Mutations in PIH proteins MOT48, TWI1 and PF13 define common and unique steps for preassembly of each, different ciliary dynein

Yamamoto, Ryōichi; Yanagi, Shiho; Nagao, Masahito; Yamasaki, Yuya; Tanaka, Yoshinori; Sale, Winfield S.; Yagi, Toshiki; Kon, Takahide

doi:10.1371/journal.pgen.1009126

Cited by 19 publications

(22 citation statements)

References 73 publications

(160 reference statements)

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“…Interestingly, this result may relate to the partial co-localization of Dnali1 with Dnai2 ( Figure 2—figure supplement 1C ) and reflects the known intimate link between assembly of ODAs and IDA- c (e.g. Yamaguchi et al, 2018 ; Yamamoto et al, 2020 ).…”

Section: Resultsmentioning

confidence: 86%

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Functional partitioning of a liquid-like organelle during assembly of axonemal dyneins

Lee

Cox

Papoulas

et al. 2020

eLife

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Ciliary motility is driven by axonemal dyneins that are assembled in the cytoplasm before deployment to cilia. Motile ciliopathy can result from defects in the dyneins themselves or from defects in factors required for their cytoplasmic pre-assembly. Recent work demonstrates that axonemal dyneins, their specific assembly factors, and broadly acting chaperones are concentrated in liquid-like organelles in the cytoplasm called DynAPs (Dynein Axonemal Particles). Here, we use in vivo imaging in Xenopus to show that inner dynein arm (IDA) and outer dynein arm (ODA) subunits are partitioned into non-overlapping sub-regions within DynAPs. Using affinity purification mass-spectrometry of in vivo interaction partners, we also identify novel partners for inner and outer dynein arms. Among these, we identify C16orf71/Daap1 as a novel axonemal dynein regulator. Daap1 interacts with ODA subunits, localizes specifically to the cytoplasm, is enriched in DynAPs, and is required for the deployment of ODAs to axonemes. Our work reveals a new complexity in the structure and function of a cell-type specific liquid-like organelle that is directly relevant to human genetic disease.

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Section: Resultsmentioning

confidence: 86%

“…2-figure supplement 1C) and reflects the known intimate link between assembly of ODAs and IDA-c (e.g. (Yamaguchi et al, 2018;Yamamoto et al, 2020).…”

Section: Daap1 Is Required For Deployment Of Odas To the Axonemementioning

confidence: 98%

Functional partitioning of a liquid-like organelle during assembly of axonemal dyneins

Lee

Cox

Papoulas

et al. 2020

eLife

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“…One approach is to determine the IDA structure of the last eukaryotic common ancestor (LECA), which is thought to possess cilia (Mitchell, 2017; Satir, Mitchell, & Jekely, 2008). The Chlamydomonas mutant lacking most of IDAs is paralyzed (Huang et al, 1979; Yamamoto et al, 2017, 2020), while mutants lacking all ODAs can still produce ciliary movement at reduced beat frequency (Kamiya, 1988; Mitchell & Rosenbaum, 1985). One interesting idea is that IDA and ODA have evolved together to amplify the efficiency and power for ciliary beating.…”

Section: Remaining Questions and Challengesmentioning

confidence: 99%

“…In addition, mutants lacking all ODAs ( oda strains) can still move albeit at reduce beat frequency (Kamiya, 1988; Mitchell & Rosenbaum, 1985). In contrast, failure in assembly of multiple IDAs (e.g., the pf23 mutant) results in paralyzed cilia or in defective motility (Huang, Piperno, & Luck, 1979; Yamamoto et al, 2017, 2020). Notably, most of the proteins associated with IDAs, including IDA subunits, are conserved in eukaryotic organisms that bear motile cilia (Wickstead & Gull, 2007), and recent studies revealed unexpected links between IDAs and human diseases (Ben Khelifa et al, 2014; Bustamante‐Marin et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2021

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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.

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“…2-figure supplement 1C) and reflects the known intimate link between assembly of ODAs and IDA- c (e.g. (Yamaguchi et al, 2018; Yamamoto et al, 2020).…”

Section: Resultsmentioning

confidence: 99%

Functional partitioning of a liquid-like organelle during assembly of axonemal dyneins

Lee

Cox

Papoulas

et al. 2020

Preprint

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Ciliary motility is driven by axonemal dyneins that are assembled in the cytoplasm before deployment to cilia. Motile ciliopathy can result from defects in the dyneins themselves or from defects in factors required for their cytoplasmic pre-assembly. Recent work demonstrates that axonemal dyneins, their specific assembly factors, and broadly acting chaperones are concentrated in liquid-like organelles in the cytoplasm called DynAPs. Here, we use in vivo imaging to show that inner dynein arm (IDA) and outer dynein arm (ODA) subunits are partitioned into non-overlapping sub-regions within DynAPs. Using affinity purification massspectrometry of in vivo interaction partners, we also identify novel partners for inner and outer dynein arms. Among these, we identify C16orf71/Daap1 as a novel axonemal dynein regulator. Daap1 interacts with ODA subunits, localizes specifically to the cytoplasm, is enriched in DynAPs, and is required for the deployment of ODAs to axonemes. Our work reveals a new complexity in the structure and function of a cell-type specific liquid-like organelle that is directly relevant to a human genetic disease.

show abstract

Mutations in PIH proteins MOT48, TWI1 and PF13 define common and unique steps for preassembly of each, different ciliary dynein

Cited by 19 publications

References 73 publications

Functional partitioning of a liquid-like organelle during assembly of axonemal dyneins

Functional partitioning of a liquid-like organelle during assembly of axonemal dyneins

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

Functional partitioning of a liquid-like organelle during assembly of axonemal dyneins

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