A short-term treatment with BKI-1294 does not protect foetuses from sheep experimentally infected with Neospora caninum tachyzoites during pregnancy

Roberto Sánchez-Sánchez1, Ignacio Ferre1, Michela Re1,2, Bárbara Pérez-Arroyo1, Darío Cleofé-Resta1, Victor Herrero García2, Manuel Pizarro Díaz2, Luis Miguel Ferrer3, Hector Ruiz3, Raquel Vallejo-García4, Julio Benavides4, Matthew A. Hulverson5, Ryan Choi5, Grant R. Whitman5, Andrew Hemphill6, Wesley C. Van Voorhis5, Luis Miguel Ortega-Mora1
1SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040, Madrid, Spain
2Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040 Madrid, Spain
3Departamento de Patología Animal, Facultad de Veterinaria C/ Miguel Servet 177, 50013 Zaragoza, Spain
4Instituto de Ganadería de Montaña (CSIC-Universidad de León), León, Spain
5Center for Emerging and Re-emerging Infectious Diseases (CERID), Division of Allergy and Infectious Diseases, Department of Medicine, University of Washington, 98109-4766, Seattle, WA, USA
6Institute of Parasitology, Vetsuisse Faculty, University of Bern, Länggass-Strasse 122, CH-3012 Berne, Switzerland

Tài liệu tham khảo

Aguado-Martínez, 2008, Usefulness of rNcGRA7- and rNcSAG4-based ELISA tests for distinguishing primo-infection, recrudescence, and chronic bovine neosporosis, Vet. Parasitol., 157, 182, 10.1016/j.vetpar.2008.08.002 Álvarez-García, 2003, Influence of age and purpose for testing on the cut-off selection of serological methods in bovine neosporosis, Vet. Res., 34, 341, 10.1051/vetres:2003009 Álvarez-García, 2002, Pattern of recognition of Neospora caninum tachyzoite antigens by naturally infected pregnant cattle and aborted foetuses, Vet. Parasitol., 107, 15, 10.1016/S0304-4017(02)00091-2 Arranz-Solís, 2015, Influence of the gestational stage on the clinical course, lesional development and parasite distribution in experimental ovine neosporosis, Vet. Res., 46, 10.1186/s13567-014-0139-y Buxton, 1998, The pathogenesis of experimental neosporosis in pregnant sheep, J. Comp. Pathol., 118, 267, 10.1016/S0021-9975(07)80003-X Cardew, 2018, The calcium-dependent protein kinase 1 from Toxoplasma gondii as target for structure-based drug design, Parasitology, 145, 210, 10.1017/S0031182017001901 Choi, 2020, Bumped kinase inhibitors as therapy for apicomplexan parasitic diseases: lessons learned, Int. J. Parasitol., 50, 413, 10.1016/j.ijpara.2020.01.006 Collantes-Fernández, 2002, Quantitative detection of Neospora caninum in bovine aborted fetuses and experimentally infected mice by real-time PCR, J. Clin. Microbiol., 40, 1194, 10.1128/JCM.40.4.1194-1198.2002 Diffay, 2002, Handling and examination of sheep and goats, 1 Dong, 2013, Development of two murine antibodies against Neospora caninum using phage display technology and application on the detection of N. caninum, PLoS One, 8 Dubey, 2017 Dubey, 2011, Neosporosis in animals—the last five years, Vet. Parasitol., 180, 90, 10.1016/j.vetpar.2011.05.031 Entrican, 2002, Immune regulation during pregnancy and host-pathogen interactions in infectious abortion, J. Comp. Pathol., 126, 79, 10.1053/jcpa.2001.0539 González-Warleta, 2018, Endogenous transplacental transmission of Neospora caninum during successive pregnancies across three generations of naturally infected sheep, Vet. Res., 49, 10.1186/s13567-018-0601-3 González-Warleta, 2014, Neospora caninum infection as a cause of reproductive failure in a sheep flock, Vet. Res., 45, 10.1186/s13567-014-0088-5 Gutierrez, 2012, Application of quantitative real-time polymerase chain reaction for the diagnosis of toxoplasmosis and enzootic abortion of ewes, J. Vet. Diagn. Invest., 24, 846, 10.1177/1040638712452730 Haerdi, 2006, Humoral immune reaction of newborn calves congenitally infected with Neospora caninum and experimentally treated with toltrazuril, Parasitol. Res., 99, 534, 10.1007/s00436-006-0199-7 Horcajo, 2016, Vaccines for bovine neosporosis: current status and key aspects for development, Parasite Immunol., 38, 709, 10.1111/pim.12342 Howe, 1998, The p29 and p35 immunodominant antigens of Neospora caninum tachyzoites are homologous to the family of surface antigens of Toxoplasma gondii, Infect. Immun., 66, 5322, 10.1128/IAI.66.11.5322-5328.1998 Huertas-López, 2021, Development and validation of a time-resolved fluorescence immunoassay for the detection of anti-Toxoplasma gondii antibodies in goats, Vet. Parasitol., 293, 109432, 10.1016/j.vetpar.2021.109432 Innes, 2007, The host-parasite relationship in pregnant cattle infected with Neospora caninum, Parasitology, 134, 1903, 10.1017/S0031182007000194 Innes, 2007, Neospora caninum emerges from the shadow of Toxoplasma gondii, Trends Parasitol., 23, 43, 10.1016/j.pt.2006.12.004 Kieschnick, 2001, Toxoplasma gondii attachment to host cells is regulated by a calmodulin-like domain protein kinase, J. Biol. Chem., 276, 12369, 10.1074/jbc.M011045200 Kritzner, 2002, An explorative study to assess the efficacy of toltrazuril-sulfone (ponazuril) in calves experimentally infected with Neospora caninum, Ann. Clin. Microbiol. Antimicrob., 1, 4, 10.1186/1476-0711-1-4 Lourido, 2010, Calcium-dependent protein kinase 1 is an essential regulator of exocytosis in Toxoplasma, Nature, 465, 359, 10.1038/nature09022 Lourido, 2012, Distinct signalling pathways control Toxoplasma egress and host-cell invasion, EMBO J., 31, 4524, 10.1038/emboj.2012.299 McAllister, 1996, Experimental neosporosis in pregnant ewes and their offspring, Vet. Pathol., 33, 647, 10.1177/030098589603300603 Müller, 2013, New approaches for the identification of drug targets in protozoan parasites, Int. Rev. Cell. Mol. Biol., 301, 359, 10.1016/B978-0-12-407704-1.00007-5 Mineo, 2010, Neospora caninum excreted/secreted antigens trigger CC-chemokine receptor 5-dependent cell migration, Int. J. Parasitol., 40, 797, 10.1016/j.ijpara.2009.12.003 Müller, 2017, Two novel calcium-dependent kinase 1-inhibitors interfere with vertical transmission in mice infected with Neospora caninum tachyzoites, Antimicrob. Agents Chemother., 10.1128/AAC.02324-16 Müller, 1996, Diagnosis of Neospora caninum and Toxoplasma gondii infection by PCR and DNA hybridization immunoassay, J. Clin. Microbiol., 34, 2850, 10.1128/jcm.34.11.2850-2852.1996 Murphy, 2010, Discovery of potent and selective inhibitors of CDPK1 from C. parvum and T. gondii, ACS Med. Chem. Lett., 1, 331, 10.1021/ml100096t Ojo, 2013, A specific inhibitor of pf CDPK4 blocks malaria transmission: chemical-genetic validation, J. Infect. Dis., 209, 275, 10.1093/infdis/jit522 Ojo, 2010, Toxoplasma gondii calcium-dependent protein kinase 1 is a target for selective kinase inhibitors, Nat. Struct. Mol. Biol., 17, 602, 10.1038/nsmb.1818 Sánchez-Sánchez, 2018, Influence of dose and route of administration on the outcome of infection with the virulent Neospora caninum isolate Nc-Spain7 