EhLimA, a novel LIM protein, localizes to the plasma membrane in Entamoeba histolytica

Eukaryotic Cell

Volumn 6, Issue 9, 2007, Pages 1646-1655

  Wender, Nomy ^a   Villalobo, Eduardo ^b   Mirelman, David ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL MEMBRANE; CHEMISTRY; CYTOSKELETON; ENTAMOEBA HISTOLYTICA; GENE SILENCING; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CLONING, MOLECULAR; CYTOSKELETON; ENTAMOEBA HISTOLYTICA; GENE SILENCING; MEMBRANE MICRODOMAINS; MOLECULAR SEQUENCE DATA; PROTOZOAN PROTEINS;

DICTYOSTELIUM DISCOIDEUM; ENTAMOEBA HISTOLYTICA; PROTOZOA;

EID: 34748838917     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00177-07     Document Type: Article

References (57)

1. Abrami, L., and F. G. van Der Goot. 1999. Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J. Cell Biol. 147:175-184.
2. Algrain, M., O. Turunen, A. Vaheri, D. Louvard, and M. Arpin. 1993. Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker. J. Cell Biol. 120:129-139.
3. Ankri, S., F. Padilla-Vaca, T. Stolarsky, L. Koole, U. Katz, and D. Mirelman. 1999. Antisense inhibition of expression of the light subunit (35 kDa) of the Gal/GalNac lectin complex inhibits Entamoeba histolytica virulence. Mol. Microbiol. 33:327-337.
4. Bach, I. 2000. The LIM domain: regulation by association. Mech. Dev. 91:5-17.
5. Baltz, R., C. Demon, D. T. Pillay, and A. Steinmetz. 1992. Characterization of a pollen-specific cDNA from sunflower encoding a zinc finger protein. Plant J. 2:713-721.
6. Becher, A., J. H. White, and R. A. McIlhinney. 2001. The γ-aminobutyric acid receptor B, but not the metabotropic glutamate receptor type-1, associates with lipid rafts in the rat cerebellum. J. Neurochem. 79:787-795.
7. Bracha, R., Y. Nuchamowitz, M. Anbar, and D. Mirelman. 2006. Transcriptional silencing of multiple genes in trophozoites of Entamoeba histolytica. PLoS Pathog. 2:e48.
8. 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 2:295-305.
9. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Brdickova, N., T. Brdicka, L. Andera, J. Spicka, P. Angelisova, S. L. Milgram, and V. Horejsi. 2001. Interaction between two adapter proteins, PAG and EBP50: a possible link between membrane rafts and actin cytoskeleton. FEBS Lett. 507:133-136.
11. Bretscher, A. 1999. Regulation of cortical structure by the ezrin-radixinmoesin protein family. Curr. Opin. Cell Biol. 11:109-116.
12. Bretscher, A., D. Reczek, and M. Berryman. 1997. Ezrin: a protein requiring conformational activation to link microfilaments to the plasma membrane in the assembly of cell surface structures. J. Cell Sci. 110:3011-3018.
13. Brown, D. A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
14. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544.
15. Cerueus, D. P., E. Ueffing, G. Posthuma, G. J. Strous, and A. van der Ende. 1993. Detergent insolubility of alkaline phosphatase during biosynthetic transport and endocytosis. Role of cholesterol. J. Biol. Chem. 268:3150-3155.
16. Chien, S., C. Y. Chung, S. Sukumaran, N. Osborne, S. Lee, C. Ellsworth, J. G. McNally, and R. A. Firtel. 2000. The Dictyostelium LIM domain-containing protein LIM2 is essential for proper Chemotaxis and morphogenesis. Mol. Biol. Cell 11:1275-1291.
17. 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 amoebic virulence. Mol. Microbiol. 61:1523-1532.
