Skip to main content
Log in

Autogenous regulation of Escherichia coli polynucleotide phosphorylase during cold acclimation by transcription termination and antitermination

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Adaptation of Escherichia coli at low temperature implicates a drastic reprogramming of gene expression patterns. Mechanisms operating downstream of transcription initiation, such as control of transcription termination, mRNA stability and translatability, play a major role in controlling gene expression in the cold acclimation phase. It was previously shown that Rho-dependent transcription termination within pnp, the gene encoding polynucleotide phosphorylase (PNPase), was suppressed in pnp nonsense mutants, whereas it was restored by complementation with wild type allele. Using a tRNA gene as a reporter and the strong Rho-dependent transcription terminator t imm of bacteriophage P4 as a tester, here we show that specific sites in the 5′-untranslated region of pnp mRNA are required for PNPase-sensitive cold-induced suppression of Rho-dependent transcription termination. We suggest that suppression of Rho-dependent transcription termination within pnp and its restoration by PNPase is an autogenous regulatory circuit that modulates pnp expression during cold acclimation.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alifano P, Rivellini F, Limauro D, Bruni CB, Carlomagno MS (1991) A consensus motif common to all Rho-dependent prokaryotic transcription terminators. Cell 64:553–563

    Article  PubMed  CAS  Google Scholar 

  • Artsimovitch I, Landick R (2002) The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109:193–203

    Article  PubMed  CAS  Google Scholar 

  • Bae W, Phadtare S, Severinov K, Inouye M (1999) Characterization of Escherichia coli cspE, whose product negatively regulates transcription of cspA, the gene for the major cold shock protein. Mol Microbiol 31:1429–1441

    Article  PubMed  CAS  Google Scholar 

  • Bae W, Xia B, Inouye M, Severinov K (2000) Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc Natl Acad Sci USA 97:7784–7789

    Article  PubMed  CAS  Google Scholar 

  • Baklanov MM, Golikova LN, Malygin EG (1996) Effect on DNA transcription of nucleotide sequences upstream to T7 promoter. Nucleic Acids Res 24:3659–3660

    Article  PubMed  CAS  Google Scholar 

  • Banerjee S, Chalissery J, Bandey I, Sen R (2006) Rho-dependent transcription termination: more questions than answers. J Microbiol 44:11–22

    PubMed  CAS  Google Scholar 

  • Bear DG, Hicks PS, Escudero KW, Andrews CL, McSwiggen JA, von Hippel PH (1988) Interactions of Escherichia coli transcription termination factor rho with RNA. II. Electron microscopy and nuclease protection experiments. J Mol Biol 199:623–635

    Article  PubMed  CAS  Google Scholar 

  • Beran RK, Simons RW (2001) Cold-temperature induction of Escherichia coli polynucleotide phosphorylase occurs by reversal of its autoregulation. Mol Microbiol 39:112–125

    Article  PubMed  CAS  Google Scholar 

  • Berlyn MKB (1998) Linkage map of Escherichia coli K-12, Edition 10: the traditional map. Microbiol Mol Biol Rev 62:814–984

    PubMed  CAS  Google Scholar 

  • Briani F, Zangrossi S, Ghisotti D, Dehò G (1996) A Rho-dependent transcription termination site regulated by bacteriophage P4 RNA immunity factor. Virology 223:57–67

    Article  PubMed  CAS  Google Scholar 

  • Briani F, Del Favero M, Capizzuto R, Consonni C, Zangrossi S, Greco C, De Gioia L, Tortora P, Dehò G (2007) Genetic analysis of polynucleotide phosphorylase structure and functions. Biochimie 89:145–157

    Article  PubMed  CAS  Google Scholar 

  • Ciampi MS (2006) Rho-dependent terminators and transcription termination. Microbiology 152:2515–2528

    Article  PubMed  CAS  Google Scholar 

  • Condon C, Squires C, Squires CL (1995) Control of rRNA transcription in Escherichia coli. Microbiol Rev 59:623–645

