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Entamoeba histolytica Cathepsin-Like Enzymes

Interactions with the Host Gut
  • Vanessa Kissoon-Singh
  • Leanne Mortimer
  • Kris Chadee
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 712)

Abstract

Cysteine proteases of the protozoan parasite Entamoeba histolytica are key virulence factors involved in overcoming host defences. These proteases are cathepsin-like enzymes with a cathepsin-L like structure, but cathepsin-B substrate specificity. In the host intestine, amoeba cysteine proteases cleave colonic mucins and degrade secretory immunoglobulin (Ig) A and IgG rendering them ineffective. They also act on epithelial tight junctions and degrade the extracellular matrix to promote Cell death. They are involved in the destruction of red blood cells and the evasion of neutrophils and macrophages and they activate pro-inflammatory cytokines IL- 1β and IL-18. In short, amoeba cysteine proteases manipulate and destroy host defences to facilitate nutrient acquisition, parasite colonization and/or invasion. Strategies to inhibit the activity of amoeba cysteine proteases could contribute significantly to host protection against E. histolytica.

Keywords

Tight Junction Cysteine Protease Mucus Layer Entamoeba Histolytica Chloromethyl Ketone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Turk B, Turk D, Turk V. Lysosomal cysteine proteases: more than scavengers. Biochim Biophys Acta 2000; 1477(1-2):98–111.PubMedGoogle Scholar
  2. 2.
    Berdowska I. Cysteine proteases as disease markers. Clin Chim Acta 2004; 342(1-2):41–69.PubMedGoogle Scholar
  3. 3.
    WHO. Amoebiasis. Weekly Epidemiological Record. Vol 72. Geneva; 1997:97–100.Google Scholar
  4. 4.
    Lejeune M, Rybicka JM, Chadee K. Recent discoveries in the pathogenesis and immune response toward Entamoeba histolytica. Future Microbiol 2009; 4:105–118.PubMedGoogle Scholar
  5. 5.
    Haque R, Huston CD, Hughes M et al. Amebiasis. N Engl J Med 2003; 348(16):1565–1573.PubMedGoogle Scholar
  6. 6.
    Haque R, Mondal D, Kirkpatrick BD et al. Epidemiologic and clinical characteristics of acute diarrhea with emphasis on Entamoeba histolytica infections in preschool children in an urban slum of Dhaka, Bangladesh. Am J Trop Med Hyg 2003; 69(4):398–405.PubMedGoogle Scholar
  7. 7.
    Lauwaet T, Oliveira MJ, Callewaert B et al. Proteinase inhibitors TPCK and TLCK prevent Entamoeba histolytica induced disturbance of tight junctions and microvilli in enteric Cell layers in vitro. Int J Parasitol 2004; 34(7):785–794.PubMedGoogle Scholar
  8. 8.
    Dey I, Chadee K. Prostaglandin E2 produced by Entamoeba histolytica binds to EP4 receptors and stimulates interleukin-8 production in human colonic cells. Infect Immun 2008; 76(11):5158–5163.PubMedGoogle Scholar
  9. 9.
    Perez-Tamayo R, Montfort I, Garcia AO et al. Pathogenesis of acute experimental liver amebiasis. Arch Med Res 2006; 37(2):203–209.PubMedGoogle Scholar
  10. 10.
    Stanley SL, Jr. The Entamoeba histolytica genome: something old, something new, something borrowed and sex too? Trends Parasitol 2005; 21(10):451–453.PubMedGoogle Scholar
  11. 11.
    Tannich E. Royal society of tropical medicine and hygiene meeting at manson house, London, 1998. Amoebic disease. Entamoeba histolytica and E. dispar: comparison of molecules considered important for host tissue destruction. Trans R Soc Trop Med Hyg 1998; 92(6):593–596.PubMedGoogle Scholar
  12. 12.
    Chadee K, Petri WA, Jr., Innes DJ et al. Rat and human colonic mucins bind to and inhibit adherence lectin of Entamoeba histolytica. J Clin Invest 1987; 80(5): 1245–1254.PubMedGoogle Scholar
  13. 13.
