Prospects for immunotherapy and vaccines against Cryptosporidium

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 6, 2014, Pages 1505-1513

  Mead, Jan R ^a,b  

^a ATLANTA VA MEDICAL CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cryptosporidium; Immunotherapy; Vaccine

Indexed keywords

BIOLOGICAL PRODUCT; PROTOZOAL VACCINE;

CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; HEALTH; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; ISOLATION AND PURIFICATION; PROCEDURES; TRENDS;

BIOLOGICAL PRODUCTS; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; GLOBAL HEALTH; HUMANS; IMMUNOTHERAPY; PROTOZOAN VACCINES;

EID: 84905865992     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.28485     Document Type: Review

References (116)

1. Huston CD, Petri WA Jr. Emerging and reemerging intestinal protozoa. Curr Opin Gastroenterol 2001; 17:17-23; PMID:17031144; http://dx.doi.org/10.1097/ 00001574-200101000-00004
2. Chalmers RM. Waterborne outbreaks of cryptosporidiosis. Ann Ist Super Sanita 2012; 48:429-46; PMID:23247139; http://dx.doi.org/10.4415/ANN-12-04-10
3. Priest JW, Li A, Khan M, Arrowood MJ, Lammie PJ, Ong CS, Roberts JM, Isaac-Renton J. Enzyme immunoassay detection of antigen-specific immunoglobulin g antibodies in longitudinal serum samples from patients with cryptosporidiosis. Clin Diagn Lab Immunol 2001; 8:415-23; PMID:11238231
4. Frost FJ, Muller TB, Calderon RL, Craun GF. Analysis of serological responses to Cryptosporidium antigen among NHANES III participants. Ann Epidemiol 2004; 14:473-8; PMID:15310525; http://dx.doi.org/10.1016/j.annepidem. 2003.06.002
5. López-Vélez R, Tarazona R, Garcia Camacho A, Gomez-Mampaso E, Guerrero A, Moreira V, Villanueva R. Intestinal and extraintestinal cryptosporidiosis in AIDS patients. Eur J Clin Microbiol Infect Dis 1995; 14:677-81; PMID:8565984; http://dx.doi.org/10.1007/BF01690873
6. Mor SM, Tzipori S. Cryptosporidiosis in children in Sub-Saharan Africa: a lingering challenge. Clin Infect Dis 2008; 47:915-21; PMID:18715159; http://dx.doi.org/10.1086/591539
7. Ives NJ, Gazzard BG, Easterbrook PJ. The changing pattern of AIDS-defining illnesses with the introduction of highly active antiretroviral therapy (HAART)in a London clinic. J Infect 2001; 42:134-9; PMID:11531320; http://dx.doi.org/10.1053/jinf.2001.0810
8. Amadi B, Kelly P, Mwiya M, Mulwazi E, Sianongo S, Changwe F, Thomson M, Hachungula J, Watuka A, Walker-Smith J, et al. Intestinal and systemic infection, HIV, and mortality in Zambian children with persistent diarrhea and malnutrition. J Pediatr Gastroenterol Nutr 2001; 32:550-4; PMID:11429515; http://dx.doi.org/10.1097/00005176-200105000-00011
9. Haque A, Saleem AF. On admission hypomagnesemia in critically ill children: Risk factors and outcome. Indian J Pediatr 2009; 76:1227-30; PMID:19936657; http://dx.doi.org/10.1007/s12098-009-0258-z
10. Checkley W, Epstein LD, Gilman RH, Black RE, Cabrera L, Sterling CR. Effects of Cryptosporidium parvum infection in Peruvian children: growth faltering and subsequent catch-up growth. Am J Epidemiol 1998; 148:497-506; PMID:9737562; http://dx.doi.org/10.1093/oxfordjournals.aje.a009675
11. Mølbak K, Andersen M, Aaby P, Højlyng N, Jakobsen M, Sodemann M, da Silva AP. Cryptosporidium infection in infancy as a cause of malnutrition: a community study from Guinea-Bissau, west Africa. Am J Clin Nutr 1997; 65:149-52; PMID:8988927
12. Guerrant DI, Moore SR, Lima AA, Patrick PD, Schorling JB, Guerrant RL. 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; 61:707-13; PMID:10586898
13. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, 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; 382:209-22; PMID:23680352; http://dx.doi.org/10.1016/S0140-6736(13)60844-2
14. Griffiths JK, Moore R, Dooley S, Keusch GT, Tzipori S. Cryptosporidium parvum infection of Caco-2 cell monolayers induces an apical monolayer defect, selectively increases transmonolayer permeability, and causes epithelial cell death. Infect Immun 1994; 62:4506-14; PMID:7927716
