scholarly journals Emerging Picture of Deuterosome-Dependent Centriole Amplification in MCCs

Cells ◽  
2018 ◽  
Vol 7 (10) ◽  
pp. 152 ◽  
Author(s):  
Umama Shahid ◽  
Priyanka Singh
Keyword(s):  
Basal Body ◽  
De Novo ◽  
Super Resolution ◽  
Basal Bodies ◽  
Parallel Pathways ◽  
Multiciliated Cells ◽  
Dependent Pathway ◽  
Microtubule Structure

Multiciliated cells (MCCs) have several hair-like structures called cilia, which are required to propel substances on their surface. A cilium is organized from a basal body which resembles a hollow microtubule structure called a centriole. In terminally differentiated MCCs, hundreds of new basal bodies/centrioles are formed via two parallel pathways: the centriole- and deuterosome-dependent pathways. The deuterosome-dependent pathway is also referred to as “de novo” because unlike the centriole-dependent pathway which requires pre-existing centrioles, in the de novo pathway multiple new centrioles are organized around non-microtubule structures called deuterosomes. In the last five years, some deuterosome-specific markers have been identified and concurrent advancements in the super-resolution techniques have significantly contributed to gaining insights about the major stages of centriole amplification during ciliogenesis. Altogether, a new picture is emerging which also challenges the previous notion that deuterosome pathway is de novo. This review is primarily focused on studies that have contributed towards the better understanding of deuterosome-dependent centriole amplification and presents a developing model about the major stages identified during this process.

scholarly journals THE DEVELOPMENT OF BASAL BODIES AND FLAGELLA IN ALLOMYCES ARBUSCULUS

1964 ◽  
Vol 23 (2) ◽  
pp. 339-354 ◽  
Author(s):  
Fernando L. Renaud ◽  
Hewson Swift
Keyword(s):  
Electron Microscope ◽  
Basal Body ◽  
De Novo ◽  
The Other ◽  
Basal Bodies ◽  
Distilled Water ◽  
Vegetative Hypha ◽  
Original Length ◽  
Large Primary ◽  
Hyphal Tip

The development of basal bodies and flagella in the water mold Allomyces arbusculus has been studied with the electron microscope. A small pre-existing centriole, about 160 mµ in length, was found in an inpocketing of the nuclear membrane in the vegetative hypha. Thus, formation of a basal body does not occur de novo. When the hyphal tip started to differentiate into gametangia, the centrioles were found to exist in pairs. One of the members of the pair then grew distally to more than three times its original length, whereas the other remained the same size. The larger centriole would correspond to the basal body of a future gamete. Gametogenesis was usually induced by transferring a "ripe" culture to distilled water. Shortly after this was done, a few vesicles were pinched off from the cell membrane of the gametangium and came in contact with the basal body. Apparently, they fused and formed a large primary vesicle. The flagellum then started to grow by invaginating into it. Flagellar fibers were evident from the very beginning. As the flagellum grew so did the vesicle by fusion with secondary vesicles, thus coming to form the flagellar sheath. The different stages of flagellar morphogenesis are described and the possible interrelationships with other processes are discussed.

scholarly journals Mcidas mutant mice reveal a two-step process for the specification and differentiation of multiciliated cells in mammals

2018 ◽  
Author(s):  
Hao Lu ◽  
Priyanka Anujan ◽  
Feng Zhou ◽  
Yiliu Zhang ◽  
Yan Ling Chong ◽  
...  
Keyword(s):  
Basal Body ◽  
Target Genes ◽  
Initial Step ◽  
Mutant Mice ◽  
Respiratory Disorder ◽  
Basal Bodies ◽  
Cell Cycle Regulators ◽  
Multiciliated Cells ◽  
Motile Cilia ◽  
Body Production

ABSTRACTMotile cilia on multiciliated cells (MCCs) function in fluid clearance over epithelia. Studies with Xenopus embryos and patients with the congenital respiratory disorder reduced generation of multiple motile cilia, have implicated the nuclear protein MCIDAS (MCI), in the transcriptional regulation of MCC specification and differentiation. Recently, a paralogous protein, GMNC, was also shown to be required for MCC formation. Surprisingly, and in contrast to the presently held view, we find that Mci mutant mice can specify MCC precursors. However, these precursors cannot produce multiple basal bodies, and mature into single ciliated cells. We show that MCI is required specifically to induce deuterosome pathway components for the production of multiple basal bodies. Moreover, GMNC and MCI associate differentially with the cell-cycle regulators E2F4 and E2F5, which enables them to activate distinct sets of target genes (ciliary transcription factor genes versus genes for basal body generation). Our data establish a previously unrecognized two-step model for MCC development: GMNC functions in the initial step for MCC precursor specification. GMNC induces Mci expression, which then drives the second step of basal body production for multiciliation.SUMMARY STATEMENTWe show how two GEMININ family proteins function in mammalian multiciliated cell development: GMNC regulates precursor specification and MCIDAS induces multiple basal body formation for multiciliation.

