Centriole

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3D rendering of centrioles showing the triplets Blausen 0214 Centrioles.png
3D rendering of centrioles showing the triplets

In cell biology a centriole is a cylindrical organelle composed mainly of a protein called tubulin. [1] Centrioles are found in most eukaryotic cells, but are not present in conifers (Pinophyta), flowering plants (angiosperms) and most fungi, and are only present in the male gametes of charophytes, bryophytes, seedless vascular plants, cycads, and Ginkgo . [2] [3] A bound pair of centrioles, surrounded by a highly ordered mass of dense material, called the pericentriolar material (PCM), [4] makes up a structure called a centrosome. [1]

Contents

Centrioles are typically made up of nine sets of short microtubule triplets, arranged in a cylinder. Deviations from this structure include crabs and Drosophila melanogaster embryos, with nine doublets, and Caenorhabditis elegans sperm cells and early embryos, with nine singlets. [5] [6] Additional proteins include centrin, cenexin and tektin. [7]

The main function of centrioles is to produce cilia during interphase and the aster and the spindle during cell division.

History

The centrosome was discovered jointly by Walther Flemming in 1875 [8] [9] and Edouard Van Beneden in 1876. [10] [9] Edouard Van Beneden made the first observation of centrosomes as composed of two orthogonal centrioles in 1883. [11] Theodor Boveri introduced the term "centrosome" in 1888 [12] [9] [13] [14] and the term "centriole" in 1895. [15] [9] The basal body was named by Theodor Wilhelm Engelmann in 1880. [16] [9] The pattern of centriole duplication was first worked out independently by Étienne de Harven and Joseph G. Gall c. 1950. [17] [18]

Role in cell division

A mother and daughter centriole, attached orthogonally Centriole-en.svg
A mother and daughter centriole, attached orthogonally

Centrioles are involved in the organization of the mitotic spindle and in the completion of cytokinesis. [19] Centrioles were previously thought to be required for the formation of a mitotic spindle in animal cells. However, more recent experiments have demonstrated that cells whose centrioles have been removed via laser ablation can still progress through the G1 stage of interphase before centrioles can be synthesized later in a de novo fashion. [20] Additionally, mutant flies lacking centrioles develop normally, although the adult flies' cells lack flagella and cilia and as a result, they die shortly after birth. [21] The centrioles can self replicate during cell division.

Cellular organization

Centrioles are a very important part of centrosomes, which are involved in organizing microtubules in the cytoplasm. [22] [23] The position of the centriole determines the position of the nucleus and plays a crucial role in the spatial arrangement of the cell.

Fertility

Sperm centrioles are important for 2 functions: [24] (1) to form the sperm flagellum and sperm movement and (2) for the development of the embryo after fertilization. The sperm supplies the centriole that creates the centrosome and microtubule system of the zygote. [25]

Ciliogenesis

In flagellates and ciliates, the position of the flagellum or cilium is determined by the mother centriole, which becomes the basal body. An inability of cells to use centrioles to make functional flagella and cilia has been linked to a number of genetic and developmental diseases. In particular, the inability of centrioles to properly migrate prior to ciliary assembly has recently been linked to Meckel–Gruber syndrome. [26]

Animal development

Electron micrograph of a centriole from a mouse embryo. Spindle centriole - embryonic brain mouse - TEM.jpg
Electron micrograph of a centriole from a mouse embryo.

Proper orientation of cilia via centriole positioning toward the posterior of embryonic node cells is critical for establishing left-right asymmetry, during mammalian development. [27]

Centriole duplication

Before DNA replication, cells contain two centrioles, an older mother centriole, and a younger daughter centriole. During cell division, a new centriole grows at the proximal end of both mother and daughter centrioles. After duplication, the two centriole pairs (the freshly assembled centriole is now a daughter centriole in each pair) will remain attached to each other orthogonally until mitosis. At that point the mother and daughter centrioles separate dependently on an enzyme called separase. [28]

The two centrioles in the centrosome are tied to one another. The mother centriole has radiating appendages at the distal end of its long axis and is attached to its daughter at the proximal end. Each daughter cell formed after cell division will inherit one of these pairs. Centrioles start duplicating when DNA replicates. [19]

Origin

LECA, the last common ancestor of all eukaryotes was a ciliated cell with centrioles.[ citation needed ] Some lineages of eukaryotes, such as land plants, do not have centrioles except in their motile male gametes. Centrioles are completely absent from all cells of conifers and flowering plants, which do not have ciliate or flagellate gametes. [29] It is unclear if the last common ancestor had one [30] or two cilia. [31] Important genes such as those coding for centrins, required for centriole growth, are only found in eukaryotes, and not in bacteria or archaea. [30]

Etymology and pronunciation

The word centriole ( /ˈsɛntrioʊl/ ) uses combining forms of centri- and -ole , yielding "little central part", which describes a centriole's typical location near the center of the cell.

