Shared and Distinct Mechanisms of Compartmentalized and Cytosolic Ciliogenesis

Abstract

Most motile and all non-motile (primary) eukaryotic cilia possess microtubule-based axonemes that are assembled at the cell surface to form hair-like or more elaborate compartments endowed with motility and/or signaling functions. Such compartmentalized ciliogenesis depends on a core intraflagellar transport (IFT) machinery and associated Bardet-Biedl syndrome complex (BBSome) for dynamic delivery of ciliary components. The transition zone (TZ), an ultrastructurally complex barrier (‘gate’) at the base of cilia, also contributes to the formation of compartmentalized cilia. Yet, some ciliated protists do not encode IFT components, and together with some metazoan spermatozoa, use IFT-independent mechanisms to build axonemes exposed to the cytosol. Moreover, various ciliated protists lack TZ components, whereas Drosophila sperm surprisingly requires the activity of dynamically-localized TZ proteins for cytosolic ciliogenesis. Here we discuss the various ways eukaryotes use IFT and/or TZ proteins to generate the wide assortment of compartmentalized and cytosolic cilia observed in nature. Consideration of the different ciliogenic pathways allows us to propose how three types of cytosol-exposed cilia (primary, secondary, tertiary), including that found in the human sperm proximal segment, are likely evolutionary derivations of compartmentalized ciliogenesis.

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

“…Together, these observations have led to the distinction between two broad types of cilia, which are classified as either “cytoplasmic” or “compartmentalized” (Avidor-Reiss and Leroux, 2015; Avidor-Reiss et al, 2004). Although this unique ciliary phenomena occurring in spermatids has been observed for many decades, little is known regarding how or why spermatid ciliogenesis forms giant centrioles and cytoplasmic axonemes.…”

“…Although a general theme of cilium biology is that the axoneme resides within a distinct compartment isolated from the cytoplasm via the transition zone, the exclusion of the axoneme from the cytoplasm is not an absolute requirement for ciliogenesis and examples of cytoplasmic axonemes are not uncommon (Avidor-Reiss and Leroux, 2015). These “cytoplasmic cilia” can occur via three different mechanisms.…”

Centriole Remodeling during Spermiogenesis in Drosophila

“…In some animals, sperm centrioles with typical ultrastructure are the origin of the first centrosomes in the zygote [2–4]. In other animals, however, sperm centrioles lose their proteins and are thought to be degenerated and nonfunctional during spermiogenesis [5, 6]. Here, we show that the two sperm centrioles (the giant centriole (GC) and the Proximal Centriole-Like structure (PCL) in Drosophila melanogaster are remodeled during spermiogenesis through protein enrichment and ultrastructure modification in parallel to previously described centrosomal reduction [7].…”

To beat, or not to beat, that is question! The spectrum of ciliopathies

“…The absence of ribosomes inside the cilium prevents the synthesis of proteins, and so new proteins required for the formation and maintenance of cilia are produced in the cell body and transported into the ciliary body through an intraflagellar transport mechanism (IFT) . IFT is a bidirectional movement of proteins along the axoneme just beneath the ciliary membrane, using specialized microtubule motors of kinesin and dynein origin for anterograde and retrograde transport, respectively …”

“…Cilia can act as motors or antennae, creating fluid movement and sensing the extracellular environment. They have key roles in cell locomotion, mucus or water propulsion, sexual reproduction, embryonic development, signaling, organ function, and homeostasis . Human cilia are usually classified into motile and non‐motile cilia (Figure ), and ciliopathies into motor and sensory ciliopathies .…”