[4.3.1]Bicyclic FKBP Ligands Inhibit Legionella Pneumophila Infection by LpMip-Dependent and LpMip-Independent Mechanisms.


Journal

Chembiochem : a European journal of chemical biology
ISSN: 1439-7633
Titre abrégé: Chembiochem
Pays: Germany
ID NLM: 100937360

Informations de publication

Date de publication:
02 11 2023
Historique:
revised: 24 07 2023
received: 14 06 2023
medline: 3 11 2023
pubmed: 25 7 2023
entrez: 25 7 2023
Statut: ppublish

Résumé

Legionella pneumophila is the causative agent of Legionnaires' disease, a serious form of pneumonia. Its macrophage infectivity potentiator (Mip), a member of a highly conserved family of FK506-binding proteins (FKBPs), plays a major role in the proliferation of the gram-negative bacterium in host organisms. In this work, we test our library of >1000 FKBP-focused ligands for inhibition of LpMip. The [4.3.1]-bicyclic sulfonamide turned out as a highly preferred scaffold and provided the most potent LpMip inhibitors known so far. Selected compounds were non-toxic to human cells, displayed antibacterial activity and block bacterial proliferation in cellular infection-assays as well as infectivity in human lung tissue explants. The results confirm [4.3.1]-bicyclic sulfonamides as anti-legionellal agents, although their anti-infective properties cannot be explained by inhibition of LpMip alone.

Identifiants

pubmed: 37489700
doi: 10.1002/cbic.202300442
doi:

Substances chimiques

Tacrolimus Binding Proteins EC 5.2.1.-
Peptidylprolyl Isomerase EC 5.2.1.8
Bacterial Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e202300442

Informations de copyright

© 2023 The Authors. ChemBioChem published by Wiley-VCH GmbH.

Références

 
G. Balsevich, A. S. Häusl, C. W. Meyer, S. Karamihalev, X. Feng, M. L. Pöhlmann, C. Dournes, A. Uribe-Marino, S. Santarelli, C. Labermaier, K. Hafner, T. Mao, M. Breitsamer, M. Theodoropoulou, C. Namendorf, M. Uhr, M. Paez-Pereda, G. Winter, F. Hausch, A. Chen, M. H. Tschöp, T. Rein, N. C. Gassen, M. V. Schmidt, Nat. Commun. 2017, 8, 1725;
M. W. Harding, A. Galat, D. E. Uehling, S. L. Schreiber, Nature 1989, 341, 758;
M. Maiarù, K. K. Tochiki, M. B. Cox, L. V. Annan, C. G. Bell, X. Feng, F. Hausch, S. M. Géranton, Sci. Transl. Med. 2016, 8, 325ra19;
L. A. Stechschulte, B. Qiu, M. Warrier, T. D. Hinds, M. Zhang, H. Gu, Y. Xu, S. S. Khuder, L. Russo, S. M. Najjar, B. Lecka-Czernik, W. Yong, E. R. Sanchez, Endocrinology 2016, 157, 3888;
C. L. Storer, C. A. Dickey, M. D. Galigniana, T. Rein, M. B. Cox, Trends Endocrinol. Metab. 2011, 22, 481.
 
J. C. Ahn, D.-W. Kim, Y. N. You, M. S. Seok, J. M. Park, H. Hwang, B.-G. Kim, S. Luan, H.-S. Park, H. S. Cho, BMC Plant Biol. 2010, 10, 253;
G. Ghartey-Kwansah, Z. Li, R. Feng, L. Wang, X. Zhou, F. Z. Chen, M. M. Xu, O. Jones, Y. Mu, S. Chen, J. Bryant, W. B. Isaacs, J. Ma, X. Xu, BMC Dev. Biol. 2018, 18, 7.
C. M. Ünal, M. Steinert, Microbiol. Mol. Biol. Rev. 2014, 78, 544.
N. P. Cianciotto, B. I. Eisenstein, C. H. Mody, G. B. Toews, N. C. Engleberg, Infect. Immun. 1989, 57, 1255.
 
