Folia Parasitologica 45[2] 117-127 (1998)
Characterization and function of the microsporidian polar tube: a review
- 1 Department of Pathology, Division of Parasitology, Albert Einstein College of Medicine, Bronx, N.Y, 10461, USA
- 2 Department of Clinical Laboratory Sciences, University of Medicine and Dentistry of New Jersey, Newark, NJ, 07107, USA
- 3 Department of Medicine, Division of Infectious Diseases, Albert Einstein College of Medicine, Bronx, N.Y,10461, USA
Microsporidia are eukaryotic, obligate intracellular organisms defined by their small spores containing a single polar tube that coils around the interior of the spore. After appropriate stimuli the germination of spores occurs. Conditions that promote germination vary widely among species, presumably reflecting the organism's adaptation to their host and external environment as well as preventing accidental discharge in the environment. It appears that calcium may be a key ion in this process. Regardless of the stimuli required for activation, all microsporidia exhibit the same response to the stimuli, that is, increasing the intrasporal osmotic pressure. This results in an influx of water into the spore accompanied by swelling of the polaroplasts and posterior vacuole. The polar tube then discharges from the anterior pole of the spore in an explosive reaction and is thought to form a hollow tube by a process of eversion. If the polar tube is discharged next to a cell, it can pierce the cell and transfer the sporoplasm into this cell. Polar tubes resist dissociation in detergents and acids but dissociate in dithiothreitol. We have developed a method for the purification of polar tube proteins (PTPs) using differential extraction followed by reverse phase high performance liquid chromatography (HPLC). This method was used to purify for subsequent characterization PTPs from Glugea americanus, Encephalitozoon cuniculi, E. hellem and E. intestinalis. These proteins appear to be members of a protein family that demonstrate conserved characteristics in solubility, hydrophobicity, mass, proline content and immunologic epitopes. These characteristics are probably important in the function of this protein in its self assembly during the eversion of the polar tube and in providing elasticity and resiliency for sporoplasm passage.
Keywords: Microsporidia, polar tube proteins, invasion mechanism, Encephalitozoon, Glugea, protein purification
Received: July 16, 1997; Accepted: October 30, 1997; Published: June 1, 1998 Show citation
References
- BARDEHLE G., JEPP-LIBUTZKI A., LINDER D., MOEHNLE K., SCHOTT H.H., ZAHNER H., ZAHRINGER U., STIRM S. 1992: Chemical composition of Litomosoides carinii microfilarial sheaths. Acta Tropica 50: 237-247
Go to original source...
Go to PubMed... - BECKERS P.J.A., DERKS G.J.M.M., VAN GOOL T., RIETVELD F.J.R., SAUERWIEN R.W. 1996: Encephalitozoon intestinalis-specific monoclonal antibodies for laboratory diagnosis of microsporidiosis. J. Clin. Microbiol. 34: 282-285
Go to original source...
Go to PubMed... - CALI A., OWEN R.L. 1988: Microsporidiosis. In: A. B ALLOWS, W.J. H AUSLER J.R., M. O HASHI and H. T URANO (Eds.) Laboratory Diagnosis of Infectious Diseases: Principles and Practice. Vol. 1, New York, Springer-Verlag, pp. 929-950
- CANNING E.U., LOM J. 1986: The Microsporidia of Vertebrates, New York, Academic Press, pp 1-16
- CONNOR R.M. 1970: Disruption of microsporidian spores for serologic studies. J. Invert. Pathol. 15: 138
Go to original source... - DALL D.J. 1983: A theory for the mechanism of polar filament extrusion in the Microspora. J. Theor. Biol. 105: 647-659
Go to original source...
Go to PubMed... - DE GRAAF D.C., MASSCHELEIN G., VANDERGEYNST F., DE BRABANDER H.F., JACOBS F.J. 1993: In vitro germination of Nosema apis (Microspora: Nosematidae) spores and its effect on their α-α-trehalose/D-glucose ratio. J. Invert. Pathol. 62: 220-225
Go to original source... - DELBAC F., DUFFIEUX F., PEYRET P., DAVID D., METENIER G., VIVARES C. 1996: Identification of sporal proteins in two microsporidian species: an immunoblotting and immunocytochemical study. J. Euk. Microbiol. 43: 101S
Go to original source...