    Chadee K, Johnson ML, Orozco E et al. Binding and internalization of rat colonic mucins by the galactose/ N-acetyl-D-galactosamine adherence lectin of Entamoeba histolytica. J Infect Dis 1988; 158(2):398–406.PubMedGoogle Scholar
  14. 14.
    Gilchrist CA, Petri WA. Virulence factors of Entamoeba histolytica. Curr Opin Microbiol 1999; 2(4):433–437.PubMedGoogle Scholar
  15. 15.
    Petri WA Jr, Snodgrass TL, Jackson TF et al. Monoclonal antibodies directed against the galactose-binding lectin of Entamoeba histolytica enhance adherence. J Immunol 1990; 144(12):4803–4809.PubMedGoogle Scholar
  16. 16.
    Solaymani-Mohammadi S, Petri WA, Jr. Intestinal invasion by Entamoeba histolytica. Subcell Biochem 2008; 47:221–232.PubMedGoogle Scholar
  17. 17.
    Horstmann RD, Leippe M, Tannich E. Host tissue destruction by Entamoeba histolytica: molecules mediating adhesion, cytolysis and proteolysis. Mem Inst Oswaldo Cruz 1992; 87Suppl 5:57–60.PubMedGoogle Scholar
  18. 18.
    Andra J, Herbst R, Leippe M. Amoebapores, archaic effector peptides of protozoan origin, are discharged into phagosomes and kill bacteria by permeabilizing their membranes. Dev Comp Immunol 2003; 27(4):291–304.PubMedGoogle Scholar
  19. 19.
    Stanley SL, Jr. Amoebiasis. Lancet 2003; 361(9362):1025–1034.PubMedGoogle Scholar
  20. 20.
    Munoz ML, Calderon J, Rojkind M. The collagenase of Entamoeba histolytica. J Exp Med 1982; 155(1):42–51.PubMedGoogle Scholar
  21. 21.
    MacFarlane RC, Singh U. Identification of an Entamoeba histolytica serine-, threonine-and isoleucine-rich protein with roles in adhesion and cytotoxicity. Eukaryot Cell 2007; 6(11):2139–2146.PubMedGoogle Scholar
  22. 22.
    Teixeira JE, Huston CD. Participation of the serine-rich Entamoeba histolytica protein in amebic phagocytosis of apoptotic host cells. Infect Immun 2008; 76(3):959–966.PubMedGoogle Scholar
  23. 23.
    Mckerrow JH, Sun E, Rosenthal PJ et al. The proteases and pathogenicity of parasitic protozoa. Annu Rev Microbiol 1993; 47:821–853.PubMedGoogle Scholar
  24. 24.
    Ankri S, Stolarsky T, Bracha R et al. Antisense inhibition of expression of cysteine proteinases affects Entamoeba histolytica-induced formation of liver abscess in hamsters. Infect Immun 1999; 67(1):421–422.PubMedGoogle Scholar
  25. 25.
    Que X, Brinen LS, Perkins P et al. Cysteine proteinases from distinct cellular compartments are recruited to phagocytic vesicles by Entamoeba histolytica. Mol Biochem Parasitol 2002; 119(1):23–32.PubMedGoogle Scholar
  26. 26.
    Reed SL, Keene WE, McKerrow JH. Thiol proteinase expression and pathogenicity of Entamoeba histolytica. J Clin Microbiol 1989; 27(12):2772–2777.PubMedGoogle Scholar
  27. 27.
    Stanley SL Jr, Zhang T, Rubin D et al. Role of the Entamoeba histolytica cysteine proteinase in amebic liver abscess formation in severe combined immunodeficient mice. Infect Immun 1995; 63(4): 1587–1590.PubMedGoogle Scholar
  28. 28.
    Li E, Yang WG, Zhang T et al. Interaction of laminin with Entamoeba histolytica cysteine proteinases and its effect on amebic pathogenesis. Infect Immun 1995; 63(10):4150–4153.PubMedGoogle Scholar
  29. 29.
