Localisation to lipid rafts correlates with increased function of the Gal/GalNAc lectin in the human protozoan parasite, Entamoeba histolytica

International Journal for Parasitology

Volumn 41, Issue 13-14, 2011, Pages 1409-1419

  Welter, Brenda H ^a   Goldston, Amanda M ^a   Temesvari, Lesly A ^a  

^a CLEMSON UNIVERSITY   (United States)

Author keywords

Actin; Adhesion; Cholesterol; Entamoeba histolytica; Gal GalNAc lectin; Lipid raft

Indexed keywords

ACTIN; ADHESIN; CELL SURFACE RECEPTOR; CHOLESTEROL; CYTOCHALASIN D; GALACTOSE; GALACTOSE N ACETYLGALACTOSAMINE INHIBITABLE LECTIN; LECTIN; N ACETYLGALACTOSAMINE; RECEPTOR; UNCLASSIFIED DRUG;

ADHESION; COMPARTMENTALIZATION; CORRELATION; MEMBRANE; PARASITE; PROTOZOAN;

ARTICLE; CELL LINE; CELL MUTANT; COMPLEX FORMATION; CONTROLLED STUDY; DEVELOPING COUNTRY; DYSENTERY; ENTAMOEBA HISTOLYTICA; HOST CELL; LIPID RAFT; LIVER ABSCESS; MICROBIAL ADHESION; NONHUMAN; PREVALENCE; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SUBUNIT; RECEPTOR BINDING; WESTERN BLOTTING;

ACETYLGALACTOSAMINE; CELL ADHESION; CELL LINE; CHOLESTEROL; ENTAMOEBA HISTOLYTICA; ENTAMOEBIASIS; GALACTOSE; HUMANS; LECTINS; MEMBRANE MICRODOMAINS; PROTEIN BINDING; PROTEIN TRANSPORT; PROTOZOAN PROTEINS;

ENTAMOEBA HISTOLYTICA; PROTOZOA;

EID: 82355191520     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2011.10.003     Document Type: Article

References (51)

