Skip to main content
SpringerLink
Log in

Construction, Structure and Dynamics of Post-Transcriptional Regulatory Network Directed by RNA-Binding Proteins

  • Chapter
RNA Infrastructure and Networks

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 722))

Abstract

Gene expression is a highly controlled process which is known to occur at several levels in eukaryotic organisms. Although messenger RNAs have been traditionally viewed as passive molecules in the pathway from transcription to translation, there is increasing evidence that their metabolism is controlled by a class of proteins called RNA-binding proteins (RBPs). In this chapter, we provide an overview of the recent developments in our understanding of the repertoire of RBPs across diverse model systems and discuss the approaches currently available for the construction of post-transcriptional networks governed by them. We also present the first analysis of the network properties of a post-transcriptional system in a model eukaryote using currently available data and discuss the implications of understanding the dynamic properties of this important class of regulatory molecules as more data detailing their dynamic, spatial and tissue-specific maps across diverse model systems accumulates. We argue that such developments would not only allow us to gain a deeper understanding of regulation at a level that has been under-appreciated over the past decades, but would also allow us to use the newly developed high-throughput approaches to interrogate the prevalence of these phenomena in different states and thereby study their relevance to physiology and disease across organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Martinez-Antonio A, Janga SC, Salgado H et al. Internal-sensing machinery directs the activity of the regulatory network in Escherichia coli. Trends Microbiol 2006; 14(1):22–27.

    Article  PubMed  CAS  Google Scholar 

  2. Babu MM, Janga SC, de Santiago I et al. Eukaryotic gene regulation in three dimensions and its impact on genome evolution. Curr Opin Genet Dev 2008; 18(6):571–582.

    Article  PubMed  CAS  Google Scholar 

  3. Janga SC, Collado-Vides J. Structure and evolution of gene regulatory networks in microbial genomes. Res Microbiol 2007; 158(10):787–794.

    Article  PubMed  CAS  Google Scholar 

  4. Babu MM, Luscombe NM, Aravind L et al. Structure and evolution of transcriptional regulatory networks. Curr Opin Struct Biol 2004; 14(3):283–291.

    Article  PubMed  CAS  Google Scholar 

  5. Ideker T, Thorsson V, Ranish JA et al. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 2001; 292(5518):929–934.

    Article  PubMed  CAS  Google Scholar 

  6. Greenbaum D, Colangelo C, Williams K et al. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 2003; 4(9): 117.

    Article  PubMed  Google Scholar 

  7. Gygi SP, Rochon Y, Franza BR et al. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999; 19(3): 1720–1730.

    PubMed  CAS  Google Scholar 

  8. Glisovic T, Bachorik JL, Yong J et al. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett 2008; 582(14):1977–1986.

    Article  PubMed  CAS  Google Scholar 

  9. Mata J, Marguerat S, Bahler J. Post-Transcriptional control of gene expression: a genome-wide perspective. Trends Biochem Sci 2005; 30(9):506–514.

    Article  PubMed  CAS  Google Scholar 

  10. Keene JD. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 2007; 8(7): 533–543.

    Article  PubMed  CAS  Google Scholar 

  11. Collins LJ, Penny D. The RNA infrastructure: dark matter of the eukaryotic cell? Trends Genet 2009; 25(3):120–128.

    Article  PubMed  CAS  Google Scholar 

  12. Sanford JR, Gray NK, Beckmann K et al. A novel role for shuttling SR proteins in mRNA translation. Genes Dev 2004; 18(7):755–768.

    Article  PubMed  CAS  Google Scholar 

  13. Zhong XY, Wang P, Han J et al. SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol Cell 2009; 35(1):1–10.

    Article  PubMed  CAS  Google Scholar 

  14. Gross T, Richert K, Mierke C et al. Identification and characterization of srp1, a gene of fission yeast encoding a RNA binding domain and a RS domain typical of SR splicing factors. Nucleic Acids Res 1998; 26(2):505–511.

    Article  PubMed  CAS  Google Scholar 

  15. Pascale A, Amadio M, Quattrone A. Defining a neuron: neuronal ELAV proteins. Cell Mol Life Sci 2008; 65(1):128–140.

    Article  PubMed  CAS  Google Scholar 

  16. Ule J, Jensen KB, Ruggiu M et al. CLIP identifies Nova-regulated RNA networks in the brain. Science 2003; 302(5648):1212–1215.