    Tran VQ, Herdman DS, Torian BE et al. The neutral cysteine proteinase of Entamoeba histolytica degrades IgG and prevents its binding. J Infect Dis 1998; 177(2):508–511.PubMedGoogle Scholar
  30. 30.
    Reed SL, Gigli I. Lysis of complement-sensitive Entamoeba histolytica by activated terminal complement components. Initiation of complement activation by an extracellular neutral cysteine proteinase. J Clin Invest 1990; 86(6):1815–1822.PubMedGoogle Scholar
  31. 31.
    Reed SL, Keene WE, McKerrow JH et al. Cleavage of C3 by a neutral cysteine proteinase of Entamoeba histolytica. J Immunol 1989; 143(1): 189–195.PubMedGoogle Scholar
  32. 32.
    Lidell ME, Moncada DM, Chadee K et al. Entamoeba histolytica cysteine proteases cleave the MUC2 mucin in its C-terminal domain and dissolve the protective colonic mucus gel. Proc Natl acad Sci USA 2006; 103(24):9298–9303.PubMedGoogle Scholar
  33. 33.
    Keene WE, Hidalgo ME, Orozco E et al. Entamoeba histolytica: correlation of the cytopathic effect of virulent trophozoites with secretion of a cysteine proteinase. Exp Parasitol 1990; 71(2):199–206.PubMedGoogle Scholar
  34. 34.
    Bruchhaus I, Loftus BJ, Hall N et al. The intestinal protozoan parasite Entamoeba histolytica contains 20 cysteine protease genes, of which only a small subset is expressed during in vitro cultivation. Eukaryot Cell 2003; 2(3):501–509.PubMedGoogle Scholar
  35. 35.
    Brinen LS, Que X, Mckerrow JH et al. Homology modeling of Entamoeba histolytica cysteine proteinases reveals the basis for cathepsin L-like structure with cathepsin B-like specificity. Arch Med Res 2000; 31(4 Suppl):S63–S64.PubMedGoogle Scholar
  36. 36.
    karrer KM, Peiffer SL, DiTomas ME. Two distinct gene subfamilies within the family of cysteine protease genes. Proc Natl Acad Sci USA 1993; 90(7):3063–3067.PubMedGoogle Scholar
  37. 37.
    Que X, Reed SL. Cysteine proteinases and the pathogenesis of amebiasis. Clin Microbiol Rev 2000; 13(2):196–206.PubMedGoogle Scholar
  38. 38.
    Lauwaet T, Oliveira MJ, Callewaert B et al. Proteolysis of enteric Cell villin by Entamoeba histolytica cysteine proteinases. J Biol Chem 2003; 278(25):22650–22656.PubMedGoogle Scholar
  39. 39.
    Riekenberg S, Witjes B, Saric M et al. Identification of EhICP1, a chagasin-like cysteine protease inhibitor of Entamoeba histolytica. FEBS Lett 2005; 579(7):1573–1578.PubMedGoogle Scholar
  40. 40.
    Saric M, Vahrmann A, Bruchhaus I et al. The second cysteine protease inhibitor, EhIcP2, has a different localization in trophozoites of Entamoeba histolytica than EhICP1. Parasitol Res 2006; 100(1):171–174.PubMedGoogle Scholar
  41. 41.
    Bansal D, Ave P, Kerneis S et al. An ex-vivo human intestinal model to study Entamoeba histolytica pathogenesis. PloS Negl Trop Dis 2009; 3(11):e551.PubMedGoogle Scholar
  42. 42.
    Loftus B, Anderson I, Davies R et al. The genome of the protist parasite Entamoeba histolytica. Nature 2005; 433(7028):865–868.PubMedGoogle Scholar
  43. 43.
    MacFarlane RC, Shah PH, Singh U. Transcriptional profiling of Entamoeba histolytica trophozoites. Int J Parasitol 2005; 35(5):533–542.PubMedGoogle Scholar
  44. 44.
