Gene Ontology (GO).

Results

A shift towards up-regulation of gene expression in early adipogenesis was detected. Genes up-regulated at the transcriptional (TC:up) and translational (TL:up) level (TC:up/TL:up) are very likely involved in control and logistics of translation. Many of them are known to contain a TOP motif. In the TC:up/TL:unchanged group we detected most of the metal binding proteins and metal transporters. In the TC:unchanged/TL:up group several factors of the olfactory receptor family were identified, while in TC:unchanged/TL:down methylation and repair genes are represented. In the TC:down/TL:up group we detected many signaling factors. The TC:down/TL:unchanged group mainly consists of regulatory factors.

Conclusions

Within the first hours of adipogenesis, changes in transcriptional and translational regulation take place. Notably, genes with a specific biological or molecular function tend to cluster in groups according to their transcriptional and translational regulation.

【 授权许可】

   
2014 von der Heyde et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Burton GR, Guan Y, Nagarajan R, McGehee RE Jr: Microarray analysis of gene expression during early adipocyte differentiation. Gene 2002, 293:21-31.
  • [2]Calkhoven CF, Müller C, Leutz A: Translational control of C/EBPalpha and C/EBPbeta isoform expression. Genes Dev 2000, 14:1920-1932.
  • [3]Kim T-H, Kim M-Y, Jo S-H, Park J-M, Ahn Y-H: Modulation of the transcriptional activity of peroxisome proliferator-activated receptor gamma by protein-protein interactions and post-translational modifications. Yonsei Med J 2013, 54:545-559.
  • [4]Melamed D, Eliyahu E, Arava Y: Exploring translation regulation by global analysis of ribosomal association. Methods San Diego Calif 2009, 48:301-305.
  • [5]Meyuhas O: Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem FEBS 2000, 267:6321-6330.
  • [6]MacDougald OA, Lane MD: Transcriptional regulation of gene expression during adipocyte differentiation. Annu Rev Biochem 1995, 64:345-373.
  • [7]Mishra A, Zhu X-G, Ge K, Cheng S-Y: Adipogenesis is differentially impaired by thyroid hormone receptor mutant isoforms. J Mol Endocrinol 2010, 44:247-255.
  • [8]Poulos SP, Dodson MV, Hausman GJ: Cell line models for differentiation: preadipocytes and adipocytes. Exp Biol Med Maywood NJ 2010, 235:1185-1193.
  • [9]Mariman ECM, Wang P: Adipocyte extracellular matrix composition, dynamics and role in obesity. Cell Mol Life Sci CMLS 2010, 67:1277-1292.
  • [10]James AW: Review of signaling pathways governing MSC osteogenic and adipogenic differentiation. Scientifica 2013, 2013:684736.
  • [11]Fromm-Dornieden C, von der Heyde S, Lytovchenko O, Salinas-Riester G, Brenig B, Beissbarth T, Baumgartner BG: Novel polysome messages and changes in translational activity appear after induction of adipogenesis in 3T3-L1 cells. BMC Mol Biol 2012, 13:9. BioMed Central Full Text
  • [12]Alexa A, Rahnenführer J, Lengauer T: Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinforma Oxf Engl 2006, 22:1600-1607.
  • [13]Hamilton TL, Stoneley M, Spriggs KA, Bushell M: TOPs and their regulation. Biochem Soc Trans 2006, 34(Pt 1):12-16.
  • [14]Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM: A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 2012, 485:109-113.
  • [15]Grillo G, Turi A, Licciulli F, Mignone F, Liuni S, Banfi S, Gennarino VA, Horner DS, Pavesi G, Picardi E, Pesole G: UTRdb and UTRsite (RELEASE 2010): a collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acids Res 2010, 38(Database issue):D75-D80.
  • [16]Elias I, Franckhauser S, Bosch F: New insights into adipose tissue VEGF-A actions in the control of obesity and insulin resistance. Adipocyte 2013, 2:109-112.
