Cryptosporidium-malnutrition interactions: Mucosal disruption, cytokines, and TLR signaling in a weaned murine model

Journal of Parasitology

Volumn 97, Issue 6, 2011, Pages 1113-1120

  Costa, Lourrany B ^a,b   Johnbull, Eric A ^a   Reeves, Jordan T ^a   Sevilleja, Jesus Emmanuel ^a   Freire, Rosemayre S ^a,b   Hoffman, Paul S ^a   Lima, Aldo A M ^a,b   Ori, Reinaldo B ^a,b   Roche, James K ^a   Guerrant, Richard L ^a   Warren, Cirle Alcantara ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; MESSENGER RNA; NITAZOXANIDE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

CHILD HEALTH; DEVELOPING WORLD; DIARRHEAL DISEASE; GROWTH RATE; INFECTIVITY; MALNUTRITION; MORPHOMETRY; PARASITIC DISEASE; PATHOGEN; PROTEIN; RODENT; WEANING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLON; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; CYTOKINE RESPONSE; DRUG TREATMENT FAILURE; FECES ANALYSIS; FEMALE; GROWTH RETARDATION; ILEUM; INTESTINE; INTESTINE CRYPT; INTESTINE MUCOSA; INTESTINE VILLUS; MALNUTRITION; MORPHOMETRICS; MOUSE; NONHUMAN; NUTRITIONAL STATUS; OOCYTE; PARASITE IDENTIFICATION; PARASITE PHENOMENA AND FUNCTIONS; PROTEIN DEFICIENCY; SIGNAL TRANSDUCTION; TH1 CELL; WEANING; WEIGHT REDUCTION;

ANIMALS; ANTIPARASITIC AGENTS; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; CYTOKINES; DISEASE MODELS, ANIMAL; DNA, PROTOZOAN; FECES; FEMALE; ILEUM; INTESTINAL MUCOSA; MALNUTRITION; MICE; MICE, INBRED C57BL; RNA, MESSENGER; THIAZOLES; TOLL-LIKE RECEPTORS; WEANING; WEIGHT GAIN;

ANIMALIA; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM PARVUM; MURINAE; MUS;

EID: 84855387264     PISSN: 00223395     EISSN: 19372345     Source Type: Journal    
DOI: 10.1645/GE-2848.1     Document Type: Article

References (48)