    Das S, Gillin FD. Chitin synthase in encysting Entamoeba invadens. Biochem J 1991; 280 (Pt 3):641–647.PubMedGoogle Scholar
  45. 45.
    Ebert F, Bachmann A, Nakada-Tsukui K et al. An Entamoeba cysteine peptidase specifically expressed during encystation. Parasitol Int 2008; 57(4):521–524.PubMedGoogle Scholar
  46. 46.
    Makioka A, Kumagai M, Kobayashi S et al. Entamoeba invadens: cysteine protease inhibitors block excystation and metacystic development. Exp Parasitol 2005; 109(1):27–32.PubMedGoogle Scholar
  47. 47.
    Sharma M, Hirata K, Herdman S et al. Entamoeba invadens: characterization of cysteine proteinases. Exp Parasitol 1996; 84(1):84–91.PubMedGoogle Scholar
  48. 48.
    Bruchhaus I, Jacobs T, Leippe M et al. Entamoeba histolytica and Entamoeba dispar: differences in numbers and expression of cysteine proteinase genes. Mol Microbiol 1996; 22(2):255–263.PubMedGoogle Scholar
  49. 49.
    Garcia-Rivera G, Rodriguez MA, Ocadiz R et al. Entamoeba histolytica: a novel cysteine protease and an adhesin form the 112 kDa surface protein. Mol Microbiol 1999; 33(3):556–568.PubMedGoogle Scholar
  50. 50.
    Jacobs T, Bruchhaus I, Dandekar T et al. Isolation and molecular characterization of a surface-bound proteinase of Entamoeba histolytica. Mol Microbiol 1998; 27(2):269–276.PubMedGoogle Scholar
  51. 51.
    de Meester F, Shaw E, Scholze H et al. Specific labeling of cysteine proteinases in pathogenic and nonpathogenic Entamoeba histolytica. Infect Immun 1990; 58(5): 1396–1401.PubMedGoogle Scholar
  52. 52.
    Freitas MA, Fernandes HC, Calixto VC et al. Entamoeba histolytica: cysteine proteinase activity and virulence. focus on cysteine proteinase 5 expression levels. Exp Parasitol 2009; 122(4):306–309.PubMedGoogle Scholar
  53. 53.
    Reed S, Bouvier J, Pollack AS et al. Cloning of a virulence factor of Entamoeba histolytica. Pathogenic strains possess a unique cysteine proteinase gene. J Clin Invest 1993; 91(4):1532–1540.PubMedGoogle Scholar
  54. 54.
    Gadasi H, Kessler E. Correlation of virulence and collagenolytic activity in Entamoeba histolytica. Infect Immun 1983; 39(2):528–531.PubMedGoogle Scholar
  55. 55.
    Gadasi H, Kobiler D. Entamoeba histolytica: correlation between virulence and content of proteolytic enzymes. Exp Parasitol 1983; 55(1):105–110.PubMedGoogle Scholar
  56. 56.
    Zhang Z, Wang L, Seydel KB et al. Entamoeba histolytica cysteine proteinases with interleukin-1 beta converting enzyme (ICE) activity cause intestinal inflammation and tissue damage in amoebiasis. Mol Microbiol 2000; 37(3):542–548.PubMedGoogle Scholar
  57. 57.
    Moncada D, Keller K, Chadee K. Entamoeba histolytica cysteine proteinases disrupt the polymeric structure of colonic mucin and alter its protective function. Infect Immun 2003; 71(2):838–844.PubMedGoogle Scholar
  58. 58.
    Moncada DM, Chadee, K. Production, Structure and function of gastrointestinal mucins. In: Blaser MJ, Smith, P.J., Ravdin, I.J., Greenberg, H.R. and Guerrant, R.L., ed. Infections of the Gastroinestinal Tract Philadelphia: Williams and Wilkins; 2002:57–79.Google Scholar
  59. 59.
    Dharmani P, Srivastv A, V, Kissoon-Singh et al. Role of intestinal mucins in innate host defense mehanisms against Pathogens. Journal of Innate Immunity 2009; 1:123–135.PubMedGoogle Scholar
  60. 60.
