Chapter 23 : Genomic and Postgenomic Approaches to Understanding the Pathogenesis of the Enteric Protozoan Parasite

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Elaborate regulation of membrane trafficking is essential for the targeting of molecules necessary for pathogenesis (e.g., lectin and CPs) to precise intracellular compartments such as the surface membrane and lysosomes. This chapter discusses the diversification of cysteine proteases (CPs) and Rab in the context of their diverse localization and function. Encystation and excystation are fundamental processes required for the transmission and development of amebiasis. The current assembly predicts that the genome contains 8,160 genes, almost 1.5-fold more than the number of genes in (5,268) or (5,538), and close to that in (12,500). The majority of ribosomal protein genes are well conserved, and only the gene for the large subunit protein L41 has not been identified. The chapter focuses only on several important pathways closely related to the parasite's molecular epidemiology, biology, and virulence. It also talks about the insights obtained from comparing their genome information with that of to understand the conservation and unique evolution of the species. Insights into the developmental regulation of CPs and Rab small GTPases during encystation are also discussed as examples of transcriptomic approaches to understand the biology and pathogenesis of this group of enteric protozoa. To gain insights into the mechanisms of encystation-specific membrane trafficking, the authors also investigated the transcriptomic changes of Rab genes during the encystation of . The kinetics of the steady-state levels of mRNA for individual Rab genes were categorized into cyst-specific, trophozoite-specific, or constitutive genes.

Citation: Nakada-Tsukui K, Nozaki T. 2011. Genomic and Postgenomic Approaches to Understanding the Pathogenesis of the Enteric Protozoan Parasite , p 321-341. In Fratamico P, Liu Y, Kathariou S (ed), Genomes of Foodborne and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816902.ch23

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RNA Polymerase II
Small Nuclear RNA
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Image of Figure 1
Figure 1

Phylogenetic analysis of CPs from and Phylogenetic analysis of CPs from the C1 family of and was performed using CLUSTAL W. Trees were drawn using MEGA4. The consensus phylogenetic trees of the CP-A, CP-B, and CP-C families are shown. The numbers at the nodes represent the bootstrap values for 1,000 iterations shown in percentages. The scale bar indicates 0.1 or 0.2 substitutions at each amino acid position.

Citation: Nakada-Tsukui K, Nozaki T. 2011. Genomic and Postgenomic Approaches to Understanding the Pathogenesis of the Enteric Protozoan Parasite , p 321-341. In Fratamico P, Liu Y, Kathariou S (ed), Genomes of Foodborne and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816902.ch23
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Image of Figure 2
Figure 2

Phylogenetic analysis of Rab genes from and Phylogenetic analysis was performed as described in the legend to Fig. 1 . An overview of the whole phylogenetic tree is shown on the left, while magnifed portions (A to D) of the tree are shown separately on the right.

Citation: Nakada-Tsukui K, Nozaki T. 2011. Genomic and Postgenomic Approaches to Understanding the Pathogenesis of the Enteric Protozoan Parasite , p 321-341. In Fratamico P, Liu Y, Kathariou S (ed), Genomes of Foodborne and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816902.ch23
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Image of Figure 3
Figure 3

Kinetics of CP and Rab gene expression during encystation in trophozoites were cultured in encystation medium. Total RNA was extracted at 0, 0.5, 2, 8, 24, 48, and 120 h, and subjected to transcriptome analysis using DNA microarrays. The normalized relative fluorescence intensity of each gene is shown.

