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Revisiting the role of VraTSR in Staphylococcus aureus response to cell wall targeting antibiotics

Fernandes PB, Reed P, Monteiro JM, Pinho MG

Accepted in J Bacteriol


DeepBacs: Bacterial image analysis using open-source deep learning approaches.

Spahn C, Laine RF, Pereira PM, Gómez-de-Mariscal E, von Chamier L, Conduit M, Pinho MG, Jacquemet G, Holden S, Heilemann M, Henriques R.

Commun Biol 2022; 5:688. doi: 10.1038/s42003-022-03634-z.


Encapsulation of the septal cell wall protects Streptococcus pneumoniae from its major peptidoglycan hydrolase and host defenses.

Figueiredo J, Henriques MX, Catalão MJ, Pinheiro S, Narciso AR, Mesquita F, Saraiva BM, Carido M, Cabanes D, Pinho MG, Filipe SR.

PLoS Pathogens 2022; 18: e1010516. doi: 10.1371/journal.ppat.1010516


Synthetic antimicrobial peptides as enhancers of the bacteriolytic action of staphylococcal phage endolysins.

Gouveia A, Pinto D, Veiga H, Antunes W, Pinho MG, São-José C.

Sci Rep 2022; 12:1245. doi: 10.1038/s41598-022-05361-1



eHooke: a tool for automated image analysis of spherical bacteria based on cell cycle progression.

Saraiva BM, Krippahl L, Filipe SR, Henriques R, Pinho MG.

Biol Imaging 2021; 1, e3. doi:10.1017/S2633903X21000027



Reassessment of the distinctive geometry of Staphylococcus aureus cell division.

Saraiva BM, Sorg M, Pereira A, Ferreira MJ, Caulat LC, Reichmann NT, Pinho MG.

Nat Commun 2020;11:4097.doi: 10.1038/s41467-020-17940-9.


Staphylococcus aureus cell growth and division are regulated by an amidase that trims peptides from uncrosslinked peptidoglycan.

Do T, Schaefer K, Santiago AG, Coe KA, Fernandes PB, Kahne D, Pinho MG, Walker S.

Nature Microbiology 2020; 5:291-303. doi: 10.1038/s41564-019-0632-1.



BPEI-Induced delocalization of PBP4 potentiates β-Lactams against MRSA.

Hill MA, Lam AK, Reed P, Harney MC, Wilson BA, Moen EL, Wright SN, Pinho MG, Rice CV.

Biochemistry. 2019; 58:3813-3822. doi: 10.1021/acs.biochem.9b00523


A comparative genomics approach for identifying host-range determinants in Streptococcus thermophilus bacteriophages.

Szymczak P, Rau M, Monteiro J, Pinho MG, Filipe SR, Vogensen F, Zeidan A and Janzen T.

Scientific Reports. 2019; 9:7991. doi: 10.1038/s41598-019-44481-z


SEDS-bPBP pairs direct lateral and septal peptidoglycan synthesis in Staphylococcus aureus.

Reichmann NT, Tavares AC, Saraiva BM, Jousselin A, Reed P, Pereira AR, Monteiro JM, VanNieuwenhze MS, Fernandes F, Pinho MG.

Nature Microbiology. 2019; 4:1368-1377.doi: 10.1038/s41564-019-0437-2.


The pentaglycine bridges of Staphylococcus aureus peptidoglycan are essential for cell integrity.

Monteiro JM, Covas G, Rausch D, Filipe SR, Schneider T, Sahl HG, Pinho MG.

Sci Rep. 2019; 9:5010. doi: 10.1038/s41598-019-41461-1.



PBP4 activity and its overexpression are necessary for PBP4-mediated high-level β-lactam resistance.

Basuino L, Jousselin A, Alexander JAN, Strynadka NCJ, Pinho MG, Chambers HF, Chatterjee SS.

J Antimicrob Chemother. 2018; 73:1177-1180. doi: 10.1093/jac/dkx531.


