A combined approach of structure-based virtual screening and NMR to interrupt the PD-1/PD-L1 axis: Biphenyl-benzimidazole containing compounds as novel PD-L1 inhibitors.

NMR PD-L1 inhibitors benzimidazole immunotherapy virtual screening

Journal

Archiv der Pharmazie
ISSN: 1521-4184
Titre abrégé: Arch Pharm (Weinheim)
Pays: Germany
ID NLM: 0330167

Informations de publication

Date de publication:
18 Dec 2023
Historique:
revised: 22 11 2023
received: 10 10 2023
accepted: 24 11 2023
medline: 19 12 2023
pubmed: 19 12 2023
entrez: 19 12 2023
Statut: aheadofprint

Résumé

Immunotherapy has emerged as a game-changing approach for cancer treatment. Although monoclonal antibodies (mAbs) targeting the programmed cell death protein 1/programmed cell death protein 1 ligand 1 (PD-1/PD-L1) axis have entered the market revolutionizing the treatment landscape of many cancer types, small molecules, although presenting several advantages including the possibility of oral administration and/or reduced costs, struggled to enter in clinical trials, suffering of water insolubility and/or inadequate potency compared with mAbs. Thus, the search for novel scaffolds for both the design of effective small molecules and possible synergistic strategies is an ongoing field of interest. In an attempt to find novel chemotypes, a virtual screening approach was employed, resulting in the identification of new chemical entities with a certain binding capability, the most versatile of which was the benzimidazole-containing compound 10. Through rational design, a small library of its derivatives was synthesized and evaluated. The homogeneous time-resolved fluorescence (HTRF) assay revealed that compound 17 shows the most potent inhibitory activity (IC

Identifiants

pubmed: 38110703
doi: 10.1002/ardp.202300583
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2300583

Subventions

Organisme : Fundacja na rzecz Nauki Polskiej
Organisme : European Regional Development Fund
Organisme : Ministero dell'Istruzione, dell'Università e della Ricerca
Organisme : Italian Ministry of Education, University, and Research (MIUR)
Organisme : Progetti di Rilevante Interesse Nazionale, PRIN 2017
ID : 2017PHRC8X
Organisme : PRIN 2022
ID : 2022YWZWB2
Organisme : POIR
ID : 04.04.00-00-420 F/17-00
Organisme : European Union

Informations de copyright

© 2023 The Authors. Archiv der Pharmazie published by Wiley-VCH GmbH on behalf of Deutsche Pharmazeutische Gesellschaft.

