Polynucleotide phosphorylase hinders mRNA degradation upon ribosomal protein S1 overexpression in Escherichia coli

被引:35
|
作者
Briani, Federica [1 ]
Curti, Serena [1 ]
Rossi, Francesca [1 ]
Carzaniga, Thomas [1 ]
Mauri, Pierluigi [2 ]
Deho, Gianni [1 ]
机构
[1] Univ Milan, Dipartimento Sci Biomol & Biotecnol, I-20133 Milan, Italy
[2] CNR, Ist Tecnol Biomed, I-20133 Milan, Italy
关键词
RNA degradation; translation regulation; ribosomal protein S1; PNPase;
D O I
10.1261/rna.1123908
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
The exoribonuclease polynucleotide phosphorylase (PNPase, encoded by pnp) is a major player in bacterial RNA decay. In Escherichia coli, PNPase expression is post-transcriptionally regulated at the level of mRNA stability. The primary transcript is very efficiently processed by the endonuclease RNase III at a specific site and the processed pnp mRNA is rapidly degraded in a PNPase-dependent manner. While investigating the PNPase autoregulation mechanism we found, by UV-cross-linking experiments, that the ribosomal protein S1 in crude extracts binds to the pnp-mRNA leader region. We assayed the potential role of S1 protein in pnp gene regulation by modulating S1 expression from depletion to overexpression. We found that S1 depletion led to a sharp decrease of the amount of pnp and other tested mRNAs, as detected by Northern blotting, whereas S1 overexpression caused a strong stabilization of pnp and the other transcripts. Surprisingly, mRNA stabilization depended on PNPase, as it was not observed in a pnp deletion strain. PNPase-dependent stabilization, however, was not detected by chemical decay assay of bulk mRNA. Overall, our data suggest that PNPase exonucleolytic activity may be modulated by the translation potential of the target mRNAs and that, upon ribosomal protein S1 overexpression, PNPase protects from degradation a set of full-length mRNAs. It thus appears that a single mRNA species may be differentially targeted to either decay or PNPase-dependent stabilization, thus preventing its depletion in conditions of fast turnover.
引用
收藏
页码:2417 / 2429
页数:13
相关论文
共 50 条
  • [21] Contribution of the second OB fold of ribosomal protein S1 from Escherichia coli to the recognition of TmRNA
    Okada, T
    Wower, WK
    Wower, J
    Zwieb, CW
    Kimura, M
    BIOSCIENCE BIOTECHNOLOGY AND BIOCHEMISTRY, 2004, 68 (11) : 2319 - 2325
  • [22] PROMOTER ACTIVITY AND TRANSCRIPT MAPPING IN THE REGULATORY REGION FOR GENES ENCODING RIBOSOMAL-PROTEIN S15 AND POLYNUCLEOTIDE PHOSPHORYLASE OF ESCHERICHIA-COLI
    EVANS, S
    DENNIS, PP
    GENE, 1985, 40 (01) : 15 - 22
  • [23] Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo
    Sorensen, MA
    Fricke, J
    Pedersen, S
    JOURNAL OF MOLECULAR BIOLOGY, 1998, 280 (04) : 561 - 569
  • [24] Binding and cross-linking of tmRNA to ribosomal protein S1, on and off the Escherichia coli ribosome
    Wower, IK
    Zwieb, CW
    Guven, SA
    Wower, J
    EMBO JOURNAL, 2000, 19 (23): : 6612 - 6621
  • [25] PRIMARY STRUCTURE OF ESCHERICHIA-COLI RIBOSOMAL-PROTEIN S1 AND OF ITS GENE RPSA
    SCHNIER, J
    KIMURA, M
    FOULAKI, K
    SUBRAMANIAN, AR
    ISONO, K
    WITTMANNLIEBOLD, B
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES, 1982, 79 (04): : 1008 - 1011
  • [26] DESTABILIZATION OF SECONDARY STRUCTURE OF RNA BY RIBOSOMAL-PROTEIN S1 FROM ESCHERICHIA-COLI
    SZER, W
    HERMOSO, JM
    BOUBLIK, M
    BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS, 1976, 70 (03) : 957 - 964
  • [27] Direct Interaction of the N-Terminal Domain of Ribosomal Protein S1 with Protein S2 in Escherichia coli
    Byrgazov, Konstantin
    Manoharadas, Salim
    Kaberdina, Anna C.
    Vesper, Oliver
    Moll, Isabella
    PLOS ONE, 2012, 7 (03):
  • [28] S1 ribosomal protein and the interplay between translation and mRNA decay
    Delvillani, Francesco
    Papiani, Giulia
    Deho, Gianni
    Briani, Federica
    NUCLEIC ACIDS RESEARCH, 2011, 39 (17) : 7702 - 7715
  • [29] Nucleic acid and protein factors involved in Escherichia coli polynucleotide phosphorylase function on RNA
    Fernandez-Ramirez, Fernando
    Bermudez-Cruz, Rosa M.
    Montanez, Cecilia
    BIOCHIMIE, 2010, 92 (05) : 445 - 454
  • [30] Polynucleotide phosphorylase is required for the rapid degradation of the RNase E-processed rpsO mRNA of Escherichia coli devoid of its 3' hairpin
    Braun, F
    Hajnsdorf, E
    Regnier, P
    MOLECULAR MICROBIOLOGY, 1996, 19 (05) : 997 - 1005