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Research Paper

Molybdopterin biosynthesis pathway contributes to the regulation of SaeRS two-component system by ClpP in Staphylococcus aureus

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Pages 727-739 | Received 04 Dec 2021, Accepted 11 Apr 2022, Published online: 28 Apr 2022

References

  • Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339(8):520–532.
  • Wang B, Muir TW. Regulation of virulence in Staphylococcus aureus: molecular mechanisms and remaining puzzles. Cell Chem Biol. 2016;23(2):214–224.
  • Cheung AL, Bayer AS, Zhang G, et al. Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol Med Microbiol. 2004;40(1):1–9.
  • Liu Q, Yeo WS, Bae T. The SaeRS two-component system of Staphylococcus aureus. Genes (Basel). 2016;7(10):81.
  • Xiong YQ, Willard J, Yeaman MR, et al. Regulation of Staphylococcus aureus α-toxin gene (hla) expression by agr, sarA, and sae in vitro and in experimental infective endocarditis. J Infect Dis. 2006;194(9):1267–1275.
  • Olson ME, Nygaard TK, Ackermann L, et al. Staphylococcus aureus nuclease is a SaeR/S-dependent virulence factor. Infect Immun. 2013;81(4):1316–1324. DOI:10.1128/IAI.01242-12
  • Ramundo MS, Beltrame CO, Botelho AM, et al. A unique SaeS allele overrides cell-density dependent expression of saeR and lukSF-PV in the ST30-SCCmecIV lineage of CA-MRSA. Int J Med Microbiol. 2016;306(6):367–380. DOI:10.1016/j.ijmm.2016.05.001
  • Adhikari RP, Novick RP. Regulatory organization of the staphylococcal sae locus. Microbiology. 2008;154(3):949–959.
  • Geiger T, Goerke C, Mainiero M, et al. The virulence regulator Sae of Staphylococcus aureus: promoter activities and response to phagocytosis-related signals. J Bacteriol. 2008;190(10):3419–3428.
  • Liu Q, Hu M, Yeo WS, et al. Rewiring of the FtsH regulatory network by a single nucleotide change in SaeS of Staphylococcus aureus. Sci Rep. 2017;7(1):8456. DOI:10.1038/s41598-017-08774-5
  • Dalbey RE, Wang P, van Dijl JM. Membrane proteases in the bacterial protein secretion and quality control pathway. Microbiol Mol Biol Rev. 2012;76(2):311–330.
  • Michel A, Agerer F, Hauck CR, et al. Global regulatory impact of ClpP protease of Staphylococcus aureus on regulons involved in virulence, oxidative stress response, autolysis, and DNA repair. J Bacteriol. 2006;188(16):5783–5796. DOI:10.1128/JB.00074-06
  • Alexopoulos JA, Guarne A, Ortega J. ClpP: a structurally dynamic protease regulated by AAA+ proteins. J Struct Biol. 2012;179(2):202–210.
  • Frees D, Chastanet A, Qazi S, et al. Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol Microbiol. 2004;54(5):1445–1462. DOI:10.1111/j.1365-2958.2004.04368.x
  • Frees D, Thomsen LE, Ingmer H. Staphylococcus aureus ClpYQ plays a minor role in stress survival. Arch Microbiol. 2005;183(4):286–291.
  • Fischer B, Rummel G, Aldridge P, et al. The FtsH protease is involved in development, stress response and heat shock control in Caulobacter crescentus. Mol Microbiol. 2002;44(2):461–478.
  • Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983;166(4):557–580.
  • Donnelly MI, Zhou M, Millard CS, et al. An expression vector tailored for large-scale, high-throughput purification of recombinant proteins. Protein Expr Purif. 2006;47(2):446–454. DOI:10.1016/j.pep.2005.12.011
  • Monk IR, Shah IM, Xu M, et al. Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. Mbio. 2012;3(2). DOI:10.1128/mBio.00277-11
  • Bae T, Schneewind O. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid. 2006;55(1):58–63.
