All A·WOL Publications to Date

Publications: A·WOL III: Macrofilaricide Drug Discovery & Development

Kelly L. Johnston1,*, Darren A. N. Cook1,*, Neil G. Berry2,*, W. David Hong2,*, Rachel H. Clare1, Megan Goddard1, Louise Ford1, Gemma L. Nixon2, Paul M. O’Neill2, Stephen A. Ward1 and Mark J. Taylor1,† Science Advances 27 Sep 2017: Vol. 3, no. 9, eaao1551 DOI: 10.1126/sciadv.aao1551 Identification and prioritization of novel anti-Wolbachia chemotypes from screening a 10,000-compound diversity library

Ghaith Aljayyoussi, Hayley E. Tyrer, Louise Ford, Hanna Sjoberg, Nicolas Pionnier, David Waterhouse, Jill Davies, Joanne Gamble, Haelly Metugene, Darren A. N. Cook, Andrew Steven, Raman Sharma, Ana F. Guimaraes, Rachel H. Clare, Andrew Cassidy, Kelly L. Johnston, Laura Myhill, Laura Hayward, Samuel Wanji, Joseph D. Turner, Mark J. Taylor & Stephen A. Ward. Scientific Reports 7, Article number: 210 (2017) Short-Course, High-Dose Rifampicin Achieves Wolbachia Depletion Predictive of Curative Outcomes in Preclinical Models of Lymphatic Filariasis and Onchocerciasis

Ute Klarmann-Schulz , Sabine Specht  , Alexander Yaw Debrah , Linda Batsa, Nana Kwame Ayisi-Boateng, Jubin Osei-Mensah, Yusif Mubarik, Peter Konadu, Arcangelo Ricchiuto, Rolf Fimmers, Sandra Arriens, Bettina Dubben, Louise Ford, Mark Taylor, Achim Hoerauf. (2017) Comparison of Doxycycline, Minocycline, Doxycycline plus Albendazole and Albendazole Alone in Their Efficacy against Onchocerciasis in a Randomized, Open-Label, Pilot Trial

Gleave, Katherine, Cook, Darren, Taylor, Mark J. and Reimer, Lisa J. (2016) 'Filarial infection influences mosquito behaviour and fecundity'. Scientific Reports, Vol 6, Issue 36319.

Tamarozzi, Francesca, Turner, Joseph, Pionnier, Nicolas, Midgley, Angela, Guimaraes, Ana, Johnston, Kelly, Edwards, Steven W and Taylor, Mark (2016) 'Wolbachia endosymbionts induce neutrophil extracellular trap formation in human onchocerciasis'. Scientific Reports, Vol 6, p. 35559.

Sharma R, Al Jayoussi G, Tyrer HE, Gamble J, Hayward L, Guimaraes AF, Davies J, Waterhouse D, Cook DA, Myhill LJ, Clare RH, Cassidy A, Steven A, Johnston KL, Ford L, Turner JD, Ward SA, Taylor MJ. Sci Rep. 2016 Mar 21;6:23458. doi: 10.1038/srep23458. Minocycline as a re-purposed anti-Wolbachia macrofilaricide: superiority compared with doxycycline regimens in a murine infection model of human lymphatic filariasis.

Halliday A, Turner JD, Guimarães A, Bates PA, Taylor MJ Parasit Vectors. 2016 Feb 20;9:96. doi: 10.1186/s13071-016-1381-0. The TLR2/6 ligand PAM2CSK4 is a Th2 polarizing adjuvant in Leishmania major and Brugia malayi murine vaccine models.

Frempong KK, Walker M, Cheke RA, Tetevi EJ, Gyan ET, Owusu EO, Wilson MD, Boakye DA, Taylor MJ, Biritwum NK, Osei-Atweneboana M, Basáñez MG. Clin Infect Dis. 2016 Jun 1;62(11):1338-47. doi: 10.1093/cid/ciw144. Epub 2016 Mar 21. Does Increasing Treatment Frequency Address Suboptimal Responses to Ivermectin for the Control and Elimination of River Blindness?