    PubMed  CAS  Google Scholar 

  • Das A, Court D, Adhya S (1976) Isolation and characterization of conditional lethal mutants of Escherichia coli defective in transcription termination factor rho. Proc Natl Acad Sci USA 73:1959–1963

    Article  PubMed  CAS  Google Scholar 

  • Dehò G, Zangrossi S, Sabbattini P, Sironi G, Ghisotti D (1992) Bacteriophage P4 immunity controlled by small RNAs via transcription termination. Mol Microbiol 6:3415–3425

    Article  PubMed  Google Scholar 

  • Dodd IB, Shearwin KE, Egan JB (2005) Revisited gene regulation in bacteriophage lambda. Curr Opin Genet Dev 15:145–152

    Article  PubMed  CAS  Google Scholar 

  • García Mena J, Das A, Sanchez-Trujillo A, Portier C, Montanez C (1999) A novel mutation in the KH domain of polynucleotide phosphorylase affects autoregulation and mRNA decay in Escherichia coli. Mol Microbiol 33:235–248

    Article  PubMed  Google Scholar 

  • Ghisotti D, Chiaramonte R, Forti F, Zangrossi S, Sironi G, Dehò G (1992) Genetic analysis of the immunity region of phage-plasmid P4. Mol Microbiol 6:3405–3413

    Article  PubMed  CAS  Google Scholar 

  • Gibson TJ, Thompson JD, Heringa J (1993) The KH domain occurs in a diverse set of RNA-binding proteins that include the antiterminator NusA and is probably involved in binding to nucleic acid. FEBS Lett 324:361–366

    Article  PubMed  CAS  Google Scholar 

  • Goldstein J, Pollitt NS, Inouye M (1990) Major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 87:283–287

    Article  PubMed  CAS  Google Scholar 

  • Gualerzi CO, Giuliodori AM, Pon CL (2003) Transcriptional and post-transcriptional control of cold-shock genes. J Mol Biol 331:527–539

    Article  PubMed  CAS  Google Scholar 

  • Henkin TM, Yanofsky C (2002) Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. Bioessays 24:700–707

    Article  PubMed  CAS  Google Scholar 

  • Herendeen SL, VanBogelen RA, Neidhardt FC (1979) Levels of major proteins of Escherichia coli during growth at different temperatures. J Bacteriol 139:185–194

    PubMed  CAS  Google Scholar 

  • Hinde P, Deighan P, Dorman CJ (2005) Characterization of the detachable Rho-dependent transcription terminator of the fimE gene in Escherichia coli K-12. J Bacteriol 187:8256–8266

    Article  PubMed  CAS  Google Scholar 

  • Ingraham JL, Marr AG (1996) Effect of temperature, pressure, pH, and osmotic stress on growth. In: Neidhardt FC (ed) Escherichia coli and Salmonella: cellular and molecular biology. American Society for Microbiology, Washington, DC pp 1570–1577

    Google Scholar 

  • Jager S, Fuhrmann O, Heck C, Hebermehl M, Schiltz E, Rauhut R, Klug G (2001) An mRNA degrading complex in Rhodobacter capsulatus. Nucleic Acids Res 29:4581–4588

    Article  PubMed  CAS  Google Scholar 

  • Jarrige AC, Mathy N, Portier C (2001) PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader. EMBO J 20:6845–6855

    Article  PubMed  CAS  Google Scholar 

  • Jiang W, Hou Y, Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272:196–202

    Article  PubMed  CAS  Google Scholar 

  • Jones PG, Mitta M, Kim Y, Jiang W, Inouye M (1996) Cold shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli. Proc Natl Acad Sci USA 93:76–80

    Article  PubMed  CAS  Google Scholar 

  • Jones PG, VanBogelen RA, Neidhardt FC (1987) Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol 169:2092–2095

    PubMed  CAS  Google Scholar 

  • Littauer UZ (2005) From polynucleotide phosphorylase to neurobiology. J Biol Chem 280:38889–38897

    Article  PubMed  CAS  Google Scholar 

  • Lopez PJ, Iost I, Dreyfus M (1994) The use of a tRNA as a transcriptional reporter: the T7 late promoter is extremely efficient in Escherichia coli but its transcripts are poorly expressed. Nucleic Acids Res 22:1186–1193