1. Arhets P., Olivo J.C., Gounon P., Sansonetti P., Guillen N. Virulence and functions of myosin II are inhibited by overexpression of light meromyosin in Entamoeba histolytica. Mol. Biol. Cell 1998, 9:1537-1547.
2. Atger V.M., de la Llera Moya M., Stoudt G.W., Rodrigueza W.V., Phillips M.C., Rothblat G.H. Cyclodextrins as catalysts for the removal of cholesterol from macrophage foam cells. J. Clin. Invest. 1997, 99:773-780.
3. Bailey G.B., Nudelman E.D., Day D.B., Harper C.F., Gilmour J.R. Specificity of glycosphingolipid recognition by Entamoeba histolytica trophozoites. Infect. Immun. 1990, 58:43-47.
4. Bansal D., Bhatti H.S., Sehgal R. Altered lipid parameters in patients infected with Entamoeba histolytica, Entamoeba dispar and Giardia lamblia. Br. J. Biomed. Sci. 2005, 62:63-65.
5. 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.
6. 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.
7. Bos H.J., van de Griend R.J. Virulence and toxicity of axenic Entamoeba histolytica. Nature 1977, 265:341-343.
8. Bracha R., Mirelman D. Adherence and ingestion of Escherichia coli serotype 055 by trophozoites of Entamoeba histolytica. Infect. Immun. 1983, 40:882-887.
9. Blazquez S., Rigothier M.-C., Huerre M., Guillén N. Initiation of inflammation and cell death during liver abscess formation by Entamoeba histolytica depends on activity of the galactose/N-acetyl-d-galactosamine lectin. Int. J. Parasitol. 2007, 37:425-433.
10. Brown D.A. Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology 2006, 21:430-439.
11. Buss S.N., Hamano S., Vidrich A., Evans C., Zhang Y., Crasta O.R., Sobral B.W., Gilchrist C.A., Petri W.A. Members of the Entamoeba histolytica transmembrane kinase family play non-redundant roles in growth and phagocytosis. Int. J. Parasitol. 2010, 40:833-843.
12. Causeret M., Taulet N., Comunale F., Favard C., Gauthier-Rouviere C. N-cadherin association with lipid rafts regulates its dynamic assembly at cell-cell junctions in C2C12 myoblasts. Mol. Biol. Cell 2005, 16:2168-2180.
13. Cheng X.J., Tsukamoto H., Kaneda Y., Tachibana H. Identification of the 150-kDa surface antigen of Entamoeba histolytica as a galactose- and N-acetyl-d-galactosamine-inhibitable lectin. Parasitol. Res. 1998, 84:632-639.
14. Cheng X.J., Hughes M.A., Huston C.D., Loftus B., Gilchrist C.A., Lockhart L.A., Ghosh S., Miller-Sims V., Mann B.J., Petri W.A., Tachibana H. Intermediate subunit of the Gal/GalNAc lectin of Entamoeba histolytica is a member of a gene family containing multiple CXXC sequence motifs. Infect. Immun. 2001, 69:5892-5898.
15. Coudrier E., Amblard F., Zimmer C., Roux P., Olive-Marin J.-C., Rigothier M.-C., Guillén N. Myosin II and the Gal-GalNAc lectin play a crucial role in tissue invasion by Entamoeba histolytica. Cell. Microbiol. 2005, 7:19-27.
16. Das S.R., Ghoshal S. Restoration of virulence to rat of axenically grown Entamoeba histolytica by cholesterol and hamster liver passage. Ann. Trop. Med. Parasitol. 1976, 70:439-443.
17. Diamond L.S., Harlow D.R., Cunnick C.C. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans. R. Soc. Trop. Med. Hyg. 1978, 72:431-432.
18. Dodson J.M., Lenkowski P.W., Eubanks A.C., Jackson T.F., Napodano J., Lyerly D.M., Lockhart L.A., Mann B.J., Petri W.A. Infection and immunity mediated by the carbohydrate recognition domain of the Entamoeba histolytica Gal/GalNAc lectin. J. Infect. Dis. 1999, 179:460-466.
19. Eroglu C., Brugger B., Wieland F., Sinning I. Glutamate-binding affinity of Drosophila metabotropic glutamate receptor is modulated by association with lipid rafts. Proc. Natl. Acad. Sci. USA 2003, 100:10219-10224.
20. Fabbri M., Di Meglio S., Gagliani M.C., Consonni E., Molteni R., Bender J.R., Tacchetti C., Pardi R. Dynamic partitioning into lipid rafts controls the endo-exocytic cycle of the αL/β2 integrin, LFA-1, during leukocyte chemotaxis. Mol. Biol. Cell 2005, 16:5793-5803.
21. Hao S., August A. Actin depolymerization transduces the strength of B-cell receptor stimulation. Mol. Biol. Cell 2005, 16:2275-2284.
22. Katiyar S.K., Prasad A.K., Ghoshal S., Das S.R., Sagar P. Cholesterol induced changes in glucose-6-phosphate generating enzymes, concanavalin A agglutinability and haemolytic activity of axenic Entamoeba histolytica. Ann. Trop. Med. Parasitol. 1987, 81:201-205.
23. 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.
24. Laughlin R.C., Temesvari L.A. Cellular and molecular mechanisms that underlie Entamoeba histolytica pathogenesis: prospects for intervention. Expert Rev. Mol. Med. 2005, 7:1-19.
25. Leitinger B., Hogg N. The involvement of lipid rafts in the regulation of integrin function. J. Cell. Sci. 2002, 115:963-972.
