Neutrophils do not mediate the pathophysiological sequelae of Cryptosporidium parvum infection in neonatal piglets

Infection and Immunity

Volumn 74, Issue 10, 2006, Pages 5497-5505

  Zadrozny, Leah M ^a   Stauffer, Stephen H ^a   Armstrong, Martha U ^a   Jones, Samuel L ^a   Gookin, Jody L ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD18 ANTIBODY; MONOCLONAL ANTIBODY; MYELOPEROXIDASE; PROSTAGLANDIN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; DIARRHEA; ENZYME ACTIVITY; INFLAMMATION; INTESTINE EPITHELIUM; INTESTINE VILLUS ATROPHY; LEUKOCYTE ACTIVATION; LIPID PEROXIDATION; NEUTROPHIL; NEWBORN; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS;

ANIMALS; ANTIBODIES; ANTIGENS, CD18; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; DIARRHEA; DISEASE MODELS, ANIMAL; ILEUM; IMMUNOGLOBULIN G; INTESTINAL MUCOSA; LIPID PEROXIDATION; NEUTROPHILS; PEROXIDASE; PEROXYNITROUS ACID; PROSTAGLANDINS; SUPEROXIDES; SWINE;

EID: 33749266724     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00153-06     Document Type: Article

References (44)

1. Argenzio, R. A., M. Armstrong, and J. M. Rhoads. 1996. Role of the enteric nervous system in piglet cryptosporidiosis. J. Pharmacol. Exp. Ther. 279:1109-1115.
2. Argenzio, R. A., J. Lecce, and D. W. Powell. 1993. Prostanoids inhibit intestinal NaCl absorption in experimental porcine cryptosporidiosis. Gastroenterology 104:440-447.
3. Argenzio, R. A., J. A. Liacos, M. L. Levy, D. J. Meuten, J. G. Lecce, and D. W. Powell. 1990. Villous atrophy, crypt hyperplasia, cellular infiltration, and impaired glucose-Na absorption in enteric cryptosporidiosis of pigs. Gastroenterology 98:1129-1140.
4. Argenzio, R. A., and J. M. Rhoads. 1997. Reactive oxygen metabolites in piglet cryptosporidiosis. Pediatr. Res. 41:521-526.
5. Chen, X. L., Q. Zhang, R. Zhao, X. Ding, P. E. Tummala, and R. M. Medford. 2003. Rac1 and superoxide are required for the expression of cell adhesion molecules induced by tumor necrosis factor-alpha in endothelial cells. J. Pharmacol. Exp. Ther. 305:573-580.
6. Crissinger, K. D., M. B. Grisham, and D. N. Granger. 1989. Developmental biology of oxidant-producing enzymes and antioxidants in the piglet intestine. Pediatr. Res. 25:612-616.
7. Deng, M., C. A. Lancto, and M. S. Abrahamsen. 2004. Cryptosporidium parvum regulation of human epithelial cell gene expression. Int. J. Parasitol. 34:73-82.
8. Genta, R. M., C. L. Chappell, A. C. White, Jr., K. T. Kimball, and R. W. Goodgame. 1993. Duodenal morphology and intensity of infection in AIDS-related intestinal cryptosporidiosis. Gastroenterology 105:1769-1775.
9. Goodgame, R. W., K. Kimball, C. N. Ou, A. C. White, Jr., R. M. Genta, C. H. Lifschitz, and C. L. Chappell. 1995. Intestinal function and injury in acquired immunodeficiency syndrome-related cryptosporidiosis. Gastroenterology 108:1075-1082.
10. Gookin, J. L., J. Allen, S. Chiang, L. Duckett, and M. U. Armstrong. 2005. Local peroxynitrite formation contributes to early control of Cryptosporidium parvum infection. Infect. Immun. 73:3929-3936.
11. Gookin, J. L., S. Chiang, J. Allen, M. U. Armstrong, S. H. Stauffer, C. Finnegan, and M. P. Murtaugh. 2006. NF-KB-mediated expression of iNOS promotes epithelial defense against infection by Cryptosporidium parvum in neonatal piglets. Am. J. Physiol. Gastrointest. Liver Physiol. 290:G164-G174.
