Transition Zone Migration: A Mechanism for Cytoplasmic Ciliogenesis and Postaxonemal Centriole Elongation

Abstract

The cilium is an elongated and continuous structure that spans two major subcellular domains. The cytoplasmic domain contains a short centriole, which serves to nucleate the main projection of the cilium. This projection, known as the axoneme, remains separated from the cytoplasm by a specialized gatekeeping complex within a ciliary subdomain called the transition zone. In this way, the axoneme is compartmentalized. Intriguingly, however, this general principle of cilium biology is altered in the sperm cells of many animals, which instead contain a cytoplasmic axoneme domain. Here, we discuss the hypothesis that the formation of specialized sperm giant centrioles and cytoplasmic cilia is mediated by the migration of the transition zone from its typical location as part of a structure known as the annulus, and examine the intrinsic properties of the transition zone that may facilitate its migratory behavior.

Length-dependent disassembly maintains four different flagellar lengths in Giardia

“…These observations support a mechanism of ciliogenesis that is not diffusion-limited and therefore does not require IFT for assembly of the cytoplasmic axonemal regions. Both mammalian and Drosophila sperm flagella employ variations of cytoplasmic ciliogenesis that require the invagination of the basal body into the cytoplasm following the initiation of compartmentalized ciliogenesis (Avidor-Reiss et al, 2017).…”

“…Due to its wide conservation in diverse microbial and multicellular flagellates, eukaryotic flagellar architecture likely predates the radiation of all extant lineages (Ishikawa, 2017; Sung & Leroux, 2013). Yet eukaryotic morphological diversity is vast, and many eukaryotes possess flagella with varied size, structure, and function presumably evolved from conserved flagellar components and assembly mechanisms (Avidor-Reiss, Ha, & Basiri, 2017; Ishikawa, 2017). Studies of flagellar assembly and length maintenance in diverse microbial eukaryotic lineages allow us to address a central question in evolutionary cell biology: how does cytoskeletal structural and functional variation arise from conserved cytoskeletal components and mechanisms?…”

Editorial: Sperm Differentiation and Spermatozoa Function: Mechanisms, Diagnostics, and Treatment

“…The ciliary transition zone is a gate separating the cilium from the cytoplasm via (Malicki and Avidor-Reiss, 2014). However, uniquely in the sperm, the transition zone migrates and separates the axoneme into two distinct compartments (Basiri et al, 2014;Avidor-Reiss and Leroux, 2015;Avidor-Reiss et al, 2017). Research papers in this collection by Persico et al show that the microtubule-depolymerizing protein Kinesin-13 Klp10A is enriched in the ciliary transition zone and the base of the migrating transition zone of Drosophila melanogaster sperm.…”

Cell type-specific structural plasticity of the ciliary transition zone inC. elegans

“…Universally conserved 9-fold symmetry of eukaryotic centriole structure templates the 9-fold symmetry of ciliary TZ structure (Lemullois et al, 1988;Sorokin, 1962;1968). TZ formation is considered to be a onetime structurally deterministic event whose completion precedes, and is required for, formation of the rest of the ciliary axoneme (Avidor-Reiss et al, 2017;Ishikawa and Marshall, 2011;Nechipurenko et al, 2017).…”