Advertisement

Amebiasis pp 447-458 | Cite as

Cysteine Peptidases in Pathogenesis

  • Iris Bruchhaus
  • Jenny Matthiesen
Chapter

Abstract

Entamoeba histolytica is characterized by its extraordinary capacity to invade and destroy human tissues. The main lytic activity has been attributed to cysteine peptidases, and a number of studies have shown that cysteine peptidases constitute major pathogenicity factors in E. histolytica. Interestingly, although most of the classes of peptidases are present in E. histolytica, only cysteine peptidases, and on a lesser scale, metallo-peptidases and serine peptidases, have been adequately studied. In this chapter, the peptidase families of E. histolytica are introduced, and their involvement in colonic invasion and in liver abscess formation are discussed.

Keywords

Cysteine Peptidase Aspartic Peptidase Liver Sinusoidal Endothelial Cell Amoebic Liver Abscess Amebic Liver Abscess 
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.

References

  1. 1.
    Ankri S, Stolarsky T, Bracha R, Padilla-Vaca F, Mirelman D (1999) Antisense inhibition of expression of cysteine proteinases affects Entamoeba histolytica-induced formation of liver abscess in hamsters. Infect Immun 67:421–422PubMedCentralPubMedGoogle Scholar
  2. 2.
    Gadasi H, Kessler E (1983) Correlation of virulence and collagenolytic activity in Entamoeba histolytica. Infect Immun 39:528–531PubMedCentralPubMedGoogle Scholar
  3. 3.
    Keene WE, Hidalgo ME, Orozco E, McKerrow JH (1990) Entamoeba histolytica: correlation of the cytopathic effect of virulent trophozoites with secretion of a cysteine proteinase. Exp Parasitol 71:199–206PubMedCrossRefGoogle Scholar
  4. 4.
    Li E, Yang WG, Zhang T, Stanley SL Jr (1995) Interaction of laminin with Entamoeba histolytica cysteine proteinases and its effect on amebic pathogenesis. Infect Immun 63:4150–4153PubMedCentralPubMedGoogle Scholar
  5. 5.
    Luaces AL, Barrett AJ (1988) Affinity purification and biochemical characterization of histolysin, the major cysteine proteinase of Entamoeba histolytica. Biochem J 250:903–909PubMedCentralPubMedGoogle Scholar
  6. 6.
    Lushbaugh WB, Hofbauer AF, Pittman FE (1985) Entamoeba histolytica: purification of cathepsin B. Exp Parasitol 59:328–336PubMedCrossRefGoogle Scholar
  7. 7.
    Reed SL, Keene WE, McKerrow JH (1989) Thiol proteinase expression and pathogenicity of Entamoeba histolytica. J Clin Microbiol 27:2772–2777PubMedCentralPubMedGoogle Scholar
  8. 8.
    Schulte W, Scholze H (1989) Action of the major protease from Entamoeba histolytica on proteins of the extracellular matrix. J Protozool 36:538–543PubMedCrossRefGoogle Scholar
  9. 9.
    Stanley SL Jr, Zhang T, Rubin D, Li E (1995) Role of the Entamoeba histolytica cysteine proteinase in amebic liver abscess formation in severe combined immunodeficient mice. Infect Immun 63:1587–1590PubMedCentralPubMedGoogle Scholar
  10. 10.
    Bracha R, Mirelman D (1984) Virulence of Entamoeba histolytica trophozoites. Effects of bacteria, microaerobic conditions, and metronidazole. J Exp Med 160:353–368PubMedCrossRefGoogle Scholar
  11. 11.
    Hellberg A, Nowak N, Leippe M, Tannich E, Bruchhaus I (2002) Recombinant expression and purification of an enzymatically active cysteine proteinase of the protozoan parasite Entamoeba histolytica. Protein Expr Purif 24:131–137PubMedCrossRefGoogle Scholar
  12. 12.
    Biller L, Schmidt H, Krause E, Gelhaus C, Matthiesen J, Handal G, Lotter H, Janssen O, Tannich E, Bruchhaus I (2009) Comparison of two genetically related Entamoeba histolytica cell lines derived from the same isolate with different pathogenic properties. Proteomics 9(17):4107–4120PubMedCrossRefGoogle Scholar
  13. 13.
