- Introduction
- Material and Methods
- Ethics statement.
- Entamoeba histolytica (HM-1:IMSS) amebic culture.
- Membrane protein extraction.
- Protein digestion and iTRAQ labeling.
- Nano-liquid chromatography coupling MALDI-MS/MS analysis.
- Nano-liquid chromatography coupling electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis.
- Database search, criteria, and parameters.
- Cytosolic fraction.
- Gene ontology, membrane protein prediction, and protein–protein interaction prediction.
- Results
- Protein identification.
- Cytosolic fraction.
- Differentially abundant proteins.
- Virulent versus avEh membrane proteins with increased abundance.
- Functional analysis of the membrane proteins with increased abundance.
- Virulent versus avEh membrane proteins with decreased abundance.
- Functional analysis of the membrane proteins with decreased abundance.
- Protein–protein interaction prediction among differentially abundant membrane proteins.
- Discussion
- Supplementary Material
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Samie A, ElBakri A, AbuOdeh RE, 2012. Amoebiasis in the tropics: epidemiology and pathogenesis. Rodriguez-Morales AJ, ed. Current Topics in Tropical Medicine. London, United Kingdom: IntechOpen, 201–226.
-
2.
Boettner DR, Huston C, Petri WA, 2002. Galactose/N-acetylgalactosamine lectin: the coordinator of host cell killing. J Biosci 27: 553–557.
-
3.
Mann BJ, 2002. Structure and function of the Entamoeba histolytica Gal/GalNAc lectin. Int Rev Cytol 216: 59–80.
-
4.
DeMeester F, Shaw E, Scholze H, Stolarsky T, Mirelman D, 1990. Specific labeling of cysteine proteinases in pathogenic and non-pathogenic Entamoeba histolytica. Infect Immun 58: 1396–1401.
-
5.
Mortimer L, Chadee K, 2010. The immunopathogenesis of Entamoeba histolytica .Exp Parasitol 126: 366–380.
-
6.
Laughlin RC, Temesvari LA, 2005. Cellular and molecular mechanisms that underlie Entamoeba histolytica pathogenesis: prospects for intervention. Expert Rev Mol Med 7: 1–19.
-
7.
Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J, 2000. Molecular Cell Biology, 4th edition. Bethesda, Maryland: National Center for Biotechnology Information, Bookshelf.
-
8.
Krogh A, Larsson B, Von Heijne G, Sonnhammer EL, 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes1. J Mol Biol 305: 567–580.
-
9.
Tsirigos K, 2017. Bioinformatics methods for topology prediction of membrane proteins. Doctoral Dissertation, Department of Biochemistry and Biophysics, Stockholm University. Available at: http://www.diva-portal.org/smash/record.jsf?pid=diva2%3A1067468&dswid=-4009. Accessed May 11, 2018.
-
10.
Nozaki T, Nakada-Tsukui K, 2006. Membrane trafficking as a virulence mechanism of the enteric protozoan parasite Entamoeba histolytica .Parasitol Res 98: 179–183.
-
11.
Stuart LM, Ezekowitz RAB, 2005. Phagocytosis: elegant complexity. Immunity 22: 539–550.
-
12.
Loftus B, Anderson I, Davies R, Alsmark UCM, 2005. The genome of the protist parasite Entamoeba histolytica .Nature 433: 865–868.
-
13.
Perdomo D, Aït-Ammar N, Syan S, Sachse M, Jhingan GD, Guillén N, 2015. Cellular and proteomics analysis of the endomembrane system from the unicellular Entamoeba histolytica .J Proteomics 112: 125–140.
-
14.
Biller L et al. 2014. The cell surface proteome of Entamoeba histolytica .Mol Cell Proteomics 13: 132–144.
-
15.
Diamond LS, Clark CG, Cunnick CC, 1995. YI-S, a casein-free medium for axenic cultivation of Entamoeba histolytica, related Entamoeba, Giardia intestinalis and Trichomonas vaginalis .J Eukaryot Microbiol 42: 277–278.
-
16.
Olivos A, Ramos E, Nequiz M, Barba C, Tello E, Castañón G, González A, Martínez RD, Montfort I, Pérez-Tamayo R, 2005. Entamoeba histolytica: mechanism of decrease of virulence of axenic cultures maintained for prolonged periods. Exp Parasitol 110: 309–312.