Citation: Nakada-Tsukui K, Nozaki T. 2011. Genomic and Postgenomic Approaches to Understanding the Pathogenesis of the Enteric Protozoan Parasite , p 321-341. In Fratamico P, Liu Y, Kathariou S (ed), Genomes of Foodborne and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816902.ch23
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1. Abed, M., and, S. Ankri. 2005. Molecular characterization of Entamoeba histolytica RNase III and AGO2, two RNA interference hallmark proteins. Exp. Parasitol. 110:265269.
2. Ali, I. K.,, S. Solaymani-Mohammadi,, J. Akhter,, S. Roy,, C. Gorrini,, A. Calderaro,, S. K. Parker,, R. Haque,, W. A. Petri, and, C. G. Clark. 2008. Tissue Invasion by Entamoeba h istolytica: Evidence of genetic selection and/or DNA reorganization events in organ tropism. PLoS Negl. Trop. Dis. 2:e219.
3. Ali, I. K.,, U. Mondal,, S. Roy,, R. Haque,, W. A. Petri, Jr., and, C. G. Clark. 2007. Evidence for a link between parasite genotype and outcome of infection with Entamoeba histolytica. J. Clin. Microbiol. 45:285289.
4. Ali, V., and, T. Nozaki. 2007. Current therapeutics, their problems, and sulfur-containing-amino-acid metabolism as a novel target against infections by “amitochondriate” protozoan parasites. Clin. Microbiol. Rev. 20:164187.
5. Ali, I. K.,, M. Zaki, and, C. G. Clark. 2005. Use of PCR amplification of tRNA gene-linked short tandem repeats for genotyping Entamoeba histolytica. J. Clin. Microbiol. 43:58425847.
6. Ali, I. K.,, M. B. Hossain,, S. Roy,, P. F. Ayeh-Kumi,, W. A. Petri, Jr.,, R. Haque, and, C. G. Clark. 2003. Entamoeba m oshkovskii infections in children, Bangladesh. Emerg. Infect. Dis. 9:580584.
7. Anamika, K.,, A. Bhattacharya, and, N. Srinivasan. 2008. Analysis of the protein kinome of Entamoeba histolytica. Proteins 71:9951006.
8. Anbar, M.,, R. Bracha,, Y. Nuchamowitz,, Y. Li,, A. Florentin, and, D. Mirelman. 2005. Involvement of a short interspersed element in epigenetic transcriptional silencing of the amoebapore gene in Entamoeba histolytica. Eukaryot. Cell 4:17751784.
9. Anderson, I. J., and, B. J. Loftus. 2005. Entamoeba histolytica: observations on metabolism based on the genome sequence. Exp. Parasitol. 110:173177.
10. Ankri, S.,, T. Stolarsky,, R. Bracha,, F. Padilla-Vaca, and, D. Mirelman. 1999. Antisense inhibition of expression of cysteine proteinases affects Entamoeba histolytica-induced formation of liver abscess in hamsters. Infect. Immun. 67:421422.
11. Baek, K. H. 2006. Cytokine-regulated protein degradation by the ubiquitination system. Curr. Protein. Pept. Sci. 7:171177.
12. Baek, K. H. 2003. Conjugation and deconjugation of ubiquitin regulating the destiny of proteins. Exp. Mol. Med. 35:17.
13. Bakre, A. A.,, K. Rawal,, R. Ramaswamy,, A. Bhattacharya, and, S. Bhattacharya. 2005. The LINEs and SINEs of Entamoeba histolytica: comparative analysis and genomic distribution. Exp. Parasitol. 110:207213.
14. Balakirev, M. Y.,, S. O. Tcherniuk,, M. Jaquinod, and, J. Chrob-oczek. 2003. Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep. 4:517522.
15. Barrett, A. J. 1998. Cysteine peptidase, p. 543-798. In A. J. Barrett,, N. D. Rawlings, and, J. F. Woessner (ed.), Handbook of Proteolytic Enzymes. Academic Press, San Diego, CA.
16. Bentley, D. L. 2005. Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr. Opin. Cell Biol. 17:251256.
17. Boettner, D. R.,, C. D. Huston,, A. S. Linford,, S. N. Buss,, E. Houpt,, N. E. Sherman, and, W. A. Petri, Jr. 2008. Entamoeba histolytica phagocytosis of human erythrocytes involves PATMK, a member of the transmembrane kinase family. PLoS Pathog. 4:e8.
18. Borodovsky, A.,, H. Ovaa,, N. Kolli,, T. Gan-Erdene,, K. D. Wilkinson,, H. L. Ploegh, and, B. M. Kessler. 2002. Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9:11491159.
19. Bourne, H. R.,, D. A. Sanders, and, F. McCormick. 1990. The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348:125132.
20. Bracha, R.,, Y. Nuchamowitz,, N. Wender, and, D. Mirelman. 2007. Transcriptional gene silencing reveals two distinct groups of Entamoeba histolytica Gal/GalNAc-lectin light sub-units. Eukaryot. Cell 6:17581765.
21. Bracha, R.,, Y. Nuchamowitz,, M. Anbar, and, D. Mirelman. 2006. Transcriptional silencing of multiple genes in trophozoites of Entamoeba histolytica. PLoS Pathog. 2:e48.
22. Bracha, R.,, Y. Nuchamowitz, and, D. Mirelman. 2003. Transcriptional silencing of an amoebapore gene in Entamoeba histolytica: molecular analysis and effect on pathogenicity. Eukaryot. Cell 2:295305.
23. Bruchhaus, I.,, B. J. Loftus,, N. Hall, and, E. Tannich. 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 2:501509.