Go to PubMed... - ERIKSON JR.B.W., VERNICK S.H., SPRAGUE V. 1968: Electron microscope study of the everted polar filament of Glutea weissenbergi (Microsporida, Nosematidae). J. Protozool. 15:758-761
Go to original source...
Go to PubMed... - FRIXIONE E., RUIZ L., SANTILLAN M., DE VARGAS L.V., TEJERO J.M., UNDEEN A.H. 1992: Dynamics of polar filament discharge and sporoplasm expulsion by microsporidian spores. Cell. Motil. Cytoskel. 22:38-50
Go to original source... - FRIXIONE E., RUIZ L., UNDEEN A.H. 1994: Monovalent cations induce microsporidian spore germination in vitro. J. Euk. Microbiol. 41: 464-468.
Go to original source... - FRIXIONE E., RUIZ L., CERBON J., 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. Euk. Microbiol. 44: 109-116
Go to original source...
Go to PubMed... - GIBBS A.J. 1953: Gurleya sp. (Microsporidia) found in the gut tissue of Trachea secalis (Lepidoptera). Parasitology 43: 143-147
Go to original source...
Go to PubMed... - HASHIMOTO K., SASAKI Y., TAKINAMI K. 1976: Conditions for extrusion of the polar filament of the spore of Plistophora anguillarum, a microsporidian parasite in Anguilla japonica. Bull. Jpn. Soc. Sci. Fish. 42: 837-845
Go to original source... - HUGER A. 1960: Electron microscope study on the cytology of a microsporidian spore by means of ultrathin sectioning. J. Insect Pathol. 2: 84-105
- ISHIHARA R. 1967: Stimuli causing extrusion of polar filaments of Glugea fumiferanae spores. Can. J. Microbiol. 13: 1321-1332
Go to original source...
Go to PubMed... - ISHIHARA R. 1968: Some observations on the fine structure of sporoplasm discharged from spores of a microsporidian, Nosema bombycis. J. Invert. Pathol. 12: 245-258
Go to original source... - IWANO H., ISHIHARA R. 1989: Intracellular germination of spores of a Nosema species immediately after their formation in cultured cell. J. Invert. Pathol. 54: 125-127
Go to original source... - KEOHANE E.M., ORR G.A., TAKVORIAN P.M., CALI A., TANOWITZ H.B., WITTNER M., WEISS L.M. 1996b: Purification and characterization of a microsporidian polar tube protein. Mol. Biochem. Parasitol. 79: 255-259
Go to original source...
Go to PubMed... - KEOHANE E.M., ORR G.A., TAKVORIAN P.M., CALI A., TANOWITZ H.B., WITTNER M., WEISS L.M. 1996c: Purification and characterization of human microsporidian polar tube proteins. J. Euk. Microbiol. 43: 100S
Go to original source...
Go to PubMed... - KEOHANE E., TAKVORIAN P.M., CALI A., TANOWITZ H.B., WITTNER M., WEISS L.M. 1994: The identification and characterization of a polar tube reactive monoclonal antibody. J. Euk. Microbiol. 41: 48S
Go to PubMed... - KEOHANE E.M., TAKVORIAN P.M., CALI A., TANOWITZ H.B., WITTNER M., WEISS L.M. 1996a: Identification of a microsporidian polar tube protein reactive monoclonal antibody. J. Euk. Microbiol. 43: 2631
Go to original source...
Go to PubMed... - KORKE V.T. 1916: On a Nosema (Nosema pulicis n. sp.) parasitic in the dog flea (Ctenocephalus felis). Ind. J. Med. Res. 3: 725-730
- KRAMER J.P. 1960: Observations on the emergence of the microsporidian sporoplasm. J. Insect Pathol. 2: 433-439
- KUDO R. 1918: Experiments on the extrusion of polar filaments of cnidosporidian spores. J. Parasitol. 4: 141147
Go to original source... - KUDO R. 1921: On the nature of structures characteristic of cnidosporidian spores. Trans. Am. Microsc. Soc. 40: 5974
Go to original source... - KUDO R.R., DANIELS E.W. 1963: An electron microscope study of the spore of a microsporidian, Thelohania californica. J. Protozool. 10: 112-120
Go to original source...