18. Dawid, I. B., J. J. Breen, and R. Toyama. 1998. LIM domains: multiple roles as adapters and functional modifiers in protein interactions. Trends Genet. 14:156-162.
19. Diamond, L. S., D. R. Harlow, and C. C. Cunnick. 1978. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans. R. Soc. Trop. Med. Hyg. 72:431-432.
20. Eliasson, A., N. Gass, C. Mundel, R. Baltz, R. Krauter, J. L. Evrard, and A. Steinmetz. 2000. Molecular and expression analysis of a LIM protein gene family from flowering plants. Mol. Gen. Genet. 264:257-267.
21. Freyd, G., S. K. Kim, and H. R. Horvitz. 1990. Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 344:876-879.
22. Funatsu, N., H. Kumanogoh, Y. Sokawa, and S. Maekawa. 2000. Identification of gelsolin as an actin regulatory component in a triton insoluble low density fraction (raft) of newborn bovine brain. Neurosci. Res. 36:311-317.
23. Guillen, N. 1996. Role of signalling and cytoskeletal rearrangements in the pathogenesis of Entamoeba histolytica. Trends Microbiol. 4:191-197.
24. Hamann, L., R. Nickel, and E. Tannich. 1995. Transfection and continuous expression of heterologous genes in the protozoan parasite Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 92:8975-8979.
25. Harder, T., and K. Simons. 1997. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9:534-542.
26. Harris, T. J., D. E. Awrey, B. J. Cox, A. Ravandi, A. Tsang, and C. H. Siu. 2001. Involvement of a triton-insoluble floating fraction in Dictyostelium cell-cell adhesion. J. Biol. Chem. 276:18640-18648.
27. Kadnnas, J. L., and M. C. Beckerle. 2004. The LIM domain: from the cytoskeleton to the nucleus. Nat. Rev. Mol. Cell Biol. 5:920-931.
28. Karlsson, O., S. Thor, T. Norberg, H. Ohlsson, and T. Edlund. 1990. Insulin gene enhancer binding protein Is1-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature 344:879-882.
29. Katz, U., S. Ankri, T. Stolarsky, Y. Nuchamowitz, and D. Mirelman. 2002. Entamoeba histolytica expressing a dominant negative N-truncated light subunit of its gal-lectin are less virulent. Mol. Biol. Cell 13:4256-4265.
30. Khurana, B., T. Khurana, N. Khaire, and A. A. Noegel. 2002. Functions of LIM proteins in cell polarity and chemotactic motility. EMBO J. 21:5331-5342.
31. Khurana, T., B. Khurana, and A. A. Noegel. 2002. LIM proteins: association with the actin cytoskeleton. Protoplasma 219:1-12.
32. Lafont, F., S. Lecat, P. Verkade, and K. Simons. 1998. Annexin XIIIb associates with lipid microdomains to function in apical delivery. J. Cell Biol. 142:1413-1427.
33. Laughlin, R. C., G. C. McGugan, R. R. Powell, B. H. Welter, and L. A. Temesvari. 2004. Involvement of raft-like plasma membrane domains of Entamoeba histolytica in pinocytosis and adhesion. Infect. Immun. 72:5349-5357.
34. Leitsch, D., C. Radauer, K. Paschinger, I. B. Wilson, H. Breiteneder, O. Scheiner, and M. Duchene. 2005. Entamoeba histolytica: analysis of the trophozoite proteome by two-dimensional Polyacrylamide gel electrophoresis. Esp. Parasitol. 110:191-195.
35. 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. Rabbinowitsch, H. Norbertczak, C. Price, Z. Wang, N. Guillen, 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 433:865-868.
36. Marion, S., C. Laurent, and N. Guillen. 2005. Signalization and cytoskeleton activity through myosin IB during the early steps of phagocytosis in Entamoeba histolytica: a proteomic approach. Cell. Microbiol. 7:1504-1518.