-
17.
Santos F et al. 2015. Maintenance of intracellular hypoxia and adequate heat shock response are essential requirements for pathogenicity and virulence of Entamoeba histolytica .Cell Microbiol 17: 1037–1051.
-
18.
Ujang JA, Kwan SH, Ismail MN, Lim BH, Noordin R, Othman N, 2016. Proteome analysis of excretory-secretory proteins of Entamoeba histolytica HM1: IMSS via LC–ESI–MS/MS and LC–MALDI–TOF/TOF. Clin Proteomics 13: 33.
-
19.
Bodnar WM, Blackburn RK, Krise JM, Moseley MA, 2003. Exploiting the complementary nature of LC/MALDI/MS/MS and LC/ESI/MS/MS for increased proteome coverage. J Am Soc Mass Spectrom 14: 971–979.
-
20.
Davis PH, Zhang X, Guo J, Townsend RR, Stanley SL, 2006. Comparative proteomic analysis of two Entamoeba histolytica strains with different virulence phenotypes identifies peroxiredoxin as an important component of amoebic virulence. Mol Microbiol 61: 1523–1532.
-
21.
Davis PH, Chen M, Zhang X, Clark CG, Townsend RR, Stanley SL Jr., 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.
-
22.
Williams RB, Chan EK, Cowley MJ, Little PF, 2007. The influence of genetic variation on gene expression. Genome Res 17: 1707–1716.
-
23.
Bosch DE, Siderovski DP, 2013. G protein signaling in the parasite Entamoeba histolytica .Exp Mol Med 45: e15.
-
24.
Gilchrist CA et al. 2006. Impact of intestinal colonization and invasion on the Entamoeba histolytica transcriptome. Mol Biochem Parasitol 147: 163–176.
-
25.
Thibeaux R, Weber C, Hon CC, Dillies MA, Avé P, Coppée JY, Labruyère E, Guillén N, 2013. Identification of the virulence landscape essential for Entamoeba histolytica invasion of the human colon. PLoS Pathog 9: e1003824.
-
26.
Hoek JB, Rydström J, 1988. Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem J 254: 1–10.
-
27.
Okada M, Nozaki T, 2006. New insights into molecular mechanisms of phagocytosis in Entamoeba histolytica by proteomic analysis. Arch Med Res 37: 244–251.
-
28.
Descoteaux S, Ayala P, Orozco E, Samuelson J, 1992. Primary sequences of two P-glycoprotein genes of Entamoeba histolytica .Mol Biochem Parasitol 54: 201–211.
-
29.
Ouellette M, Légaré D, Papadopoulou B, 2001. Multidrug resistance and ABC transporters in parasitic protozoa. J Mol Microbiol Biotechnol 3: 201–206.
-
30.
Orozco E, Lopez C, Gomez C, Perez DG, Marchat L, Banuelos C, Delgadillo DM, 2002. Multidrug resistance in the protozoan parasite Entamoeba histolytica .Parasitol Int 51: 353–359.
-
31.
Bansal D, Sehgal R, Chawla Y, Malla N, Mahajan RC, 2006. Multidrug resistance in amoebiasis patients. Indian J Med Res 124: 189–194.
-
32.
Alekshun MN, Levy SB, 2007. Molecular mechanisms of antibacterial multidrug resistance. Cell 128: 1037–1050.
-
33.
Li XZ, Nikaido H, 2009. Efflux-mediated drug resistance in bacteria. Drugs 69: 1555–1623.
-
34.
Nikaido H, 2009. Multidrug resistance in bacteria. Annu Rev Biochem 78: 119–146.
-
35.
Michalak M, Corbett EF, Mesaeli N, Nakamura K, Opas M, 1999. Calreticulin: one protein, one gene, many functions. Biochem J 344: 281–292.
-
36.
González E et al. 2011. Entamoeba histolytica calreticulin: an endoplasmic reticulum protein expressed by trophozoites into experimentally induced amoebic liver abscesses. Parasitol Res 108: 439–449.
-
37.
