930
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

A novel aquaporin Aagp contributes to Streptococcus suis H2O2 efflux and virulence

, , , , , & ORCID Icon show all
Article: 2249789 | Received 13 Apr 2023, Accepted 13 Aug 2023, Published online: 24 Aug 2023

References

  • Goyette-Desjardins G, Auger JP, Xu J, et al. Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg Microbes Infect. 2014 Jun;3(6):e45. doi: 10.1038/emi.2014.45
  • Ferrando ML, de Greeff A, van Rooijen WJ, et al. Host-pathogen interaction at the intestinal mucosa correlates with zoonotic potential of Streptococcus suis. J Infect Dis. 2015 Jul 1;212(1):95–11.
  • Ferrando ML, Schultsz C. A hypothetical model of host-pathogen interaction of Streptococcus suis in the gastro-intestinal tract. Gut Microbes. 2016;7(2):154–162. doi: 10.1080/19490976.2016.1144008
  • Fuangthong M, Helmann JD. The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proc Natl Acad Sci U S A. 2002 May 14;99(10):6690–6695.
  • Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol. 2003;57(1):395–418. doi: 10.1146/annurev.micro.57.030502.090938
  • Sobota JM, Imlay JA. Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc Natl Acad Sci U S A. 2011 Mar 29;108(13):5402–5407.
  • Dubbs JM, Mongkolsuk S. Peroxide-sensing transcriptional regulators in bacteria. J Bacteriol. 2012 Oct;194(20):5495–5503. doi: 10.1128/JB.00304-12
  • Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol. 2013 Jul;11(7):443–454. doi: 10.1038/nrmicro3032
  • Panday A, Sahoo MK, Osorio D, et al. NADPH oxidases: an overview from structure to innate immunity-associated pathologies. Cell Mol Immunol. 2015 Jan;12(1):5–23. doi: 10.1038/cmi.2014.89
  • Li H, Zhou X, Huang Y, et al. Reactive oxygen species in pathogen clearance: the killing mechanisms, the adaption response, and the side effects. Front Microbiol. 2020;11:622534. doi: 10.3389/fmicb.2020.622534
  • Willenborg J, Koczula A, Fulde M, et al. FlpS, the FNR-Like protein of Streptococcus suis is an essential, oxygen-sensing activator of the arginine deiminase System. Pathogens. 2016 Jul 21;5(3):51.
  • Zhang T, Ding Y, Li T, et al. A Fur-like protein PerR regulates two oxidative stress response related operons dpr and metQIN in Streptococcus suis. BMC Microbiol. 2012 May 30;12(1):85.
  • Hu Y, Hu Q, Wei R, et al. The XRE family transcriptional regulator SrtR in Streptococcus suis is involved in oxidant tolerance and virulence. Front Cell Infect Microbiol. 2018;8:452. doi: 10.3389/fcimb.2018.00452
  • Zheng C, Xu J, Li J, et al. Two spx regulators modulate stress tolerance and virulence in Streptococcus suis serotype 2. PLoS One. 2014;9(9):e108197. doi: 10.1371/journal.pone.0108197
  • Zhu H, Wang Y, Ni Y, et al. The redox-sensing regulator rex contributes to the virulence and oxidative stress response of Streptococcus suis serotype 2. Front Cell Infect Microbiol. 2018;8:317. doi: 10.3389/fcimb.2018.00317
  • Wu Z, Zhang W, Lu C. Comparative proteome analysis of secreted proteins of Streptococcus suis serotype 9 isolates from diseased and healthy pigs. Microb Pathog. 2008 Sep;45(3):159–166. doi: 10.1016/j.micpath.2008.04.009
  • Wang S, Ma M, Liang Z, et al. Pathogenic investigations of Streptococcus pasteurianus, an underreported zoonotic pathogen, isolated from a diseased piglet with meningitis. Transbound Emerg Dis. 2022 Sep;69(5):2609–2620. doi: 10.1111/tbed.14413
  • Wu Z, Wu C, Shao J, et al. The Streptococcus suis transcriptional landscape reveals adaptation mechanisms in pig blood and cerebrospinal fluid. RNA. 2014 Jun;20(6):882–898. doi: 10.1261/rna.041822.113
  • Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012 Mar 4;9(4):357–359.
  • Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010 Jan 1;26(1):139–140.
  • Dai J, Lai L, Tang H, et al. Streptococcus suis synthesizes deoxyadenosine and adenosine by 5’-nucleotidase to dampen host immune responses. Virulence. 2018;9(1):1509–1520. doi: 10.1080/21505594.2018.1520544
  • Zhu Y, Dong W, Ma J, et al. Utilization of the ComRS system for the rapid markerless deletion of chromosomal genes in Streptococcus suis. Future Microbiol. 2019 Feb;14(3):207–222. doi: 10.2217/fmb-2018-0279