A. G. Lundemose, S. Birkelund, S. J. Fey, P. M. Larsen, G. Christiansen, Mol. Microbiol. 1991, 5, 109;
P. Monaghan, D. B. Leneghan, W. Shaw, A. Bell, Parasitology 2017, 144, 869;
A. Moro, F. Ruiz-Cabello, A. Fernández-Cano, R. P. Stock, A. González, EMBO J. 1995, 14, 2483;
I. H. Norville, N. J. Harmer, S. V. Harding, G. Fischer, K. E. Keith, K. A. Brown, M. Sarkar-Tyson, R. W. Titball, Infect. Immun. 2011, 79, 4299.
C. Baron, Curr. Opin. Microbiol. 2010, 13, 100.
A. A. Khweek, A. Amer, Front. Microbiol. 2010, 1, 133.
J. E. McDade, C. C. Shepard, D. W. Fraser, T. R. Tsai, M. A. Redus, W. R. Dowdle, N. Engl. J. Med. 1977, 297, 1197.
N. P. Cianciotto, B. S. Fields, Proc. Natl. Acad. Sci. USA 1992, 89, 5188.
 
G. Fischer, H. Bang, B. Ludwig, K. Mann, J. Hacker, Mol. Microbiol. 1992, 6, 1375;
A. Riboldi-Tunnicliffe, B. König, S. Jessen, M. S. Weiss, J. Rahfeld, J. Hacker, G. Fischer, R. Hilgenfeld, Nat. Struct. Biol. 2001, 8, 779;
B. Schmidt, J. Rahfeld, A. Schierhorn, B. Ludwig, J. Hacker, G. Fischer, FEBS Lett. 1994, 352, 185.
E. Wintermeyer, B. Ludwig, M. Steinert, B. Schmidt, G. Fischer, J. Hacker, Infect. Immun. 1995, 63, 4576.
R. Köhler, J. Fanghänel, B. König, E. Lüneberg, M. Frosch, J.-U. Rahfeld, R. Hilgenfeld, G. Fischer, J. Hacker, M. Steinert, Infect. Immun. 2003, 71, 4389.
 
C. M. Ünal, M. Steinert, Biochim. Biophys. Acta 2015, 1850, 2096;
C. Wagner, A. S. Khan, T. Kamphausen, B. Schmausser, C. Unal, U. Lorenz, G. Fischer, J. Hacker, M. Steinert, Cell. Microbiol. 2007, 9, 450.
M. S. Karagöz, C. M. Ünal, B. E. Mayer, M. Müsken, J. M. Borrero-de Acuña, M. Steinert, Infect. Immun. 2022, 90, e0027622.
 
J. M. Kolos, A. M. Voll, M. Bauder, F. Hausch, Front. Pharmacol. 2018, 9, 1425;
N. J. Scheuplein, N. M. Bzdyl, E. A. Kibble, T. Lohr, U. Holzgrabe, M. Sarkar-Tyson, J. Med. Chem. 2020, 63, 13355.
H. O. Sintim, J. A. I. Smith, J. Wang, S. Nakayama, L. Yan, Future Med. Chem. 2010, 2, 1005.
C. Ünal, K. F. Schwedhelm, A. Thiele, M. Weiwad, K. Schweimer, F. Frese, G. Fischer, J. Hacker, C. Faber, M. Steinert, Cell. Microbiol. 2011, 13, 1558.
C. Christner, R. Wyrwa, S. Marsch, G. Küllertz, R. Thiericke, S. Grabley, D. Schumann, G. Fischer, J. Med. Chem. 1999, 42, 3615.
 