Références

N. A. Carreau, A. C. Pavlick, Future Oncol. 2019, 15, 349.
L. Sun, L. Zhang, J. Yu, Y. Zhang, X. Pang, C. Ma, M. Shen, S. Ruan, H. S. Wasan, S. Qiu, Sci. Rep. 2020, 10, 2083.
A. Patnaik, S. P. Kang, D. Rasco, K. P. Papadopoulos, J. Elassaiss-Schaap, M. Beeram, R. Drengler, C. Chen, L. Smith, G. Espino, K. Gergich, L. Delgado, A. Daud, J. A. Lindia, X. N. Li, R. H. Pierce, J. H. Yearley, D. Wu, O. Laterza, M. Lehnert, R. Iannone, A. W. Tolcher, Clin. Cancer Res. 2015, 21, 4286.
S. L. Topalian, F. S. Hodi, J. R. Brahmer, S. N. Gettinger, D. C. Smith, D. F. McDermott, J. D. Powderly, R. D. Carvajal, J. A. Sosman, M. B. Atkins, P. D. Leming, D. R. Spigel, S. J. Antonia, L. Horn, C. G. Drake, D. M. Pardoll, L. Chen, W. H. Sharfman, R. A. Anders, J. M. Taube, T. L. McMiller, H. Xu, A. J. Korman, M. Jure-Kunkel, S. Agrawal, D. McDonald, G. D. Kollia, A. Gupta, J. M. Wigginton, M. Sznol, N. Engl. J. Med. 2012, 366, 2443.
J. R. Brahmer, S. S. Tykodi, L. Q. M. Chow, W.-J. Hwu, S. L. Topalian, P. Hwu, C. G. Drake, L. H. Camacho, J. Kauh, K. Odunsi, H. C. Pitot, O. Hamid, S. Bhatia, R. Martins, K. Eaton, S. Chen, T. M. Salay, S. Alaparthy, J. F. Grosso, A. J. Korman, S. M. Parker, S. Agrawal, S. M. Goldberg, D. M. Pardoll, A. Gupta, J. M. Wigginton, N. Engl. J. Med. 2012, 366, 2455.
A. Constantinidou, C. Alifieris, D. T. Trafalis, Pharmacol. Ther. 2019, 194, 84.
J. D. Twomey, B. Zhang, AAPS. J. 2021, 23, 39.
X. Lin, X. Lu, G. Luo, H. Xiang, Eur. J. Med. Chem. 2020, 186, 111876.
L. S. Chupak, X. Zheng. WO034820A1, 2015.
M. Konieczny, B. Musielak, J. Kocik, L. Skalniak, D. Sala, M. Czub, K. Magiera-Mularz, I. Rodriguez, M. Myrcha, M. Stec, M. Siedlar, T. A. Holak, J. Plewka, J. Med. Chem. 2020, 63, 11271.
C. Sun, M. Yin, Y. Cheng, Z. Kuang, X. Liu, G. Wang, X. Wang, K. Yuan, W. Min, J. Dong, Y. Hou, L. Hu, G. Zhang, W. Pei, L. Wang, Y. Sun, X. Yu, Y. Xiao, H. Deng, P. Yang, J. Med. Chem. 2023, 66, 2064.
R. Butera, M. Ważyńska, K. Magiera-Mularz, J. Plewka, B. Musielak, E. Surmiak, D. Sala, R. Kitel, M. de Bruyn, H. W. Nijman, P. H. Elsinga, T. A. Holak, A. Dömling, ACS Med. Chem. Lett. 2021, 12, 768.
T. Wang, S. Cai, Y. Cheng, W. Zhang, M. Wang, H. Sun, B. Guo, Z. Li, Y. Xiao, S. Jiang, J. Med. Chem. 2022, 65, 3879.
P. Russomanno, G. Assoni, J. Amato, V. M. D'Amore, R. Scaglia, D. Brancaccio, M. Pedrini, G. Polcaro, V. La Pietra, P. Orlando, M. Falzoni, L. Cerofolini, S. Giuntini, M. Fragai, B. Pagano, G. Donati, E. Novellino, C. Quintavalle, G. Condorelli, F. Sabbatino, P. Seneci, D. Arosio, S. Pepe, L. Marinelli, J. Med. Chem. 2021, 64, 16020.
J.-J. Park, E. P. Thi, V. H. Carpio, Y. Bi, A. G. Cole, B. D. Dorsey, K. Fan, T. Harasym, C. L. Iott, S. Kadhim, J. H. Kim, A. C. H. Lee, D. Nguyen, B. S. Paratala, R. Qiu, A. White, D. Lakshminarasimhan, C. Leo, R. K. Suto, R. Rijnbrand, S. Tang, M. J. Sofia, C. B. Moore, Nat. Commun. 2021, 12, 1222.
E. Aktoudianakis, A. C. Du, M. Graupe, L. T. LAD, P. A. Machicao Tello, J. W. Medley, S. E. Metobo, P. K. Mukherjeed, D. Naduthambi, E. Q. Parkhill, B. W. Phillips, S. Preston Simonovich, N. H. Squires, P. Wang, W. J. Watkins, J. Xu, K. S. Yang, C. A. Ziebenhaus, WO2019160882A1, 2019.
Clinicaltrials.gov. 2019.
J. Li, C. Qi, F. Zhang, Z. Li, W. Zhu, Z. Yu, K. Xiao, L. Lu, S. Mei, D. Qian, C. He, T. Ye, M. Xu, W. Yao, WO119266. 2018.
G. Sun, D. Rong, Z. Li, G. Sun, F. Wu, X. Li, H. Cao, Y. Cheng, W. Tang, Y. Sun, Front. Cell. Dev. Biol. 2021, 9, 694363.
M. Giustiniano, S. Daniele, S. Pelliccia, V. La Pietra, D. Pietrobono, D. Brancaccio, S. Cosconati, A. Messere, S. Giuntini, L. Cerofolini, M. Fragai, C. Luchinat, S. Taliani, G. La Regina, F. Da Settimo, R. Silvestri, C. Martini, E. Novellino, L. Marinelli, J. Med. Chem. 2017, 60, 8115.
A. Cipriano, C. Milite, A. Feoli, M. Viviano, G. Pepe, P. Campiglia, G. Sarno, S. Picaud, S. Imaide, N. Makukhin, P. Filippakopoulos, A. Ciulli, S. Castellano, G. Sbardella, ChemMedChem 2022, 17, e202200343.
C. Milite, G. Amendola, A. Nocentini, S. Bua, A. Cipriano, E. Barresi, A. Feoli, E. Novellino, F. Da Settimo, C. T. Supuran, S. Castellano, S. Cosconati, S. Taliani, J. Enzyme Inhib. Med. Chem. 2019, 34, 1697.
S. Taliani, I. Pugliesi, E. Barresi, F. Simorini, S. Salerno, C. La Motta, A. M. Marini, B. Cosimelli, S. Cosconati, S. Di Maro, L. Marinelli, S. Daniele, M. L. Trincavelli, G. Greco, E. Novellino, C. Martini, F. Da Settimo, J. Med. Chem. 2012, 55, 1490.
