721
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Arginine 58 is indispensable for proper function of the Francisella tularensis subsp. holarctica FSC200 HU protein, and its substitution alters virulence and mediates immunity against wild-type strain

ORCID Icon & ORCID Icon
Pages 1790-1809 | Received 16 May 2022, Accepted 01 Oct 2022, Published online: 17 Oct 2022

References

  • McCoy GW, Chapin CW. Further observations on a plague-like disease of rodents with a preliminary note on the causative agent, bacterium tularense. J Infect Dis. 1912;10(1):61–72.
  • Dennis DT, Inglesby TV, Henderson DA, et al. Tularemia as a biological weapon: medical and public health management. JAMA. 2001;285:2763–2773.
  • Tärnvik A. Nature of Protective Immunity to Francisella Tularensis. Rev Infect Dis. 1989;11:440–451.
  • Spidlova P, Stulik J. Francisella tularensis type VI secretion system comes of age. Virulence. 2017;8:628–631.
  • Nano FE, Zhang N, Cowley SC, et al. A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol. 2004;186:6430–6436.
  • Santic M, Molmeret M, Klose KE, et al. The Francisella tularensis pathogenicity island protein iglc and its regulator mgla are essential for modulating phagosome biogenesis and subsequent bacterial escape into the cytoplasm. Cell Microbiol. 2005;7:969–979.
  • Baron GS, Nano FE. MglA and MglB are required for the intramacrophage growth of Francisella novicida. Mol Microbiol. 1998;29:247–259.
  • Brotcke A, Weiss DS, Kim CC, et al. Identification of MglA-regulated genes reveals novel virulence factors in Francisella tularensis. Infect Immun. 2006;74:6642–6655.
  • Bell BL, Mohapatra NP, Gunn JS. Regulation of virulence gene transcripts by the Francisella novicida orphan response regulator PmrA: role of phosphorylation and evidence of MglA/SspA interaction. Infect Immun. 2010;78:2189–2198.
  • Brotcke A, Monack DM. Identification of FevR, a novel regulator of virulence gene expression in Francisella novicida. Infect Immun. 2008;76:3473–3480.
  • Dai S, Mohapatra NP, Schlesinger LS, et al. Regulation of Francisella tularensis virulence. Front Microbiol. 2010;1:144.
  • Spidlova P, Stojkova P, Sjöstedt A, et al. Control of Francisella tularensis virulence at gene level: network of transcription factors. Microorganisms. 2020;8:1622.
  • Ali Azam T, Iwata A, Nishimura A, et al. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol. 1999;181:6361–6370.
  • Dillon SC, Dorman CJ. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol. 2010;8:185–195.
  • Kamashev D, Rouviere-Yaniv J. The histone-like protein HU binds specifically to DNA recombination and repair intermediates. Embo J. 2000;19:6527–6535.
  • Prieto AI, Kahramanoglou C, Ali RM, et al. Genomic analysis of DNA binding and gene regulation by homologous nucleoid-associated proteins IHF and HU in Escherichia coli K12. Nucleic Acids Res. 2012;40:3524–3537.
  • Bonnefoy E, Rouvière-Yaniv J. HU, the major histone-like protein of E. Coli, modulates the binding of IHF to OriC. Embo J. 1992;11:4489–4496.
  • Oberto J, Nabti S, Jooste V, et al. The HU regulon is composed of genes responding to anaerobiosis, acid stress, high osmolarity and SOS induction. PLoS One. 2009;4:e4367.
  • Preobrajenskaya, Preobrajenskaya O, Boullard A, et al. The protein HU can displace the LexA repressor from its DNA-binding sites. Mol Microbiol. 1994;13:459–467.
  • Stojkova P, Spidlova P, Lenco J, et al. HU protein is involved in intracellular growth and full virulence of Francisella tularensis. Virulence. 2018;9:754–770.
  • Priyadarshini R, Cugini C, Arndt A, et al. The nucleoid-associated protein HUβ affects global gene expression in porphyromonas gingivalis. Microbiology. 2013;159:219–229.
  • Mangan MW, Lucchini S, Croinin TO, et al. Nucleoid-associated protein HU controls three regulons that coordinate virulence, response to stress and general physiology in salmonella enterica serovar typhimurium. Microbiology. 2011;157:1075–1087.
  • Ramirez-Medina E, Vuono EA, Pruitt S, et al. Deletion of African swine fever virus histone-like protein, A104R from the Georgia isolate drastically reduces virus virulence in domestic pigs. Viruses. 2022;14:1112.
  • Frouco G, Freitas FB, Coelho J, et al. DNA-binding properties of African swine fever virus PA104R, a histone-like protein involved in viral replication and transcription. J Virol 2017;91: e02498-16: 10.1128/JVI.02498-16.
