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Chapter 6 : The Structure, Function, and Composition of the Microsporidian Polar Tube

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Abstract:

The spores of microsporidia possess a unique, highly specialized structure, the polar tube, which is used to inject the parasite from the spore into a new host cell. Several theories have been proposed regarding the method by which the sporoplasm exits the spore and on the function of the polar filament or tube in this process. Electron-dense, particulate material fills the center of the filament. Weidner proposed that this material was unpolymerized polar tube protein (PTP). On the basis of ultrastructural observations, the eversion of the polar tube has been likened to a tube sliding within a tube. This chapter presents details on spore activation and discharge. When sporoblasts form, each one contains five to six coils of the preformed polar filament with the anchoring disk positioned at the anterior end. The major amino acids coded by the and PTP genes were proline and glycine. Application of the techniques of modern biology has resulted in the identification of several PTPs although the interactions and functional significance of these proteins remains to be determined.

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6

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Rough Endoplasmic Reticulum
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High-Performance Liquid Chromatography
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Sodium Dodecyl Sulfate
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Transmission Electron Microscopy
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Image of FIGURE 1
FIGURE 1

Polar tube extrusion. A spore of the microsporidium after polar tube extrusion by mechanical pressure is shown ( ).

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 2
FIGURE 2

Scanning electron micrograph of sporoplasm passage. The micrograph shows an spore with an extruded polar tube. Arrows indicate sporoplasm passage through the polar tube. (Reprinted with permission from .)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 3
FIGURE 3

Scanning electron micrograph of a microsporidian infection of a host cell. The micrograph shows an extruded polar tube of a spore of piercing and infecting Vero E6 green monkey kidney cells in tissue culture. (Reprinted with permission from .)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 4
FIGURE 4

Diagram of a microsporidian spore. Spores range in size from 1 to 10 μm. The spore coat consists of an electron-dense exospore (Ex), electron-lucent endospore (En), and plasma membrane (Pm). It is thinner at the anterior end of the spore. The sporoplasm (Sp) contains a single nucleus (Nu), the posterior vacuole (PV), and ribosomes. The polar filament is attached to the anterior end of the spore by an anchoring disk (AD) and is divided into two regions: the manubroid or straight portion (M) and the posterior region forming five coils (PT) around the sporoplasm. The manubroid polar filament is surrounded by the lamellar polaroplast (PI) and vesicular polaroplast (VP1). The inset depicts a cross section of the polar tube coils (five coils in this spore), demonstating the various concentric layers of different electron density and electron-dense core present in such cross sections.

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 5
FIGURE 5

Transmission electron micrograph of a longitudinal section of a spore of . The manubroid polar filament (M) is attached to the anterior end of the spore by an anchoring disk (open arrow) and then forms 33 coils (Pt and solid arrow) around the sporoplasm in one to three rows. PI, lamellar polaroplast; e, electron-lucent endospore. Note that the endopsore layer is thinner at the apical end and that the polar tube contains concentric layers of varying electron density with a dense core. The spore measures 2.8 by 4.6 μm. (Reprinted with permission from .)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 6
FIGURE 6

Morphology of anchoring disk. (A) Electron micrograph of the anterior portion of a longitudinal section of a spore of showing the mushroom-shaped anchoring disk (a) connected to the manubroid polar filament (p).The polar filament and anchoring disk are surrounded by a limiting membrane. Note the thin endospore area above the anchoring disk. (Reprinted with permission from Peter M.Takvorian.) (B) Electron micrograph of the anterior portion of a longitudinal section of a spore of a sp. showing polar filament extrusion. Collarlike structures (a) formed from the anchoring disk hold the polar tube (p) in place during extrusion. This figure also demonstrates eversion of the polar tube. Note that the hinge region (dark lines in the anchoring disk) and the anchoring disk have rotated 90° during extrusion of the polar tube. (Reprinted with permission from .)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 7
FIGURE 7

Polar tube solubility. Shown are negative stain transmission electron micrographs of spores of disrupted with 0.5 μm acid washed glass beads in a Mini Beadbeater (Biospec Products, Bardesville, Okla.). (Panels 1 and 2) Disrupted spores after being extracted five times with 1% SDS and once with 9 M urea. Note broken spores (S) and straight and twisted polar tubes (PT and closed arrows). (Panel 3) Disrupted spores after being washed five times with 1% SDS and once with 9 M urea and incubated 2 h with 2% DTT. Note broken spores (S), lack of spore contents (open arrows), and absence of polar tubes. (Reprinted with permission from Keohane et al., 1996c.)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 8
FIGURE 8

Immunogold electron microscopy of a polar tube-specific monoclonal antibody. Shown is an immunogold electron micrograph of a spore with mAb 3C8.23.1 ( ), and a secondary antibody labeled with 12-nm colloidal gold, stained with 1% uranyl acetate. (Panels 1 to 3) Note gold localization on longitudinal, transverse, and cross sections of polar tubes (PT). (Panel 4) four polar tube (PT) cross sections, a portion of the lamellar polaroplast (PL), and a sagittal cut through the anterior straight portion (manubroid) of the polar tube (MPT) indicated by arrowheads. Note the localization of the gold on the “sheath” or outer portion, the “dense” core or center, and the medium-dense material of the polar tube. (Reprinted with permission from Keohane etal, 1996c).