Peptidoglycan synthesis drives an FtsZ-treadmilling-independent step of cytokinesis.

Monteiro JM, Pereira AR, Reichmann NT, Saraiva BM, Fernandes PB, Veiga H, Tavares AC, Santos M, Ferreira MT, Macário V, VanNieuwenhze MS, Filipe SR, Pinho MG.

Nature. 2018; 554:528-532. doi: 10.1038/nature25506.



Synergy between ursolic and oleanolic acids from Vitellaria paradoxa leaf extract and β-lactams against Methicillin-Resistant Staphylococcus aureus: in vitro and in vivo activity and underlying mechanisms.

Catteau L, Reichmann NT, Olson J, Pinho MG, Nizet V, Van Bambeke F, Quetin-Leclercq J.

Molecules. 2017; 22: E2245. doi: 10.3390/molecules22122245.


The ClpXP protease is dispensable for degradation of unfolded proteins in Staphylococcus aureus.

Stahlhut SG, Alqarzaee AA, Jensen C, Fisker NS, Pereira AR, Pinho MG, Thomas VC, Frees D.

Sci Rep. 2017; 7:11739. doi: 10.1038/s41598-017-12122-y.


Role of SCCmec type in resistance to the synergistic activity of oxacillin and cefoxitin in MRSA.

Reichmann NT, Pinho MG.

Sci Rep. 2017; 7:6154. doi: 10.1038/s41598-017-06329-2.


A quinolinol-based small molecule with anti-MRSA activity that targets bacterial membrane and promotes fermentative metabolism.

Nair DR, Chen J, Monteiro JM, Josten M, Pinho MG, Sahl HG, Wu J, Cheung A.

J Antibiot. 2017; 70:1009-1019. doi: 10.1038/ja.2017.79.


Staphylococcus aureus requires at least one FtsK/SpoIIIE protein for correct chromosome segregation.

Veiga H, Pinho MG.

Mol Microbiol. 2017; 103:504-517. doi: 10.1111/mmi.13572.



FtsZ-Dependent Elongation of a Coccoid Bacterium.

Pereira AR, Hsin J, Król E, Tavares AC, Flores P, Hoiczyk E, Ng N, Dajkovic A, Brun YV, VanNieuwenhze MS, Roemer T, Carballido-Lopez R, Scheffers DJ, Huang KC, Pinho MG.

MBio. 2016 Sep 6;7(5). pii: e00908-16. doi: 10.1128/mBio.00908-16.


Analysis of Cell Wall Teichoic Acids in Staphylococcus aureus.

Covas G, Vaz F, Henriques G, Pinho MG, Filipe SR.

Methods Mol Biol. 2016;1440:201-13. doi: 10.1007/978-1-4939-3676-2_15.

Chemical Genetic Analysis and Functional Characterization of Staphylococcal Wall Teichoic Acid 2-Epimerases Reveals Unconventional Antibiotic Drug Targets.

Mann PA, Müller A, Wolff KA, Fischmann T, Wang H, Reed P, Hou Y, Li W, Müller CE, Xiao J, Murgolo N, Sher X, Mayhood T, Sheth PR, Mirza A, Labroli M, Xiao L, McCoy M, Gill CJ, Pinho MG, Schneider T, Roemer T.

PLoS Pathog. 2016 May 4;12(5):e1005585. doi: 10.1371/journal.ppat.1005585.

The SpoIIQ-SpoIIIAH complex of Clostridium difficile controls forespore engulfment and late stages of gene expression and spore morphogenesis.

Serrano M, Crawshaw AD, Dembek M, Monteiro JM, Pereira FC, Pinho MG, Fairweather NF, Salgado PS, Henriques AO.

Mol Microbiol. 2016 Apr;100(1):204-28. doi: 10.1111/mmi.13311.



The Staphylococcus aureus Chaperone PrsA Is a New Auxiliary Factor of Oxacillin Resistance Affecting Penicillin-Binding Protein 2A.

