Unique physiology of host-parasite interactions in microsporidia infections

Cellular Microbiology

Volumn 11, Issue 11, 2009, Pages 1551-1560

  Williams, Bryony A P ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL STRUCTURE; CYTOPLASM; FUNGAL SPORE GERMINATION; GENE SEQUENCE; HOST PARASITE INTERACTION; HYPERTROPHY; IMMUNOCOMPROMISED PATIENT; MICROSPORIDIAN SPORE; MICROSPORIDIOSIS; MICROSPOROGENESIS; MICROTUBULE ASSEMBLY; MITOCHONDRIAL RESPIRATION; MOLECULAR PHYLOGENY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SEX RATIO; SIGNAL TRANSDUCTION; SPECIES DIVERSITY;

ANIMALS; HOST-PARASITE INTERACTIONS; HUMANS; MAMMALS; MICROSPORIDIA; MODELS, BIOLOGICAL; VIRULENCE;

ANIMALIA; EUKARYOTA; FUNGI; MAMMALIA; MICROSPORIDIA;

EID: 72749101415     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01362.x     Document Type: Review

References (68)

1. Akiyoshi, D.E., Morrison, H.G., Lei, S., Feng, X., Zhang, Q., Corradi, N., et al. (2009) Genomic survey of the noncultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLoS Pathog 5: e1000261
2. Andreadis, T.G. (2005) Evolutionary strategies and adaptations for survival between mosquito-parasitic microsporidia and their intermediate copepod hosts: a comparative examination of Amblyospora connecticus and Hyalinocysta chapmani (Microsporidia: Amblyosporidae). Folia Parasitol (Praha) 52: 23-35
3. Belkorchia, A., Biderre, C., Militon, C., Polonais, V., Wincker, P., Jubin, C., et al. (2008) In vitro propagation of the microsporidian pathogen Brachiola algerae and studies of its chromosome and ribosomal DNA organization in the context of the complete genome sequencing project. Parasitol Int 57: 62-71
4. Bulnheim, H.P., and Vávra, J. (1968) Infection by the microsporidian Octosporea effeminans sp. n. and its sex determining influence in the amphipod Gammarus duebeni. J Parasitol 54: 241-248
5. Cali, A., and Takvorian, P. (1999) Microsporidian developmental morphology and life cycles. In The Microsporidia and Microsporidiosis. Wittner, M., and Weiss, L.M. (eds). Washington, DC: ASM Press, pp. 85-128
6. Cali, A., Weiss, L.M., and Takvorian, P.M. (2002) Brachiola algerae spore membrane systems, their activity during extrusion, and a new structural entity, the multilayered interlaced network, associated with the polar tube and the sporoplasm. J Eukaryot Microbiol 49: 164-174
7. Cavalier-Smith, T. (1983) A 6-kingdom classification and a unified phylogeny. In Endocytobiology, Vol. II. Schenk H.E.A., and Schwemmler, W. (eds). Berlin: Walter de Gruyter, pp. 1027-1034
8. Cavalier-Smith, T. (2001) What are Fungi? In The Mycota VII, Part A. McLaughlin, D.J., McLaughlin, E.G., and Lemke, P.A. (eds). Berlin: Springer-Verlag, pp. 1-37
9. Chioralia, G., Trammer, T., Maier, W.A., and Seitz, H.M. (1998) Morphologic changes in Nosema algerae (Microspora) during extrusion. Parasitol Res 84: 123-131
10. Cornillot, E., Méténier, G., Vivarès, C.P., and Dassa, E. (2002) Comparative analysis of sequences encoding ABC systems in the genome of the microsporidian Encephalitozoon cuniculi. FEMS Microbiol Lett 210: 39-47
11. Cornman, R.S., Chen, Y.P., Schatz, M.C., Street, C., Zhao, Y., Desany, B., et al. (2009) Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog 5: e1000466.
12. Delbac, F., David, D., Méténier, G., and Vivarès, C. (1997) First complete amino acid sequence of a polar tube protein in a microsporidian species, Encephalitozoon cuniculi. J Eukaryot Microbiol 44: 77S
