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Seminars in Cell & Developmental Biology Sep 2021Centrosomes were first described by Edouard Van Beneden and named and linked to chromosome segregation by Theodor Boveri around 1870. In the 1960-1980s, electron... (Review)
Review
Centrosomes were first described by Edouard Van Beneden and named and linked to chromosome segregation by Theodor Boveri around 1870. In the 1960-1980s, electron microscopy studies have revealed the remarkable ultrastructure of a centriole -- a nine-fold symmetrical microtubular assembly that resides within a centrosome and organizes it. Less than two decades ago, proteomics and genomic screens conducted in multiple species identified hundreds of centriole and centrosome core proteins and revealed the evolutionarily conserved nature of the centriole assembly pathway. And now, super resolution microscopy approaches and improvements in cryo-tomography are bringing an unparalleled nanoscale-detailed picture of the centriole and centrosome architecture. In this chapter, we summarize the current knowledge about the architecture of human centrioles. We discuss the structured organization of centrosome components in interphase, focusing on localization/function relationship. We discuss the process of centrosome maturation and mitotic spindle pole assembly in centriolar and acentriolar cells, emphasizing recent literature.
Topics: Centrioles; Centrosome; Humans; Interphase
PubMed: 33836946
DOI: 10.1016/j.semcdb.2021.03.020 -
Current Opinion in Structural Biology Feb 2021Centrioles are microtubule-based structures involved in cell division and ciliogenesis. Centriole formation is a highly regulated cellular process and aberrations in... (Review)
Review
Centrioles are microtubule-based structures involved in cell division and ciliogenesis. Centriole formation is a highly regulated cellular process and aberrations in centriole structure, size or numbers have implications in multiple human pathologies. In this review, we propose that the proteins that control centriole length can be subdivided into two classes based on their antagonistic activities on centriolar microtubules, which we refer to as 'centriole elongation activators' (CEAs) and 'centriole elongation inhibitors' (CEIs). We discuss and illustrate the structure-function relationship of CEAs and CEIs as well as their interaction networks. Based on our current knowledge, we formulate some outstanding open questions in the field and present possible routes for future studies.
Topics: Cell Cycle; Cell Cycle Proteins; Centrioles; Humans; Microtubules; Proteins
PubMed: 33220554
DOI: 10.1016/j.sbi.2020.10.011 -
Philosophical Transactions of the Royal... Sep 2014Centrioles are among the largest protein-based structures found in most cell types, measuring approximately 250 nm in diameter and approximately 500 nm long in... (Review)
Review
Centrioles are among the largest protein-based structures found in most cell types, measuring approximately 250 nm in diameter and approximately 500 nm long in vertebrate cells. Here, we briefly review ultrastructural observations about centrioles and associated structures. At the core of most centrioles is a microtubule scaffold formed from a radial array of nine triplet microtubules. Beyond the microtubule triplets of the centriole, we discuss the critically important cartwheel structure and the more enigmatic luminal density, both found on the inside of the centriole. Finally, we discuss the connectors between centrioles, and the distal and subdistal appendages outside of the microtubule scaffold that reflect centriole age and impart special functions to the centriole. Most of the work we review has been done with electron microscopy or electron tomography of resin-embedded samples, but we also highlight recent work performed with cryoelectron microscopy, cryotomography and subvolume averaging. Significant opportunities remain in the description of centriolar structure, both in mapping of component proteins within the structure and in determining the effect of mutations on components that contribute to the structure and function of the centriole.
Topics: Cell Cycle; Centrioles; Cryoelectron Microscopy; Electron Microscope Tomography; Microtubules; Models, Molecular; Species Specificity
PubMed: 25047611
DOI: 10.1098/rstb.2013.0457 -
Open Biology Nov 2023Centrioles are microtubule-based structures crucial for forming flagella, cilia and centrosomes. Through these roles, centrioles are critical notably for proper cell... (Review)
Review
Centrioles are microtubule-based structures crucial for forming flagella, cilia and centrosomes. Through these roles, centrioles are critical notably for proper cell motility, signalling and division. Recent years have advanced significantly our understanding of the mechanisms governing centriole assembly and architecture. Although centrioles are typically very stable organelles, persisting over many cell cycles, they can also be eliminated in some cases. Here, we review instances of centriole elimination in a range of species and cell types. Moreover, we discuss potential mechanisms that enable the switch from a stable organelle to a vanishing one. Further work is expected to provide novel insights into centriole elimination mechanisms in health and disease, thereby also enabling scientists to readily manipulate organelle fate.