Publications: A·WOL II: Discovery & Development of Macrofilaricidal Drugs & Regimens

Sarkies, Peter, Selkirk, Murray E., Jones, John T., Blok, Vivian, Boothby, Thomas, Goldstein, Bob, Hanelt, Ben, Ardila-Garcia, Alex, Fast, Naomi M., Schiffer, Phillip M., Kraus, Christopher, Taylor, Mark, Koutsovoulos, Georgios, Blaxter, Mark L. and Miska, Eric A. (2015) 'Ancient and Novel Small RNA Pathways Compensate for the Loss of piRNAs in Multiple Independent Nematode Lineages'. PLoS Biology, Vol 13, Issue 2, e1002061.

Molyneux DH, Ward SA. (2015) Reflections on the Nobel Prize for Medicine 2015 - The Public Health Legacy and Impact of Avermectin and Artemisinin. Trends Parasitol. 2015 Nov 6. pii: S1471-4922(15)00231-7. doi: 10.1016/j.pt.2015.10.008.

Lisa J Reimer, Emily R Adams, Mark JI Paine, Hilary Ranson, Marlize Coleman, Edward K Thomsen, Eleanor E MacPherson, T Deirdre Hollingsworth, Louise A Kelly-Hope, Moses J Bockarie, Louise Ford, Robert A Harrison, J Russell Stothard, Mark J Taylor, Nicholas Hamon and Stephen J Torr. Fit for purpose: do we have the right tools to sustain NTD elimination? BMC Proceedings 2015, 9(Suppl 10):S5 doi:10.1186/1753-6561-9-S10-S5 Published: 18 December 2015.

Walker M, Specht S, Churcher TS, Hoerauf A, Taylor MJ, Basáñez MG. (2015) Therapeutic efficacy and macrofilaricidal activity of doxycycline for the treatment of river blindness. Clin Infect Dis. 2015 60(8):1199-207.

Clare RH, Cook DA, Johnston KL, Ford L, Ward SA, Taylor MJ. (2015) Development and validation of a high-throughput anti-Wolbachia whole-cell screen: a route to macrofilaricidal drugs against onchocerciasis and lymphatic filariasis. J Biomol Screen. 2015 20(1):64-9.

Vollmer J, Schiefer A, Schneider T, Jülicher K, Johnston KL, Taylor MJ, Sahl HG, Hoerauf A, Pfarr K. Requirement of lipid II biosynthesis for cell division in cell wall-less Wolbachia, endobacteria of arthropods and filarial nematodes. Int J Med Microbiol. 2013 Apr;303(3):140-9.

Ioannidis P, Johnston KL, Riley DR, Kumar N, White JR, Olarte KT, Ott S, Tallon LJ, Foster JM, Taylor MJ, Dunning Hotopp JC. BMC Genomics. 2013 Sep 22;14:639. doi: 10.1186/1471-2164-14-639. Extensively duplicated and transcriptionally active recent lateral gene transfer from a bacterial Wolbachia endosymbiont to its host filarial nematode Brugia malayi

Foster JM, Landmann F, Ford L, Johnston KL, Elsasser SC, Schulte-Hostedde AI, Taylor MJ, Slatko BE. Parasit Vectors. 2014 Mar 31;7:140. doi: 10.1186/1756-3305-7-140. Absence of Wolbachia endobacteria in the human parasitic nematode Dracunculus medinensis and two related Dracunculus species infecting wildlife.

Tamarozzi F, Wright HL, Johnston KL, Edwards SW, Turner JD, Taylor MJ. Parasite Immunol. 2014 Oct;36(10):494-502. doi: 10.1111/pim.12122. Human filarial Wolbachia lipopeptide directly activates human neutrophils in vitro.

Voronin D, Guimarães AF, Molyneux GR, Johnston KL, Ford L, Taylor MJ Parasit Vectors. 2014 Oct 6;7:462. doi: 10.1186/s13071-014-0462-1. Wolbachia lipoproteins: abundance, localisation and serology of Wolbachia peptidoglycan associated lipoprotein and the Type IV Secretion System component, VirB6 from Brugia malayi and Aedes albopictus.

Johnston KL, Ford L, Umareddy I, Townson S, Specht S, Pfarr K, Hoerauf A, Altmeyer R, Taylor MJ Int J Parasitol Drugs Drug Resist. 2014 Sep 16;4(3):278-86. doi: 10.1016/j.ijpddr.2014.09.001. eCollection 2014. Repurposing of approved drugs from the human pharmacopoeia to target Wolbachia endosymbionts of onchocerciasis and lymphatic filariasis.

Halliday A, Guimaraes AF, Tyrer HE, Metuge HM, Patrick CN, Arnaud KO Kwenti TD, Forsbrook G, Steven A, Cook D, Enyong P, Wanji S, Taylor MJ, Turner JD. Parasit Vectors. 2014 Oct 24;7:472. doi: 10.1186/s13071-014-0472-z. A murine macrofilaricide pre-clinical screening model for onchocerciasis and lymphatic filariasis.

Landmann F, Bain O, Martin C, Uni S, Taylor MJ, Sullivan W Biol Open. 2012 Jun 15;1(6):536-47. doi: 10.1242/bio.2012737. Epub 2012 Apr 18. Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes.

Schroeder JH, Simbi BH, Ford L, Cole SR, Taylor MJ, Lawson C, Lawrence RA. PLoS Negl Trop Dis. 2012;6(11):e1914. doi: 10.1371/journal.pntd.0001914. Epub 2012 Nov 29. Live Brugia malayi microfilariae inhibit transendothelial migration of neutrophils and monocytes.

Wu B, Novelli J, Jiang D, Dailey HA, Landmann F, Ford L, Taylor MJ, Carlow CK, Kumar S, Foster JM, Slatko BE. Proc Natl Acad Sci U S A. 2013 May 7;110(19):7748-53. doi: 10.1073/pnas.1304049110. Epub 2013 Apr 22. Interdomain lateral gene transfer of an essential ferrochelatase gene in human parasitic nematodes.

Reviews

Taylor MJ, Voronin D, Johnston KL, Ford L. Wolbachia filarial interactions. Cell Microbiol. 2013 Apr;15(4):520-6. doi: 10.1111/cmi.12084. Epub 2012 Dec 24.

Mark J. Taylor, Louise Ford, Achim Hoerauf, Ken Pfarr, Jeremy M. Foster, Sanjay Kumar and Barton E. Slatko. 2012. Drugs and Targets to Perturb the Symbiosis of Wolbachia and Filarial Nematodes. In Parasitic Helminths: Targets, Screens, Drugs, and Vaccines

Johnston KL, Ford L, Taylor MJ. J Biomol Screen. 2014 Mar;19(3):335-43. doi: 10.1177/1087057113511270. Epub 2013 Nov 15. Overcoming the challenges of drug discovery for neglected tropical diseases: the A·WOL experience.

Taylor MJ, Hoerauf A, Townson S, Slatko BE, Ward SA. Parasitology. 2014 Jan;141(1):119-27. doi: 10.1017/S0031182013001108. Epub 2013 Jul 18. Anti-Wolbachia drug discovery and development: safe macrofilaricides for onchocerciasis and lymphatic filariasis.

Publications: A∙WOL I: Anti Symbiotic Treatment of Filariasis

Johnston, Kelly, Wu, B., Guimaraes, A., Ford, Louise, Ambrose, Pauline, Slatko, B. E. and Taylor, Mark (2008) 'Globomycin: A New Class of Drug with Efficacy against Wolbachia and Filarial Nematodes'. American Journal of Tropical Medicine and Hygiene, Vol 79, Issue 6 Sup., p. 128

Turner JD, Tendongfor N, Esum M, Johnston KL, Langley RS, Ford L, Faragher B, Specht S, Mand S, Hoerauf A, Enyong P, Wanji S, Taylor MJ. (2010) Macrofilaricidal activity after doxycycline only treatment of Onchocerca volvulus in an area of Loa loa co-endemicity: a randomized controlled trial. PLoS Neglected Tropical Diseases, 4 (4): e660

Landmann F, Foster JM, Slatko B, Sullivan W. (2010) Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues. PLoS Neglected Tropical Diseases, 4(7): e758

Strübing U, Lucius R, Hoerauf A, Pfarr KM. (2010) Mitochondrial genes for heme-dependent respiratory chain complexes are up-regulated after depletion of Wolbachia from filarial nematodes. International Journal for Parasitology, 40(10): 1193-202.

Johnston KL, Wu B, Guimarães A, Ford L, Slatko BE, Taylor MJ. (2010) Lipoprotein biosynthesis as a target for anti-Wolbachia treatment of filarial nematodes. Parasites and Vectors. 3:99

Wanji S, Tendongfor N, Nji T, Esum M, Che JN, Nkwescheu A, Alassa F, Kamnang G, Enyong PA, Taylor MJ, Hoerauf A and Taylor DW (2009). Community-directed delivery of doxycycline for the treatment of onchocerciasis in areas of co-endemicity with loiasis in Cameroon. Parasites and Vectors 2: 39.