  • Liu R, Sun Y, Chai Y, et al. The structural basis of African swine fever virus PA104R binding to DNA and its inhibition by stilbene derivatives. Proc Natl Acad Sci U S A. 2020;117:11000–11009.
  • Stojkova P, Spidlova P, Stulik J. Nucleoid-associated protein HU: a lilliputian in gene regulation of bacterial virulence. Front Cell Infect Microbiol. 2019;9. DOI:10.3389/fcimb.2019.00159.
  • Stojkova P, Spidlova P. Bacterial nucleoid-associated protein HU as an extracellular player in host-pathogen interaction. Front Cell Infect Microbiol. 2022. DOI:10.3389/fcimb.2022.999737
  • Bhowmick T, Ghosh S, Dixit K, et al. Targeting mycobacterium tuberculosis nucleoid-associated protein HU with structure-based inhibitors. Nat Commun. 2014;5:4124.
  • Pettijohn DE. Histone-like proteins and bacterial chromosome structure. J Biol Chem. 1988;263:12793–12796.
  • Marchler-Bauer A, Bo Y, Han L, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45:D200–203.
  • Charity JC, Blalock LT, Costante-Hamm MM, et al. Small molecule control of virulence gene expression in Francisella tularensis. PLoS Pathog. 2009;5:e1000641.
  • Cuthbert BJ, Ross W, Rohlfing AE, et al. Dissection of the molecular circuitry controlling virulence in Francisella tularensis. Genes Dev. 2017;31:1549–1560.
  • Rohlfing AE, Dove SL. Coordinate control of virulence gene expression in Francisella tularensis involves direct interaction between key regulators. J Bacteriol. 2014;196:3516–3526.
  • Alam A, Bröms JE, Kumar R, et al. The role of ClpB in bacterial stress responses and virulence. Front Mol Biosci. 2021;8:668910.
  • Alam A, Golovliov I, Javed E, et al. ClpB mutants of Francisella tularensis subspecies holarctica and tularensis are defective for type VI secretion and intracellular replication. Sci Rep. 2018;8:11324.
  • Alam A, Golovliov I, Javed E, et al. Dissociation between the critical role of ClpB of Francisella tularensis for the heat shock response and the dnak interaction and its important role for efficient type VI secretion and bacterial virulence. PLoS Pathog. 2020;16:e1008466.
  • Rodriguez SA, Yu J-J, Davis G, et al. Targeted inactivation of Francisella tularensis genes by group II introns. Appl Environ Microbiol. 2008;74:2619–2626.
  • Spidlova P, Stojkova P, Dankova V, et al. Francisella tularensis D-Ala D-Ala carboxypeptidase DacD is involved in intracellular replication and it is necessary for bacterial cell wall integrity. Front Cell Infect Microbiol. 2018;8. DOI:10.3389/fcimb.2018.00111.
  • Balandina A, Kamashev D, Rouviere-Yaniv J. The bacterial histone-like protein HU specifically recognizes similar structures in all nucleic acids DNA, RNA, and THEIR HYBRIDS. J Biol Chem. 2002;277:27622–27628.
  • Lee EC, Hales LM, Gumport RI, et al. The isolation and characterization of mutants of the integration Host Factor (IHF) of Escherichia coli with altered, expanded DNA-binding specificities. Embo J. 1992;11:305–313.
  • Rice PA, Yang S, Mizuuchi K, et al. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-Turn. Cell. 1996;87:1295–1306.
  • Saitoh F, Kawamura S, Yamasaki N, et al. Arginine-55 in the beta-arm is essential for the activity of DNA-binding protein HU from bacillus stearothermophilus. Biosci Biotechnol Biochem. 1999;63:2232–2235.
  • Gupta M, Sajid A, Sharma K, et al. HupB, a nucleoid-associated protein of mycobacterium tuberculosis, is modified by Serine/Threonine protein kinases in vivo. J Bacteriol. 2014;196:2646–2657.
  • Rouvière-Yaniv J, Yaniv M, Germond J-E-E. Coli DNA binding protein HU forms nucleosome-like structure with circular double-stranded DNA. Cell. 1979;17:265–274.
  • Maurer S, Fritz J, Muskhelishvili G. A systematic in vitro study of nucleoprotein complexes formed by bacterial nucleoid-associated proteins revealing novel types of DNA organization. J Mol Biol. 2009;387:1261–1276.
  • Guo F, Adhya S. Spiral structure of Escherichia coli hualphabeta provides foundation for DNA supercoiling. Proc Natl Acad Sci U S A. 2007;104:4309–4314.
  • Broyles SS, Pettijohn DE. Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch. J Mol Biol. 1986;187:47–60.
  • Lassak J, Koller F, Krafczyk R, et al. Exceptionally versatile - arginine in bacterial post-translational protein modifications. Biol Chem. 2019;400:1397–1427.