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Inhibitors of malaria parasite cyclic nucleotide phosphodiesterases block asexual blood-stage development and mosquito transmission

  • Paula Josefina Gomez-Gonzalez
  • , Antima Gupta
  • , Laura G. Drought
  • , Avnish Patel
  • , John Okombo
  • , Mariëtte van der Watt
  • , Ryan Walker-Gray
  • , Kyra A. Schindler
  • , Anna Y. Burkhard
  • , Tomas Yeo
  • , Sunil K. Narwal
  • , Talia S. Bloxham
  • , Christian Flueck
  • , Eloise M. Walker
  • , Joshua A. Rey
  • , Kate J. Fairhurst
  • , Janette Reader
  • , Heekuk Park
  • , Harry G. Pollard
  • , Lindsay B. Stewart
  • Luke Brandner-Garrod, Mojca Kristan, Geert Jan Sterk, Youri M. van Nuland, Emilia Manko, Donelly A. van Schalkwyk, Yang Zheng, Rob Leurs, Koen J. Dechering, Anna Caroline C. Aguiar, Rafael V.C. Guido, Dhelio B. Pereira, Patrick K. Tumwebaze, Samuel L. Nosbya, Philip J. Rosenthal, Roland A. Cooper, Mike Palmer, Tanya Parkinson, Jeremy N. Burrows, Anne Catrin Uhlemann, Lyn Marié Birkholtz, Jennifer L. Small-Saunders, James Duffy, David A. Fidock, Alan Brown, Mark Gardner*, David A. Baker*
*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Cyclic nucleotide–dependent phosphodiesterases (PDEs) play essential roles in regulating the malaria parasite life cycle, suggesting that they may be promising antimalarial drug targets. PDE inhibitors are used safely to treat a range of noninfectious human disorders. Here, we report three subseries of fast-acting and potent Plasmodium falciparum PDEβ inhibitors that block asexual blood-stage parasite development and that are also active against human clinical isolates. Two of the inhibitor subseries also have potent transmission-blocking activity by targeting PDEs expressed during sexual parasite development. In vitro drug selection experiments generated parasites with moderately reduced susceptibility to the inhibitors. Whole-genome sequencing of these parasites detected no mutations in PDEβ but rather mutations in downstream effectors: either the catalytic or regulatory subunits of cyclic adenosine monophosphate–dependent protein kinase (PKA) or in the 3-phosphoinositide-dependent protein kinase that is required for PKA activation. Several properties of these P. falciparum PDE inhibitor series make them attractive for further progression through the antimalarial drug discovery pipeline.

Original languageEnglish
Article numbereadq1383
Pages (from-to)1-19
JournalScience advances
Volume10
Issue number49
Early online date6 Dec 2024
DOIs
Publication statusPublished - 6 Dec 2024

Bibliographical note

Publisher Copyright:
Copyright © 2024 The Authors, some rights reserved

Funding

We would like to thank G. Henriques for training staff in handling P. falciparum. We are grateful to M. Blackman (Francis Crick Institute) and A. Bell (Salvensis) for discussions on aspects of this work. We would like to thank the CRO synthetic chemists and drug discovery biologists at TCG-LS for making the compounds used in this study and performing key assays. We would also like to thank E. Chenu and D. Baud at MMV for logistical support during the project. We are grateful to W. Chen (MSc placement student from University College, London) for assistance with initial screening of compounds for activity against Plasmodium PDE activity. We are grateful to C. Sutherland for facilitating the SMFA experiments carried out in the Human Malaria Transmission Facility at LSHTM. We would like to thank M. Noe from Pfizer for helping arrange the release of information and compounds to LSHTM and also J. Warmus, M. Troutman, J. Mills, and I. Reza for arranging to have ADME properties tested on selected compounds at Pfizer. We are grateful to the Wellcome Trust for Innovator (209367/Z/17/Z and 223849/Z/21/Z) and Investigator Awards (106240/Z/14/Z and 220318/Z/20/Z) to D.A.B. and the Biomedical Resources Grant (221363/Z/20/Z) that supports the Human Malaria Transmission Facility at LSHTM. Resistance selection studies and research on Ugandan parasites were supported in part by the US National Institutes of Health (R01 AI185559 to D.A.F., R01 AI1075045 and R01 AI139179 to P.J.R., and K08AI163497 to J.L.S.-S.) and the Bill & Melinda Gates Foundation (INV-033538 to D.A.F.). D.A.F., D.A.B., L.-M.B., and P.J.R. also acknowledge support from the Medicines for Malaria Venture. Acknowledgments: We would like to thank G. henriques for training staff in handling P. falciparum. We are grateful to M. Blackman (Francis crick institute) and A. Bell (Salvensis) for discussions on aspects of this work. We would like to thank the cRO synthetic chemists and drug discovery biologists at tcG-lS for making the compounds used in this study and performing key assays. We would also like to thank e. chenu and D. Baud at MMv for logistical support during the project. We are grateful to W. chen (MSc placement student from University college, london) for assistance with initial screening of compounds for activity against Plasmodium PDe activity. We are grateful to c. Sutherland for facilitating the SMFA experiments carried out in the human Malaria transmission Facility at lShtM. We would like to thank M. noe from Pfizer for helping arrange the release of information and compounds to lShtM and also J. Warmus, M. troutman, J. Mills, and i. Reza for arranging to have ADMe properties tested on selected compounds at Pfizer. Funding: We are grateful to the Wellcome trust for innovator (209367/Z/17/Z and 223849/Z/21/Z) and investigator Awards (106240/Z/14/Z and 220318/Z/20/Z) to D.A.B. and the Biomedical Resources Grant (221363/Z/20/Z) that supports the human Malaria transmission Facility at lShtM. Resistance selection studies and research on Ugandan parasites were supported in part by the US national institutes of health (R01 Ai185559 to D.A.F., R01 Ai1075045 and R01 Ai139179 to P.J.R., and K08Ai163497 to J.l.S.-S.) and the Bill & Melinda Gates Foundation (inv-033538 to D.A.F.).

FundersFunder number
London School of Hygiene and Tropical Medicine
Human Malaria Transmission Facility
Medicines for Malaria Venture
University College
Pfizer
National Institutes of HealthR01 Ai139179, K08Ai163497, R01 Ai185559, R01 Ai1075045
Wellcome Trust for Innovator106240/Z/14/Z, 209367/Z/17/Z, 221363/Z/20/Z, 220318/Z/20/Z, 223849/Z/21/Z
Bill and Melinda Gates FoundationINV-033538

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