scholarly journals Protein turnover dynamics suggest a diffusion-to-capture mechanism for peri-basal body recruitment and retention of intraflagellar transport proteins

2021 ◽  
pp. mbc.E20-11-0717
Author(s):  
Jaime V.K. Hibbard ◽  
Neftali Vazquez ◽  
Rohit Satija ◽  
John B. Wallingford
Keyword(s):  
Protein Dynamics ◽  
Basal Body ◽  
Fluorescence Recovery After Photobleaching ◽  
Protein Complexes ◽  
Intraflagellar Transport ◽  
Basal Bodies ◽  
Multiciliated Cells ◽  
Capture Mechanism ◽  
Body Components ◽  
Ciliary Signaling

Intraflagellar transport (IFT) is essential for construction and maintenance of cilia. IFT proteins concentrate at the basal body, where they are thought to assemble into trains and bind cargoes for transport. To study the mechanisms of IFT recruitment to this peri-basal body pool, we quantified protein dynamics of eight IFT proteins, as well as five other basal body localizing proteins, using fluorescence recovery after photobleaching in vertebrate multiciliated cells. We found that members of the IFT-A and IFT-B protein complexes show distinct turnover kinetics from other basal body components. Additionally, known IFT sub-complexes displayed shared dynamics, suggesting shared basal body recruitment and/or retention mechanisms. Finally, we evaluated the mechanisms of basal body recruitment by depolymerizing cytosolic MTs, which suggested that IFT proteins are recruited to basal bodies through a diffusion-to-capture mechanism. Our survey of IFT protein dynamics provides new insights into IFT recruitment to basal bodies, a crucial step in ciliogenesis and ciliary signaling.

scholarly journals De novo formation of basal bodies in Naegleria gruberi

2005 ◽  
Vol 169 (5) ◽  
pp. 719-724 ◽  
Author(s):  
Hong-Kyung Kim ◽  
Jeong-Gu Kang ◽  
Shigehiko Yumura ◽  
Charles J. Walsh ◽  
Jin Won Cho ◽  
...  
Keyword(s):  
Western Blotting ◽  
Basal Body ◽  
Gel Electrophoresis ◽  
De Novo ◽  
Myosin Ii ◽  
Basal Bodies ◽  
2D Gel Electrophoresis ◽  
2D Gel ◽  
Naegleria Gruberi

The de novo formation of basal bodies in Naegleria gruberi was preceded by the transient formation of a microtubule (MT)-nucleating complex containing γ-tubulin, pericentrin, and myosin II complex (GPM complex). The MT-nucleating activity of GPM complexes was maximal just before the formation of visible basal bodies and then rapidly decreased. The regulation of MT-nucleating activity of GPM complexes was accomplished by a transient phosphorylation of the complex. Inhibition of dephosphorylation after the formation of basal bodies resulted in the formation of multiple flagella. 2D-gel electrophoresis and Western blotting showed a parallel relationship between the MT-nucleating activity of GPM complexes and the presence of hyperphosphorylated γ-tubulin in the complexes. These data suggest that the nucleation of MTs by GPM complexes precedes the de novo formation of basal bodies and that the regulation of MT-nucleating activity of GPM complexes is essential to the regulation of basal body number.

scholarly journals The Distal Appendage Protein CEP164 Is Essential for Efferent Duct Multiciliogenesis and Male Fertility

2020 ◽  
Author(s):  
Mohammed Hoque ◽  
Danny Chen ◽  
Rex A. Hess ◽  
Feng-Qian Li ◽  
Ken-Ichi Takemaru
Keyword(s):  
Basal Body ◽  
Male Fertility ◽  
Apical Cell ◽  
Proper Function ◽  
Seminiferous Tubules ◽  
Basal Bodies ◽  
Epithelial Surface ◽  
Efferent Ducts ◽  
Multiciliated Cells