24. Bruchhaus, I.,, M. Leippe,, C. Lioutas, and, E. Tannich. 1993. Unusual gene organization in the protozoan parasite Entamoeba histolytica. DNA Cell Biol. 2:925933.
25. Bujanover, S.,, U. Katz,, R. Bracha, and, D. Mirelman. 2003. A virulence attenuated amoebapore-less mutant of Entamoeba histolytica and its interaction with host cells. Int. J. Parasitol. 33:16551663.
26. Buratowski, S. 2005. Connections between mRNA 3′ end processing and transcription termination. Curr. Opin. Cell Biol. 17:25722561.
27. Cho, E. J. 2007. RNA polymerase II carboxy-terminal domain with multiple connections. Exp. Mol. Med. 39:247254.
28. Clark, C. G.,, U. C. Alsmark,, M. Tazreiter,, Y. Saito-Nakano,, V. Ali,, S. Marion,, C. Weber,, C. Mukherjee,, I. Bruchhaus,, E. Tannich,, M. Leippe,, T. Sicheritz-Ponten,, P. G. Foster,, J. Samuelson,, J. Noël,, R. P. Hirt,, T. M. Embley,, C. A. Gilchrist,, B. J. Mann,, U. Singh,, J. P. Ackers,, S. Bhattacharya,, A. Bhattacharya,, A. Lohia,, N. Guillén,, M. Duchêne,, T. Nozaki, and, N. Hall. 2007. Structure and content of the Entamoeba h istolytica genome. Adv. Parasitol. 65:51190.
29. Clark, C. G.,, I. K. Ali,, M. Zaki,, B. J. Loftus, and, N. Hall. 2006. Unique organization of tRNA genes in Entamoeba histolytica. Mol. Biochem. Parasitol. 146:2429.
30. Clark, C. G., and, L. S. Diamond. 1997. Intraspecific variation and phylogenetic relationships in the genus Entamoeba as revealed by riboprinting. J. Eukaryot. Microbiol. 44:142154.
31. Clark, C. G., and, L. S. Diamond. 1991. Ribosomal RNA genes of ‘pathogenic’ and ‘nonpathogenic’ Entamoeba histolytica are distinct. Mol. Biochem. Parasitol. 49:297302.
32. Clark, C. G., and, L. S. Diamond. 1991. The Laredo strain and other “Entamoeba histolytica-like” amoebae are Entamoeba moshkovskii. Mol. Biochem. Parasitol. 46:1118.
33. Davis, P. H.,, M. Chen,, X. Zhang,, C. G. Clark,, R. R. Townsend, and, S. L. Stanley. 2009. Proteomic comparison of Entamoeba histolytica and Entamoeba dispar and the Role of E. histolytica alcohol dehydrogenase 3 in virulence. PLoS Negl. Trop. Dis. 3:e415.
34. Davis, P. H.,, J. Schulze, and, S. L. Stanley, Jr. 2007. Transcrip-tomic 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. 151:118128.
35. Davis, P. H.,, X. Zhang,, J. Guo,, R. R. Townsend, and, S. L. Stanley, Jr. 2006. Comparative proteomic analysis of two Entamoeba histolytica strains with different virulence phenotypes identifies peroxiredoxin as an important component of amebic virulence. Mol. Microbiol. 61:15231532.
36. Davis, P. H.,, Z. Zhang,, M. Chen,, X. Zhang,, S. Chakraborty, and, S. L. Stanley, Jr. 2006. Identification of a family of BspA like surface proteins of Entamoeba histolytica with novel leu-cine rich repeats. Mol. Biochem. Parasitol. 145:111116.
37. Diamond, L. S., and, C. G. Clark. 1993. A redescription of Entamoeba histolytica Schaudinn, 1903 (Emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. J. Eukaryot. Microbiol. 40:340344.
38. Duggal, P.,, R. Haque,, S. Roy,, D. Mondal,, R. B. Sack,, B. M. Farr,, T. H. Beaty, and, W. A. Petri, Jr. 2004. Influence of human leukocyte antigen class II alleles on susceptibility to Entamoeba histolytica infection in Bangladeshi children. J. Infect. Dis. 189:520526.
39. Ebert, F.,, A. Bachmann,, K. Nakada-Tsukui, I. Hennings,, B. Drescher,, T. Nozaki,, E. Tannich, and, I. Bruchhaus. 2008. An Entamoeba cysteine peptidase specifically expressed during encystation. Parasitol. Int. 7:521524.
40. Ehrenkaufer, G. M.,, J. A. Hackney, and, U. Singh. 2009. A developmentally regulated Myb domain protein regulates expression of a subset of stage-specific genes in Entamoeba histolytica. Cell Microbiol. 11:898910.
41. Ehrenkaufer, G. M.,, R. Haque,, J. A. Hackney,, D. J. Eich-inger, and, U. Singh. 2007. Identification of developmentally regulated genes in Entamoeba histolytica: insights into mechanisms of stage conversion in a protozoan parasite. Cell Microbiol. 9:14261444.
42. Eichinger, L.,, J. A. Pachebat,, G. Glöckner, M. A. Rajandream,, R. Sucgang,, M. Berriman,, J. Song,, R. Olsen,, K. Szafranski,, Q. Xu,, B. Tunggal,, S. Kummerfeld,, M. Madera,, B. A. Konfortov,, F. Rivero,, A. T. Bankier,, R. Lehmann,, N. Hamlin,, R. Davies,, P. Gaudet,, P. Fey,, K. Pilcher,, G. Chen,, D. Saunders,, E. Sodergren,, P. Davis,, A. Kerhornou,, X. Nie,, N. Hall,, C. Anjard,, L. Hemp-hill,, N. Bason,, P. Farbrother,, B. Desany,, E. Just,, T. Morio,, R. Rost,, C. Churcher,, J. Cooper,, S. Haydock,, N. van Driessche,, A. Cronin,, I. Goodhead,, D. Muzny,, T. Mourier,, A. Pain,, M. Lu,, D. Harper,, R. Lindsay,, H. Hauser,, K. James,, M. Quiles,, M. Madan Babu,, T. Saito,, C. Buchrieser,, A. Wardroper,, M. Felder,, M. Thangavelu,, D. Johnson,, A. Knights,, H. Loulseged,, K. Mungall,, K. Oliver,, C. Price,, M. A. Quail,, H. Urushihara,, J. Hernandez,, E. Rabbinowitsch,, D. Steffen,, M. Sanders,, J. Ma,, Y. Kohara,, S. Sharp,, M. Simmonds,, S. Spiegler,, A. Tivey,, S. Sugano,, B. White,, D. Walker,, J. Woodward,, T. Winckler,, Y. Tanaka,, G. Shaulsky,, M. Schleicher,, G. Weinstock,, A. Rosen-thal,, E. C. Cox,, R. L. Chisholm,, R. Gibbs,, W. F. Loomis,, M. Platzer,, R. R. Kay,, J. Williams,, P. H. Dear,, A. A. Noegel,, B. Barrell, and, A. Kuspa. 2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435:4357.