    Moncada DM. Production, Structure and function of gastrointestinal mucins. Montreal, McGill University; 2006.Google Scholar
  61. 61.
    Tse SK, Chadee K. The interaction between intestinal mucus glycoproteins and enteric infections. Parasitol Today 1991; 7(7):163–172.PubMedGoogle Scholar
  62. 62.
    Bevins CL, Martin-Porter E, Ganz T. Defensins and innate host defence of the gastrointestinal tract. Gut 1999; 45(6):911–915.PubMedGoogle Scholar
  63. 63.
    Zanetti M. Cathelicidins, multifunctional peptides of the innate immunity. J Leukoc Biol 2004; 75(1):39–48.PubMedGoogle Scholar
  64. 64.
    Bergstrom KS, Guttman JA, Rumi M et al. Modulation of intestinal goblet Cell function during infection by an attaching and effacing bacterial pathogen. Infect Immun 2008; 76(2):796–811.PubMedGoogle Scholar
  65. 65.
    Johansson ME, Thomsson KA, Hansson GC. Proteomic analyses of the two mucus layers of the colon barrier reveal that their main component, the Muc2 mucin, is strongly bound to the Fcgbp protein. J Proteome Res 2009; 8(7):3549–3557.PubMedGoogle Scholar
  66. 66.
    Belley A, Keller K, Grove J et al. Interaction of LS174T human colon cancer Cell mucins with Entamoeba histolytica: an in vitro model for colonic disease. Gastroenterology 1996; 111(6): 1484–1492.PubMedGoogle Scholar
  67. 67.
    Chadee K, Meerovitch E. Entamoeba histolytica: early progressive pathology in the cecum of the gerbil (Meriones unguiculatus). Am J Trop Med Hyg 1985; 34(2):283–291.PubMedGoogle Scholar
  68. 68.
    Tse SK, Chadee K. Biochemical characterization of rat colonic mucins secreted in response to Entamoeba histolytica. Infect Immun 1992; 60(4):1603–1612.PubMedGoogle Scholar
  69. 69.
    Moncada D, Yu Y, Keller K et al. Entamoeba histolytica cysteine proteinases degrade human colonic mucin and alter its function. Arch Med Res 2000; 31(4 Suppl):S224–S225.PubMedGoogle Scholar
  70. 70.
    Moncada D, Keller K, Ankri S et al. Antisense inhibition of Entamoeba histolytica cysteine proteases inhibits colonic mucus degradation. Gastroenterology 2006; 130(3):721–730.PubMedGoogle Scholar
  71. 71.
    ATTC. American Type Culture Colletion.Google Scholar
  72. 72.
    Garcia-Nieto RM, Rico-Mata R, Arias-Negrete S et al. Degradation of human secretory Iga1 and Iga2 by Entamoeba histolytica surface-associated proteolytic activity. Parasitol Int 2008; 57(4):417–423.PubMedGoogle Scholar
  73. 73.
    Woof JM, Kerr MA. The function of immunoglobulin a in immunity. J Pathol 2006; 208(2):270–282.PubMedGoogle Scholar
  74. 74.
    Kilian M, Mestecky J, Russell MW. Defense mechanisms involving Fc-dependent functions of immunoglobulin A and their subversion by bacterial immunoglobulin a proteases. Microbiol Rev 1988; 52(2):296–303.PubMedGoogle Scholar
  75. 75.
    Haque R, Ali IM, Sack RB et al. Amebiasis and mucosal Iga antibody against the Entamoeba histolytica adherence lectin in Bangladeshi children. J Infect Dis 2001; 183(12): 1787–1793.PubMedGoogle Scholar
  76. 76.
    Carrero JC, Diaz MY, Viveros M et al. Human secretory immunoglobulin A anti-Entamoeba histolytica antibodies inhibit adherence of amebae to MDCK cells. Infect Immun 1994; 62(2):764–767.PubMedGoogle Scholar
  77. 77.
