1887

Abstract

and are closely related free-living amoebae found in the environment. causes primary amoebic meningoencephalitis (PAM), a rapidly fatal disease of the central nervous system, while is non-pathogenic. infection occurs when the amoebae access the nasal passages, attach to the nasal mucosa and its epithelial lining, and migrate to the brain. This process involves interaction with components of the host extracellular matrix (ECM). Since the ability to invade tissues can be a characteristic that distinguishes pathogenic from non-pathogenic amoebae, the objective of this study was to assess adhesion to, and invasion of, the ECM by these two related but distinct species. exhibited a higher level of adhesion to the ECM components laminin-1, fibronectin and collagen I. Scanning electron microscopy revealed that attached on ECM substrata exhibited a spread-out appearance that included the presence of focal adhesion-like structures. Western immunoblotting revealed two integrin-like proteins for both species, but one of these, with a molecular mass of approximately 70 kDa, was detected at a higher level in . Confocal microscopy indicated that the integrin-like proteins co-localized to the focal adhesion-like structures. Furthermore, anti-integrin antibody decreased adhesion of to ECM components. Finally, disrupted 3D ECM scaffolds, while had a minimal effect. Collectively, these results indicate a distinction in adhesion to, and invasion of, ECM proteins between and

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.055020-0
2012-03-01
2020-01-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/3/791.html?itemId=/content/journal/micro/10.1099/mic.0.055020-0&mimeType=html&fmt=ahah

References

  1. Aldape K., Huizinga H., Bouvier J., McKerrow J.. ( 1994;). Naegleria fowleri: characterization of a secreted histolytic cysteine protease. Exp Parasitol78:230–241 [CrossRef][PubMed]
    [Google Scholar]
  2. Alderete J. F., Benchimol M., Lehker M. W., Crouch M. L.. ( 2002;). The complex fibronectin–Trichomonas vaginalis interactions and trichomonosis. Parasitol Int51:285–292 [CrossRef][PubMed]
    [Google Scholar]
  3. Anderson K., Jamieson A.. ( 1972;). Primary amoebic meningoencephalitis. Lancet299:902–903 [CrossRef][PubMed]
    [Google Scholar]
  4. Bandyopadhyay K., Karmakar S., Ghosh A., Das P. K.. ( 2001;). Role of 67 kDa cell surface laminin binding protein of Leishmania donovani in pathogenesis. J Biochem130:141–148[PubMed][CrossRef]
    [Google Scholar]
  5. Barczyk M., Carracedo S., Gullberg D.. ( 2010;). Integrins. Cell Tissue Res339:269–280 [CrossRef][PubMed]
    [Google Scholar]
  6. Berrier A. L., Yamada K. M.. ( 2007;). Cell–matrix adhesion. J Cell Physiol213:565–573 [CrossRef][PubMed]
    [Google Scholar]
  7. Boshuizen J. A., Rossen J. W., Sitaram C. K., Kimenai F. F., Simons-Oosterhuis Y., Laffeber C., Büller H. A., Einerhand A. W.. ( 2004;). Rotavirus enterotoxin NSP4 binds to the extracellular matrix proteins laminin-beta3 and fibronectin. J Virol78:10045–10053[CrossRef]
    [Google Scholar]
  8. 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 Biochem72:248–254 [CrossRef][PubMed]
    [Google Scholar]
  9. Burridge K., Chrzanowska-Wodnicka M.. ( 1996;). Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol12:463–519 [CrossRef][PubMed]
    [Google Scholar]
  10. Carter R. F.. ( 1968;). Primary amoebic meningo-encephalitis: clinical, pathological and epidemiological features of six fatal cases. J Pathol Bacteriol96:1–25 [CrossRef][PubMed]
    [Google Scholar]
  11. Carter R. F.. ( 1972;). Primary amoebic meningo-encephalitis. An appraisal of present knowledge. Trans R Soc Trop Med Hyg66:193–208 [CrossRef][PubMed]
    [Google Scholar]
  12. Casta e Silva Filho F., de Souza W., Lopes J. D.. ( 1988;). Presence of laminin-binding proteins in trichomonads and their role in adhesion. Proc Natl Acad Sci U S A85:8042–8046 [CrossRef][PubMed]
    [Google Scholar]