43. Eichinger, D. 1997. Encystation of entamoeba parasites. Bioessays 19:633639.
44. Evans, P. C.,, T. S. Smith,, M. J. Lai,, M. G. Williams,, D. F. Burke,, K. Heyninck,, M. M. Kreike,, R. Beyaert,, T. L. Blundell, and, P. J. Kilshaw. 2003. A novel type of deubiquitinating enzyme. J. Biol. Chem. 278:2318023186.
45. Fotedar, R.,, D. Stark,, D. Marriott,, J. Ellis, and, J. Harkness. 2008. Entamoeba moshkovskii infections in Sydney, Australia. Eur. J. Clin. Microbiol. Infect. Dis. 27:133137.
46. Frederick, J. R., and, W. A. Petri, Jr. 2005. Roles for the galactose/ N-acetylgalactosamine-binding lectin of Entamoeba in parasite virulence and differentiation. Glycobiology 15:53R59R.
47. Gadasi, H., and, E. Kessler. 1983. Correlation of virulence and collagenolytic activity in Entamoeba histolytica. Infect. I mmun. 39:5285231.
48. Gardner, M. J.,, N. Hall,, E. Fung,, O. White,, M. Berriman,, R. W. Hyman,, J. M. Carlton,, A. Pain,, K. E. Nelson,, S. Bowman,, I. T. Paulsen,, K. James,, J. A. Eisen,, K. Rutherford,, S. L. Salzberg,, A. Craig,, S. Kyes,, M. S. Chan,, V. Nene,, S. J. Shallom,, B. Suh,, J. Peterson,, S. Angiuoli,, M. Pertea,, J. Allen,, J. Selengut,, D. Haft,, M. W. Mather,, A. B. Vaidya,, D. M. Martin,, A. H. Fairlamb,, M. J. Fraunholz,, D. S. Roos,, S. A. Ralph,, G. I. Mc-Fadden,, L. M. Cummings,, G. M. Subramanian,, C. Mungall,, J. C. Venter,, D. J. Carucci,, S. L. Hoffman,, C. Newbold,, R. W. Davis,, C. M. Fraser, and, B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 19:498511.
49. Gelderman, A. H.,, I. L. Bartgis,, D. B. Keister, and, L. S. D iamond. 1971. A comparison of genome sizes and thermal-denaturation-derived base composition of DNAs from several members of Entamoeba (histolytica group). J. Parasitol. 57:912916.
50. Gelderman, A. H.,, D. B. Keister,, I. L. Bartgis, and, L. S. Diamond. 1971. Characterization of the deoxyribonucleic acid of representative strains of Entamoeba histolytica, E. histolytica-like amebae, and E. moshkovskii. J. Parasitol. 57:906911.
51. Ghadirian, E., and, E. Meerovitch. 1984. Lectin-induced agglutination of trophozoites of different species and strains of Entamoeba. Z. Parasitenkd. 70:14752.
52. Gilchrist, C. A.,, E. Houpt,, N. Trapaidze,, Z. Fei,, O. Crasta,, A. Asgharpour,, C. Evans,, S. Martino-Catt,, D. J. Baba,, S. Stroup,, S. Hamano,, G. Ehrenkaufer,, M. Okada,, U. Singh,, T. Nozaki,, B. J. Mann, and, W. A. Petri, Jr. 2006. Impact of intestinal colonization and invasion on the Entamoeba histolytica tran-scriptome. Mol. Biochem. Parasitol. 147:163176.
53. Goffeau, A.,, B. G. Barrell,, H. Bussey,, R. W. Davis,, B. Dujon,, H. Feldmann,, F. Galibert,, J. D. Hoheisel,, C. Jacq,, M. Johnston,, E. J. Louis,, H. W. Mewes,, Y. Murakami,, P. Philippsen,, H. Tettelin, and, S. G. Oliver. 1996. Life with 6000 genes. Science 274:546, 563567.
54. Hacker, J.,, U. Hentschel, and, U. Dobrindt. 2003. Prokaryotic chromosomes and disease. Science. 301:790793.
55. Haque, R.,, C. D. Huston,, M. Hughes,, E. Houpt, and, W. A. Petri, Jr. 2003. Amebiasis. N. Engl. J. Med. 348:15651573.
56. Haque, R.,, P. Duggal,, I. M. Ali,, M. B. Hossain,, D. Mondal,, R. B. Sack,, B. M. Farr,, T. H. Beaty, and, W. A. Petri, Jr. 2002. Innate and acquired resistance to amebiasis in Bangladeshi children. J. Infect. Dis. 186:547552.
57. Haque, R.,, I. K. Ali,, S. Akther, and, W. A. Petri, Jr. 1998. Comparison of PCR, isoenzyme analysis, and antigen detection for diagnosis of Entamoeba histolytica infection. J. Clin. Microbiol. 36:449452.
58. Hernández, R.,, J. P. Luna-Arias, and, E. Orozco. 1997. Comparison of the Entamoeba histolytica TATA-binding protein (TBP) structure with other TBP. Arch. Med. Res. 28:4345.
59. Hirata, K. K.,, X. Que,, S. G. Melendez-Lopez,, A. Debnath,, S. Myers,, D. S. Herdman,, E. Orozco,, A. Bhattacharya,, J. H. McKerrow, and, S. L. Reed. 2007. A phagocytosis mutant of Entamoeba histolytica is less virulent due to deficient protei-nase expression and release. Exp. Parasitol. 115:192199.
60. Huston, C. D. 2004. Parasite and host contributions to the pathogenesis of amebic colitis. Trends Parasitol. 20:2326.