Jousselin A, Manzano C, Biette A, Reed P, Pinho MG, Rosato AE, Kelley WL, Renzoni A.

Antimicrob Agents Chemother. 2015 Dec 28;60(3):1656-66. doi: 10.1128/AAC.02333-15.

Antimicrobial Contact-Active Oligo(2-oxazoline)s-Grafted Surfaces for Fast Water Disinfection at the Point-of-Use.

Correia VG, Ferraria AM, Pinho MG, Aguiar-Ricardo A.

Biomacromolecules. 2015 Dec 14;16(12):3904-15. doi: 10.1021/acs.biomac.5b01243.


MreC and MreD Proteins Are Not Required for Growth of Staphylococcus aureus.

Tavares AC, Fernandes PB, Carballido-López R, Pinho MG.

PLoS One. 2015 Oct 15;10(10):e0140523. doi: 10.1371/journal.pone.0140523.


Cell shape dynamics during the staphylococcal cell cycle.

Monteiro JM, Fernandes PB, Vaz F, Pereira AR, Tavares AC, Ferreira MT, Pereira PM, Veiga H, Kuru E, VanNieuwenhze MS, Brun YV, Filipe SR, Pinho MG.

Nat Commun. 2015 Aug 17;6:8055. doi: 10.1038/ncomms9055.


An Activity-Based Probe for Studying Crosslinking in Live Bacteria.

Gautam S, Kim T, Shoda T, Sen S, Deep D, Luthra R, Ferreira MT, Pinho MG, Spiegel DA.

Angew Chem Int Ed Engl. 2015 Sep 1;54(36):10492-6. doi: 10.1002/anie.201503869.


Staphylococcus aureus Survives with a Minimal Peptidoglycan Synthesis Machine but Sacrifices Virulence and Antibiotic Resistance.

Reed P, Atilano ML, Alves R, Hoiczyk E, Sher X, Reichmann NT, Pereira PM, Roemer T, Filipe SR, Pereira-Leal JB, Ligoxygakis P, Pinho MG.

PLoS Pathog. 2015 May 7;11(5):e1004891. doi: 10.1371/journal.ppat.1004891.


Characterization of a novel small molecule that potentiates β-lactam activity against gram-positive and gram-negative pathogens.

Nair DR, Monteiro JM, Memmi G, Thanassi J, Pucci M, Schwartzman J, Pinho MG, Cheung AL.

Antimicrob Agents Chemother. 2015 Apr;59(4):1876-85. doi: 10.1128/AAC.04164-14.



Reduction of the peptidoglycan crosslinking causes a decrease in stiffness of the Staphylococcus aureus cell envelope.

Loskill P, Pereira PM, Jung P, Bischoff M, Herrmann M, Pinho MG, Jacobs K.

Biophys J. 2014 Sep 2;107(5):1082-9. doi: 10.1016/j.bpj.2014.07.029.


Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the Drosophila innate immune system.

Atilano ML, Pereira PM, Vaz F, Catalão MJ, Reed P, Grilo IR, Sobral RG, Ligoxygakis P, Pinho MG, Filipe SR.

Elife. 2014 Apr 1;3:e02277. doi: 10.7554/eLife.02277.


Differential localization of LTA synthesis proteins and their interaction with the cell division machinery in Staphylococcus aureus.

Reichmann NT, Piçarra Cassona C, Monteiro JM, Bottomley AL, Corrigan RM, Foster SJ, Pinho MG, Gründling A.

Mol Microbiol. 2014 Apr;92(2):273-86. doi: 10.1111/mmi.12551.



Murgocil is a highly bioactive staphylococcal-specific inhibitor of the peptidoglycan glycosyltransferase enzyme MurG.

Mann PA, Müller A, Xiao L, Pereira PM, Yang C, Ho Lee S, Wang H, Trzeciak J, Schneeweis J, Dos Santos MM, Murgolo N, She X, Gill C, Balibar CJ, Labroli M, Su J, Flattery A, Sherborne B, Maier R, Tan CM, Black T, Onder K, Kargman S, Monsma FJ Jr, Pinho MG, Schneider T, Roemer T.