13. Delbac, F., Peuvel, I., Méténier, G., Peyretaillade, E., and Vivarès, C.P. (2001) 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 69: 1016-1024
14. Dia, N., Lavie, L., Méténier, G., Toguebaye, B.S., Vivarès, C.P., and Cornillot, E. (2007) InterB multigenic family, a gene repertoire associated with subterminal chromosome regions of Encephalitozoon cuniculi and conserved in several human-infecting microsporidian species. Curr Genet 51: 171-186
15. Didier, E.S. (2005) Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop 94: 61-76
16. Edlind, T.D., Li, J., Visversvara, G.S., Vodkin, M.H., McLaughlin, G.L., and Katiyar, S.K. (1996) Phylogenetic analysis of the b-tubulin sequences from amitochondriate protozoa. Mol Phylogenet Evol 5: 359-367
17. Fasshauer, V., Gross, U., and Bohne, W. (2005) The parasitophorous vacuole membrane of Encephalitozoon cuniculi lacks host cell membrane proteins immediately after invasion. Eukaryot Cell 4: 221-224
18. Findley, A.M., Weidner, E.H., Carman, K.R., Xu, Z., and Godbar, J.S. (2005) Role of the posterior vacuole in Spraguea lophii (Microsporidia) spore hatching. Folia Parasitol (Praha) 52: 111-117
19. Frixione, E., Ruiz, L., Santillan, M., de Vargas, L.V., Tejero, J.M., and Undeen, A.H. (1992) Dynamics of polar filament discharge and sporoplasm expulsion by microsporidian spores. Cell Motil Cytoskelet 22: 38-50.
20. Frixione, E., Ruiz, L., Cerbon, J., and Undeen, A.H. (1997) Germination of Nosema algerae (Microspora) spores: conditional inhibition by D2O, ethanol and Hg2+ suggests dependence of water influx upon membrane hydration and specific transmembrane pathways. J Eukaryot Microbiol 44: 109-116.
21. Ghosh, K., Cappiello, C.D., McBride, S.M., Occi, J.L., Cali, A., Takvorian, P.M., et al. (2006) Functional characterization of a putative aquaporin from Encephalitozoon cuniculi, a microsporidia pathogenic to humans. Int J Parasitol 36: 57-62.v
22. Goldberg, A.V., Molik, S., Tsaousis, A.D., Neumann, K., Kuhnke, G., Delbac, F., et al. (2008) Localization and functionality of microsporidian iron-sulphur cluster assembly proteins. Nature 452: 624-628
23. Held, A.A. (1972) Host-parasite relations between Allomyces and Rozella - parasite penetration depends on growth response of host cell-wall. Arch Mikrobiologie 82: 128- 139
24. Higes, M., Martin-Hernandez, R., Botias, C., Bailon, E.G., Gonzalez-Porto, A.V., Barrios, L., et al. (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10: 2659-2669
25. Hinkle, G., Morrison, H.G., and Sogin, M.L. (1997) Genes coding for reverse transcriptase, DNA-directed RNA polymerase, and chitin synthase from the microsporidian Spraguea lophii. Biol Bull 193: 250-251
26. Hirt, R.P., Logsdon, J.M., Jr, Healy, B., Dorey, M.W., Doolittle, W.F., and Embley, T.M. (1999) Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci USA 96: 580-585
27. Hoch, G., Schafellner, C., Henn, M.W., and Schopf, A. (2002) Alterations in carbohydrate and fatty acid levels of Lymantria dispar larvae caused by a microsporidian infection and potential adverse effects on a co-occurring endoparasitoid, Glyptapanteles liparidis. Arch Insect Biochem Physiol 50: 109-120
28. Hurst, L.D. (1991) The Incidences and Evolution of Cytoplasmic Male Killers. Proc R Soc Lond [Biol] 244: 91-99. de Jong, J.C., McCormack, B.J., Smirnoff, N., and Talbot, N.J. (1997) Glycerol generates turgor in rice blast. Nature 389: 244-245