61. Jurica, M. S., and, M. J. Moore. 2003. Pre-mRNA splicing: awash in a sea of proteins. Mol. Cell. 12:514.
62. Keene, W. E.,, M. E. Hidalgo,, E. Orozco, and, J. H. McKerrow. 1990. Entamoeba histolytica: correlation of the cytopathic effect of virulent trophozoites with secretion of a cysteine pro-teinase. Exp. Parasitol. 71:199206.
63. Kimura, R. H.,, P. V. Choudary,, K. K. Stone, and, C. W. Schmid. 2001. Stress induction of Bm1 RNA in silkworm larvae: SINEs, an unusual class of stress genes. Cell Stress Chaperones 6:263272.
64. Klionsky, D. J. 2007. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8:931937.
65. Kuchay, S. M, and, A. H. Chishti. 2007. Calpain-mediated regulation of platelet signaling pathways. Curr. Opin. Hematol. 14:24922954.
66. Kunji, E. R. 2004. The role and structure of mitochondrial carriers. FEBS Lett. 564:239244.
67. Lebart, M. C., and, Y. Benyamin. 2006. Calpain involvement in the remodeling of cytoskeletal anchorage complexes. FEBS J. 273:34153426.
68. Leitsch, D.,, D. Kolarich,, I. B. Wilson,, F. Altmann, and, M. Duchêne. 2007. Nitroimidazole action in Entamoeba histolytica: a central role for thioredoxin reductase. PLoS Biol. 5:e211.
69. Leitsch, D.,, C. Radauer,, K. Paschinger,, I. B. Wilson,, H. Breiteneder,, O. Scheiner, and, M. Duchêne. 2005. Entamoeba histolytica: analysis of the trophozoite proteome by two-dimensional polyacrylamide gel electrophoresis. Exp. Parasitol. 110:191195.
70. Li, Y.,, Z. Y. Chen,, W. Wang,, C. C. Baker, and, R. M. Krug. 2001. The 3′-end-processing factor CPSF is required for the splicing of single-intron pre-mRNAs in vivo. RNA. 7:920923.
71. Li, E.,, W. G. Yang,, T. Zhang, and, S. L. Stanley, Jr. 1995. Interaction of laminin with Entamoeba histolytica cysteine protei-nases and its effect on amebic pathogenesis. Infect. Immun. 63:41504153.
72. Linford, A. S.,, H. Moreno,, K. R. Good,, H. Zhang,, U. Singh, and, W. A. Petri, Jr. 2009. Short hairpin RNA-mediated knockdown of protein expression in Entamoeba histolytica. BMC Microbiol. 9:38.
73. Lioutas, C., and, E. Tannich. 1995. Transcription of protein-coding genes in Entamoeba histolytica is insensitive to high concentrations of alpha-amanitin. Mol. Biochem. Parasitol. 73:259261.
74. Loftus, B.,, I. Anderson,, R. Davies,, U. C. Alsmark,, J. Samuelson,, P. Amedeo,, P. Roncaglia,, M. Berriman,, R. P. Hirt,, B. J. Mann,, T. Nozaki,, B. Suh,, M. Pop,, M. Duchene,, J. Ackers,, E. Tannich,, M. Leippe,, M. Hofer,, I. Bruchhaus,, U. Willhoeft,, A. Bhattacharya,, T. Chillingworth,, C. Churcher,, Z. Hance,, B. Harris,, D. Harris,, K. Jagels,, S. Moule,, K. Mungall,, D. Ormond,, R. Squares,, S. Whitehead,, M. A. Quail,, E. Rabbin-owitsch,, H. Norbertczak,, C. Price,, Z. Wang,, N. Guillén,, C. Gilchrist,, S. E. Stroup,, S. Bhattacharya,, A. Lohia,, P. G. Foster,, T. Sicheritz-Ponten,, C. Weber,, U. Singh,, C. Mukherjee,, N. M. El-Sayed,, W. A. Petri, Jr.,, C. G. Clark,, T. M. Embley,, B. Barrell,, C. M. Fraser, and, N. Hall. 2005. The genome of the protist parasite Entamoeba histolytica. Nature 433:865858.
75. Lorenzi, H.,, M. Thiagarajan,, B. Haas,, J. Wortman,, N. Hall, and, E. Caler. 2008. Genome wide survey, discovery and evolution of repetitive elements in three Entamoeba species. BMC Genomics 9:595.
76. Lowther, S. A.,, M. S. Dworkin, and, D. L. Hanson. 2000. Entamoeba histolytica/Entamoeba dispar infections in human immunodeficiency virus-infected patients in the United States. Clin. Infect. Dis. 30:955959.
77. Luaces, A. L., and, A. J. Barrett. 1988. Affinity purification and biochemical characterization of histolysin, the major cysteine proteinase of Entamoeba histolytica. Biochem. J. 250:903909.
78. Lushbaugh, W. B.,, A. F. Hofbauer, and, F. E. Pittman. 1985. Entamoeba histolytica: purification of cathepsin B. Exp. P arasitol. 59:328336.
79. MacFarlane, R. C., and, U. Singh. 2006. Identification of differentially expressed genes in virulent and nonvirulent Entamoeba species: potential implications for amebic pathogenesis. Infect. Immun. 74:340351.
80. MacFarlane, R.,, D. Bhattacharya, and, U. Singh. 2005. Genomic DNA microarrays for Entamoeba histolytica: applications for use in expression profiling and strain genotyping. Exp. Parasitol. 110:196202.
81. Marion, S.,, C. Laurent, and, N. Guillén. 2005. Signalization and cytoskeleton activity through myosin IB during the early steps of phagocytosis in Entamoeba histolytica: a proteomic approach. Cell Microbiol. 7:15041518.
82. McGugan, G. C., Jr., and, L. A. Temesvari. 2003. Characterization of a Rab11-like GTPase, EhRab11, of Entamoeba histolytica. Mol. Biochem. Parasitol. 129:137146.
83. McKerrow, J. H.,, C. Caffrey,, B. Kelly,, P. Loke, and, M. Sajid. 2006. Proteases in parasitic diseases. Annu. Rev. Pathol. 1:497536.