    Article  PubMed  CAS  Google Scholar 

  • Luttinger A, Hahn J, Dubnau D (1996) Polynucleotide phosphorylase is necessary for competence development in Bacillus subtilis. Mol Microbiol 19:343–356

    Article  PubMed  CAS  Google Scholar 

  • Marcaida MJ, Depristo MA, Chandran V, Carpousis AJ, Luisi BF (2006) The RNA degradosome: life in the fast lane of adaptive molecular evolution. Trends Biochem Sci 31:359–365

    Article  PubMed  CAS  Google Scholar 

  • McClain WH, Foss K, Jenkins RA, Schneider J (1991) Rapid determination of nucleotides that define tRNA(Gly) acceptor identity. Proc Natl Acad Sci USA 88:6147–6151

    Article  PubMed  CAS  Google Scholar 

  • Mohanty BK, Kushner SR (2000a) Polynucleotide phosphorylase functions both as a 3′ > 5′ exonuclease and a poly(A) polymerase in Escherichia coli. Proc Natl Acad Sci USA 97:11966–11971

    Article  CAS  Google Scholar 

  • Mohanty BK, Kushner SR (2000b) Polynucleotide phosphorylase, RNase II and RNase E play different roles in the in vivo modulation of polyadenylation in Escherichia coli. Mol Microbiol 36:982–994

    Article  CAS  Google Scholar 

  • Morgan WD, Bear DG, Litchman BL, von Hippel PH (1985) RNA sequence and secondary structure requirements for rho-dependent transcription termination. Nucleic Acids Res 13:3739–3754

    Article  PubMed  CAS  Google Scholar 

  • Ng H, Ingrahm JL, Mitta M (1962) Damage and derepression in Escherichia coli resulting from growth at low temperatures. J Bacteriol 84:331–339

    PubMed  CAS  Google Scholar 

  • Phadtare S, Alsina J, Inouye M (1999) Cold-shock response and cold-shock proteins. Curr Opin Microbiol 2:175–180

    Article  PubMed  CAS  Google Scholar 

  • Phadtare S, Inouye M, Severinov K (2002) The nucleic acid melting activity of Escherichia coli CspE is critical for transcription antitermination and cold acclimation of cells. J Biol Chem 277:7239–7245

    Article  PubMed  CAS  Google Scholar 

  • Piazza F, Zappone M, Sana M, Briani F, Dehò G (1996) Polynucleotide phosphorylase of Escherichia coli is required for the establishment of bacteriophage P4 immunity. J Bacteriol 178:5513–5521

    PubMed  CAS  Google Scholar 

  • Portier C, Dondon L, Grunberg Manago M, Régnier P (1987) The first step in the functional inactivation of the Escherichia coli polynucleotide phosphorylase messenger is a ribonuclease III processing at the 5′ end. EMBO J 6:2165–2170

    PubMed  CAS  Google Scholar 

  • Prud’homme-Généreux A, Beran RK, Iost I, Ramey CS, Mackie GA, Simons RW (2004) Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a ‘cold shock degradosome’. Mol Microbiol 54:1409–1421

    Article  PubMed  CAS  Google Scholar 

  • Régnier P, Portier C (1986) Initiation, attenuation and RNase III processing of transcripts from the Escherichia coli operon encoding ribosomal protein S15 and polynucleotide phosphorylase. J Mol Biol 187:23–32

    Article  PubMed  Google Scholar 

  • Régnier P, Grunberg Manago M, Portier C (1987) Nucleotide sequence of the pnp gene of Escherichia coli encoding polynucleotide phosphorylase. Homology of the primary structure of the protein with the RNA-binding domain of ribosomal protein S1. J Biol Chem 262:63–68

    PubMed  Google Scholar 

  • Regonesi ME, Briani F, Ghetta A, Zangrossi S, Ghisotti D, Tortora P, Dehò G (2004) A mutation in polynucleotide phosphorylase from Escherichia coli impairing RNA binding and degradosome stability. Nucleic Acids Res 32:1006–1017

