Entamoeba histolytica infection and secreted proteins proteolytically damage enteric neurons

Infection and Immunity

Volumn 78, Issue 12, 2010, Pages 5332-5340

  Lourenssen, Sandra ^a   Houpt, Eric R ^b   Chadee, Kris ^c   Blennerhassett, Michael G ^a,d  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

^d KINGSTON GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; PROTOZOAL PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

AMEBIASIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CECUM; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; ENTAMOEBA HISTOLYTICA; GLIA; IN VITRO STUDY; MALE; MOUSE; NERVE CELL; NERVE CELL LESION; NERVE FIBER; NERVE FIBER DEGENERATION; NEUROTOXICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; WILD TYPE;

ANIMALS; AXONS; CECUM; CELL COUNT; CELLS, CULTURED; DYSENTERY, AMEBIC; ENTAMOEBA HISTOLYTICA; MALE; MICE; MICE, INBRED CBA; MUSCLE, SMOOTH; NEURONS; RATS;

EID: 78649948639     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00699-10     Document Type: Article

References (41)

1. Abrahan, C. E., M. F. Insua, L. E. Politi, O. L. German, and N. P. Rotstein. 2009. Oxidative stress promotes proliferation and dedifferentiation of retina glial cells in vitro. J. Neurosci. Res. 87:964-977.
2. Berninghausen, O., and M. Leippe. 1997. Necrosis versus apoptosis as the mechanism of target cell death induced by Entamoeba histolytica. Infect. Immun. 65:3615-3621.
3. Blennerhassett, M. G., and S. Lourenssen. 2000. Neural regulation of intestinal smooth muscle growth in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 279:G511-G519.
4. Blennerhassett, M. G., P. Vignjevic, D. L. Vermillion, and S. M. Collins. 1992. Inflammation causes hyperplasia and hypertrophy in smooth muscle of rat small intestine. Am. J. Physiol. 262:G1041-G1046.
5. Bracha, R., Y. Nuchamowitz, M. Anbar, and D. Mirelman. 2006. Transcriptional silencing of multiple genes in trophozoites of Entamoeba histolytica. PLoS Pathog. 2:e48.
6. Bradley, J. S., Jr., E. J. Parr, and K. A. Sharkey. 1997. Effects of inflammation on cell proliferation in the myenteric plexus of the guinea pig ileum. Cell Tissue Res. 289:455-461.
7. Bruchhaus, I., T. Jacobs, M. Leippe, and E. Tannich. 1996. Entamoeba histolytica and Entamoeba dispar: differences in numbers and expression of cysteine proteinase genes. Mol. Microbiol. 22:255-263.
8. Chadee, K., and E. Meerovitch. 1984. The Mongolian gerbil (Meriones unguiculatus) as an experimental host for Entamoeba histolytica. Am. J. Trop. Med. Hyg. 33:47-54.
9. Chadee, K., and E. Meerovitch. 1984. The pathogenesis of experimentally induced amebic liver abscess in the gerbil (Meriones unguiculatus). Am. J. Pathol. 117:71-80.
10. Das, A., M. K. Guyton, J. T. Butler, S. K. Ray, and N. L. Banik. 2008. Activation of calpain and caspase pathways in demyelination and neurodegeneration in animal model of multiple sclerosis. CNS Neurol. Disord. Drug Targets 7:313-320.
11. Dey, I., and K. Chadee. 2008. Prostaglandin E2 produced by Entamoeba histolytica binds to EP4 receptors and stimulates interleukin-8 production in human colonic cells. Infect. Immun. 76:5158-5163.
12. Ferrante, M., G. de Hertog, T. Hlavaty, G. D'Haens, F. Penninckx, A. D'Hoore, S. Vermeire, P. Rutgeerts, K. Geboes, and G. van Assche. 2006. The value of myenteric plexitis to predict early postoperative Crohn's disease recurrence. Gastroenterology 130:1595-1606. (Pubitemid 43668839)
13. Freitas, M. A., H. C. Fernandes, V. C. Calixto, A. S. Martins, E. F. Silva, J. L. Pesquero, and M. A. Gomes. 2009. Entamoeba histolytica: cysteine proteinase activity and virulence: focus on cysteine proteinase 5 expression levels. Exp. Parasitol. 122:306-309.
14. Gougeon, P. Y., S. Lourenssen, A. Li, and M. G. Blennerhassett. 2010. TNF and IL-1 potentiate axonal growth of myenteric neurons via indirect action on smooth muscle cells. Can. J. Gastroenterol. 24(Suppl. A):A137.
15. Guyton, M. K., E. A. Sribnick, S. K. Ray, and N. L. Banik. 2005. A role for calpain in optic neuritis. Ann. N. Y. Acad. Sci. 1053:48-54.
16. Hamano, S., A. Asgharpour, S. E. Stroup, T. A. Wynn, E. H. Leiter, and E. Houpt. 2006. Resistance of C57BL/6 mice to amoebiasis is mediated by nonhemopoietic cells but requires hemopoietic IL-10 production. J. Immunol. 177:1208-1213. (Pubitemid 44036625)
17. He, C., G. P. Nora, E. L. Schneider, I. D. Kerr, E. Hansell, K. Hirata, D. Gonzalez, M. Sajid, S. E. Boyd, P. Hruz, E. R. Cobo, C. Le, W. T. Liu, L. Eckmann, P. C. Dorrestein, E. R. Houpt, L. S. Brinen, C. S. Craik, W. R. Roush, J. McKerrow, and S. L. Reed. 2010. A novel Entamoeba histolytica cysteine proteinase, EhCP4, is key for invasive amebiasis and a therapeutic target. J. Biol. Chem. 285:18516-18527.
