A Proposed Target Product Profile and Developmental Cascade for New Cryptosporidiosis Treatments

PLoS Neglected Tropical Diseases

Volumn 9, Issue 10, 2015, Pages 1-10

  Huston, Christopher D ^a   Spangenberg, Thomas ^b,d   Burrows, Jeremy ^b   Willis, Paul ^b   Wells, Timothy N C ^b   van Voorhis, Wesley ^b,c  

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

^b Medicines for Malaria Venture ^*  (Switzerland)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d MERCK SERONO S A   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

NITAZOXANIDE;

ARTICLE; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM HOMINIS; CRYPTOSPORIDIUM PARVUM; DIARRHEA; DRUG COST; DRUG EFFICACY; DRUG RESPONSE; DRUG SAFETY; DRUG SCREENING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALNUTRITION; NONHUMAN;

EID: 84946073631     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003987     Document Type: Article

References (54)

1. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, et al. 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. 2013 382: 209–222. doi: 10.1016/S0140-6736(13)60844-2 23680352
2. Malebranche R, Arnoux E, Guerin JM, Pierre GD, Laroche AC, et al. Acquired immunodeficiency syndrome with severe gastrointestinal manifestations in Haiti. Lancet. 1983 2: 873–878. 6137696
3. Navin TR, Weber R, Vugia DJ, Rimland D, Roberts JM, et al. Declining CD4+ T-lymphocyte counts are associated with increased risk of enteric parasitosis and chronic diarrhea: results of a 3-year longitudinal study. J Acquir Immune Defic Syndr Hum Retrovirol. 1999 20: 154–159. 10048902
4. Mac Kenzie WR, Hoxie NJ, Proctor ME, Gradus MS, Blair KA, et al. A Massive Outbreak in Milwaukee of Cryptosporidium Infection Transmitted through the Public Water Supply. N Engl J Med. 1994 331: 161–167. 7818640
5. Shirley DA, Moonah SN, Kotloff KL, Burden of disease from cryptosporidiosis. Curr Opin Infect Dis. 2012 25: 555–563. doi: 10.1097/QCO.0b013e328357e569 22907279
6. Macfarlane DE, Horner-Bryce J, Cryptosporidiosis in well-nourished and malnourished children. Acta Paediatr Scand. 1987 76: 474–477. 3604664
7. Newman RD, Zu SX, Wuhib T, Lima AA, Guerrant RL, et al. Household epidemiology of Cryptosporidium parvum infection in an urban community in northeast Brazil. Ann Intern Med. 1994 120: 500–505. 8311373
8. Guerrant DI, Moore SR, Lima AA, Patrick PD, Schorling JB, et al. 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. 1999 61: 707–713. 10586898
9. Newman RD, Sears CL, Moore SR, Nataro JP, Wuhib T, et al. Longitudinal study of Cryptosporidium infection in children in northeastern Brazil. J Infect Dis. 1999 180: 167–175. 10353875
10. Dillingham RA, Lima AA, Guerrant RL, Cryptosporidiosis: epidemiology and impact. Microbes Infect. 2002 4: 1059–1066. 12191656
11. Bushen OY, Kohli A, Pinkerton RC, Dupnik K, Newman RD, et al. Heavy cryptosporidial infections in children in northeast Brazil: comparison of Cryptosporidium hominis and Cryptosporidium parvum. Trans R Soc Trop Med Hyg. 2007 101: 378–384. 16934303
12. Abdel-Messih IA, Wierzba TF, Abu-Elyazeed R, Ibrahim AF, Ahmed SF, et al. Diarrhea associated with Cryptosporidium parvum among young children of the Nile River Delta in Egypt. J Trop Pediatr. 2005 51: 154–159. 15831665