  • Liu Q, Wang X, Qin J, et al. The ATP-dependent protease ClpP inhibits biofilm formation by regulating Agr and cell wall hydrolase Sle1 in Staphylococcus aureus. Front Cell Infect Microbiol. 2017;7:181.
  • Sun F, Cho H, Jeong DW, et al. Aureusimines in Staphylococcus aureus are not involved in virulence. PLoS One. 2011;5(12):e15703.
  • Ni T, Ye F, Liu X, et al. Characterization of gain-of-function mutant provides new insights into ClpP structure. ACS Chem Biol. 2016;11(7):1964–1972. DOI:10.1021/acschembio.6b00390
  • Chen J, Ram G, Yoong P, et al. An rpsL-based allelic exchange vector for Staphylococcus aureus. Plasmid. 2015;79:8–14.
  • Yeo WS, Anokwute C, Marcadis P, et al. A membrane-bound transcription factor is proteolytically regulated by the AAA+ protease FtsH in Staphylococcus aureus. J Bacteriol. 2020;202(9). DOI:10.1128/JB.00019-20
  • Frees D, Savijoki K, Varmanen P, et al. Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, gram-positive bacteria. Mol Microbiol. 2007;63(5):1285–1295.
  • Lithgow JK, Ingham E, Foster SJ. Role of the hprT–ftsh locus in Staphylococcus aureus. Microbiology. 2004;150(2):373–381.
  • Frees D, Andersen JH, Hemmingsen L, et al. New insights into Staphylococcus aureus stress tolerance and virulence regulation from an analysis of the role of the ClpP protease in the strains Newman, COL, and SA564. J Proteome Res. 2012;11(1):95–108. DOI:10.1021/pr200956s
  • Feng J, Michalik S, Varming AN, et al. Trapping and proteomic identification of cellular substrates of the ClpP protease in Staphylococcus aureus. J Proteome Res. 2013;12(2):547–558. DOI:10.1021/pr300394r
  • Kihara A, Akiyama Y, Ito K. A protease complex in the Escherichia coli plasma membrane: HflKC (HflA) forms a complex with FtsH (HflB), regulating its proteolytic activity against SecY. Embo J. 1996;15(22):6122–6131.
  • Leimkuhler S. The biosynthesis of the molybdenum cofactors in Escherichia coli. Environ Microbiol. 2020;22(6):2007–2026.
  • Schwarz G, Mendel RR. Molybdenum cofactor biosynthesis and molybdenum enzymes. Annu Rev Plant Biol. 2006;57(1):623–647.
  • Wang W, Zhang W, Lu J, et al. MoeA, an enzyme in the molybdopterin synthesis pathway, is required for rifamycin SV production in Amycolatopsis mediterranei U32. Appl Microbiol Biotechnol. 2002;60(1–2):139–146. DOI:10.1007/s00253-002-1093-6
  • Richardson AR, Somerville GA, Sonenshein AL. Regulating the intersection of metabolism and pathogenesis in gram-positive bacteria. Microbiol Spectr. 2015;3(3). DOI:10.1128/microbiolspec.MBP-0004-2014
  • Ericson ME, Subramanian C, Frank MW, et al. Role of fatty acid kinase in cellular lipid homeostasis and SaeRS-dependent virulence factor expression in Staphylococcus aureus. MBio. 2017;8(4). DOI:10.1128/mBio.00988-17
  • Schurig-Briccio LA, Parraga Solorzano PK, Lencina AM, et al. Role of respiratory NADH oxidation in the regulation of Staphylococcus aureus virulence. EMBO Rep. 2020;21(5):e45832. DOI:10.15252/embr.201845832
  • Krute CN, Rice KC, Bose JL. VfrB is a key activator of the Staphylococcus aureus SaeRS two-component system. J Bacteriol. 2017;199:e00828–16.
  • Liu Q, Cho H, Yeo WS, et al. The extracytoplasmic linker peptide of the sensor protein SaeS tunes the kinase activity required for staphylococcal virulence in response to host signals. PLoS Pathog. 2015;11(4):e1004799.
  • Hinton SM, Dean D. Biogenesis of molybdenum cofactors. Crit Rev Microbiol. 1990;17(3):169–188.
  • Mashruwala AA, Gries CM, Scherr TD, et al. SaeRS is responsive to cellular respiratory status and regulates fermentative biofilm formation in Staphylococcus aureus. Infect Immun. 2017;85(8). DOI:10.1128/IAI.00157-17