Topics: Centrioles; Centrosome; Cell Cycle; Microtubules; Cilia
PubMed: 37963546
DOI: 10.1098/rsob.230222 -
Current Opinion in Cell Biology Aug 2022Multiciliated cells (MCC) are evolutionary conserved, highly specialized cell types that contain dozens to hundreds of motile cilia that they use to propel fluid... (Review)
Review
Multiciliated cells (MCC) are evolutionary conserved, highly specialized cell types that contain dozens to hundreds of motile cilia that they use to propel fluid directionally. To template these cilia, each MCC produces between 30 and 500 basal bodies via a process termed centriole amplification. Much progress has been made in recent years in understanding the pathways involved in MCC fate determination, differentiation, and ciliogenesis. Recent studies using mammalian cell culture systems, mice, Xenopus, and other model organisms have started to uncover the mechanisms involved in centriole and cilia biogenesis. Yet, how MCC progenitor cells regulate the precise number of centrioles and cilia during their differentiation remains largely unknown. In this review, we will examine recent findings that address this fundamental question.
Topics: Animals; Cell Differentiation; Centrioles; Cilia; Mammals; Mice; Xenopus laevis
PubMed: 35716530
DOI: 10.1016/j.ceb.2022.102105 -
Molecular and Cellular Endocrinology Dec 2020Centrioles are eukaryotic subcellular structures that produce and regulate massive cytoskeleton superstructures. They form centrosomes and cilia, regulate new centriole... (Review)
Review
Centrioles are eukaryotic subcellular structures that produce and regulate massive cytoskeleton superstructures. They form centrosomes and cilia, regulate new centriole formation, anchor cilia to the cell, and regulate cilia function. These basic centriolar functions are executed in sperm cells during their amplification from spermatogonial stem cells during their differentiation to spermatozoa, and finally, after fertilization, when the sperm fuses with the egg. However, sperm centrioles exhibit many unique characteristics not commonly observed in other cell types, including structural remodeling, centriole-flagellum transition zone migration, and cell membrane association during meiosis. Here, we discuss five roles of sperm centrioles: orchestrating early spermatogenic cell divisions, forming the spermatozoon flagella, linking the spermatozoon head and tail, controlling sperm tail beating, and organizing the cytoskeleton of the zygote post-fertilization. We present the historic discovery of the centriole as a sperm factor that initiates embryogenesis, and recent genetic studies in humans and other mammals evaluating the current evidence for the five functions of sperm centrioles. We also examine information connecting the various sperm centriole functions to distinct clinical phenotypes. The emerging picture is that centrioles are essential sperm components with remarkable functional diversity and specialization that will require extensive and in-depth future studies.
Topics: Animals; Cell Differentiation; Centrioles; Embryonic Development; Fertilization; Humans; Male; Meiosis; Spermatozoa
PubMed: 32810575
DOI: 10.1016/j.mce.2020.110987 -
Seminars in Cell & Developmental Biology Mar 2023Centrioles are microtubule-based cell organelles present in most eukaryotes. They participate in the control of cell division as part of the centrosome, the major... (Review)
Review
Centrioles are microtubule-based cell organelles present in most eukaryotes. They participate in the control of cell division as part of the centrosome, the major microtubule-organizing center of the cell, and are also essential for the formation of primary and motile cilia. During centriole assembly as well as across its lifetime, centriolar tubulin display marks defined by post-translational modifications (PTMs), such as glutamylation or acetylation. To date, the functions of these PTMs at centrioles are not well understood, although pioneering experiments suggest a role in the stability of this organelle. Here, we review the current knowledge regarding PTMs at centrioles with a particular focus on a possible link between these modifications and centriole's architecture, and propose possible hypothesis regarding centriolar tubulin PTMs's function.