15. Chen XM, Levine SA, Splinter PL, Tietz PS, Ganong AL, Jobin C, Gores GJ, Paya CV, LaRusso NF. Cryptosporidium parvum activates nuclear factor kappaB in biliary epithelia preventing epithelial cell apoptosis. Gastroenterology 2001; 120:1774-83; PMID:11375958; http://dx.doi.org/10.1053/gast.2001.24850
16. Chen XM, O'Hara SP, Nelson JB, Splinter PL, Small AJ, Tietz PS, Limper AH, LaRusso NF. Multiple TLRs are expressed in human cholangiocytes and mediate host epithelial defense responses to Cryptosporidium parvum via activation of NF-kappaB. J Immunol 2005; 175:7447-56; PMID:16301652
17. Gookin JL, Duckett LL, Armstrong MU, Stauffer SH, Finnegan CP, Murtaugh MP, Argenzio RA. Nitric oxide synthase stimulates prostaglandin synthesis and barrier function in C. parvum-infected porcine ileum. Am J Physiol Gastrointest Liver Physiol 2004; 287:G571-81; PMID:15155179; http://dx.doi.org/10.1152/ajpgi. 00413.2003
18. Leitch GJ, He Q. Reactive nitrogen and oxygen species ameliorate experimental cryptosporidiosis in the neonatal BALB/c mouse model. Infect Immun 1999; 67:5885-91; PMID:10531244
19. Zaalouk TK, Bajaj-Elliott M, George JT, McDonald V. Differential regulation of beta-defensin gene expression during Cryptosporidium parvum infection. Infect Immun 2004; 72:2772-9; PMID:15102787; http://dx.doi.org/10. 1128/IAI.72.5.2772-2779.2004
20. Barakat FM, McDonald V, Foster GR, Tovey MG, Korbel DS. Cryptosporidium parvum infection rapidly induces a protective innate immune response involving type I interferon. J Infect Dis 2009; 200:1548-55; PMID:19821721; http://dx.doi.org/10.1086/644601
21. McDonald V, Bancroft GJ. Mechanisms of innate and acquired resistance to Cryptosporidium parvum infection in SCID mice. Parasite Immunol 1994; 16:315-20; PMID:7970868; http://dx.doi.org/10.1111/j.1365-3024.1994.tb00354.x
22. Hayward AR, Chmura K, Cosyns M. Interferon-gamma is required for innate immunity to Cryptosporidium parvum in mice. J Infect Dis 2000; 182:1001-4; PMID:10950807; http://dx.doi.org/10.1086/315802
23. Gomez Morales MA, La Rosa G, Ludovisi A, Onori AM, Pozio E. Cytokine profile induced by Cryptosporidium antigen in peripheral blood mononuclear cells from immunocompetent and immunosuppressed persons with cryptosporidiosis. J Infect Dis 1999; 179:967-73; PMID:10068593; http://dx.doi.org/10.1086/314665
24. Preidis GA, Wang HC, Lewis DE, Castellanos-Gonzalez A, Rogers KA, Graviss EA, Ward HD, White AC Jr. Seropositive human subjects produce interferon gamma after stimulation with recombinant Cryptosporidium hominis gp15. Am J Trop Med Hyg 2007; 77:583-5; PMID:17827383
25. Rohlman VC, Kuhls TL, Mosier DA, Crawford DL, Greenfield RA. Cryptosporidium parvum infection after abrogation of natural killer cell activity in normal and severe combined immunodeficiency mice. J Parasitol 1993; 79:295-7; PMID:8459345; http://dx.doi.org/10.2307/3283525
26. Dann SM, Wang HC, Gambarin KJ, Actor JK, Robinson P, Lewis DE, Caillat-Zucman S, White AC Jr. Interleukin-15 activates human natural killer cells to clear the intestinal protozoan cryptosporidium. J Infect Dis 2005; 192:1294-302; PMID:16136475; http://dx.doi.org/10.1086/444393
27. Pollok RC, Farthing MJ, Bajaj-Elliott M, Sanderson IR, McDonald V. Interferon gamma induces enterocyte resistance against infection by the intracellular pathogen Cryptosporidium parvum. Gastroenterology 2001; 120:99-107; PMID:11208718; http://dx.doi.org/10.1053/gast.2001.20907
28. Lean IS, McDonald V, Pollok RC. The role of cytokines in the pathogenesis of Cryptosporidium infection. Curr Opin Infect Dis 2002; 15:229-34; PMID:12015455; http://dx.doi.org/10.1097/00001432-200206000-00003
29. Heine J, Moon HW, Woodmansee DB. Persistent Cryptosporidium infection in congenitally athymic (nude) mice. Infect Immun 1984; 43:856-9; PMID:6607888
