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PMID: 9482869 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

A poly(A) binding protein functions in the chloroplast as a message-specific translation factor.

Yohn CB, Cohen A, Danon A, Mayfield SP

Abstract

High-affinity binding of a set of proteins with specificity for the 5' untranslated region (UTR) of the Chlamydomonas reinhardtii chloroplast psbA mRNA correlates with light-regulated translational activation of this message. We have isolated a cDNA encoding the main psbA RNA binding protein, RB47, and identified this protein as a member of the poly(A) binding protein family. Poly(A) binding proteins are a family of eukaryotic, cytoplasmic proteins thought to bind poly(A) tails of mRNAs and play a role in translational regulation. In vitro translation of RNA transcribed from the RB47 cDNA produces a precursor protein that is efficiently transported into the chloroplast and processed to the mature 47-kDa protein. RB47 expressed and purified from Escherichia coli binds to the psbA 5' UTR with similar specificity and affinity as RB47 isolated from C. reinhardtii chloroplasts. The identification of a normally cytoplasmic translation factor in the chloroplast suggests that the prokaryotic-like chloroplast translation machinery utilizes a eukaryotic-like initiation factor to regulate the translation of a key chloroplast mRNA. These data also suggest that poly(A) binding proteins may play a wider role in translation regulation than previously appreciated.