R. S. Keri, A. Hiremathad, S. Budagumpi, B. M. Nagaraja, Chem. Biol. Drug Des. 2015, 86, 19.
Y. F. Li, G. F. Wang, P. L. He, W. G. Huang, F. H. Zhu, H. Y. Gao, W. Tang, Y. Luo, C. L. Feng, L. P. Shi, Y. D. Ren, W. Lu, J. P. Zuo, J. Med. Chem. 2006, 49, 4790.
T. L. Mistry, L. Truong, A. K. Ghosh, M. E. Johnson, S. Mehboob, ACS Infect. Dis. 2017, 3, 54.
G. A. Dziwornu, D. Coertzen, M. Leshabane, C. M. Korkor, C. K. Cloete, M. Njoroge, L. Gibhard, N. Lawrence, J. Reader, M. van der Watt, S. Wittlin, L. M. Birkholtz, K. Chibale, J. Med. Chem. 2021, 64, 5198.
J. J. Nué-Martinez, D. Cisneros, M. V. Moreno-Blázquez, C. Fonseca-Berzal, J. I. Manzano, D. Kraeutler, M. A. Ungogo, M. A. Aloraini, H. Elati, A. Ibáñez-Escribano, L. Lagartera, T. Herraiz, F. Gamarro, H. P. de Koning, A. Gómez-Barrio, C. Dardonville, J. Med. Chem. 2023, 66, 13452.
G. Donati, V. M. D'Amore, P. Russomanno, L. Cerofolini, J. Amato, S. Marzano, M. Salobehaj, D. Rizzo, G. Assoni, A. Carotenuto, V. La Pietra, D. Arosio, P. Seneci, M. Fragai, D. Brancaccio, F. S. Di Leva, L. Marinelli, Comput. Struct. Biotechnol. J. 2023, 21, 3355.
K. M. Zak, P. Grudnik, K. Guzik, B. J. Zieba, B. Musielak, A. Dömling, G. Dubin, T. A. Holak, Oncotarget 2016, 7, 30323.
M. Konstantinidou, T. Zarganes-Tzitzikas, K. Magiera-Mularz, T. A. Holak, A. Dömling, Angew. Chem. Int. Ed. 2018, 57, 4840.
M. Waqas, S. A. Halim, A. Alsalman, A. Khan, E. Elkord, A. Al-Harrasi, J. Biomol. Struct. Dyn. 2023, 1.
Glide, Schrödinger, LLC, New York, NY, 2021.
K. Guzik, K. M. Zak, P. Grudnik, K. Magiera, B. Musielak, R. Törner, L. Skalniak, A. Dömling, G. Dubin, T. A. Holak, J. Med. Chem. 2017, 60, 5857.
R. Kitel, I. Rodríguez, X. del Corte, J. Atmaj, M. Żarnik, E. Surmiak, D. Muszak, K. Magiera-Mularz, G. M. Popowicz, T. A. Holak, B. Musielak, ACS Chem. Biol. 2022, 17, 2655.
B. Cheng, W. Wang, X. Niu, Y. Ren, T. Liu, H. Cao, S. Wang, Y. Tu, J. Chen, S. Liu, X. Yang, J. Chen, J. Med. Chem. 2020, 63, 15946.
M. Qin, Q. Cao, S. Zheng, Y. Tian, H. Zhang, J. Xie, H. Xie, Y. Liu, Y. Zhao, P. Gong, J. Med. Chem. 2019, 62, 4703.
L. Di, P. V. Fish, T. Mano, Drug Discov. Today 2012, 17, 486.
LigPrep, Schrödinger, LLC, New York, NY, 2021.
Epik, Schrödinger, LLC, New York, NY, 2021.
ConfGen, Schrödinger, LLC, New York, NY, 2021.
S. L. Dixon, A. M. Smondyrev, S. N. Rao, Chem. Biol. Drug Des. 2006, 67, 370.
V. Limongelli, L. Marinelli, S. Cosconati, H. A. Braun, B. Schmidt, E. Novellino, ChemMedChem 2007, 2, 667.
E. Da Pozzo, V. La Pietra, B. Cosimelli, F. Da Settimo, C. Giacomelli, L. Marinelli, C. Martini, E. Novellino, S. Taliani, G. Greco, ACS Chem. Neurosci. 2014, 5, 390.
Maestro, Schrödinger, LLC, New York, NY, 2021.
Protein Preparation Wizard, Schrödinger, LLC, New York, NY, 2021.
G. Madhavi Sastry, M. Adzhigirey, T. Day, R. Annabhimoju, W. Sherman, J. Comput.-Aided Mol. Des. 2013, 27, 221.
Prime, Schrödinger, LLC, New York, NY, 2021.
M. H. M. Olsson, C. R. Søndergaard, M. Rostkowski, J. H. Jensen, J. Chem. Theory Comput. 2011, 7, 525.
J. L. Banks, H. S. Beard, Y. Cao, A. E. Cho, W. Damm, R. Farid, A. K. Felts, T. A. Halgren, D. T. Mainz, J. R. Maple, R. Murphy, D. M. Philipp, M. P. Repasky, L. Y. Zhang, B. J. Berne, R. A. Friesner, E. Gallicchio, R. M. Levy, J. Comput. Chem. 2005, 26, 1752.
R. A. Friesner, R. B. Murphy, M. P. Repasky, L. L. Frye, J. R. Greenwood, T. A. Halgren, P. C. Sanschagrin, D. T. Mainz, J. Med. Chem. 2006, 49, 6177.
T. A. Halgren, R. B. Murphy, R. A. Friesner, H. S. Beard, L. L. Frye, W. T. Pollard, J. L. Banks, J. Med. Chem. 2004, 47, 1750.
R. A. Friesner, J. L. Banks, R. B. Murphy, T. A. Halgren, J. J. Klicic, D. T. Mainz, M. P. Repasky, E. H. Knoll, M. Shelley, J. K. Perry, D. E. Shaw, P. Francis, P. S. Shenkin, J. Med. Chem. 2004, 47, 1739.
J. C. Shelley, A. Cholleti, L. L. Frye, J. R. Greenwood, M. R. Timlin, M. Uchimaya, J. Comput.-Aided Mol. Des. 2007, 21, 681.
MacroModel, Schrödinger, LLC, New York, NY, 2021.
E. F. Pettersen, T. D. Goddard, C. C. Huang, E. C. Meng, G. S. Couch, T. I. Croll, J. H. Morris, T. E. Ferrin, Protein Sci. 2021, 30, 70.
P. Schanda, Ē. Kupče, B. Brutscher, J. Biomol. NMR 2005, 33, 199.
QikProp, version 2.3; Schrödinger, Inc., New York, 2005