Topics: Centrioles; Tubulin; Microtubule-Organizing Center; Microtubules; Cilia
PubMed: 34896019
DOI: 10.1016/j.semcdb.2021.12.001 -
Annual Review of Biochemistry Jun 2019The centriole is an ancient microtubule-based organelle with a conserved nine-fold symmetry. Centrioles form the core of centrosomes, which organize the interphase... (Review)
Review
The centriole is an ancient microtubule-based organelle with a conserved nine-fold symmetry. Centrioles form the core of centrosomes, which organize the interphase microtubule cytoskeleton of most animal cells and form the poles of the mitotic spindle. Centrioles can also be modified to form basal bodies, which template the formation of cilia and play central roles in cellular signaling, fluid movement, and locomotion. In this review, we discuss developments in our understanding of the biogenesis of centrioles and cilia and the regulatory controls that govern their structure and number. We also discuss how defects in these processes contribute to a spectrum of human diseases and how new technologies have expanded our understanding of centriole and cilium biology, revealing exciting avenues for future exploration.
Topics: Animals; Cell Cycle; Centrioles; Cilia; Ciliopathies; Eukaryota; Humans; Mitosis; Organelle Biogenesis; Signal Transduction
PubMed: 30601682
DOI: 10.1146/annurev-biochem-013118-111153 -
Current Opinion in Genetics &... Jun 2019Multiciliated cells (MCCs) are specialized in fluid propulsion through directional beating of myriads of superficial motile cilia, which rest on modified centrioles... (Review)
Review
Multiciliated cells (MCCs) are specialized in fluid propulsion through directional beating of myriads of superficial motile cilia, which rest on modified centrioles named basal bodies. MCCs are found throughout metazoans, and serve functions as diverse as feeding and locomotion in marine organisms, as well as mucus clearance, cerebrospinal fluid circulation, and egg transportation in mammals. Impaired MCC differentiation or activity causes diseases characterized by severe chronic airway infections and reduced fertility. Through studies in Xenopus and mouse mainly, MCC biology has made significant progress on several fronts in recent years. The gene regulatory network that controls MCC specification and differentiation has been deciphered to a large extent. The enigmatic deuterosomes, which serve as centriole amplification platforms in vertebrate MCCs, have started to be studied at the molecular level. Principles of ciliary beating coordination within and between MCCs have been identified.
Topics: Animals; Cell Differentiation; Centrioles; Cilia; Ependyma; Epidermis; Mice; Microscopy, Electron, Scanning; Trimethoprim, Sulfamethoxazole Drug Combination; Xenopus laevis
PubMed: 31102978
DOI: 10.1016/j.gde.2019.04.006 -
Reproduction (Cambridge, England) Feb 2019Cells that divide during embryo development require precisely two centrioles during interphase and four centrioles during mitosis. This precise number is maintained by... (Review)
Review
Cells that divide during embryo development require precisely two centrioles during interphase and four centrioles during mitosis. This precise number is maintained by allowing each centriole to nucleate only one centriole per cell cycle (i.e. centriole duplication). Yet, how the first cell of the embryo, the zygote, obtains two centrioles has remained a mystery in most mammals and insects. The mystery arose because the female gamete (oocyte) is thought to have no functional centrioles and the male gamete (spermatozoon) is thought to have only one functional centriole, resulting in a zygote with a single centriole. However, recent studies in fruit flies, beetles and mammals, including humans, suggest an alternative explanation: spermatozoa have a typical centriole and an atypical centriole. The sperm typical centriole has a normal structure but distinct protein composition, whereas the sperm atypical centriole is distinct in both. During fertilization, the atypical centriole is released into the zygote, nucleates a new centriole and participates in spindle pole formation. Thus, the spermatozoa's atypical centriole acts as a second centriole in the zygote. Here, we review centriole biology in general and especially in reproduction, we describe the discovery of the spermatozoon atypical centriole, and we provide an updated model for centriole inherence during sexual reproduction. While we focus on humans and other non-rodent mammals, we also provide a broader evolutionary perspective.
Topics: Animals; Centrioles; Embryo, Mammalian; Embryonic Development; Female; Fertilization; Humans; Male; Mitosis; Oocytes; Spermatozoa
PubMed: 30496124
DOI: 10.1530/REP-18-0350