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Type VII Secretion Substrates of Pathogenic Mycobacteria Are Processed by a Surface Protease.

Burggraaf MJ, Speer A, Meijers AS, Ummels R, van der Sar AM, Korotkov KV, Bitter W, Kuijl C.

MBio. 2019 Oct 29;10(5). pii: e01951-19. doi: 10.1128/mBio.01951-19.


Optimization of secretion and surface localization of heterologous OVA protein in mycobacteria by using LipY as a carrier.

Burggraaf MJ, Ates LS, Speer A, van der Kuij K, Kuijl C, Bitter W.

Microb Cell Fact. 2019 Mar 6;18(1):44. doi: 10.1186/s12934-019-1093-1.


Role of Mycobacterium avium lysate INF-γ, IL-17, and IL-2 ELISPOT assays in diagnosing nontuberculous mycobacteria lymphadenitis in children.

Della Bella C, Venturini E, Devente S, Piccini P, Tapinassi S, Bianchi L, Grassi A, Benagiano M, Alnwaisri HFM, Montagnani C, Chiappini E, Bitter W, D'Elios MM, de Martino M, Galli L.

Eur J Clin Microbiol Infect Dis. 2019 Jun;38(6):1113-1122. doi: 10.1007/s10096-019-03506-1. Epub 2019 Mar 5.


Function, essentiality, and expression of cytochrome P450 enzymes and their cognate redox partners in Mycobacterium tuberculosis: are they drug targets?

Ortega Ugalde S, Boot M, Commandeur JNM, Jennings P, Bitter W, Vos JC.

Appl Microbiol Biotechnol. 2019 May;103(9):3597-3614. doi: 10.1007/s00253-019-09697-z. Epub 2019 Feb 27. Review.


Protease domain and transmembrane domain of the type VII secretion mycosin protease determine system-specific functioning in mycobacteria.

van Winden VJC, Damen MPM, Ummels R, Bitter W, Houben ENG.

J Biol Chem. 2019 Mar 29;294(13):4806-4814. doi: 10.1074/jbc.RA118.007090. Epub 2019 Jan 28.


Integrated transcriptomic and proteomic analysis of pathogenic mycobacteria and their esx-1 mutants reveal secretion-dependent regulation of ESX-1 substrates and WhiB6 as a transcriptional regulator.

Abdallah AM, Weerdenburg EM, Guan Q, Ummels R, Borggreve S, Adroub SA, Malas TB, Naeem R, Zhang H, Otto TD, Bitter W, Pain A.

PLoS One. 2019 Jan 23;14(1):e0211003. doi: 10.1371/journal.pone.0211003. eCollection 2019.


Fluorescent Benzothiazinone Analogues Efficiently and Selectively Label Dpre1 in Mycobacteria and Actinobacteria.

Sommer R, Neres J, Piton J, Dhar N, van der Sar A, Mukherjee R, Laroche T, Dyson PJ, McKinney JD, Bitter W, Makarov V, Cole ST.

ACS Chem Biol. 2018 Nov 16;13(11):3184-3192. doi: 10.1021/acschembio.8b00790. Epub 2018 Oct 25.


Linking cytochrome P450 enzymes from Mycobacterium tuberculosis to their cognate ferredoxin partners.

Ortega Ugalde S, de Koning CP, Wallraven K, Bruyneel B, Vermeulen NPE, Grossmann TN, Bitter W, Commandeur JNM, Vos JC.

Appl Microbiol Biotechnol. 2018 Nov;102(21):9231-9242. doi: 10.1007/s00253-018-9299-4. Epub 2018 Aug 22.


EspH is a hypervirulence factor for Mycobacterium marinum and essential for the secretion of the ESX-1 substrates EspE and EspF.

Phan TH, van Leeuwen LM, Kuijl C, Ummels R, van Stempvoort G, Rubio-Canalejas A, Piersma SR, Jiménez CR, van der Sar AM, Houben ENG, Bitter W.

PLoS Pathog. 2018 Aug 13;14(8):e1007247. doi: 10.1371/journal.ppat.1007247. eCollection 2018 Aug.


RD5-mediated lack of PE_PGRS and PPE-MPTR export in BCG vaccine strains results in strong reduction of antigenic repertoire but little impact on protection.