    Guerrero-Manriquez GG, Sanchez-Ibarra F, Avila EE. Inhibition of Entamoeba histolytica proteolytic activity by human salivary Iga antibodies. Apmis 1998; 106(11):1088–1094.PubMedGoogle Scholar
  78. 78.
    Leon-Sicairos N, Lopez-Soto F, Reyes-Lopez M et al. Amoebicidal activity of milk, apo-lactoferrin, sIgA and lysozyme. Clin Med Res 2006; 4(2): 106–113.PubMedGoogle Scholar
  79. 79.
    Kelsall BL, Ravdin JI. Degradation of human IgA by Entamoeba histolytica. J Infect Dis 1993; 168(5): 1319–1322.PubMedGoogle Scholar
  80. 80.
    Yoshida M, Claypool SM, Wagner JS et al. Human neonatal FC receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 2004; 20(6):769–783.PubMedGoogle Scholar
  81. 81.
    Murphy K, Travers P, Walport M. Janeway’s Immunobiology. 7th ed. New York, New York: Garland Science, Taylor and Francis Group; 2008.Google Scholar
  82. 82.
    Jackson TF, Gathiram V, Simjee AE. Seroepidemiological study of antibody responses to the zymodemes of Entamoeba histolytica. Lancet 1985; 1(8431):716–719.PubMedGoogle Scholar
  83. 83.
    Bontempi E, Cazzulo JJ. Digestion of human immunoglobulin G by the major cysteine proteinase (cruzipain) from Trypanosoma cruzi. FEMS Microbiol Lett 1990; 58(3):337–341.PubMedGoogle Scholar
  84. 84.
    Al-Sadi R, Boivin M, Ma T. Mechanism of cytokine modulation of epithelial tight junction barrier. Front Biosci 2009; 14:2765–2778.PubMedGoogle Scholar
  85. 85.
    Laukoetter MG, Bruewer M, Nusrat A. Regulation of the intestinal epithelial barrier by the apical junctional complex. Curr Opin Gastroenterol 2006; 22(2):85–89.PubMedGoogle Scholar
  86. 86.
    Muller CA, Autenrieth IB, Peschel A. Innate defenses of the intestinal epithelial barrier. Cell Mol life Sci 2005;62(12):1297–1307.PubMedGoogle Scholar
  87. 87.
    Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 2008; 8(6):411–420.PubMedGoogle Scholar
  88. 88.
    Sansonetti PJ. War and peace at mucosal surfaces. Nat Rev Immunol 2004; 4(12):953–964.PubMedGoogle Scholar
  89. 89.
    Goke M, Podolsky DK. Regulation of the mucosal epithelial barrier. Baillieres Clin Gastroenterol 1996; 10(3):393–405.PubMedGoogle Scholar
  90. 90.
    Ravdin JI, Guerrant RL. Role of adherence in cytopathogenic mechanisms of Entamoeba histolytica. Study with mammalian tissue culture cells and human erythrocytes. J Clin Invest 1981; 68(5): 1305–1313.PubMedGoogle Scholar
  91. 91.
    Petri WA Jr, Smith RD, Schlesinger PH et al. Isolation of the galactose-binding lectin that mediates the in vitro adherence of Entamoeba histolytica. J Clin Invest 1987; 80(5):1238–1244.PubMedGoogle Scholar
  92. 92.
    Schulte W, Scholze H. Action of the major protease from Entamoeba histolytica on proteins of the extracellular matrix. J Protozool 1989; 36(6):538–543.PubMedGoogle Scholar
  93. 93.
    Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994; 124(4):619–626.PubMedGoogle Scholar
  94. 94.
    Taupin DR, Kinoshita K, Podolsky DK. Intestinal trefoil factor confers colonic epithelial resistance to apoptosis. Proc Natl Acad Sci USA 2000; 97(2):799–804.PubMedGoogle Scholar
  95. 95.
    Keene WE, Petitt MG, Allen S et al. The major neutral proteinase of Entamoeba histolytica. J Exp Med 1986; 163(3):536–549.PubMedGoogle Scholar
  96. 96.
