Posttranscriptional Control During Stem Cells Differentiation

  • Bruno Dallagiovanna
  • Fabiola Holetz
  • Patricia Shigunov
Chapter
First Online:

Abstract

Stem cells have the potential to both proliferate and self-renew. These extraordinary cells also have pluri- or multipotency rendering them the ability to differentiate into several tissue-specific lineages. These characteristics make these cells ideal candidates for use in cell therapy. However, it is essential for a successful therapy that these cells could be exclusively committed to the cell type that is needed. Commitment involves the activation of a particular genetic program and this process can be regulated at multiple levels during gene expression. An understanding of the gene regulatory networks involved in the committing of these cells to differentiation into a specific cell type is essential for the successful repair of injured tissue or even whole organogenesis.

Keywords

Translational Regulation Translational Control Posttranscriptional Regulation Ribosome Profile Upstream Open Reading Frame 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

Supported by Ministério da Saúde Brazil, Fundação Araucária, and FIOCRUZ. P.S. received fellowship from FIOCRUZ and B.D. from CNPq Brazil.

References

  1. Arava Y (2003) Isolation of polysomal RNA for microarray analysis. Methods Mol Biol 224:79–87PubMedGoogle Scholar
  2. Arava Y, Wang Y, Storey JD et al (2003) Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 100(7):3889–3894PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bates JG, Salzman J, May D et al (2012) Extensive gene-specific translational reprogramming in a model of B cell differentiation and Abl-dependent transformation. PLoS One 7(5):e37108CrossRefGoogle Scholar
  4. Blázquez-Domingo M, Grech G, von Lindern M (2005) Translation initiation factor 4E inhibits differentiation of erythroid progenitors. Mol Cell Biol 25(19):8496–8506PubMedCentralPubMedCrossRefGoogle Scholar
  5. Cheadle C, Fan J, Cho-Chung YS et al (2005) Stability regulation of mRNA and the control of gene expression. Ann N Y Acad Sci 1058:196–204PubMedCrossRefGoogle Scholar
  6. Cho J, Chang H, Kwon SC et al (2012) LIN28A is a suppressor of ER-associated translation in embryonic stem cells. Cell 151(4):765–777PubMedCrossRefGoogle Scholar
  7. Dana A, Tuller T (2012) Determinants of translation elongation speed and ribosomal profiling biases in mouse embryonic stem cells. PLoS Comput Biol 8(11):e1002755CrossRefGoogle Scholar
  8. de Jong M, van Breukelen B, Wittink FR et al (2006) Membrane-associated transcripts in Arabidopsis; their isolation and characterization by DNA microarray analysis and bioinformatics. Plant J 46(4):708–721PubMedCrossRefGoogle Scholar
  9. Dever TE, Green R (2012) The elongation, termination, and recycling phases of translation in eukaryotes. Cold Spring Harb Perspect Biol 4(7):a013706CrossRefGoogle Scholar
  10. Diehn M, Eisen MB, Botstein D et al (2000) Large-scale identification of secreted and membrane-associated gene products using DNA microarrays. Nat Genet 25(1):58–62PubMedCrossRefGoogle Scholar
  11. Diehn M, Bhattacharya R, Botstein D et al (2006) Genome-scale identification of membrane-associated human mRNAs. PLoS Genet 2(1):e11CrossRefGoogle Scholar
  12. dos Reis M, Savva R, Wernisch L (2004) Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res 32(17):5036–5044PubMedCentralPubMedCrossRefGoogle Scholar
  13. Fabian MR, Sonenberg N, Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351–379PubMedCrossRefGoogle Scholar
  14. Fromm-Dornieden C, von der Heyde S, Lytovchenko O et al (2012) Novel polysome messages and changes in translational activity appear after induction of adipogenesis in 3T3-L1 cells. BMC Mol Biol 13:19CrossRefGoogle Scholar
  15. Gebauer F, Preiss T, Hentze MW (2012) From cis-regulatory elements to complex RNPs and back. Cold Spring Harb Perspect Biol 4(7):a012245CrossRefGoogle Scholar
  16. Gkogkas CG, Sonenberg N (2013) Translational control and autism-like behaviors. Cell Logist 3(1):e24551Google Scholar
