Choosing sides – asymmetric centriole and basal body assembly

Abstract

Centrioles and basal bodies (CBBs) are microtubule-rich cylindrical structures that nucleate and organize centrosomes and cilia, respectively. Despite their apparent ninefold rotational symmetry, the nine sets of triplet microtubules in CBBs possess asymmetries in their morphology and in the structures that associate with them. These asymmetries define the position of nascent CBB assembly, the orientation of ciliary beating, the orientation of spindle poles and the maintenance of cellular geometry. For some of these functions, the orientation of CBBs is first established during new CBB biogenesis when the daughter structure is positioned adjacent to the mother. The mother CBB organizes the surrounding environment that nascent CBBs are born into, thereby providing a nest for the new CBB to develop. Protists, including ciliates and algae, highlight the importance of this environment with the formation of asymmetrically placed scaffolds onto which new basal bodies assemble and are positioned. Recent studies illuminate the positioning of nascent centrioles relative to a modular pericentriolar material (PCM) environment and suggest that, like ciliates, centrosomes organize an immediate environment surrounding centrioles for their biogenesis and positioning. In this Commentary, I will explore the positioning of nascent CBB assembly as the first event in building cellular asymmetries and describe how the environment surrounding both basal bodies and centrioles may define asymmetric assembly.

The Rise of the Cartwheel: Seeding the Centriole Organelle

“…Part of the answer may come from the observation that the procentriole assembles in the vicinity of a particular microtubule triplet of the parental centriole in several unicellular organisms. Thus, the Chlamydomonas, Paramecium , and Tetrahymena centrioles contain asymmetric structural elements that enable specific triplet microtubules to be identified . Interestingly, the cartwheel assembles next to a given microtubule triplet of the parental centriole in these species.…”

“…Thus, the Chlamydomonas, Paramecium, and Tetrahymena centrioles contain asymmetric structural elements that enable specific triplet microtubules to be identified. [17,55,56] Interestingly, the cartwheel assembles next to a given microtubule triplet of the parental centriole in these species. This raises the possibility that the parental centriole is not a perfect radially symmetric structure, but instead a cylinder with distinct molecular ensembles next to given triplet microtubules, as is the case in flagella.…”

Primary Cilium Polarity: Morphogenetic Consequences<strong> </strong><strong> </strong>

“…Mouse node and zebrafish Kupffer's vesicle show how centrioles and centrosomes may actually work in Left-Right patterning. Geimer and Melkonian (2004; reviewed by Marshall (2012, Pearson, (2014, Dutcher and O'Toole (2016) described inside the basal-body of Chlamydomonas "an 'acorn-like' asymmetric structure, adhering in a highly inter-individual reproducible and invariable manner to triplets N. 2-1-9-8-7" and another structure, shaped like the uppercase letter 'V' (centrin V-fiber) in contact with triplets N. 9, 5 and 4: "Whereas the cartwheel is thought to nucleate the nine-fold rotational symmetry of the microtubular triplets, the acorn might play an equally important role imposing rotational asymmetry on the microtubular triplets, perhaps leading to the asymmetric assembly of basal-body-associated fibers and hence cellular asymmetry in general" (Geimer and Melkonian, 2004). A marker of "rotational asymmetry" can be arranged clockwise or counter-clockwise like a belt, thus originating two enantiomeric structures, inversely polarized; indeed, it seems that the 9-fold architecture of ciliary locomotive machinery has been utilized to build discrete geometric tools, circumferentially polarized for carrying out finely tuned directional tasks: centriole 9-fold architecture has been adopted by distal and subdistal appendages of mother centrioles, transition fibers of basal bodies, Y-shaped linkers of the cilium transition zone, pericentriolar material of centrosomes, whose 9-scaffold toroidal geometry is sustained by pericentrin (Mennella et al, 2012;Mennella 2014).…”

Primary cilium polarity: morphogenetic consequences.

“…Mouse node and zebrafish Kupffer's vesicle show how centrioles and centrosomes may actually work in Left-Right patterning. Geimer and Melkonian (2004; reviewed by Marshall (2012, Pearson, (2014, Dutcher and O'Toole (2016) described inside the basal-body of Chlamydomonas "an 'acorn-like' asymmetric structure, adhering in a highly inter-individual reproducible and invariable manner to triplets N. 2-1-9-8-7" and another structure, shaped like the uppercase letter 'V' (centrin V-fiber) in contact with triplets N. 9, 5 and 4: "Whereas the cartwheel is thought to nucleate the nine-fold rotational symmetry of the microtubular triplets, the acorn might play an equally important role imposing rotational asymmetry on the microtubular triplets, perhaps leading to the asymmetric assembly of basal-body-associated fibers and hence cellular asymmetry in general" (Geimer and Melkonian, 2004). A marker of "rotational asymmetry" can be arranged clockwise or counter-clockwise like a belt, thus originating two enantiomeric structures, inversely polarized; indeed, it seems that the 9-fold architecture of ciliary locomotive machinery has been utilized to build discrete geometric tools, circumferentially polarized for carrying out finely tuned directional tasks: centriole 9-fold architecture has been adopted by distal and subdistal appendages of mother centrioles, transition fibers of basal bodies, Y-shaped linkers of the cilium transition zone, pericentriolar material of centrosomes, whose 9-scaffold toroidal geometry is sustained by pericentrin (Mennella et al, 2012;Mennella 2014).…”