Identification of cryptosporidium parvum active chemical series by repurposing the open access malaria box

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 5, 2014, Pages 2731-2739

  Bessoff, Kovi ^a   Spangenberg, Thomas ^b   Foderaro, Jenna E ^a   Jumani, Rajiv S ^c   Ward, Gary E ^a,c   Hustona, Christopher D ^a,c  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b Medicines for Malaria Venture   (Switzerland)

^c UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DIAMINOQUINAZOLINE DERIVATIVE; 8 QUINOLINOL DERIVATIVE; ALLOPURINOL; ANTISPOROZOAL AGENT; DIMETHYL SULFOXIDE; NITAZOXANIDE; ANTIPROTOZOAL AGENT; QUINAZOLINE DERIVATIVE; QUINOLINOL DERIVATIVE; THIAZOLE DERIVATIVE;

ADENOCARCINOMA; ARTICLE; BIOLOGICAL ACTIVITY; CARCINOMA CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYPTOSPORIDIUM PARVUM; DRUG CYTOTOXICITY; DRUG DATABASE; DRUG IDENTIFICATION; DRUG POTENCY; DRUG REPOSITIONING; DRUG SCREENING; GROWTH INHIBITION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; MICROBIAL GROWTH; NONHUMAN; OPEN ACCESS MALARIA BOX; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PUBLIC-PRIVATE PARTNERSHIP; TOXOPLASMA GONDII; CHEMISTRY; DRUG EFFECTS; PROCEDURES; TOXOPLASMA;

ANTIPROTOZOAL AGENTS; CRYPTOSPORIDIUM PARVUM; DRUG REPOSITIONING; HUMANS; HYDROXYQUINOLINES; QUINAZOLINES; THIAZOLES; TOXOPLASMA;

EID: 84898650563     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02641-13     Document Type: Article

References (42)