C. Juli, M. Sippel, J. Jäger, A. Thiele, M. Weiwad, K. Schweimer, P. Rösch, M. Steinert, C. A. Sotriffer, U. Holzgrabe, J. Med. Chem. 2011, 54, 277;
F. Seufert, M. Kuhn, M. Hein, M. Weiwad, M. Vivoli, I. H. Norville, M. Sarkar-Tyson, L. E. Marshall, K. Schweimer, H. Bruhn, P. Rösch, N. J. Harmer, C. A. Sotriffer, U. Holzgrabe, Bioorg. Med. Chem. 2016, 24, 5134.
S. L. Schreiber, G. R. Crabtree, Immunol. Today 1992, 13, 136.
S. Pomplun, C. Sippel, A. Hähle, D. Tay, K. Shima, A. Klages, C. M. Ünal, B. Rieß, H. T. Toh, G. Hansen, H. S. Yoon, A. Bracher, P. Preiser, J. Rupp, M. Steinert, F. Hausch, J. Med. Chem. 2018, 61, 3660.
C. Wiedemann, J. J. Whittaker, V. H. Pérez Carrillo, B. Goretzki, M. Dajka, F. Tebbe, J.-M. Harder, P. Krajczy, B. Joseph, F. Hausch, A. Guskov, U. A. Hellmich, 2023, arXiv preprint DOI: 10.1101/2023.04.24.538046.
M. Bauder, C. Meyners, P. L. Purder, S. Merz, W. O. Sugiarto, A. M. Voll, T. Heymann, F. Hausch, J. Med. Chem. 2021, 64, 3320.
M. Bischoff, P. Mayer, C. Meyners, F. Hausch, Chem. Eur. J. 2020, 26, 4677.
M. Bischoff, C. Sippel, A. Bracher, F. Hausch, Org. Lett. 2014, 16, 5254.
X. Feng, C. Sippel, A. Bracher, F. Hausch, J. Med. Chem. 2015, 58, 7796.
X. Feng, C. Sippel, F. H. Knaup, A. Bracher, S. Staibano, M. F. Romano, F. Hausch, J. Med. Chem. 2020, 63, 231.
S. Gaali, X. Feng, A. Hähle, C. Sippel, A. Bracher, F. Hausch, J. Med. Chem. 2016, 59, 2410.
S. Gaali, A. Kirschner, S. Cuboni, J. Hartmann, C. Kozany, G. Balsevich, C. Namendorf, P. Fernandez-Vizarra, C. Sippel, A. S. Zannas, R. Draenert, E. B. Binder, O. F. X. Almeida, G. Rühter, M. Uhr, M. V. Schmidt, C. Touma, A. Bracher, F. Hausch, Nat. Chem. Biol. 2015, 11, 33.
R. Gopalakrishnan, C. Kozany, S. Gaali, C. Kress, B. Hoogeland, A. Bracher, F. Hausch, J. Med. Chem. 2012, 55, 4114.
R. Gopalakrishnan, C. Kozany, Y. Wang, S. Schneider, B. Hoogeland, A. Bracher, F. Hausch, J. Med. Chem. 2012, 55, 4123.
J. M. Kolos, S. Pomplun, S. Jung, B. Rieß, P. L. Purder, A. M. Voll, S. Merz, M. Gnatzy, T. M. Geiger, I. Quist-Løkken, J. Jatzlau, P. Knaus, T. Holien, A. Bracher, C. Meyners, P. Czodrowski, V. Krewald, F. Hausch, Chem. Sci. 2021, 12, 14758.
S. Pomplun, Y. Wang, A. Kirschner, C. Kozany, A. Bracher, F. Hausch, Angew. Chem. Int. Ed. 2015, 54, 345.
A. M. Voll, C. Meyners, M. C. Taubert, T. Bajaj, T. Heymann, S. Merz, A. Charalampidou, J. Kolos, P. L. Purder, T. M. Geiger, P. Wessig, N. C. Gassen, A. Bracher, F. Hausch, Angew. Chem. Int. Ed. 2021, 60, 13257.
Y. Wang, A. Kirschner, A.-K. Fabian, R. Gopalakrishnan, C. Kress, B. Hoogeland, U. Koch, C. Kozany, A. Bracher, F. Hausch, J. Med. Chem. 2013, 56, 3922.
C. Kozany, A. März, C. Kress, F. Hausch, ChemBioChem 2009, 10, 1402.
M. T. Gnatzy, T. M. Geiger, A. Kuehn, N. Gutfreund, M. Walz, J. M. Kolos, F. Hausch, ChemBioChem 2021, 22, 2257.
“14:00-17:00. ISO 10993-5 : 2009. ISO.”, can be found under http://www.iso.org/standard/36406.html (2022-12-11).
A. Galat, J. Chem. Inf. Model. 2008, 48, 1118.
J. R. Walker, M. P. Hall, C. A. Zimprich, M. B. Robers, S. J. Duellman, T. Machleidt, J. Rodriguez, W. Zhuo, ACS Chem. Biol. 2017, 1028.
E. P. Coutant, G. Gagnot, V. Hervin, R. Baatallah, S. Goyard, Y. Jacob, T. Rose, Y. L. Janin, Chem. Eur. J. 2020, 26, 948.
R. I. Jepras, R. B. Fitzgeorge, A. Baskerville, J. Hyg. 1985, 95, 29.
ISO 20776-2 : 2021 (en), “Clinical laboratory testing and in vitro diagnostic test systems - Suscepti-bility testing of infectious agents and evaluation of performance of antimi-crobial susceptibility test devices - Part 2: Evaluation of performance of antimicrobial susceptibility test devices against reference broth micro-dilution.”, can be found under http://www.iso.org/obp/ui/#iso:std:iso:20776:-2:ed-2:v1:en (2022-12-11).