30. Mead JR, Arrowood MJ, Sidwell RW, Healey MC. Chronic Cryptosporidium parvum infections in congenitally immunodeficient SCID and nude mice. J Infect Dis 1991; 163:1297-304; PMID:2037795; http://dx.doi.org/10.1093/infdis/163.6. 1297
31. Huang DB, White AC. An updated review on Cryptosporidium and Giardia. [viii.]. Gastroenterol Clin North Am 2006; 35:291-314, viii; PMID:16880067; http://dx.doi.org/10.1016/j.gtc.2006.03.006
32. Chen W, Harp JA, Harmsen AG. Requirements for CD4+ cells and gamma interferon in resolution of established Cryptosporidium parvum infection in mice. Infect Immun 1993; 61:3928-32; PMID:8103040
33. Leav BA, Yoshida M, Rogers K, Cohen S, Godiwala N, Blumberg RS, Ward H. An early intestinal mucosal source of gamma interferon is associated with resistance to and control of Cryptosporidium parvum infection in mice. Infect Immun 2005; 73:8425-8; PMID:16299343; http://dx.doi.org/10.1128/IAI.73.12.8425- 8428.2005
34. Pantenburg B, Castellanos-Gonzalez A, Dann SM, Connelly RL, Lewis DE, Ward HD, White AC Jr. Human CD8(+) T cells clear Cryptosporidium parvum from infected intestinal epithelial cells. Am J Trop Med Hyg 2010; 82:600-7; PMID:20348507; http://dx.doi.org/10.4269/ajtmh.2010.09-0590
35. Urban JF Jr., Fayer R, Chen SJ, Gause WC, Gately MK, Finkelman FD. IL-12 protects immunocompetent and immunodeficient neonatal mice against infection with Cryptosporidium parvum. J Immunol 1996; 156:263-8; PMID:8598471
36. McDonald V, Pollok RC, Dhaliwal W, Naik S, Farthing MJ, Bajaj-Elliott M. A potential role for interleukin-18 in inhibition of the development of Cryptosporidium parvum. Clin Exp Immunol 2006; 145:555-62; PMID:16907926; http://dx.doi.org/10.1111/j.1365-2249.2006.03159.x
37. Ehigiator HN, Romagnoli P, Borgelt K, Fernandez M, McNair N, Secor WE, Mead JR. Mucosal cytokine and antigen-specific responses to Cryptosporidium parvum in IL-12p40 KO mice. Parasite Immunol 2005; 27:17-28; PMID:15813719; http://dx.doi.org/10.1111/j.1365-3024.2005.00736.x
38. Tessema TS, Schwamb B, Lochner M, Förster I, Jakobi V, Petry F. Dynamics of gut mucosal and systemic Th1/Th2 cytokine responses in interferon-gamma and interleukin-12p40 knock out mice during primary and challenge Cryptosporidium parvum infection. Immunobiology 2009; 214:454-66; PMID:19155092; http://dx.doi.org/10.1016/j.imbio.2008.11.015
39. Ehigiator HN, McNair N, Mead JR. Cryptosporidium parvum: the contribution of Th1-inducing pathways to the resolution of infection in mice. Exp Parasitol 2007; 115:107-13; PMID:16920103; http://dx.doi.org/10.1016/j.exppara.2006.07.001
40. Kassa M, Comby E, Lemeteil D, Brasseur P, Ballet J-J. Characterization of anti-Cryptosporidium IgA antibodies in sera from immunocompetent individuals and HIV-infected patients. J Protozool 1991; 38:179S-80S; PMID:1818157
41. Ungar BLP, Soave R, Fayer R, Nash TE. Enzyme immunoassay detection of immunoglobulin M and G antibodies to Cryptosporidium in immunocompetent and immunocompromised persons. J Infect Dis 1986; 153:570-8; PMID:3950440; http://dx.doi.org/10.1093/infdis/153.3.570
42. Okhuysen PC, Chappell CL, Sterling CR, Jakubowski W, DuPont HL. Susceptibility and serologic response of healthy adults to reinfection with Cryptosporidium parvum. Infect Immun 1998; 66:441-3; PMID:9453592
43. Cheng L, Rasmussen KR, Healey MC, Yang S. Primary and secondary infections with Cryptosporidium parvum in immunosuppressed adult mice. Am J Trop Med Hyg 1996; 55:324-9; PMID:8842123
44. Ehigiator HN, McNair N, Mead JR. IL-12 knockout C57BL/6 mice are protected from re-infection with Cryptosporidium parvum after challenge. J Eukaryot Microbiol 2003; 50(Suppl):539-41; PMID:14736155; http://dx.doi.org/10. 1111/j.1550-7408.2003.tb00622.x
45. Surl CG, Kim HC. Concurrent response to challenge infection with Cryptosporidium parvum in immunosuppressed C57BL/6N mice. J Vet Sci 2006; 7:47-51; PMID:16434849; http://dx.doi.org/10.4142/jvs.2006.7.1.47