13. Cama VA, Bern C, Roberts J, Cabrera L, Sterling CR, et al. Cryptosporidium species and subtypes and clinical manifestations in children, Peru. Emerg Infect Dis. 2008 14: 1567–1574. doi: 10.3201/eid1410.071273 18826821
14. Chintu C, Luo C, Baboo S, Khumalo-Ngwenya B, Mathewson J, et al. Intestinal parasites in HIV-seropositive Zambian children with diarrhoea. J Trop Pediatr. 1995 41: 149–152. 7636933
15. Mondal D, Haque R, Sack RB, Kirkpatrick BD, Petri WA, Jr.Attribution of malnutrition to cause-specific diarrheal illness: evidence from a prospective study of preschool children in Mirpur, Dhaka, Bangladesh. Am J Trop Med Hyg. 2009 80: 824–826. 19407131
16. Mor SM, Tzipori S, Cryptosporidiosis in Children in Sub-Saharan Africa: A Lingering Challenge. Clin Infect Dis. 2008 47: 915–921. doi: 10.1086/591539 18715159
17. Moyo SJ, Gro N, Matee MI, Kitundu J, Myrmel H, et al. Age specific aetiological agents of diarrhoea in hospitalized children aged less than five years in Dar es Salaam, Tanzania. BMC Pediatr. 2011 11: 19. doi: 10.1186/1471-2431-11-19 21345186
18. Tumwine JK, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, et al. Cryptosporidiosis and microsporidiosis in ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am J Trop Med Hyg. 2005 73: 921–925. 16282304
19. Zu SX, Li JF, Barrett LJ, Fayer R, Shu SY, et al. Seroepidemiologic study of Cryptosporidium infection in children from rural communities of Anhui, China and Fortaleza, Brazil. Am J Trop Med Hyg. 1994 51: 1–10. 8059906
20. Amadi B, Mwiya M, Musuku J, Watuka A, Sianongo S, et al. Effect of nitazoxanide on morbidity and mortality in Zambian children with cryptosporidiosis: a randomised controlled trial. Lancet. 2002 360: 1375–1380. 12423984
21. Rossignol JF, Hidalgo H, Feregrino M, Higuera F, Gomez WH, et al. A double-'blind' placebo-controlled study of nitazoxanide in the treatment of cryptosporidial diarrhoea in AIDS patients in Mexico. Trans R Soc Trop Med Hyg. 1998 92: 663–666. 10326116
22. Amadi B, Mwiya M, Sianongo S, Payne L, Watuka A, et al. High dose prolonged treatment with nitazoxanide is not effective for cryptosporidiosis in HIV positive Zambian children: a randomised controlled trial. BMC Infect Dis. 2009 9: 195. doi: 10.1186/1471-2334-9-195 19954529
23. Murphy RC, Ojo KK, Larson ET, Castellanos-Gonzalez A, Perera BG, et al. Discovery of Potent and Selective Inhibitors of Calcium-Dependent Protein Kinase 1 (CDPK1) from C. parvum and T. gondii. ACS Med Chem Lett. 2010 1: 331–335. 21116453
24. Zhang Z, Ojo KK, Johnson SM, Larson ET, He P, et al. Benzoylbenzimidazole-based selective inhibitors targeting Cryptosporidium parvum and Toxoplasma gondii calcium-dependent protein kinase-1. Bioorg Med Chem Lett. 2012 22: 5264–5267. doi: 10.1016/j.bmcl.2012.06.050 22795629
25. Castellanos-Gonzalez A, White AC, Jr.Ojo KK, Vidadala RS, Zhang Z, et al. A novel calcium-dependent protein kinase inhibitor as a lead compound for treating cryptosporidiosis. J Infect Dis. 2013 208: 1342–1348. doi: 10.1093/infdis/jit327 23878324