González E, Rico G, Mendoza G, Ramos F, García G, Morán P, Valadez A, Melendro EI, Ximénez C, 2002. Calreticulin-like molecule in trophozoites of Entamoeba histolytica HM1: IMSS (Swissprot: accession P83003). Am J Trop Med Hyg 67: 636–639.
-
38.
Ximénez C et al. 2014. Entamoeba histolytica and E. dispar calreticulin: inhibition of classical complement pathway and differences in the level of expression in amoebic liver abscess. Biomed Res Int 2014: 127453.
-
39.
Riekenberg S, Flockenhaus B, Vahrmann A, Müller MC, Leippe M, Kieß M, Scholze H, 2004. The beta-N-acetylhexosaminidase of Entamoeba histolytica is composed of two homologous chains and has been localized to cytoplasmic granules. Mol Biochem Parasitol 138: 217–225.
-
40.
Moncada D, Keller K, Chadee K, 2005. Entamoeba histolytica-secreted products degrade colonic mucin oligosaccharides. Infect Immun 73: 3790–3793.
-
41.
Riahi Y, Ankri S, 2000. Involvement of serine proteinases during encystation of Entamoeba invadens .Arch Med Res 31: S187–S189.
-
42.
Makioka A, Kumagai M, Kobayashi S, Takeuchi T, 2009. Involvement of serine proteases in the excystation and metacystic development of Entamoeba invadens .Parasitol Res 105: 977–987.
-
43.
Markiewicz JM, 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: e1002.
-
44.
Wong H, Schotz MC, 2002. The lipase gene family. J lipid Res 43: 993–999.
-
45.
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: 170.
-
46.
Touz MC, Nores MJ, Slavin I, Piacenza L, Acosta D, Carmona C, Luján HD, 2002. Membrane-associated dipeptidyl peptidase IV is involved in encystation-specific gene expression during Giardia differentiation. Biochem J 364: 703–710.
-
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Gething MJ, Sambrook J, 1992. Protein folding in the cell. Nature 355: 33–45.
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48.
Tovy A, Hertz R, Siman-Tov R, Syan S, Faust D, Guillen N, Ankri S, 2011. Glucose starvation boosts Entamoeba histolytica virulence. PLoS Negl Trop Dis 5: e1247.
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Furukawa A, Nakada-Tsukui K, Nozaki T, 2013. Cysteine protease-binding protein family 6 mediates the trafficking of amylases to phagosomes in the enteric protozoan Entamoeba histolytica .Infect Immun 81: 1820–1829.
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Entamoeba histolytica: Quantitative Proteomics Analysis Reveals Putative Virulence-Associated Differentially Abundant Membrane Proteins
Yee Ling Ng
Yee Ling Ng
Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia, Penang, Malaysia;
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Alfonso Olivos-García
Alfonso Olivos-García
Departamento de Medicina Experimental, Facultad de Medicina, Universidad Nacional Autónoma de México, México D.F., Mexico;
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Teck Kwang Lim
Teck Kwang Lim
Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore
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Rahmah Noordin
Rahmah Noordin
Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia, Penang, Malaysia;
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Qingsong Lin
Qingsong Lin
Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore
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Nurulhasanah Othman
Nurulhasanah Othman
Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia, Penang, Malaysia;
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Entamoeba histolytica is a protozoan parasite that causes amebiasis and poses a significant health risk for populations in endemic areas. The molecular mechanisms involved in the pathogenesis and regulation of the parasite are not well characterized. We aimed to identify and quantify the differentially abundant membrane proteins by comparing the membrane proteins of virulent and avirulent variants of E. histolytica HM-1:IMSS, and to investigate the potential associations among the differentially abundant membrane proteins. We performed quantitative proteomics analysis using isobaric tags for relative and absolute quantitation labeling, in combination with two mass spectrometry instruments, that is, nano-liquid chromatography (nanoLC)-matrix-assisted laser desorption/ionization-mass spectrometry/mass spectrometry and nanoLC-electrospray ionization tandem mass spectrometry. Overall, 37 membrane proteins were found to be differentially abundant, whereby 19 and 18 membrane proteins of the virulent variant of E. histolytica increased and decreased in abundance, respectively. Proteins that were differentially abundant include Rho family GTPase, calreticulin, a 70-kDa heat shock protein, and hypothetical proteins. Analysis by Protein ANalysis THrough Evolutionary Relationships database revealed that the differentially abundant membrane proteins were mainly involved in catalytic activities (29.7%) and metabolic processes (32.4%). Differentially abundant membrane proteins that were found to be involved mainly in the catalytic activities and the metabolic processes were highlighted together with their putative roles in relation to the virulence. Further investigations should be performed to elucidate the roles of these proteins in E. histolytica pathogenesis.