  17. Guttman M, Amit I, Garber M et al (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458(7235):223–227PubMedCentralPubMedCrossRefGoogle Scholar
  18. Guttman M, Garber M, Levin JZ et al (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28(5):503–510PubMedCentralPubMedCrossRefGoogle Scholar
  19. Guttman M, Russell P, Ingolia NT et al (2013) Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154(1):240–251PubMedCentralPubMedCrossRefGoogle Scholar
  20. Hashem Y, des Georges A, Dhote V et al (2013) Structure of the mammalian ribosomal 43S preinitiation complex bound to the scanning factor DHX29. Cell 153(5):1108–1119PubMedCentralPubMedCrossRefGoogle Scholar
  21. Haston KM, Tung JY, Reijo Pera RA (2009) 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 4(5):e5654CrossRefGoogle Scholar
  22. Hendrickson DG, Hogan DJ, McCullough HL et al (2009) Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNAs. PLoS Biol 7(11):e1000238CrossRefGoogle Scholar
  23. Hershey JW, Sonenberg N, Mathews MB (2012) Principles of translational control: an overview. Cold Spring Harb Perspect Biol 4(12):a011528CrossRefGoogle Scholar
  24. Holetz FB, Correa A, Avila AR et al (2007) Evidence of P-body-like structures in Trypanosoma cruzi. Biochem Biophys Res Commun 356(4):1062–1067PubMedCrossRefGoogle Scholar
  25. Hurt JA, Robertson AD, Burge CB (2013) Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res 23(10):1636–1650PubMedCentralPubMedCrossRefGoogle Scholar
  26. Ingolia NT (2014) Ribosome profiling: new views of translation, from single codons to genome scale. Nat Rev Genet 15(3):205–213PubMedCrossRefGoogle Scholar
  27. Ingolia NT, Ghaemmaghami S, Newman JR et al (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324(5924):218–223PubMedCentralPubMedCrossRefGoogle Scholar
  28. Ingolia NT, Lareau LF, Weissman JS (2011) Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147(4):789–802PubMedCentralPubMedCrossRefGoogle Scholar
  29. Ivanova NB, Dimos JT, Schaniel C et al (2002) A stem cell molecular signature. Science 298(5593):601–604PubMedCrossRefGoogle Scholar
  30. Jackson RJ, Hellen CU, Pestova TV (2012) Termination and post-termination events in eukaryotic translation. Adv Protein Chem Struct Biol 86:45–93PubMedCrossRefGoogle Scholar
  31. Jeong JA, Ko KM, Bae S et al (2007) Genome-wide differential gene expression profiling of human bone marrow stromal cells. Stem Cells 25(4):994–1002PubMedCrossRefGoogle Scholar
  32. Ji Z, Lee JY, Pan Z et al (2009) Progressive lengthening of 3’ untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc Natl Acad Sci U S A 106(17):7028–7033PubMedCentralPubMedCrossRefGoogle Scholar
  33. Kolle G, Ho M, Zhou Q et al (2009) Identification of human embryonic stem cell surface markers by combined membrane-polysome translation state array analysis and immunotranscriptional profiling. Stem Cells 27(10):2446–2456PubMedCrossRefGoogle Scholar
  34. Kolle G, Shepherd JL, Gardiner B et al (2011) Deep-transcriptome and ribonome sequencing redefines the molecular networks of pluripotency and the extracellular space in human embryonic stem cells. Genome Res 21(12):2014–2025PubMedCentralPubMedCrossRefGoogle Scholar
  35. Larsson O, Tian B, Sonenberg N (2013) Toward a genome-wide landscape of translational control. Cold Spring Harb Perspect Biol 5(1):a012302CrossRefGoogle Scholar
  36. Livingstone M, Atas E, Meller A et al (2010) Mechanisms governing the control of mRNA translation. Phys Biol 7(2):021001PubMedCrossRefGoogle Scholar
  37. Lu J, Deutsch C (2008) Electrostatics in the ribosomal tunnel modulate chain elongation rates. J Mol Biol 384(1):73–86PubMedCentralPubMedCrossRefGoogle Scholar
  38. MacDougald OA, Lane MD (1995) Transcriptional regulation of gene expression during adipocyte differentiation. Annu Rev Biochem 64:345–373PubMedCrossRefGoogle Scholar
  39. Menssen A, Haupl T, Sittinger M et al (2011) Differential gene expression profiling of human bone marrow-derived mesenchymal stem cells during adipogenic development. BMC Genomics 12:461PubMedCentralPubMedCrossRefGoogle Scholar