46. McDonald V, Robinson HA, Kelly JP, Bancroft GJ. Immunity to Cryptosporidium muris infection in mice is expressed through gut CD4+ intraepithelial lymphocytes. Infect Immun 1996; 64:2556-62; PMID:8698479
47. McNair NN, Mead JR. CD4+ effector and memory cell populations protect against Cryptosporidium parvum infection. Microbes Infect 2013; 15:599-606; PMID:23644177; http://dx.doi.org/10.1016/j.micinf.2013.04.009
48. Gomez Morales MA, Mele R, Ludovisi A, Bruschi F, Tosini F, Riganò R, Pozio E. Cryptosporidium parvum-specific CD4 Th1 cells from sensitized donors responding to both fractionated and recombinant antigenic proteins. Infect Immun 2004; 72:1306-10; PMID:14977932; http://dx.doi.org/10.1128/IAI.72.3.1306- 1310.2004
49. Jakobi V, Petry F. Humoral immune response in IL-12 and IFN-gamma deficient mice after infection with Cryptosporidium parvum. Parasite Immunol 2008; 30:151-61; PMID:18179628; http://dx.doi.org/10.1111/j.1365-3024.2007. 01013.x
50. Chappell CL, Okhuysen PC, Sterling CR, Wang C, Jakubowski W, Dupont HL. Infectivity of Cryptosporidium parvum in healthy adults with pre-existing anti-C. parvum serum immunoglobulin G. Am J Trop Med Hyg 1999; 60:157-64; PMID:9988341
51. Freitas do Rosário AP, Muxel SM, Rodríguez-Málaga SM, Sardinha LR, Zago CA, Castillo-Méndez SI, Alvarez JM, D'Império Lima MR. Gradual decline in malaria-specific memory T cell responses leads to failure to maintain long-term protective immunity to Plasmodium chabaudi AS despite persistence of B cell memory and circulating antibody. J Immunol 2008; 181:8344-55; PMID:19050251
52. Jenkins M, Higgins J, Kniel K, Trout J, Fayer R. Protection of calves against cryptosporiosis by oral inoculation with gamma-irradiated Cryptosporidium parvum oocysts. J Parasitol 2004; 90:1178-80; PMID:15562625; http://dx.doi.org/10.1645/GE-3333RN
53. Kelly GS. Bovine colostrums: a review of clinical uses. Altern Med Rev 2003; 8:378-94; PMID:14653766
54. Crabb JH. Antibody-based immunotherapy of cryptosporidiosis. Adv Parasitol 1998; 40:121-49; PMID:9554072; http://dx.doi.org/10.1016/S0065- 308X(08)60119-0
55. Tzipori S, Roberton D, Chapman C. Remission of diarrhoea due to cryptosporidiosis in an immunodeficient child treated with hyperimmune bovine colostrum. Br Med J (Clin Res Ed) 1986; 293:1276-7; PMID:3096462; http://dx.doi.org/10.1136/bmj.293.6557.1276
56. Saxon A, Weinstein W. Oral administration of bovine colostrum anti-cryptosporidia antibody fails to alter the course of human cryptosporidiosis. J Parasitol 1987; 73:413-5; PMID:3585635; http://dx.doi.org/10.2307/3282099
57. Nord J, Ma P, DiJohn D, Tzipori S, Tacket CO. Treatment with bovine hyperimmune colostrum of cryptosporidial diarrhea in AIDS patients. AIDS 1990; 4:581-4; PMID:2201320; http://dx.doi.org/10.1097/00002030-199006000-00015
58. Ungar BLP, Ward DJ, Fayer R, Quinn CA. Cessation of Cryptosporidium- associated diarrhea in an acquired immunodeficiency syndrome patient after treatment with hyperimmune bovine colostrum. Gastroenterology 1990; 98:486-9; PMID:2295405
59. Florén CH, Chinenye S, Elfstrand L, Hagman C, Ihse I. ColoPlus, a new product based on bovine colostrum, alleviates HIV-associated diarrhoea. Scand J Gastroenterol 2006; 41:682-6; PMID:16716966; http://dx.doi.org/10.1080/ 00365520500380817
60. Greenberg PD, Cello JP. Treatment of severe diarrhea caused by Cryptosporidium parvum with oral bovine immunoglobulin concentrate in patients with AIDS. J Acquir Immune Defic Syndr Hum Retrovirol 1996; 13:348-54; PMID:8948373; http://dx.doi.org/10.1097/00042560-199612010-00008
61. Fries L, Hillman K, Crabb JH, Linberg S, Hamer D, Griffiths J, Keusch G, Soave R, Petersen C. Clinical and microbiological effects of bovine anti-Cryptosporidium immunoglobulin (BACI) on cryptosporidial diarrhea in patients with AIDS. 34th Interscience Conference on Antimicrobial Agents and Chemotherapy. Orlando, FL, 1994:Abstract 198.
