Members of the Entamoeba histolytica transmembrane kinase family play non-redundant roles in growth and phagocytosis

International Journal for Parasitology

Volumn 40, Issue 7, 2010, Pages 833-843

  Buss, Sarah N ^a   Hamano, Shinjiro ^b   Vidrich, Alda ^c   Evans, Clive ^d   Zhang, Yan ^d   Crasta, Oswald R ^d   Sobral, Bruno W ^d   Gilchrist, Carol A ^a   Petri, William A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b NAGASAKI UNIVERSITY   (Japan)

^c UNIVERSITY OF VIRGINIA   (United States)

^d VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

Author keywords

Entamoeba histolytica; Laser capture microdissection; Lectin; Phagocytosis; Transmembrane kinase

Indexed keywords

PEPTIDE ANTIBODY; PROTOZOAL PROTEIN; TRANSMEMBRANE KINASE; TRANSMEMBRANE KINASE 39; TRANSMEMBRANE KINASE 54; UNCLASSIFIED DRUG;

ANTIBODY; BIOASSAY; BIOCHEMISTRY; FLOW CYTOMETRY; GENETIC ANALYSIS; INHIBITION; MEMBRANE; PARASITE; PEPTIDE; PROTOZOAN;

ARTICLE; CELL FUNCTION; CELL SURFACE; CONFOCAL MICROSCOPY; ENTAMOEBA HISTOLYTICA; ENZYME LOCALIZATION; FLOW CYTOMETRY; LASER CAPTURE MICRODISSECTION; LYMPHOCYTE; MICROARRAY ANALYSIS; MICROBIAL GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; TROPHOZOITE;

ENTAMOEBA HISTOLYTICA; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHAGOCYTOSIS; PROTOZOAN PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES;

ENTAMOEBA HISTOLYTICA;

EID: 77952525256     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2009.12.007     Document Type: Article

References (50)