- Supplemental Materials (PDF 109 KB)
Author Notes
Authors’ addresses: Yee Ling Ng, Rahmah Noordin, and Nurulhasanah Othman, Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia, Penang, Malaysia, E-mails: elyne_ng23@hotmail.com, rahmah8485@gmail.com, and nurulhasanah@usm.my. Alfonso Olivos-García, Departamento de Medicina Experimental, Facultad de Medicina, Universidad Nacional Autónoma de México, México D.F., Mexico, E-mail: olivosa@yahoo.com. Teck Kwang Lim and Qingsong Lin, Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore, E-mails: dbslimtk@nus.edu.sg and dbslinqs@nus.edu.sg.
- Introduction
- Material and Methods
- Ethics statement.
- Entamoeba histolytica (HM-1:IMSS) amebic culture.
- Membrane protein extraction.
- Protein digestion and iTRAQ labeling.
- Nano-liquid chromatography coupling MALDI-MS/MS analysis.
- Nano-liquid chromatography coupling electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis.
- Database search, criteria, and parameters.
- Cytosolic fraction.
- Gene ontology, membrane protein prediction, and protein–protein interaction prediction.
- Results
- Protein identification.
- Cytosolic fraction.
- Differentially abundant proteins.
- Virulent versus avEh membrane proteins with increased abundance.
- Functional analysis of the membrane proteins with increased abundance.
- Virulent versus avEh membrane proteins with decreased abundance.
- Functional analysis of the membrane proteins with decreased abundance.
- Protein–protein interaction prediction among differentially abundant membrane proteins.
- Discussion
- Supplementary Material
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Samie A, ElBakri A, AbuOdeh RE, 2012. Amoebiasis in the tropics: epidemiology and pathogenesis. Rodriguez-Morales AJ, ed. Current Topics in Tropical Medicine. London, United Kingdom: IntechOpen, 201–226.
-
2.
Boettner DR, Huston C, Petri WA, 2002. Galactose/N-acetylgalactosamine lectin: the coordinator of host cell killing. J Biosci 27: 553–557.
-
3.
Mann BJ, 2002. Structure and function of the Entamoeba histolytica Gal/GalNAc lectin. Int Rev Cytol 216: 59–80.
-
4.
DeMeester F, Shaw E, Scholze H, Stolarsky T, Mirelman D, 1990. Specific labeling of cysteine proteinases in pathogenic and non-pathogenic Entamoeba histolytica. Infect Immun 58: 1396–1401.
-
5.
Mortimer L, Chadee K, 2010. The immunopathogenesis of Entamoeba histolytica .Exp Parasitol 126: 366–380.
-
6.
Laughlin RC, Temesvari LA, 2005. Cellular and molecular mechanisms that underlie Entamoeba histolytica pathogenesis: prospects for intervention. Expert Rev Mol Med 7: 1–19.
-
7.
Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J, 2000. Molecular Cell Biology, 4th edition. Bethesda, Maryland: National Center for Biotechnology Information, Bookshelf.
-
8.
Krogh A, Larsson B, Von Heijne G, Sonnhammer EL, 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes1. J Mol Biol 305: 567–580.
-
9.
Tsirigos K, 2017. Bioinformatics methods for topology prediction of membrane proteins. Doctoral Dissertation, Department of Biochemistry and Biophysics, Stockholm University. Available at: http://www.diva-portal.org/smash/record.jsf?pid=diva2%3A1067468&dswid=-4009. Accessed May 11, 2018.
-
10.
Nozaki T, Nakada-Tsukui K, 2006. Membrane trafficking as a virulence mechanism of the enteric protozoan parasite Entamoeba histolytica .Parasitol Res 98: 179–183.
-
11.
