Home LiteratureArticle Details
PMID: 18922466 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

A solution to limited genomic capacity: using adaptable binding surfaces to assemble the functional HIV Rev oligomer on RNA.

Molecular cell ·Vol. 31 ·No. 6 ·2008-09-26 ·Pages 824-34

Daugherty MD, D'Orso I, Frankel AD

Abstract

Many ribonucleoprotein (RNP) complexes assemble into large, organized structures in which protein subunits are positioned by interactions with RNA and other proteins. Here we demonstrate that HIV Rev, constrained in size by a limited viral genome, also forms an organized RNP by assembling a homo-oligomer on the Rev response element (RRE) RNA. Rev subunits bind cooperatively to discrete RNA sites using an oligomerization domain and an adaptable protein-RNA interface, forming a complex with 500-fold higher affinity than the tightest single interaction. High-affinity binding correlates strongly with RNA export activity. Rev utilizes different surfaces of its alpha-helical RNA-binding domain to recognize several low-affinity binding sites, including the well-characterized stem IIB site and an additional site in stem IA. We propose that adaptable RNA-binding surfaces allow the Rev oligomer to assemble economically into a discrete, stable RNP and provide a mechanistic role for Rev oligomerization during the HIV life cycle.

MeSH Terms
Base Sequence Binding Sites Genome, Viral/genetics HIV/genetics Models, Biological Molecular Sequence Data Mutation/genetics Nucleic Acid Conformation Peptides/metabolism Protein Binding Protein Structure, Quaternary RNA Transport RNA, Viral/chemistry,genetics,metabolism Response Elements/genetics rev Gene Products, Human Immunodeficiency Virus/chemistry,metabolism
Chemicals
Peptides RNA, Viral rev Gene Products, Human Immunodeficiency Virus
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Daugherty Matthew D
Chemistry and Chemical Biology Graduate Program, University of California, San Francisco, CA 94158, USA.
D'Orso Iván
Frankel Alan D
References (45)
45 references, click to expand
  1. RanGTP-regulated interactions of CRM1 with nucleoporins and a shuttling DEAD-box helicase.
    Mol Cell Biol. 1999 Sep;19(9):6276-85 PMID: 10454574
  2. RNA architecture dictates the conformations of a bound peptide.
    Chem Biol. 1999 Sep;6(9):657-69 PMID: 10467126
  3. Structural model for the cooperative assembly of HIV-1 Rev multimers on the RRE as deduced from analysis of assembly-defective mutants.
    Mol Cell. 2001 Mar;7(3):603-14 PMID: 11463385
  4. An RNA-binding chameleon.
    Mol Cell. 2000 Nov;6(5):1067-76 PMID: 11106746
  5. Probability-based protein secondary structure identification using combined NMR chemical-shift data.
    Protein Sci. 2002 Apr;11(4):852-61 PMID: 11910028
  6. Structure of the SRP19 RNA complex and implications for signal recognition particle assembly.
    Nature. 2002 Jun 13;417(6890):767-71 PMID: 12050674
  7. Modulation of DNA-binding domains for sequence-specific DNA recognition.
    Gene. 2003 Jan 30;304:1-12 PMID: 12568710
  8. Nuclear mRNA export: insights from virology.
    Trends Biochem Sci. 2003 Aug;28(8):419-24 PMID: 12932730
  9. Structural basis of a phototropin light switch.
    Science. 2003 Sep 12;301(5639):1541-4 PMID: 12970567
  10. Yeast telomerase RNA: a flexible scaffold for protein subunits.
    Proc Natl Acad Sci U S A. 2004 Jul 6;101(27):10024-9 PMID: 15226497
  11. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA.
    Nature. 1989 Mar 16;338(6212):254-7 PMID: 2784194
  12. Mutational analysis of the human immunodeficiency virus type 1 Rev transactivator: essential residues near the amino terminus.
    J Virol. 1990 Nov;64(11):5360-6 PMID: 2120472
  13. Structural analysis of the interaction between the human immunodeficiency virus Rev protein and the Rev response element.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):683-7 PMID: 1992459
  14. Minimal Rev-response element for type 1 human immunodeficiency virus.
    J Virol. 1991 Apr;65(4):2131-4 PMID: 2002556
  15. HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency.
    Cell. 1991 Apr 19;65(2):241-8 PMID: 2015625
  16. Characterization of HIV-1 REV protein: binding stoichiometry and minimal RNA substrate.
    Nucleic Acids Res. 1991 Apr 11;19(7):1577-83 PMID: 2027765
  17. Human immunodeficiency virus type 1 regulator of virion expression, rev, forms nucleoprotein filaments after binding to a purine-rich "bubble" located within the rev-responsive region of viral mRNAs.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7366-70 PMID: 1871141
  18. Identification of a high-affinity RNA-binding site for the human immunodeficiency virus type 1 Rev protein.
    Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):758-62 PMID: 1731351