    Article  PubMed  CAS  Google Scholar 

  • Regonesi ME, Del Favero M, Basilico F, Briani F, Benazzi L, Tortora P, Mauri P, Dehò G (2006) Analysis of the Escherichia coli RNA degradosome composition by a proteomic approach. Biochimie 88:151–161

    Article  PubMed  CAS  Google Scholar 

  • Reiner AM (1969a) Characterization of polynucleotide phosphorylase mutants of Escherichia coli. J Bacteriol 97:1437–1443

    CAS  Google Scholar 

  • Reiner AM (1969b) Isolation and mapping of polynucleotide phosphorylase mutants of Escherichia coli. J Bacteriol 97:1431–1436

    CAS  Google Scholar 

  • Robert-Le Meur M, Portier C (1992) E. coli polynucleotide phosphorylase expression is autoregulated through an RNase III-dependent mechanism. EMBO J 11:2633–2641

    PubMed  CAS  Google Scholar 

  • Robert-Le Meur M, Portier C (1994) Polynucleotide phosphorylase of Escherichia coli induces the degradation of its RNase III processed messenger by preventing its translation. Nucleic Acids Res 22:397–403

    Article  PubMed  CAS  Google Scholar 

  • Sasaki I, Bertani G (1965) Growth abnormalities in Hfr derivatives of Escherichia coli strain C. J Gen Microbiol 40:365–376

    PubMed  CAS  Google Scholar 

  • Sloan SB, Weisberg RA (1993) Use of a gene encoding a suppressor tRNA as a reporter of transcription: analyzing the action of the Nun protein of bacteriophage HK022. Proc Natl Acad Sci USA 90:9842–9846

    Article  PubMed  CAS  Google Scholar 

  • Symmons MF, Jones GH, Luisi BF (2000) A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Struct Fold Des 8:1215–1226

    Article  CAS  Google Scholar 

  • Torres M, Balada JM, Zellars M, Squires C, Squires CL (2004) In vivo effect of NusB and NusG on rRNA transcription antitermination. J Bacteriol 186:1304–1310

    Article  PubMed  CAS  Google Scholar 

  • Vicari D, Artsimovitch I (2004) Virulence regulators RfaH and YaeQ do not operate in the same pathway. Mol Genet Genomics 272:489–496

    Article  PubMed  CAS  Google Scholar 

  • Wang N, Yamanaka K, Inouye M (1999) CspI, the ninth member of the CspA family of Escherichia coli, is induced upon cold shock. J Bacteriol 181:1603–1609

    PubMed  CAS  Google Scholar 

  • Weber MHW, Marahiel MA (2003) Bacterial cold shock responses. Sci Prog 86:9–75

    Article  PubMed  CAS  Google Scholar 

  • Yamanaka K, Fang L, Inouye M (1998) The CspA family in Escherichia coli: multiple gene duplication for stress adaptation. Mol Microbiol 27:247–255

    Article  PubMed  CAS  Google Scholar 

  • Zangrossi S, Briani F, Ghisotti D, Regonesi ME, Tortora P, Dehò G (2000) Transcriptional and post-transcriptional control of polynucleotide phosphorylase during cold acclimation in Escherichia coli. Mol Microbiol 36:1470–1480

    Article  PubMed  CAS  Google Scholar 

  • Zuker M, Mathews D, Turner D (1999) Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In: Barciszewski J, Clark B (eds) RNA biochemistry and biotechnology. Kluwer, Dordrecht, pp 11–43

Download references

Acknowledgments

This research was supported by joint grants from the Ministero dell’Istruzione, dell’Università e della Ricerca and Università degli Studi di Milano (PRIN 2003, PRIN 2005, and FIRB 2001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gianni Dehò.

Additional information

Communicated by D. Andersson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marchi, P., Longhi, V., Zangrossi, S. et al. Autogenous regulation of Escherichia coli polynucleotide phosphorylase during cold acclimation by transcription termination and antitermination. Mol Genet Genomics 278, 75–84 (2007). https://doi.org/10.1007/s00438-007-0231-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-007-0231-3

Keywords

Navigation