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1 October 2014 Functional Diversity of Axonemal Dyneins as Assessed by in Vitro and in Vivo Motility Assays of Chlamydomonas Mutants
Ritsu Kamiya, Toshiki Yagi
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This review outlines the current knowledge of the functional diversity of axonemal dyneins, as revealed by studies with the model organism Chlamydomonas. Axonemal dyneins, which comprise outer and inner dynein arms, power cilia and flagella beating by producing sliding movements between adjacent outer-doublet microtubules. Outer- and inner-arm dyneins have traditionally been considered similar in structure and function. However, recent evidence suggests that they differ rather strikingly in subunit composition, axonemal arrangement, and molecular motor properties. We posit that these arms make up two largely independent motile systems; whereas outer-arm dynein can generate axonemal beating by itself under certain conditions, inner-arm dynein can generate beating only in cooperation with the central pair/radial spokes. This conclusion is supported by genome analyses of various organisms. Outer-arm dynein appears to be particularly important for nodal cilia of mammalian embryos that function for determination of left-right body asymmetry.


Cilia and flagella are cell organelles that perform a variety of motility and signaling functions. This review addresses their motility mechanisms, focusing on the properties of axonemal dyneins, the motor proteins that generate force (King, 2011), as studied in the model organism Chlamydomonas (Witman, 2009). Most data presented herein may be relevant to motile cilia and flagella of other organisms as well, as the structure and protein composition of the axoneme (internal structure of cilia/flagella) are extremely well conserved among many organisms ranging from protozoa to humans. More specific topics regarding metazoan axonemal dyneins can be found elsewhere (Inaba, 2007, 2011). Because cilia and flagella are essentially identical in structure and function, the term “cilia” will be used to describe both cilia and flagella, while the term “flagella” will only be used when its distinction from cilia is necessary.

Cilia are peculiar organelles that generate bending waves, which produce cell movements or fluid flow over tissue surfaces. This movement is somewhat similar to the undulating motion of eels or snakes, which is generated by neuro-muscular circuits. How this subcellular structure produces such elaborate movements is a long-standing puzzle. In nearly all species, cilia possess a unique “9+2” structure, containing nine microtubules (termed outer-doublet microtubules) surrounding a pair of central microtubules (Fig. 1). Despite extensive studies, the origin of this particular structure and its functional advantages are not yet understood. Another striking feature of motile cilia is the presence of multiple motor protein species (dyneins) within a single cilium. Functional difference between different dyneins will be discussed in detail in this review.

The beating of cilia is generated by dynein-driven sliding between adjacent outer-doublet microtubules (Satir, 1968; Summers and Gibbons, 1971). The basic process of ciliary beating is therefore the same as in other cell motility phenomena, such as muscle contraction and vesicle transport, which are also based on a sliding motion between cytoskeletal filaments and motor proteins. However, the microtubule sliding in cilia has several distinct features not found in other systems. Most importantly, ciliary sliding velocity periodically varies along the length of the nine outer-doublet microtubules. The variability of sliding velocity is the basis for bend formation.

Fig. 1.

Chlamydomonas axoneme. Flagella are demembranated by detergent treatment and observed by thin-section electron microscopy. This photo shows a view from the flagellar bottom to the tip. Nine outer-doublet microtubules (outer-doublets) surround a pair of singlet microtubules (the central pair) at the center, forming the so-called “9+2” structure. ODA, outer dynein arm; IDA, inner dynein arm. * denotes doublet #1, which lacks ODA. All other outer-doublets are numbered #2-#9 in the clockwise direction. Scale bar, 100 nm.


Unlike other cell motility systems, which typically involve only one kind of motor protein, the axoneme uses multiple types. Axonemal dyneins are largely classified as outer- or inner-arm. Biochemical and genetic studies have established that outer-arm dynein comprises a single species containing two (in metazoan and some unicellular organisms) or three (in many unicellular organisms) force-generating dynein heavy chains (DHCs). On the other hand, inner-arm dynein exists as several species