1. Adam R.D., Aggarwal A., Lal A.A., de La Cruz V.F., McCutchan T., Nash T.E. Antigenic variation of a cysteine-rich protein in Giardia lamblia. J. Exp. Med. 1988, 167:109-118.
2. Aley S.B., Scott W.A., Cohn Z.A. Plasma membrane of Entamoeba histolytica. J. Exp. Med. 1980, 152:391-404.
3. Barrett T., Suzek T.O., Troup D.B., Wilhite S.E., Ngau W., Ledoux P., Rudnev D., Lash A.E., Fujibuchi W., Edgar R. NCBI GEO: mining millions of expression profiles - database and tools. Nucleic Acids Res. 2005, 33:D562-566.
4. Beck D.L., Boettner D.R., Dragulev B., Ready K., Nozaki T., Petri W.A. Identification and gene expression analysis of a large family of transmembrane kinases related to the Gal/GalNAc lectin in Entamoeba histolytica. Eukaryotic Cell 2005, 4:722-732.
5. Boettner D.R., Huston C.D., Linford A.S., Buss S.N., Houpt E., Sherman N.E., Petri W.A. Entamoeba histolytica phagocytosis of human erythrocytes involves PATMK, a member of the transmembrane kinase family. PLoS Pathog. 2008, 4:e8.
6. Boettner D.R., Huston C.D., Sullivan J.A., Petri W.A. Entamoeba histolytica and Entamoeba dispar utilize externalized phosphatidylserine for recognition and phagocytosis of erythrocytes. Infect. Immun. 2005, 73:3422-3430.
7. Borst P., Genest P. Parasitology: switching like for like. Nature 2006, 439:926-927.
8. Bratosin D., Estaquier J., Petit F., Arnoult D., Quatannens B., Tissier J.P., Slomianny C., Sartiaux C., Alonso C., Huart J.J., Montreuil J., Ameisen J.C. Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria. Cell Death Differ. 2001, 8:1143-1156.
9. Calderón J., de Lourdes Muñoz M., Acosta H.M. Surface redistribution and release of antibody-induced caps in entamoebae. J. Exp. Med. 1980, 151:184-193.
10. Champion A., Kreis M., Mockaitis K., Picaud A., Henry Y. Arabidopsis kinome: after the casting. Funct. Integr. Genomics 2004, 4:163-187.
11. Diamond L.S. Axenic cultivation of Entamoeba histolytica 1961, Science, 134, 336-337.
12. Esumi S., Wu S., Yanagawa Y., Obata K., Sugimoto Y., Tamamaki N. Method for single-cell microarray analysis and application to gene-expression profiling of GABAergic neuron progenitors. Neurosci. Res. 2008, 60:439-451.
13. Gilchrist C.A., Houpt E., Trapaidze N., Fei Z., Crasta O., Asgharpour A., Evans C., Martino-Catt S., Baba D.J., Stroup S., Hamano S., Ehrenkaufer G., Okada M., Singh U., Nozaki T., Mann B.J., Petri W.A. Impact of intestinal colonization and invasion on the Entamoeba histolytica transcriptome. Mol. Biochem. Parasitol. 2006, 147:163-176.
14. Goldberg J.M., Manning G., Liu A., Fey P., Pilcher K.E., Xu Y., Smith J.L. The Dictyostelium kinome - analysis of the protein kinases from a simple model organism. PLoS Genet. 2006, 2:e38.
15. Grimsley C., Ravichandran K.S. Cues for apoptotic cell engulfment: eat-me, don't eat-me and come-get-me signals. Trends Cell Biol. 2003, 13:648-656.
16. Hamann L., Buss H., Tannich E. Tetracycline-controlled gene expression in Entamoeba histolytica. Mol. Biochem. Parasitol. 1997, 84:83-91.
17. Haque R., Ali I., Sack R., Farr B., Ramakrishnan G., Petri J. Amebiasis and mucosal IgA antibody against the Entamoeba histolytica adherence lectin in Bangladeshi children. J. Infect. Dis. 2001, 183:1787-1793.
18. Haque R., Duggal P., Ali I., Hossain M., Mondal D., Sack R., Farr B., Beaty T., Petri J. Innate and acquired resistance to amebiasis in Bangladeshi children. J. Infect. Dis. 2002, 186:547-552.
19. Heldin C. Dimerization of cell surface receptors in signal transduction. Cell 1995, 80:213-223.
20. Huston C.D., Boettner D.R., Miller-Sims V., Petri W.A. Apoptotic killing and phagocytosis of host cells by the parasite Entamoeba histolytica. Infect. Immun. 2003, 71:964-972.
21. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., Speed T.P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
22. King N., Carroll S.B. A receptor tyrosine kinase from choanoflagellates: molecular insights into early animal evolution. Proc. Natl. Acad. Sci. USA 2001, 98:15032-15037.
23. Kocks C., Cho J.H., Nehme N., Ulvila J., Pearson A.M., Meister M., Strom C., Conto S.L., Hetru C., Stuart L.M., Stehle T., Hoffmann J.A., Reichhart J., Ferrandon D., Rämet M., Ezekowitz R.A.B. Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 2005, 123:335-346.