12. Gookin, J. L., L. L. Duckett, M. U. Armstrong, S. H. Stauffer, C. P. Finnegan, M. P. Murtaugh, and R. A. Argenzio. 2004. Nitric oxide synthase stimulates prostaglandin synthesis and barrier function in C. parvum-infected porcine ileum. Am. J. Physiol. Gastrointest. Liver Physiol. 287:G571-G581.
13. Grisham, M. B., L. A. Hernandez, and D. N. Granger. 1986. Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am. J. Physiol. 251:G567-G574.
14. Grisham, M. B., D. Jourd'Heuil, and D. A. Wink. 1999. Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites: implications in inflammation. Am. J. Physiol. 276:G315-G321.
15. Huang, K., and S. Yang. 2002. Inhibitory effect of selenium on Cryptosporidium parvum infection in vitro and in vivo. Biol. Trace Elem. Res. 90:261-272.
16. Kagnoff, M. F., and L. Eckmann. 1997. Epithelial cells as sensors for microbial infection. J. Clin. Investig. 100:6-10.
17. Kandil, H. M., H. M. Berschneider, and R. A. Argenzio. 1994. Tumour necrosis factor alpha changes porcine intestinal ion transport through a paracrine mechanism involving prostaglandins. Gut 35:934-940.
18. Kishimoto, T. K., and R. Rothlein. 1994. Integrins, ICAMs, and selectins: role and regulation of adhesion molecules in neutrophil recruitment to inflammatory sites. Adv. Pharmacol. 25:117-169.
19. Kruidenier, L., M. E. van Meeteren, I. Kuiper, D. Jaarsma, C. B. Lamers, F. J. Zijlstra, and H. W. Verspaget. 2003. Attenuated mild colonic inflammation and improved survival from severe DSS-colitis of transgenic Cu/Zn-SOD mice. Free Radic. Biol. Med. 34:753-765.
20. Kucharzik, T., J. T. Hudson III, A. Lugering, J. A. Abbas, M. Bettini, J. G. Lake, M. E. Evans, T. R. Ziegler, D. Merlin, J. L. Madara, and I. R. Williams. 2005. Acute induction of human IL-8 production by intestinal epithelium triggers neutrophil infiltration without mucosal injury. Gut 54:1565-1572.
21. Lacroix-Lamandé, S., R. Mancassola, M. Naciri, and F. Laurent. 2002. Role of gamma interferon in chemokine expression in the ileum of mice and in a murine intestinal epithelial cell line after Cryptosporidium parvum infection. Infect. Immun. 70:2090-2099.
22. Laurent, F., L. Eckmann, T. C. Savidge, G. Morgan, C. Theodos, M. Naciri, and M. F. Kagnoff. 1997. Cryptosporidium parvum infection of human intestinal epithelial cells induces the polarized secretion of C-X-C chemokines. Infect. Immun. 65:5067-5073.
23. Lumadue, J. A., Y. C. Manabe, R. D. Moore, P. C. Belitsos, C. L. Sears, and D. P. Clark. 1998. A clinicopathologic analysis of AIDS-related cryptosporidiosis. AIDS 12:2459-2466.
24. Madara, J. L., T. W. Patapoff, B. Gillece-Castro, S. P. Colgan, C. A. Parkos, C. Delp, and R. J. Mrsny. 1993. 5′-Adenosine monophosphate is the neutrophil-derived paracrine factor that elicits chloride secretion from T84 intestinal epithelial cell monolayers. J. Clin. Investig. 91:2320-2325.
25. Maillot, C., G. Gargala, A. Delaunay, P. Ducrotte, P. Brasseur, J. J. Ballet, and L. Favennec. 2000. Cryptosporidium parvum infection stimulates the secretion of TGF-beta, IL-8 and RANTES by Caco-2 cell line. Parasitol. Res. 86:947-949.
26. Meisel, J. L., D. R. Perera, C. Meligro, and C. E. Rubin. 1976. Overwhelming watery diarrhea associated with a cryptosporidium in an immunosuppressed patient. Gastroenterology 70:1156-1160.
