Antitubercular polyhalogenated phenothiazines and phenoselenazine with reduced binding to CNS receptors

  • Eur J Med Chem. 2020 Sep 1:201:112420. doi: 10.1016/j.ejmech.2020.112420.
Maria Giulia Nizi  1 Jenny Desantis  1 Yoshio Nakatani  2 Serena Massari  1 Maria Angela Mazzarella  1 Gauri Shetye  3 Stefano Sabatini  1 Maria Letizia Barreca  1 Giuseppe Manfroni  1 Tommaso Felicetti  1 Rowena Rushton-Green  2 Kiel Hards  2 Gniewomir Latacz  4 Grzegorz Satała  5 Andrzej J Bojarski  5 Violetta Cecchetti  1 Michal H Kolář  6 Jadwiga Handzlik  4 Gregory M Cook  2 Scott G Franzblau  3 Oriana Tabarrini  7
Affiliations
  • 1. Department of Pharmaceutical Sciences, University of Perugia, Via Del Liceo 1, Perugia, 06100, Italy.
  • 2. Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealand.
  • 3. Institute for Tuberculosis Research, College of Pharmacy, University of Illinois at Chicago, Chicago, IL, USA.
  • 4. Department of Technology and Biotechnology of Drugs, Faculty of Pharmacy, Jagiellonian University Medical College, Medyczna 9, 30-688, Kraków, Poland.
  • 5. Department of Medicinal Chemistry May Institute of Pharmacology, Polish Academy of Sciences, Smętna 12, 31-343, Kraków, Poland.
  • 6. Department of Physical Chemistry, University of Chemistry and Technology, Technicka 5, 16628, Prague, Czech Republic.
  • 7. Department of Pharmaceutical Sciences, University of Perugia, Via Del Liceo 1, Perugia, 06100, Italy. Electronic address: [email protected].
Abstract

Targeting energy metabolism in Mycobacterium tuberculosis (Mtb) is a new paradigm in the search for innovative anti-TB drugs. NADH:menaquinone oxidoreductase is a non-proton translocating type II NADH dehydrogenase (NDH-2) that is an essential enzyme in the respiratory chain of Mtb and is not found in mammalian mitochondria. Phenothiazines (PTZs) represent one of the most known class of NDH-2 inhibitors, but their use as anti-TB drugs is currently limited by the wide range of potentially serious off-target effects. In this work, we designed and synthesized a series of new PTZs by decorating the scaffold in an unconventional way, introducing various halogen atoms. By replacing the sulfur atom with selenium, a dibromophenoselenazine 20 was also synthesized. Among the synthesized poly-halogenated PTZs (HPTZs), dibromo and tetrachloro derivatives 9 and 11, along with the phenoselenazine 20, emerged with a better anti-TB profile than the therapeutic thioridazine (TZ). They targeted non-replicating Mtb, were bactericidal, and synergized with rifampin and bedaquiline. Moreover, their anti-TB activity was found to be related to the NDH-2 inhibition. Most important, they showed a markedly reduced affinity to dopaminergic and serotonergic receptors respect to the TZ. From this work emerged, for the first time, as the poly-halogenation of the PTZ core, while permitting to maintain good anti-TB profile could conceivably lead to fewer CNS side-effects risk, making more tangible the use of PTZs for this alternative therapeutic application.

Keywords
Halogenated-phenothiazines; NDH-2; Phenoselenazine; Phenothiazines; Respiratory chain; Tuberculosis.