26. Lopez-Revilla R., Cano-Mancera R. Adhesion of Entamoeba histolytica trophozoites to human erythrocytes. Infect. Immun. 1982, 37:281-285.
27. Mata-Cardenas B.D., Vargas-Villarreal J., Gonzalez-Salazar F., Martinez-Rodriguez H., Morales-Vallarta M., Said-Fernandez S. Entamoeba histolytica is unable to use free cholesterol, phospholipids, and fatty acids under axenic cultivation conditions. Arch. Med. Res. 2000, 31:S212-S213.
28. McCoy J.J., Mann B.J. Proteomic analysis of Gal/GalNAc lectin-associated proteins in Entamoeba histolytica. Exp. Parasitol. 2005, 110:220-225.
29. Mittal K., Welter B.H., Temesvari L.A. Entamoeba histolytica: lipid rafts are involved in adhesion of trophozoites to host extracellular matrix components. Exp. Parasitol. 2008, 120:127-153.
30. Neal R.A., Vincent P. Strain variation in Entamoeba histolytica. II. The effect of serial liver passage on the virulence. Parasitology 1956, 46:173-182.
31. Oh H., Mohler E.R., Tian A., Baumgart T., Diamond S.L. Membrane cholesterol is a biomechanical regulator of neutrophil adhesion. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1290-1297.
32. Pang L., Graziano M., Wang S. Membrane cholesterol modulates galanin-GalR2 interaction. Biochemistry 1999, 38:12003-12011.
33. 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.
34. 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.
35. Powell R.R., Temesvari L.A. Involvement of a Rab8-like protein of Dictyostelium discoideum, Sas1, in the formation of membrane extensions, secretion and adhesion during development. Microbiology 2004, 150:2513-2525.
36. Powell R.R., Welter B.H., Hwu R., Bowersox B., Attaway C., Temesvari L.A. Entamoeba histolytica: FYVE-finger domains, phosphatidylinositol 3-phosphate biosensors, associate with phagosomes but not fluid filled endosomes. Exp. Parasitol. 2006, 112:221-231.
37. Pucadyil T.J., Chattopadhyay A. Cholesterol modulates ligand binding and G-protein coupling to serotonin (1A) receptors from bovine hippocampus. Biochim. Biophys. Acta 2004, 1663:188-200.
38. Ravdin J.I., Guerrant R.L. Role of adherence in cytopathogenic mechanisms of Entamoeba histolytica. Study with mammalian tissue culture cells and human erythrocytes. J. Clin. Invest. 1981, 68:1305-1313.
39. Reversi A., Rimoldi V., Brambillasca S., Chini B. Effects of cholesterol manipulation on the signaling of the human oxytocin receptor. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291:R861-R869.
40. Sateriale A., Huston C.D. A sequential model of host cell killing and phagocytosis by Entamoeba histolytica. J. Parasitol. Res. 2011, 2011:926706.
41. Saxena A., Kaul D., Vinayak V.K. Amoebic erythrophagocytosis: significance of membrane cholesterol to phospholipid ratio. Int. Res. Commun. Syst. Med. Sci. 1986, 14:330-331.
42. Serrano-Luna J., Gutierrez-Meza M., Mejia-Zepeda R., Galindo-Gomez S., Tsutsumi V., Shibayama M. Effect of phosphatidylcholine-cholesterol liposomes on Entamoeba histolytica virulence. Can. J. Microbiol. 2010, 56:987-995.
43. Sharma R. Effect of cholesterol on the growth and virulence of Entamoeba histolytica. Trans. R. Soc. Trop. Med. Hyg. 1959, 53:278-281.
44. Singh B.N., Srivastava R.V., Dutta G.P. Virulence of strains of Entamoeba histolytica to rats and the effect of cholesterol, rat caecal and hamster liver passage on the virulence of non-invasive strains. Indian J. Exp. Biol. 1971, 9:21-27.
45. Tavares P., Rigothier M.-C., Khun H., Roux P., Huerre M., Guillén N. Roles of cell adhesion and cytoskeleton activity in Entamoeba histolytica pathogenesis: a delicate balance. Infect. Immun. 2005, 73:1771-1778.
46. Valensin S., Paccani S.R., Ulivieri C., Mercati D., Pacini S., Patrussi L., Hirst T., Lupetti P., Baldari C.T. F-actin dynamics control segregation of the TCR signaling cascade to clustered lipid rafts. Eur. J. Immunol. 2002, 32:435-446.
47. 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 β2 integrin motif. Mol. Biol. Cell 1998, 9:2069-2079.
48. Wang C., Yoo Y., Fan H., Kim E., Guan K.L., Guan J.L. Regulation of integrin β1 recycling to lipid rafts by Rab1a to promote cell migration. J. Biol. Chem. 2010, 285:29398-29405.
49. Welter B.H., Powell R.R., Leo M., Smith C.M., Temesvari L.A. A unique Rab GTPase, EhRabA, is involved in motility and polarization of Entamoeba histolytica cells. Mol. Biochem. Parasitol. 2005, 140:161-173.
50. Welter B.H., Temesvari L.A. 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 2009, 8:1014-1026.
51. Wong K., Li X., Ma Y. Paraformaldehyde induces elevation of intracellular calcium and phosphatidylserine externalization in platelets. Thromb. Res. 2006, 117:537-542.