  19. Recognition of the high affinity binding site in rev-response element RNA by the human immunodeficiency virus type-1 rev protein.
    Nucleic Acids Res. 1992 Dec 25;20(24):6465-72 PMID: 1282702
  20. RNA recognition by an isolated alpha helix.
    Cell. 1993 Jun 4;73(5):1031-40 PMID: 7684657
  21. The basic domain of Rev from human immunodeficiency virus type 1 specifically blocks the entry of U4/U6.U5 small nuclear ribonucleoprotein in spliceosome assembly.
    J Virol. 1993 Aug;67(8):4769-76 PMID: 8331728
  22. A molecular rheostat. Co-operative rev binding to stem I of the rev-response element modulates human immunodeficiency virus type-1 late gene expression.
    J Mol Biol. 1994 Aug 12;241(2):193-207 PMID: 8057359
  23. Costabilization of peptide and RNA structure in an HIV Rev peptide-RRE complex.
    Biochemistry. 1994 Dec 6;33(48):14579-85 PMID: 7981219
  24. Multiple RNA binding domains (RBDs) just don't add up.
    Nucleic Acids Res. 1995 Mar 11;23(5):725-8 PMID: 7535921
  25. Identification of a signal for rapid export of proteins from the nucleus.
    Cell. 1995 Aug 11;82(3):463-73 PMID: 7634336
  26. Flexible regions of RNA structure facilitate co-operative Rev assembly on the Rev-response element.
    J Mol Biol. 1996 May 24;258(5):763-77 PMID: 8637008
  27. Anti-peptide aptamers recognize amino acid sequence and bind a protein epitope.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7475-80 PMID: 8755498
  28. Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex.
    Science. 1996 Sep 13;273(5281):1547-51 PMID: 8703216
  29. A structural model for the HIV-1 Rev-RRE complex deduced from altered-specificity rev variants isolated by a rapid genetic strategy.
    Cell. 1996 Oct 4;87(1):115-25 PMID: 8858154
  30. A dynamic in vivo view of the HIV-I Rev-RRE interaction.
    J Mol Biol. 1997 Mar 14;266(5):950-62 PMID: 9086273
  31. The effect of viral regulatory protein expression on gene delivery by human immunodeficiency virus type 1 vectors produced in stable packaging cell lines.
    J Virol. 1997 Aug;71(8):5841-8 PMID: 9223473
  32. Multiple RRMs contribute to RNA binding specificity and affinity for polypyrimidine tract binding protein.
    Biochemistry. 1997 Sep 30;36(39):11881-90 PMID: 9305981
  33. CRM1 is an export receptor for leucine-rich nuclear export signals.
    Cell. 1997 Sep 19;90(6):1051-60 PMID: 9323133
  34. Retroviruses as model systems for the study of nuclear RNA export pathways.
    Virology. 1998 Sep 30;249(2):203-10 PMID: 9791012
  35. The HIV-1 Rev protein.
    Annu Rev Microbiol. 1998;52:491-532 PMID: 9891806
  36. Polyvalent Rev decoys act as artificial Rev-responsive elements.
    J Virol. 1999 May;73(5):4341-9 PMID: 10196332
  37. Protein structure and oligomerization are important for the formation of export-competent HIV-1 Rev-RRE complexes.
    Protein Sci. 2008 Mar;17(3):420-30 PMID: 18218716
  38. NMRPipe: a multidimensional spectral processing system based on UNIX pipes.
    J Biomol NMR. 1995 Nov;6(3):277-93 PMID: 8520220
  39. A pathway of sequential arginine-serine-rich domain-splicing signal interactions during mammalian spliceosome assembly.
    Mol Cell. 2004 Nov 5;16(3):363-73 PMID: 15525510
  40. HIV-1 Rev oligomerization is not obligatory in the presence of an extra basic domain.
    Retrovirology. 2005;2:39 PMID: 15949040
  41. A simple motif for protein recognition in DNA secondary structures.
    J Mol Biol. 2005 Sep 2;351(5):982-94 PMID: 16055152
  42. Arginine-rich motifs present multiple interfaces for specific binding by RNA.
    RNA. 2005 Dec;11(12):1848-57 PMID: 16314457
  43. RNA-binding proteins: modular design for efficient function.
    Nat Rev Mol Cell Biol. 2007 Jun;8(6):479-90 PMID: 17473849
  44. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution.
    Science. 2000 Aug 11;289(5481):905-20 PMID: 10937989
  45. Exchange of the basic domain of human immunodeficiency virus type 1 Rev for a polyarginine stretch expands the RNA binding specificity, and a minimal arginine cluster is required for optimal RRE RNA binding affinity, nuclear accumulation, and trans-activation.
    J Virol. 2001 Mar;75(6):2957-71 PMID: 11222721
Article Info
Journal
Molecular cell
Abbr.
Mol Cell
ISSN
1097-4164
Published
2008-09-26
Pages
824-34
Language
English
Region
United States
NLM ID
9802571
PMCID
PMC2651398
Subset
IM
Grants
NIGMS NIH HHS · P50 GM082250-01 · United States
NIGMS NIH HHS · P01 GM056531-060007 · United States
NIGMS NIH HHS · P01 GM056531 · United States
NIGMS NIH HHS · P50 GM082250 · United States
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · P50GM82250 · United States
NIGMS NIH HHS · P01GM56531 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com