29. de Jong, J.C., McCormack, B.J., Smirnoff, N., and Talbot, N.J. (1997) Glycerol generates turgor in rice blast. Nature 389: 244-245
30. Katinka, M.D., Duprat, S., Cornillot, E., Méténier, G., Thomarat, F., Prensier, G., et al. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450-453
31. Keeling, P.J. (2003) Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet Biol 38: 298-309.
32. Keeling, P.J., and Doolittle, W.F. (1996) Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol Biol Evol 13: 1297-1305
33. Kent, M.L., and Speare, D.J. (2005) Review of the sequential development of Loma salmonae (Microsporidia) based on experimental infections of rainbow trout (Oncorhynchus mykiss) and Chinook salmon (O. tshawytscha). Folia Parasitol (Praha) 52: 63-68
34. Keohane, E., and Weiss, L.M. (1999) The structure, function, and composotion of the microsporidian polar tube. In The Microsporidia and Microsporidiosis. Wittner, M., and Weiss, L.M. (eds). Washington DC: ASM Press, pp. 196- 224
35. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580
36. Krylov, D.M., Wolf, Y.I., Rogozin, I.B., and Koonin, E.V. (2003) Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res 13: 2229- 2235
37. Kudo, R. (1918) Experiments on the extrusion of polar filaments of cnidosporidian spores. J Parasitol 4: 141-147.
38. Lee, J.J., Leedale, G.F., and Bradbury, P.C. (2000) An Illustrated Guide to the Protozoa: Organisms Traditionally Referred to as Protozoa, or Newly Discovered Groups. Lawrence, KS: Society of Protozoologists.
39. Lee, S.C., Corradi, N., Byrnes, E.J., 3rd, Torres-Martinez, S., Dietrich, F.S., Keeling, P.J., and Heitman, J. (2008) Microsporidia evolved from ancestral sexual fungi. Curr Biol 18: 1675-1679
40. Li, Y., Wu, Z., Pan, G., He, W., Zhang, R., Hu, J., and Zhou, Z. (2009) Identification of a novel spore wall protein (SWP26) from microsporidia Nosema bombycis. Int J Parasitol 39: 391-398
41. Lom, J., and Dykova, I. (2005) Microsporidian xenomas in fish seen in wider perspective. Folia Parasitol (Praha) 52: 69-81
42. Lom, J., and Vávra, J. (1963) The mode of sporoplasm extrusion in microsporidian spores. Acta Protozoologica 1: 81-92
43. Lom, J., Vávra, J., Weiss, L.M., and Bukva, V. (eds). (2005) Microsporidia of invertebrate and vertebrate hosts: papers and abstracts from the NATO Advanced Research Workshop 'Emergent Pathogens in the 21st Century: First United Workshop on Microsporidia from Invertebrate and Vertebrate Hosts' C? eské Bude? jovice, 12-15 July 2004. Folia Parasitol (Praha) 52: 195
44. Miranda-Saavedra, D., Stark, M.J., Packer, J.C., Vivarès, C.P., Doerig, C., and Barton, G.J. (2007) The complement of protein kinases of the microsporidium Encephalitozoon cuniculi in relation to those of Saccharomyces cerevisiae and Schizosaccharomyces pombe. BMC Genomics 8: 309.
45. Mommsen, T.P. (2001) Paradigms of growth in fish. Comp Biochem Physiol B Biochem Mol Biol 129: 207-219.
46. Pasteur, L. (1870) études sur la maladie des vers a soie. Paris: Gauthier-Villars.
47. Pettersson, E., Lundeberg, J., and Ahmadian, A. (2009) Generations of sequencing technologies. Genomics 93: 105- 111
48. Peuvel, I., Peyret, P., Méténier, G., Vivarès, C.P., and Delbac, F. (2002) The microsporidian polar tube: evidence for a third polar tube protein (PTP3) in Encephalitozoon cuniculi. Mol Biochem Parasitol 122: 69-80
49. Peyretaillade, E., Biderre, C., Peyret, P., Duffieux, F., Méténier, G., Gouy, M., et al. (1998) Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. Nucleic Acids Res 26: 3513-3520