Ates LS, Sayes F, Frigui W, Ummels R, Damen MPM, Bottai D, Behr MA, van Heijst JWJ, Bitter W, Majlessi L, Brosch R.

PLoS Pathog. 2018 Jun 18;14(6):e1007139. doi: 10.1371/journal.ppat.1007139. eCollection 2018 Jun.


Mycobacteria employ two different mechanisms to cross the blood-brain barrier.

van Leeuwen LM, Boot M, Kuijl C, Picavet DI, van Stempvoort G, van der Pol SMA, de Vries HE, van der Wel NN, van der Kuip M, van Furth AM, van der Sar AM, Bitter W.

Cell Microbiol. 2018 Sep;20(9):e12858. doi: 10.1111/cmi.12858. Epub 2018 May 30.


Accelerating Early Antituberculosis Drug Discovery by Creating Mycobacterial Indicator Strains That Predict Mode of Action.

Boot M, Commandeur S, Subudhi AK, Bahira M, Smith TC 2nd, Abdallah AM, van Gemert M, Lelièvre J, Ballell L, Aldridge BB, Pain A, Speer A, Bitter W.

Antimicrob Agents Chemother. 2018 Jun 26;62(7). pii: e00083-18. doi: 10.1128/AAC.00083-18. Print 2018 Jul.


The novel antibiotic rhodomyrtone traps membrane proteins in vesicles with increased fluidity.

Saeloh D, Tipmanee V, Jim KK, Dekker MP, Bitter W, Voravuthikunchai SP, Wenzel M, Hamoen LW.

PLoS Pathog. 2018 Feb 16;14(2):e1006876. doi: 10.1371/journal.ppat.1006876. eCollection 2018 Feb.


Environmental Mycobacterium avium subsp. hominissuis have a higher probability to act as a recipient in conjugation than clinical strains.

Shoulah SA, Oschmann AM, Selim A, Semmler T, Schwarz C, Kamal E, Hamouda F, Galila E, Bitter W, Lewin A.

Plasmid. 2018 Jan;95:28-35. doi: 10.1016/j.plasmid.2018.01.003. Epub 2018 Jan 16.


Mutations in ppe38 block PE_PGRS secretion and increase virulence of Mycobacterium tuberculosis.

Ates LS, Dippenaar A, Ummels R, Piersma SR, van der Woude AD, van der Kuij K, Le Chevalier F, Mata-Espinosa D, Barrios-Payán J, Marquina-Castillo B, Guapillo C, Jiménez CR, Pain A, Houben ENG, Warren RM, Brosch R, Hernández-Pando R, Bitter W.

Nat Microbiol. 2018 Feb;3(2):181-188. doi: 10.1038/s41564-017-0090-6. Epub 2018 Jan 15.


Cell envelope stress in mycobacteria is regulated by the novel signal transduction ATPase IniR in response to trehalose.

Boot M, van Winden VJC, Sparrius M, van de Weerd R, Speer A, Ummels R, Rustad T, Sherman DR, Bitter W.

PLoS Genet. 2017 Dec 27;13(12):e1007131. doi: 10.1371/journal.pgen.1007131. eCollection 2017 Dec.


Engineering a self-sufficient Mycobacterium tuberculosis CYP130 by gene fusion with the reductase-domain of CYP102A1 from Bacillus megaterium.

Ortega Ugalde S, Luirink RA, Geerke DP, Vermeulen NPE, Bitter W, Commandeur JNM.

J Inorg Biochem. 2018 Mar;180:47-53. doi: 10.1016/j.jinorgbio.2017.12.003. Epub 2017 Dec 7.


A fluorescence-based reporter for monitoring expression of mycobacterial cytochrome bd in response to antibacterials and during infection.

Boot M, Jim KK, Liu T, Commandeur S, Lu P, Verboom T, Lill H, Bitter W, Bald D.

Sci Rep. 2017 Sep 6;7(1):10665. doi: 10.1038/s41598-017-10944-4.


New Insights into the Regulation of Cell-Surface Signaling Activity Acquired from a Mutagenesis Screen of the Pseudomonas putida IutY Sigma/Anti-Sigma Factor.

Bastiaansen KC, Civantos C, Bitter W, Llamas MA.

Front Microbiol. 2017 May 2;8:747. doi: 10.3389/fmicb.2017.00747. eCollection 2017.


Structure of the mycobacterial ESX-5 type VII secretion system membrane complex by single-particle analysis.

