Skip to main content

The Microsporidian Polar Tube and Its Role in Invasion

  • Chapter
Molecular Mechanisms of Parasite Invasion

Part of the book series: Subcellular Biochemistry ((SCBI,volume 47))

Abstract

The Microsporidia are a phylum of small unicellular eukaryotes comprising more than 150 genera and 1200 species. They are obligate intracellular parasites which are able to form environmentally resistant spores. Historically, Nosema bombycis, was the first described species in this phylum and is the etiological agent of “pébrine” disease that nearly destroyed the silk-worm industry in the nineteenth century. Although the majority of microsporidia that have been described are found in arthropods and fishes, being responsible of important economic losses in the apiculture and fish farms, there are several species of medical and veterinary significance which infect animals and humans.1,2 Cerebral microsporidian infections attributed to Encephalitozoon cuniculi were initially described in 1922 in rabbits with granulomatous encephalitis and several infections were then reported in most vertebrate groups. The first case of microsporidiosis in a human was identified in 1959 in a nine-year-old boy suffering from neurological disorders.3 While reports of humans infected with microsporidia were extremely rare before the AIDS epidemic, these organisms are now recognized as significant emerging pathogens in immunocompromised hosts (HIV-infected patients with AIDS and organ transplant recipients) and is a cause of intestinal, ocular, muscular and systemic diseases.2 Some clinical manifestations have been also reported in immunocompetent hosts. Serological studies with blood donors and pregnant women revealed a prevalence of about 8%,4 suggesting that infections by microsporidia may be common in humans. So far, species belonging to seven different genera Brachiola (recendy renamed Anncaliia), Encephalitozoon, Enterocytozoon, Nosema, Pleistophora, Trachipleistophora and Vittaforma have been found in human infections. Although the origin of infection and epidemiology still remain to be documented for human microsporidiosis, horizontal transmission of most microsporidia occurs by oral ingestion of spores, with the site of initial infection being the gastrointestinal tract.5

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Weiss LM. Microsporidia: Emerging pathogenic protists. Acta Trop 2001; 78:89–102.

    Article  PubMed  CAS  Google Scholar 

  2. Didier ES. Microsporidiosis: An emerging and opportunistic infection in humans and animals. Acta Trop 2005; 94:61–76.

    Article  PubMed  CAS  Google Scholar 

  3. Matsubayashi H, Koike T, Mikata I et al. A case of Encephalitozoon-like body infection in man. AMA Arch Pathol 1959; 67:181–187.

    PubMed  CAS  Google Scholar 

  4. van Gool T, Vetter JC, Weinmayr B et al. High seroprevalence of Encephalitozoon species in immunocompetent subjects. J Infect Dis 1997; 175:1020–1024.

    Article  PubMed  Google Scholar 

  5. Mathis A, Weber R, Deplazes P. Zoonotic potential of the microsporidia. Clin Microbiol Rev 2005; 18:423–445.

    Article  PubMed  CAS  Google Scholar 

  6. Van de Peer Y, Ben Ali A, Meyer A. Microsporidia: Accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi. Gene 2000; 246:1–8.

    Article  PubMed  Google Scholar 

  7. Keeling PJ. Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet Biol 2003; 38:298–309.

    Article  PubMed  CAS  Google Scholar 

  8. Thomarat F, Vivares CP, Gouy M. Phylogenetic analysis of the complete genome sequence of Encephalitozoon cuniculi supports the fungal origin of microsporidia and reveals a high frequency of fast-evolving genes. J Mol Evol 2004; 59:780–791.

    Article  PubMed  CAS  Google Scholar 

  9. Williams BA, Hirt RP, Lucocq JM et al. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 2002; 418:865–869.

    Article  PubMed  CAS  Google Scholar 

  10. Katinka MD, Duprat S, Cornillot E et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 2001; 414:450–453.

    Article  PubMed  CAS  Google Scholar 

  11. Takvorian PM, Cali A. Enzyme histochemical identification of the Golgi apparatus in the microsporidian, Glugea stephani. J Eukaryot Microbiol 1994; 41:63S–64S.

    PubMed  CAS  Google Scholar 

  12. Weidner E, Byrd W, Scarborough A et al. Microsporidian spore discharge and the transfer of polaroplast organelle membrane into plasma membrane. J Protozool 1984; 31:195–198.

    Google Scholar 

  13. Bigliardi E, Sacchi L. Cell biology and invasion of the microsporidia. Microbes Infect 2001; 3:373–379.

    Article  PubMed  CAS  Google Scholar 

  14. Frixione E, Ruiz L, Cerbon J et al. Germination of Nosema algerae (Microspora) spores: Conditional inhibition by D2O, ethanol and Hg2+ suggests dependence of water influxupon membrane hydration and specific transmembrane pathways. J Eukaryot Microbiol 1997; 44:109–116.