    Article  PubMed  CAS  Google Scholar 

  17. Ule J, Stefani G, Mele A et al. An RNA map predicting Nova-dependent splicing regulation. Nature 2006; 444(7119):580–586.

    Article  PubMed  CAS  Google Scholar 

  18. Gruter P, Tabernero C, von Kobbe C et al. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell 1998; 1(5):649–659.

    Article  PubMed  CAS  Google Scholar 

  19. Hogan DJ, Riordan DP, Gerber AP et al. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol 2008; 6(10):e255.

    Article  PubMed  Google Scholar 

  20. Maris C, Dominguez C, Allain FH. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 2005; 272(9):2118–2131.

    Article  PubMed  CAS  Google Scholar 

  21. Ciesla J. Metabolic enzymes that bind RNA: yet another level of cellular regulatory network? Acta Biochim Pol 2006; 53(1): 11–32.

    PubMed  CAS  Google Scholar 

  22. Hu S, Xie Z, Onishi A et al. Profiling the human protein-DNA interactome reveals ERK2 as atranscriptional repressor of interferon signaling. Cell 2009; 139(3):610–622.

    Article  PubMed  CAS  Google Scholar 

  23. Pinero DJ, Hu J, Connor JR. Alterations in the interaction between iron regulatory proteins and their iron responsive element in normal and Alzheimer’s diseased brains. Cell Mol Biol (Noisy-le-grand) 2000; 46(4):761–776.

    CAS  Google Scholar 

  24. Thomson AM, Rogers JT, Walker CE et al. Optimized RNA gel-shift and UV cross-linking assays for characterization of cytoplasmic RNA-protein interactions. Biotechniques 1999; 27(5): 1032–1039, 1042.

    PubMed  Google Scholar 

  25. Wilhelm JE, Vale RD. A one-hybrid system for detecting RNA-protein interactions. Genes Cells 1996; 1(3):317–323.

    Article  PubMed  CAS  Google Scholar 

  26. SenGupta DJ, Zhang B, Kraemer B et al. A three-hybrid system to detect RNA-protein interactions in vivo. Proc Natl Acad Sci USA 1996; 93(16):8496–8501.

    Article  PubMed  CAS  Google Scholar 

  27. Gerber AP, Herschlag D, Brown PO. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol 2004; 2(3):E79.

    Article  PubMed  Google Scholar 

  28. Hieronymus H, Silver PA. Genome-wide analysis of RNA-protein interactions illustrates specificity of the mRNA export machinery. Nat Genet 2003; 33(2):155–161.

    Article  PubMed  CAS  Google Scholar 

  29. Galante PA, Sandhu D, de Sousa Abreu R et al. A comprehensive in silico expression analysis of RNA binding proteins in normal and tumor tissue: Identification of potential players in tumor formation. RNA Biol 2009; 6(4):426–433.

    Article  PubMed  CAS  Google Scholar 

  30. Hall DA, Zhu H, Zhu X et al. Regulation of gene expression by a metabolic enzyme. Science 2004; 306(5695):482–484.

    Article  PubMed  CAS  Google Scholar 

  31. Fasolo J, Snyder M. Protein microarrays. Methods Mol Biol 2009; 548:209–222.

    Article  PubMed  CAS  Google Scholar 

  32. Zhu H, Bilgin M, Bangham R et al. Global analysis of protein activities using proteome chips. Science 2001; 293(5537):2101–2105.

    Article  PubMed  CAS  Google Scholar 

  33. Zeng F, Peritz T, Kannanayakal TJ et al. A protocol for PAIR: PNA-assisted identification of RNA binding proteins in living cells. Nat Protoc 2006; 1(2):920–927.

    Article  PubMed  CAS  Google Scholar 

  34. Zielinski J, Kilk K, Peritz T et al. In vivo identification of ribonucleoprotein-RNA interactions. Proc Natl Acad Sci USA 2006; 103(5):1557–1562.

    Article  PubMed  CAS  Google Scholar 

  35. Ho AM, Johnson MD, Kingsley DM. Role of the mouse ank gene in control of tissue calcification and arthritis. Science 2000; 289(5477):265–270.

