Relationship Between Spatial Pattern of Basal Bodies and Membrane Skeleton (Epiplasm) During the Cell Cycle of <i>Tetrahymena</i>: <i>cdaA</i> Mutant and Anti‐Membrane Skeleton Immunostaining

Kaczanowska, Janina; Bużañska, Leonora; Ostrowski, Marek

doi:10.1111/j.1550-7408.1993.tb04470.x

Cited by 20 publications

(15 citation statements)

References 26 publications

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“…The asymmetry of the developing fission zone has also been documented at the molecular level by the finding that one of the three major membrane-skeletal proteins, the EpiB protein, discovered by Williams and coworkers (162,164), is asymmetrically distributed on opposite sides of the fission zone in predividing and early-dividing cells (84,87), as are other cortical markers (84,85,116).…”

Section: The Organism: Anatomy and Topologymentioning

confidence: 99%

What Do Genic Mutations Tell Us about the Structural Patterning of a Complex Single-Celled Organism?

Frankel

2008

Eukaryot Cell

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PROLOGUE: FROM THE CYTOPLASM TO THE NUCLEUSStructural inheritance in the ciliate cortex. Ciliates make up a distinctive group of unicellular organisms characterized by dualism of germ line and somatic nuclei, sex by reciprocal exchange of gametic nuclei with subsequent replacement of the somatic nucleus, and an extraordinarily complex organization of the cell surface layer. This organization is dominated by cytoskeletal structures, including rows of basal bodies, cilia, and accessory fibrillar structures, and is perpetuated by longitudinal extension of these structural ensembles during clonal growth.This mode of perpetuation provides an ideal opportunity for the demonstration and analysis of cellular heredity at a nongenic level. This opportunity was seized by three gifted biologists, the comparative zoologist Emmanuel Fauré-Fremiet, the experimental embryologist Vance Tartar, and the geneticist Tracy Sonneborn, who together led the way in establishing the principle that structural variations of nongenic origin in the ciliate cortex can indeed be faithfully transmitted to progeny over numerous cell generations.Although this review is primarily devoted to the contribution of genic mutations to the understanding of the ciliate cortex, the interpretation of some of the more interesting of these mutations becomes more meaningful against a background of the three major arenas of nongenic structural inheritance in the ciliate cortex, all of which were solidly established before the genetic approach was initiated.The best-known form of structural inheritance is the organization of the longitudinal ciliary rows that cover the surfaces of most ciliates. This was first demonstrated by Beisson and Sonneborn (12), who showed that an inversion (180°rotation) of one or more ciliary rows of Paramecium tetraurelia (then Paramecium aurelia, syngen 4) (Fig. 1A) could be nongenically inherited; Sonneborn gave the name "cytotaxis" to "this ordering and arranging of new structures under the influence of pre-existing cell structure" (137). This demonstration was later repeated for Tetrahymena thermophila (then Tetrahymena pyriformis, syngen 1) (118) and for other ciliates (62,63,71). It was extended by Nanney's observation that the preexisting number of ciliary rows in T. thermophila tended to be conserved (103, 104), presumably due to the same structural constraints that conserve the geometrical organization of these rows.A second form of structural inheritance is demonstrated by the propagation of the number of complete sets of cortical structures. This was investigated in detail by 32), who noted that ciliates that became fused side by side, as a consequence of blockage of division followed by anterior sliding of the presumptive posterior daughter cell, could propagate their duality. Later, Vance Tartar (147) demonstrated that microsurgically constructed Siamese-twin doublets in the large ciliate Stentor coeruleus could perpetuate their doublet condition. In both cases, the way in which the doublets were created virtually rules o...

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Section: The Organism: Anatomy and Topologymentioning

confidence: 99%

What Do Genic Mutations Tell Us about the Structural Patterning of a Complex Single-Celled Organism?