27. Molla, M., M. Gironella, A. Salas, D. Closa, A. Biete, M. Gimeno, P. Coronel, J. M. Pique, and J. Panes. 2005. Protective effect of superoxide dismutase in radiation-induced intestinal inflammation. Int. J. Radiat. Oncol. Biol. Phys. 61:1159-1166.
28. Nathan, C., and M. U. Shiloh. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97:8841-8848.
29. Nusrat, A., C. A. Parkos, T. W. Liang, D. K. Carnes, and J. L. Madara. 1997. Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology 113:1489-1500.
30. Oshitani, N., A. Kitano, H. Okabe, S. Nakamura, T. Matsumoto, and K. Kobayashi. 1993. Location of superoxide anion generation in human colonic mucosa obtained by biopsy. Gut 34:936-938.
31. Pavlick, K. P., F. S. Laroux, J. Fuseler, R. E. Wolf, L. Gray, J. Hoffman, and M. B. Grisham. 2002. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease. Free Radic. Biol. Med. 33:311-322.
32. Pratico, D., J. Rokach, J. Lawson, and G. A. FitzGerald. 2004. F2-isoprostanes as indices of lipid peroxidation in inflammatory diseases. Chem. Phys. Lipids 128:165-171.
33. Prophet, E. B., B. Mills, J. B. Arrington, and L. H. Sobin (ed.). 199. AFIP laboratory methods in histotechnology. American Registry of Pathology, Washington, D.C.
34. Ray, R., and A. M. Shah. 2005. NADPH oxidase and endothelial cell function. Clin. Sci. (London) 109:217-226.
35. 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. J. Infect. Chemother. 9:278-281.
36. Sears, C. L., and R. L. Guerrant. 1994. Cryptosporidiosis: the complexity of intestinal pathophysiology. Gastroenterology 106:252-254.
37. Segui, J., M. Gironella, M. Sans, S. Granell, F. Gil, M. Gimeno, P. Coronel, J. M. Pique, and J. Panes. 2004. Superoxide dismutase ameliorates TNBS-induced colitis by reducing oxidative stress, adhesion molecule expression, and leukocyte recruitment into the inflamed intestine. J. Leukoc. Biol. 76:537-544.
38. Seydel, K. B., T. Zhang, G. A. Champion, C. Fichtenbaum, P. E. Swanson, S. Tzipori, J. K. Griffiths, and S. L. Stanley, Jr. 1998. Cryptosporidium parvum infection of human intestinal xenografts in SCID mice induces production of human tumor necrosis factor alpha and interleukin-8. Infect. Immun. 66:2379-2382.
39. Stephens, J., M. Cosyns, M. Jones, and A. Hayward. 1999. Liver and bile duct pathology following Cryptosporidium parvum infection of immunodeficient mice. Hepatology 30:27-35.
40. Suzuki, M., W. Inauen, P. R. Kvietys, M. B. Grisham, C. Meininger, M. E. Schelling, H. J. Granger, and D. N. Granger. 1989. Superoxide mediates reperfusion-induced leukocyte-endothelial cell interactions. Am. J. Physiol. 257:H1740-H1745.
41. Waters, W. R., M. J. Wannemuehler, R. E. Sacco, M. V. Palmer, J. S. Haynes, B. A. Pesch, and J. A. Harp. 1999. Cryptosporidium parvum-induced inflammatory bowel disease of TCR-beta- × TCR-delta-deficient mice. J. Parasitol. 85:1100-1105.
42. Weiss, R. H., D. J. Fretland, D. A. Baron, U. S. Ryan, and D. P. Riley. 1996. Manganese-based superoxide dismutase mimetics inhibit neutrophil infiltration in vivo. J. Biol. Chem. 271:26149-26156.
43. Wright, S. D., P. E. Rao, W. C. Van Voorhis, L. S. Craigmyle, K. Iida, M. A. Talle, E. F. Westberg, G. Goldstein, and S. C. Silverstein. 1983. Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies. Proc. Natl. Acad. Sci. USA 80:5699-5703.
44. Yassien, N. A., E. A. Khalifa, and K. A. el-Nouby. 2001. Role of antioxidant preparation (oxi-guard) on Cryptosporidium parvum infection in albino mice. J. Egypt. Soc. Parasitol. 31:95-106.