84. Mehra, A.,, J. Fredrick,, W. A. Petri, Jr.,, S. Bhattacharya, and, A. Bhattacharya. 2006. Expression and function of a family of transmembrane kinases from the protozoan parasite Entamoeba histolytica. Infect. Immun. 74:53414351.
85. Mi-ichi, F.,, M. A. Yousuf,, K. Nakada-Tsukui, and, T. Nozaki. 2009. Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc. Natl. Acad. Sci. USA 106:2173121736.
86. Mirelman, D.,, M. Anbar, and, R. Bracha. 2008. Epigenetic transcriptional gene silencing in Entamoeba histolytica. IUBMB Life 60:598604.
87. Mitra, B. N.,, Y. Saito-Nakano,, K. Nakada-Tsukui,, D. Sato, and, T. Nozaki. 2007. Rab11B small GTPase regulates secretion of cysteine proteases in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol. 9:21122125.
88. Nakada-Tsukui, K.,, Y. Saito-Nakano,, V. Ali, and, T. Nozaki. 2005. A retromerlike complex is a novel Rab7 effector that is involved in the transport of the virulence factor cysteine protease in the enteric protozoan parasite Entamoeba histolytica. Mol. Biol. Cell 16:52945303.
89. World Health Organization. 1997. WHO/PAHO/UNESCO report. A consultation with experts on amoebiasis. Mexico City, Mexico January 28-29, 1997. Epidemiol. Bull. 18:1314.
90. Novick, P., and, M. Zerial. 1997. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9:496504.
91. Nozaki, X,, S. Kobayashi,, T. Takeuchi, and, A. Haghighi. 2006. Diversity of clinical isolates of Entamoeba histolytica in Japan. Arch. Med. Res. 37:277279.
92. Nozaki, X, and, K. Nakada-Tsukui. 2006. Membrane trafficking as a virulence mechanism of the enteric protozoan parasite Entamoeba histolytica. Parasitol. Res. 98:179183.
93. Nozaki, X,, V. Ali, and, M. Tokoro. 2005. Sulfur-containing amino acid metabolism in parasitic protozoa. Adv. Parasitol. 60:199.
94. Okada, M.,, C. D. Huston,, M. Oue,, B. J. Mann,, W. A. Petri, Jr.,, K. Kita, and, X Nozaki. 2006. Kinetics and strain variation of phagosome proteins of Entamoeba histolytica by proteomic analysis. Mol. Biochem. Parasitol. 145:171183.
95. Okada, M.,, C. D. Huston,, B. J. Mann,, W. A. Petri, Jr.,, K. Kita, and, X Nozaki. 2005. Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryot. Cell 4:827831.
96. Orozco, E.,, G. Guarneros,, A. Martinez-Palomo, and, X Sánchez. 1983. Entamoeba histolytica. Phagocytosis as a virulence factor. J. Exp. Med. 158:15111521.
97. Ostertag, E. M., and, H. H. Kazazian, Jr. 2001. Biology of mammalian L1 retrotransposons. Annu. Rev. Genet. 35:501538.
98. Palmieri, F.,, G. Agrimi,, E. Blanco,, A. Castegna,, M. A. Di Noia,, V. Iacobazzi,, F. M. Lasorsa,, C. M. Marobbio,, L. Palmieri,, P. Scarcia,, S. Todisco,, A. Vozza, and, J. Walker. 2006. Identification of mitochondrial carriers in Saccharomyces cerevisiae by transport assay of reconstituted recombinant proteins. Biochim. Biophys. Acta. 1757:12491262.
99. Parija, S. C., and, K. Khairnar. 2005. Entamoeba mosh kovskii and Entamoeba dispar-associated infections in Pondicherry, India. J. Health Popul. Nutr. 23:292295.
100. Pereira-Leal, J. B., and, M. C. Seabra. 2001. Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313:889901.
101. Perrin, B. J., and, A. Huttenlocher. 2002. Calpain. Int. J. Biochem. Cell Biol. 34:722725.
102. Phatnani, H. P., and, A. L. Greenleaf. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20:29222936.
103. Picazarri, K.,, K. Nakada-Tsukui, and, X Nozaki. 2008. Au-tophagy during proliferation and encystation in the protozoan parasite Entamoeba invadens. Infect. Immun. 76:278288.
104. Picazarri, K., K. Nakada-Tsukui, D. Sato, and X Nozaki. 2008. Analysis of autophagy in the enteric protozoan parasite Entamoeba. Methods Enzymol. 451:359371.
105. Pritham, E. J.,, C. Feschotte, and, S. R. Wessler. 2005. Unexpected diversity and differential success of DNA transposons in four species of entamoeba protozoans. Mol. Biol. Evol. 22:17511763.
106. Purdy, J. E.,, L. T. Pho,, B. J. Mann, and, W. A. Petri, Jr. 1996. Upstream regulatory elements controlling expression of the Entamoeba histolytica lectin. Mol. Biochem. Parasitol. 78:91103.
107. Que, X., and, S. L. Reed. 2000. Cysteine proteinases and the pathogenesis of amebiasis. Clin. Microbiol. Rev. 13:196206.
108. Quon, D. V.,, M. G. Delgadillo, and, P. J. Johnson. 1996. Transcription in the early diverging eukaryote Trichomo-nas vaginalis: an unusual RNA polymerase II and alpha-amanitin-resistant transcription of protein-coding genes. J. Mol. Evol. 43:253262.
109. Ramakrishnan, G.,, C. A. Gilchrist,, H. Musa,, M. S. Torok,, P. A. Grant,, B. J. Mann, and, W. A. Petri, Jr. 2004. Histone acetyltransferases and deacetylase in Entamoeba histolytica. Mol. Biochem. Parasitol. 138:205216.