AbstractCilia are evolutionarily conserved microtubule-based structures that perform diverse biological functions. Cilia are assembled on basal bodies and anchored to the plasma membrane via distal appendages. Multiciliated cells (MCCs) are a specialized cell type with hundreds of motile multicilia, lining the brain ventricles, airways, and reproductive tracts to propel fluids/substances across the epithelial surface. In the male reproductive tract, MCCs in efferent ducts (EDs) move in a whip-like motion to stir the luminal contents and prevent sperm agglutination. Previously, we demonstrated that the essential distal appendage protein CEP164 recruits Chibby1 (Cby1), a small coiled-coil-containing protein, to basal bodies to facilitate basal body docking and ciliogenesis. Mice lacking CEP164 in MCCs (FoxJ1-Cre;CEP164fl/fl) show a significant loss of multicilia in the trachea, oviduct, and ependyma. In addition, we observed male sterility, however, the precise role of CEP164 in male fertility remained unknown. Here, we report that the seminiferous tubules and rete testis of FoxJ1-Cre;CEP164fl/fl mice exhibit substantial dilation, indicative of dysfunctional multicilia in the EDs. Consistent with these findings, multicilia were hardly detectable in the EDs of FoxJ1-Cre;CEP164fl/fl mice although FoxJ1-positive immature cells were present. Sperm aggregation and agglutination were commonly noticeable in the lumen of the seminiferous tubules and EDs of FoxJ1-Cre;CEP164fl/fl mice. In FoxJ1-Cre;CEP164fl/fl mice, the apical localization of Cby1 and the transition zone marker NPHP1 was severely diminished, suggesting basal body docking defects. TEM analysis of EDs further confirmed basal body accumulation in the cytoplasm of MCCs. Collectively, we conclude that deletion of CEP164 in the MCCs of EDs causes basal body docking defects and loss of multicilia, leading to sperm agglutination, obstruction of EDs, and male infertility. Our study therefore unravels an essential role of the distal appendage protein CEP164 in male fertility.Author SummaryMulticilia are tinny hair-like microtubule-based structures that beat in a whip-like pattern to generate a fluid flow on the apical cell surface. Multiciliated cells are essential for the proper function of major organs such as brain, airway, and reproductive tracts. In the male reproductive system, multiciliated cells are present in the efferent ducts, which are small tubules that connect the testis to the epididymis. However, the importance of multiciliated cells in male fertility remains poorly understood. Here, we investigated the role of the critical ciliary protein CEP164 in male fertility using a mouse model lacking CEP164 in multiciliated cells. Male mice are infertile with reduced sperm counts. We demonstrate that, in the absence of CEP164, multiciliated cells are present in the efferent ducts but fail to extend multicilia due to basal body docking defects. Consistent with this, the recruitment of key ciliary proteins is perturbed. As a result, these mice show sperm agglutination, obstruction of sperm transport, and degeneration of germ cells in the testis, leading to infertility. Our study therefore reveals essential roles of CEP164 in the formation of multicilia in the efferent ducts and male fertility.

scholarly journals REGULATION OF MICROTUBULES IN TETRAHYMENA

1973 ◽  
Vol 56 (2) ◽  
pp. 458-465 ◽  
Author(s):  
Norman E. Williams ◽  
E. Marlo Nelsen
Keyword(s):  
Basal Body ◽  
De Novo ◽  
Basal Bodies ◽  
De Novo Synthesis

Experiments are reported which were designed to test for induced synthesis of microtubule proteins associated with the rapid proliferation of basal bodies and associated intracytoplasmic microtubules which occurs during oral replacement in Tetrahymena. None was found. Instead, it is shown that these structures can be formed with de novo synthesis of as little as 6% of their microtubule proteins. It is suggested that basal body proliferation may be controlled by synthesis of morphogenetic regulator proteins.

scholarly journals WDR5 stabilizes actin architecture to promote multiciliated cell formation

2017 ◽  
Author(s):  
Saurabh S. Kulkarni ◽  
John N. Griffin ◽  
Karel F. Liem ◽  
Mustafa K. Khokha
Keyword(s):  
Cell Surface ◽  
Actin Cytoskeleton ◽  
Basal Body ◽  
Chromatin Modification ◽  
Cell Formation ◽  
Basal Bodies ◽  
Actin Network ◽  
Tissue Morphogenesis ◽  
Multiciliated Cells ◽  
Intracellular Organelles

The actin cytoskeleton is critical to shape cells and pattern intracellular organelles to drive tissue morphogenesis. In multiciliated cells (MCCs), apical actin forms a lattice that drives expansion of the cell surface necessary to host hundreds of cilia. The actin lattice also uniformly distributes basal bodies across this surface. This apical actin network is dynamically remodeled, but the molecules that regulate its architecture remain poorly understood. We identify the chromatin modifier, WDR5, as a regulator of apical F-actin in multiciliated cells. Unexpectedly, WDR5 functions independently of chromatin modification in MCCs. Instead, we discover a scaffolding role for WDR5 between the basal body and F-actin. Specifically, WDR5 binds to basal bodies and migrates apically, where F-actin organizes around WDR5. Using a monomer trap for G-actin, we show that WDR5 stabilizes F-actin to maintain apical lattice architecture. In summary, we identify a novel, non-chromatin role for WDR5 in stabilizing F-actin in multiciliated cells.

scholarly journals Naegleria gruberi De Novo Basal Body Assembly Occurs via Stepwise Incorporation of Conserved Proteins