Auteurs

Robin C E Deutscher (RCE)

Institute for Organic Chemistry and Biochemistry, Technical University Darmstadt, Peter-Grünberg-Straße 4, 64287, Darmstadt, Germany.

M Safa Karagöz (M)

Institut für Mikrobiologie, Technische Universität Braunschweig, Spielmannstr. 7, 38106, Braunschweig, Germany.

Patrick L Purder (PL)

Institute for Organic Chemistry and Biochemistry, Technical University Darmstadt, Peter-Grünberg-Straße 4, 64287, Darmstadt, Germany.

Jürgen M Kolos (JM)

Institute for Organic Chemistry and Biochemistry, Technical University Darmstadt, Peter-Grünberg-Straße 4, 64287, Darmstadt, Germany.

Christian Meyners (C)

Institute for Organic Chemistry and Biochemistry, Technical University Darmstadt, Peter-Grünberg-Straße 4, 64287, Darmstadt, Germany.

Wisely Oki Sugiarto (W)

Institute for Organic Chemistry and Biochemistry, Technical University Darmstadt, Peter-Grünberg-Straße 4, 64287, Darmstadt, Germany.

Patryk Krajczy (P)

Institute for Organic Chemistry and Biochemistry, Technical University Darmstadt, Peter-Grünberg-Straße 4, 64287, Darmstadt, Germany.

Frederike Tebbe (F)

Institute of Organic Chemistry & Macromolecular Chemistry (IOMC), Friedrich Schiller University Germany, Humboldtstraße 10, 07743, Jena, Germany.

Thomas M Geiger (TM)

Institute for Organic Chemistry and Biochemistry, Technical University Darmstadt, Peter-Grünberg-Straße 4, 64287, Darmstadt, Germany.

Can Ünal (C)

Institut für Mikrobiologie, Technische Universität Braunschweig, Spielmannstr. 7, 38106, Braunschweig, Germany.

Ute A Hellmich (UA)

Institute of Organic Chemistry & Macromolecular Chemistry (IOMC), Friedrich Schiller University Germany, Humboldtstraße 10, 07743, Jena, Germany.
Center for Biomolecular Magnetic Resonance (BMRZ), Goethe University, Max-von-Laue-Str. 9, 60438, Frankurt/Main, Germany.
Cluster of Excellence Balance of the Microverse, Friedrich Schiller University Jena, Jena, Germany.

Michael Steinert (M)

Institut für Mikrobiologie, Technische Universität Braunschweig, Spielmannstr. 7, 38106, Braunschweig, Germany.
Helmholtz Centre for Infection Research, 38106, Braunschweig, Germany.

Felix Hausch (F)

Institute for Organic Chemistry and Biochemistry, Technical University Darmstadt, Peter-Grünberg-Straße 4, 64287, Darmstadt, Germany.
Centre for Synthetic Biology, Technical University of Darmstadt, 64287, Darmstadt, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH