The adaptive potential of a survival artist: Characterization of the in vitro interactions of Toxoplasma gondii tachyzoites with di-cationic compounds in human fibroblast cell cultures

Parasitology

Volumn 139, Issue 2, 2012, Pages 208-220

  Kropf, Christian ^a   Debache, Karim ^a   Rampa, Christoph ^a   Barna, Fabienne ^a   Schorer, Michelle ^a   Stephens, Chad E ^b   Ismail, Mohamed A ^c,d   Boykin, David W ^c   Hemphill, Andrew ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b AUGUSTA STATE UNIVERSITY   (United States)

^c GEORGIA STATE UNIVERSITY   (United States)

^d KING FAISAL UNIVERSITY   (Saudi Arabia)

Author keywords

arylimidamides; di cationic pentamidine analogues; in vitro models; proliferation; tachyzoites; Toxoplasma gondii

Indexed keywords

AMIDE; ANTIPROTOZOAL AGENT; DB 1127; DB 1282; DB 1341; DB 1362; DB 1407; DB 1450; DB 1479; DB 1980; DB 1996; DB 1997; DB 2001; DB 2002; DB 2006; DB 2007; DB 2018; DB 666; DB 667; DB 702; DB 710; DB 745; DB 750; DB 780; DB 786; DB 865; DB 891; DB 930; PENTAMIDINE DERIVATIVE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADAPTATION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIPROTOZOAL ACTIVITY; ARTICLE; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG SCREENING; DRUG STRUCTURE; FIBROBLAST; FIBROBLAST CULTURE; HOST CELL; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; MOLECULAR WEIGHT; MONOLAYER CULTURE; NONHUMAN; PARASITE SURVIVAL; PRIORITY JOURNAL; TACHYZOITE; TOXOPLASMA GONDII; TRANSMISSION ELECTRON MICROSCOPY;

AMIDINES; ANIMALS; ANTIPROTOZOAL AGENTS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; FIBROBLASTS; FURANS; HUMANS; MOLECULAR STRUCTURE; PYRIDINES; TOXOPLASMA; VERO CELLS;

TOXOPLASMA GONDII;

EID: 84856843507     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011001776     Document Type: Article

References (43)

1. Barratt, J. L., Harkness, J., Marriott, D., Ellis, J. T. and Stark, D. (2010). Importance of nonenteric protozoan infections in immunocompromised people. Clinical Microbiology Reviews 23, 795-836.
2. Batista, D. G., Batista, M. M., De Oliveira, G. M., do Amaral, P. B., Lannes-Vieira, J., Britto, C. C., Junqueira, A., Lima, M. M., Romanha, A. J., Sales Junior, P. A., Stephens, C. E., Boykin, D.W. and Soeiro, M. N. (2010a). ArylimidamiDe DB766, a potential chemotherapeutic candidate for Chagas' disease treatment. Antimicrobial Agents and Chemotherapy 54, 2940-2952.
3. Batista, D. G., Pacheco, M. G., Kumar, A., Branowska, D., Ismail, M. A., Hu, L., Boykin, D.W., and Soeiro, M. N. (2010b). Biological, ultrastructural effect and subcellular localization of aromatic diamidines in Trypanosoma cruzi. Parasitology 137, 251-259.
4. Bougdour, A., Braun, L., Cannella, D. and Hakimi, M. A. (2010). Chromatin modifications: implications in the regulation of gene expression in Toxoplasma gondii. Cellular Microbiology 12, 413-423.
5. Buckner, F. S. and Navabi, N. (2010). AdVances in Chagas disease drug development: 2009-2010. Current Opinion in Infectious Diseases 23, 609-616.
6. Carruthers, V. B., and Suzuki, Y. (2007). Effects of Toxoplasma gondii infection on the brain. Schizophreny Bulletin 33, 745-751. (Pubitemid 47343715)
7. Cortes, H. C., Muller, N., Boykin, D.W., Stephens, C. E. and Hemphill, A. (2011). In vitro effects of arylimidamides against Besnoitia besnoiti infection in Vero cells. Parasitology 138, 583-592.
8. Costa, J. M., Pautas, C., Ernault, P., Foulet, F., Cordonnier, C. and Bretagne, S. (2000). Real-time PCR for diagnosis and follow-up of Toxoplasma reactivation after allogeneic stem cell transplantation using fluorescence resonance energy transfer hybridization probes. Journal of Clinical Microbiology 38, 2929-2932. (Pubitemid 30640576)
9. Dabritz, H. A. and Conrad, P. A. (2010). Cats and Toxoplasma: implications for public health. Zoonoses and Public Health 57, 34-52
10. Dardé, M. L. (2008). Toxoplasma gondii, "new" genotypes and virulence. Parasite 15, 366-371.
11. Debache, K., Guinaud, C., Kropf, C., Boykin, D., Stephens, C. E. and Hemphill, A. (2011). Experimental treatment of Neospora caninuminfected mice with the arylimidamiDe DB750 and the thiazoliDe nitazoxanide. Experimental Parasitology 129, 95-100.
12. Dedicoat, M. and Livesley, N. (2006). Management of toxoplasmic encephalitis in HIV-infected adults (with an emphasis on resource-poor settings). Cochrane Database Systemic Reviews 19;3, CD005420.
13. Dubey, J. P. (2009). History of the discovery of the life cycle of Toxoplasma gondii. International Journal for Parasitology 39, 877-882.
14. Dubey, J. P., Schares, G. and Ortega-Mora, L. M. (2007). Epidemiology and control of neosporosis and Neospora caninum. Clinical Microbiology Reviews 20, 323-367. (Pubitemid 46709307)
15. Feldman, D. M., Timms, D. and Borgida, D. F. (2010). Toxoplasmosis, parvovirus, and cytomegalovirus in pregnancy. Clinical Laboratory Medicine 30, 709-720.
16. Hemphill, A. (1996). Subcellular localization and functional characterization of Nc-p43, a major Neospora caninum tachyzoite surface protein. Infection and Immunity 64, 4279-4287. (Pubitemid 26318154)
17. Hemphill, A., Gottstein, B. and Kaufmann, H. (1996). Adhesion and invasion of bovine endothelial cells by Neospora caninum. Parasitology 112, 183-197. (Pubitemid 26069945)
18. Hemphill, A., Vonlaufen, N., Naguleswaran, A., Keller, N., Riesen, M., Guetg, N., Srinivasan, S. and Alaeddine, F. (2004). Tissue culture and explant approaches to studying and visualizing Neospora caninum and its interactions with the host cell. Microscopy and Microanalysis 10, 602-620. (Pubitemid 39404023)
19. Hemphill, A., Vonlaufen, N. and Naguleswaran, A. (2006). Cellular and immunological basis of the host-parasite relationship during infection with Neospora caninum. Parasitology 133, 261-278. (Pubitemid 44214941)
20. Henriquez, F. L., Woods, S., Cong, H., McLeod, R. and Roberts, C.W. (2010). Immunogenetics of Toxoplasma gondii informs vaccine design. Trends in Parasitology 26, 550-555.
21. Laliberté, J. and Carruthers, V. B. (2008). Host cell manipulation by the human pathogen Toxoplasma gondii. Cellular and Molecular Life Science 65l, 1900-1915.
22. Lanteri, C. A., Stewart, M. L., Brock, J. M., Alibu, V. P., Meshnick, S. R., Tidwell, R. R. and Barrett, M. P. (2006). Roles for the Trypanosoma brucei P2 transporter in DB75 uptake and resistance. Molecular Pharmacology 70, 1585-1592.
23. Leepin, A., Studli, A., Brun, R., Stephens, C. E., Boykin, D.W. and Hemphill, A. (2008). Host cells participate in the in vitro effects of novel diamidine analogues against tachyzoites of the intracellular apicomplexan parasites Neospora caninum and Toxoplasma gondii. Antimicrobial Agents and Chemotherapy 52, 1999-2008. (Pubitemid 351758535)
24. Lindsay, D. S., Blagburn, B. L., Hall, J. E. and Tidwell, R. R. (1991). Activity of pentamidine and pentamidine analogs against Toxoplasma gondii in cell cultures. Antimicrobial Agents and Chemotherapy 35, 1914-1916.
25. Matovu, E., Stewart, M. L., Geiser, F., Brun, R., Maser, P., Wallace, L. J., Burchmore, R. J., Enyaru, J. C., Barrett, M. P., Kaminsky, R., Seebeck, T. and De Koning, H. P. (2003). Mechanisms of arsenical and diamidine uptake and resistance in Trypanosoma brucei. Eukaryotic Cell 2, 1003-1008. (Pubitemid 37298713)
26. McFadden, D. C., Seeber, F. and Boothroyd, J. C. (1997). Use of Toxoplasma gondii expressing beta-galactosidase for colorimetric assessment of drug activity in vitro. Antimicrobial Agents and Chemotherapy 41, 1849-1853. (Pubitemid 27383215)
27. Ming, X., Ju,W., Wu, H., Tidwell, R. R., Hall, J. E. and Thakker, D. R. (2009). Transport of dicationic drugs pentamidine and furamidine by human organic cationic transporters. Drug Metabolism and Disposition 37, 424-430.
28. Montoya, J. G. and Liesenfeld, O. (2004). Toxoplasmosis. Lancet. 363, 1965-1976. (Pubitemid 38759657)
29. Muller, J., Limban, C., Stadelmann, B., Missir, A. V., Chirita, I. C., Chifiriuc, M. C., Nitulescu, M. G. and Hemphill, A. (2009). Thioureides of 2-(phenoxymethyl)benzoic acid 4-R substituted: a novel class of anti-parasitic compounds. Parasitology International 58. 128-135.
30. Naguleswaran, A., Muller, N. and Hemphill, A. (2003). Neospora caninum and Toxoplasma gondii: a novel adhesion/invasion assay reveals distinct differences in tachyzoite-host cell interactions. Experimental Parasitology 104, 149-158. (Pubitemid 37211303)
31. Pereira-Chioccola, V. L., Vidal, J. E. and Su, C. (2009). Toxoplasma gondii infection and cerebral toxoplasmosis in HIV-infected patients. Future Microbiology 4, 1363-1379.
32. Ribera Pascuet, E., López Aldeguer, J., Pérez Elías, M. J. and Podzamczer Palter, D. (1998). Cerebral toxoplasmosis. Enfermeria. Infecciology. Microbiology Clinica 16 Suppl 1, 45-51. (Pubitemid 28530732)
33. Sauvage, V., Aubert, D., Escotte-Binet, S. and Villena, I. (2009). The role of ATP-binding cassette (ABC) proteins in protozoan parasites. Molecular and Biochemical Parasitology 167, 81-94.
34. Scheidegger, A., Vonlaufen, N., Naguleswaran, A., Gianinazzi, C., Muller, N., Leib, S. L. and Hemphill, A. (2005). Differential effects of interferon-gamma and tumor necrosis factor-alpha on Toxoplasma gondii proliferation in organotypic rat brain slice cultures. Journal of Parasitology 91, 307-315. (Pubitemid 40756267)
35. Silva, C. F., Batista, M. M., Mota, R. A., De Souza, E. M., Stephens, C. E., Som, P., Boykin, D.W. and Soeiro, M. N. (2007a). Activity of "reversed" diamidines against Trypanosoma cruzi "in vitro". Biochemical Pharmacology 15, 1939-1946. (Pubitemid 46677912)
36. Silva, C. F., Meuser, M. B., De Souza, E. M., Meirelles, M. N., Stephens, C. E., Som, P., Boykin, D.W. and Soeiro, M. N. (2007b). Cellular effects of reversed amidines on Trypanosoma cruzi. Antimicrobial Agents and Chemotherapy 51, 3803-3809. (Pubitemid 350057774)
37. Soeiro, M. N., De Souza, E. M., Stephens, C. E. and Boykin, D.W. (2005). Aromatic diamidines as antiparasitic agents. Expert Opinion in Investigational Drugs 14, 957-972. (Pubitemid 41131649)
38. Stephens, C. E., Brun, R., Salem, M. N., Werbovetz, K. A., Tanious, F., Wilson, W. D. and Boykin, D.W. (2003). The activity of diguanidino and 'reversed' diamidino 2,5-diarylfurans versus Trypanosoma cruzi and Leishmania donoVani. Bioorganic Medicinal Chemistry Letters 16, 2065-2069. (Pubitemid 36638411)
39. Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217-1258.
40. Wang, M. Z., Zhu, X., Srivastava, A., Liu, Q., Sweat, J. M., Pandharkar, T., Stephens, C. E., Riccio, E., Parman, T., Munde, M., Mandal, S., Madhubala, R., Tidwell, R. R., Wilson, W. D., Boykin, D.W., Hall, J. E., Kyle, D. E. and Werbovetz, K. A. (2010). Novel arylimidamides for treatment of visceral leishmaniasis. Antimicrobial Agents and Chemotherapy 54, 2507-2516.
41. Werbovetz, K. (2006). Diamidines as antitrypanosomal, antileishmanial and antimalarial agents. Current Opinion in Investigational Drugs 6, 147-157. (Pubitemid 43230911)
42. Wilson, W. D., Tanious, F. A., Mathis, A., Tevis, D., Hall, J. E. and Boykin, D.W. (2008). Antiparasitic compounds that target DNA. Biochimie 90, 999-1014.
43. Witola, W. H., Inoue, N., Ohashi, K. and Onuma, M. (2004). RNAinterference silencing of the adenosine transporter-1 gene in Trypanosoma eVansi confers resistance to diminazene aceturate. Experimental Parasitology 107, 47-57. (Pubitemid 38781071)