50. Rodgers-Gray, T.P., Smith, J.E., Ashcroft, A.E., Isaac, R.E., and Dunn, A.M. (2004) Mechanisms of parasite-induced sex reversal in Gammarus duebeni. Int J Parasitol 34: 747-753.
51. Ronnebaumer, K., Gross, U., and Bohne, W. (2008) The nascent parasitophorous vacuole membrane of Encephalitozoon cuniculi is formed by host cell lipids and contains pores which allow nutrient uptake. Eukaryot Cell 7: 1001- 1008
52. Scanlon, M., Leitch, G.J., Visvesvara, G.S., and Shaw, A.P. (2004) Relationship between the host cell mitochondria and the parasitophorous vacuole in cells infected with Encephalitozoon microsporidia. J Eukaryot Microbiol 51: 81-87
53. Sinai, A.P., and Joiner, K.A. (2001) The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J Cell Biol 154: 95-108.
54. Southern, T.R., Jolly, C.E., Lester, M.E., and Hayman, J.R. (2006) Identification of a microsporidia protein potentially involved in spore adherence to host cells. J Eukaryot Microbiol 53 (Suppl. 1): S68-S69
55. Terry, R.S., Smith, J.E., Sharpe, R.G., Rigaud, T., Littlewood, D.T., Ironside, J.E., et al. (2004) Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proc Biol Sci 271: 1783- 1789
56. Troemel, E.R., Felix, M.A., Whiteman, N.K., Barriere, A., and Ausubel, F.M. (2008) Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol 6: 2736-2752
57. Tsaousis, A.D., Kunji, E.R., Goldberg, A.V., Lucocq, J.M., Hirt, R.P., and Embley, T.M. (2008) A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453: 553-556
58. Undeen, A.H., and Vander Meer, R.K. (1999) Microsporidian intrasporal sugars and their role in germination. J Invertebr Pathol 73: 294-302
59. Vávra, J., and Larsson, J.I.R. (1999) Structure of the Microsporidia. In The Microsporidia and Microsporidiosis. Wittner, M., and Weiss, L.M. (eds). Washington, DC: ASM Press, pp. 7-84.v
60. Weidner, E., and Byrd, W. (1982) The microsporidian spore invasion tube. II. Role of calcium in the activation of invasion tube discharge. J Cell Biol 93: 970-975
61. Weidner, E., Byrd, W., Scarborough, A., Pleshinger, J., and Sibley, D. (1984) Microsporidian spore discharge and the transfer of polaroplast organelle membrane into plasmamembrane. J Protozool 31: 195-198.
62. Weidner, E., Findley, A.M., Dolgikh, V., and Sokolova, J. (1999) Microsporidian biochemistry and physiology. In The Microsporidia and Microsporidiosis. Wittner, M., and Weiss, L.M. (eds). Washington, DC: ASM Press, pp. 172- 195.
63. Williams, B.A., Hirt, R.P., Lucocq, J.M., and Embley, T.M. (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418: 865-869
64. Williams, B.A., Lee, R.C., Becnel, J.J., Weiss, L.M., Fast, N.M., and Keeling, P.J. (2008) Genome sequence surveys of Brachiola algerae and Edhazardia aedis reveal microsporidia with low gene densities. BMC Genomics 9: 200
65. Wilson, E.O. (2007) The Creation: An Appeal to Save Life on Earth. New York; London: W. W. Norton.
66. Wittner, M., and Weiss, L.M. (1999) The Microsporidia and Microsporidiosis. Washington, DC: ASM Press.
67. Xu, J., Pan, G., Fang, L., Li, J., Tian, X., Li, T., et al. (2006) The varying microsporidian genome: existence of longterminal repeat retrotransposon in domesticated silkworm parasite Nosema bombycis. Int J Parasitol 36: 1049-1056.
68. Xu, Y., Takvorian, P., Cali, A., and Weiss, L.M. (2003) Lectin binding of the major polar tube protein (PTP1) and its role in invasion. J Eukaryot Microbiol 50 (Suppl.): 600-601