Stuart LM, Ezekowitz RAB, 2005. Phagocytosis: elegant complexity. Immunity 22: 539–550.
-
12.
Loftus B, Anderson I, Davies R, Alsmark UCM, 2005. The genome of the protist parasite Entamoeba histolytica .Nature 433: 865–868.
-
13.
Perdomo D, Aït-Ammar N, Syan S, Sachse M, Jhingan GD, Guillén N, 2015. Cellular and proteomics analysis of the endomembrane system from the unicellular Entamoeba histolytica .J Proteomics 112: 125–140.
-
14.
Biller L et al. 2014. The cell surface proteome of Entamoeba histolytica .Mol Cell Proteomics 13: 132–144.
-
15.
Diamond LS, Clark CG, Cunnick CC, 1995. YI-S, a casein-free medium for axenic cultivation of Entamoeba histolytica, related Entamoeba, Giardia intestinalis and Trichomonas vaginalis .J Eukaryot Microbiol 42: 277–278.
-
16.
Olivos A, Ramos E, Nequiz M, Barba C, Tello E, Castañón G, González A, Martínez RD, Montfort I, Pérez-Tamayo R, 2005. Entamoeba histolytica: mechanism of decrease of virulence of axenic cultures maintained for prolonged periods. Exp Parasitol 110: 309–312.
-
17.
Santos F et al. 2015. Maintenance of intracellular hypoxia and adequate heat shock response are essential requirements for pathogenicity and virulence of Entamoeba histolytica .Cell Microbiol 17: 1037–1051.
-
18.
Ujang JA, Kwan SH, Ismail MN, Lim BH, Noordin R, Othman N, 2016. Proteome analysis of excretory-secretory proteins of Entamoeba histolytica HM1: IMSS via LC–ESI–MS/MS and LC–MALDI–TOF/TOF. Clin Proteomics 13: 33.
-
19.
Bodnar WM, Blackburn RK, Krise JM, Moseley MA, 2003. Exploiting the complementary nature of LC/MALDI/MS/MS and LC/ESI/MS/MS for increased proteome coverage. J Am Soc Mass Spectrom 14: 971–979.
-
20.
Davis PH, Zhang X, Guo J, Townsend RR, Stanley SL, 2006. Comparative proteomic analysis of two Entamoeba histolytica strains with different virulence phenotypes identifies peroxiredoxin as an important component of amoebic virulence. Mol Microbiol 61: 1523–1532.
-
21.
Davis PH, Chen M, Zhang X, Clark CG, Townsend RR, Stanley SL Jr., 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.
-
22.
Williams RB, Chan EK, Cowley MJ, Little PF, 2007. The influence of genetic variation on gene expression. Genome Res 17: 1707–1716.
-
23.
Bosch DE, Siderovski DP, 2013. G protein signaling in the parasite Entamoeba histolytica .Exp Mol Med 45: e15.
-
24.
Gilchrist CA et al. 2006. Impact of intestinal colonization and invasion on the Entamoeba histolytica transcriptome. Mol Biochem Parasitol 147: 163–176.
-
25.
Thibeaux R, Weber C, Hon CC, Dillies MA, Avé P, Coppée JY, Labruyère E, Guillén N, 2013. Identification of the virulence landscape essential for Entamoeba histolytica invasion of the human colon. PLoS Pathog 9: e1003824.
-
26.
Hoek JB, Rydström J, 1988. Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem J 254: 1–10.
-
27.
Okada M, Nozaki T, 2006. New insights into molecular mechanisms of phagocytosis in Entamoeba histolytica by proteomic analysis. Arch Med Res 37: 244–251.
-
28.
Descoteaux S, Ayala P, Orozco E, Samuelson J, 1992. Primary sequences of two P-glycoprotein genes of Entamoeba histolytica .Mol Biochem Parasitol 54: 201–211.
-
29.
Ouellette M, Légaré D, Papadopoulou B, 2001. Multidrug resistance and ABC transporters in parasitic protozoa. J Mol Microbiol Biotechnol 3: 201–206.
-
30.
Orozco E, Lopez C, Gomez C, Perez DG, Marchat L, Banuelos C, Delgadillo DM, 2002. Multidrug resistance in the protozoan parasite Entamoeba histolytica .Parasitol Int 51: 353–359.