Atypical centrioles

Typical centrioles are made of 9 triplets of microtubules organized with radial symmetry. [32] Centrioles can vary the number of microtubules and can be made of 9 doublets of microtubules (as in Drosophila melanogaster ) or 9 singlets of microtubules as in C. elegans. Atypical centrioles are centrioles that do not have microtubules, such as the Proximal Centriole-Like found in D. melanogaster sperm, [33] or that have microtubules with no radial symmetry, such as in the distal centriole of human spermatozoon. [34] Atypical centrioles may have evolved at least eight times independently during vertebrate evolution and may evolve in the sperm after internal fertilization evolves. [35]

It wasn't clear why centriole become atypical until recently. The atypical distal centriole forms a dynamic basal complex (DBC) that, together with other structures in the sperm neck, facilitates a cascade of internal sliding, coupling tail beating with head kinking. The atypical distal centriole's properties suggest that it evolved into a transmission system that couples the sperm tail motors to the whole sperm, thereby enhancing sperm function. [36]

Related Research Articles

<span class="mw-page-title-main">Mitosis</span> Process in which chromosomes are replicated and separated into two new identical nuclei

Mitosis is a part of the cell cycle in which replicated chromosomes are separated into two new nuclei. Cell division by mitosis is an equational division which gives rise to genetically identical cells in which the total number of chromosomes is maintained. Mitosis is preceded by the S phase of interphase and is followed by telophase and cytokinesis, which divide the cytoplasm, organelles, and cell membrane of one cell into two new cells containing roughly equal shares of these cellular components. The different stages of mitosis altogether define the mitotic phase of a cell cycle—the division of the mother cell into two daughter cells genetically identical to each other.

<span class="mw-page-title-main">Microtubule</span> Polymer of tubulin that forms part of the cytoskeleton

Microtubules are polymers of tubulin that form part of the cytoskeleton and provide structure and shape to eukaryotic cells. Microtubules can be as long as 50 micrometres, as wide as 23 to 27 nm and have an inner diameter between 11 and 15 nm. They are formed by the polymerization of a dimer of two globular proteins, alpha and beta tubulin into protofilaments that can then associate laterally to form a hollow tube, the microtubule. The most common form of a microtubule consists of 13 protofilaments in the tubular arrangement.

<span class="mw-page-title-main">Fertilisation</span> Union of gametes of opposite sexes during the process of sexual reproduction to form a zygote

Fertilisation or fertilization, also known as generative fertilisation, syngamy and impregnation, is the fusion of gametes to give rise to a zygote and initiate its development into a new individual organism or offspring. While processes such as insemination or pollination, which happen before the fusion of gametes, are also sometimes informally referred to as fertilisation, these are technically separate processes. The cycle of fertilisation and development of new individuals is called sexual reproduction. During double fertilisation in angiosperms, the haploid male gamete combines with two haploid polar nuclei to form a triploid primary endosperm nucleus by the process of vegetative fertilisation.

<span class="mw-page-title-main">Centrosome</span> Cell organelle in animal cell helping in cell division

In cell biology, the centrosome is an organelle that serves as the main microtubule organizing center (MTOC) of the animal cell, as well as a regulator of cell-cycle progression. The centrosome provides structure for the cell. The centrosome is thought to have evolved only in the metazoan lineage of eukaryotic cells. Fungi and plants lack centrosomes and therefore use other structures to organize their microtubules. Although the centrosome has a key role in efficient mitosis in animal cells, it is not essential in certain fly and flatworm species.

The microtubule-organizing center (MTOC) is a structure found in eukaryotic cells from which microtubules emerge. MTOCs have two main functions: the organization of eukaryotic flagella and cilia and the organization of the mitotic and meiotic spindle apparatus, which separate the chromosomes during cell division. The MTOC is a major site of microtubule nucleation and can be visualized in cells by immunohistochemical detection of γ-tubulin. The morphological characteristics of MTOCs vary between the different phyla and kingdoms. In animals, the two most important types of MTOCs are 1) the basal bodies associated with cilia and flagella and 2) the centrosome associated with spindle formation.

