The first histidine triad motif of PhtD is critical for zinc homeostasis in Streptococcus pneumoniae

Infection and Immunity

Volumn 84, Issue 2, 2016, Pages 407-415

  Eijkelkamp, Bart A ^a   Pederick, Victoria G ^a   Plumptre, Charles D ^a   Harvey, Richard M ^a   Hughes, Catherine E ^a   Paton, James C ^a   McDevitt, Christopher A ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE; MUTANT PROTEIN; POLYHISTIDINE; POLYHISTIDINE TRIAD D; UNCLASSIFIED DRUG; ZINC ION; BACTERIAL PROTEIN; ZINC;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; HISTIDINE TRIAD MOTIF; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; STREPTOCOCCUS PNEUMONIAE; ZINC HOMEOSTASIS; ANIMAL; BACTERIAL LOAD; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; HUMAN; METABOLISM; MUTATION; PATHOGENICITY; REPRODUCTIVE FITNESS;

AMINO ACID MOTIFS; ANIMALS; BACTERIAL LOAD; BACTERIAL PROTEINS; GENETIC FITNESS; HISTIDINE; HOMEOSTASIS; HUMANS; MICE; MUTATION; STREPTOCOCCUS PNEUMONIAE; ZINC;

EID: 84957676566     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01082-15     Document Type: Article

References (27)

1. Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, O'Brien KL, Campbell H, Black RE. 2013. Global burden of childhood pneumonia and diarrhoea. Lancet 381:1405-1416. http://dx.doi.org/10.1016/S0140-6736(13)60222-6.
2. Bayle L, Chimalapati S, Schoehn G, Brown J, Vernet T, Durmort C. 2011 Zinc uptake by Streptococcus pneumoniae depends on both AdcA and AdcAII and is essential for normal bacterial morphology and virulence. Mol Microbiol 82:904-916. http://dx.doi.org/10.1111/j.1365-2958.2011.07862.x.
3. Lewis VG, Ween MP, McDevitt CA. 2012. The role of ATP-binding cassette transporters in bacterial pathogenicity. Protoplasma 249:919-942 http://dx.doi.org/10.1007/s00709-011-0360-8.
4. Plumptre CD, Eijkelkamp BA, Morey JR, Behr F, Counago RM, Ogunniyi AD, Kobe B, O'Mara ML, Paton JC, McDevitt CA. 2014. AdcA and AdcAII employ distinct zinc acquisition mechanisms and contribute additively to zinc homeostasis in Streptococcus pneumoniae. Mol Microbiol 91:834-851. http://dx.doi.org/10.1111/mmi.12504.
5. Plumptre CD, Hughes CE, Harvey RM, Eijkelkamp BA, McDevitt CA, Paton JC. 2014. Overlapping functionality of the Pht proteins in zinc homeostasis of Streptococcus pneumoniae. Infect Immun 82:4315-4324. http://dx.doi.org/10.1128/IAI.02155-14.
6. Plumptre CD, Ogunniyi AD, Paton JC. 2012. Polyhistidine triad proteins of pathogenic streptococci. Trends Microbiol 20:485-493. http://dx.doi.org/10.1016/j.tim.2012.06.004.
7. Plumptre CD, Ogunniyi AD, Paton JC. 2013. Surface association of Pht proteins of Streptococcus pneumoniae. Infect Immun 81:3644-3651. http://dx.doi.org/10.1128/IAI.00562-13.
8. Loisel E, Chimalapati S, Bougault C, Imberty A, Gallet B, Di Guilmi AM, Brown J, Vernet T, Durmort C. 2011. Biochemical characterization of the histidine triad protein PhtD as a cell surface zinc-binding protein of pneumococcus. Biochemistry 50:3551-3558. http://dx.doi.org/10.1021/bi200012f.
9. Godfroid F, Hermand P, Verlant V, Denoel P, Poolman JT. 2011. Preclinical evaluation of the Pht proteins as potential cross-protective pneumococcal vaccine antigens. Infect Immun 79:238-245. http://dx.doi.org/10.1128/IAI.00378-10.
10. Prymula R, Pazdiora P, Traskine M, Ruggeberg JU, Borys D. 2014. Safety and immunogenicity of an investigational vaccine containing two common pneumococcal proteins in toddlers: a phase II randomized clinical trial. Vaccine 32:3025-3034. http://dx.doi.org/10.1016/j.vaccine.2014.03.066.
11. Plumptre CD, Ogunniyi AD, Paton JC. 2013. Vaccination against Streptococcus pneumoniae using truncated derivatives of polyhistidine triad protein D. PLoS One 8:e78916. http://dx.doi.org/10.1371/journal.pone.0078916.
12. Ferreira DM, Jambo KC, Gordon SB. 2011. Experimental human pneumococcal carriage models for vaccine research. Trends Microbiol 19:464-470 http://dx.doi.org/10.1016/j.tim.2011.06.003.
13. Pauksens K, Nilsson AC, Caubet M, Pascal TG, Van Belle P, Poolman JT, Vandepapeliere PG, Verlant V, Vink PE. 2014. Randomized controlled study of the safety and immunogenicity of pneumococcal vaccine formulations containing PhtD and detoxified pneumolysin with alum or adjuvant system AS02V in elderly adults. Clin Vaccine Immunol 21:651-660 http://dx.doi.org/10.1128/CVI.00807-13.
14. Rioux S, Neyt C, Di Paolo E, Turpin L, Charland N, Labbe S, Mortier MC, Mitchell TJ, Feron C, Martin D, Poolman JT. 2011. Transcriptional regulation, occurrence and putative role of the Pht family of Streptococcus pneumoniae. Microbiology 157:336-348. http://dx.doi.org/10.1099/mic.0.042184-0.
15. Bersch B, Bougault C, Roux L, Favier A, Vernet T, Durmort C. 2013. New insights into histidine triad proteins: solution structure of a Streptococcus pneumoniae PhtD domain and zinc transfer to AdcAII. PLoS One 8:e81168. http://dx.doi.org/10.1371/journal.pone.0081168.
16. Ilari A, Alaleona F, Tria G, Petrarca P, Battistoni A, Zamparelli C, Verzili D, Falconi M, Chiancone E. 2014. The Salmonella enterica ZinT structure, zinc affinity and interaction with the high-affinity uptake protein ZnuA provide insight into the management of periplasmic zinc. Biochim Biophys Acta 1840:535-544. http://dx.doi.org/10.1016/j.bbagen.2013.10.010.
17. Riboldi-Tunnicliffe A, Isaacs NW, Mitchell TJ. 2005. 1.2 Angstroms crystal structure of the S. pneumoniae PhtA histidine triad domain a novel zinc binding fold. FEBS Lett 579:5353-5360. http://dx.doi.org/10.1016/j.febslet.2005.08.066.
18. 2+-dependent repressor AdcR and inhibit complement deposition through the recruitment of complement factor H. FASEB J 23:731-738 http://dx.doi.org/10.1096/fj.08-119537.
19. McDevitt CA, Ogunniyi AD, Valkov E, Lawrence MC, Kobe B, McEwan AG, Paton JC. 2011. A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog 7:e1002357. http://dx.doi.org/10.1371/journal.ppat.1002357.
20. Begg SL, Eijkelkamp BA, Luo Z, Counago RM, Morey JR, Maher MJ, Ong CL, McEwan AG, Kobe B, O'Mara ML, Paton JC, McDevitt CA. 2015 Dysregulation of transition metal ion homeostasis is the molecular basis for cadmium toxicity in Streptococcus pneumoniae. Nat Commun 6:6418. http://dx.doi.org/10.1038/ncomms7418.
21. Eijkelkamp BA, Morey JR, Ween MP, Ong CL, McEwan AG, Paton JC, McDevitt CA. 2014. Extracellular zinc competitively inhibits manganese uptake and compromises oxidative stress management in Streptococcus pneumoniae. PLoS One 9:e89427. http://dx.doi.org/10.1371/journal.pone.0089427.
22. Clementi EA, Marks LR, Roche-Hakansson H, Hakansson AP. 2014. Monitoring changes in membrane polarity, membrane integrity, and intracellular ion concentrations in Streptococcus pneumoniae using fluorescent dyes. J Vis Exp 2014:e51008. http://dx.doi.org/10.3791/51008.
23. Adamou JE, Heinrichs JH, Erwin AL, Walsh W, Gayle T, Dormitzer M, Dagan R, Brewah YA, Barren P, Lathigra R, Langermann S, Koenig S, Johnson S. 2001. Identification and characterization of a novel family of pneumococcal proteins that are protective against sepsis. Infect Immun 69:949-958. http://dx.doi.org/10.1128/IAI.69.2.949-958.2001.
24. Beghetto E, Gargano N, Ricci S, GarufiG, Peppoloni S, Montagnani F, Oggioni M, Pozzi G, Felici F. 2006. Discovery of novel Streptococcus pneumoniae antigens by screening a whole-genome lambda-display library. FEMS Microbiol Lett 262:14-21. http://dx.doi.org/10.1111/j.1574-6968.2006.00360.x.
25. 2+ limitation and the repressor/activator function of AdcR. Metallomics 3:609-618. http://dx.doi.org/10.1039/c1mt00030f.
26. Kallio A, Sepponen K, Hermand P, Denoel P, Godfroid F, Melin M. 2014 Role of Pht proteins in attachment of Streptococcus pneumoniae to respiratory epithelial cells. Infect Immun 82:1683-1691. http://dx.doi.org/10.1128/IAI.00699-13.
27. Melin M, Di Paolo E, Tikkanen L, Jarva H, Neyt C, Kayhty H, Meri S, Poolman J, Vakevainen M. 2010. Interaction of pneumococcal histidine triad proteins with human complement. Infect Immun 78:2089-2098. http://dx.doi.org/10.1128/IAI.00811-09.