An interference microscopical and cytochemical analysis of local mass changes in the mitotic apparatus during mitosis

Rustad, Ronald C.

doi:10.1016/0014-4827(59)90125-9

Cited by 39 publications

(12 citation statements)

References 6 publications

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“…Early efforts to define the molecular composition of the mitotic apparatus by Amano (1954), Stich (1954), Mazia (1955), Shimamura and Ohta (1956), Rustad (1959), Zimmerman (1960 and others revealed evidence for RNA. These studies had several limitations that have been largely overcome in later years due to the development of higher resolution imaging and more specific histochemical probes.…”

Section: Experimental Backgroundmentioning

confidence: 99%

The centrosome and spindle as a ribonucleoprotein complex

Alliegro

2011

Chromosome Res

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1 The Subject in ContextThe presence of nucleic acids in centrosomes and the spindle have been proposed, observed, and reported since the 1950s. Why did the subject remain, perhaps even until today, such a controversial issue? The explanation is manifold, and includes legitimate concern over contamination from other cellular compartments in biochemical preparations. With a typically high background of cytoplasmic ribosomes, even microscopic images of stained intact cells could be difficult to interpret. Also, evidence for RNA and DNA in centrosomes accumulated for approximately 40 years but was interspersed with contradictory studies, primarily regarding the presence of DNA (reviewed in Johnson and Rosenbaum, 1991;Marshall and Rosenbaum, 2000). Perhaps less tangible but still a likely cause for lingering controversy is that the presence of nucleic acids in the spindle or centrosomes will require us to look differently at these structures from a functional, and more to the point, evolutionary standpoint.From the earliest studies, our overriding focus has been on the protein components of the cell division apparatus. The centrosome, centriole, and particularly the spindle, were long thought of as, first and foremost, microtubule-based structures. After all, microtubules are the most visually dominant structures, at least with the imaging techniques and probes we have had until recently, and tubulin is the dominant protein component. As other protein components were discovered, the analytical frame of reference was usually their protein-protein interactions with tubulin. Nucleic acids, in the form of chromatin, were cargo (albeit with a more proactive role, we learned as time passed). However, there is evidence that all four classes of biomolecules -protein, 2 carbohydrate (Chang et al., 2004), lipid (Ackerman, 1961Tsai et al., 2006), nucleic acid (references below) -are closely associated with the spindle, and integral to its structure and function. We are likely selling this biological machine short by referring to it only as a ribonucleoprotein complex (RNP). These other classes of biomolecules must be incorporated into our models for the genesis and function of the centrosomes and spindle, especially since their presence and activities may precede those of the hallmark proteins we have focused on for so long.Thinking of the cell division apparatus as not just a protein machine, but as a comprehensive unit composed of all classes of biomolecules (almost a cell within a cell) may also help us to understand its evolution, and by extension, eukaryosis. We agree that approaching the cell division apparatus as an evolutionary seme (Margulis et al., 2009) will ultimately be more informative than focusing on individual (or small groups of) molecules. This can make the difference, for example, between viewing nucleic acids or lipids and their respective metabolizing enzymes as later recruits rather than original components. A step in this direction is to broaden our description of the cell division apparatus to that ...

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Section: Experimental Backgroundmentioning

confidence: 99%

The centrosome and spindle as a ribonucleoprotein complex

Alliegro

2011

Chromosome Res

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“…4,36) and presence of ribosome-like particles (12, 33) in the mitotic apparatus has caused speculation that synthesis of protein and filament formation take place concurrently (12). In regard to such a hypothesis, Went (41) has presented contrary evidence and our study of the micronucleus shows that no ribosomes are present when the micronuclear filaments aggregate and function.…”