Go to PubMed... - LANGLEY R.C. JR., CALI A., SOMBERG E.W. 1987: Two dimenstional electrophoretic analysis of spore proteins of microsporidia. J. Parasitol. 73: 910-918
Go to original source...
Go to PubMed... - LEITCH G.J., HE Q., WALLACE S., VISVESVARA G.S. 1993: Inhibition of spore polar filament extrusion of the microsporidium, Encephalitozoon hellem, isolated from an AIDS patient. J. Euk. Microbiol. 40: 711-717
Go to original source...
Go to PubMed... - LEVINE N.D., CORLISS J.O., COX F.E.G., DEROUX G., GRAIN J., HONIGBERG B.M., LEEDALE G.F., LOEBLICH III A.R., LOM J., LYNN D., MERINFELD E.G., PAGE F.C., POLJANSKY G., SPRAGUE V., VAVRA J., WALLACE F.G. 1980: A newly revised classification of the protozoa. J. Protozool. 27: 37-58
Go to original source...
Go to PubMed... - LIU T.P., DAVIES D.M. 1973: Ultrastructural architecture and organization of the spore envelope during development in Thelohania bracteata (Strickland, 1913) after freeze-etching. J. Protozool. 20: 622-630
Go to original source... - LOM J. 1972: On the structure of the extruded microsporidian polar filament. Z. Parasitenkd. 38: 200-213
Go to original source... - LOM J., CORLISS J.O. 1967: Ultrastructural observations on the development of the microsporidian protozoon, Plistophora hyphessobryconis Schaeperclaus. J. Protozool. 14: 141-152
Go to original source... - LOM J., VAVRA J. 1963: The mode of sporoplasm extrusion in microsporidian spores. Acta Protozool. 1: 81-92
- MALONE L.A. 1984: Factors controlling in vitro hatching of Vairimorpha plodiae (Microspora) spores and their infectivity to Plodia interpunctella, Heliothis virescens and Pieris brassicae. J. Invert. Pathol. 44: 192-197
Go to original source... - MALONE L.A. 1990: In vitro spore hatching of two microsporidia, Nosema costelytrae and Vavraia oncoperae from New Zealand pasture insects. J. Invert. Pathol. 55: 441-443
Go to original source... - OLSEN P.E., RICE W.A., LIU T.P. 1986: In vitro germination of Nosema apis spores under conditions favorable for the generation and maintenance of sporoplasms. J. Invert. Pathol. 47: 65-73
Go to original source... - OSHIMA K. 1927: A preliminary note on the structure of the polar filament of Nosema bombycis and its functional significance. Annot. Zool. Jpn. 11: 235-243
- OSHIMA K. 1937: On the function of the polar filament of Nosema bombycis. Parasitology 29: 220-224
Go to original source... - OSHIMA K. 1964: Effect of potassium ion on filament evagination of spores of Nosema bombycis as studied by neutralization method. Annot. Zool. Jpn. 37: 102-103
- OSHIMA K. 1966: Emergence mechanism of sporoplasm from the spore of Nosema bombycis and the action of filament during evagination. Jpn. J. Zool. 15: 203-220
- PLESHINGER J., WEIDNER E. 1985: The microsporidian spore invasion tube IV. Discharge activation begins with pH-triggered Ca+2 influx. J. Cell Biol. 100: 1834-1838
Go to original source...
Go to PubMed... - SCARBOROUGH-BULL A., WEIDNER E. 1985: Some properties of discharged Glugea hertwigi (Microsporida) sporoplasms. J. Protozool. 32: 284-289
Go to original source... - SCHWARTZ D.A., VISVESVARA G.S., LEITCH G.J., TASHJIAN L., POLLACK M., HOLDEN J., BRYAN R.T. 1993: Pathology of symptomatic microsporial (Encephalitozoon hellem) bronchiolitis in the acquired immunodeficiency syndrome: a new respiratory pathogen diagnosed from lung biopsy, brochoalveolar lavage, sputum and tissue culture. Human Pathol. 24: 937-943
Go to original source...
