Centrosomes and Cilia: Always at the Center of the Action

EDITORIAL

https://doi.org/10.1038/s42003-020-01519-7 OPEN Centrosomes and cilia: always at the center of the action

✉ Tiago J. Dantas1,2

Centrosomes are the main microtubule-organizing centers in animal cells, indispensable for cell divi-

1234567890():,; sion and the building of a wide range of cilia, which include sensory and motile cilia. We are now inviting submissions related to the fascinating ﬁeld of centrosomes, cilia and all of the processes that they are involved in with the aim of highlighting this work in a Special Collection.

he term centrosome was ﬁrst the microtubule cytoskeleton. The interaction used by Theodor Boveri in the ofcentrosomesandtheirmicrotubulenet- 19th century when referring to work with molecular motors allows the cell to the center body inside the cell. strategically position them, for instance at the TIndeed, we now know that cen- spindle poles during mitosis or in the leading trosomes have a central role in a vast process of a migrating neuronal precursor. range of cellular processes, which include Each of the two centrioles at the center mitosis, cytokinesis, ciliogenesis and cell of the PCM is composed of nine micro- migration. Most of these processes rely on tubule triplets elegantly organized in nine- the ability of centrosomes to function as fold symmetry (Fig. 1a). The older, more the main microtubule-organizing centers mature centriole (generally referred to as (MTOCs)1,2. “mother” centriole) has a central role in Intense work over ciliogenesis as it serves as a nucleating basal the last 30 years body for all types of sensory and motile “With your contribution, we has helped unraveling cilia. In fact, the presence of centrioles at believe that we can make this the complexity of this the center of centrosomes is deeply inter- organelle but many connected with the ability of organisms to Collection a very useful questions remain unan- assemble cilia2 and species that do not swered. At its core, each make cilia have “centriole-less” centro- resource to our community and centrosome contains a somes, such as yeast which have spindle pair of barrel-shaped, pole bodies instead. deepen our understanding of microtubule-based cen- During the onset of ciliogenesis, the the underlying causes of the trioles surrounded by a “mother” centriole uses specialized appen- mesh of pericentriolar dages at its distal end to attach to ciliary disorders associated with material (PCM) and vesicles and to the plasma membrane. centriolar satellites. It is Microtubule doublets then extend from the centrosome and cilia the PCM that binds γ- centriole to form the ciliary axoneme dysfunction.” tubulin ring complexes (Fig. 1b), which functions as a highway for to nucleate and anchor specialized molecular motors in a process

1 i3S—Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal. 2 IBMC—Instituto de Biologia Molecular e Celular, Universidade ✉ do Porto, Porto, Portugal. email: [email protected]

COMMUNICATIONS BIOLOGY | (2020) 3:785 | https://doi.org/10.1038/s42003-020-01519-7 | www.nature.com/commsbio 1 EDITORIAL COMMUNICATIONS BIOLOGY | https://doi.org/10.1038/s42003-020-01519-7

For example, spindle positioning is of particular importance for the proliferation of neural progenitors during brain development as the cell division axis is involved in fate determination. Clustering of centrosomes is also an important mechanism being studied as cancer cells with supernumerary centrosomes use it to form pseudo-bipolar spindles, reducing the rate of mitotic catastrophe induced by multi- polarity. The active research of these topics is very promising for identifying and test- ing potential targets of novel chemother- apeutic drugs for cancer treatment.

Call for papers on centrosomes and cilia for a Special Collection The past years have yielded a significant improvement of our understanding of the key players and mechanisms regulating the biogenesis and functions of centrosomes and cilia. We at Communications Biology Fig. 1 The ultrastructure of centrosomes and cilia. Transmission electron microscopy images of (a) are very excited by the recent develop- the nine-fold symmetry of centriolar microtubule triplets in a human U2OS cell, (b) a primary cilium in ments in the field, as illustrated by the a human RPE-1 cell and (c) a centrosome at one of the poles of a mitotic spindle in a chicken DT40 papers we have already published on these – lymphocyte. Scale bars, 200 nm. topics3,5 8. To promote the efforts in advancing centrosome and cilia research, known as intraflagellar transport (IFT). Thus, the mechanisms controlling faithful we decided to organize a Special Collection IFT is an important and very active area of centrosome duplication have been on these topics. We invite you to submit research1,3 as it is essential for building another topic of intensive research1,2,8. studies that dissect further the biogenesis cilia and for most ciliary functions. It is Now we understand that there are two and functions of centrosomes and cilia. We therefore not surprising that mutations in main pathways/modes of producing cen- are also happy to receive studies focusing many genes encoding ciliary and IFT fac- trioles/centrosomes: template-dependent on all of the cellular and developmental tors are associated with multi-system dis- centrosome duplication and de novo processes that these remarkable organelles orders commonly known as ciliopathies. assembly. As implied by the name, the are involved in. We are confident that The severe abnormalities associated with first pathway uses a preexisting centriole state-of-the-art imaging and biochemical defects in cilia often include: neural tube as a template to orthogonally assemble a techniques, will continue to unravel the and brain developmental defects, mental nascent procentriole. This is a highly interplay between the hundreds of com- retardation, blindness, obesity, polydactyly regulated pathway that ensures a tight ponents that integrate centrosomes and and defects in the skeletal system, poly- control over centrosome number in pro- cilia-associated pathways. These approa- cystic kidney and/or liver, infertility, situs liferating cells. Conversely, the de novo ches will also allow our community to inversus and airway infections4. These pathway forms a high number of cen- better understand the surveillance abnormalities in different organs reflect the trioles without the need of a template and mechanisms used by cells to monitor cen- wide range of cilia and their specialized is generally required for the assembly of trosome and cilia integrity/functions. functions in higher organisms5,6. However, high numbers of cilia in multiciliated As an early career researcher at the more work is needed to further understand cells, or in cells that completely lack Institute for Research and Innovation in how mutations in genes encoding different centrioles. Health (i3S) in Portugal, I am also aware of subsets of centrosome/ciliary components Overall, despite recent insights into the the challenges faced by my peers with lead to very different tissue abnormalities sophisticated architecture of centrosomes regards to making our research visible to the during development. and cilia, there is still much to learn larger community. As we develop this Cen- Interestingly, both cilia and centro- about them. For instance, why does each trosome and Cilia Collection at Commu- somes function as signaling hubs and are centrosome have two centrioles rather nications Biology, we aim to be inclusive of intrinsically associated with cell cycle than one, as these duplicate anyway once exciting research from all career levels and progression, cell proliferation and every cell cycle? Also, how do variations hope to contribute to the exposure of young differentiation1,7. In fact, defects in cilia in the structure and composition of each and rising investigators in the field. With disassembly and centrosome integrity type of cilia relate to their specialized your contribution, we believe that we can result in a strong arrest at the G1 to S- functions in different cell types? make this Collection a very useful resource phase transition1. On the other hand, the A parallel exciting area of research is the to our community and deepen our under- presence of supernumerary centrosomes motor-dependent separation and align- standing of the underlying causes of the is also associated with increased chro- ment of centrosomes during the assembly disorders associated with centrosome and mosome mis-segregation and cancer. of the bipolar spindle in mitosis4 (Fig. 1c). cilia dysfunction.

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