    Kelsall BL, Ravdin JI (1993) Degradation of human IgA by Entamoeba histolytica. J Infect Dis 168:1319–1322PubMedCrossRefGoogle Scholar
  14. 14.
    Tran VQ, Herdman DS, Torian BE, Reed SL (1998) The neutral cysteine proteinase of Entamoeba histolytica degrades IgG and prevents its binding. J Infect Dis 177:508–511PubMedCrossRefGoogle Scholar
  15. 15.
    Reed SL, Keene WE, McKerrow JH, Gigli I (1989) Cleavage of C3 by a neutral cysteine proteinase of Entamoeba histolytica. J Immunol 143:189–195PubMedGoogle Scholar
  16. 16.
    Melendez-Lopez SG, Herdman S, Hirata K, Choi MH, Choe Y, Craik C, Caffrey CR, Hansell E, Chavez-Munguia B, Chen YT, Roush WR, McKerrow J, Eckmann L, Guo J, Stanley SL Jr, Reed SL (2007) Use of recombinant Entamoeba histolytica cysteine proteinase 1 to identify a potent inhibitor of amebic invasion in a human colonic model. Eukaryot Cell 6:1130–1136PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Reed SL, Ember JA, Herdman DS, DiScipio RG, Hugli TE, Gigli I (1995) The extracellular neutral cysteine proteinase of Entamoeba histolytica degrades anaphylatoxins C3a and C5a. J Immunol 155:266–274PubMedGoogle Scholar
  18. 18.
    Que X, Kim SH, Sajid M, Eckmann L, Dinarello CA, McKerrow JH, Reed SL (2003) A surface amebic cysteine proteinase inactivates interleukin-18. Infect Immun 71:1274–1280PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Zhang Z, Wang L, Seydel KB, Li E, Ankri S, Mirelman D, Stanley SL Jr (2000) Entamoeba histolytica cysteine proteinases with interleukin-1 beta converting enzyme (ICE) activity cause intestinal inflammation and tissue damage in amoebiasis. Mol Microbiol 37:542–548PubMedCrossRefGoogle Scholar
  20. 20.
    Tillack M, Nowak N, Lotter H, Bracha R, Mirelman D, Tannich E, Bruchhaus I (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 149:58–64PubMedCrossRefGoogle Scholar
  21. 21.
    Bansal D, Ave P, Kerneis S, Frileux P, Boche O, Baglin AC, Dubost G, Leguern AS, Prevost MC, Bracha R, Mirelman D, Guillen N, Labruyere E (2009) An ex-vivo human intestinal model to study Entamoeba histolytica pathogenesis. PLoS Negl Trop Dis 3:e551PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    McLaughlin J, Faubert G (1977) Partial purification and some properties of a neutral sulfhydryl and an acid proteinase from Entamoeba histolytica. Can J Microbiol 23:420–425PubMedCrossRefGoogle Scholar
  23. 23.
    Lushbaugh WB, Hofbauer AF, Kairalla AA, Cantey JR, Pittman FE (1984) Relationship of cytotoxins of axenically cultivated Entamoeba histolytica to virulence. Gastroenterology 86:1488–1495PubMedGoogle Scholar
  24. 24.
    Keene WE, Petitt MG, Allen S, McKerrow JH (1986) The major neutral proteinase of Entamoeba histolytica. J Exp Med 163:536–549PubMedCrossRefGoogle Scholar
  25. 25.
    Luaces AL, Pico T, Barrett AJ (1992) The ENZYMEBA test: detection of intestinal Entamoeba histolytica infection by immuno-enzymatic detection of histolysain. Parasitology 105(pt 2):203–205PubMedCrossRefGoogle Scholar
  26. 26.
    Scholze H, Lohden-Bendinger U, Muller G, Bakker-Grunwald T (1992) Subcellular distribution of amebapain, the major cysteine proteinase of Entamoeba histolytica. Arch Med Res 23:105–108PubMedGoogle Scholar
  27. 27.
    Scholze H, Schulte W (1988) On the specificity of a cysteine proteinase from Entamoeba histolytica. Biomed Biochim Acta 47:115–123PubMedGoogle Scholar
  28. 28.