ACS Chem Biol. 2013 Nov 15;8(11):2442-51. doi: 10.1021/cb400487f.


How to get (a)round: mechanisms controlling growth and division of coccoid bacteria.

Pinho MG, Kjos M, Veening JW.

Nat Rev Microbiol. 2013 Sep;11(9):601-14. doi: 10.1038/nrmicro3088. Review.


Auxiliary factors: a chink in the armor of MRSA resistance to β-lactam antibiotics.

Roemer T, Schneider T, Pinho MG.

Curr Opin Microbiol. 2013 Oct;16(5):538-48. doi: 10.1016/j.mib.2013.06.012. Review.

Effect of oxygen on glucose metabolism: utilization of lactate in Staphylococcus aureus as revealed by in vivo NMR studies.

Ferreira MT, Manso AS, Gaspar P, Pinho MG, Neves AR.


PLoS One. 2013;8(3):e58277. doi: 10.1371/journal.pone.0058277.

Anti-biofouling 3D porous systems: the blend effect of oxazoline-based oligomers on chitosan scaffolds.

Correia VG, Coelho M, Barroso T, Raje VP, Bonifácio VD, Casimiro T, Pinho MG, Aguiar-Ricardo A.

Biofouling. 2013;29(3):273-82. doi: 10.1080/08927014.2013.766172.


The Holliday junction resolvase RecU is required for chromosome segregation and DNA damage repair in Staphylococcus aureus.

Pereira AR, Reed P, Veiga H, Pinho MG.

BMC Microbiol. 2013 Jan 28;13:18. doi: 10.1186/1471-2180-13-18.


The Staphylococcus aureus Membrane Protein SA2056 Interacts with Peptidoglycan Synthesis Enzymes.

Quiblier C, Luczak-Kadlubowska A, Holdener E, Alborn D, Schneider T, Wiedemann I, Pinho MG, Sahl HG, Rohrer S, Berger-Bächi B, Senn MM.

Antibiotics (Basel). 2013 Jan 22;2(1):11-27. doi: 10.3390/antibiotics2010011.


Inhibition of WTA synthesis blocks the cooperative action of PBPs and sensitizes MRSA to β-lactams.

Farha MA, Leung A, Sewell EW, D'Elia MA, Allison SE, Ejim L, Pereira PM, Pinho MG, Wright GD, Brown ED.

ACS Chem Biol. 2013 Jan 18;8(1):226-33. doi: 10.1021/cb300413m.



Restoring methicillin-resistant Staphylococcus aureus susceptibility to β-lactam antibiotics.

Tan CM, Therien AG, Lu J, Lee SH, Caron A, Gill CJ, Lebeau-Jacob C, Benton-Perdomo L, Monteiro JM, Pereira PM, Elsen NL, Wu J, Deschamps K, Petcu M, Wong S, Daigneault E, Kramer S, Liang L, Maxwell E, Claveau D, Vaillancourt J, Skorey K, Tam J, Wang H, Meredith TC, Sillaots S, Wang-Jarantow L, Ramtohul Y, Langlois E, Landry F, Reid JC, Parthasarathy G, Sharma S, Baryshnikova A, Lumb KJ, Pinho MG, Soisson SM, Roemer T.

Sci Transl Med. 2012 Mar 21;4(126):126ra35. doi: 10.1126/scitranslmed.3003592.



EzrA contributes to the regulation of cell size in Staphylococcus aureus.

Jorge AM, Hoiczyk E, Gomes JP, Pinho MG.

PLoS One. 2011;6(11):e27542. doi: 10.1371/journal.pone.0027542.


New role of the disulfide stress effector YjbH in β-lactam susceptibility of Staphylococcus aureus.

Göhring N, Fedtke I, Xia G, Jorge AM, Pinho MG, Bertsche U, Peschel A.