Section: Discussionmentioning

confidence: 99%

The Structure and Formation of Cilia and Filaments in Rumen Protozoa

Roth

Shigenaka

1964

The Journal of Cell Biology

126

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The large oligotrich rumen protozoa Diplodiniurn ecaudatum and Ophryoscolex caudatus have been studied by electron microscopy during interphase and division. The structure of mature cilia is contrasted with that seen during their formation particularly in a tuft where development lags and is arrested. Here the shaft is only a few micra long and is composed of filaments that have circular cross-sections not in the typical circular arrangement. In their diameter and appearance the filaments are similar to filaments associated with the nuclei during division. The macronucleus has within it randomly directed filaments, while the micronuclcus contains well aligned filaments and other arrangements typical of an intranuclear mitotic process. An extranuclear filament system is also present and is elaborated during division. The infraciliary filament system is particularly elaborate in these organisms.Filaments ranging from 14 to 22 m# have been observed with some tendency for a bimodal distribution in diameters of 15 and 21 m#. Formation of such filaments has been observed and consists of an initial orientation of very fine elements followed by filament formation. The observations are discussed in relation to filament involvements in cell movements. The concepts are discussed that filaments are metastable structures and that the transitions from one state to another are functionally significant.

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“…The question of whether centrosomes or centrioles contain nucleic acids has remained unresolved since biochemical studies of the mitotic apparatus in the 1950s revealed ''pentosenucleic acid'' in the polar regions (4)(5)(6)(7)(8). The consensus, expressed in the most recent review on the subject, concludes that evidence for DNA in centrosomes is lacking and that significant evidence exists to the contrary (9).…”

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confidence: 99%

Centrosome-associated RNA in surf clam oocytes

Alliegro

Alliegro²,

Palazzo³

2006

Proc. Natl. Acad. Sci. U.S.A.

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Centrosomes are the major microtubule-organizing center in animal cells. They are composed of a pair of [9(3) ؉ 0] centrioles surrounded by a relatively ill-defined pericentriolar matrix, provide the ciliary centriole-kinetosome (basal body) progenitor, and organize the assembly of microtubules into the mitotic spindle during cell division. Despite >100 years of microscopic observation and their obvious significance, our understanding of centrosome composition, dynamic organization, and mechanism of action is limited when compared with that of other cellular organelles. Centrosomes duplicate only once per cell cycle to ensure development of a normal bipolar spindle. The initial event in centrosome duplication is centriole replication, which is generative, semiconservative, and independent of the nucleus. Such observations led to the proposal that centrosomes contain their own complement of nucleic acids, possibly representative of an organellar genome comparable with those described for mitochondria and chloroplasts. The consensus in the field is that centrosomes lack DNA but may contain RNA. We isolated centrosomes from oocytes of the surf clam, Spisula solidissima, and purified from them a unique set of RNAs. We show here by biochemical means and subcellular in situ hybridization that the first transcript we analyzed is intimately associated with centrosomes. Sequence analysis reveals that this centrosome-associated RNA encodes a conserved RNA-directed polymerase domain. The hypothesis that centrosomes contain an intrinsic complement of specific RNAs suggests new opportunities to address the century-old problem of centrosome function, heredity, and evolution.centriole ͉ centrosomal RNA ͉ microtubule-organizing center T he process of centrosome duplication is tightly regulated and under the control of both cytoplasmic and intrinsic factors (1, 2) to ensure that a normal bipolar spindle is formed during mitosis and that the genome is divided equally between daughter cells. The first observable event in centrosome duplication is centriole replication. Like mitochondria and chloroplasts, centriole replication in embryos is independent of the nucleus, but unlike the former two classes of organelles, centrioles replicate not by fission but in a semiconservative, generative manner. These and other observations have led some investigators to propose that the centrosome (or more specifically, the centriole) is of endosymbiotic evolutionary origin and, like mitochondria and chloroplasts, may contain its own genome (3).The question of whether centrosomes or centrioles contain nucleic acids has remained unresolved since biochemical studies of the mitotic apparatus in the 1950s revealed ''pentosenucleic acid'' in the polar regions (4-8). The consensus, expressed in the most recent review on the subject, concludes that evidence for DNA in centrosomes is lacking and that significant evidence exists to the contrary (9). The existence of RNA in these organelles, however, remains an open question, although much of the historica...

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An interference microscopical and cytochemical analysis of local mass changes in the mitotic apparatus during mitosis

Cited by 39 publications

References 6 publications

The centrosome and spindle as a ribonucleoprotein complex

The centrosome and spindle as a ribonucleoprotein complex

The Structure and Formation of Cilia and Filaments in Rumen Protozoa

Centrosome-associated RNA in surf clam oocytes

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