    Article  PubMed  CAS  Google Scholar 

  15. Bohne W, Ferguson DJP, Kohler K et al. Developmental expression of tandemly repeated, glycine-and serine-rich spore wall protein in the microsporidian pathogen Encephalitozoon cuniculi. Infect Immun 2000; 68:2268–2275.

    Article  PubMed  CAS  Google Scholar 

  16. Hayman JR, Hayes SF, Amon J et al. Developmental expression of two spore wall proteins during maturation of the microsporidian Encephalitozoon intestinalis. Infect Immun 2001; 69:7057–7066.

    Article  PubMed  CAS  Google Scholar 

  17. Brosson D, Kuhn L, Prensier G et al. The putative chitin deacetylase of Encephalitozoon cuniculi: A surface protein implicated in microsporidian spore-wall formation. FEMS Microbiol Lett 2005; 247:81–90.

    Article  PubMed  CAS  Google Scholar 

  18. Peuvel-Fanget I, Polonais V, Brosson D et al. EnP1 and EnP2, two proteins associated with the Encephalitozoon cuniculi endospore, the chitin-rich inner layer of the microsporidian spore wall. Int J Parasitol 2006; 36:309–318.

    Article  PubMed  CAS  Google Scholar 

  19. Xu Y, Takvorian P, Cali A et al. Identification of a new spore wall protein from Encephalitozoon cuniculi. Infect Immun 2006; 74:239–247.

    Article  PubMed  CAS  Google Scholar 

  20. Brosson D, Kuhn L, Delbac F et al. Proteomic analysis of the eukaryotic parasite Encephalitozoon cuniculi (Microsporidia): A reference map for proteins expressed in late sporogonial stages. Proteomics 2006; 6:3625–3635.

    Article  PubMed  CAS  Google Scholar 

  21. Franzen C. Microsporidia: How can they invade other cells? Trends in Parasitol 2004; 20:275–276.

    Article  CAS  Google Scholar 

  22. Xu Y, Weiss LM. The microsporidian polar tube: A highly specialised invasion organelle. Int J Parasitol 2005; 35:941–953.

    Article  PubMed  Google Scholar 

  23. Canning EU, Curry A, Lacey CJN et al. Ultrastructure of Encephalitozoon sp. Infecting the conjunctival, corneal and nasal epithelia of a patient with AIDS. Europ J Protistol 1992; 28:226–237.

    Google Scholar 

  24. Chioralia G, Trammer T, Maier WA et al. Morphologic changes in Nosema algerae (Microspora) during extrusion. Parasitol Res 1998; 84:123–131.

    Article  PubMed  CAS  Google Scholar 

  25. Weidner E. The microsporidian spore invasion tube. The ultrastructure, isolation, and characterization of the protein comprising the tube. J Cell Biol 1976; 71:23–34.

    Article  PubMed  CAS  Google Scholar 

  26. Weidner E. The microsporidian spore invasion tube. III. Tube extrusion and assembly. J Cell Biol 1982; 93:976–979.

    Article  PubMed  CAS  Google Scholar 

  27. Frixione E, Ruiz L, Santillan M et al. Dynamics of polar filament discharge and sporoplasm expulsion by microsporidian spores. Cell Motil Cytoskel 1992; 22:38–50.

    Article  Google Scholar 

  28. Desportes I. Ultrastructure de Stempellia mutabilis Leger et Hesse, microsporidie parasite de l’éphémère Ephemera vulgata. Protistologica 1976; 12:121–150.

    Google Scholar 

  29. Takvorian PM, Cali A. Polar tube formation and nucleoside diphosphatase activity in the microsporidian, Glugea stephani. J Eukaryot Microbiol 1996; 43:102S–103S.

    Article  PubMed  CAS  Google Scholar 

  30. Delbac F, Peuvel I, Méténier G et al. Microsporidian invasion apparatus: Identification of a novel Polar Tube Protein and evidence for clustering of ptp1 and ptp2 genes in three Encephalitozoon species. Infect Immun 2001; 69:1016–1024.

    Article  PubMed  CAS  Google Scholar 

  31. Desportes-Livage I, Hilmarsdottir I, Romana C et al. The characteristics of the microsporidian Enterocytozoon bieneusi: A consequence of its development within the short living-enterocytes. J Protozool 1991; 38:111S–113S.

    PubMed  CAS  Google Scholar 

  32. Hilmarsdottir I, Desportes-Livage I, Datry A et al. Morphogenesis of the polaroplast in Enterocytozoon bieneusi Desportes et al, 1985, a microsporidian parasite of HIV infected patients. Europ J Protistol 1993; 29:88–97.