-
31.
Bansal D, Sehgal R, Chawla Y, Malla N, Mahajan RC, 2006. Multidrug resistance in amoebiasis patients. Indian J Med Res 124: 189–194.
-
32.
Alekshun MN, Levy SB, 2007. Molecular mechanisms of antibacterial multidrug resistance. Cell 128: 1037–1050.
-
33.
Li XZ, Nikaido H, 2009. Efflux-mediated drug resistance in bacteria. Drugs 69: 1555–1623.
-
34.
Nikaido H, 2009. Multidrug resistance in bacteria. Annu Rev Biochem 78: 119–146.
-
35.
Michalak M, Corbett EF, Mesaeli N, Nakamura K, Opas M, 1999. Calreticulin: one protein, one gene, many functions. Biochem J 344: 281–292.
-
36.
González E et al. 2011. Entamoeba histolytica calreticulin: an endoplasmic reticulum protein expressed by trophozoites into experimentally induced amoebic liver abscesses. Parasitol Res 108: 439–449.
-
37.
González E, Rico G, Mendoza G, Ramos F, García G, Morán P, Valadez A, Melendro EI, Ximénez C, 2002. Calreticulin-like molecule in trophozoites of Entamoeba histolytica HM1: IMSS (Swissprot: accession P83003). Am J Trop Med Hyg 67: 636–639.
-
38.
Ximénez C et al. 2014. Entamoeba histolytica and E. dispar calreticulin: inhibition of classical complement pathway and differences in the level of expression in amoebic liver abscess. Biomed Res Int 2014: 127453.
-
39.
Riekenberg S, Flockenhaus B, Vahrmann A, Müller MC, Leippe M, Kieß M, Scholze H, 2004. The beta-N-acetylhexosaminidase of Entamoeba histolytica is composed of two homologous chains and has been localized to cytoplasmic granules. Mol Biochem Parasitol 138: 217–225.
-
40.
Moncada D, Keller K, Chadee K, 2005. Entamoeba histolytica-secreted products degrade colonic mucin oligosaccharides. Infect Immun 73: 3790–3793.
-
41.
Riahi Y, Ankri S, 2000. Involvement of serine proteinases during encystation of Entamoeba invadens .Arch Med Res 31: S187–S189.
-
42.
Makioka A, Kumagai M, Kobayashi S, Takeuchi T, 2009. Involvement of serine proteases in the excystation and metacystic development of Entamoeba invadens .Parasitol Res 105: 977–987.
-
43.
Markiewicz JM, 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: e1002.
-
44.
Wong H, Schotz MC, 2002. The lipase gene family. J lipid Res 43: 993–999.
-
45.
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: 170.
-
46.
Touz MC, Nores MJ, Slavin I, Piacenza L, Acosta D, Carmona C, Luján HD, 2002. Membrane-associated dipeptidyl peptidase IV is involved in encystation-specific gene expression during Giardia differentiation. Biochem J 364: 703–710.
-
47.
Gething MJ, Sambrook J, 1992. Protein folding in the cell. Nature 355: 33–45.
-
48.
Tovy A, Hertz R, Siman-Tov R, Syan S, Faust D, Guillen N, Ankri S, 2011. Glucose starvation boosts Entamoeba histolytica virulence. PLoS Negl Trop Dis 5: e1247.
-
49.
Gupta RS, Golding GB, 1993. Evolution of HSP70 gene and its implications regarding relationships between archaebacteria, eubacteria, and eukaryotes. J Mol Evol 37: 573–582.
-
50.
Lo H, Reeves RE, 1978. Pyruvate-to-ethanol pathway in Entamoeba histolytica .Biochem J 171: 225–230.
-
51.
Harding JJW, Pyeritz EA, Copeland ES, White HB, 1975. Role of glycerol 3-phosphate dehydrogenase in glyceride metabolism. Effect of diet on enzyme activities in chicken liver. Biochem J 146: 223–229.
-
52.
Furukawa A, Nakada-Tsukui K, Nozaki T, 2013. Cysteine protease-binding protein family 6 mediates the trafficking of amylases to phagosomes in the enteric protozoan Entamoeba histolytica .Infect Immun 81: 1820–1829.
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