Auteurs

Greta Donati (G)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Monica Viviano (M)

Department of Pharmacy, University of Salerno, Fisciano, Italy.

Vincenzo Maria D'Amore (VM)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Alessandra Cipriano (A)

Department of Pharmacy, University of Salerno, Fisciano, Italy.

Isidora Diakogiannaki (I)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Jussara Amato (J)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Stefano Tomassi (S)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Diego Brancaccio (D)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Pasquale Russomanno (P)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Francesco Saverio Di Leva (FS)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Daniela Arosio (D)

Istituto di Scienze e Tecnologie Chimiche "Giulio Natta" (SCITEC), Consiglio Nazionale delle Ricerche (CNR), Milan, Italy.

Pierfausto Seneci (P)

Department of Chemistry, University of Milan, Milan, Italy.

Sabrina Taliani (S)

Department of Pharmacy, University of Pisa, Pisa, Italy.

Katarzyna Magiera-Mularz (K)

Department of Organic Chemistry, Faculty of Chemistry, Jagiellonian University, Cracow, Poland.

Bogdan Musielak (B)

Department of Organic Chemistry, Faculty of Chemistry, Jagiellonian University, Cracow, Poland.

Lukasz Skalniak (L)

Department of Organic Chemistry, Faculty of Chemistry, Jagiellonian University, Cracow, Poland.

Tad A Holak (TA)

Department of Organic Chemistry, Faculty of Chemistry, Jagiellonian University, Cracow, Poland.

Sabrina Castellano (S)

Department of Pharmacy, University of Salerno, Fisciano, Italy.

Valeria La Pietra (V)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Luciana Marinelli (L)

Department of Pharmacy, University of Naples Federico II, Naples, Italy.

Classifications MeSH