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Compartment and signal-specific codependence in the transcriptional control of Salmonella periplasmic copper homeostasis.
Proc Natl Acad Sci U S A. 2016 10 11; 113(41):11573-11578.PN

Abstract

Copper homeostasis is essential for bacterial pathogen fitness and infection, and has been the focus of a number of recent studies. In Salmonella, envelope protection against copper overload and macrophage survival depends on CueP, a major copper-binding protein in the periplasm. This protein is also required to deliver the metal ion to the Cu/Zn superoxide dismutase SodCII. The Salmonella-specific CueP-coding gene was originally identified as part of the Cue regulon under the transcriptional control of the cytoplasmic copper sensor CueR, but its expression differs from the rest of CueR-regulated genes. Here we show that cueP expression is controlled by the concerted action of CueR, which detects the presence of copper in the cytoplasm, and by CpxR/CpxA, which monitors envelope stress. Copper-activated CueR is necessary for the appropriate spatial arrangement of the -10 and -35 elements of the cueP promoter, and CpxR is essential to recruit the RNA polymerase. The integration of two ancestral sensory systems-CueR, which provides signal specificity, and CpxR/CpxA, which detects stress in the bacterial envelope-restricts the expression of this periplasmic copper resistance protein solely to cells encountering surplus copper that disturbs envelope homeostasis, emulating the role of the CusR/CusS regulatory system present in other enteric bacteria.

Authors+Show Affiliations

Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Instituto de Biología Molecular y Celular de Rosario, Universidad Nacional de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas, 2000-Rosario, Argentina.Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Instituto de Biología Molecular y Celular de Rosario, Universidad Nacional de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas, 2000-Rosario, Argentina.Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Instituto de Biología Molecular y Celular de Rosario, Universidad Nacional de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas, 2000-Rosario, Argentina.Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Instituto de Biología Molecular y Celular de Rosario, Universidad Nacional de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas, 2000-Rosario, Argentina soncini@ibr-conicet.gov.ar.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

27679850

Citation

Pezza, Alejandro, et al. "Compartment and Signal-specific Codependence in the Transcriptional Control of Salmonella Periplasmic Copper Homeostasis." Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 41, 2016, pp. 11573-11578.
Pezza A, Pontel LB, López C, et al. Compartment and signal-specific codependence in the transcriptional control of Salmonella periplasmic copper homeostasis. Proc Natl Acad Sci U S A. 2016;113(41):11573-11578.
Pezza, A., Pontel, L. B., López, C., & Soncini, F. C. (2016). Compartment and signal-specific codependence in the transcriptional control of Salmonella periplasmic copper homeostasis. Proceedings of the National Academy of Sciences of the United States of America, 113(41), 11573-11578.
Pezza A, et al. Compartment and Signal-specific Codependence in the Transcriptional Control of Salmonella Periplasmic Copper Homeostasis. Proc Natl Acad Sci U S A. 2016 10 11;113(41):11573-11578. PubMed PMID: 27679850.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Compartment and signal-specific codependence in the transcriptional control of Salmonella periplasmic copper homeostasis. AU - Pezza,Alejandro, AU - Pontel,Lucas B, AU - López,Carolina, AU - Soncini,Fernando C, Y1 - 2016/09/27/ PY - 2016/9/30/pubmed PY - 2018/1/27/medline PY - 2016/9/29/entrez KW - CpxR/CpxA KW - CueP KW - Salmonella KW - periplasmic copper homeostasis KW - transcriptional codependence SP - 11573 EP - 11578 JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc Natl Acad Sci U S A VL - 113 IS - 41 N2 - Copper homeostasis is essential for bacterial pathogen fitness and infection, and has been the focus of a number of recent studies. In Salmonella, envelope protection against copper overload and macrophage survival depends on CueP, a major copper-binding protein in the periplasm. This protein is also required to deliver the metal ion to the Cu/Zn superoxide dismutase SodCII. The Salmonella-specific CueP-coding gene was originally identified as part of the Cue regulon under the transcriptional control of the cytoplasmic copper sensor CueR, but its expression differs from the rest of CueR-regulated genes. Here we show that cueP expression is controlled by the concerted action of CueR, which detects the presence of copper in the cytoplasm, and by CpxR/CpxA, which monitors envelope stress. Copper-activated CueR is necessary for the appropriate spatial arrangement of the -10 and -35 elements of the cueP promoter, and CpxR is essential to recruit the RNA polymerase. The integration of two ancestral sensory systems-CueR, which provides signal specificity, and CpxR/CpxA, which detects stress in the bacterial envelope-restricts the expression of this periplasmic copper resistance protein solely to cells encountering surplus copper that disturbs envelope homeostasis, emulating the role of the CusR/CusS regulatory system present in other enteric bacteria. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/27679850/Compartment_and_signal_specific_codependence_in_the_transcriptional_control_of_Salmonella_periplasmic_copper_homeostasis_ L2 - http://www.pnas.org/cgi/pmidlookup?view=long&pmid=27679850 DB - PRIME DP - Unbound Medicine ER -