Abstract
Staphylococcus aureus hibernation promoting factor (SaHPF) is a 22,2 kDa protein which plays a crucial role in 100S Staphylococcus aureus ribosome formation during stress. SaHPF consists of N-terminal domain (NTD) that prevents proteins synthesis by binding to the 30S subunit at the P- and A-sites, connected through a flexible linker with a C-terminal domain (CTD) that keeps ribosomes in 100S form via homodimerization. Recently obtained 100S ribosome structure of S. aureus by cryo-EM shown that SaHPF-NTD bound to the ribosome active sites, however due to the absence of SaHPF-NTD structure it was modeled by homology with the E. coli hibernation factors HPF and YfiA. In present paper we have determined the solution structure of SaHPF-NTD by high-resolution NMR spectroscopy which allows us to increase structural knowledge about HPF structure from S. aureus.
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Data availability
Structural data are available in the Protein Data Bank/BioMagResBank databases under the accession number 6QBZ / 27085.
References
Akanuma G et al (2016) Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis. Microbiology 162:448–458
Akiyama T et al (2017) Resuscitation of Pseudomonas aeruginosa from dormancy requires hibernation promoting factor (PA4463) for ribosome preservation. Proc Natl Acad Sci USA 114:3204–3209
Bardiaux B, Malliavin T, Nilges M (2012) ARIA for solution and solid-state NMR. Methods Mol Biol 831:453–483
Basu A, Yap MNF (2016) Ribosome hibernation factor promotes Staphylococcal survival and differentially represses translation. Nucleic Acids Res 44:4881–4893
Beckert B et al (2017) Structure of the Bacillus subtilis hibernating 100S ribosome reveals the basis for 70S dimerization. EMBO J 36:2061–2072
Bieri P, Leibundgut M, Saurer M, Boehringer D, Ban N (2017) The complete structure of the chloroplast 70S ribosome in complex with translation factor pY. EMBO J 36:475–486
Brunger AT et al (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54:905–921
De Bari H, Berry EA (2013) Structure of Vibrio cholerae ribosome hibernation promoting factor. Acta Crystallogr Sect F 69:228–236
de las Heras A, Cain RJ, Bielecka MK, Vazquez-Boland JA (2011) Regulation of Listeria virulence: PrfA master and commander. Curr Opin Microbiol 14:118–127
Izutsu K et al (2001) Escherichia coli ribosome-associated protein SRA, whose copy number increases during stationary phase. J Bacteriol 183:2765–2773
Kato T et al (2010) Structure of the 100S ribosome in the hibernation stage revealed by electron cryomicroscopy. Structure 18:719–724
Khusainov I et al (2017a) Structures and dynamics of hibernating ribosomes from Staphylococcus aureus mediated by intermolecular interactions of HPF. EMBO J 36:2073–2087
Khusainov I et al (2017b) Structure of the 70S ribosome from human pathogen Staphylococcus aureus. Nucleic Acids Res 45:1026
Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477–486
Maki Y, Yoshida H, Wada A (2000) Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary phase Escherichia coli. Genes Cells 5:965–974
McKay SL, Portnoy DA (2015) Ribosome hibernation facilitates tolerance of stationary-phase bacteria to aminoglycosides. Antimicrob Agents Chemother 59:6992–6999
Pettersen EF et al (2004) UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612
Polikanov YS, Blaha GM, Steitz TA (2012) How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science 336:915–918
Puri P et al (2014) Lactococcus lactis YfiA is necessary and sufficient for ribosome dimerization. Mol Microbiol 91:394–407
Russell JB, Cook GM (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59:48–62
Sato A et al (2009) Solution structure of the E. coli ribosome hibernation promoting factor HPF: implications for the relationship between structure and function. Biochem Biophys Res Commun 389:580–585
Sharma MR et al (2010) PSRP1 is not a ribosomal protein, but a ribosome-binding factor that is recycled by the ribosome-recycling factor (RRF) and elongation factor G (EF-G). J Biol Chem 285:4006–4014
Tagami K et al (2012) Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp(0) mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. Microbiologyopen 1:115–134
Ueta M et al (2008) Role of HPF (hibernation promoting factor) in translational activity in Escherichia coli. J Biochem 143:425–433
Ueta M, Wada C, Wada A (2010) Formation of 100S ribosomes in Staphylococcus aureus by the hibernation promoting factor homolog SaHPF. Genes Cells 15:43–58
Ueta M et al (2013) Conservation of two distinct types of 100S ribosome in bacteria. Genes Cells 18:554–574
Usachev KS, Ayupov RK, Validov SZ, Khusainov IS, Yusupov MM (2018) NMR assignments of the N-terminal domain of Staphylococcus aureus hibernation promoting factor (SaHPF). Biomol NMR Assign 12:85–89
Vila-Sanjurjo A, Schuwirth BS, Hau CW, Cate JH (2004) Structural basis for the control of translation initiation during stress. Nat Struct Mol Biol 11:1054–1059
Yoshida H, Wada A (2014) The 100S ribosome: ribosomal hibernation induced by stress. Wiley Interdiscip Rev RNA 5:723–732
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This work was supported by the Russian Science Foundation (Grant 16-14-10014).
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Usachev, K.S., Validov, S.Z., Khusainov, I.S. et al. Solution structure of the N-terminal domain of the Staphylococcus aureus hibernation promoting factor. J Biomol NMR 73, 223–227 (2019). https://doi.org/10.1007/s10858-019-00254-4
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DOI: https://doi.org/10.1007/s10858-019-00254-4