The staphylococcus aureus chaperone PrsA is a new auxiliary factor of oxacillin resistance affecting penicillin-binding protein 2A

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 3, 2016, Pages 1656-1666

  Jousselin, Ambre ^a,b   Manzano, Caroline ^a   Biette, Alexandra ^a   Reed, Patricia ^b   Pinho, Mariana G ^b   Rosato, Adriana E ^c   Kelley, William L ^a   Renzoni, Adriana ^a  

^a University Hospital and Medical Faculty of Geneva   (Switzerland)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BACITRACIN; CEFACLOR; CEFOTAXIME; CEFOXITIN; CEFTAROLINE; CHAPERONE; CHLORAMPHENICOL; FOSFOMYCIN; KANAMYCIN; MESSENGER RNA; NALIDIXIC ACID; OXACILLIN; PENICILLIN BINDING PROTEIN 2A; PEPTIDOGLYCAN; PRSA PROTEIN; TETRACYCLINE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; LIPOPROTEIN; MECA PROTEIN, STAPHYLOCOCCUS AUREUS; MEMBRANE PROTEIN; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; PRSA PROTEIN, BACTERIA;

AMINO TERMINAL SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIOPHAGE; CARBOXY TERMINAL SEQUENCE; GENE DELETION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; WESTERN BLOTTING; BIOSYNTHESIS; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST; PROTEIN FOLDING;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; LIPOPROTEINS; MEMBRANE PROTEINS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; OXACILLIN; PENICILLIN-BINDING PROTEINS; PEPTIDOGLYCAN; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; PROTEIN FOLDING; RNA, MESSENGER;

EID: 84960158574     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02333-15     Document Type: Article

References (53)

1. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF. 2010. Communityassociated methicillin-resistant Staphylococcus aureus. Lancet 375:1557-1568. http://dx.doi.org/10.1016/S0140-6736 (09) 61999-1.
2. Viana D, Comos M, McAdam PR, Ward MJ, Selva L, Guinane CM, González-Muñoz BM, Tristan A, Foster SJ, Fitzgerald JR, Penadés JR. 2015. A single natural nucleotide mutation alters bacterial pathogen host tropism. Nat Genet 47:361-366. http://dx.doi.org/10.1038/ng.3219.
3. de Kraker ME, Davey PG, Grundmann H, group Bs. 2011. Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe. PLoS Med 8:e1001104. http://dx.doi.org/10.1371/journal.pmed.1001104.
4. Holland TL, Arnold C, Fowler VG. 2014. Clinical management of Staphylococcus aureus bacteremia: a review. JAMA 312:1330-1341. http://dx.doi.org/10.1001/jama.2014.9743.
5. Chambers HF, Deleo FR. 2009. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7:629-641. http://dx.doi.org/10.1038/nrmicro2200.
6. Gardete S, Tomasz A. 2014. Mechanisms of vancomycin resistance in Staphylococcus aureus. J Clin Invest 124:2836-2840. http://dx.doi.org/10.1172/JCI68834.
7. Gardete S, Kim C, Hartmann BM, Mwangi M, Roux CM, Dunman PM, Chambers HF, Tomasz A. 2012. Genetic pathway in acquisition and loss of vancomycin resistance in a methicillin-resistant Staphylococcus aureus (MRSA) strain of clonal type USA300. PLoS Pathog 8:e1002505. http://dx.doi.org/10.1371/journal.ppat.1002505.
8. Wang H, Gill CJ, Lee SH, Mann P, Zuck P, Meredith TC, Murgolo N, She X, Kales S, Liang L, Liu J, Wu J, Santa Maria J, Su J, Pan J, Hailey J, Mcguinness D, Tan CM, Flattery A, Walker S, Black T, Roemer T. 2013. Discovery of wall teichoic acid inhibitors as potential anti-MRSA β-lactam combination agents. Chem Biol 20:272-284. http://dx.doi.org/10.1016/j.chembiol.2012.11.013.
9. Jousselin A, Kelley WL, Barras C, Lew DP, Renzoni A. 2013. The Staphylococcus aureus thiol/oxidative stress global regulator Spx controls trfA, a gene implicated in cell wall antibiotic resistance. Antimicrob Agents Chemother 57:3283-3292. http://dx.doi.org/10.1128/AAC.00220-13.
10. Renzoni A, Andrey DO, Jousselin A, Barras C, Monod A, Vaudaux P, Lew D, Kelley WL. 2011. Whole-genome sequencing and complete genetic analysis reveals novel pathways to glycopeptide resistance in Staphylococcus aureus. PLoS One 6:e21577. http://dx.doi.org/10.1371/journal.pone.0021577.
11. Bæk KT, Gründling A, Mogensen RG, Thøgersen L, Petersen A, Paulander W, Frees D. 2014. β-Lactam resistance in methicillin-resistant Staphylococcus aureus USA300 is increased by inactivation of the ClpXP protease. Antimicrob Agents Chemother 58:4593-4603. http://dx.doi.org/10.1128/AAC.02802-14.
12. Jousselin A, Renzoni A, Andrey DO, Monod A, Lew DP, Kelley WL. 2012. The posttranslocational chaperone lipoprotein PrsA is involved in both glycopeptide and oxacillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 56:3629-3640. http://dx.doi.org/10.1128/AAC.06264-11.
13. Kontinen VP, Sarvas M. 1988. Mutants of Bacillus subtilis defective in protein export. J Gen Microbiol 134:2333-2344.
14. Kontinen VP, Saris P, Sarvas M. 1991. A gene (prsA) of Bacillus subtilis involved in a novel, late stage of protein export. Mol Microbiol 5:1273-1283. http://dx.doi.org/10.1111/j.1365-2958.1991.tb01901.x.
15. Hyyryläinen HL, Marciniak BC, Dahncke K, Pietiäinen M, Courtin P, Vitikainen M, Seppala R, Otto A, Becher D, Chapot-Chartier MP, Kuipers OP, Kontinen VP. 2010. Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis. Mol Microbiol 77:108-127. http://dx.doi.org/10.1111/j.1365-2958.2010.07188.x.
16. Guo L, Wu T, Hu W, He X, Sharma S, Webster P, Gimzewski JK, Zhou X, Lux R, Shi W. 2013. Phenotypic characterization of the foldase homologue PrsA in Streptococcus mutans. Mol Oral Microbiol 28:154-165. http://dx.doi.org/10.1111/omi.12014.
17. Alonzo F, Xayarath B, Whisstock JC, Freitag NE. 2011. Functional analysis of the Listeria monocytogenes secretion chaperone PrsA2 and its multiple contributions to bacterial virulence. Mol Microbiol 80:1530-1548. http://dx.doi.org/10.1111/j.1365-2958.2011.07665.x.
18. Stoll H, Dengjel J, Nerz C, Götz F. 2005. Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect Immun 73:2411-2423. http://dx.doi.org/10.1128/IAI.73.4.2411-2423.2005.