2010 ◽  
Vol 9 (6) ◽  
pp. 860-865 ◽  
Author(s):  
Lillian K. Fritz-Laylin ◽  
Zoe June Assaf ◽  
Sean Chen ◽  
W. Zacheus Cande
Keyword(s):  
Basal Body ◽  
De Novo ◽  
Unicellular Eukaryote ◽  
Basal Bodies ◽  
Microtubule Cytoskeleton ◽  
Cytoplasmic Microtubule ◽  
Content Type ◽  
Genes Encoding ◽  
Associated Proteins ◽  
Naegleria Gruberi

ABSTRACT Centrioles and basal bodies are discrete structures composed of a cylinder of nine microtubule triplets and associated proteins. Metazoan centrioles can be found at mitotic spindle poles and are called basal bodies when used to organize microtubules to form the core structure of flagella. Naegleria gruberi, a unicellular eukaryote, grows as an amoeba that lacks a cytoplasmic microtubule cytoskeleton. When stressed, Naegleria rapidly (and synchronously) differentiates into a flagellate, forming a complete cytoplasmic cytoskeleton de novo, including two basal bodies and flagella. Here, we show that Naegleria has genes encoding conserved centriole proteins. Using novel antibodies, we describe the localization of three centrosomal protein homologs (SAS-6, γ-tubulin, and centrin-1) during the assembly of the flagellate microtubule cytoskeleton. We also used these antibodies to show that Naegleria expresses the proteins in the same order as their incorporation into basal bodies, with SAS-6 localizing first, followed by centrin and finally γ-tubulin. The similarities between basal body assembly in Naegleria and centriole assembly in animals indicate that mechanisms of assembly, as well as structure, have been conserved throughout eukaryotic evolution.

scholarly journals Protein turnover dynamics suggest a diffusion to capture mechanism for peri-basal body recruitment and retention of intraflagellar transport proteins

2020 ◽  
Author(s):  
Jaime V.K. Hibbard ◽  
Neftali Vazquez ◽  
Rohit Satija ◽  
John B. Wallingford
Keyword(s):  
Protein Dynamics ◽  
Basal Body ◽  
Fluorescence Recovery After Photobleaching ◽  
Protein Complexes ◽  
Intraflagellar Transport ◽  
Transport Proteins ◽  
Basal Bodies ◽  
Multiciliated Cells ◽  
Capture Mechanism ◽  
Body Components

ABSTRACTIntraflagellar transport (IFT) is essential for construction and maintenance of cilia. IFT proteins concentrate at the basal body, where they are thought to assemble into trains and bind cargoes for transport. To study the mechanisms of IFT recruitment to this peri-basal body pool, we quantified protein dynamics of eight IFT proteins, as well as five other basal body localizing proteins, using fluorescence recovery after photobleaching in vertebrate multiciliated cells. We found that members of the IFT-A and IFT-B protein complexes show distinct turnover kinetics from other basal body components. Additionally, known IFT sub-complexes displayed shared dynamics, and these dynamics were not altered during cilia regeneration as compared to homeostasis. Finally, we evaluated the mechanisms of basal body recruitment by depolymerizing cytosolic MTs, which suggested that IFT proteins are recruited to basal bodies through a diffusion-to-capture mechanism. Our survey of IFT protein dynamics provides new insights into IFT recruitment to basal bodies, a crucial step in ciliogenesis.

scholarly journals Tetrahymena Poc1 ensures proper intertriplet microtubule linkages to maintain basal body integrity

2016 ◽  
Vol 27 (15) ◽  
pp. 2394-2403 ◽  
Author(s):  
Janet B. Meehl ◽  
Brian A. Bayless ◽  
Thomas H. Giddings ◽  
Chad G. Pearson ◽  
Mark Winey
Keyword(s):  
Basal Body ◽  
Electron Tomography ◽  
Force Distribution ◽  
Basal Bodies ◽  
Unknown Mechanism ◽  
Ciliary Beating ◽  
Beat Pattern ◽  
Motile Cilia ◽  
Microtubule Structure

Basal bodies comprise nine symmetric triplet microtubules that anchor forces produced by the asymmetric beat pattern of motile cilia. The ciliopathy protein Poc1 stabilizes basal bodies through an unknown mechanism. In poc1∆ cells, electron tomography reveals subtle defects in the organization of intertriplet linkers (A-C linkers) that connect adjacent triplet microtubules. Complete triplet microtubules are lost preferentially near the posterior face of the basal body. Basal bodies that are missing triplets likely remain competent to assemble new basal bodies with nine triplet microtubules, suggesting that the mother basal body microtubule structure does not template the daughter. Our data indicate that Poc1 stabilizes basal body triplet microtubules through linkers between neighboring triplets. Without this stabilization, specific triplet microtubules within the basal body are more susceptible to loss, probably due to force distribution within the basal body during ciliary beating. This work provides insights into how the ciliopathy protein Poc1 maintains basal body integrity.

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