  13. Cerva L., Novăk K.. ( 1968;). Amoebic meningoencephalitis: 16 fatalities. Science160:92 [CrossRef][PubMed]
    [Google Scholar]
  14. Cline M., Marciano-Cabral F., Bradley S. G.. ( 1983;). Comparison of Naegleria fowleri and Naegleria gruberi cultivated in the same nutrient medium. J Protozool30:387–391[PubMed][CrossRef]
    [Google Scholar]
  15. Cline M., Carchman R., Marciano-Cabral F.. ( 1986;). Movement of Naegleria fowleri stimulated by mammalian cells in vitro. J Protozool33:10–13[PubMed][CrossRef]
    [Google Scholar]
  16. Cornillon S., Gebbie L., Benghezal M., Nair P., Keller S., Wehrle-Haller B., Charette S. J., Brückert F., Letourneur F., Cosson P.. ( 2006;). An adhesion molecule in free-living Dictyostelium amoebae with integrin β features. EMBO Rep7:617–621[PubMed]
    [Google Scholar]
  17. Craun G. F., Calderon R. L., Craun M. F.. ( 2005;). Outbreaks associated with recreational water in the United States. Int J Environ Health Res15:243–262 [CrossRef][PubMed]
    [Google Scholar]
  18. de Bentzmann S., Tristan A., Etienne J., Brousse N., Vandenesch F., Lina G.. ( 2004;). Staphylococcus aureus isolates associated with necrotizing pneumonia bind to basement membrane type I and IV collagens and laminin. J Infect Dis190:1506–1515 [CrossRef][PubMed]
    [Google Scholar]
  19. De Jonckheere J. F.. ( 2004;). Molecular definition and the ubiquity of species in the genus Naegleria. . Protist155:89–103[CrossRef]
    [Google Scholar]
  20. de Lourdes Muñoz M., Das P., Tovar R.. ( 2001;). Entamoeba histolytica trophozoites activated by collagen type I and Ca2+ have a structured cytoskeleton during collagenase secretion. Cell Motil Cytoskeleton50:45–54 [CrossRef][PubMed]
    [Google Scholar]
  21. Flores-Robles D., Rosales C., Rosales-Encina J. L., Talamás-Rohana P.. ( 2003;). Entamoeba histolytica: a β1 integrin-like fibronectin receptor assembles a signaling complex similar to those of mammalian cells. Exp Parasitol103:8–15 [CrossRef][PubMed]
    [Google Scholar]
  22. Fritz-Laylin L. K., Prochnik S. E., Ginger M. L., Dacks J. B., Carpenter M. L., Field M. C., Kuo A., Paredez A., Chapman J.. & other authors ( 2010;). The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell140:631–642 [CrossRef][PubMed]
    [Google Scholar]
  23. Gordon V. R., Asem E. K., Vodkin M. H., McLaughlin G. L.. ( 1993;). Acanthamoeba binds to extracellular matrix proteins in vitro. Invest Ophthalmol Vis Sci34:658–662[PubMed]
    [Google Scholar]
  24. Gozalbo D., Gil-Navarro I., Azorín I., Renau-Piqueras J., Martínez J. P., Gil M. L.. ( 1998;). The cell wall-associated glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is also a fibronectin and laminin binding protein. Infect Immun66:2052–2059[PubMed]
    [Google Scholar]
  25. Grinnell F.. ( 2008;). Fibroblast mechanics in three-dimensional collagen matrices. J Bodyw Mov Ther12:191–193 [CrossRef][PubMed]
    [Google Scholar]
  26. Gyori E.. ( 2003;). December 2002: 19-year old male with febrile illness after jet ski accident. Brain Pathol13:237–239[PubMed]
    [Google Scholar]
  27. Han K. L., Lee H. J., Shin M. H., Shin H. J., Im K. I., Park S. J.. ( 2004;). The involvement of an integrin-like protein and protein kinase C in amoebic adhesion to fibronectin and amoebic cytotoxicity. Parasitol Res94:53–60 [CrossRef][PubMed]
    [Google Scholar]
  28. Hernández-Ramírez V. I., Anaya-Ruiz M., Rios A., Talamás-Rohana P.. ( 2000;). Entamoeba histolytica: tyrosine kinase activity induced by fibronectin through the β1-integrin-like molecule. Exp Parasitol95:85–95 [CrossRef][PubMed]
    [Google Scholar]
  29. Hersen P., Ladoux B.. ( 2011;). Biophysics: push it, pull it. Nature470:340–341 [CrossRef][PubMed]
    [Google Scholar]
  30. Hostetter M. K.. ( 1999;). Integrin-like proteins in Candida spp. and other microorganisms. Fungal Genet Biol28:135–145 [CrossRef][PubMed]
    [Google Scholar]
  31. Hynes R. O., Yamada K. M.. ( 1982;). Fibronectins: multifunctional modular glycoproteins. J Cell Biol95:369–377 [CrossRef][PubMed]
    [Google Scholar]