19. Heikkinen O, Seppala R, Tossavainen H, Heikkinen S, Koskela H, Permi P, Kilpeläinen I. 2009. Solution structure of the parvulin-type PPIase domain of Staphylococcus aureus PrsA: implications for the catalytic mechanism of parvulins. BMC Struct Biol 9:17. http://dx.doi.org/10.1186/1472-6807-9-17.
20. Vitikainen M, Lappalainen I, Seppala R, Antelmann H, Boer H, Taira S, Savilahti H, Hecker M, Vihinen M, Sarvas M, Kontinen VP. 2004. Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J Biol Chem 279:19302-19314. http://dx.doi.org/10.1074/jbc. M400861200.
21. Schallenberger MA, Niessen S, Shao C, Fowler BJ, Romesberg FE. 2012. Type I signal peptidase and protein secretion in Staphylococcus aureus. J Bacteriol 194:2677-2686. http://dx.doi.org/10.1128/JB.00064-12.
22. Craney A, Romesberg FE. 2015. A putative cro-like repressor contributes to arylomycin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 59:3066-3074. http://dx.doi.org/10.1128/AAC.04597-14.
23. Hyyryläinen HL, Sarvas M, Kontinen VP. 2005. Transcriptome analysis of the secretion stress response of Bacillus subtilis. Appl Microbiol Biotechnol 67:389-396. http://dx.doi.org/10.1007/s00253-005-1898-1.
24. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counterselection. Plasmid 55:58-63. http://dx.doi.org/10.1016/j.plasmid.2005.05.005.
25. Göhring N, Fedtke I, Xia G, Jorge AM, Pinho MG, Bertsche U, Peschel A. 2011. New role of the disulfide stress effector YjbH in β-lactam susceptibility of Staphylococcus aureus. Antimicrob Agents Chemother 55:5452-5458. http://dx.doi.org/10.1128/AAC.00286-11.
26. Tavares AC, Fernandes PB, Carballido-López R, Pinho MG. 2015. MreC and MreD Proteins are not required for growth of Staphylococcus aureus. PLoS One 10:e0140523. http://dx.doi.org/10.1371/journal.pone.0140523.
27. Otero LH, Rojas-Altuve A, Llarrull LI, Carrasco-López C, Kumarasiri M, Lastochkin E, Fishovitz J, Dawley M, Hesek D, Lee M, Johnson JW, Fisher JF, Chang M, Mobashery S, Hermoso JA. 2013. How allosteric control of Staphylococcus aureus penicillin-binding protein 2a enables methicillin resistance and physiological function. Proc Natl Acad SciUSA 110:16808-16813. http://dx.doi.org/10.1073/pnas.1300118110.
28. Arêde P, Milheiriço C, de Lencastre H, Oliveira DC. 2012. The antirepressor MecR2 promotes the proteolysis of the mecA repressor and enables optimal expression of β-lactam resistance in MRSA. PLoS Pathog 8:e1002816. http://dx.doi.org/10.1371/journal.ppat.1002816.
29. Drouault S, Anba J, Bonneau S, Bolotin A, Ehrlich SD, Renault P. 2002. The peptidyl-prolyl isomerase motif is lacking in PmpA, the PrsA-like protein involved in the secretion machinery of Lactococcus lactis. Appl Environ Microbiol 68:3932-3942. http://dx.doi.org/10.1128/AEM.68.8.3932-3942.2002.
30. Pereira SF, Henriques AO, Pinho MG, de Lencastre H, Tomasz A. 2009. Evidence for a dual role of PBP1 in the cell division and cell separation of Staphylococcus aureus. Mol Microbiol 72:895-904. http://dx.doi.org/10.1111/j.1365-2958.2009.06687.x.
31. Pinho MG, de Lencastre H, Tomasz A. 2001. An acquired and a native penicillin-binding protein cooperate in building the cell wall of drugresistant staphylococci. Proc Natl Acad Sci U S A 98:10886-10891. http://dx.doi.org/10.1073/pnas.191260798.
32. Atilano ML, Pereira PM, Yates J, Reed P, Veiga H, Pinho MG, Filipe SR. 2010. Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. Proc Natl Acad Sci U S A 107:18991-18996. http://dx.doi.org/10.1073/pnas.1004304107.
33. Lovering AL, de Castro LH, Lim D, Strynadka NC. 2007. Structural insight into the transglycosylation step of bacterial cell wall biosynthesis. Science 315:1402-1405. http://dx.doi.org/10.1126/science.1136611.
34. Navratna V, Nadig S, Sood V, Prasad K, Arakere G, Gopal B. 2010. Molecular basis for the role of Staphylococcus aureus penicillin-binding protein 4 in antimicrobial resistance. J Bacteriol 192:134-144. http://dx.doi.org/10.1128/JB.00822-09.
35. Yoshida H, Kawai F, Obayashi E, Akashi S, Roper DI, Tame JR, Park SY. 2012. Crystal structures of penicillin-binding protein 3 (PBP3) from methicillin-resistant Staphylococcus aureus in the apo and cefotaximebound forms. J Mol Biol 423:351-364. http://dx.doi.org/10.1016/j.jmb.2012.07.012.