    Article  PubMed  CAS  Google Scholar 

  36. Eberwine J, Belt B, Kacharmina JE et al. Analysis of subcellularly localized mRNAs using in situ hybridization, mRNA amplification and expression profiling. Neurochem Res 2002; 27(10): 1065–1077.

    Article  PubMed  CAS  Google Scholar 

  37. Keene JD, Tenenbaum SA. Eukaryotic mRNPs may represent post-transcriptional operons. Mol Cell 2002; 9(6):1161–1167.

    Article  PubMed  CAS  Google Scholar 

  38. Townley-Tilson WH, Pendergrass SA, Marzluff WF et al. Genome-wide analysis of mRNAs bound to the histone stem-loop binding protein. RNA 2006; 12(10):1853–1867.

    Article  PubMed  CAS  Google Scholar 

  39. Keene JD, Lager PJ. Post-Transcriptional operons and regulons co-ordinating gene expression. Chromosome Res 2005; 13(3):327–337.

    Article  PubMed  CAS  Google Scholar 

  40. Pullmann R, Jr., Kim HH, Abdelmohsen K et al. Analysis of turnover and translation regulatory RNA-binding protein expression through binding to cognate mRNAs. Mol Cell Biol 2007; 27(18):6265–6278.

    Article  PubMed  CAS  Google Scholar 

  41. Junker BH, Koschutzki D, Schreiber F. Exploration of biological network centralities with CentiBiN. BMC Bioinformatics 2006; 7:219.

    Article  PubMed  Google Scholar 

  42. Barabasi AL, Oltvai ZN. Network biology: understanding the cell’s functional organization. Nat Rev Genet 2004; 5(2):101–113.

    Article  PubMed  CAS  Google Scholar 

  43. Lukong KE, Chang KW, Khandjian EW et al. RNA-binding proteins in human genetic disease. Trends Genet 2008; 24(8):416–425.

    Article  PubMed  CAS  Google Scholar 

  44. Cooper TA, Wan L, Dreyfuss G. RNA and disease. Cell 2009; 136(4):777–793.

    Article  PubMed  CAS  Google Scholar 

  45. Musunuru K. Cell-specific RNA-binding proteins in human disease. Trends Cardiovasc Med 2003; 13(5):188–195.

    Article  PubMed  CAS  Google Scholar 

  46. Kim MY, Hur J, Jeong S. Emerging roles of RNA and RNA-binding protein network in cancer cells. BMB Rep 2009; 42(3):125–130.

    Article  PubMed  CAS  Google Scholar 

  47. Alberti S, Halfmann R, King O et al. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 2009; 137(1):146–158.

    Article  PubMed  CAS  Google Scholar 

  48. Mittal N, Roy N, Babu MM et al. Dissecting the expression dynamics of RNA-binding proteins in post-transcriptional regulatory networks. Proc Natl Acad Sci USA 2009; 106(48):20300–20305.

    Article  PubMed  CAS  Google Scholar 

  49. Anantharaman V, Koonin EV, Aravind L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res 2002; 30(7):1427–1464.

    Article  PubMed  CAS  Google Scholar 

  50. Paulsson J. Summing up the noise in gene networks. Nature 2004; 427(6973):415–418.

    Article  PubMed  CAS  Google Scholar 

  51. Schullery DS, Ostrowski J, Denisenko ON et al. Regulated interaction of protein kinase Cdelta with the heterogeneous nuclear ribonucleoprotein K protein. J Biol Chem 1999; 274(21):15101–15109.

    Article  PubMed  CAS  Google Scholar 

  52. Vassileva MT, Matunis MJ. SUMO modification of heterogeneous nuclear ribonucleoproteins. Mol Cell Biol 2004; 24(9):3623–3632.

    Article  PubMed  CAS  Google Scholar 

  53. Yu MC, Bachand F, McBride AE et al. Arginine methyltransferase affects interactions and recruitment of mRNA processing and export factors. Genes Dev 2004; 18(16):2024–2035.

    Article  PubMed  CAS  Google Scholar 

  54. Halbeisen RE, Galgano A, Scherrer T et al. Post-transcriptional gene regulation: from genome-wide studies to principles. Cell Mol Life Sci 2008; 65(5):798–813.

    Article  PubMed  CAS  Google Scholar 

  55. Lackner DH, Beilharz TH, Marguerat S et al. A network of multiple regulatory layers shapes gene expression in fission yeast. Mol Cell 2007; 26(1):145–155.

