Polysome profiling shows extensive posttranscriptional regulation during human adipocyte stem cell differentiation into adipocytes

Stem Cell Research

Volumn 11, Issue 2, 2013, Pages 902-912

  Spangenberg, Lucia ^b   Shigunov, Patricia ^a   Abud, Ana Paula R ^a   Cofré, Axel R ^a   Stimamiglio, Marco A ^a   Kuligovski, Crisciele ^a   Zych, Jaiesa ^a   Schittini, Andressa V ^a   Costa, Alexandre Dias Tavares ^a   Rebelatto, Carmen K ^c   Brofman, Paulo R S ^c   Goldenberg, Samuel ^a   Correa, Alejandro ^a   Naya, Hugo ^b   Dallagiovanna, Bruno ^a  

^a INSTITUTO CARLOS CHAGAS   (Brazil)

^b INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^c PONTIFICAL CATHOLIC UNIVERSITY OF PARANÁ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ADIPOCYTE; ADIPOGENESIS; ADULT; ARTICLE; CASE REPORT; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; DIFFERENTIATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; POLYSOME; PRIORITY JOURNAL; REGULATORY MECHANISM; RIBOSOME; STEM CELL; UNTRANSLATED REGION;

3' UNTRANSLATED REGIONS; ADIPOCYTES; ADIPOGENESIS; ADULT; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION REGULATION; GLUTATHIONE; HUMANS; MALE; MIDDLE AGED; POLYRIBOSOMES; RNA, MESSENGER; STEM CELLS; TRANSCRIPTION, GENETIC; YOUNG ADULT;

EID: 84880378722     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.06.002     Document Type: Article

References (54)