26. Fritzler JM, Zhu G, Novel anti-Cryptosporidium activity of known drugs identified by high-throughput screening against parasite fatty acyl-CoA binding protein (ACBP). J Antimicrob Chemother. 2012 67: 609–617. doi: 10.1093/jac/dkr516 22167242
27. Guo F, Zhang H, Fritzler JM, Rider SD, Jr.Xiang L, et al. Amelioration of Cryptosporidium parvum infection in vitro and in vivo by targeting parasite fatty acyl-coenzyme A synthetases. J Infect Dis. 2014 209: 1279–1287. doi: 10.1093/infdis/jit645 24273180
28. Ndao M, Nath-Chowdhury M, Sajid M, Marcus V, Mashiyama ST, et al. A cysteine protease inhibitor rescues mice from a lethal Cryptosporidium parvum infection. Antimicrob Agents Chemother. 2013 57: 6063–6073. doi: 10.1128/AAC.00734-13 24060869
29. Umejiego NN, Gollapalli D, Sharling L, Volftsun A, Lu J, et al. Targeting a prokaryotic protein in a eukaryotic pathogen: identification of lead compounds against cryptosporidiosis. Chem Biol. 2008 15: 70–77. doi: 10.1016/j.chembiol.2007.12.010 18215774
30. Kirubakaran S, Gorla SK, Sharling L, Zhang M, Liu X, et al. Structure-activity relationship study of selective benzimidazole-based inhibitors of Cryptosporidium parvum IMPDH. Bioorg Med Chem Lett. 2012 22: 1985–1988. doi: 10.1016/j.bmcl.2012.01.029 22310229
31. Gorla SK, Kavitha M, Zhang M, Chin JE, Liu X, et al. Optimization of benzoxazole-based inhibitors of Cryptosporidium parvum inosine 5'-monophosphate dehydrogenase. J Med Chem. 2013 56: 4028–4043. doi: 10.1021/jm400241j 23668331
32. Maurya SK, Gollapalli DR, Kirubakaran S, Zhang M, Johnson CR, et al. Triazole inhibitors of Cryptosporidium parvum inosine 5'-monophosphate dehydrogenase. J Med Chem. 2009 52: 4623–4630. doi: 10.1021/jm900410u 19624136
33. Gorla SK, McNair NN, Yang G, Gao S, Hu M, et al. Validation of IMP dehydrogenase inhibitors in a mouse model of cryptosporidiosis. Antimicrob Agents Chemother. 2014 58: 1603–1614. doi: 10.1128/AAC.02075-13 24366728
34. Bessoff K, Sateriale A, Lee KK, Huston CD, Drug repurposing screen reveals FDA-approved inhibitors of human HMG-CoA reductase and isoprenoid synthesis that block Cryptosporidium parvum growth. Antimicrob Agents Chemother. 2013 57: 1804–1814. doi: 10.1128/AAC.02460-12 23380723
35. Bessoff K, Spangenberg T, Foderaro JE, Jumani RS, Ward GE, et al. Identification of Cryptosporidium parvum active chemical series by repurposing the open access malaria box. Antimicrob Agents Chemother. 2014 58: 2731–2739. doi: 10.1128/AAC.02641-13 24566188
36. Checkley W, White AC, Jr.Jaganath D, Arrowood MJ, Chalmers RM, et al. A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for cryptosporidium. Lancet Infect Dis. 2015 15: 85–94. doi: 10.1016/S1473-3099(14)70772-8 25278220
37. Rossignol JF, Kabil SM, el-Gohary Y, Younis AM, Effect of nitazoxanide in diarrhea and enteritis caused by Cryptosporidium species. Clin Gastroenterol Hepatol. 2006 4: 320–324. 16527695
38. Hussien SM, Abdella OH, Abu-Hashim AH, Aboshiesha GA, Taha MA, et al. Comparative study between the effect of nitazoxanide and paromomycin in treatment of cryptosporidiosis in hospitalized children. J Egypt Soc Parasitol. 2013 43: 463–470. 24260825
39. DuPont HL, Chappell CL, Sterling CR, Okhuysen PC, Rose JB, et al. The infectivity of Cryptosporidium parvum in healthy volunteers. N Engl J Med. 1995 332: 855–859. 7870140