1. ABREU, M. T., M. FUKATA, AND M. ARDITI. 2005. TLR signaling in the gut in health and disease. Journal of Immunology 174: 4453-4460.
2. ABUBAKAR, I., S. H. ALIYU, C. ARUMUGAM, P. R. HUNTER, AND N. K. USMAN. 2007. Prevention and treatment of cryptosporidiosis in immunocompromised patients. Cochrane Database Systems Review CD004932.
3. AGNEW, D. G., A. A. LIMA, R. D. NEWMAN, T. WUHIB, R. D. MOORE, R. L. GUERRANT, AND C. L. SEARS. 1998. Cryptosporidiosis in northeastern Brazilian children: Association with increased diarrhea morbidity. Journal of Infectious Disease 177: 754-760. (Pubitemid 28099893)
4. ALCANTARA, W. C., R. V. DESTURA, J. E. SEVILLEJA, L. F. BARROSO, H. CARVALHO, L. J. BARRETT, A. D. O'BRIEN, AND R. L. GUERRANT. 2008. Detection of epithelial-cell injury, and quantification of infection, in the HCT-8 organoid model of cryptosporidiosis. Journal of Infectious Diseases 198: 143-149. (Pubitemid 351920301)
5. AMADI, B, M. MWIYA, S. SIANONGO, L. PAYNE, A. WATUKA, M. KATUBULUSHI, AND P. KELLY. 2009. High dose prolonged treatment with nitazoxanide is not effective for cryptosporidiosis in HIV positive Zambian children: A randomised controlled trial. BMC Infectious Diseases 9: 195.
6. ANDERSON, V. R., AND M. P. CURRAN. 2007. Nitazoxanide: A review of its use in the treatment of gastrointestinal infections. Drugs 67: 1947-1967. (Pubitemid 47347408)
7. ARMSON, A., R. C. THOMPSON, AND J. A. REYNOLDSON. 2003. A review of chemotherapeutic approaches to the treatment of cryptosporidiosis. Expert Review of Anti-Infective Therapy 1: 297-305. (Pubitemid 38855094)
8. BARRIER, M., S. LACROIX-LAMANDE, R. MANCASSOLA, G. AURAY, N. BERNARDET, A.M. CHAUSSE, S. UEMATSU, S. AKIRA, AND F. LAURENT. 2006. Oral and intraperitoneal administration of phosphorothioate oligodeoxynucleotides leads to control of Cryptosporidium parvum infection in neonatal mice. Journal of Infectious Diseases 193: 1400-1407. (Pubitemid 43673388)
9. BLAGBURN, B. L., K. L. DRAIN, T. M. LAND, R. G. KINARD, P. H. MOORE, D. S. LINDSAY, D. A. PATRICK, D. W. BOYKIN, AND R. R. TIDWELL. 1998. Comparative efficacy evaluation of dicationic carbazole compounds, nitazoxanide, and paromomycin against Cryptosporidium parvum infections in a neonatal mouse model. Antimicrobial Agents and Chemothery 42: 2877-2882. (Pubitemid 28501219)
10. BORAD, A., AND H. WARD. 2010. Human immune responses in cryptosporidiosis. Future Microbiology 5: 507-519.
11. BRANTLEY, R. K., K. R. WILLIAMS, T. M. SILVA, M. SISTROM, N. M. THIELMAN, H. WARD,A. A. LIMA, AND R. L. GUERRANT. 2003. AIDSassociated diarrhea and wasting in northeast Brazil is associated with subtherapeutic plasma levels of antiretroviral medications and with both bovine and human subtypes of Cryptosporidium parvum. Brazilian Journal of Infectious Diseases 7: 16-22.
12. BUSHEN, O. Y., A. KOHLI, R. C. PINKERTON, K. DUPNIK, R. D. NEWMAN, C. L. SEARS, R. FAYER, A. A. LIMA, AND R. L. GUERRANT. 2007. Heavy cryptosporidial infections in children in northeast Brazil: Comparison of Cryptosporidium hominis and Cryptosporidium parvum. Transactions of the Royal Society of Tropical Medicine and Hygiene 101: 378-384. (Pubitemid 46205893)
13. CHEN, X. M., S. P. O'HARA, J. B. NELSON, P. L. SPLINTER, A. J. SMALL, P. S. TIETZ, A. H. LIMPER, AND N. F. LARUSSO. 2005. Multiple TLRs are expressed in human cholangiocytes and mediate host epithelial defense responses to Cryptosporidium parvum via activation of NFkappaB. Journal of Immunology 175: 7447-7456. (Pubitemid 41713442)
14. -, P. L. SPLINTER, S. P. O'HARA, AND N. F. LARUSSO. 2007. A cellular micro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. Journal of Biological Chemistry 282: 28929-28938. (Pubitemid 47610421)