    Hellberg A, Nickel R, Lotter H et al. Overexpression of cysteine proteinase 2 in Entamoeba histolytica or Entamoeba dispar increases amoeba-induced monolayer destruction in vitro but does not augment amoebic liver abscess formation in gerbils. Cell Microbiol 2001; 3(1):13–20.PubMedGoogle Scholar
  97. 97.
    Carpeniseanu S, Hirata K, Que X et al. L6: a proteinase-and phagocytosis-deficient mutant of Entamoeba histolytica. Arch Med Res 2000; 31(4 Suppl):S237–S238.PubMedGoogle Scholar
  98. 98.
    Hou Y, Kissoon-Singh V, Fodor I et al. Entamoeba histolytica CP5 targets integrin to induce NF-kB proinflammatory signaling. In press. 2009.Google Scholar
  99. 99.
    Fasano A, Baudry B, Pumplin DW et al. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc Natl acad Sci USA 1991; 88(12):5242–5246.PubMedGoogle Scholar
  100. 100.
    Leroy A, Lauwaet T, De Bruyne G et al. Entamoeba histolytica disturbs the tight junction complex in human enteric T84 cell layers. Faseb J 2000; 14(9):1139–1146.PubMedGoogle Scholar
  101. 101.
    Ankri S, Stolarsky T, Mirelman D. Antisense inhibition of expression of cysteine proteinases does not affect Entamoeba histolytica cytopathic or haemolytic activity but inhibits phagocytosis. Mol Microbiol 1998;28(4):777–785.PubMedGoogle Scholar
  102. 102.
    Irmer H, Tillack M, Biller L et al. Major cysteine peptidases of Entamoeba histolytica are required for aggregation and digestion of erythrocytes but are dispensable for phagocytosis and cytopathogenicity. Mol Microbiol 2009; 72(3):658–667.PubMedGoogle Scholar
  103. 103.
    Serrano-Luna JJ, Negrete E, Reyes M et al. Entamoeba histolytica HM1:IMSS: hemoglobin-degrading neutral cysteine proteases. Exp Parasitol 1998; 89(1):71–77.PubMedGoogle Scholar
  104. 104.
    Seydel KB, Zhang T, Stanley SL, Jr. Neutrophils play a critical role in early resistance to amebic liver abscesses in severe combined immunodeficient mice. Infect Immun 1997; 65(9):3951–3953.PubMedGoogle Scholar
  105. 105.
    Asgharpour A, Gilchrist C, Baba D et al. Resistance to intestinal Entamoeba histolytica infection is conferred by innate immunity and Gr-1+ cells. Infect Immun 2005; 73(8):4522–4529.PubMedGoogle Scholar
  106. 106.
    Seydel KB, Li E, Zhang Z et al. Epithelial cell-initiated inflammation plays a crucial role in early tissue damage in amebic infection of human intestine. Gastroenterology 1998; 115(6):1446–1453.PubMedGoogle Scholar
  107. 107.
    Chadee K, Moreau F, Meerovitch E. Entamoeba histolytica: chemoattractant activity for gerbil neutrophils in vivo and in vitro. Exp Parasitol 1987; 64(1):12–23.PubMedGoogle Scholar
  108. 108.
    Denis M, Chadee K. Human neutrophils activated by interferon-gamma and tumour necrosis factor-alpha kill Entamoeba histolytica trophozoites in vitro. J Leukoc Biol 1989; 46(3):270–274.PubMedGoogle Scholar
  109. 109.
    Lin JY, Keller K, Chadee K. Entamoeba histolytica proteins modulate the respiratory burst potential by murine macrophages. Immunology 1993; 78(2):291–297.PubMedGoogle Scholar
  110. 110.
    Seguin R, Mann BJ, Keller K et al. The tumor necrosis factor alpha-stimulating region of galactose-inhibitable lectin of Entamoeba histolytica activates gamma interferon-primed macrophages for amebicidal activity mediated by nitric oxide. Infect Immun 1997; 65(7):2522–2527.PubMedGoogle Scholar
  111. 111.