1. Xiao L, Fayer R, Ryan U, Upton SJ. 2004. Cryptosporidium taxonomy: recent advances and implications for public health. Clin. Microbiol. Rev. 17:72-97. http://dx.doi.org/10.1128/CMR.17.1.72-97.2004.
2. Chen XM, Keithly JS, Paya CV, LaRusso NF. 2002. Cryptosporidiosis. N. Engl. J. Med. 346:1723-1731. http://dx.doi.org/10.1056/NEJMra013170.
3. Yoder JS, Wallace RM, Collier SA, Beach MJ, Hlavsa MC. 2012. Cryptosporidiosis surveillance-United States, 2009-2010. MMWR Morb. Mortal. Wkly. Rep. 61:1-12.
4. Mac Kenzie WR, Hoxie NJ, Proctor ME, Gradus MS, Blair KA, Peterson DE, Kazmierczak JJ, Addiss DG, Fox KR, Rose JB, Davis JP. 1994. A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. N. Engl. J. Med. 331:161-167. http://dx.doi.org/10.1056/ NEJM199407213310304.
5. Hlavsa MC, Roberts VA, Anderson AR, Hill VR, Kahler AM, Orr M, Garrison LE, Hicks LA, Newton A, Hilborn ED, Wade TJ, Beach MJ, Yoder JS. 2011. Surveillance for waterborne disease outbreaks and other health events associated with recreational water-United States, 2007-2008. MMWR Morb. Mortal. Wkly. Rep. 60:1-32.
6. Centers for Disease Control and Prevention. 2012. Outbreak of cryptosporidiosis associated with a firefighting response-Indiana and Michigan, June 2011. MMWR Morb. Mortal. Wkly. Rep. 61:153-156.
7. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani DG, Jha P, Campbell H, Walker CF, Cibulskis R, Eisele T, Liu L, Mathers C, Child Health Epidemiology Reference Group of WHO and UNICEF. 2010. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 375:1969-1987. http://dx.doi.org/10.1016/S0140-6736(10)60549-1.
8. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382:209-222. http://dx.doi.org/10.1016/S0140-6736(13)60844-2.
9. Guerrant DI, Moore SR, Lima AA, Patrick PD, Schorling JB, Guerrant RL. 1999. Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am. J. Trop. Med. Hyg. 61:707-713.
10. Macfarlane DE, Horner-Bryce J. 1987. Cryptosporidiosis in wellnourished and malnourished children. Acta Paediatr. Scand. 76:474-477. http://dx.doi.org/10.1111/j.1651-2227.1987.tb10502.x.
11. O'Connor RM, Shaffie R, Kang G, Ward HD. 2011. Cryptosporidiosis in patients with HIV/AIDS. AIDS 25:549-560. http://dx.doi.org/10.1097/QAD. 0b013e3283437e88.
12. Shirley DA, Moonah SN, Kotloff KL. 2012. Burden of disease from cryptosporidiosis. Curr. Opin. Infect. Dis. 25:555-563. http://dx.doi.org/10. 1097/QCO.0b013e328357e569.
13. Abubakar I, Aliyu SH, Arumugam C, Hunter PR, Usman NK. 2007. Prevention and treatment of cryptosporidiosis in immunocompromised patients. Cochrane Database Syst. Rev. (1):CD004932. http://dx.doi.org/10.1002/14651858.CD004932. pub2.
14. Adams CP, Brantner VV. 2006. Estimating the cost of new drug development: is it really $802 million? Health Aff. (Millwood) 25:420-428. http://dx.doi.org/10.1377/hlthaff.25.2.420.
15. Reich MR. 2000. The global drug gap. Science 287:1979-1981. http://dx.doi.org/10.1126/science.287.5460.1979.
16. Abdulla S, Sagara I, Borrmann S, D'Alessandro U, González R, Hamel M, Ogutu B, Mårtensson A, Lyimo J, Maiga H, Sasi P, Nahum A, Bassat Q, Juma E, Otieno L, Björkman A, Beck HP, Andriano K, Cousin M, Lefèvre G, Ubben D, Premji Z. 2008. Efficacy and safety of artemetherlumefantrine dispersible tablets compared with crushed commercial tablets in African infants and children with uncomplicated malaria: a randomised, single-blind, multicentre trial. Lancet 372:1819-1827. http://dx.doi.org/10.1016/S0140-6736(08)61492-0.
17. Gamo FJ, Sanz LM, Vidal J, de Cozar C, Alvarez E, Lavandera JL, Vanderwall DE, Green DV, Kumar V, Hasan S, Brown JR, Peishoff CE, Cardon LR, Garcia-Bustos JF. 2010. Thousands of chemical starting points for antimalarial lead identification. Nature 465:305-310. http://dx.doi.org/10.1038/nature09107.
18. Meister S, Plouffe DM, Kuhen KL, Bonamy GM, Wu T, Barnes SW, Bopp SE, Borboa R, Bright AT, Che J, Cohen S, Dharia NV, Gagaring K, Gettayacamin M, Gordon P, Groessl T, Kato N, Lee MC, McNamara CW, Fidock DA, Nagle A, Nam TG, Richmond W, Roland J, Rottmann M, Zhou B, Froissard P, Glynne RJ, Mazier D, Sattabongkot J, Schultz PG, Tuntland T, Walker JR, Zhou Y, Chatterjee A, Diagana TT, Winzeler EA. 2011. Imaging of Plasmodium liver stages to drive nextgeneration antimalarial drug discovery. Science 334:1372-1377. http://dx.doi.org/10.1126/science.1211936.
19. Guiguemde WA, Shelat AA, Bouck D, Duffy S, Crowther GJ, Davis PH, Smithson DC, Connelly M, Clark J, Zhu F, Jiménez-Díaz MB, Martinez MS, Wilson EB, Tripathi AK, Gut J, Sharlow ER, Bathurst I, El Mazouni F, Fowble JW, Forquer I, McGinley PL, Castro S, Angulo-Barturen I, Ferrer S, Rosenthal PJ, DeRisi JL, Sullivan DJ, Lazo JS, Roos DS, Riscoe MK, Phillips MA, Rathod PK, Van Voorhis WC, Avery VM, Guy RK. Chemical genetics of Plasmodium falciparum. Nature 465:311-315. http://dx.doi.org/10.1038/nature09099.
20. Spangenberg T, Burrows JN, Kowalczyk P, McDonald S, Wells TN, Willis P. 2013. The open access Malaria Box: a drug discovery catalyst for neglected diseases. PLoS One 8:e62906. http://dx.doi.org/10.1371/journal.pone.0062906.
21. Bessoff K, Sateriale A, Lee KK, Huston CD. 2013. Drug repurposing screen reveals FDA-Approved inhibitors of human HMG-CoA reductase and isoprenoid synthesis that block Cryptosporidium parvum growth. Antimicrob. Agents Chemother. 57:1804-1814. http://dx.doi.org/10.1128/AAC.02460-12.
22. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng M, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V. 2004. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304:441-445. http://dx.doi.org/10.1126/science.1094786.
23. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, Serrano MG, Puiu D, Manque P, Akiyoshi D, Mackey AJ, Pearson WR, Dear PH, Bankier AT, Peterson DL, Abrahamsen MS, Kapur V, Tzipori S, Buck GA. 2004. The genome of Cryptosporidium hominis. Nature 431:1107-1112. http://dx.doi.org/10.1038/nature02977.
24. Wernimont AK, Artz JD, Finerty P, Jr, Lin YH, Amani M, Allali-Hassani A, Senisterra G, Vedadi M, Tempel W, Mackenzie F, Chau I, Lourido S, Sibley LD, Hui R. 2010. Structures of apicomplexan calcium-dependent protein kinases reveal mechanism of activation by calcium. Nat. Struct. Mol. Biol. 17:596-601. http://dx.doi.org/10.1038/nsmb.1795.
25. Murphy RC, Ojo KK, Larson ET, Castellanos-Gonzalez A, Perera BG, Keyloun KR, Kim JE, Bhandari JG, Muller NR, Verlinde CL, White AC, Jr, Merritt EA, Van Voorhis WC, Maly DJ. 2010. Discovery of potent and selective inhibitors of calcium-dependent protein kinase 1 (CDPK1) from C. parvum and T. gondii. ACS Med. Chem. Lett. 1:331-335. http://dx.doi.org/10.1021/ml100096t.
26. Gut J, Nelson RG. 1999. Cryptosporidium parvum: synchronized excystation in vitro and evaluation of sporozoite infectivity with a new lectinbased assay. J. Eukaryot. Microbiol. 46:56S-57S.
27. Gubbels MJ, Li C, Striepen B. 2003. High-throughput growth assay for Toxoplasma gondii using yellow fluorescent protein. Antimicrob. Agents Chemother. 47:309-316. http://dx.doi.org/10.1128/AAC.47.1.309-316.2003.
28. Striepen B, Kissinger JC. 2004. Genomics meets transgenics in search of the elusive Cryptosporidium drug target. Trends Parasitol. 20:355-358. http://dx.doi.org/10.1016/j.pt.2004.06.003.
29. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. 2001. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 46:3-26. http://dx.doi.org/10.1016/S0169-409X(00)00129-0.
30. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL. 2007. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat. Rev. Drug Discov. 6:29-40. http://dx.doi.org/10.1038/nrd2201.
31. Bauer RA, Wurst JM, Tan DS. 2010. Expanding the range of 'druggable' targets with natural product-based libraries: an academic perspective. Curr. Opin. Chem. Biol. 14:308-314. http://dx.doi.org/10.1016/j.cbpa.2010.02.001.
32. Keller TH, Shi PY, Wang QY. 2011. Anti-infectives: can cellular screening deliver? Curr. Opin. Chem. Biol. 15:529-533. http://dx.doi.org/10.1016/j.cbpa. 2011.06.007.
33. Huang BQ, Chen XM, LaRusso NF. 2004. Cryptosporidium parvum attachment to and internalization by human biliary epithelia in vitro: a morphologic study. J. Parasitol. 90:212-221. http://dx.doi.org/10.1645/GE-3204.
34. Lumb R, Smith K, O'Donoghue PJ, Lanser JA. 1988. Ultrastructure of the attachment of Cryptosporidium sporozoites to tissue culture cells. Parasitol. Res. 74:531-536. http://dx.doi.org/10.1007/BF00531630.
35. Striepen B, White MW, Li C, Guerini MN, Malik SB, Logsdon JM, Jr, Liu C, Abrahamsen MS. 2002. Genetic complementation in apicomplexan parasites. Proc. Natl. Acad. Sci. U. S. A. 99:6304-6309. http://dx.doi.org/10.1073/pnas. 092525699.
36. Baum EZ, Crespo-Carbone SM, Klinger A, Foleno BD, Turchi I, Macielag M, Bush K. 2007. A MurF inhibitor that disrupts cell wall biosynthesis in Escherichia coli. Antimicrob. Agents Chemother. 51:4420-4426. http://dx.doi.org/10.1128/AAC.00845-07.
37. Coombs GS, Schmitt AA, Canning CA, Alok A, Low IC, Banerjee N, Kaur S, Utomo V, Jones CM, Pervaiz S, Toone EJ, Virshup DM. 2012. Modulation of Wnt/H-catenin signaling and proliferation by a ferrous iron chelator with therapeutic efficacy in genetically engineered mouse models of cancer. Oncogene 31:213-225. http://dx.doi.org/10.1038/onc.2011.228.
38. Fraser RS, Creanor J. 1975. The mechanism of inhibition of ribonucleic acid synthesis by 8-hydroxyquinoline and the antibiotic lomofungin. Biochem. J. 147:401-410.
39. Phillips JP. 1956. The reactions of 8-quinolinol. Chem. Rev. 56:271-297. http://dx.doi.org/10.1021/cr50008a003.
40. Chou TF, Brown SJ, Minond D, Nordin BE, Li K, Jones AC, Chase P, Porubsky PR, Stoltz BM, Schoenen FJ, Patricelli MP, Hodder P, Rosen H, Deshaies RJ. 2011. Reversible inhibitor of p97, DBeQ, impairs both ubiquitin-dependent and autophagic protein clearance pathways. Proc. Natl. Acad. Sci. U. S. A. 108:4834-4839. http://dx.doi.org/10.1073/pnas.1015312108.
41. Harbut MB, Patel BA, Yeung BK, McNamara CW, Bright AT, Ballard J, Supek F, Golde TE, Winzeler EA, Diagana TT, Greenbaum DC. 2012. Targeting the ERAD pathway via inhibition of signal peptide peptidase for antiparasitic therapeutic design. Proc. Natl. Acad. Sci. U. S. A. 109:21486-21491. http://dx.doi.org/10. 1073/pnas.1216016110.
42. Terkeltaub R, Bushinsky DA, Becker MA. 2006. Recent developments in our understanding of the renal basis of hyperuricemia and the development of novel antihyperuricemic therapeutics. Arthritis Res. Ther. 8:S4. http://dx.doi.org/10. 1186/ar1909.