The centrosome and spindle as a ribonucleoprotein complex

Abstract

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 ...

Crucial steps to life: From chemical reactions to code using agents

“…Additionally we find this phenomenon in very conserved DNA genome content such as telomeres and centromeres (Witzany, 2008;Alliegro, 2011).…”

RNA localization regulates diverse and dynamic cellular processes

“…The centrosome is the major microtubule organizing center of most animal cells and directs the formation of the mitotic spindle in dividing cells . While the centrosome is often discussed as a proteinaceous organelle, there are longstanding hints that RNA may contribute to its biology (see Marshall and Rosenbaum and Alliegro). There are multiple, non‐exclusive hypotheses for the function of RNA at centrosomes (Figure ).…”

Centrosome RNA: A Molecular Basis for Non-Equivalence of Triplets in Centrioles and Centrosomes?

“…A single-stranded RNA ring (memorized linearly in DNA, which encodes nine different molecular labels, in an orderly sequence and equally spaced) possesses all the characteristics to be the molecular platform of the non-equivalence of the nine centriolar blades. A ring of RNA can, in turn, bind different polypeptides to form ribonucleoproteins [22] or various oligosaccharides [23].…”

“…Hiedemann et al, reported RNase sensitivity of Chlamydomonas basal bodies; Snyder [24] showed that RNase inhibited microtubule nucleation in PtK1 cells; Alliegro et al, [22,[25][26][27] isolated centrosomal RNAs (cnRNAs), absent from the remaining cytoplasm, in Spisula Solidissima; Chichinadze [28] and colleagues continued the studies on Spisula cnRNAs, focusing attention on a reverse transcriptase domain and a ribonucleoprotein consensus RNA-binding site contained in one of cnRNAs. The importance of RNA in centrosomes has been reaffirmed also by Ishigaki et al showing that RBM8A/MAGOH heterodimer (a member of exon junction complex on exporting mRNA, required for mRNA splicing, mRNA export and nonsense-mediated mRNA decay) formed a complex in centrosomes.…”