Go to PubMed... - SINDEN R.E., CANNING E.U. 1974: The ultrastructure of the spore of Nosema algerae (Protozoa, Microsporida) in relation to the hatching mechanism of microsporidian spores. J. Gen. Microbiol. 85: 350-357
Go to original source... - STEMPELL W. 1909: Ueber Nosema bombycis naegeli nebst Bemerkungen ueber Mikrophotographie mit gewoehnlichem und ultraviolettem licht. Arch. Protistenkd. 16: 281-358
- THELOHAN P. 1892: Observations sur les Myxosporidies et essai de classification de ces organismes. Bull. Soc. Philom. 4: 165-172
- THELOHAN P. 1894: Sur la presence d'une capsule a filament dans les spores des microsporidies. C.R. Acad. Sci. Paris 118: 1425-1427
- TOGUEBAYE B.S., MARCHAND B. 1987: Intracellular emergence of the microsporidian sporoplasm as revealed by electron microscopy in Nosema couilloudi (Microspora, Nosematidae). Arch. Protistenkd. 134: 397-407
Go to original source... - UNDEEN A.H. 1976: In vivo germination and host specificity of Nosema algerae in mosquitos. J. Invert. Pathol. 27: 343-347
Go to original source...
Go to PubMed... - UNDEEN A.H. 1978: Spore hatching processes in some Nosema species with particular reference to N. algerae (Vavra and Undeen). In: W.M. B ROOKS (Ed.), Selected Topics on the Genus Nosema (Microsporida). Misc. Publ. Entomol. Soc. Am. 11: 29-49
- UNDEEN A.H. 1983: The germination of Vavraia culicis. J. Protozool. 30: 247-277
Go to original source... - UNDEEN A.H. 1990: A proposed mechanism for the germination of microsporidian (Protozoa: Microspora) spores. J. Theor. Biol. 142: 223-235
Go to original source... - UNDEEN A.H., AVERY S.W. 1984: Germination of experimentally nontransmissible microsporidia. J. Invert. Pathol. 43: 299-301
Go to original source... - UNDEEN A.H., AVERY S.W. 1988a: Effect of anions on the germination of Nosema algerae (Microspora: Nosematidae) spores. J. Invert. Pathol. 52: 84-89
Go to original source... - UNDEEN A.H., AVERY S.W. 1988b: Ammonium chloride inhibition of the germination of spores of Nosema algerae (Microspora: Nosematidae). J. Invert. Pathol. 52: 326-334
Go to original source... - UNDEEN A.H., EL GAZZAR L.M., VANDER MEER R.K., NARANG S. 1987: Trehalose levels and trehalase activity in germinated and ungerminated spores of Nosema algerae (Microspora: Nosematidae). J. Invert. Pathol. 50: 230-237
Go to original source... - UNDEEN A.H., EPSKY N.D. 1990: In vitro and in vivo germination of Nosema locustae (Microspora: Nosematidae) spores. J. Invert. Pathol. 56: 371-379
Go to original source... - UNDEEN A.H., FRIXIONE E. 1990: The role of osmotic pressure in the germination of Nosema algerae spores. J. Protozool. 37: 561-567
Go to original source...
Go to PubMed... - UNDEEN A.H., FRIXIONE E. 1991: Structural alteration of the plasma membrane in spores of the microsporidium Nosema algerae on germination. J. Protozool. 38: 511518
Go to original source...
Go to PubMed... - UNDEEN A.H., VANDER MEER R.K. 1990: The effect of ultraviolet radiation on the germination of Nosema algerae Vavra and Undeen (Microsporida: Nosematidae) spores. J. Protozool. 37: 194-199
Go to original source...