40. Parr JB, Sevilleja JE, Samie A, Alcantara C, Stroup SE, et al. Detection and quantification of Cryptosporidium in HCT-8 cells and human fecal specimens using real-time polymerase chain reaction. Am J Trop Med Hyg. 2007 76: 938–942. 17488919
41. Stroup SE, Roy S, McHele J, Maro V, Ntabaguzi S, et al. Real-time PCR detection and speciation of Cryptosporidium infection using Scorpion probes. J Med Microbiol. 2006 55: 1217–1222. 16914651
42. Stroup S, Tongjai S, Swai N, Maro A, Kibiki G, et al. Dual probe DNA capture for sensitive real-time PCR detection of Cryptosporidium and Giardia. Mol Cell Probes. 2012 26: 104–106. doi: 10.1016/j.mcp.2011.12.003 22227113
43. Haque R, Roy S, Siddique A, Mondal U, Rahman SM, et al. Multiplex real-time PCR assay for detection of Entamoeba histolytica, Giardia intestinalis, and Cryptosporidium spp. Am J Trop Med Hyg. 2007 76: 713–717. 17426176
44. Van den Bossche D, Cnops L, Verschueren J, Van Esbroeck M, Comparison of four rapid diagnostic tests, ELISA, microscopy and PCR for the detection of Giardia lamblia, Cryptosporidium spp. and Entamoeba histolytica in feces. J Microbiol Methods. 2015 110: 78–84. doi: 10.1016/j.mimet.2015.01.016 25615719
45. Mary C, Chapey E, Dutoit E, Guyot K, Hasseine L, et al. Multicentric evaluation of a new real-time PCR assay for quantification of Cryptosporidium spp. and identification of Cryptosporidium parvum and Cryptosporidium hominis. J Clin Microbiol. 2013 51: 2556–2563. doi: 10.1128/JCM.03458-12 23720792
46. Ward LA, Wang Y, Rapid methods to isolate Cryptosporidium DNA from frozen feces for PCR. Diagn Microbiol Infect Dis. 2001 41: 37–42. 11687312
47. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science. 2004 304: 441–445. 15044751
48. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, et al. The genome of Cryptosporidium hominis. Nature. 2004 431: 1107–1112. 15510150
49. Clavel A, Arnal AC, Sanchez EC, Cuesta J, Letona S, et al. Respiratory cryptosporidiosis: case series and review of the literature. Infection. 1996 24: 341–346. 8923043
50. Burrows JN, Burlot E, Campo B, Cherbuin S, Jeanneret S, et al. Antimalarial drug discovery—the path towards eradication. Parasitology. 2014 141: 128–139. doi: 10.1017/S0031182013000826 23863111
51. Costa LB, JohnBull EA, Reeves JT, Sevilleja JE, Freire RS, et al. Cryptosporidium-Malnutrition Interactions: Mucosal Disruption, Cytokines, and TLR Signaling In A Weaned Murine Model. JParasitol. 2011 97: 1113–1120.
52. Costa LB, Noronha FJ, Roche JK, Sevilleja JE, Warren CA, et al. Novel in vitro and in vivo models and potential new therapeutics to break the vicious cycle of Cryptosporidium infection and malnutrition. J Infect Dis. 2012 205: 1464–1471. doi: 10.1093/infdis/jis216 22454464
53. Theodos CM, Griffiths JK, D'Onfro J, Fairfield A, Tzipori S, Efficacy of nitazoxanide against Cryptosporidium parvum in cell culture and in animal models. Antimicrob Agents Chemother. 1998 42: 1959–1965. 9687390
54. Ollivett TL, Nydam DV, Bowman DD, Zambriski JA, Bellosa ML, et al. Effect of nitazoxanide on cryptosporidiosis in experimentally infected neonatal dairy calves. J Dairy Sci. 2009 92: 1643–1648. doi: 10.3168/jds.2008-1474 19307646