36. Huber J, Donald RG, Lee SH, Jarantow LW, Salvatore MJ, Meng X, Painter R, Onishi RH, Occi J, Dorso K, Young K, Park YW, Skwish S, Szymonifka MJ, Waddell TS, Miesel L, Phillips JW, Roemer T. 2009. Chemical genetic identification of peptidoglycan inhibitors potentiating carbapenem activity against methicillin-resistant Staphylococcus aureus. Chem Biol 16:837-848. http://dx.doi.org/10.1016/j.chembiol.2009.05.012.
37. Lee SH, Jarantow LW, Wang H, Sillaots S, Cheng H, Meredith TC, Thompson J, Roemer T. 2011. Antagonism of chemical genetic interaction networks resensitize MRSA to β-lactam antibiotics. Chem Biol 18:1379-1389. http://dx.doi.org/10.1016/j.chembiol.2011.08.015.
38. Aiba Y, Katayama Y, Hishinuma T, Murakami-Kuroda H, Cui L, Hiramatsu K. 2013. Mutation of RNA polymerase β-subunit gene promotes heterogeneous-to-homogeneous conversion of β-lactam resistance in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 57:4861-4871. http://dx.doi.org/10.1128/AAC.00720-13.
39. Kim C, Mwangi M, Chung M, Milheiriço C, Milheirço C, de Lencastre H, Tomasz A. 2013. The mechanism of heterogeneous beta-lactam resistance in MRSA: key role of the stringent stress response. PLoS One 8:e82814. http://dx.doi.org/10.1371/journal.pone.0082814.
40. Vitikainen M, Pummi T, Airaksinen U, Wahlström E, Wu H, Sarvas M, Kontinen VP. 2001. Quantitation of the capacity of the secretion apparatus and requirement for PrsA in growth and secretion of alpha-amylase in Bacillus subtilis. J Bacteriol 183:1881-1890. http://dx.doi.org/10.1128/JB.183.6.1881-1890.2001.
41. Wu SC, Ye R, Wu XC, Ng SC, Wong SL. 1998. Enhanced secretory production of a single-chain antibody fragment from Bacillus subtilis by coproduction of molecular chaperones. J Bacteriol 180:2830-2835.
42. Sibbald MJ, Ziebandt AK, Engelmann S, Hecker M, de Jong A, Harmsen HJ, Raangs GC, Stokroos I, Arends JP, Dubois JY, van Dijl JM. 2006. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol Mol Biol Rev 70:755-788. http://dx.doi.org/10.1128/MMBR.00008-06.
43. Ravipaty S, Reilly JP. 2010. Comprehensive characterization of methicillinresistant Staphylococcus aureus subsp. aureus COL secretome by two-dimensional liquid chromatography and mass spectrometry. Mol Cell Proteomics 9:1898-1919. http://dx.doi.org/10.1074/mcp. M900494-MCP200.
44. Enany S, Yoshida Y, Magdeldin S, Zhang Y, Bo X, Yamamoto T. 2012. Extensive proteomic profiling of the secretome of European community acquired methicillin resistant Staphylococcus aureus clone. Peptides 37:128-137. http://dx.doi.org/10.1016/j.peptides.2012.06.011.
45. Quiblier C, Seidl K, Roschitzki B, Zinkernagel AS, Berger-Bächi B, Senn MM. 2013. Secretome analysis defines the major role of SecDF in Staphylococcus aureus virulence. PLoS One 8:e63513. http://dx.doi.org/10.1371/journal.pone.0063513.
46. Hirokawa T, Boon-Chieng S, Mitaku S. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378-379. http://dx.doi.org/10.1093/bioinformatics/14.4.378.
47. Boyle-Vavra S, Yin S, Daum RS. 2006. The VraS/VraR two-component regulatory system required for oxacillin resistance in communityacquired methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett 262:163-171. http://dx.doi.org/10.1111/j.1574-6968.2006.00384.x.
48. Cahoon LA, Freitag NE. 2015. Identification of conserved and speciesspecific functions of the Listeria monocytogenes PrsA2 secretion chaperone. Infect Immun 83:4028-4041. http://dx.doi.org/10.1128/IAI.00504-15.
49. Kreiswirth BN, Löfdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS, Novick RP. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712. http://dx.doi.org/10.1038/305709a0.
50. Dyke KG, Jevons MP, Parker MT. 1966. Penicillinase production and intrinsic resistance to penicillins in Staphylococcus aureus. Lancet i:835-838.
51. Lee CY, Buranen SL, Ye ZH. 1991. Construction of single-copy integration vectors for Staphylococcus aureus. Gene 103:101-105. http://dx.doi.org/10.1016/0378-1119 (91) 90399-V.
52. Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y, Hori S, Fukuchi Y, Kobayashi I. 1997. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 350:1670-1673. http://dx.doi.org/10.1016/S0140-6736 (97) 07324-8.
53. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, Kuroda H, Cui L, Yamamoto K, Hiramatsu K. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819-1827. http://dx.doi.org/10.1016/S0140-6736 (02) 08713-5.