Go to PubMed... - UNDEEN A.H., VANDER MEER R.K. 1994: Conversion of intrasporal trehalose into reducing sugars during germination of Nosema algerae (Protista: Microspora) spores: a quantitative study. J. Euk. Microbiol. 41: 129132
Go to original source... - UNDEEN A.H., VANDER MEER R.K., SMITTLE B.J., AVERY S.W. 1984: The effect of gamma radiation on Nosema algerae (Microspora: Nosematidae) spore viability, germination and carbohydrates. J. Protozool. 31: 479-482
Go to original source... - VANDERMEER J.W., GOCHNAUER T.A. 1971: Trehalase activity associated with spores of Nosema apis. J. Invert. Pathol. 17: 38-41
Go to original source... - VAN GOOL T., VETTER J.C.M., WEINMAYR B., VAN DAM A., DEROUIN F., DANKERT J. 1997: High seroprevalence of Encephalitozoon species in immunocompetent subjects. J. Infect. Dis. 175: 10201024
Go to original source...
Go to PubMed... - VAVRA J., JOYON L., DE PUYTORAC P. 1966: Observation sur l'ultrastructure de filament polaire des microsporidies. Protistologica 2: 109-112
- VAVRA J., VINCKIER D., TORPIER G., PORCHET E., VIVIER E. 1986: A freeze-fracture study of microsporidia I (Protozoa: Microspora). The sporophorous vesicle, the spore wall and the spore plasma membrane. Protistologica 22: 143-154
- WEIDNER E. 1972: Ultrastructural study of microsporidian invasion into cells. Z. Parasitenkd. 40: 227-242
Go to PubMed... - WEIDNER E. 1976: The microsporidian spore invasion tube. The ultrastructure, isolation, and characterization of the protein comprising the tube. J. Cell Biol. 71: 23-34
Go to original source...
Go to PubMed... - WEIDNER E. 1982: The microsporidian spore invasion tube. III. Tube extrusion and assembly. J. Cell Biol. 93: 976979
Go to original source...
Go to PubMed... - WEIDNER E. 1992: Cytoskeletal proteins expressed by microsporidian parasites. In: J.L. A VILA and J.R. H ARRIS (Eds.), Subcellular Biochemistry. Vol. 18. Plenum Press., New York., pp. 385-399
Go to original source... - WEIDNER E., 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
Go to original source...
Go to PubMed... - WEIDNER E., BYRD W., SCARBOROUGH A., PLESHINGER J., SIBLEY D. 1984: Microsporidian spore discharge and the transfer of polaroplast organelle membrane into plasma membrane. J. Protozool. 31: 195198
Go to original source... - WEIDNER E., MANALE S.B., HALONEN S.K., LYNN J.W. 1994: Microsporidian spore invasion tubes as revealed by fluorescent probes. Biol. Bull. 187: 255-256
Go to original source...
Go to PubMed... - WEIDNER E., MANALE S.B., HALONEN S.K., LYNN J.W. 1995: Protein-membrane interaction is essential to normal assembly of the microsporidian spore invasion tube. Biol. Bull. 188: 128-135
Go to original source...
Go to PubMed... - WEST A.F. JR. 1960: The biology of a new species of Nosema (Sporozoa, Microsporidia) parasitic in the flour beetle Tribolium confusum. J. Parasitol. 46: 747-753
Go to original source...
Go to PubMed... - WHITLOCK V.H., JOHNSON S. 1990: Stimuli for the in vitro germination and inhibition of Nosema locusta (Microspora: Nosematidae) spores. J. Invert. Pathol. 56: 57-62
Go to original source... - WOOD P.J., SIDDIQUI I.R., VANDERMEER J.W., GOCHNAUER T.A. 1970: Carbohydrates of Nosema apis spores. Carbohyd. Res. 15: 154-158.
Go to original source... - ZAHNER H., HOBOM G., STIRM S. 1995: The microfilarial sheath and its proteins. Parasitol. Today 11: 116-120
Go to original source... - ZIERDT C.H., GILL V.J., ZIERDT W.S. 1993: Detection of microsporidian spores in clinical samples by indirect fluorescent-antibody assay using whole-cell antisera to Encephalitozoon cuniculi and Encephalitozon hellem. J. Clin. Microbiol. 31: 3071-3074
Go to original source...
Go to PubMed... - ZWOLFER W. 1926: Pleistophora blochmanni, eine neue Microsporidia aus Gammarus pulex. L. Arch. Protistenkd. 54: 261-340