  32. Jamerson M., Remmers K., Cabral G., Marciano-Cabral F.. ( 2009;). Survey for the presence of Naegleria fowleri amebae in lake water used to cool reactors at a nuclear power generating plant. Parasitol Res104:969–978 [CrossRef][PubMed]
    [Google Scholar]
  33. Jarolim K. L., McCosh J. K., Howard M. J., John D. T.. ( 2000;). A light microscopy study of the migration of Naegleria fowleri from the nasal submucosa to the central nervous system during the early stage of primary amebic meningoencephalitis in mice. J Parasitol86:50–55[PubMed][CrossRef]
    [Google Scholar]
  34. Kleinman H. K., Jacob K.. ( 2001;). Invasion assays. Curr Protoc Cell Biol12:12.2.1–12.2.5[PubMed]
    [Google Scholar]
  35. Kleinman H. K., Martin G. R.. ( 2005;). Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol15:378–386 [CrossRef][PubMed]
    [Google Scholar]
  36. Kottom T. J., Kennedy C. C., Limper A. H.. ( 2008;). Pneumocystis PCINT1, a molecule with integrin-like features that mediates organism adhesion to fibronectin. Mol Microbiol67:747–761 [CrossRef][PubMed]
    [Google Scholar]
  37. Lama A., Kucknoor A., Mundodi V., Alderete J. F.. ( 2009;). Glyceraldehyde-3-phosphate dehydrogenase is a surface-associated, fibronectin-binding protein of Trichomonas vaginalis . Infect Immun77:2703–2711 [CrossRef][PubMed]
    [Google Scholar]
  38. LeBleu V. S., MacDonald B., Kalluir R.. ( 2007;). Structure and function of basement membrane. Exp Biol Med232:1121–1129 [CrossRef]
    [Google Scholar]
  39. Li E., Yang W. G., Zhang T., Stanley S. L. Jr. ( 1995;). Interaction of laminin with Entamoeba histolytica cysteine proteinases and its effect on amebic pathogenesis. Infect Immun63:4150–4153[PubMed]
    [Google Scholar]
  40. Marciano-Cabral F., Cabral G. A.. ( 2007;). The immune response to Naegleria fowleri amebae and pathogenesis of infection. FEMS Immunol Med Microbiol51:243–259 [CrossRef][PubMed]
    [Google Scholar]
  41. Marciano-Cabral F. M., Fulford D. E.. ( 1986;). Cytopathology of pathogenic and nonpathogenic Naegleria species for cultured rat neuroblastoma cells. Appl Environ Microbiol51:1133–1137[PubMed]
    [Google Scholar]
  42. Marciano-Cabral F. M., Patterson M., John D. T., Bradley S. G.. ( 1982;). Cytopathogenicity of Naegleria fowleri and Naegleria gruberi for established mammalian cell cultures. J Parasitol68:1110–1116 [CrossRef][PubMed]
    [Google Scholar]
  43. Marciano-Cabral F., MacLean R., Mensah A., LaPat-Polasko L.. ( 2003;). Identification of Naegleria fowleri in domestic water sources by nested PCR. Appl Environ Microbiol69:5864–5869 [CrossRef][PubMed]
    [Google Scholar]
  44. Martinez A. J.. ( 1985;). Free-Living Amoebas: Natural History, Prevention, Diagnosis, Pathology, and Treatment of Disease Boca Raton, FL: CRC Press;
    [Google Scholar]
  45. Martinez A. J., Visvesvara G. S.. ( 1997;). Free-living, amphizoic and opportunistic amebas. Brain Pathol7:583–598 [CrossRef][PubMed]
    [Google Scholar]
  46. Martinez J., Duma R. J., Nelson E. C., Moretta F. L.. ( 1973;). Experimental Naegleria meningoencephalitis in mice. Penetration of the olfactory mucosal epithelium by Naegleria and pathologic changes produced: a light and electron microscope study. Lab Invest29:121–133[PubMed]
    [Google Scholar]
  47. Meza I.. ( 2000;). Extracellular matrix-induced signaling in Entamoeba histolytica: its role in invasiveness. Parasitol Today16:23–28 [CrossRef][PubMed]
    [Google Scholar]
  48. Nimni M. E.. ( 1983;). Collagen: structure, function, and metabolism in normal and fibrotic tissues. Semin Arthritis Rheum13:1–86 [CrossRef][PubMed]
    [Google Scholar]
  49. Pillai D. R., Kain K. C.. ( 2005;). Entamoeba histolytica: identification of a distinct β2 integrin-like molecule with a potential role in cellular adherence. Exp Parasitol109:135–142 [CrossRef][PubMed]
    [Google Scholar]
  50. Riveline D., Zamir E., Balaban N. Q., Schwarz U. S., Ishizaki T., Narumiya S., Kam Z., Geiger B., Bershadsky A. D.. ( 2001;). Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol153:1175–1186 [CrossRef][PubMed]