24. Laughlin R.C., McGugan G.C., Powell R.R., Welter B.H., Temesvari L.A. Involvement of raft-like plasma membrane domains of Entamoeba histolytica in pinocytosis and adhesion. Infect. Immun. 2004, 72:5349-5357.
25. Lemmon M.A., Schlessinger J. Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem. Sci. 1994, 19:459-463.
26. Linggi B., Carpenter G. ErbB receptors: new insights on mechanisms and biology. Trends Cell Biol. 2006, 16:649-656.
27. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
28. Manning G., Young S.L., Miller W.T., Zhai Y. The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan. Proc. Natl. Acad. Sci. USA 2008, 105:9674-9679.
29. Marion S., Laurent C., Guillén N. Signalization and cytoskeleton activity through myosin IB during the early steps of phagocytosis in Entamoeba histolytica: a proteomic approach. Cell. Microbiol. 2005, 7:1504-1518.
30. Mehra A., Fredrick J., Petri W.A., Bhattacharya S., Bhattacharya A. Expression and function of a family of transmembrane kinases from the protozoan parasite Entamoeba histolytica. Infect. Immun. 2006, 74:5341-5351.
31. Naccache P., Jean N., Liao N., Bator J., McColl S., Kubes P. Regulation of stimulated integrin surface expression in human neutrophils by tyrosine phosphorylation. Blood 1994, 84:616-624.
32. Okada M., Huston C.D., Oue M., Mann B.J., Petri W.A., Kita K., Nozaki T. Kinetics and strain variation of phagosome proteins of Entamoeba histolytica by proteomic analysis. Mol. Biochem. Parasitol. 2006, 145:171-183.
33. Pani B., Singh B.B. Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium 2009, 45:625-633.
34. Parsons M., Worthey E.A., Ward P.N., Mottram J.C. Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 2005, 6:127.
35. Parton R.G., Hancock J.F. Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol. 2004, 14:141-147.
36. Petri W.A., Chapman M.D., Snodgrass T., Mann B.J., Broman J., Ravdin J.I. Subunit structure of the galactose and N-acetyl-d-galactosamine-inhibitable adherence lectin of Entamoeba histolytica. J. Biol. Chem. 1989, 264:3007-3012.
37. Petri W.A., Smith R.D., Schlesinger P.H., Murphy C.F., Ravdin J.I. Isolation of the galactose-binding lectin that mediates the in vitro adherence of Entamoeba histolytica. J. Clin. Invest. 1987, 80:1238-1244.
38. Petri W.A., Haque R., Mann B.J. The bittersweet interface of parasite and host: lectin-carbohydrate interactions during human invasion by the parasite Entamoeba histolytica. Annu. Rev. Microbiol. 2002, 56:39-64.
39. Pike L.J. Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J. Lipid Res. 2006, 47:1597-1598.
40. Ravdin J.I., Croft B.Y., Guerrant R.L. Cytopathogenic mechanisms of Entamoeba histolytica. J. Exp. Med. 1980, 152:377-390.
41. Roberts D.J., Craig A.G., Berendt A.R., Pinches R., Nash G., Marsh K., Newbold C.I. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 1992, 357:689-692.
42. Shiu S., Karlowski W.M., Pan R., Tzeng Y., Mayer K.F.X., Li W. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 2004, 16:1220-1234.
43. Somanath P.R., Ciocea A., Byzova T.V. Integrin and growth factor receptor alliance in angiogenesis. Cell Biochem. Biophys. 2009, 53:53-64.
44. Stockdale C., Swiderski M.R., Barry J.D., McCulloch R. Antigenic variation in Trypanosoma brucei: joining the DOTs. PLoS Biol. 2008, 6:e185.
45. Su X., Heatwole V.M., Wertheimer S.P., Guinet F., Herrfeldt J.A., Peterson D.S., Ravetch J.A., Wellems T.E. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum - infected erythrocytes. Cell 1995, 82:89-100.
46. Teixeira J.E., Huston C.D. Participation of the serine-rich Entamoeba histolytica protein in amebic phagocytosis of apoptotic host cells. Infect. Immun. 2008, 76:959-966.
47. Ueno H., Colbert H., Escobedo J.A., Williams L.T. Inhibition of PDGF β receptor signal transduction by coexpression of a truncated receptor. Sci., New Ser. 1991, 252:844-848.
48. Vines R.R., Ramakrishnan G., Rogers J.B., Lockhart L.A., Mann B.J., Petri W.A. Regulation of adherence and virulence by the Entamoeba histolytica lectin cytoplasmic domain, which contains a beta 2 integrin motif. Mol. Biol. Cell 1998, 9:2069-2079.
49. Ward P., Equinet L., Packer J., Doerig C. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 2004, 5:79.
50. WHO/PAHO/UNESCO. A consultation with experts on amoebiasis. Mexico City, Mexico 28-29 January, 1997. Epidemiol. Bull. 1997, 18:13-14.