Antimicrob Agents Chemother. 2011 Dec;55(12):5452-8. doi: 10.1128/AAC.00286-11.


Oxazoline-based antimicrobial oligomers: synthesis by CROP using supercritical CO2.

Correia VG, Bonifácio VD, Raje VP, Casimiro T, Moutinho G, da Silva CL, Pinho MG, Aguiar-Ricardo A.

Macromol Biosci. 2011 Aug 11;11(8):1128-37. doi: 10.1002/mabi.201100126.


Absence of nucleoid occlusion effector Noc impairs formation of orthogonal FtsZ rings during Staphylococcus aureus cell division.

Veiga H, Jorge AM, Pinho MG.

Mol Microbiol. 2011 Jun;80(5):1366-80. doi: 10.1111/j.1365-2958.2011.07651.x.


Monofunctional transglycosylases are not essential for Staphylococcus aureus cell wall synthesis.

Reed P, Veiga H, Jorge AM, Terrak M, Pinho MG.

J Bacteriol. 2011 May;193(10):2549-56. doi: 10.1128/JB.01474-10.



Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus.

Atilano ML, Pereira PM, Yates J, Reed P, Veiga H, Pinho MG, Filipe SR.

Proc Natl Acad Sci U S A. 2010 Nov 2;107(44):18991-6. doi: 10.1073/pnas.1004304107.


Insertion of epicatechin gallate into the cytoplasmic membrane of methicillin-resistant Staphylococcus aureus disrupts penicillin-binding protein (PBP) 2a-mediated beta-lactam resistance by delocalizing PBP2.

Bernal P, Lemaire S, Pinho MG, Mobashery S, Hinds J, Taylor PW.

J Biol Chem. 2010 Jul 30;285(31):24055-65. doi: 10.1074/jbc.M110.114793.


Fluorescent reporters for studies of cellular localization of proteins in Staphylococcus aureus.

Pereira PM, Veiga H, Jorge AM, Pinho MG.

Appl Environ Microbiol. 2010 Jul;76(13):4346-53. doi: 10.1128/AEM.00359-10.



Evidence for a dual role of PBP1 in the cell division and cell separation of Staphylococcus aureus.

Pereira SF, Henriques AO, Pinho MG, de Lencastre H, Tomasz A.

Mol Microbiol. 2009 May;72(4):895-904. doi: 10.1111/j.1365-2958.2009.06687.x.


Inactivation of the SauI type I restriction-modification system is not sufficient to generate Staphylococcus aureus strains capable of efficiently accepting foreign DNA.

Veiga H, Pinho MG.

Appl Environ Microbiol. 2009 May;75(10):3034-8. doi: 10.1128/AEM.01862-08.



Staphylococcus aureus PBP4 is essential for beta-lactam resistance in community-acquired methicillin-resistant strains.

Memmi G, Filipe SR, Pinho MG, Fu Z, Cheung A.

Antimicrob Agents Chemother. 2008 Nov;52(11):3955-66. doi: 10.1128/AAC.00049-08.


The different shapes of cocci.

Zapun A, Vernet T, Pinho MG.

FEMS Microbiol Rev. 2008 Mar;32(2):345-60. doi: 10.1111/j.1574-6976.2007.00098.x. Review.


Fluorescence ratio imaging microscopy shows decreased access of vancomycin to cell wall synthetic sites in vancomycin-resistant Staphylococcus aureus.

Pereira PM, Filipe SR, Tomasz A, Pinho MG.

Antimicrob Agents Chemother. 2007 Oct;51(10):3627-33.



Role of PBP1 in cell division of Staphylococcus aureus.

Pereira SF, Henriques AO, Pinho MG, de Lencastre H, Tomasz A.

J Bacteriol. 2007 May;189(9):3525-31.



Bacterial cell wall synthesis: new insights from localization studies.

Scheffers DJ, Pinho MG.

Microbiol Mol Biol Rev. 2005 Dec;69(4):585-607. Review.




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