Beckham KS, Ciccarelli L, Bunduc CM, Mertens HD, Ummels R, Lugmayr W, Mayr J, Rettel M, Savitski MM, Svergun DI, Bitter W, Wilmanns M, Marlovits TC, Parret AH, Houben EN.

Nat Microbiol. 2017 Apr 10;2:17047. doi: 10.1038/nmicrobiol.2017.47.


Recombinant BCG Expressing ESX-1 of Mycobacterium marinum Combines Low Virulence with Cytosolic Immune Signaling and Improved TB Protection.

Gröschel MI, Sayes F, Shin SJ, Frigui W, Pawlik A, Orgeur M, Canetti R, Honoré N, Simeone R, van der Werf TS, Bitter W, Cho SN, Majlessi L, Brosch R.

Cell Rep. 2017 Mar 14;18(11):2752-2765. doi: 10.1016/j.celrep.2017.02.057.


Identification of a substrate domain that determines system specificity in mycobacterial type VII secretion systems.

Phan TH, Ummels R, Bitter W, Houben EN.

Sci Rep. 2017 Feb 16;7:42704. doi: 10.1038/srep42704.


Mycosins Are Required for the Stabilization of the ESX-1 and ESX-5 Type VII Secretion Membrane Complexes.

van Winden VJ, Ummels R, Piersma SR, Jiménez CR, Korotkov KV, Bitter W, Houben EN.

MBio. 2016 Oct 18;7(5). pii: e01471-16. doi: 10.1128/mBio.01471-16.


Infection of zebrafish embryos with live fluorescent Streptococcus pneumoniae as a real-time pneumococcal meningitis model.

Jim KK, Engelen-Lee J, van der Sar AM, Bitter W, Brouwer MC, van der Ende A, Veening JW, van de Beek D, Vandenbroucke-Grauls CM.

J Neuroinflammation. 2016 Aug 19;13(1):188. doi: 10.1186/s12974-016-0655-y.


iniBAC induction Is Vitamin B12- and MutAB-dependent in Mycobacterium marinum.

Boot M, Sparrius M, Jim KK, Commandeur S, Speer A, van de Weerd R, Bitter W.

J Biol Chem. 2016 Sep 16;291(38):19800-12. doi: 10.1074/jbc.M116.724088. Epub 2016 Jul 29.


The ESX-5 System of Pathogenic Mycobacteria Is Involved In Capsule Integrity and Virulence through Its Substrate PPE10.

Ates LS, van der Woude AD, Bestebroer J, van Stempvoort G, Musters RJ, Garcia-Vallejo JJ, Picavet DI, Weerd Rv, Maletta M, Kuijl CP, van der Wel NN, Bitter W.

PLoS Pathog. 2016 Jun 9;12(6):e1005696. doi: 10.1371/journal.ppat.1005696. eCollection 2016 Jun.


The Ag85B protein of the BCG vaccine facilitates macrophage uptake but is dispensable for protection against aerosol Mycobacterium tuberculosis infection.

Prendergast KA, Counoupas C, Leotta L, Eto C, Bitter W, Winter N, Triccas JA.

Vaccine. 2016 May 17;34(23):2608-15. doi: 10.1016/j.vaccine.2016.03.089. Epub 2016 Apr 6.


Inorganic Phosphate Limitation Modulates Capsular Polysaccharide Composition in Mycobacteria.

van de Weerd R, Boot M, Maaskant J, Sparrius M, Verboom T, van Leeuwen LM, Burggraaf MJ, Paauw NJ, Dainese E, Manganelli R, Bitter W, Appelmelk BJ, Geurtsen J.

J Biol Chem. 2016 May 27;291(22):11787-99. doi: 10.1074/jbc.M116.722454. Epub 2016 Apr 4.


Type VII Secretion: A Highly Versatile Secretion System.

Ates LS, Houben ENG, Bitter W.

Microbiol Spectr. 2016 Feb;4(1). doi: 10.1128/microbiolspec.VMBF-0011-2015.


Genomic expression catalogue of a global collection of BCG vaccine strains show evidence for highly diverged metabolic and cell-wall adaptations.

Abdallah AM, Hill-Cawthorne GA, Otto TD, Coll F, Guerra-Assunção JA, Gao G, Naeem R, Ansari H, Malas TB, Adroub SA, Verboom T, Ummels R, Zhang H, Panigrahi AK, McNerney R, Brosch R, Clark TG, Behr MA, Bitter W, Pain A.