Frankel

2008

Eukaryot Cell

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“…Prior to cytokinesis, the decrease in the level of Epi B protein follows two segmental gradients in the shell of the apical regions of the parental cell and in the corresponding region of the opisthe ( Fig. 2B; Kaczanowska et al, 1993). In contrast, the "fenestrin protein", the other member of the membrane skeleton transiently appears in apical areas of both nascent offsprings (Nelsen et al, 1994;Kaczanowska et al, 2003).…”

Section: Abstract: Tetrahymena Polarity Cytoskeleton Mark Armadillomentioning

confidence: 99%

“…The assembly of LM-bands is unidirectional (Allen 1967;Ng 1978Ng , 1979Ng and Frankel, 1977) and they play an important role in divisional morphogenesis as a putative cytospindle (JerkaDziadosz et al, 1995). The anterior-posterior axis is preserved during cell division that results in anterior and posterior offspring (Frankel et al, 1981;Frankel 1989;Kaczanowska et al, 1993; 250 J. Kaczanowska et al Nelsen et al, 1994) (Fig. 1A).…”

Section: Abstract: Tetrahymena Polarity Cytoskeleton Mark Armadillomentioning

confidence: 99%

“…Williams, Iowa University, U.S.A.) and the antifenestrin antibodies (9a7 against T. thermophila and 3A7 against T. pyriformis, both in dilution 1:40; (gifts from Drs J. Frankel and N. Williams, Iowa University, U.S.A.). Immunostainings was performed exactly as described earlier (Kaczanowska et al, 1993;1999;2003).…”

Section: Immunostainingmentioning

confidence: 99%

“…Protargol staining was performed according to routine protocol (Kaczanowska et al, 1993). The preparations were used for analysis of the fractional distributions in different morphogenetic stages in accordance with accepted morphological criteria for divisional morphogenesis and for the oral replacement (Frankel,1967;Williams and Frankel, 1973).…”

Section: Permanent Preparationsmentioning

confidence: 99%

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Acquisition of cell polarity during cell cycle and oral replacement in Tetrahymena

Kaczanowska

Kaczanowski²,

Kiersnowska³

et al. 2008

Int. J. Dev. Biol.

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The aim of this study was to search for a mechanism responsible for the acquisition of cell polarity in a ciliate Tetrahymena. Homologs of the mammalian genes coding for CDC42-GSK3β-MARK/PAR1-MAPs proteins were found in the Tetrahymena genome (Eisen et al., 2006, and this study). These proteins belong to a pathway which controls assembly and disassembly of microtubule bundles and cell polarity in neural cells. In Tetrahymena, there are two types of morphogenesis: divisional and oral replacement (OR). In divisional morphogenesis, an elongation of longitudinal microtubule bundles (LMs) takes place during cell division. In contrast, in OR type morphogenesis, which occurs in starved non-dividing cells, a polar retraction of LMs occurs. In T. pyriformis, the frequency of developmental switch to OR morphogenesis increases in the presence of wortmannin, an inhibitor of the CDC42-GSK3β-MARK pathway. In contrast, wortmannin when applied to dividing cells does not affect divisional morphogenesis. Using immunostaining with the antibody against mammalian mitotic phosphoproteins (MPM-2) we show that these proteins co-localize with the LMs and are distributed along the anterior-posterior gradient. In addition, we show that during OR type morphogenesis, the fate of LMs correlates with the anterior-posterior gradient of instability of the cortical structures. We used the conditional mouthless mutant of T. thermophila (Tiedtke et al., 1988) to test if the presence of the oral apparatus is required for the maintenance of cell polarity. We discuss our results in relation to the hypothesis of GSK3-β-MARK pathway involvement in the acquisition of cell polarity in Tetrahymena. KEY WORDS: Tetrahymena, polarity, cytoskeleton, MARK, armadilloThe Tetrahymena (like other ciliates) is a permanently polarized cell. Longitudinal ciliary rows (CR) define its anterior-posterior axis and a sub-apically located oral apparatus (OA) marks its ventral side. The position of other cortical structures depends on the position of the oral apparatus (Frankel 1999) (Fig. 1A and Fig. 7A). In Tetrahymena the spatial deployment of the cytoskeletal proteins is under genetic control of a mechanism of global positioning (Kaczanowski 1975, Williams et al., 1987, JerkaDziadosz et al., 1995, Kaczanowska et al., 2003, StrzyzewskaJowko et al., 2003. The aim of the present study was to gain an insight into the mechanism responsible for the acquisition and maintenance of cell polarity, during morphogenesis of Tetrahymena.In Tetrahymena there are two types of morphogenesis: divisional and oral replacement (OR). The cortex of Tetrahymena contains a regular array of polarized longitudinal microtubular Int. J. Dev. Biol. 52: 249-258 (2008) Abbreviations used in this paper: AF, anarchic field of oral primordium; CR, ciliary rows of basal body units; CVP, the contractile vacuole pore located at the posterior area of the cell to the right of the ventral side; EHT, end of heat treatment; LM, Longitudinal microtubule bands; nOA, newly formed oral apparatus that a...