62. Okhuysen PC, Chappell CL, Crabb J, Valdez LM, Douglass ET, DuPont HL. Prophylactic effect of bovine anti-Cryptosporidium hyperimmune colostrum immunoglobulin in healthy volunteers challenged with Cryptosporidium parvum. Clin Infect Dis 1998; 26:1324-9; PMID:9636857; http://dx.doi.org/10.1086/516374
63. Jenkins MC, O'Brien C, Trout J, Guidry A, Fayer R. Hyperimmune bovine colostrum specific for recombinant Cryptosporidium parvum antigen confers partial protection against cryptosporidiosis in immunosuppressed adult mice. Vaccine 1999; 17:2453-60; PMID:10392628; http://dx.doi.org/10.1016/S0264- 410X(98)00369-7
64. Perryman LE, Kapil SJ, Jones ML, Hunt EL. Protection of calves against cryptosporidiosis with immune bovine colostrum induced by a Cryptosporidium parvum recombinant protein. Vaccine 1999; 17:2142-9; PMID:10367947; http://dx.doi.org/10.1016/S0264-410X(98)00477-0
65. Burton AJ, Nydam DV, Jones G, Zambriski JA, Linden TC, Cox G, Davis R, Brown A, Bowman DD. Antibody responses following administration of a Cryptosporidium parvum rCP15/60 vaccine to pregnant cattle. Vet Parasitol 2011; 175:178-81; PMID:20951499; http://dx.doi.org/10.1016/j.vetpar.2010.09.013
66. Arrowood MJ, Mead JR, Mahrt JL, Sterling CR. Effects of immune colostrum and orally administered antisporozoite monoclonal antibodies on the outcome of Cryptosporidium parvum infections in neonatal mice. Infect Immun 1989; 57:2283-8; PMID:2744847
67. Doyle PS, Crabb J, Petersen C. Anti-Cryptosporidium parvum antibodies inhibit infectivity in vitro and in vivo. Infect Immun 1993; 61:4079-84; PMID:8406795
68. Perryman LE, Riggs MW, Mason PH, Fayer R. Kinetics of Cryptosporidium parvum sporozoite neutralization by monoclonal antibodies, immune bovine serum, and immune bovine colostrum. Infect Immun 1990; 58:257-9; PMID:2294054
69. Riggs MW, Stone AL, Yount PA, Langer RC, Arrowood MJ, Bentley DL. Protective monoclonal antibody defines a circumsporozoite-like glycoprotein exoantigen of Cryptosporidium parvum sporozoites and merozoites. J Immunol 1997; 158:1787-95; PMID:9029117
70. Schaefer DA, Auerbach-Dixon BA, Riggs MW. Characterization and formulation of multiple epitope-specific neutralizing monoclonal antibodies for passive immunization against cryptosporidiosis. Infect Immun 2000; 68:2608-16; PMID:10768951; http://dx.doi.org/10.1128/IAI.68.5.2608-2616.2000
71. Fan X, Upadhyaya B, Wu L, Koh C, Santín-Durán M, Pittaluga S, Uzel G, Kleiner D, Williams E, Ma CA, et al. CD40 agonist antibody mediated improvement of chronic Cryptosporidium infection in patients with X-linked hyper IgM syndrome. Clin Immunol 2012; 143:152-61; PMID:22459705; http://dx.doi.org/10.1016/j.clim.2012.01.014
72. Imboden M, Riggs MW, Schaefer DA, Homan EJ, Bremel RD. Antibodies fused to innate immune molecules reduce initiation of Cryptosporidium parvum infection in mice. Antimicrob Agents Chemother 2010; 54:1385-92; PMID:20086143; http://dx.doi.org/10.1128/AAC.00754-09
73. Abubakar I, Aliyu SH, Arumugam C, Usman NK, Hunter PR. Treatment of cryptosporidiosis in immunocompromised individuals: systematic review and meta-analysis. Br J Clin Pharmacol 2007; 63:387-93; PMID:17335543; http://dx.doi.org/10.1111/j.1365-2125.2007.02873.x
74. Dillingham RA, Lima AA, Guerrant RL. Cryptosporidiosis: epidemiology and impact. Microbes Infect 2002; 4:1059-66; PMID:12191656; http://dx.doi.org/10. 1016/S1286-4579(02)01630-1
75. Pasetti MF, Simon JK, Sztein MB, Levine MM. Immunology of gut mucosal vaccines. Immunol Rev 2011; 239:125-48; PMID:21198669; http://dx.doi.org/10. 1111/j.1600-065X.2010.00970.x