  • [17]Lu H, Ward MG, Adeola O, Ajuwon KM: Regulation of adipocyte differentiation and gene expression-crosstalk between TGFβ and wnt signaling pathways. Mol Biol Rep 2013, 40:5237-5245.
  • [18]Wang Y, Hudak C, Sul HS: Role of preadipocyte factor 1 in adipocyte differentiation. Clin Lipidol 2010, 5:109-115.
  • [19]Briand N, le Lay S, Sessa WC, Ferré P, Dugail I: Distinct roles of endothelial and adipocyte caveolin-1 in macrophage infiltration and adipose tissue metabolic activity. Diabetes 2011, 60:448-453.
  • [20]Tenney R, Stansfield K, Pekala PH: Interleukin 11 signaling in 3T3-L1 adipocytes. J Cell Physiol 2005, 202:160-166.
  • [21]Shi X, Shi W, Li Q, Song B, Wan M, Bai S, Cao X: A glucocorticoid-induced leucine-zipper protein, GILZ, inhibits adipogenesis of mesenchymal cells. EMBO Rep 2003, 4:374-380.
  • [22]Jackson B, Tilli CMLJ, Hardman MJ, Avilion AA, MacLeod MC, Ashcroft GS, Byrne C: Late cornified envelope family in differentiating epithelia–response to calcium and ultraviolet irradiation. J Invest Dermatol 2005, 124:1062-1070.
  • [23]Rinnerthaler M, Duschl J, Steinbacher P, Salzmann M, Bischof J, Schuller M, Wimmer H, Peer T, Bauer JW, Richter K: Age-related changes in the composition of the cornified envelope in human skin. Exp Dermatol 2013, 22:329-335.
  • [24]Ishii I, Ikeguchi Y, Mano H, Wada M, Pegg AE, Shirahata A: Polyamine metabolism is involved in adipogenesis of 3T3-L1 cells. Amino Acids 2012, 42:619-626.
  • [25]Wang T, Zhang J-C, Chen Y, Xiao P-G, Yang M-S: Effect of zinc ion on the osteogenic and adipogenic differentiation of mouse primary bone marrow stromal cells and the adipocytic trans-differentiation of mouse primary osteoblasts. J Trace Elem Med Biol Organ Soc Miner Trace Elem GMS 2007, 21:84-91.
  • [26]Vardatsikos G, Pandey NR, Srivastava AK: Insulino-mimetic and anti-diabetic effects of zinc. J Inorg Biochem 2013, 120:8-17.
  • [27]Garrido-Sánchez L, García-Fuentes E, Fernández-García D, Escoté X, Alcaide J, Perez-Martinez P, Vendrell J, Tinahones FJ: Zinc-alpha 2-glycoprotein gene expression in adipose tissue is related with insulin resistance and lipolytic genes in morbidly obese patients. PLoS One 2012, 7:e33264.
  • [28]Yang M, Liu R, Li S, Luo Y, Zhang Y, Zhang L, Liu D, Wang Y, Xiong Z, Boden G, Chen S, Li L, Yang G: Zinc-α2-glycoprotein is associated with insulin resistance in humans and is regulated by hyperglycemia, hyperinsulinemia, or liraglutide administration: cross-sectional and interventional studies in normal subjects, insulin-resistant subjects, and subjects with newly diagnosed diabetes. Diabetes Care 2013, 36:1074-1082.
  • [29]Wei S, Zhang L, Zhou X, Du M, Jiang Z, Hausman GJ, Bergen WG, Zan L, Dodson MV: Emerging roles of zinc finger proteins in regulating adipogenesis. Cell Mol Life Sci CMLS 2013, 70:4569-4584.
  • [30]Kang S, Akerblad P, Kiviranta R, Gupta RK, Kajimura S, Griffin MJ, Min J, Baron R, Rosen ED: Regulation of early adipose commitment by Zfp521. PLoS Biol 2012, 10:e1001433.