  • Wu Z, Shao J, Ren H, et al. A Streptococcus suis LysM domain surface protein contributes to bacterial virulence. Vet Microbiol. 2016 May 1;187:64–69.
  • Savage DF, O’Connell JD 3rd, Miercke LJ, et al. Structural context shapes the aquaporin selectivity filter. Proc Natl Acad Sci U S A. 2010 Oct 5;107(40):17164–17169.
  • Hu Q, Tong H, Wang J, et al. A novel aquaporin subfamily imports oxygen and contributes to pneumococcal virulence by controlling the production and release of virulence factors. MBio. 2021 Aug 31;12(4):e0130921.
  • Tong H, Wang X, Dong Y, et al. A Streptococcus aquaporin acts as peroxiporin for efflux of cellular hydrogen peroxide and alleviation of oxidative stress. J Biol Chem. 2019 Mar 22;294(12):4583–4595.
  • Ma Z, Peng J, Yu D, et al. A streptococcal Fic domain-containing protein disrupts blood-brain barrier integrity by activating moesin in endothelial cells. PLOS Pathog. 2019 May;15(5):e1007737. doi: 10.1371/journal.ppat.1007737
  • Borgnia MJ, Agre P. Reconstitution and functional comparison of purified GlpF and AqpZ, the glycerol and water channels from Escherichia coli. Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2888–2893.
  • Doi Y. Glycerol metabolism and its regulation in lactic acid bacteria. Appl Microbiol Biotechnol. 2019 Jul;103(13):5079–5093. doi: 10.1007/s00253-019-09830-y
  • Zheng C, Ren S, Xu J, et al. Contribution of NADH oxidase to oxidative stress tolerance and virulence of Streptococcus suis serotype 2. Virulence. 2017 Jan 2;8(1):53–65.
  • Wu T, Zhao Z, Zhang L, et al. Trigger factor of Streptococcus suis is involved in stress tolerance and virulence. Microb Pathog. 2011 Jul-Aug;51(1–2):69–76. doi: 10.1016/j.micpath.2010.10.001
  • Shokolenko IN, Alexeyev MF, Robertson FM, et al. The expression of Exonuclease III from E. coli in mitochondria of breast cancer cells diminishes mitochondrial DNA repair capacity and cell survival after oxidative stress. DNA Repair (Amst). 2003 May 13;2(5):471–482.
  • Bhat SV, Booth SC, Vantomme EA, et al. Oxidative stress and metabolic perturbations in Escherichia coli exposed to sublethal levels of 2,4-dichlorophenoxyacetic acid. Chemosphere. 2015 Sep;135:453–461.
  • Tesse A, Grossini E, Tamma G, et al. Aquaporins as targets of dietary bioactive phytocompounds. Front Mol Biosci. 2018;5:30. doi: 10.3389/fmolb.2018.00030
  • Mitchell TJ, Dalziel CE. The biology of pneumolysin. Subcell Biochem. 2014;80:145–160.
  • Ishibashi K, Morishita Y, Tanaka Y. The evolutionary aspects of aquaporin family. Adv Exp Med Biol. 2017;969:35–50.
  • Bienert GP, Chaumont F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta. 2014 May;1840(5):1596–1604. doi: 10.1016/j.bbagen.2013.09.017
  • Siefritz F, Tyree MT, Lovisolo C, et al. PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell. 2002 Apr;14(4):869–876. doi: 10.1105/tpc.000901
  • Al Ghouleh I, Frazziano G, Rodriguez AI, et al. Aquaporin 1, Nox1, and Ask1 mediate oxidant-induced smooth muscle cell hypertrophy. Cardiovasc Res. 2013 Jan 1;97(1):134–142.
  • Medra?O-Fernandez I, Bestetti S, Bertolotti M, et al. Stress regulates aquaporin-8 permeability to impact cell growth and survival. Antioxid Redox Signal. 2016;24(18):1031–1044. doi: 10.1089/ars.2016.6636
  • Chen Z, Wang X, Yang F, et al. Molecular insights into hydrogen peroxide-sensing mechanism of the metalloregulator mntr in controlling bacterial resistance to oxidative stresses. J Biol Chem. 2017 Mar 31;292(13):5519–5531.
  • Bienert GP, Desguin B, Chaumont F, et al. Channel-mediated lactic acid transport: a novel function for aquaglyceroporins in bacteria. Biochem J. 2013 Sep 15;454(3):559–570.
  • Johri AK, Margarit I, Broenstrup M, et al. Transcriptional and proteomic profiles of group B Streptococcus type V reveal potential adherence proteins associated with high-level invasion. Infect Immun. 2007 Mar;75(3):1473–1483. doi: 10.1128/IAI.00638-06
  • Monniot C, Zebre AC, Ake FM, et al. Novel listerial glycerol dehydrogenase- and phosphoenolpyruvate-dependent dihydroxyacetone kinase system connected to the pentose phosphate pathway. J Bacteriol. 2012 Sep;194(18):4972–4982. doi: 10.1128/JB.00801-12