An Outer Arm Dynein Conformational Switch Is Required for Metachronal Synchrony of Motile Cilia in Planaria

Rompolas, Panteleimon; Patel‐King, Ramila S.; King, Stephen M.

doi:10.1091/mbc.e10-04-0373

Cited by 105 publications

(120 citation statements)

References 59 publications

(73 reference statements)

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“…As the lack of LC1 would lead to exposure of a hydrophobic region on one HC, this mutation might therefore result in the partial failure of outer arm assembly due to indirect effects mediated through aggregation of other component(s) that are no longer stable in the absence of LC1. This scenario would be consistent with the observed reduction of outer arms in trypanosomes following LC1 RNAi (28), although similar knockdowns in planaria did not appear to affect arm assembly (29).…”

Section: Discussionsupporting

confidence: 83%

“…Similar mutations in Trypanosoma also lead to defective motility (20), whereas RNAi-driven knockdowns caused failure of outer arm dynein assembly (28). In the context of a ciliated epithelium, reduction of LC1 levels in the planarian Schmidtea mediterranea resulted in lower beat frequency and disruption of the hydrodynamic coupling necessary for generating metachronal synchrony but did not appear to affect dynein assembly (29).…”

Section: Discussionmentioning

confidence: 98%

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Functional Architecture of the Outer Arm Dynein Conformational Switch

King

Patel‐King

2012

Journal of Biological Chemistry

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Background: Ciliary dyneins monitor and respond to the mechanical state or curvature of the microtubular axoneme. Results: NMR chemical shift mapping and binding assays define functional subdomains within a key component (LC1) of this system. Conclusion: LC1 provides a direct tether between a dynein motor unit and the microtubule that modulates motor function. Significance: This study provides insight into the mechanism by which dyneins are coordinated during ciliary beating.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 98%

Functional Architecture of the Outer Arm Dynein Conformational Switch

King

Patel‐King

2012

Journal of Biological Chemistry

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“…Further studies will elucidate whether, in a WT situation, both paralogs are involved in signal transduction for a single Wnt ligand. (25,26). To address whether Smed-dvl-1/2 functions as a component of the PCP network, we analyzed the polarization of the ventral epithelium after Smed-dvl-1/2 interference.…”

Section: Resultsmentioning

confidence: 99%

Dishevelled is essential for neural connectivity and planar cell polarity in planarians

Almuedo-Castillo

Saló

Adell

2011

Proc. Natl. Acad. Sci. U.S.A.

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The Wingless/Integrated (Wnt) signaling pathway controls multiple events during development and homeostasis. It comprises multiple branches, mainly classified according to their dependence on β-catenin activation. The Wnt/β-catenin branch is essential for the establishment of the embryonic anteroposterior (AP) body axis throughout the phylogenetic tree. It is also required for AP axis establishment during planarian regeneration. Wnt/β-catenin-independent signaling encompasses several different pathways, of which the most extensively studied is the planar cell polarity (PCP) pathway, which is responsible for planar polarization of cell structures within an epithelial sheet. Dishevelled (Dvl) is the hub of Wnt signaling because it regulates and channels the Wnt signal into every branch. Here, we analyze the role of Schmidtea mediterranea Dvl homologs (Smed-dvl-1 and Smed-dvl-2) using gene silencing. We demonstrate that in addition to a role in AP axis specification, planarian Dvls are involved in at least two different β-catenin-independent processes. First, they are essential for neural connectivity through Smed-wnt5 signaling. Second, Smed-dvl-2, together with the S. mediterranea homologs of Van-Gogh (Vang) and Diversin (Div), is required for apical positioning of the basal bodies of epithelial cells. These data represent evidence not only of the function of the PCP network in lophotrocozoans but of the involvement of the PCP core elements Vang and Div in apical positioning of the cilia.neural patterning | axial polarity | cilia basal body W ingless/Integrated (Wnt) signaling controls multiple events, including cell migration, planar cell polarity (PCP), and stem cell self-renewal (1, 2). It acts through two main pathways: the canonical or β-catenin-dependent pathway and the noncanonical or β-catenin-independent pathways, which include the PCP and Wnt/calcium pathways. Dishevelled (Dvl) is common to all three pathways (3). In the β-catenin-dependent pathway, Dvl is recruited by the receptor Frizzled (Fz), promoting disassembly of the β-catenin destruction complex through the subsequent recruitment of Axin. As a consequence, β-catenin translocates to the nucleus, where it acts as a master regulator. A common role of the β-catenin/Wnt pathway is in establishing the anteroposterior (AP) axis during development (4). PCP signals are transmitted from cell to cell and are responsible for the polarization of cell structures. During PCP signaling, Dvl is also recruited by a Fz receptor and promotes the asymmetrical localization of the PCP core proteins within the cell, such that the Fz-Dvl-Diversin (Div)/-Diego (Dgo) complex is oppositely localized to the Strabismus (Stbm)/Van-Gogh (Vang)-Prickle (Pk) complex. The asymmetrical subcellular localization of these elements in an epithelial sheet directs cytoskeletal reorganization that results, for instance, in a hair emerging solely from the distal edge of the cell (5-7). The same mechanism is used in mesenchymal cells to direct cell movement and migration during gastrulat...

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“…The ventral surface of the planarian epidermis is composed of multiciliated epithelial cells, and in order for normal gliding locomotion to occur, these motile cilia must be formed properly as well as coordinate their beating in 'metachronal synchrony' (Glazer et al, 2010;Rink et al, 2009;Rompolas et al, 2010;Salathe, 2007). If adjacent cilia are not coordinated in their beating, they will not produce net forward movement.…”

Section: Lhx1/5-1 and Pitx Are Required For Ventral Cilia Coordinatiomentioning

confidence: 99%

Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians

2013

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SUMMARYIn contrast to most adult organisms, freshwater planarians can regenerate any injured body part, including their entire nervous system. This allows for the analysis of genes required for both the maintenance and regeneration of specific neural subtypes. In addition, the loss of specific neural subtypes may uncover previously unknown behavioral roles for that neural population in the context of the adult animal. Here we show that two homeodomain transcription factor homologs, Smed-lhx1/5-1 and Smed-pitx, are required for the maintenance and regeneration of serotonergic neurons in planarians. When either lhx1/5-1 or pitx was knocked down by RNA interference, the expression of multiple canonical markers for serotonergic neurons was lost. Surprisingly, the loss of serotonergic function uncovered a role for these neurons in the coordination of motile cilia on the ventral epidermis of planarians that are required for their nonmuscular gliding locomotion. Finally, we show that in addition to its requirement in serotonergic neurons, Smed-pitx is required for proper midline patterning during regeneration, when it is required for the expression of the midline-organizing molecules Smed-slit in the anterior and Smed-wnt1 in the posterior.

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An Outer Arm Dynein Conformational Switch Is Required for Metachronal Synchrony of Motile Cilia in Planaria

Cited by 105 publications

References 59 publications

Functional Architecture of the Outer Arm Dynein Conformational Switch

Functional Architecture of the Outer Arm Dynein Conformational Switch

Dishevelled is essential for neural connectivity and planar cell polarity in planarians

Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians

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