1. Arteel G.E., Sies H. The biochemistry of selenium and the glutathione system. Environ. Toxicol. Pharmacol. 2001, 10:153-158.
2. Baer P.C., Geiger H. Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int. 2012, 2012:812693.
3. Bar M., Wyman S.K., Fritz B.R., Qi J., Garg K.S., Parkin R.K., Kroh E.M., Bendoraite A., Mitchell P.S., Nelson A.M., Ruzzo W.L., Ware C., Radich J.P., Gentleman R., Ruohola-Baker H., Tewari M. MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries. Stem Cells 2008, 26:2496-2505.
4. Barski O.A., Tipparaju S.M., Bhatnagar A. The aldo-keto reductase superfamily and its role in drug metabolism and detoxification. Drug Metab. Rev. 2008, 40:553-624.
5. Brigelius-Flohe R. Tissue-specific functions of individual glutathione peroxidases. Free Radic. Biol. Med. 1999, 27:951-965.
6. Dai M., Thompson R.C., Maher C., Contreras-Galindo R., Kaplan M.H., Markovitz D.M., Omenn G., Meng F. NGSQC: cross-platform quality analysis pipeline for deep sequencing data. BMC Genomics 2010, 11(Suppl. 4):S7.
7. De Ugarte D.A., Morizono K., Elbarbary A., Alfonso Z., Zuk P.A., Zhu M., Dragoo J.L., Ashjian P., Thomas B., Benhaim P., Chen I., Fraser J., Hedrick M.H. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003, 174:101-109.
8. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
9. Fromm-Dornieden C., von der Heyde S., Lytovchenko O., Salinas-Riester G., Brenig B., Beissbarth T., Baumgartner B.G. Novel polysome messages and changes in translational activity appear after induction of adipogenesis in 3T3-L1 cells. BMC Mol. Biol. 2012, 13:9.
10. Gimble J.M., Katz A.J., Bunnell B.A. Adipose-derived stem cells for regenerative medicine. Circ. Res. 2007, 100:1249-1260.
11. Ginsburg E., Vonderhaar B.K. Prolactin synthesis and secretion by human breast cancer cells. Cancer Res. 1995, 55:2591-2595.
12. Green C.B., Douris N., Kojima S., Strayer C.A., Fogerty J., Lourim D., Keller S.R., Besharse J.C. Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9888-9893.
13. Halbeisen R.E., Gerber A.P. Stress-dependent coordination of transcriptome and translatome in yeast. PLoS Biol. 2009, 7:e1000105.
14. Haston K.M., Tung J.Y., Reijo Pera R.A. Dazl functions in maintenance of pluripotency and genetic and epigenetic programs of differentiation in mouse primordial germ cells in vivo and in vitro. PLoS One 2009, 4:e5654.
15. Holetz F.B., Correa A., Avila A.R., Nakamura C.V., Krieger M.A., Goldenberg S. Evidence of P-body-like structures in Trypanosoma cruzi. Biochem. Biophys. Res. Commun. 2007, 356:1062-1067.
16. Hugo E.R., Brandebourg T.D., Comstock C.E., Gersin K.S., Sussman J.J., Ben-Jonathan N. LS14: a novel human adipocyte cell line that produces prolactin. Endocrinology 2006, 147:306-313.
17. Ivanova N.B., Dimos J.T., Schaniel C., Hackney J.A., Moore K.A., Lemischka I.R. A stem cell molecular signature. Science 2002, 298:601-604.
18. Jash A., Yun K., Sahoo A., So J.S., Im S.H. Looping mediated interaction between the promoter and 3' UTR regulates type II collagen expression in chondrocytes. PLoS One 2012, 7:e40828.
19. Jeong J.A., Ko K.M., Bae S., Jeon C.J., Koh G.Y., Kim H. Genome-wide differential gene expression profiling of human bone marrow stromal cells. Stem Cells 2007, 25:994-1002.
20. Jeong J.A., Ko K.M., Park H.S., Lee J., Jang C., Jeon C.J., Koh G.Y., Kim H. Membrane proteomic analysis of human mesenchymal stromal cells during adipogenesis. Proteomics 2007, 7:4181-4191.
21. Ji Z., Lee J.Y., Pan Z., Jiang B., Tian B. Progressive lengthening of 3' untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7028-7033.
22. Kawai M., Green C.B., Lecka-Czernik B., Douris N., Gilbert M.R., Kojima S., Ackert-Bicknell C., Garg N., Horowitz M.C., Adamo M.L., Clemmons D.R., Rosen C.J. A circadian-regulated gene, Nocturnin, promotes adipogenesis by stimulating PPAR-gamma nuclear translocation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10508-10513.
23. Keene J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 2007, 8:533-543.
24. Keene J.D. The global dynamics of RNA stability orchestrates responses to cellular activation. BMC Biol. 2010, 8:95.
25. Kheterpal I., Ku G., Coleman L., Yu G., Ptitsyn A.A., Floyd Z.E., Gimble J.M. Proteome of human subcutaneous adipose tissue stromal vascular fraction cells versus mature adipocytes based on DIGE. J. Proteome Res. 2011, 10:1519-1527.
26. Kim J., Choi Y.S., Lim S., Yea K., Yoon J.H., Jun D.J., Ha S.H., Kim J.W., Kim J.H., Suh P.G., Ryu S.H., Lee T.G. Comparative analysis of the secretory proteome of human adipose stromal vascular fraction cells during adipogenesis. Proteomics 2010, 10:394-405.
27. Kolle G., Shepherd J.L., Gardiner B., Kassahn K.S., Cloonan N., Wood D.L., Nourbakhsh E., Taylor D.F., Wani S., Chy H.S., Zhou Q., McKernan K., Kuersten S., Laslett A.L., Grimmond S.M. Deep-transcriptome and ribonome sequencing redefines the molecular networks of pluripotency and the extracellular space in human embryonic stem cells. Genome Res. 2011, 21:2014-2025.