  40. Parent R, Beretta L (2008) Translational control plays a prominent role in the hepatocytic differentiation of HepaRG liver progenitor cells. Genome Biol 9(1):R19CrossRefGoogle Scholar
  41. Preiss T, Baron-Benhamou J, Ansorge W et al (2003) Homodirectional changes in transcriptome composition and mRNA translation induced by rapamycin and heat shock. Nat Struct Biol 10(12):1039–1047PubMedCrossRefGoogle Scholar
  42. Sampath P, Pritchard DK, Pabon L et al (2008) A hierarchical network controls protein translation during murine embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2(5):448–460PubMedCrossRefGoogle Scholar
  43. Sandberg R, Neilson JR, Sarma A et al (2008) Proliferating cells express mRNAs with shortened 3’ untranslated regions and fewer microRNA target sites. Science 320(5883):1643–1647PubMedCentralPubMedCrossRefGoogle Scholar
  44. Schwanhäusser B, Busse D, Li N et al (2011) Global quantification of mammalian gene expression control. Nature 473(7347):337–342PubMedCrossRefGoogle Scholar
  45. Slavoff SA, Mitchell AJ, Schwaid AG et al (2013) Peptidomic discovery of short open reading frame-encoded peptides in human cells. Nat Chem Biol 9(1):59–64PubMedCentralPubMedCrossRefGoogle Scholar
  46. Sobala A, Hutvagner G (2013) Small RNAs derived from the 5’ end of tRNA can inhibit protein translation in human cells. RNA Biol 10(4):553–563PubMedCentralPubMedCrossRefGoogle Scholar
  47. Sonenberg N, Hershey JWB, Matheus MB (2000) Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.Google Scholar
  48. Song L, Webb NE, Song Y et al (2006) Identification and functional analysis of candidate genes regulating mesenchymal stem cell self-renewal and multipotency. Stem Cells 24(7):1707–1718PubMedCrossRefGoogle Scholar
  49. Spangenberg L, Correa A, Dallagiovanna B et al (2013a) Role of alternative polyadenylation during adipogenic differentiation: an in silico approach. PLoS One 8(10):e75578Google Scholar
  50. Spangenberg L, Shigunov P, Abud AP et al (2013b) Polysome profiling shows extensive posttranscriptional regulation during human adipocyte stem cell differentiation into adipocytes. Stem Cell Res 11(2):902–912Google Scholar
  51. Stitziel NO, Mar BG, Liang J et al (2004) Membrane-associated and secreted genes in breast cancer. Cancer Res 64(23):8682–8687PubMedCrossRefGoogle Scholar
  52. Szostak E, Gebauer F (2013) Translational control by 3’-UTR-binding proteins. Brief Funct Genomics 12(1):58–65PubMedCentralPubMedCrossRefGoogle Scholar
  53. Tebaldi T, Re A, Viero G et al (2012) Widespread uncoupling between transcriptome and translatome variations after a stimulus in mammalian cells. BMC Genomics 13:220PubMedCentralPubMedCrossRefGoogle Scholar
  54. Tuller T, Veksler-Lublinsky I, Gazit N et al (2011) Composite effects of gene determinants on the translation speed and density of ribosomes. Genome Biol 12(11):R110CrossRefGoogle Scholar
  55. Unwin RD, Smith DL, Blinco D et al (2006) Quantitative proteomics reveals posttranslational control as a regulatory factor in primary hematopoietic stem cells. Blood 107(12):4687–4694PubMedCrossRefGoogle Scholar
  56. Wells SE, Hillner PE, Vale RD et al (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2(1):135–140PubMedCrossRefGoogle Scholar
  57. Williamson AJ, Smith DL, Blinco D et al (2008) Quantitative proteomics analysis demonstrates post-transcriptional regulation of embryonic stem cell differentiation to hematopoiesis. Mol Cell Proteomics 7(3):459–472PubMedCrossRefGoogle Scholar
  58. Zaretsky JZ, Wreschner DH (2008) Protein multifunctionality: principles and mechanisms. Transl Oncogenomics 3:99–136PubMedCentralPubMedGoogle Scholar
  59. Zong Q, Schummer M, Hood L et al (1999) Messenger RNA translation state: the second dimension of high-throughput expression screening. Proc Natl Acad Sci U S A 96(19):10632–10636PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Bruno Dallagiovanna
    • 1
  • Fabiola Holetz
    • 1
  • Patricia Shigunov
    • 1
  1. 1.Instituto Carlos ChagasFIOCRUZ ParanáCuritibaBrazil

Personalised recommendations