37. Meza, I., P. Talamas-Rohana, and M. A. Vargas. 2006. The cytoskeleton of Entamoeba histolytica: structure, function, and regulation by signaling pathways. Arch. Med. Res. 37:234-243.
38. Moshitch-Moshkovitch, S., T. Stolarsky, D. Mirelman, and R. N. Alon. 1996. Stable episomal transfection and gene expression in Entamoeba dispar. Mol. Biochem. Parasitol. 83:257-261.
39. Muller, L., G. Xu, R. Wells, C. P. Hollenberg, and W. Piepersberg. 1994. LRG1 is expressed during sporulation in Saccharomyces cerevisiae and contains motifs similar to LIM and rho/racGAP domains. Nucleic Acids Res. 22:3151-3154.
40. Mundel, C., R. Baltz, A. Eliasson, R. Bronner, N. Grass, R. Krauter, J. L. Evrard, and A. Steinmetz. 2000. A LIM-domain protein from sunflower is localized to the cytoplasm and/or nucleus in a wide variety of tissues and is associated with the phragmoplast in dividing cells. Plant Mol. Biol. 42:291-302.
41. Niggli, V., C. Andreoli, C. Roy, and P. Mangeat. 1995. Identification of a phosphatidylinositol-4,5-bisphosphate-binding domain in the N-terminal region of ezrin. FEBS Lett. 376:172-176.
42. Pal-Bhowmick, I., H. K. Vora, and G. K. Jarori. 2007. Sub-cellular localization and post-translational modifications of the Plasmodium yoelii enolase suggest moonlighting functions. Malaria J. 6:45.
43. Pancholi, V. 2001. Multifunctional α-enolase: its role in diseases. Cell. Mol. Life Sci. 58:902-920.
44. Pike, L. J. 2004. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378:281-292.
45. Prassler, J., A. Murr, S. Stocker, J. Faix, J. Murphy, and G. Marriott. 1998. DdLIM is a cytoskeleton-associated protein involved in the protrusion of lamellipodia in Dictyostelium. Mol. Biol. Cell 9:545-559.
46. Sahoo, N., E. Labruyere, S. Bhattacharya, P. Sen, N. Guillen, and A. Bhattacharya. 2004. Calcium binding protein 1 of the protozoan parasite Entamoeba histolytica interacts with actin and is involved in cytoskeleton dynamics. J. Cell Sci. 117:3625-3634.
47. Scheiffele, P., M. G. Roth, and K. Simons. 1997. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16:5501-5508.
48. Schneider, N., I. Weber, J. Faix, J. Prassler, A. Muller-Taubenberger, J. Kohler, E. Burghardt, G. Gerisch, and G. Marriott. 2003. A Lim protein involved in the progression of cytokinesis and regulation of the mitotic spindle. Cell Motil. Cytoskelet. 56:130-139.
49. Schroeder, R., E. London, and D. Brown. 1994. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc. Natl. Acad. Sci. USA 91:12130-12134.
50. Schuck, S., M. Honsho, K. Ekroos, A. Shevchenko, and K. Simons. 2003. Resistance of cell membranes to different detergents. Proc. Natl. Acad. Sci. USA 100:5795-5800.
51. 2 influences cytoskeletal protein activity at the plasma membrane. J. Cell Sci. 113:3685-3695.
52. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569-572.
53. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
54. Taira, M., J. L. Evrard, A. Steinmetz, and I. B. Dawid. 1995. Classification of LIM proteins. Trends Genet. 11:431-432.
55. Vargas, M., P. Sansonetti, and N. Guillen. 1996. Identification and cellular localization of the actin-binding protein ABP-120 from Entamoeba histolytica. Mol. Microbiol. 22:849-857.
56. Vargas, M., H. Voigt, P. Sansonetti, and N. Guillen. 1997. Molecular characterization of myosin IB from the lower eukaryote Entamoeba histolytica, a human parasite. Mol. Biochem. Parasitol. 86:61-73.
57. Way, J. C., and M. Chalfie. 1988. mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54:5-16.