    Google Scholar 

  33. Keohane EM, Orr GA, Takvorian PM et al. Purification and characterization of a microsporidian polar tube protein. Mol Biochem Parasitol 1996; 79:255–259.

    Article  PubMed  CAS  Google Scholar 

  34. Keohane EM, Orr GA, Takvorian PM et al. Polar tube proteins of microsporidia of the family Encephalitozoonidae. J Eukaryot Microbiol 1999; 46:1–5.

    Article  PubMed  CAS  Google Scholar 

  35. Delbac F, Peyret P, Méténier G et al. On proteins of the microsporidian invasive apparatus: Complete sequence of a Polar Tube Protein of Encephalitozoon cuniculi. Mol Microbiol 1998; 29:825–834.

    Article  PubMed  CAS  Google Scholar 

  36. Keohane EM, Orr GA, Zhang HS et al. The molecular characterization of the major polar tube protein gene from Encephalitozoon hellem, a microsporidian parasite of humans. Mol Biochem Parasitol 1998; 94:227–236.

    Article  PubMed  CAS  Google Scholar 

  37. Peuvel I, Delbac F, Metenier G et al. Polymorphism of the gene encoding a major polar tube protein PTP1 in two microsporidia of the genus Encephalitozoon. Parasitology 2000; 121:581–587.

    Article  PubMed  CAS  Google Scholar 

  38. Xiao L, Li L, Moura H et al. Genotyping Encephalitozoon hellem isolates by analysis of the polar tube protein gene. J Clin Microbiol 2001; 39:2191–2196.

    Article  PubMed  CAS  Google Scholar 

  39. Vavra J. Detection of polysaccharides in microsporidian spores by means of the periodic acid-thio semicarbazide-silver proteinate test. J Microscopie 1972; 14:357–360.

    CAS  Google Scholar 

  40. Xu Y, Takvorian PM, Cali A et al. Glycosylation of the major polar tube protein of Encephalitozoon hellem, a microsporidian parasite that infects humans. Infect Immun 2004; 72:6341–6350.

    Article  PubMed  CAS  Google Scholar 

  41. Peek R, Delbac F, Speijer D et al. Carbohydrate moieties of microsporidian polar tube proteins are targeted by immunoglobulin G in immunocompetent individuals. Infect Immun 2005; 73:7906–7913.

    Article  PubMed  CAS  Google Scholar 

  42. van Gool T, Biderre C, Delbac F et al. Serodiagnostic studies in an immunocompetent individual infected with Encephalitozoon cuniculi. J Infect Dis 2004; 189:2243–2249.

    Article  PubMed  Google Scholar 

  43. Delbac F, Duffieux F, David D et al. Immunocytochemical identification of spore proteins in two microsporidia, with emphasis on extrusion apparatus. J Eukaryot Microbiol 1998; 45:224–231.

    Article  PubMed  CAS  Google Scholar 

  44. Beckers PJ, Derks GJ, Gool T et al. Encephalytozoon intestinalis-specific monoclonal antibodies for laboratory diagnosis of microsporidiosis. J Clin Microbiol 1996; 34:282–285.

    PubMed  CAS  Google Scholar 

  45. Polonais V, Prensier G, Méténier G et al. Microsporidian polar tube proteins: Highly divergent but closely linked genes encode PTP1 and PTP2 in members of the evolutionarily distant Antonospora and Encephalitozoon groups. Fungal Genet Biol 2005; 42:791–803.

    Article  PubMed  CAS  Google Scholar 

  46. Peuvel I, Peyret P, Méténier G et al. The microsporidian polar tube: Evidence for a third polar tube protein (PTP3) in Encephalitozoon cuniculi. Mol Biochem Parasitol 2002; 122:69–80.

    Article  PubMed  CAS  Google Scholar 

  47. Vivarès CP, Méténier G. The microsporidia genome: Living with minimal genes as an intracellular eukaryote. In: Lindsay DS, Weiss LM, eds. Opportunistic Infections: Toxoplasma, Sarcocystis and Microsporidia, World Class Parasites. Vol. 9. Boston: Kluwer Acad Pub, 2004:215–242.

    Chapter  Google Scholar 

  48. Undeen AH, Avery SW. Effect of anions on the germination of Nosema algerae (Microspora: Nosematidae) spores. J Invertebr Pathol 1988; 52:84–89.

    Article  CAS  Google Scholar 

  49. Undeen AH, Vander Meer RK. The effect of ultraviolet radiation on the germination of Nosema algerae Vavra and Undeen (Microsporida: Nosematidae) spores. J Protozool 1990; 37:194–199.