18. + T cells. J. Immunol. 169:4496-4503.
19. Huston, C. D., E. R. Houpt, B. J. Mann, C. S. Hahn, and W. A. Petri, Jr. 2000. Caspase 3-dependent killing of host cells by the parasite Entamoeba histolytica. Cell Microbiol. 2:617-625.
20. Lejeune, M., J. M. Rybicka, and K. Chadee. 2009. Recent discoveries in the pathogenesis and immune response toward Entamoeba histolytica. Future Microbiol. 4:105-118.
21. Lin, A., S. Lourenssen, R. D. Stanzel, and M. G. Blennerhassett. 2005. Selective loss of NGF-sensitive neurons following experimental colitis. Exp. Neurol. 191:337-343.
22. Linden, D. R., J. M. Couvrette, A. Ciolino, C. McQuoid, H. Blaszyk, K. A. Sharkey, and G. M. Mawe. 2005. Indiscriminate loss of myenteric neurons in the TNBS-inflamed guinea-pig distal colon. Neurogastroenterol. Motil. 17: 751-760.
23. Lourenssen, S., K. G. Miller, and M. G. Blennerhassett. 2009. Discrete responses of myenteric neurons to structural and functional damage by neurotoxins in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 297:G228-G239.
24. Lourenssen, S., R. W. Wells, and M. G. Blennerhassett. 2005. Differential responses of intrinsic and extrinsic innervation of smooth muscle cells in rat colitis. Exp. Neurol. 195:497-507.
25. Martorell, L., J. Martinez-Gonzalez, C. Rodriguez, M. Gentile, O. Calvayrac, and L. Badimon. 2008. Thrombin and protease-activated receptors (PARs) in atherothrombosis. Thromb. Haemost. 99:305-315.
26. Melendez-Lopez, S. G., S. Herdman, K. Hirata, M. H. Choi, Y. Choe, C. Craik, C. R. Caffrey, E. Hansell, B. Chavez-Munguia, Y. T. Chen, W. R. Roush, J. McKerrow, L. Eckmann, J. Guo, S. L. Stanley, Jr., and S. L. Reed. 2007. Use of recombinant Entamoeba histolytica cysteine proteinase 1 to identify a potent inhibitor of amebic invasion in a human colonic model. Eukaryot. Cell 6:1130-1136.
27. Moncada, D., K. Keller, S. Ankri, D. Mirelman, and K. Chadee. 2006. Antisense inhibition of Entamoeba histolytica cysteine proteases inhibits colonic mucus degradation. Gastroenterology 130:721-730.
28. Moncada, D., K. Keller, and K. Chadee. 2003. Entamoeba histolytica cysteine proteinases disrupt the polymeric structure of colonic mucin and alter its protective function. Infect. Immun. 71:838-844.
29. Neunlist, M., D. Reiche, K. Michel, H. Pfannkuche, S. Hoppe, and M. Schemann. 1999. The enteric nervous system: region and target specific projections and neurochemical codes. Eur. J. Morphol. 37:233-240.
30. Pritt, B. S., and C. G. Clark. 2008. Amebiasis. Mayo Clin. Proc. 83:1154-1159.
31. Que, X., and S. L. Reed. 2000. Cysteine proteinases and the pathogenesis of amebiasis. Clin. Microbiol. Rev. 13:196-206.
32. Ragland, B. D., L. S. Ashley, D. L. Vaux, and W. A. Petri, Jr. 1994. Entamoeba histolytica: target cells killed by trophozoites undergo DNA fragmentation which is not blocked by Bcl-2. Exp. Parasitol. 79:460-467.
33. Reed, S. L., W. E. Keene, and J. H. McKerrow. 1989. Thiol proteinase expression and pathogenicity of Entamoeba histolytica. J. Clin. Microbiol. 27:2772-2777.
34. Sanovic, S., D. P. Lamb, and M. G. Blennerhassett. 1999. Damage to the enteric nervous system in experimental colitis. Am. J. Pathol. 155:1051-1057.
35. Schemann, M., and C. Schaaf. 1995. Differential projection of cholinergic and nitroxidergic neurons in the myenteric plexus of guinea pig stomach. Am. J. Physiol. 269:G186-G195.
36. Tillack, M., L. Biller, H. Irmer, M. Freitas, M. A. Gomes, E. Tannich, and I. Bruchhaus. 2007. The Entamoeba histolytica genome: primary structure and expression of proteolytic enzymes. BMC Genomics 8:170.
37. Tillack, M., N. Nowak, H. Lotter, R. Bracha, D. Mirelman, E. Tannich, and I. Bruchhaus. 2006. Increased expression of the major cysteine proteinases by stable episomal transfection underlines the important role of EhCP5 for the pathogenicity of Entamoeba histolytica. Mol. Biochem. Parasitol. 149:58-64.
38. Vosler, P. S., C. S. Brennan, and J. Chen. 2008. Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration. Mol. Neurobiol. 38:78-100.
39. Walsh, J. A. 1986. Problems in recognition and diagnosis of amebiasis: estimation of the global magnitude of morbidity and mortality. Rev. Infect. Dis. 8:228-238.
40. Waters, E. M., and R. B. Simerly. 2009. Estrogen induces caspase-dependent cell death during hypothalamic development. J. Neurosci. 29:9714-9718.
41. Yu, Y., and K. Chadee. 1997. Entamoeba histolytica stimulates interleukin 8 from human colonic epithelial cells without parasite-enterocyte contact. Gastroenterology 112:1536-1547.