    Que X, Kim SH, Sajid M et al. A surface amebic cysteine proteinase inactivates interleukin-18. Infect Immun 2003; 71(3):1274–1280.PubMedGoogle Scholar
  112. 112.
    Stanley SL Jr, Reed SL. Microbes and microbial toxins: paradigms for microbial-mucosal interactions. VI. Entamoeba histolytica: parasite-host interactions. Am J Physiol Gastrointest Liver Physiol 2001; 280(6):G1049–G1054.PubMedGoogle Scholar
  113. 113.
    Eckmann L, Reed SL, Smith JR et al. Entamoeba histolytica trophozoites induce an inflammatory cytokine response by cultured human cells through the paracrine action of cytolytically released interleukin-1 alpha. J Clin Invest 1995; 96(3):1269–1279.PubMedGoogle Scholar
  114. 114.
    Huston CD. Parasite and host contributions to the pathogenesis of amebic colitis. Trends Parasitol 2004; 20(1):23–26.PubMedGoogle Scholar
  115. 115.
    Biet F, Locht C, Kremer L. Immunoregulatory functions of interleukin 18 and its role in defense against bacterial pathogens. J Mol Med 2002; 80(3):147–162.PubMedGoogle Scholar
  116. 116.
    Lundwall A, Eggertsen G. Isolation of human complement factors C3, C5 and H. J Immunol Methods 1985;81(1):147–160.PubMedGoogle Scholar
  117. 117.
    Ventura-Juarez J, Campos-Rodriguez R, Jarillo-Luna RA et al. Trophozoites of Entamoeba histolytica express a CD59-like molecule in human colon. Parasitol Res 2009; 104(4):821–826.PubMedGoogle Scholar
  118. 118.
    Kindt TJ, Goldsby RA, Osborne BA. Immunology. 6th ed. New York: W.H. Freeman and Company; 2007.Google Scholar
  119. 119.
    Reed SL, Ember JA, Herdman DS et al. The extracellular neutral cysteine proteinase of Entamoeba histolytica degrades anaphylatoxins C3a and C5a. J Immunol 1995; 155(1):266–274.PubMedGoogle Scholar
  120. 120.
    Reed SL, Curd JG, Gigli I et al. Activation of complement by pathogenic and nonpathogenic Entamoeba histolytica. J Immunol 1986; 136(6):2265–2270.PubMedGoogle Scholar
  121. 121.
    Campbell D, Chadee K. Survival strategies of Entamoeba histolytica: Modulation of cell-mediated immune responses. Parasitol Today 1997; 13(5): 184–190.PubMedGoogle Scholar
  122. 122.
    Ocadiz R, Orozco E, Carrillo E et al. EhCP112 is an Entamoeba histolytica secreted cysteine protease that may be involved in the parasite-virulence. Cell Microbiol 2005; 7(2):221–232.PubMedGoogle Scholar
  123. 123.
    Martinez MB, Rodriguez MA, Garcia-Rivera G et al. A pcDNA-Ehcpadh vaccine against Entamoeba histolytica elicits a protective th1-like response in hamster liver. Vaccine 2009; 27(31):4176–4186.PubMedGoogle Scholar
  124. 124.
    Moncada DM. E. histolytica cysteine proteinases. Montreal, McGill University; 2006.Google Scholar
  125. 125.
    Bruchhaus I, Tannich E. A gene highly homologous to ACP1 encoding cysteine proteinase 3 in Entamoeba histolytica is present and expressed in E. dispar. Parasitol Res 1996; 82(2): 189–192.PubMedGoogle Scholar
  126. 126.
    Tillack M, Nowak N, Lotter H et al. 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 2006; 149(1):58–64.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Vanessa Kissoon-Singh
    • 1
  • Leanne Mortimer
    • 1
  • Kris Chadee
    • 1
  1. 1.Gastrointestinal Research GroupUniversity of CalgaryCalgaryCanada

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