Sci Rep. 2015 Oct 21;5:15443. doi: 10.1038/srep15443.


The Soluble Periplasmic Domains of Escherichia coli Cell Division Proteins FtsQ/FtsB/FtsL Form a Trimeric Complex with Submicromolar Affinity.

Glas M, van den Berg van Saparoea HB, McLaughlin SH, Roseboom W, Liu F, Koningstein GM, Fish A, den Blaauwen T, Heck AJ, de Jong L, Bitter W, de Esch IJ, Luirink J.

J Biol Chem. 2015 Aug 28;290(35):21498-509. doi: 10.1074/jbc.M115.654756. Epub 2015 Jul 9.


Essential Role of the ESX-5 Secretion System in Outer Membrane Permeability of Pathogenic Mycobacteria.

Ates LS, Ummels R, Commandeur S, van de Weerd R, Sparrius M, Weerdenburg E, Alber M, Kalscheuer R, Piersma SR, Abdallah AM, Abd El Ghany M, Abdel-Haleem AM, Pain A, Jiménez CR, Bitter W, Houben EN.

PLoS Genet. 2015 May 4;11(5):e1005190. doi: 10.1371/journal.pgen.1005190. eCollection 2015 May. Erratum in: PLoS Genet. 2015 May;11(5):e1005270. van der Weerd, Robert [corrected to van de Weerd, Robert].


Self-cleavage of the Pseudomonas aeruginosa Cell-surface Signaling Anti-sigma Factor FoxR Occurs through an N-O Acyl Rearrangement.

Bastiaansen KC, van Ulsen P, Wijtmans M, Bitter W, Llamas MA.

J Biol Chem. 2015 May 8;290(19):12237-46. doi: 10.1074/jbc.M115.643098. Epub 2015 Mar 25.


Genome-wide transposon mutagenesis indicates that Mycobacterium marinum customizes its virulence mechanisms for survival and replication in different hosts.

Weerdenburg EM, Abdallah AM, Rangkuti F, Abd El Ghany M, Otto TD, Adroub SA, Molenaar D, Ummels R, Ter Veen K, van Stempvoort G, van der Sar AM, Ali S, Langridge GC, Thomson NR, Pain A, Bitter W.

Infect Immun. 2015 May;83(5):1778-88. doi: 10.1128/IAI.03050-14. Epub 2015 Feb 17.


Processing of cell-surface signalling anti-sigma factors prior to signal recognition is a conserved autoproteolytic mechanism that produces two functional domains.

Bastiaansen KC, Otero-Asman JR, Luirink J, Bitter W, Llamas MA.

Environ Microbiol. 2015 Sep;17(9):3263-77. doi: 10.1111/1462-2920.12776. Epub 2015 Feb 14.


Animal models of tuberculosis: zebrafish.

van Leeuwen LM, van der Sar AM, Bitter W.

Cold Spring Harb Perspect Med. 2014 Nov 20;5(3):a018580. doi: 10.1101/cshperspect.a018580. Review.


Impact of protein domains on PE_PGRS30 polar localization in Mycobacteria.

De Maio F, Maulucci G, Minerva M, Anoosheh S, Palucci I, Iantomasi R, Palmieri V, Camassa S, Sali M, Sanguinetti M, Bitter W, Manganelli R, De Spirito M, Delogu G.

PLoS One. 2014 Nov 12;9(11):e112482. doi: 10.1371/journal.pone.0112482. eCollection 2014.


Pathogens under stress.

van Strijp JA, Bitter W.

FEMS Microbiol Rev. 2014 Nov;38(6):1089-90. doi: 10.1111/1574-6976.12090. No abstract available.


Targeting bacterial virulence: the coming out of type VII secretion inhibitors.

Bitter W, Kuijl C.

Cell Host Microbe. 2014 Oct 8;16(4):430-2. doi: 10.1016/j.chom.2014.09.010.


Identification of a novel conjugative plasmid in mycobacteria that requires both type IV and type VII secretion.

Ummels R, Abdallah AM, Kuiper V, Aâjoud A, Sparrius M, Naeem R, Spaink HP, van Soolingen D, Pain A, Bitter W.