    Scholze H, Tannich E (1994) Cysteine endopeptidases of Entamoeba histolytica. Methods Enzymol 244:512–523PubMedCrossRefGoogle Scholar
  29. 29.
    Bruchhaus I, Jacobs T, Leippe M, Tannich E (1996) Entamoeba histolytica and Entamoeba dispar: differences in numbers and expression of cysteine proteinase genes. Mol Microbiol 22:255–263PubMedCrossRefGoogle Scholar
  30. 30.
    Bruchhaus I, Loftus BJ, Hall N, Tannich E (2003) 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 2:501–509PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Jacobs T, Bruchhaus I, Dandekar T, Tannich E, Leippe M (1998) Isolation and molecular characterization of a surface-bound proteinase of Entamoeba histolytica. Mol Microbiol 27:269–276PubMedCrossRefGoogle Scholar
  32. 32.
    Garcia-Rivera G, Rodriguez MA, Ocadiz R, Martinez-Lopez MC, Arroyo R, Gonzalez-Robles A, Orozco E (1999) Entamoeba histolytica: a novel cysteine protease and an adhesin form the 112 kDa surface protein. Mol Microbiol 33:556–568PubMedCrossRefGoogle Scholar
  33. 33.
    Reed S, Bouvier J, Pollack AS, Engel JC, Brown M, Hirata K, Que X, Eakin A, Hagblom P, Gillin F et al (1993) Cloning of a virulence factor of Entamoeba histolytica. Pathogenic strains possess a unique cysteine proteinase gene. J Clin Invest 91:1532–1540PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Tannich E, Scholze H, Nickel R, Horstmann RD (1991) Homologous cysteine proteinases of pathogenic and nonpathogenic Entamoeba histolytica. Differences in structure and expression. J Biol Chem 266:4798–4803PubMedGoogle Scholar
  35. 35.
    Tannich E, Nickel R, Buss H, Horstmann RD (1992) Mapping and partial sequencing of the genes coding for two different cysteine proteinases in pathogenic Entamoeba histolytica. Mol Biochem Parasitol 54:109–111PubMedCrossRefGoogle Scholar
  36. 36.
    Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, Moule S, Mungall K, Ormond D, Squares R, Whitehead S, Quail MA, Rabbinowitsch E, Norbertczak H, Price C, Wang Z, Guillen N, Gilchrist C, Stroup SE, Bhattacharya S, Lohia A, Foster PG, Sicheritz-Ponten T, Weber C, Singh U, Mukherjee C, El-Sayed NM, Petri WA Jr, Clark CG, Embley TM, Barrell B, Fraser CM, Hall N (2005) The genome of the protist parasite Entamoeba histolytica. Nature (Lond) 433:865–868CrossRefGoogle Scholar
  37. 37.
    Clark CG, Alsmark UC, Tazreiter M, Saito-Nakano Y, Ali V, Marion S, Weber C, Mukherjee C, Bruchhaus I, Tannich E, Leippe M, Sicheritz-Ponten T, Foster PG, Samuelson J, Noel CJ, Hirt RP, Embley TM, Gilchrist CA, Mann BJ, Singh U, Ackers JP, Bhattacharya S, Bhattacharya A, Lohia A, Guillen N, Duchene M, Nozaki T, Hall N (2007) Structure and content of the Entamoeba histolytica genome. Adv Parasitol 65:51–190PubMedCrossRefGoogle Scholar
  38. 38.
    Tillack M, Biller L, Irmer H, Freitas M, Gomes MA, Tannich E, Bruchhaus I (2007) The Entamoeba histolytica genome: primary structure and expression of proteolytic enzymes. BMC Genomics 8:170PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Baxt LA, Baker RP, Singh U, Urban S (2008) An Entamoeba histolytica rhomboid protease with atypical specificity cleaves a surface lectin involved in phagocytosis and immune evasion. Genes Dev 22:1636–1646PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Barrios-Ceballos MP, Martinez-Gallardo NA, Anaya-Velazquez F, Mirelman D, Padilla-Vaca F (2005) A novel protease from Entamoeba histolytica homologous to members of the family S28 of serine proteases. Exp Parasitol 110:270–275PubMedCrossRefGoogle Scholar
  41. 41.