    [Google Scholar]
  51. Rocha-Azevedo B., Jamerson M., Cabral G. A., Silva-Filho F. C., Marciano-Cabral F.. ( 2007;). The interaction between the amoeba Balamuthia mandrillaris and extracellular matrix glycoproteins in vitro . Parasitology134:51–58 [CrossRef][PubMed]
    [Google Scholar]
  52. Rocha-Azevedo B. D., Jamerson M., Cabral G. A., Silva-Filho F. C., Marciano-Cabral F.. ( 2009;). Acanthamoeba interaction with extracellular matrix glycoproteins: biological and biochemical characterization and role in cytotoxicity and invasiveness. J Eukaryot Microbiol56:270–278 [CrossRef][PubMed]
    [Google Scholar]
  53. Ruoslahti E.. ( 1996;). RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol12:697–715 [CrossRef][PubMed]
    [Google Scholar]
  54. Santoni G., Birarelli P., Hong L. J., Gamero A., Djeu J. Y., Piccoli M.. ( 1995;). An α 5 β 1-like integrin receptor mediates the binding of less pathogenic Candida species to fibronectin. J Med Microbiol43:360–367 [CrossRef][PubMed]
    [Google Scholar]
  55. Sengupta K., Hernández-Ramírez V. I., Rios A., Mondragón R., Talamás-Rohana P.. ( 2001;). Entamoeba histolytica: monoclonal antibody against the β1 integrin-like molecule (140 kDa) inhibits cell adhesion to extracellular matrix components. Exp Parasitol98:83–89 [CrossRef][PubMed]
    [Google Scholar]
  56. Shibayama M., Serrano-Luna J. J., Rojas-Hernández S., Campos-Rodríguez R., Tsutsumi V.. ( 2003;). Interaction of secretory immunoglobulin A antibodies with Naegleria fowleri trophozoites and collagen type I. Can J Microbiol49:164–170 [CrossRef][PubMed]
    [Google Scholar]
  57. Stevens A. R., De Jonckheere J., Willaert E.. ( 1980;). Naegleria lovaniensis new species: isolation and identification of six thermophilic strains of a new species found in association with Naegleria fowleri . Int J Parasitol10:51–64 [CrossRef][PubMed]
    [Google Scholar]
  58. Talamás-Rohana P., Meza I.. ( 1988;). Interaction between pathogenic amebas and fibronectin: substrate degradation and changes in cytoskeleton organization. J Cell Biol106:1787–1794 [CrossRef][PubMed]
    [Google Scholar]
  59. Talamás-Rohana P., Hernández V. I., Rosales-Encina J. L.. ( 1994;). A β1 integrin-like molecule in Entamoeba histolytica . Trans R Soc Trop Med Hyg88:596–599 [CrossRef][PubMed]
    [Google Scholar]
  60. Thong Y. H., Ferrante A.. ( 1986;). Migration patterns of pathogenic and nonpathogenic Naegleria spp. Infect Immun51:177–180[PubMed]
    [Google Scholar]
  61. Toney D. M., Marciano-Cabral F.. ( 1992;). Alterations in protein expression and complement resistance of pathogenic Naegleria amoebae. Infect Immun60:2784–2790[PubMed]
    [Google Scholar]
  62. Towbin H., Staehelin T., Gordon J.. ( 1979;). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A76:4350–4354 [CrossRef][PubMed]
    [Google Scholar]
  63. Tuckwell D.. ( 1999;). Evolution of von Willebrand factor A (VWA) domains. Biochem Soc Trans27:835–840[PubMed]
    [Google Scholar]
  64. Whittaker C. A., Hynes R. O.. ( 2002;). Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell13:3369–3387 [CrossRef][PubMed]
    [Google Scholar]
  65. Yoder J. S., Blackburn B. G., Craun G. F., Hill V., Levy D. A., Chen N., Lee S. H., Calderon R. L., Beach M. J.. ( 2004;). Surveillance for waterborne-disease outbreaks associated with recreational water–United States, 2001–2002. MMWR Surveill Summ53:1–22[PubMed]
    [Google Scholar]
  66. Yoder J. S., Eddy B. A., Visvesvara G. S., Capewell L., Beach M. J.. ( 2010;). The epidemiology of primary amoebic meningoencephalitis in the USA, 1962–2008. Epidemiol Infect138:968–975 [CrossRef][PubMed]
    [Google Scholar]
  67. Yurchenco P. D., Schittny J. C.. ( 1990;). Molecular architecture of basement membranes. FASEB J4:1577–1590[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.055020-0
Loading
/content/journal/micro/10.1099/mic.0.055020-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error