in pregnant sheep at mid-gestation, Vet. Res., 49, 42, 10.1186/s13567-018-0539-5 Sánchez-Sánchez, 2018, Safety and efficacy of the bumped kinase inhibitor BKI-1553 in pregnant sheep experimentally infected with Neospora caninum tachyzoites, Int. J. Parasitol. Drugs. Drug. Resist., 8, 112, 10.1016/j.ijpddr.2018.02.003 Sánchez-Sánchez, 2019, Treatment with bumped kinase inhibitor 1294 is safe and leads to significant protection against abortion and vertical transmission in sheep experimentally infected with Toxoplasma gondii during pregnancy, Antimicrob. Agents Chemother., 63, 10.1128/AAC.02527-18 Sánchez-Sánchez, 2018, Treatment of toxoplasmosis and neosporosis in farm ruminants: state of knowledge and future trends, Curr. Top. Med. Chem., 18, 1304, 10.2174/1568026618666181002113617 Schaefer, 2016, Novel bumped kinase inhibitors are safe and effective therapeutics in the calf clinical model for cryptosporidiosis, J. Infect. Dis., 214, 1856, 10.1093/infdis/jiw488 Syed-Hussain, 2015, Study on the use of toltrazuril to eliminate Neospora caninum in congenitally infected lambs born from experimentally infected ewes, Vet. Parasitol., 210, 141, 10.1016/j.vetpar.2015.03.019 Tatipaka, 2014, Substituted 2-phenylimidazopyridines: a new class of drug leads for human African trypanosomiasis, J. Med. Chem., 57, 828, 10.1021/jm401178t Van Voorhis, 2017, Extended-spectrum antiprotozoal bumped kinase inhibitors: a review, Exp. Parasitol., 180, 71, 10.1016/j.exppara.2017.01.001 Van Voorhis, 2021, One health therapeutics: target-based drug development for cryptosporidiosis and other apicomplexa diseases, Vet. Parasitol., 289, 109336, 10.1016/j.vetpar.2020.109336 Vanleeuwen, 2011, Monensin use against Neospora caninum challenge in dairy cattle, Vet. Parasitol., 175, 372, 10.1016/j.vetpar.2010.10.016 Vidadala, 2016, Development of an orally available and central nervous system (CNS) penetrant Toxoplasma gondii calcium-dependent protein kinase 1 (tg CDPK1) inhibitor with minimal human ether-a-go-go-related gene (hERG) activity for the treatment of toxoplasmosis, J. Med. Chem., 59, 6531, 10.1021/acs.jmedchem.6b00760 Walker, 2017, Placental transporter localization and expression in the human: the importance of species, sex, and gestational age differences, Biol. Reprod., 96, 733, 10.1093/biolre/iox012 West, 2006, A possible role for Neospora caninum in ovine abortion in New Zealand, Small Rumin. Res., 62, 135, 10.1016/j.smallrumres.2005.07.041 Weston, 2009, Dose-titration challenge of young pregnant sheep with Neospora caninum tachyzoites, Vet. Parasitol., 164, 183, 10.1016/j.vetpar.2009.05.013 Williams, 2009, Endogenous and exogenous transplacental transmission of Neospora caninum - how the route of transmission impacts on epidemiology and control of disease, Parasitology, 136, 1895, 10.1017/S0031182009990588 Winzer, 2020, Neospora caninum: structure and fate of multinucleated complexes induced by the bumped kinase inhibitor BKI-1294, Pathogens, 9, 382, 10.3390/pathogens9050382 Winzer, 2020, Neospora caninum: differential proteome of multinucleated complexes induced by the bumped kinase inhibitor BKI-1294, Microorganisms, 8, 801, 10.3390/microorganisms8060801 Winzer, 2015, In vitro and in vivo effects of the bumped kinase inhibitor 1294 in the related cyst-forming apicomplexans Toxoplasma gondii and Neospora caninum, Antimicrob. Agents Chemother., 59, 6361, 10.1128/AAC.01236-15