110. Ramos, M. A.,, G. C. Mercado,, L. M. Salgado,, R. Sanchez-Lopez,, R. P. Stock,, P. M. Lizardi, and, A. Alagón. 1997. E ntamoeba histolytica contains a gene encoding a homologue to the 54 kDa subunit of the signal recognition particle. Mol. Biochem. Parasitol. 88:225235.
111. Reed, S. L.,, W. E. Keene, and, J. H. McKerrow. 1989. Thiol proteinase expression and pathogenicity of Entamoeba histolytica. J. Clin. Microbiol. 27:27722777.
112. Rivera, W. L.,, S. R. Santos, and, H. Kanbara. 2006. Prevalence and genetic diversity of Entamoeba histolytica in an institution for the mentally retarded in the Philippines. Parasitol. Res. 98:106110.
113. Rojas, R.,, T. van Vlijmen,, G. A. Mardones,, Y. Prabhu,, A. L. Rojas,, S. Mohammed,, A. J. Heck,, G. Raposo,, P. van der Sluijs,, J. S. Bonifacino. 2008. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183:513526.
114. Saito-Nakano, Y.,, B. N. Mitra,, K. Nakada-Tsukui, D. Sato, and, T. Nozaki. 2007. Two Rab7 isotypes, EhRab7A and EhRab7B, play distinct roles in biogenesis of lysosomes and phagosomes in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol. 9:17961808.
115. Saito-Nakano, Y.,, B. J. Loftus,, N. Hall, and, T. Nozaki. 2005. The diversity of Rab GTPases in Entamoeba histolytica. Exp. Parasitol. 110:244252.
116. Saito-Nakano, Y.,, T. Yasuda,, K. Nakada-Tsukui, M. Leippe, and, T. Nozaki. 2004. Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. J. Biol. Chem. 279:4949749507.
117. Sajid, M., and, J. H. McKerrow. 2002. Cysteine proteases of parasitic organisms. Mol. Biochem. Parasitol. 120:121.
118. Sanchez, L.,, V. Enea, and, D. Eichinger. 1994. Identification of a developmentally regulated transcript expressed during encystation of Entamoeba invadens. Mol. Biochem. Parasitol. 67:125135.
119. Schulte, W., and, H. Scholze. 1989. Action of the major protease from Entamoeba histolytica on proteins of the extracellular matrix. J. Protozool. 6:538543.
120. Shah, P. H.,, R. C. MacFarlane,, D. Bhattacharya,, J. C. Ma-tese,, J. Demeter,, S. E. Stroup, and, U. Singh. 2005. Comparative genomic hybridizations of Entamoeba strains reveal unique genetic fingerprints that correlate with virulence. Eukaryot. Cell 4:504515.
121. Sharma, R.,, A. Bagchi,, A. Bhattacharya, and, S. B hattacharya. 2001. Characterization of a retrotransposon-like element from Entamoeba histolytica. Mol. Biochem. Parasitol. 116:4553.
122. Shire, A. M., and, J. P. Ackers. 2007. SINE elements of Entamoeba dispar. Mol. Biochem. Parasitol. 152:4752.
123. Singh, U.,, C. A. Gilchrist,, J. M. Schaenman,, J. B. Rogers,, J. W. Hockensmith,, B. J. Mann, and, W. A. Petri. 2002. Context-dependent roles of the Entamoeba histolytica core promoter element GAAC in transcriptional activation and protein complex assembly. Mol. Biochem. Parasitol. 120:107116.
124. Singh, U., and, J. B. Rogers. 1998. The novel core promoter element GAAC in the hgl5 gene of Entamoeba histolytica is able to direct a transcription start site independent of TATA or initiator regions. J. Biol. Chem. 273:2166321668.
125. Singh, U.,, J. B. Rogers,, B. J. Mann, and, W. A. Petri, Jr. 1997. Transcription initiation is controlled by three core promoter elements in the hgl5 gene of the protozoan parasite Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 94:88128817.
126. Smith, M.,, V. Bhaskar,, J. Fernandez, and, A. J. Courey. 2004. Drosophila Ulp1, a nuclear pore-associated SUMO protease, prevents accumulation of cytoplasmic SUMO conjugates. J. Biol. Chem. 279:4380543814.
127. Stanley, S. L.,, Jr.,. T. Zhang,, D. Rubin, and, E. Li. 1995. Role of the Entamoeba histolytica cysteine proteinase in amebic liver abscess formation in severe combined immunodeficient mice. Infect. Immun. 63:15871590.
128. Stauffer, W., and, J. I. Ravdin. 2003. Entamoeba histolytica: an update. Curr. Opin. Infect. Dis. 16:479485.
129. Suzuki, J.,, S. Kobayashi,, I. Iku,, R. Murata,, Y. Yanagawa, and, T. Takeuchi. 2008. Seroprevalence of Entamoeba histolytica infection in female outpatients at a sexually transmitted disease sentinel clinic in Tokyo, Japan. Jpn. J. Infect. Dis. 61:175178.
130. Takai, Y.,, T. Sasaki, and, T. Matozaki. 2001. Small GTP-binding proteins. Physiol. Rev. 81:153208.
131. Tanyuksel, M.,, M. Ulukanligil,, Z. Guclu,, E. Araz,, O. Koru, and, W. A. Petri, Jr. 2007. Two cases of rarely recognized infection with Entamoeba moshkovskii. Am. J. Trop. Med. Hyg. 76:723724.
132. Tanyuksel, M., and, W. A. Petri, Jr. 2003. Laboratory diagnosis of amebiasis. Clin. Microbiol. Rev. 16:713729.