MeSH Terms
Amino Acid Sequence Animals Binding Sites Chlamydomonas reinhardtii/metabolism Chloroplasts/metabolism Cloning, Molecular Conserved Sequence Molecular Sequence Data Photosynthetic Reaction Center Complex Proteins/biosynthesis,genetics Photosystem II Protein Complex Poly(A)-Binding Proteins Protein Biosynthesis RNA, Messenger/metabolism RNA-Binding Proteins/biosynthesis,chemistry,metabolism Receptors, Cytoplasmic and Nuclear/metabolism Recombinant Proteins/biosynthesis,chemistry,metabolism Sequence Alignment Sequence Homology, Amino Acid Transcription, Genetic
Chemicals
Photosynthetic Reaction Center Complex Proteins Photosystem II Protein Complex Poly(A)-Binding Proteins RNA, Messenger RNA-Binding Proteins Receptors, Cytoplasmic and Nuclear Recombinant Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Yohn C B
Department of Cell Biology and The Skaggs Institute of Chemical Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA.
Cohen A
Danon A
Mayfield S P
References (47)
47 references, click to expand
  1. Translational control of poly(A)-binding protein expression.
    Eur J Biochem. 1996 Apr 1;237(1):143-52 PMID: 8620866
  2. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability.
    Mol Cell Biol. 1987 Sep;7(9):3268-76 PMID: 3313012
  3. RNA-binding proteins as developmental regulators.
    Genes Dev. 1989 Apr;3(4):431-7 PMID: 2470643
  4. Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii.
    EMBO J. 1989 Apr;8(4):1013-21 PMID: 2663467
  5. Expression of the poly(A)-binding protein during development of Xenopus laevis.
    Mol Cell Biol. 1989 Jun;9(6):2756-60 PMID: 2761544
  6. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation.
    Cell. 1989 Sep 8;58(5):857-67 PMID: 2673535
  7. Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II.
    Cell. 1989 Sep 8;58(5):869-76 PMID: 2673536
  8. Control of prokaryotic translational initiation by mRNA secondary structure.
    Prog Nucleic Acid Res Mol Biol. 1990;38:1-35 PMID: 2183291
  9. Evidence for allosteric coupling between the ribosome and repressor binding sites of a translationally regulated mRNA.
    Biochemistry. 1990 May 8;29(18):4434-9 PMID: 2112408
  10. Use of T7 RNA polymerase to direct expression of cloned genes.
    Methods Enzymol. 1990;185:60-89 PMID: 2199796
  11. The Xenopus laevis poly(A) binding protein is composed of multiple functionally independent RNA binding domains.
    EMBO J. 1990 Nov;9(11):3699-705 PMID: 2209558
  12. Translational stimulation: RNA sequence and structure requirements for binding of Com protein.
    Cell. 1991 Apr 19;65(2):259-69 PMID: 1826635
  13. RNA recognition: towards identifying determinants of specificity.
    Trends Biochem Sci. 1991 Jun;16(6):214-20 PMID: 1716386
  14. Chloroplast protein topogenesis: import, sorting and assembly.
    Biochim Biophys Acta. 1991 Nov 13;1071(3):221-53 PMID: 1958688
  15. Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins.
    EMBO J. 1991 Dec;10(13):3993-4001 PMID: 1721866
  16. A nuclear mutation affects the synthesis of the chloroplast psbA gene production Chlamydomonas reinhardtii.
    Curr Genet. 1992 Jul;22(1):47-52 PMID: 1377098
  17. Post-transcriptional steps in the expression of chloroplast genes.
    Annu Rev Cell Biol. 1992;8:1-28 PMID: 1282351
  18. Regulation of translation in eukaryotic systems.
    Annu Rev Cell Biol. 1992;8:197-225 PMID: 1335743
  19. Accumulation of D1 polypeptide in tobacco plastids is regulated via the untranslated region of the psbA mRNA.
    EMBO J. 1993 Feb;12(2):601-6 PMID: 8440249
  20. Gene phylogenies and the endosymbiotic origin of plastids.
    Biosystems. 1992;28(1-3):75-90 PMID: 1292669
  21. Drosophila melanogaster poly(A)-binding protein: cDNA cloning reveals an unusually long 3'-untranslated region of the mRNA, also present in other eukaryotic species.
    Gene. 1993 Apr 30;126(2):295-6 PMID: 8482550
  22. Differential organ-specific expression of three poly(A)-binding-protein genes from Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6686-90 PMID: 8341686
  23. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity.
    Exp Cell Res. 1994 Apr;211(2):400-7 PMID: 7908267
  24. ADP-dependent phosphorylation regulates RNA-binding in vitro: implications in light-modulated translation.
    EMBO J. 1994 May 1;13(9):2227-35 PMID: 8187775
  25. Molecular characterization of PAB2, a member of the multigene family coding for poly(A)-binding proteins in Arabidopsis thaliana.
    Plant Physiol. 1993 Oct;103(2):525-33 PMID: 8029336
  26. The 5' leader of a chloroplast mRNA mediates the translational requirements for two nucleus-encoded functions in Chlamydomonas reinhardtii.
    Mol Cell Biol. 1994 Aug;14(8):5268-77 PMID: 8035805
  27. A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms.
    EMBO J. 1994 Jul 1;13(13):3170-81 PMID: 8039510
  28. Vir-115 gene product is required to stabilize D1 translation intermediates in chloroplasts.
    Plant Mol Biol. 1994 Jun;25(3):459-67 PMID: 7914100
  29. Light-regulated translation of chloroplast messenger RNAs through redox potential.
    Science. 1994 Dec 9;266(5191):1717-9 PMID: 7992056
  30. Translation of the psbA mRNA of Chlamydomonas reinhardtii requires a structured RNA element contained within the 5' untranslated region.
    J Cell Biol. 1994 Dec;127(6 Pt 1):1537-45 PMID: 7798310
  31. Chloroplast ribosomes and protein synthesis.
    Microbiol Rev. 1994 Dec;58(4):700-54 PMID: 7854253
  32. Translational regulation of gene expression in chloroplasts and mitochondria.
    Annu Rev Genet. 1994;28:71-93 PMID: 7893142
  33. Autoregulation of poly(A)-binding protein synthesis in vitro.
    Nucleic Acids Res. 1995 Jun 25;23(12):2198-205 PMID: 7610048
  34. Xenopus poly(A) binding protein: functional domains in RNA binding and protein-protein interaction.
    J Mol Biol. 1996 Feb 16;256(1):20-30 PMID: 8609610
  35. Protein disulfide isomerase as a regulator of chloroplast translational activation.
    Science. 1997 Dec 12;278(5345):1954-7 PMID: 9395399
  36. Ribosomal association of poly(A)-binding protein in poly(A)-deficient Saccharomyces cerevisiae.
    J Biol Chem. 1996 May 3;271(18):10859-65 PMID: 8631901
  37. Altered mRNA binding activity and decreased translational initiation in a nuclear mutant lacking translation of the chloroplast psbA mRNA.
    Mol Cell Biol. 1996 Jul;16(7):3560-6 PMID: 8668172
  38. The role of proteolysis in cell cycle progression in Schizosaccharomyces pombe.
    EMBO J. 1996 Oct 1;15(19):5268-79 PMID: 8895572
  39. Addition of destabilizing poly (A)-rich sequences to endonuclease cleavage sites during the degradation of chloroplast mRNA.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13398-403 PMID: 8917603
  40. Polyadenylation accelerates degradation of chloroplast mRNA.
    EMBO J. 1996 Dec 16;15(24):7137-46 PMID: 9003789
  41. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G.
    EMBO J. 1996 Dec 16;15(24):7168-77 PMID: 9003792
  42. Precursors to two nuclear-encoded chloroplast proteins bind to the outer envelope membrane before being imported into chloroplasts.
    J Biol Chem. 1985 Mar 25;260(6):3691-6 PMID: 3882712
  43. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression.
    Cell. 1986 Jun 20;45(6):827-35 PMID: 3518950
  44. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence.
    Mol Cell Biol. 1986 Aug;6(8):2932-43 PMID: 3537727
  45. Synthesis of the small subunit of ribulose-bisphosphate carboxylase from genes cloned into plasmids containing the SP6 promoter.
    Biochem J. 1986 Dec 15;240(3):709-15 PMID: 3827863
  46. Human mRNA polyadenylate binding protein: evolutionary conservation of a nucleic acid binding motif.
    Nucleic Acids Res. 1987 Jun 25;15(12):4771-87 PMID: 2885805
  47. Bacteriophage T4 regA protein binds to mRNAs and prevents translation initiation.
    Proc Natl Acad Sci U S A. 1987 Nov;84(22):7822-6 PMID: 3120177
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1998-03-03
Pages
2238-43
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC19305
Subset
IM
Grants
NIGMS NIH HHS · F32 GM015639 · United States
NIGMS NIH HHS · GM15639-03 · United States
Databases
GENBANK
AF043297
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