    Baxt LA, Rastew E, Bracha R, Mirelman D, Singh U (2010) Downregulation of an Entamoeba histolytica rhomboid protease reveals roles in regulating parasite adhesion and phagocytosis. Eukaryot Cell 9:1283–1293PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Joshi PB, Kelly BL, Kamhawi S, Sacks DL, McMaster WR (2002) Targeted gene deletion in Leishmania major identifies leishmanolysin (GP63) as a virulence factor. Mol Biochem Parasitol 120:33–40PubMedCrossRefGoogle Scholar
  43. 43.
    Brittingham A, Morrison CJ, McMaster WR, McGwire BS, Chang KP, Mosser DM (1995) Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. J Immunol 155:3102–3111PubMedGoogle Scholar
  44. 44.
    Kulkarni MM, McMaster WR, Kamysz E, Kamysz W, Engman DM, McGwire BS (2006) The major surface-metalloprotease of the parasitic protozoan, Leishmania, protects against antimicrobial peptide-induced apoptotic killing. Mol Microbiol 62:1484–1497PubMedCrossRefGoogle Scholar
  45. 45.
    McGwire BS, Chang KP, Engman DM (2003) Migration through the extracellular matrix by the parasitic protozoan Leishmania is enhanced by surface metalloprotease gp63. Infect Immun 71:1008–1010PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Teixeira JE, Sateriale A, Bessoff KE, Huston CD (2012) Control of Entamoeba histolytica adherence involves metallosurface protease 1, an M8 family surface metalloprotease with homology to leishmanolysin. Infect Immun 80:2165–2176PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    Biller L, Davis PH, Tillack M, Matthiesen J, Lotter H, Stanley SL Jr, Tannich E, Bruchhaus I (2010) Differences in the transcriptome signatures of two genetically related Entamoeba histolytica cell lines derived from the same isolate with different pathogenic properties. BMC Genomics 11:63PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Barrett AJ (1998) In: Barrett AJ, Rawlings ND, Woessner JF (eds) Handbook of proteolytic enzymes. Academic Press, LondonGoogle Scholar
  49. 49.
    He C, Nora GP, Schneider EL, Kerr ID, Hansell E, Hirata K, Gonzalez D, Sajid M, Boyd SE, Hruz P, Cobo ER, Le C, Liu WT, Eckmann L, Dorrestein PC, Houpt ER, Brinen LS, Craik CS, Roush WR, McKerrow J, Reed SL (2010) A novel Entamoeba histolytica cysteine proteinase, EhCP4, is key for invasive amebiasis and a therapeutic target. J Biol Chem 285:18516–18527PubMedCentralPubMedCrossRefGoogle Scholar
  50. 50.
    Hellberg A, Leippe M, Bruchhaus I (2000) Two major ‘higher molecular mass proteinases’ of Entamoeba histolytica are identified as cysteine proteinases 1 and 2. Mol Biochem Parasitol 105:305–309PubMedCrossRefGoogle Scholar
  51. 51.
    Irmer H, Tillack M, Biller L, Handal G, Leippe M, Roeder T, Tannich E, Bruchhaus I (2009) Major cysteine peptidases of Entamoeba histolytica are required for aggregation and digestion of erythrocytes but are dispensable for phagocytosis and cytopathogenicity. Mol Microbiol 72:658–667PubMedCrossRefGoogle Scholar
  52. 52.
    Ocadiz R, Orozco E, Carrillo E, Quintas LI, Ortega-Lopez J, Garcia-Perez RM, Sanchez T, Castillo-Juarez BA, Garcia-Rivera G, Rodriguez MA (2005) EhCP112 is an Entamoeba histolytica secreted cysteine protease that may be involved in the parasite-virulence. Cell Microbiol 7:221–232PubMedCrossRefGoogle Scholar
  53. 53.
    Hou Y, Mortimer L, Chadee K (2010) Entamoeba histolytica cysteine proteinase 5 binds integrin on colonic cells and stimulates NFkappaB-mediated pro-inflammatory responses. J Biol Chem 285:35497–35504PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Temesvari LA, Harris EN, Stanley SL Jr, Cardelli JA (1999) Early and late endosomal compartments of Entamoeba histolytica are enriched in cysteine proteases, acid phosphatase and several Ras-related Rab GTPases. Mol Biochem Parasitol 103:225–241PubMedCrossRefGoogle Scholar
  55. 55.