76. McDonald V, Shirley MW. Past and future: vaccination against Eimeria. Parasitology 2009; 136:1477-89; PMID:19523251; http://dx.doi.org/10.1017/ S0031182009006349
77. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, Serrano MG, Puiu D, Manque P, Akiyoshi D, Mackey AJ, et al. The genome of Cryptosporidium hominis. Nature 2004; 431:1107-12; PMID:15510150; http://dx.doi.org/10.1038/nature02977
78. Borad AJ, Allison GM, Wang D, Ahmed S, Karim MM, Kane AV, Moy J, Hibberd PL, Ajjampur SS, Kang G, et al. Systemic antibody responses to the immunodominant p23 antigen and p23 polymorphisms in children with cryptosporidiosis in Bangladesh. Am J Trop Med Hyg 2012; 86:214-22; PMID:22302851; http://dx.doi.org/10.4269/ajtmh.2012.11-0273
79. Sheoran A, Wiffin A, Widmer G, Singh P, Tzipori S. Infection with Cryptosporidium hominis provides incomplete protection of the host against Cryptosporidium parvum. J Infect Dis 2012; 205:1019-23; PMID:22279124; http://dx.doi.org/10.1093/infdis/jir874
80. Glass RI, Patel M, Parashar U. Lessons from the US rotavirus vaccination program. JAMA 2011; 306:1701-2; PMID:22009102; http://dx.doi.org/10.1001/jama. 2011.1475
81. Vesikari T. Rotavirus vaccination: a concise review. Clin Microbiol Infect 2012; 18(Suppl 5):57-63; PMID:22882248; http://dx.doi.org/10.1111/j.1469- 0691.2012.03981.x
82. Yu JR, Park WY. The effect of gamma-irradiation on the viability of Cryptosporidium parvum. J Parasitol 2003; 89:639-42; PMID:12880278; http://dx.doi.org/10.1645/0022-3395(2003)089[0639:TEOIOT]2.0.CO;2
83. Boulter-Bitzer JI, Lee H, Trevors JT. Molecular targets for detection and immunotherapy in Cryptosporidium parvum. Biotechnol Adv 2007; 25:13-44; PMID:17055210; http://dx.doi.org/10.1016/j.biotechadv.2006.08.003
84. Wanyiri JW, O'Connor R, Allison G, Kim K, Kane A, Qiu J, Plaut AG, Ward HD. Proteolytic processing of the Cryptosporidium glycoprotein gp40/15 by human furin and by a parasite-derived furin-like protease activity. Infect Immun 2007; 75:184-92; PMID:17043102; http://dx.doi.org/10.1128/IAI.00944-06
85. O'Connor RM, Wanyiri JW, Cevallos AM, Priest JW, Ward HD. Cryptosporidium parvum glycoprotein gp40 localizes to the sporozoite surface by association with gp15. Mol Biochem Parasitol 2007; 156:80-3; PMID:17719100; http://dx.doi.org/10.1016/j.molbiopara.2007.07.010
86. Priest JW, Xie LT, Arrowood MJ, Lammie PJ. The immunodominant 17-kDa antigen from Cryptosporidium parvum is glycosylphosphatidylinositol-anchored. Mol Biochem Parasitol 2001; 113:117-26; PMID:11254960; http://dx.doi.org/10. 1016/S0166-6851(00)00386-8
87. Gut J, Nelson RG. Cryptosporidium parvum sporozoites deposit trails of 11A5 antigen during gliding locomotion and shed 11A5 antigen during invasion of MDCK cells in vitro. J Eukaryot Microbiol 1994; 41:42S-3S; PMID:7528594
88. Arrowood MJ, Sterling CR, Healey MC. Immunofluorescent microscopical visualization of trails left by gliding Cryptosporidium parvum sporozoites. J Parasitol 1991; 77:315-7; PMID:2010865; http://dx.doi.org/10.2307/3283104
89. Perryman LE, Jasmer DP, Riggs MW, Bohnet SG, McGuire TC, Arrowood MJ. A cloned gene of Cryptosporidium parvum encodes neutralization-sensitive epitopes. Mol Biochem Parasitol 1996; 80:137-47; PMID:8892291; http://dx.doi.org/10.1016/ 0166-6851(96)02681-3
90. Mueller AK, Labaied M, Kappe SH, Matuschewski K. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 2005; 433:164-7; PMID:15580261; http://dx.doi.org/10.1038/nature03188
91. Widmer G, Sullivan S. Genomics and population biology of Cryptosporidium species. Parasite Immunol 2012; 34:61-71; PMID:21595702; http://dx.doi.org/10. 1111/j.1365-3024.2011.01301.x