  • [31]Gupta RK, Arany Z, Seale P, Mepani RJ, Ye L, Conroe HM, Roby YA, Kulaga H, Reed RR, Spiegelman BM: Transcriptional control of preadipocyte determination by Zfp423. Nature 2010, 464:619-623.
  • [32]Meruvu S, Hugendubler L, Mueller E: Regulation of adipocyte differentiation by the zinc finger protein ZNF638. J Biol Chem 2011, 286:26516-26523.
  • [33]Hasegawa R, Tomaru Y, de Hoon M, Suzuki H, Hayashizaki Y, Shin JW: Identification of ZNF395 as a novel modulator of adipogenesis. Exp Cell Res 2013, 319:68-76.
  • [34]Lee Y, Kim SH, Lee YJ, Kang ES, Lee B-W, Cha BS, Kim JW, Song DH, Lee HC: Transcription factor Snail is a novel regulator of adipocyte differentiation via inhibiting the expression of peroxisome proliferator-activated receptor γ. Cell Mol Life Sci CMLS 2013, 70:3959-3971.
  • [35]Wu Z, Wang S: Role of kruppel-like transcription factors in adipogenesis. Dev Biol 2013, 373:235-243.
  • [36]Kawagishi H, Wakoh T, Uno H, Maruyama M, Moriya A, Morikawa S, Okano H, Sherr CJ, Takagi M, Sugimoto M: Hzf regulates adipogenesis through translational control of C/EBPalpha. EMBO J 2008, 27:1481-1490.
  • [37]Shang CA, Thompson BJL, Teasdale R, Brown RJ, Waters MJ: Genes induced by growth hormone in a model of adipogenic differentiation. Mol Cell Endocrinol 2002, 189:213-219.
  • [38]Abu-Farha M, Tiss A, Abubaker J, Khadir A, Al-Ghimlas F, Al-Khairi I, Baturcam E, Cherian P, Elkum N, Hammad M, John J, Kavalakatt S, Warsame S, Behbehani K, Dermime S, Dehbi M: Proteomics analysis of human obesity reveals the epigenetic factor HDAC4 as a potential target for obesity. PLoS One 2013, 8:e75342.
  • [39]Kong P, Gonzalez-Quesada C, Li N, Cavalera M, Lee D-W, Frangogiannis NG: Thrombospondin-1 regulates adiposity and metabolic dysfunction in diet-induced obesity enhancing adipose inflammation and stimulating adipocyte proliferation. Am J Physiol Endocrinol Metab 2013, 305:E439-E450.
  • [40]Oguro R, Kamide K, Katsuya T, Akasaka H, Sugimoto K, Congrains A, Arai Y, Hirose N, Saitoh S, Ohishi M, Miura T, Rakugi H: A single nucleotide polymorphism of the adenosine deaminase, RNA-specific gene is associated with the serum triglyceride level, abdominal circumference, and serum adiponectin concentration. Exp Gerontol 2012, 47:183-187.
  • [41]Akerblad P, Lind U, Liberg D, Bamberg K, Sigvardsson M: Early B-cell factor (O/E-1) is a promoter of adipogenesis and involved in control of genes important for terminal adipocyte differentiation. Mol Cell Biol 2002, 22:8015-8025.
  • [42]Liberg D, Sigvardsson M, Akerblad P: The EBF/Olf/Collier family of transcription factors: regulators of differentiation in cells originating from all three embryonal germ layers. Mol Cell Biol 2002, 22:8389-8397.
  • [43]Jimenez MA, Akerblad P, Sigvardsson M, Rosen ED: Critical role for Ebf1 and Ebf2 in the adipogenic transcriptional cascade. Mol Cell Biol 2007, 27:743-757.
  • [44]Zhu D, Shi S, Wang H, Liao K: Growth arrest induces primary-cilium formation and sensitizes IGF-1-receptor signaling during differentiation induction of 3T3-L1 preadipocytes. J Cell Sci 2009, 122(Pt 15):2760-2768.