    Okada M, Huston CD, Mann BJ, Petri WA Jr, Kita K, Nozaki T (2005) Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryot Cell 4:827–831PubMedCentralPubMedCrossRefGoogle Scholar
  56. 56.
    Que X, Brinen LS, Perkins P, Herdman S, Hirata K, Torian BE, Rubin H, McKerrow JH, Reed SL (2002) Cysteine proteinases from distinct cellular compartments are recruited to phagocytic vesicles by Entamoeba histolytica. Mol Biochem Parasitol 119:23–32PubMedCrossRefGoogle Scholar
  57. 57.
    Becker I, Perez-Montfort R, Perez-Torres A, Rondan-Zarate A, Montfort I, Perez-Tamayo R (1996) Entamoeba histolytica: localization of a 30-kDa cysteine proteinase using a monoclonal antibody. Exp Parasitol 82:171–181PubMedCrossRefGoogle Scholar
  58. 58.
    Araiza-Orozco LM, Avila EE, Munoz ML, Arias-Negrete S (1999) Entamoeba histolytica: surface proteolytic activity and its relationship with in vitro virulence. Folia Parasitol (Praha) 46:161–167Google Scholar
  59. 59.
    Leippe M, Sievertsen HJ, Tannich E, Horstmann RD (1995) Spontaneous release of cysteine proteinases but not of pore-forming peptides by viable Entamoeba histolytica. Parasitology 111:569–574PubMedCrossRefGoogle Scholar
  60. 60.
    Mitra BN, Saito-Nakano Y, Nakada-Tsukui K, Sato D, Nozaki T (2007) Rab11B small GTPase regulates secretion of cysteine proteases in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol 9:2112–2125PubMedCrossRefGoogle Scholar
  61. 61.
    Marquay Markiewicz J, Syan S, Hon CC, Weber C, Faust D, Guillen N (2011) A proteomic and cellular analysis of uropods in the pathogen Entamoeba histolytica. PLoS Negl Trop Dis 5:e1002PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Moncada D, Keller K, Chadee K (2003) Entamoeba histolytica cysteine proteinases disrupt the polymeric structure of colonic mucin and alter its protective function. Infect Immun 71:838–844PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Lidell ME, Moncada DM, Chadee K, Hansson GC (2006) 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 103:9298–9303PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Lauwaet T, Oliveira MJ, Callewaert B, De Bruyne G, Saelens X, Ankri S, Vandenabeele P, Mirelman D, Mareel M, Leroy A (2003) Proteolysis of enteric cell villin by Entamoeba histolytica cysteine proteinases. J Biol Chem 278:22650–22656PubMedCrossRefGoogle Scholar
  65. 65.
    Sharma M, Vohra H, Bhasin D (2005) Enhanced pro-inflammatory chemokine/cytokine response triggered by pathogenic Entamoeba histolytica: basis of invasive disease. Parasitology 131:783–796PubMedCrossRefGoogle Scholar
  66. 66.
    Navarro-Garcia F, Chavez-Duenas L, Tsutsumi V, Posadas del Rio F, Lopez-Revilla R (1995) Entamoeba histolytica: increase of enterotoxicity and of 53- and 75-kDa cysteine proteinases in a clone of higher virulence. Exp Parasitol 80:361–372PubMedCrossRefGoogle Scholar
  67. 67.
    Olivos-Garcia A, Tello E, Nequiz-Avendano M, Gonzalez-Canto A, Lopez-Vancell R, Garcia de Leon MC, Montfort I, Perez-Tamayo R (2004) Cysteine proteinase activity is required for survival of the parasite in experimental acute amoebic liver abscesses in hamsters. Parasitology 129:19–25PubMedCrossRefGoogle Scholar
  68. 68.