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 9
FIGURE 9

HPLC purification of polar tube components. Reverse-phase HPLC of the DTT-solubilized PTPs of obtained from SDS-urea extracted spores was performed. Spores of were disrupted by glass beads and sequentially extracted according to a previously published protocol ( ). The proteins were subjected to reductive alkylation by 4-vinylpyridine, followed by reverse-phase HPLC with a linear gradient of HO and acetonitrile containing 0.1% trifluoroacetic acid ( ). (Inset, lane A) SDS-PAGE (10% polyacrylamide) silver stain of the major ultraviolet-absorbing peak, demonstrating a 43-kDa protein. Peaks corresponding to the previously reported 23- and 34-kDa proteins in the DTT-solubilized material were also identified. (Inset, lane B) The purified 43-kDa PTP demonstrated strong immunoblot activity with polar tube specific mAb 3C8.23.1. (Inset, lane C) A polyclonal mouse antiserum to this 43-kDa protein (anti-Ga PTP) reacted with a 43-kDa antigen in spore lysate. Anti-Ga PTP also reacted with extruded and intrasporal polar tubes of spores by immunogold electron microscopy. (Reprinted with permission from .)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 10
FIGURE 10

Comparison of and PTPs. Reverse-phase HPLC of the major DTT-solubilized PTP of and was performed. The method of purification is the same as that shown in Fig. 9 . Note the similarity in the retention times of the PTPs of these two microsporidia.

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 11
FIGURE 11

Transmission electron micrographs of polar tube discharge. Electron micrographs of anterior portion of longitudinal sections of the spores of are shown. (Panel 1) Swelling of the anterior end of the spore and disruption of the anchoring disk. Note protein filaments already present above the anterior end of the spore. (Panel 2) Eversion of polar tube membrane (arrow) and release of material (presumably PTP) from the polar tube (p). (Panel 3) Further formation of the polar tube (p). Note polar tube membrane and deposition of PTP coat on the outside of the membrane (arrow). (Reprinted with permission from Peter M.Takvorian.)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 12
FIGURE 12

Model of polar tube discharge. (A) A resting spore. (B) Initial eversion of the polar filament. Note that the anchoring disk has everted or rotated to form a collar and that the polaroplast membranes have swollen. Unpolymerized PTP is released from the polar tube core and polymerizes on the outside of the membrane scaffolding as it is being everted. AD, anchoring disk, PI, polaroplast membranes: Ex, exospore; En, endospore; PT, polar tube; PTP, polar tube protein(s).

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 13
FIGURE 13

Model of sporoplasm exit from microsporidian spores. (A) As the polar tube (PT) continues to form with polymerization of the polar tube protein(s) (PTP), the polaroplast membrane begins to enter the hollow portion of the tube. The posterior vacuole (PV) starts to enlarge. (B) Sporoplasm (SP) and nucleus (Nu) flow into the tube surrounded by the polaroplast membrane (PI), leaving behind the plasma membrane (Pm) (still attached to the spore coat [Ex and En]).The polar tube has penetrated a host cell, and the posterior vacuole (PV) has swollen and fills the space vacated by the sporoplasm. The swelling of the posterior vacuole generates the osmotic pressure driving the extrusion of the contents of the spore. (C) After the polar tube has pierced the host cell membrane, the sporoplasm and nucleus now surrounded by the polaroplast membrane emerge from the tip of the hollow polar tube inside the host cell. The spore contains the plasma membrane (Pm), posterior vacuole (PV), and spore coat (exospore [Ex] and endospore [En]) which are left behind. The limiting membrane of the sporoplasm in the host cell is provided by the polaroplast membranes (PI).

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 14
FIGURE 14

Extruded polar tube, demonstrating membranes and polar tube protein coat. A transmission electron micrograph of an extruded polar tube of demonstrating a polar tube membrane (curved arrow) and the coating of PTP over the membrane (straight arrow) is shown. (Reprinted with permission from Peter M. Takvorian.)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Image of FIGURE 15
FIGURE 15

Micrograph of sporoplasm passage through the polar tube. A negative stain of transmission electron microscopy of discharged spores of () shows extruded polar tubes. Arrows indicate appearance of sporoplasm at the end of the discharged polar tube. (Reprinted with permission from .)

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
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Tables

Generic image for table
TABLE 1

Polar tube proteins

Cloned gene ( ).

Cloned gene ( ).

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
Generic image for table
TABLE 2

Comparison of PTP genes and predicted proteins

Underlined amino acids in PTP are an alternating motif. Amino acids in a boldface type are substitutions in the repeat sequences.

.

.

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6
Generic image for table
TABLE 3

Reported conditions for activation and discharge of polar tubes

Also known as .

Citation: Keohane E, Weiss L. 1999. The Structure, Function, and Composition of the Microsporidian Polar Tube, p 196-224. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch6

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