  • [45]Boekhoff I, Tareilus E, Strotmann J, Breer H: Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J 1990, 9:2453-2458.
  • [46]Al-Aidaroos AQO, Yuen HF, Guo K, Zhang SD, Chung T-H, Chng WJ, Zeng Q: Metastasis-associated PRL-3 induces EGFR activation and addiction in cancer cells. J Clin Invest 2013, 123:3459-3471.
  • [47]Firestein S: How the olfactory system makes sense of scents. Nature 2001, 413:211-218.
  • [48]Lee J, Saha PK, Yang Q-H, Lee S, Park JY, Suh Y, Lee S-K, Chan L, Roeder RG, Lee JW: Targeted inactivation of MLL3 histone H3-Lys-4 methyltransferase activity in the mouse reveals vital roles for MLL3 in adipogenesis. Proc Natl Acad Sci U S A 2008, 105:19229-19234.
  • [49]Gan GN, Wittschieben JP, Wittschieben BØ, Wood RD: DNA polymerase zeta (pol zeta) in higher eukaryotes. Cell Res 2008, 18:174-183.
  • [50]Sleeman MW, Wortley KE, Lai K-MV, Gowen LC, Kintner J, Kline WO, Garcia K, Stitt TN, Yancopoulos GD, Wiegand SJ, Glass DJ: Absence of the lipid phosphatase SHIP2 confers resistance to dietary obesity. Nat Med 2005, 11:199-205.
  • [51]Wang M, Wang JJ, Li J, Park K, Qian X, Ma J, Zhang SX: Pigment epithelium-derived factor suppresses adipogenesis via inhibition of the MAPK/ERK pathway in 3T3-L1 preadipocytes. Am J Physiol Endocrinol Metab 2009, 297:E1378-E1387.
  • [52]Cho H, Black SC, Looper D, Shi M, Kelly-Sullivan D, Timofeevski S, Siegel K, Yu X-H, McDonnell SR, Chen P, Yie J, Ogilvie KM, Fraser J, Briscoe CP: Pharmacological characterization of a small molecule inhibitor of c-Jun kinase. Am J Physiol Endocrinol Metab 2008, 295:E1142-E1151.
  • [53]DuBois RN, Gupta R, Brockman J, Reddy BS, Krakow SL, Lazar MA: The nuclear eicosanoid receptor, PPARgamma, is aberrantly expressed in colonic cancers. Carcinogenesis 1998, 19:49-53.
  • [54]Ali AT, Hochfeld WE, Myburgh R, Pepper MS: Adipocyte and adipogenesis. Eur J Cell Biol 2013, 92:229-236.
  • [55]Adachi H, Kurachi H, Homma H, Adachi K, Imai T, Morishige K, Matsuzawa Y, Miyake A: Epidermal growth factor promotes adipogenesis of 3T3-L1 cell in vitro. Endocrinology 1994, 135:1824-1830.
  • [56]Harrington M, Pond-Tor S, Boney CM: Role of epidermal growth factor and ErbB2 receptors in 3T3-L1 adipogenesis. Obes Silver Spring Md 2007, 15:563-571.
  • [57]Nakano N, Miyazawa N, Sakurai T, Kizaki T, Kimoto K, Takahashi K, Ishida H, Takahashi M, Suzuki K, Ohno H: Gliclazide inhibits proliferation but stimulates differentiation of white and brown adipocytes. J Biochem (Tokyo) 2007, 142:639-645.
  • [58]Rogers C, Moukdar F, McGee MA, Davis B, Buehrer BM, Daniel KW, Collins S, Barakat H, Robidoux J: EGF receptor (ERBB1) abundance in adipose tissue is reduced in insulin-resistant and type 2 diabetic women. J Clin Endocrinol Metab 2012, 97:E329-E340.