28. Kratchmarova I., Blagoev B., Haack-Sorensen M., Kassem M., Mann M. Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 2005, 308:1472-1477.
29. Liao Y., Smith G.K., Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013, 41(10):e108.
30. Lundberg E., Fagerberg L., Klevebring D., Matic I., Geiger T., Cox J., Algenas C., Lundeberg J., Mann M., Uhlen M. Defining the transcriptome and proteome in three functionally different human cell lines. Mol. Syst. Biol. 2010, 6:450.
31. McAveney K.M., Gimble J.M., Yu-Lee L. Prolactin receptor expression during adipocyte differentiation of bone marrow stroma. Endocrinology 1996, 137:5723-5726.
32. Menssen A., Haupl T., Sittinger M., Delorme B., Charbord P., Ringe J. Differential gene expression profiling of human bone marrow-derived mesenchymal stem cells during adipogenic development. BMC Genomics 2011, 12:461.
33. Mignone F., Gissi C., Liuni S., Pesole G. Untranslated regions of mRNAs. Genome Biol. 2002, 3. (REVIEWS0004).
34. Mittal N., Roy N., Babu M.M., Janga S.C. Dissecting the expression dynamics of RNA-binding proteins in posttranscriptional regulatory networks. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20300-20305.
35. Molina H., Yang Y., Ruch T., Kim J.W., Mortensen P., Otto T., Nalli A., Tang Q.Q., Lane M.D., Chaerkady R., Pandey A. Temporal profiling of the adipocyte proteome during differentiation using a five-plex SILAC based strategy. J. Proteome Res. 2009, 8:48-58.
36. Nanbu-Wakao R., Fujitani Y., Masuho Y., Muramatu M., Wakao H. Prolactin enhances CCAAT enhancer-binding protein-beta (C/EBP beta) and peroxisome proliferator-activated receptor gamma (PPAR gamma) messenger RNA expression and stimulates adipogenic conversion of NIH-3T3 cells. Mol. Endocrinol. 2000, 14:307-316.
37. Nielsen A.E., Bohr A., Penkowa M. The balance between life and death of cells: roles of metallothioneins. Biomark. Insights 2007, 1:99-111.
38. Preiss T., Baron-Benhamou J., Ansorge W., Hentze M.W. Homodirectional changes in transcriptome composition and mRNA translation induced by rapamycin and heat shock. Nat. Struct. Biol. 2003, 10:1039-1047.
39. Ptitsyn A.A., Gimble J.M. Analysis of circadian pattern reveals tissue-specific alternative transcription in leptin signaling pathway. BMC Bioinformatics 2007, 8(Suppl. 7):S15.
40. Rebelatto C.K., Aguiar A.M., Moretao M.P., Senegaglia A.C., Hansen P., Barchiki F., Oliveira J., Martins J., Kuligovski C., Mansur F., Christofis A., Amaral V.F., Brofman P.S., Goldenberg S., Nakao L.S., Correa A. Dissimilar differentiation of mesenchymal stem cells from bone marrow, umbilical cord blood, and adipose tissue. Exp. Biol. Med. (Maywood) 2008, 233:901-913.
41. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
42. Sampath P., Pritchard D.K., Pabon L., Reinecke H., Schwartz S.M., Morris D.R., Murry C.E. A hierarchical network controls protein translation during murine embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2008, 2:448-460.
43. Sandberg R., Neilson J.R., Sarma A., Sharp P.A., Burge C.B. Proliferating cells express mRNAs with shortened 3' untranslated regions and fewer microRNA target sites. Science 2008, 320:1643-1647.
44. Sharova L.V., Sharov A.A., Nedorezov T., Piao Y., Shaik N., Ko M.S. Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res. 2009, 16:45-58.
45. Song L., Webb N.E., Song Y., Tuan R.S. Identification and functional analysis of candidate genes regulating mesenchymal stem cell self-renewal and multipotency. Stem Cells 2006, 24:1707-1718.
46. Stewart W.C., Baugh J.E., Floyd Z.E., Stephens J.M. STAT 5 activators can replace the requirement of FBS in the adipogenesis of 3T3-L1 cells. Biochem. Biophys. Res. Commun. 2004, 324:355-359.
47. Tebaldi T., Re A., Viero G., Pegoretti I., Passerini A., Blanzieri E., Quattrone A. Widespread uncoupling between transcriptome and translatome variations after a stimulus in mammalian cells. BMC Genomics 2012, 13:220.
48. Viengchareun S., Servel N., Feve B., Freemark M., Lombes M., Binart N. Prolactin receptor signaling is essential for perinatal brown adipocyte function: a role for insulin-like growth factor-2. PLoS One 2008, 3:e1535.
49. Vigilanza P., Aquilano K., Baldelli S., Rotilio G., Ciriolo M.R. Modulation of intracellular glutathione affects adipogenesis in 3T3-L1 cells. J. Cell. Physiol. 2011, 226:2016-2024.
50. Washburn M.P., Koller A., Oshiro G., Ulaszek R.R., Plouffe D., Deciu C., Winzeler E., Yates J.R. Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3107-3112.
51. Yang S.R., Rahman I., Trosko J.E., Kang K.S. Oxidative stress-induced biomarkers for stem cell-based chemical screening. Prev. Med. 2012, 54:S42-S49. (Suppl.).
52. Young M.D., Wakefield M.J., Smyth G.K., Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010, 11:R14.
53. Zhang H., Lee J.Y., Tian B. Biased alternative polyadenylation in human tissues. Genome Biol. 2005, 6:R100.
54. Zhang Q., Ramlee M.K., Brunmeir R., Villanueva C.J., Halperin D., Xu F. Dynamic and distinct histone modifications modulate the expression of key adipogenesis regulatory genes. Cell Cycle 2012, 11:4310-4322.