    Article  PubMed  CAS  Google Scholar 

  56. Hieronymus H, Silver PA. A systems view of mRNP biology. Genes Dev 2004; 18(23):2845–2860.

    Article  PubMed  CAS  Google Scholar 

  57. Wang Y, Liu CL, Storey JD et al. Precision and functional specificity in mRNA decay. Proc Natl Acad Sci USA 2002; 99(9):5860–5865.

    Article  PubMed  CAS  Google Scholar 

  58. Arava Y, Wang Y, Storey JD et al. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2003; 100(7):3889–3894.

    Article  PubMed  CAS  Google Scholar 

  59. Belle A, Tanay A, Bitincka L et al. Quantification of protein half-lives in the budding yeast proteome. Proc Natl Acad Sci USA 2006; 103(35):13004–13009.

    Article  PubMed  CAS  Google Scholar 

  60. Ghaemmaghami S, Huh WK, Bower K et al. Global analysis of protein expression in yeast. Nature 2003; 425(6959):737–741.

    Article  PubMed  CAS  Google Scholar 

  61. Newman JR, Ghaemmaghami S, Ihmels J et al. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 2006; 441(7095):840–846.

    Article  PubMed  CAS  Google Scholar 

  62. Finn RD, Mistry J, Tate J et al. The Pfam protein families database. Nucleic Acids Res 38(Database issue):D211–222.

    Google Scholar 

  63. Lee MH, Schedl T. RNA-binding proteins. WormBook 2006:1–13.

    Google Scholar 

  64. Lasko P. The drosophila melanogaster genome: translation factors and RNA binding proteins. J Cell Biol 2000; 150(2):F51–56.

    Article  PubMed  CAS  Google Scholar 

  65. McKee AE, Minet E, Stern C et al. A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain. BMC Dev Biol 2005; 5:14.

    Article  PubMed  Google Scholar 

  66. Sanchez-Diaz P, Penalva LO. Post-Transcription meets postgenomic: the saga of RNA binding proteins in a new era. RNA Biol 2006; 3(3):101–109.

    Article  PubMed  CAS  Google Scholar 

  67. Ray D, Kazan H, Chan ET et al. Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat Biotechnol 2009; 27(7):667–670.

    Article  PubMed  CAS  Google Scholar 

  68. Tenenbaum SA, Carson CC, Lager PJ et al. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc Natl Acad Sci USA 2000; 97(26):14085–14090.

    Article  PubMed  CAS  Google Scholar 

  69. Stelzl U, Nierhaus KH. SERF: in vitro election of random RNA fragments to identify protein binding sites within large RNAs. Methods 2001; 25(3):351–357.

    Article  PubMed  CAS  Google Scholar 

  70. Paraskeva E, Atzberger A, Hentze MW. A translational repression assay procedure (TRAP) for RNA-protein interactions in vivo. Proc Natl Acad Sci USA 1998; 95(3):951–956.

    Article  PubMed  CAS  Google Scholar 

  71. Rodgers ND, Jiao X, Kiledjian M. Identifying mRNAs bound by RNA-binding proteins using affinity purification and differential display. Methods 2002; 26(2):115–122.

    Article  PubMed  CAS  Google Scholar 

  72. Butter F, Scheibe M, Morl M et al. Unbiased RNA-protein interaction screen by quantitative proteomics. Proc Natl Acad Sci USA 2009; 106(26):10626–10631.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. MRC Laboratory of Molecular Biology, Cambridge, UK

    Sarath Chandra Janga

  2. Department of Biotechnology, National Institute of Pharmaceutical Education and Research, SAS Nagar, Punjab, India

    Nitish Mittal

  3. Institute of Genomic Biology, University of Illiniois at Urbana Champaign, Urbana, IL, USA

    Sarath Chandra Janga

Authors
  1. Sarath Chandra Janga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nitish Mittal
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand

    Lesley J. Collins

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Landes Bioscience and Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Janga, S.C., Mittal, N. (2011). Construction, Structure and Dynamics of Post-Transcriptional Regulatory Network Directed by RNA-Binding Proteins. In: Collins, L.J. (eds) RNA Infrastructure and Networks. Advances in Experimental Medicine and Biology, vol 722. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0332-6_7

Download citation

Publish with us

Policies and ethics

Search

Navigation