  • [59]Harmon AW, Patel YM, Harp JB: Genistein inhibits CCAAT/enhancer-binding protein beta (C/EBPbeta) activity and 3T3-L1 adipogenesis by increasing C/EBP homologous protein expression. Biochem J 2002, 367(Pt 1):203-208.
  • [60]Moore T, Beltran L, Carbajal S, Hursting SD, DiGiovanni J: Energy balance modulates mouse skin tumor promotion through altered IGF-1R and EGFR crosstalk. Cancer Prev Res Phila Pa 2012, 5:1236-1246.
  • [61]Moore T, Beltran L, Carbajal S, Strom S, Traag J, Hursting SD, DiGiovanni J: Dietary energy balance modulates signaling through the Akt/mammalian target of rapamycin pathways in multiple epithelial tissues. Cancer Prev Res Phila Pa 2008, 1:65-76.
  • [62]Davis AA, Kaklamani VG: Metabolic syndrome and triple-negative breast cancer: a new paradigm. Int J Breast Cancer 2012, 2012:809291.
  • [63]Saxena NK, Taliaferro-Smith L, Knight BB, Merlin D, Anania FA, O’Regan RM, Sharma D: Bidirectional crosstalk between leptin and insulin-like growth factor-I signaling promotes invasion and migration of breast cancer cells via transactivation of epidermal growth factor receptor. Cancer Res 2008, 68:9712-9722.
  • [64]Ogunwobi O, Mutungi G, Beales ILP: Leptin stimulates proliferation and inhibits apoptosis in Barrett’s esophageal adenocarcinoma cells by cyclooxygenase-2-dependent, prostaglandin-E2-mediated transactivation of the epidermal growth factor receptor and c-Jun NH2-terminal kinase activation. Endocrinology 2006, 147:4505-4516.
  • [65]Prasad NK, Tandon M, Handa A, Moore GE, Babbs CF, Snyder PW, Bose S: High expression of obesity-linked phosphatase SHIP2 in invasive breast cancer correlates with reduced disease-free survival. Tumour Biol J Int Soc Oncol Dev Biol Med 2008, 29:330-341.
  • [66]Prasad NK, Decker SJ: SH2-containing 5′-inositol phosphatase, SHIP2, regulates cytoskeleton organization and ligand-dependent down-regulation of the epidermal growth factor receptor. J Biol Chem 2005, 280:13129-13136.
  • [67]Miettinen PJ, Ustinov J, Ormio P, Gao R, Palgi J, Hakonen E, Juntti-Berggren L, Berggren P-O, Otonkoski T: Downregulation of EGF receptor signaling in pancreatic islets causes diabetes due to impaired postnatal beta-cell growth. Diabetes 2006, 55:3299-3308.
  • [68]Hwang DL, Lev-Ran A, Tay YC, Chen CR, Dev N: Epidermal growth factor excretion and receptor binding in diabetic rats. Life Sci 1989, 44:407-416.
  • [69]Okamoto M, Kahn CR, Maron R, White MF: Decreased autophosphorylation of EGF receptor in insulin-deficient diabetic rats. Am J Physiol 1988, 254(4 Pt 1):E429-E434.
  • [70]Karasik A, Kahn CR: Dexamethasone-induced changes in phosphorylation of the insulin and epidermal growth factor receptors and their substrates in intact rat hepatocytes. Endocrinology 1988, 123:2214-2222.
  • [71]Supek F, Bošnjak M, Škunca N, Šmuc T: REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 2011, 6:e21800.
  • [72]Beissbarth T: Interpreting experimental results using gene ontologies. Methods Enzymol 2006, 411:340-352.
  • [73]Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, Kent WJ: The UCSC Table Browser data retrieval tool. Nucleic Acids Res 2004, 32(Database issue):D493-D496.
  • [74]R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.
  • [75]Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3(1):1-26. ISSN (Online) 1544-6115, doi:10.2202/1544-6115.1027
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