    PubMed  CAS  Google Scholar 

  50. Leitch GJ, He Q, Wallace S et al. Inhibition of the spore polar filament extrusion of the microsporidium, Encephalitozoon hellem, isolated from an AIDS patient. J Eukaryot Microbiol 1993; 40:711–717.

    Article  PubMed  CAS  Google Scholar 

  51. Frixione E, Ruiz L, Undeen AH. Monovalent cations induce microsporidian spore germination in vitro. J Eukaryot Microbiol 1994; 41:464–468.

    Article  CAS  Google Scholar 

  52. Weidner E, Byrd W. The microsporidian spore invasion tube. II. Role of calcium in the activation of invasion tube discharge. J Cell Biol 1982; 93:970–975.

    Article  PubMed  CAS  Google Scholar 

  53. Pleshinger J, Weidner E. The microsporidian spore invasion tube. IV. Discharge activation begins with pH-triggered Ca2+ influx. J Cell Biol 1985; 100:1834–1838.

    Article  PubMed  CAS  Google Scholar 

  54. Hayman JR, Southern TR, Nash TE. Role of sulfated glycans in adherence of the microsporidian Encephalitozoon intestinalis to host cells in vitro. Infect Immun 2005; 73:841–848.

    Article  PubMed  CAS  Google Scholar 

  55. Southern TR, Jolly CE, Russell Hayman J. Augmentation of microsporidia adherence and host cell infection by divalent cations. FEMS Microbiol Lett 2006; 260:143–149.

    Article  PubMed  CAS  Google Scholar 

  56. Lorn J, Vavra J. The mode of sporoplasm extrusion in microsporidian spores. Acta Protozol 1963; 1:81–92.

    Google Scholar 

  57. Ghosh K, Cappiello CD, McBride SM et al. Functional characterization of a putative aquaporin from Encephalitozoon cuniculi, a microsporidia pathogenic to humans. Int J Parasitol 2006; 36:57–62.

    Article  PubMed  CAS  Google Scholar 

  58. Undeen AH, Vander Meer RK. Conversion of intrasporal trehalose into reducing sugars during germination of Nosema algerae (Protista: Microspora) spores: A quantitative study. J Eukaryot Microbiol 1994; 41:129–132.

    Article  CAS  Google Scholar 

  59. Magaud A, Achbarou A, Desportes-Livage I. Cell invasion by the microsporidium Encephalitozoon intestinalis. J Eukaryot Microbiol 1997; 44:81S.

    Article  PubMed  CAS  Google Scholar 

  60. Couzinet S, Cejas E, Schittny J et al. Phagocytic uptake of Encephalitozoon cuniculi by nonprofessional phagocytes. Infect Immun 2000; 68:6939–6945.

    Article  PubMed  CAS  Google Scholar 

  61. Foucault C, Drancourt M. Actin mediates Encephalitozoon intestinalis entry into the human enterocyte-like cell line, Caco-2. Microb Pathog 2000; 28:51–58.

    Article  PubMed  CAS  Google Scholar 

  62. Franzen C, Muller A, Hartmann P et al. Cell invasion and intracellular fate of Encephalitozoon cuniculi (Microsporidia). Parasitology 2005; 130:285–292.

    Article  PubMed  CAS  Google Scholar 

  63. Leitch GJ, Ward TL, Shaw AP et al. Apical spore phagocytosis is not a significant route of infection of differentiated enterocytes by Encephalitozoon intestinalis. Infect Immun 2005; 73:7697–7704.

    Article  PubMed  CAS  Google Scholar 

  64. Fasshauer V, Gross U, Bohne W. The parasitophorous vacuole membrane of Encephalitozoon cuniculi lacks host cell membrane proteins immediately after invasion. Eukaryot Cell 2005; 4:221–224.

    Article  PubMed  CAS  Google Scholar 

  65. Takvorian PM, Weiss LM, Cali A. The early events of Brachiola algerae (Microsporidia) infection: Spore germination, sporoplasm structure, and development within host cells. Folia Parasitol 2005; 52:118–129.

    Article  PubMed  Google Scholar 

  66. Vivares CP, Metenier G. The microsporidian Encephalitozoon. Bioessays 2001; 23:194–202.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Frédéric Delbac .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Delbac, F., Polonais, V. (2008). The Microsporidian Polar Tube and Its Role in Invasion. In: Burleigh, B.A., Soldati-Favre, D. (eds) Molecular Mechanisms of Parasite Invasion. Subcellular Biochemistry, vol 47. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78267-6_17

Download citation

Publish with us

Policies and ethics