15. CHENG, L., K. R. RASMUSSEN, M. C.HEALEY, AND S. YANG. 1996. Primary and secondary infections with Cryptosporidium parvum in immunosuppressed adult mice. American Journal of Tropical Medicine and Hygiene 55: 324-329. (Pubitemid 26321840)
16. COUTINHO, B. P., R. B. ORIA, C.M.VIEIRA, J. E. SEVILLEJA, C. A.WARREN, J. G. MACIEL, M. R. THOMPSON, R. C. PINKERTON, A. A. LIMA, AND R. L. GUERRANT. 2008. Cryptosporidium infection causes undernutrition and, conversely, weanling undernutrition intensifies infection. Journal of Parasitology 94: 1225-1232.
17. DIAZ, E., J. MONDRAGON, E. RAMIREZ, AND R. BERNAL. 2003. Epidemiology and control of intestinal parasites with nitazoxanide in children in Mexico. American Journal of Tropical Medicine and Hygiene 68:384-385. (Pubitemid 38230634)
18. DILLINGHAM, R. A., A. A. LIMA, AND R. L. GUERRANT. 2002. Cryptosporidiosis: Epidemiology and impact. Microbes and Infection 4:1059-1066. (Pubitemid 35015174)
19. GARGALA, G. 2008. Drug treatment and novel drug target against Cryptosporidium. Parasite 15: 275-281.
20. -, A. DELAUNAY, X. LI, P. BRASSEUR, L. FAVENNEC, AND J. J. BALLET. 2000. Efficacy of nitazoxanide, tizoxanide and tizoxanide glucuronide against Cryptosporidium parvum development in sporozoite-infected HCT-8 enterocytic cells. Journal of Antimicrobial Chemotherapy 46:57-60. (Pubitemid 30466196)
21. GENDREL, D., J. M. TRELUYER, AND D. RICHARD-LENOBLE. 2003. Parasitic diarrhea in normal and malnourished children. Fundamental and Clinical Pharmacology 17: 189-197. (Pubitemid 36513210)
22. GRIFFITHS, J. K., C. THEODOS, M. PARIS, AND S. TZIPORI. 1998. The gamma interferon gene knockout mouse: A highly sensitive model for evaluation of therapeutic agents against Cryptosporidium parvum. Journal of Clinical Microbiology 36: 2503-2508. (Pubitemid 28380946)
23. GUERRANT, D. I., A. A. LIMA, AND F. DAVIDSON. 2000. Micronutrients and infection: Interactions and implications with enteric and other infections and future priorities. Journal of Infecious Diseases 182(Suppl. 1): S134-S138.
24. -, S. R. MOORE, A. A. LIMA, P. D. PATRICK, J. B. SCHORLING, AND R. L. GUERRANT. 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. American Journal of Tropical Medicine and Hygiene 61: 707-713.
25. HUANG, D. B., C. CHAPPELL, AND P. C. OKHUYSEN. 2004. Cryptosporidiosis in children. Seminars in Pediatric Infectious Disease 15: 253-259. (Pubitemid 39371106)
26. KATONA, P., AND J. KATONA-APTE. 2008. The interaction between nutrition and infection. Clinical Infectious Diseases 46:1582-1588. (Pubitemid 351706741)
27. MAGGI, P., A. M. LAROCCA, M. QUARTO, G. SERIO, O. BRANDONISIO, G. ANGARANO, AND G. PASTOREL. 2000. Effect of antiretroviral therapy on cryptosporidiosis and microsporidiosis in patients infected with human immunodeficiency virus type 1. European Journal of Clinical Microbiology and Infectious Diseases 19: 213-217. (Pubitemid 30201298)
28. MEAD, J. R., M. J. ARROWOOD, R.W. SIDWELL, AND M. C. HEALEY. 1991. Chronic Cryptosporidium parvum infections in congenitally immunodeficient SCID and nude mice. Journal of Infectious Diseases 163:1297-1304.
29. MONDAL, D., R. HAQUE, R. B. SACK, B. D. KIRKPATRICK, AND W. A. PETRI, JR. 2009. Attribution of malnutrition to cause-specific diarrheal illness: Evidence from a prospective study of preschool children in Mirpur, Dhaka, Bangladesh. American Journal of Tropical Medicine and Hygiene 80: 824-836.
30. NEWMAN, R. D., C. L. SEARS, S. R. MOORE, J. P. NATARO, T. WUHIB, D. A. AGNEW, R. L. GUERRANT, AND A. A. LIMA. 1999. Longitudinal study of Cryptosporidium infection in children in northeastern Brazil. Journal of Infectious Diseases 180: 167-175. (Pubitemid 29293931)