92. Hong-Xuan H, Lei C, Cheng-Min W, Kai Z, Yi T, Xi-Ming Q, Ming-Xing D. Expression of the recombinant fusion protein CP15-23 of Cryptosporidium parvum and its protective test. J Nanosci Nanotechnol 2005; 5:1292-6; PMID:16193995; http://dx.doi.org/10.1166/jnn.2005.210
93. Jenkins M, Kerr D, Fayer R, Wall R. Serum and colostrum antibody responses induced by jet-injection of sheep with DNA encoding a Cryptosporidium parvum antigen. Vaccine 1995; 13:1658-64; PMID:8719516; http://dx.doi.org/10. 1016/0264-410X(95)00121-G
94. Sagodira S, Buzoni-Gatel D, Iochmann S, Naciri M, Bout D. Protection of kids against Cryptosporidium parvum infection after immunization of dams with CP15-DNA. Vaccine 1999; 17:2346-55; PMID:10392616; http://dx.doi.org/10.1016/ S0264-410X(99)00041-9
95. Sagodira S, Iochmann S, Mevelec MN, Dimier-Poisson I, Bout D. Nasal immunization of mice with Cryptosporidium parvum DNA induces systemic and intestinal immune responses. Parasite Immunol 1999; 21:507-16; PMID:10587377; http://dx.doi.org/10.1046/j.1365-3024.1999.00247.x
96. Tilley M, Upton SJ, Fayer R, Barta JR, Chrisp CE, Freed PS, Blagburn BL, Anderson BC, Barnard SM. Identification of a 15-kilodalton surface glycoprotein on sporozoites of Cryptosporidium parvum. Infect Immun 1991; 59:1002-7; PMID:1705238
97. He H, Zhao B, Liu L, Zhou K, Qin X, Zhang Q, Li X, Zheng C, Duan M. The humoral and cellular immune responses in mice induced by DNA vaccine expressing the sporozoite surface protein of Cryptosporidium parvum. DNA Cell Biol 2004; 23:335-9; PMID:15169612; http://dx.doi.org/10.1089/104454904323090967
98. Ehigiator HN, Romagnoli P, Priest JW, Secor WE, Mead JR. Induction of murine immune responses by DNA encoding a 23-kDa antigen of Cryptosporidium parvum. Parasitol Res 2007; 101:943-50; PMID:17487508; http://dx.doi.org/10. 1007/s00436-007-0565-0
99. Wang C, Luo J, Amer S, Guo Y, Hu Y, Lu Y, Wang H, Duan M, He H. Multivalent DNA vaccine induces protective immune responses and enhanced resistance against Cryptosporidium parvum infection. Vaccine 2010; 29:323-8; PMID:21029808; http://dx.doi.org/10.1016/j.vaccine.2010.10.034
100. Priest JW, Kwon JP, Montgomery JM, Bern C, Moss DM, Freeman AR, Jones CC, Arrowood MJ, Won KY, Lammie PJ, et al. Cloning and characterization of the acidic ribosomal protein P2 of Cryptosporidium parvum, a new 17-kilodalton antigen. Clin Vaccine Immunol 2010; 17:954-65; PMID:20410328; http://dx.doi.org/10.1128/CVI.00073-10
101. Benitez A, Priest JW, Ehigiator HN, McNair N, Mead JR. Evaluation of DNA encoding acidic ribosomal protein P2 of Cryptosporidium parvum as a potential vaccine candidate for cryptosporidiosis. Vaccine 2011; 29:9239-45; PMID:21968447; http://dx.doi.org/10.1016/j.vaccine.2011.09.094
102. Kang DH. Development of membrane filter holder (MFH) method for recovery of heat-injured Escherichia coli O157:H7 and Salmonella typhimurium. Lett Appl Microbiol 2002; 34:62-6; PMID:11849495; http://dx.doi.org/10.1046/j.1472-765x. 2002.01038.x
103. Konjufca V, Jenkins M, Wang S, Juarez-Rodriguez MD, Curtiss R 3rd. Immunogenicity of recombinant attenuated Salmonella enterica serovar Typhimurium vaccine strains carrying a gene that encodes Eimeria tenella antigen SO7. Infect Immun 2008; 76:5745-53; PMID:18809658; http://dx.doi.org/10.1128/IAI. 00897-08
104. Qu D, Yu H, Wang S, Cai W, Du A. Induction of protective immunity by multiantigenic DNA vaccine delivered in attenuated Salmonella typhimurium against Toxoplasma gondii infection in mice. Vet Parasitol 2009; 166:220-7; PMID:19740610; http://dx.doi.org/10.1016/j.vetpar.2009.08.016