MBio. 2014 Sep 23;5(5):e01744-14. doi: 10.1128/mBio.01744-14.


Structure of the Mycobacterium tuberculosis type VII secretion system chaperone EspG5 in complex with PE25-PPE41 dimer.

Korotkova N, Freire D, Phan TH, Ummels R, Creekmore CC, Evans TJ, Wilmanns M, Bitter W, Parret AH, Houben EN, Korotkov KV.

Mol Microbiol. 2014 Oct;94(2):367-82. doi: 10.1111/mmi.12770. Epub 2014 Sep 15.


Modeling tuberculous meningitis in zebrafish using Mycobacterium marinum.

van Leeuwen LM, van der Kuip M, Youssef SA, de Bruin A, Bitter W, van Furth AM, van der Sar AM.

Dis Model Mech. 2014 Sep;7(9):1111-22. doi: 10.1242/dmm.015453. Epub 2014 Jul 4.


Towards a new combination therapy for tuberculosis with next generation benzothiazinones.

Makarov V, Lechartier B, Zhang M, Neres J, van der Sar AM, Raadsen SA, Hartkoorn RC, Ryabova OB, Vocat A, Decosterd LA, Widmer N, Buclin T, Bitter W, Andries K, Pojer F, Dyson PJ, Cole ST.

EMBO Mol Med. 2014 Mar;6(3):372-83. doi: 10.1002/emmm.201303575. Epub 2014 Feb 5.


The Prc and RseP proteases control bacterial cell-surface signalling activity.

Bastiaansen KC, Ibañez A, Ramos JL, Bitter W, Llamas MA.

Environ Microbiol. 2014 Aug;16(8):2433-43. doi: 10.1111/1462-2920.12371. Epub 2014 Jan 21.


Take five - Type VII secretion systems of Mycobacteria.

Houben EN, Korotkov KV, Bitter W.

Biochim Biophys Acta. 2014 Aug;1843(8):1707-16. doi: 10.1016/j.bbamcr.2013.11.003. Epub 2013 Nov 18. Review.


Analysis of SecA2-dependent substrates in Mycobacterium marinum identifies protein kinase G (PknG) as a virulence effector.

van der Woude AD, Stoop EJ, Stiess M, Wang S, Ummels R, van Stempvoort G, Piersma SR, Cascioferro A, Jiménez CR, Houben EN, Luirink J, Pieters J, van der Sar AM, Bitter W.

Cell Microbiol. 2014 Feb;16(2):280-95. doi: 10.1111/cmi.12221. Epub 2013 Nov 6.


Understanding specificity of the mycosin proteases in ESX/type VII secretion by structural and functional analysis.

Wagner JM, Evans TJ, Chen J, Zhu H, Houben EN, Bitter W, Korotkov KV.

J Struct Biol. 2013 Nov;184(2):115-28. doi: 10.1016/j.jsb.2013.09.022. Epub 2013 Oct 7.


Mannan core branching of lipo(arabino)mannan is required for mycobacterial virulence in the context of innate immunity.

Stoop EJ, Mishra AK, Driessen NN, van Stempvoort G, Bouchier P, Verboom T, van Leeuwen LM, Sparrius M, Raadsen SA, van Zon M, van der Wel NN, Besra GS, Geurtsen J, Bitter W, Appelmelk BJ, van der Sar AM.

Cell Microbiol. 2013 Dec;15(12):2093-108. doi: 10.1111/cmi.12175. Epub 2013 Aug 22.


Fine-mapping the contact sites of the Escherichia coli cell division proteins FtsB and FtsL on the FtsQ protein.

van den Berg van Saparoea HB, Glas M, Vernooij IG, Bitter W, den Blaauwen T, Luirink J.

J Biol Chem. 2013 Aug 23;288(34):24340-50. doi: 10.1074/jbc.M113.485888. Epub 2013 Jul 11.


Differential detergent extraction of mycobacterium marinum cell envelope proteins identifies an extensively modified threonine-rich outer membrane protein with channel activity.

van der Woude AD, Mahendran KR, Ummels R, Piersma SR, Pham TV, Jiménez CR, de Punder K, van der Wel NN, Winterhalter M, Luirink J, Bitter W, Houben EN.

J Bacteriol. 2013 May;195(9):2050-9. doi: 10.1128/JB.02236-12. Epub 2013 Mar 1.

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