Turner JD, Langley RS, Johnston KL, Gentil K, Ford L, Wu B, Graham M, Sharpley F, Slatko B, Pearlman E andTaylor MJ (2009). Wolbachia lipoprotein stimulates innate and adaptive immunity through Toll-like receptors 2 and 6 to induce disease manifestations of filariasis. Journal of Biological Chemistry 284: 22364-22378.

Taylor MJ, Awadzi K, Basáñez MG, Biritwum N, Boakye D, Boatin B, Bockarie M, Churcher TS, Debrah A, Edwards G, Hoerauf A, Mand S, Matthews G, Osei-Atweneboana M, Prichard RK, Wanji S and Adjei O (2009). Onchocerciasis Control: Vision for the Future from a Ghanian perspective. Parasites and Vectors 2: 7.

Foster J, Kumar S, Ford L, Johnston KL, Ben R, Graeff-Teixeira C and Taylor MJ (2008). Absence of Wolbachia endobacteria in the non-filariid nematodes Angiostrongylus cantonensis and A. costaricensis. Parasites and Vectors1: 31.

Tamarozzi F, Tendongfor N, Enyong PA, Esum M, Faragher B, Wanji S, Taylor MJ.
Parasit Vectors. 2012 Mar 20;5:53. doi: 10.1186/1756-3305-5-53. Long term impact of large scale community-directed delivery of doxycycline for the treatment of onchocerciasis.

Landmann F, Voronin D, Sullivan W, Taylor MJ. PLoS Pathog. 2011 Nov;7(11):e1002351. doi: 10.1371/journal.ppat.1002351. Epub 2011 Nov 3. Anti-filarial activity of antibiotic therapy is due to extensive apoptosis after Wolbachia depletion from filarial nematodes.

Debrah AY, Mand S, Marfo-Debrekyei Y, Batsa L, Pfarr K, Lawson B, Taylor M, Adjei O, Hoerauf A.
Am J Trop Med Hyg. 2009 Jun;80(6):956-63. Reduction in levels of plasma vascular endothelial growth factor-A and improvement in hydrocele patients by targeting endosymbiotic Wolbachia sp. in Wuchereria bancrofti with doxycycline.

Holman AG, Davis PJ, Foster JM, Carlow CK, Kumar S. BMC Microbiol. 2009 Nov 28;9:243. doi: 10.1186/1471-2180-9-243. Computational prediction of essential genes in an unculturable endosymbiotic bacterium, Wolbachia of Brugia malayi.

Voronin D, Cook DA, Steven A, Taylor MJ.
Proc Natl Acad Sci U S A. 2012 Jun 19;109(25):E1638-46. doi: 10.1073/pnas.1203519109. Epub 2012 May 29. Autophagy regulates Wolbachia populations across diverse symbiotic associations.

Schiefer A1, Schmitz A, Schäberle TF, Specht S, Lämmer C, Johnston KL, Vassylyev DG, König GM, Hoerauf A, Pfarr KJ Infect Dis. 2012 Jul 15;206(2):249-57. doi: 10.1093/infdis/jis341. Epub 2012 May 14. Corallopyronin A specifically targets and depletes essential obligate Wolbachia endobacteria from filarial nematodes in vivo.

Reviews

Slatko BE, Taylor MJ, Foster JM. (2010) The Wolbachia endosymbiont as an anti-filarial nematode target. Symbiosis, 51(1): 55-65.

Taylor MJ, Hoerauf A, Bockarie M. (2010) Lymphatic filariasis and onchocerciasis. Lancet, 2; 376(9747):1175-85.

Bockarie MJ1, Taylor MJ, Gyapong JO. Expert Rev Anti Infect Ther. 2009 Jun;7(5):595-605. doi: 10.1586/eri.09.36. Current practices in the management of lymphatic filariasis.

Tamarozzi F, Halliday A, Gentil K, Hoerauf A, Pearlman E, Taylor MJ.Clin Microbiol Rev. 2011 Jul;24(3):459-68. doi: 10.1128/CMR.00057-10. Onchocerciasis: the role of Wolbachia bacterial endosymbionts in parasite biology, disease pathogenesis, and treatment.