31. O'HARA, S. P., A. J. SMALL, G. B. GAJDOS, A. D. BADLEY, X. M. CHEN, AND N. F. LARUSSO. 2009. HIV-1 Tat protein suppresses cholangiocyte toll-like receptor 4 expression and defense against Cryptosporidium parvum. Journal of Infectious Diseases 199: 1195-1204.
32. ORENSTEIN, J. M. 1997. Cryptosporidiosis. In Pathology of infectious diseases, D. H. Connor, F. W. Chandler, H. J. Manz, D. A. Schwartz, and E. E. Lack (eds.). Appleton and Lange, Stamford, Connecticut, p. 1147-1168.
33. PANTENBURG, B., S. M. DANN, H. C. WANG, P. ROBINSON, A. CASTELLANOS-GONZALEZ, D. E. LEWIS, AND A. C. WHITE, JR. 2008. Intestinal immune response to human Cryptosporidium sp. infection. Infection and Immunity 76: 23-29.
34. PFAFFL, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: e45.
35. POZIO, E., G. REZZA, A.BOSCHINI, P. PEZZOTTI, A. TAMBURRINI, P.ROSSI, C. DI FINE SMACCHIA, A. SCHIESARI, E. GATTEI, R. ZUCCONI, AND P. BALLARINI. 1997. Clinical cryptosporidiosis and human immunodeficiency virus (HIV)-induced immunosuppression: Findings from a longitudinal study of HIV-positive and HIV-negative former injection drug users. Journal of Infectious Diseases 176: 969-975. (Pubitemid 27411039)
36. RASMUSSEN, K. R., AND M. C. HEALEY. 1992. Experimental Cryptosporidium parvum infections in immunosuppressed adult mice. Infection and Immunity 60: 1648-1652.
37. ROGERS, K. A., A. B. ROGERS, B. A. LEAV, A. SANCHEZ, E. VANNIER, S. UEMATSU, S. AKIRA, D. GOLENBOCK, AND H. D.WARD. 2006. MyD88-dependent pathways mediate resistance to Cryptosporidium parvum infection in mice. Infection and Immunity 74: 549-556. (Pubitemid 43023110)
38. ROSSIGNOL, J. F. 2010. Cryptosporidium and Giardia: Treatment options and prospects for new drugs. Experimental Parasitology 124: 45-53.
39. -, A. AYOUB, AND M. S. AYERS. 2001. Treatment of diarrhea caused by Cryptosporidium parvum: A prospective randomized, double-blind, placebo-controlled study of nitazoxanide. Journal of Infectious Diseases 184:103-106. (Pubitemid 32568508)
40. SASAHARA, T., H. MARUYAMA, M. AOKI, R. KIKUNO, T. SEKIGUCHI, A. TAKAHASHI, Y. SATOH, H. KITASATO, Y. TAKAYAMA, AND M. INOUE. 2003. Apoptosis of intestinal crypt epithelium after Cryptosporidium parvum infection. Journal of Infection and Chemotherapy 9: 278-281. (Pubitemid 37288297)
41. SMITH, H. V., AND G. D. CORCORAN. 2004. New drugs and treatment for cryptosporidiosis. Current Opinion in Infectious Diseases 17:557-564. (Pubitemid 39627517)
42. SURL, C. G., AND H. C. KIM. 2006. Concurrent response to challenge infection with Cryptosporidium parvum in immunosuppressed C57BL/6N mice. Journal of Veterinary Science 7: 47-51.
43. THEODOS, C. M., J. K. GRIFFITHS, J. D'ONFRO, A. FAIRFIELD, AND S. TZIPORI. 1998. Efficacy of nitazoxanide against Cryptosporidium parvum in cell culture and in animal models. Antimicrobial Agents and Chemotherapy 42: 1959-1965. (Pubitemid 28363076)
44. TZIPORI, S., W. RAND, AND C. THEODOS. 1995. Evaluation of a two-phase scid mouse model preconditioned with anti-interferon-gamma monoclonal antibody for drug testing against Cryptosporidium parvum. Journal of Infectious Diseases 172: 1160-1164.
45. -, AND H. WARD. 2002. Cryptosporidiosis: Biology, pathogenesis, and disease. Microbes and Infection 4: 1047-1058.
46. -, AND G. WIDMER. 2008. A hundred-year retrospective on cryptosporidiosis. Trends in Parasitology 24: 184-189.
47. UNGAR, B. L., J. A. BURRIS, C. A. QUINN, AND F. D. FINKELMAN. 1990. New mouse models for chronic Cryptosporidium infection in immunodeficient hosts. Infection and Immunity 58: 961-969. (Pubitemid 20117026)
48. ZULU, I., P. KELLY, L. NJOBVU, S. SIANONGO, K. KAONGA, V. MCDONALD, M. FARTHING, AND R. POLLOK. 2005. Nitazoxanide for persistent diarrhoea in Zambian acquired immune deficiency syndrome patients: A randomized-controlled trial. Alimentary Pharmacology and Therapeutics 21: 757-563.