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Molecular Subdivision of the Cortex of Dividing Tetrahymena Is Coupled with the Formation of the Fission Zone

Kaczanowska

Joachimiak

Bużañska

et al. 1999

Developmental Biology

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In contrast to a mitotic-spindle-associated bipolar cytokinesis, the cytokinesis of polarized ciliates is preceded by a reorganization of the cortex into dual metameric patterns for prospective daughter cells and then separated by a transverse fission line. This study concerns relations between the generation of cortical metamery and the formation of the fission line in an amicronuclear (i.e., without mitotic spindle) ciliate, Tetrahymena pyriformis. The fission line appears in the division of T. pyriformis as a transverse line formed by equatorial gaps in the meridional ciliary rows, with the second oral structure (OA2) formed posterior to it. It was found that the metamery of cortical morphogenesis is expressed by the appearance of increased MPM2 antibody binding in dividing cells in an apical area and posterior to the fission line gaps, including patterned changes of this binding in both oral apparatuses (OA1 and OA2), and by a reciprocal decrease of binding of an anti-epiplasm antibody. These tested antigens are localized to different cortical structures, but in predividing cells both uniformly show formation of the fission line contrast of labeling. A serine/threonine kinase inhibitor, 6-dimethylaminopurine (6-DMAP), was applied to dividing T. pyriformis at specific stages: (1) if 6-DMAP was added to early dividing cells, it prevented cells from initiating cytokinesis. (2) If 6-DMAP was added to cells at stages close to the physiological transition point of cell division, it yielded either (i) a partial formation of the fission line on the ventral side, combined with modified growth of undivided cortex adjacent to the fission line, with abnormal cytokinesis, or (ii) variable anterior displacement of the complete fission line, which contracted slowly but uniformly. (3) If 6-DMAP was applied during cytokinesis, it did not delay cell division, but daughter cells become abnormal and underwent an incomplete oral reorganization. These results suggest that the generation of metamerism in the cortex of T. pyriformis involves differentiation of the asymmetric fission zone. At least four stage-dependent 6-DMAP-sensitive effects jointly control the progress of cell division and the mutual spatial relations between the generation of metamery and the appearance, completeness, and position of the fission zone in the cortex of polarized T. pyriformis.

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Relationship Between Spatial Pattern of Basal Bodies and Membrane Skeleton (Epiplasm) During the Cell Cycle of Tetrahymena: cdaA Mutant and Anti‐Membrane Skeleton Immunostaining

Cited by 20 publications

References 26 publications

What Do Genic Mutations Tell Us about the Structural Patterning of a Complex Single-Celled Organism?

What Do Genic Mutations Tell Us about the Structural Patterning of a Complex Single-Celled Organism?

Acquisition of cell polarity during cell cycle and oral replacement in Tetrahymena

Molecular Subdivision of the Cortex of Dividing Tetrahymena Is Coupled with the Formation of the Fission Zone

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