Composition and function of ciliary inner‐dynein‐arm subunits studied in Chlamydomonas reinhardtii

Abstract

Motile cilia (also interchangeably called “flagella”) are conserved organelles extending from the surface of many animal cells and play essential functions in eukaryotes, including cell motility and environmental sensing. Large motor complexes, the ciliary dyneins, are present on ciliary outer‐doublet microtubules and drive movement of cilia. Ciliary dyneins are classified into two general types: the outer dynein arms (ODAs) and the inner dynein arms (IDAs). While ODAs are important for generation of force and regulation of ciliary beat frequency, IDAs are essential for control of the size and shape of the bend, features collectively referred to as waveform. Also, recent studies have revealed unexpected links between IDA components and human diseases. In spite of their importance, studies on IDAs have been difficult since they are very complex and composed for several types of IDA motors, each unique in composition and location in the axoneme. Thanks in part to genetic, biochemical, and structural analysis of Chlamydomonas reinhardtii, we are beginning to understand the organization and function of the ciliary IDAs. In this review, we summarize the composition of Chlamydomonas IDAs particularly focusing on each subunit, and discuss the assembly, conservation, and functional role(s) of these IDA subunits. Furthermore, we raise several additional questions/challenges regarding IDAs, and discuss future perspectives of IDA studies.

Ordered deployment of distinct ciliary beating machines in growing axonemes of vertebrate multiciliated cells

“…While ODAs drive ciliary beating, a larger and more diverse set of IDAs tune the waveform (Fig. 1A, right)(Yamamoto et al, 2021). We next examined the IDA(f) subunit Wdr78 and the IDA(a,c,d) subunit Dnali1 and found that each deployed substantially faster than did the ODAs (Fig.…”

“…For example, Microtubule Inner Proteins (MIPs) project inside the outer doublet microtubules, provide structural stability, and likely regulate axonemal dynein function (Ichikawa and Bui, 2018). The axonemal dyneins, in turn, reside outside these doublet microtubules, and include both the outer and inner dynein arms (ODAs, IDAs) (King, 2018;Yamamoto et al, 2021). In the center of the axoneme are the central pair microtubules and these are surrounded by the central apparatus (Loreng and Smith, 2017).…”

FBB18 participates in preassembly of almost all axonemal dyneins independent of R2TP complex

“…Interestingly, only three but none of the other subunits of IDA were enriched. IC140 and IC97 are components of double-headed dyneins while p28 is a component of dynein a, c, and d [ 1 ]. Taken together, these data suggest that FBB18 participates in the folding/maturation of most of the DHCs and likely some of the IDA accessory components before they are assembled into large dynein complexes for transporting into cilia though we do not exclude other possibilities.…”

“…In addition to propelling sperm movement, it functions in circulation of cerebrospinal fluid in the brain, mucus clearance in airways, egg movement in fallopian tubes, sperm transport from testis to epididymis and nodal flow in embryonic node. Ciliary beating requires axonemal dyneins, which consist of heavy chains (HCs), intermediate chains (ICs), light intermediate chains (LICs) and light chains (LCs) while the exact composition of each dynein differs [ 1 , 2 ]. The axonemal dyneins are organized into outer and inner dynein arms (ODAs and IDAs) as revealed by electron microscopy.…”

Proteomic analysis of flagella fromChlamydomonasmutants lacking the central pair apparatus reveals loss of radial spoke head proteins

“…The internal structure of most motile cilia and flagella consists of nine parallel doublet microtubules arranged around a central pair of singlet microtubules ( Figure 1A ). Force for propulsion is provided by thousands of dynein motors, anchored in two rows along one side of each doublet and organized into multi-headed complexes called the inner and outer dynein arms (DiBella 2001; Yamamoto 2021), that can walk along the microtubule of the adjacent doublet.…”