    Ehrenkaufer GM, Haque R, Hackney JA, Eichinger DJ, Singh U (2007) Identification of developmentally regulated genes in Entamoeba histolytica: insights into mechanisms of stage conversion in a protozoan parasite. Cell Microbiol 9(6):1426–1444PubMedCrossRefGoogle Scholar
  69. 69.
    Makioka A, Kumagai M, Kobayashi S, Takeuchi T (2005) Entamoeba invadens: cysteine protease inhibitors block excystation and metacystic development. Exp Parasitol 109:27–32PubMedCrossRefGoogle Scholar
  70. 70.
    Gilchrist CA, Houpt E, Trapaidze N, Fei Z, Crasta O, Asgharpour A, Evans C, Martino-Catt S, Baba DJ, Stroup S, Hamano S, Ehrenkaufer G, Okada M, Singh U, Nozaki T, Mann BJ, Petri WA Jr (2006) Impact of intestinal colonization and invasion on the Entamoeba histolytica transcriptome. Mol Biochem Parasitol 147:163–176PubMedCrossRefGoogle Scholar
  71. 71.
    Freitas MA, Fernandes HC, Calixto VC, Martins AS, Silva EF, Pesquero JL, Gomes MA (2009) Entamoeba histolytica: cysteine proteinase activity and virulence. Focus on cysteine proteinase 5 expression levels. Exp Parasitol 122:306–309PubMedCrossRefGoogle Scholar
  72. 72.
    Davis PH, Schulze J, Stanley SL Jr (2007) Transcriptomic comparison of two Entamoeba histolytica strains with defined virulence phenotypes identifies new virulence factor candidates and key differences in the expression patterns of cysteine proteases, lectin light chains, and calmodulin. Mol Biochem Parasitol 151:118–128PubMedCrossRefGoogle Scholar
  73. 73.
    Thibeaux R, Dufour A, Roux P, Bernier M, Baglin AC, Frileux P, Olivo-Marin JC, Guillen N, Labruyere E (2012) Newly visualized fibrillar collagen scaffolds dictate Entamoeba histolytica invasion route in the human colon. Cell Microbiol 14:609–621PubMedCrossRefGoogle Scholar
  74. 74.
    Ankri S, Stolarsky T, Mirelman D (1998) Antisense inhibition of expression of cysteine proteinases does not affect Entamoeba histolytica cytopathic or haemolytic activity but inhibits phagocytosis. Mol Microbiol 28:777–785PubMedCrossRefGoogle Scholar
  75. 75.
    Moncada D, Keller K, Ankri S, Mirelman D, Chadee K (2006) Antisense inhibition of Entamoeba histolytica cysteine proteases inhibits colonic mucus degradation. Gastroenterology 130:721–730PubMedCrossRefGoogle Scholar
  76. 76.
    Bracha R, Nuchamowitz Y, Anbar M, Mirelman D (2006) Transcriptional silencing of multiple genes in trophozoites of Entamoeba histolytica. PLoS Pathog 2:e48PubMedCentralPubMedCrossRefGoogle Scholar
  77. 77.
    Bracha R, Nuchamowitz Y, Mirelman D (2003) Transcriptional silencing of an amoebapore gene in Entamoeba histolytica: molecular analysis and effect on pathogenicity. Eukaryot Cell 2:295–305PubMedCentralPubMedCrossRefGoogle Scholar
  78. 78.
    Faust DM, Marquay Markiewicz J, Danckaert A, Soubigou G, Guillen N (2011) Human liver sinusoidal endothelial cells respond to interaction with Entamoeba histolytica by changes in morphology, integrin signalling and cell death. Cell Microbiol 13:1091–1106PubMedCrossRefGoogle Scholar
  79. 79.
    Mora-Galindo J, Anaya-Velazquez F, Ramirez-Romo S, Gonzalez-Robles A (2004) Entamoeba histolytica: correlation of assessment methods to measure erythrocyte digestion, and effect of cysteine proteinases inhibitors in HM-1:IMSS and HK-9:NIH strains. Exp Parasitol 108:89–100PubMedCrossRefGoogle Scholar
  80. 80.
    Hellberg A, Nickel R, Lotter H, Tannich E, Bruchhaus I (2001) 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 3:13–20PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  1. 1.Bernhard Nocht Institute for Tropical MedicineHamburgGermany

Personalised recommendations