133. Tazreiter, M.,, D. Leitsch,, E. Hatzenbichler,, G. E. Mair-Scorpio,, R. Steinborn,, M. Schreiber, and, M. Duchêne. 2008. Entamoeba histolytica: response of the parasite to metron-idazole challenge on the levels of mRNA and protein expression. Exp. Parasitol. 120:403410.
134. 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.
135. 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. 149:5864.
136. Tokoro, M.,, T. Asai,, S. Kobayashi,, T. Takeuchi, and, T. Nozaki. 2003. Identification and characterization of two isoenzymes of methionine gamma-lyase from Entamoeba histolytica: a key enzyme of sulfur-amino acid degradation in an anaerobic parasitic protist that lacks forward and reverse trans-sulfuration pathways. J. Biol. Chem. 278:4271742727.
137. Tolstrup, J.,, E. Krause,, E. Tannich, and, I. Bruchhaus. 2007. Proteomic analysis of Entamoeba histolytica. Parasitology 34:289298.
138. Touz, M. C.,, M. J. Nores,, I. Slavin,, C. Carmona,, J. T. Conrad,, M. R. Mowatt,, T. E. Nash,, C. E. Coronel, and, H. D. Luján. 2002. The activity of a developmentally regulated cysteine proteinase is required for cyst wall formation in the primitive eukaryote Giardia lamblia. J. Biol. Chem. 277:84748481.
139. Tshalaia, L. E. 1941. On a species of Entamoeba detected in sewage effluents. Med. Parazit. (Moscow) 10:244252.
140. Vanacova, S.,, D. R. Liston,, J. Tachezy, and, P. J. Johnson. 2003. Molecular biology of the amitochondriate parasites, Giardia intestinalis, Entamoeba histolytica and Trichomonas vaginalis. Int. J. Parasitol. 33:235255.
141. Vargas, M., and, C. H. Gonzalez-de la Rosa. 2007. Structural and functional organization of the RhoGEF proteins from Entamoeba histolytica, p. 339-359. In L. I. Terrazes (ed.), Advances in the Immunobiology of Parasitic Diseases. Research Signpost, Kerala, India.
142. Vayssié, L.,, M. Vargas,, C. Weber, and, N. Guillén. 2004. Double-stranded RNA mediates homology-dependent gene silencing of gamma-tubulin in the human parasite Entamoeba histolytica. Mol. Biochem. Parasitol. 138:2128.
143. Vicente, J. B.,, G. M. Ehrenkaufer,, L. M. Saraiva,, M. Teixeira, and, U. Singh. 2009. Entamoeba histolytica modulates a complex repertoire of novel genes in response to oxidative and nitrosative stresses: implications for amebic pathogen-esis. Cell Microbiol. 11:5169.
144. Weber, C.,, L. A. Marchat,, N. Guillen, and, C. López-Camarillo. 2009. Effects of DNA damage induced by UV irradiation on gene expression in the protozoan parasite Entamoeba histolytica. Mol. Biochem. Parasitol. 164:165169.
145. Weber, C.,, G. Guigon,, C. Bouchier,, L. Frangeul,, S. Moreira,, O. Sismeiro,, C. Gouyette,, D. Mirelman,, J. Y. Coppee, and, N. Guillén. 2006. Stress by heat shock induces massive down regulation of genes and allows differential allelic expression of the Gal/GalNAc lectin in Entamoeba histolytica. Eukaryot. Cell 5:871875.
146. Welter, B. H., and, L. A. Temesvari. 2009. Overexpression of a mutant form of EhRabA, a unique Rab GTPase of Entamoeba histolytica, alters endoplasmic reticulum morphology and localization of the Gal/GalNAc adherence lectin. Eukaryot. Cell 8:10141026.
147. Welter, B. H.,, R. R. Powell,, M. Leo,, C. M. Smith, and, L. A. Temesvari. 2005. A unique Rab GTPase, EhRabA, is involved in motility and polarization of Entamoeba histolytica cells. Mol. Biochem. Parasitol. 140:161173.
148. Willhoeft, U., and, E. Tannich. 1999. The electrophoretic karyotype of Entamoeba histolytica. Mol. Biochem. Parasitol. 99:4153.
149. Yoshimori, T. 2004. Autophagy: a regulated bulk degradation process inside cells. Biochem. Biophys. Res. Commun. 313:453458.
150. Zhang, X.,, Z. Zhang,, D. Alexander,, R. Bracha,, D. Mirelman, and, S. L. Stanley, Jr. 2004. Expression of amoebapores is required for full expression of Entamoeba histolytica virulence in amebic liver abscess but is not necessary for the induction of inflammation or tissue damage in amebic colitis. Infect. Immun. 72:678683.
151. Zhang, J. 2000. Protein-length distributions for the three domains of life. Trends Genet. 16:107109.


Generic image for table
Table 1

CPs from and

Citation: Nakada-Tsukui K, Nozaki T. 2011. Genomic and Postgenomic Approaches to Understanding the Pathogenesis of the Enteric Protozoan Parasite , p 321-341. In Fratamico P, Liu Y, Kathariou S (ed), Genomes of Foodborne and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816902.ch23
Generic image for table
Table 2

Rab genes from and

Citation: Nakada-Tsukui K, Nozaki T. 2011. Genomic and Postgenomic Approaches to Understanding the Pathogenesis of the Enteric Protozoan Parasite , p 321-341. In Fratamico P, Liu Y, Kathariou S (ed), Genomes of Foodborne and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816902.ch23

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