105. Benitez AJ, McNair N, Mead JR. Oral immunization with attenuated Salmonella enterica serovar Typhimurium encoding Cryptosporidium parvum Cp23 and Cp40 antigens induces a specific immune response in mice. Clin Vaccine Immunol 2009; 16:1272-8; PMID:19605593; http://dx.doi.org/10.1128/CVI.00089-09
106. Manque PA, Tenjo F, Woehlbier U, Lara AM, Serrano MG, Xu P, Alves JM, Smeltz RB, Conrad DH, Buck GA. Identification and immunological characterization of three potential vaccinogens against Cryptosporidium species. Clin Vaccine Immunol 2011; 18:1796-802; PMID:21918117; http://dx.doi.org/10.1128/CVI.05197-11
107. Roche JK, Rojo AL, Costa LB, Smeltz R, Manque P, Woehlbier U, Bartelt L, Galen J, Buck G, Guerrant RL. Intranasal vaccination in mice with an attenuated Salmonella enterica Serovar 908htr A expressing Cp15 of Cryptosporidium: impact of malnutrition with preservation of cytokine secretion. Vaccine 2013; 31:912-8; PMID:23246541; http://dx.doi.org/10.1016/j.vaccine.2012.12.007
108. Di Cristina M, Ghouze F, Kocken CH, Naitza S, Cellini P, Soldati D, Thomas AW, Crisanti A. Transformed Toxoplasma gondii tachyzoites expressing the circumsporozoite protein of Plasmodium knowlesi elicit a specific immune response in rhesus monkeys. Infect Immun 1999; 67:1677-82; PMID:10085003
109. Charest H, Sedegah M, Yap GS, Gazzinelli RT, Caspar P, Hoffman SL, Sher A. Recombinant attenuated Toxoplasma gondii expressing the Plasmodium yoelii circumsporozoite protein provides highly effective priming for CD8+ T cell-dependent protective immunity against malaria. J Immunol 2000; 165:2084-92; PMID:10925293
110. O'Connor RM, Kim K, Khan F, Ward HD. Expression of Cpgp40/15 in Toxoplasma gondii: a surrogate system for the study of Cryptosporidium glycoprotein antigens. Infect Immun 2003; 71:6027-34; PMID:14500524; http://dx.doi.org/10.1128/IAI.71.10.6027-6034.2003
111. Shirafuji H, Xuan X, Kimata I, Takashima Y, Fukumoto S, Otsuka H, Nagasawa H, Suzuki H. Expression of P23 of Cryptosporidium parvum in Toxoplasma gondii and evaluation of its protective effects. J Parasitol 2005; 91:476-9; PMID:15986633; http://dx.doi.org/10.1645/GE-364R1
112. Jongert E, Roberts CW, Gargano N, Förster-Waldl E, Petersen E. Vaccines against Toxoplasma gondii: challenges and opportunities. Mem Inst Oswaldo Cruz 2009; 104:252-66; PMID:19430651; http://dx.doi.org/10.1590/S0074- 02762009000200019
113. Geriletu XR, Xu R, Jia H, Terkawi MA, Xuan X, Zhang H. Immunogenicity of orally administrated recombinant Lactobacillus casei Zhang expressing Cryptosporidium parvum surface adhesion protein P23 in mice. Curr Microbiol 2011; 62:1573-80; PMID:21336991; http://dx.doi.org/10.1007/s00284-011-9894-4
114. Douradinha B, Reis V, Rogers M, Torres F, Evans J, Marques E Jr. Novel insights in genetic transformation of the probiotic yeast Saccharomyces boulardii. Bioengineered 2013; 5: (Forthcoming); PMID:24013355
115. Zimmermann S, Dalpke A, Heeg K. CpG oligonucleotides as adjuvant in therapeutic vaccines against parasitic infections. Int J Med Microbiol 2008; 298:39-44; PMID:17716944; http://dx.doi.org/10.1016/j.ijmm.2007.07.011
116. Barrier M, Lacroix-Lamandé S, Mancassola R, Auray G, Bernardet N, Chaussé AM, Uematsu S, Akira S, Laurent F. Oral and intraperitoneal administration of phosphorothioate oligodeoxynucleotides leads to control of Cryptosporidium parvum infection in neonatal mice. J Infect Dis 2006; 193:1400-7; PMID:16619188; http://dx.doi.org/10.1086/503748