<span class="mw-page-title-main">Karyogamy</span> Fusion of the nuclei of two haploid eukaryotic cells

Karyogamy is the final step in the process of fusing together two haploid eukaryotic cells, and refers specifically to the fusion of the two nuclei. Before karyogamy, each haploid cell has one complete copy of the organism's genome. In order for karyogamy to occur, the cell membrane and cytoplasm of each cell must fuse with the other in a process known as plasmogamy. Once within the joined cell membrane, the nuclei are referred to as pronuclei. Once the cell membranes, cytoplasm, and pronuclei fuse, the resulting single cell is diploid, containing two copies of the genome. This diploid cell, called a zygote or zygospore can then enter meiosis, or continue to divide by mitosis. Mammalian fertilization uses a comparable process to combine haploid sperm and egg cells (gametes) to create a diploid fertilized egg.

<span class="mw-page-title-main">Basal body</span> Protein structure found at the base of cilium or flagellum).

A basal body is a protein structure found at the base of a eukaryotic undulipodium. The basal body was named by Theodor Wilhelm Engelmann in 1880. It is formed from a centriole and several additional protein structures, and is, essentially, a modified centriole. The basal body serves as a nucleation site for the growth of the axoneme microtubules. Centrioles, from which basal bodies are derived, act as anchoring sites for proteins that in turn anchor microtubules, and are known as the microtubule organizing center (MTOC). These microtubules provide structure and facilitate movement of vesicles and organelles within many eukaryotic cells.

<span class="mw-page-title-main">Pronucleus</span> Nucleus of a sperm or an egg cell during fertilization

A pronucleus denotes the nucleus found in either a sperm or egg cell during the process of fertilization. The sperm cell undergoes a transformation into a pronucleus after entering the egg cell but prior to the fusion of the genetic material of both the sperm and egg. In contrast, the egg cell possesses a pronucleus once it becomes haploid, not upon the arrival of the sperm cell. Haploid cells, such as sperm and egg cells in humans, carry half the number of chromosomes present in somatic cells, with 23 chromosomes compared to the 46 found in somatic cells. It is noteworthy that the male and female pronuclei do not physically merge, although their genetic material does. Instead, their membranes dissolve, eliminating any barriers between the male and female chromosomes, facilitating the combination of their chromosomes into a single diploid nucleus in the resulting embryo, which contains a complete set of 46 chromosomes.

<span class="mw-page-title-main">Sperm</span> Male reproductive cell in anisogamous forms of sexual reproduction

Sperm is the male reproductive cell, or gamete, in anisogamous forms of sexual reproduction. Animals produce motile sperm with a tail known as a flagellum, which are known as spermatozoa, while some red algae and fungi produce non-motile sperm cells, known as spermatia. Flowering plants contain non-motile sperm inside pollen, while some more basal plants like ferns and some gymnosperms have motile sperm.

<span class="mw-page-title-main">Sperm motility</span> Process involved in the controlled movement of a sperm cell

Sperm motility describes the ability of sperm to move properly through the female reproductive tract or through water to reach the egg. Sperm motility can also be thought of as the quality, which is a factor in successful conception; sperm that do not "swim" properly will not reach the egg in order to fertilize it. Sperm motility in mammals also facilitates the passage of the sperm through the cumulus oophorus and the zona pellucida, which surround the mammalian oocyte.

<span class="mw-page-title-main">Centrin</span> Family of calcium-binding phosphoproteins

Centrins, also known as caltractins, are a family of calcium-binding phosphoproteins found in the centrosome of eukaryotes. Centrins are small calcium binding proteins that are ubiquitous centrosome components. There are about 350 “signature” proteins that are unique to eukaryotic cells but have no significant homology to proteins in archaea and bacteria. They are a type of protein that is essential and present in almost all eukaryotic cells and are found in the centrioles and pericentriolar lattice. Human centrin genes are CETN1, CETN2 and CETN3.

<span class="mw-page-title-main">Centrin 2</span> Protein-coding gene in humans

Centrin-2 is a protein that in humans is encoded by the CETN2 gene. It belongs to the centrin family of proteins.

<span class="mw-page-title-main">Centrin 3</span> Protein-coding gene in the species Homo sapiens

Centrin-3 is a protein that in humans is encoded by the CETN3 gene. It belongs to the centrin family of proteins.

<span class="mw-page-title-main">CEP170</span> Protein-coding gene in the species Homo sapiens

Centrosomal protein 170kDa, also known as CEP170, is a protein that in humans is encoded by the CEP170 gene.

<span class="mw-page-title-main">Pericentriolar material</span>

Pericentriolar material is a highly structured, dense mass of protein which makes up the part of the animal centrosome that surrounds the two centrioles. The PCM contains proteins responsible for microtubule nucleation and anchoring including γ-tubulin, pericentrin and ninein.

<span class="mw-page-title-main">Centrosome cycle</span> Centrioles are nine triplets microtubules

Centrosomes are the major microtubule organizing centers (MTOC) in mammalian cells. Failure of centrosome regulation can cause mistakes in chromosome segregation and is associated with aneuploidy. A centrosome is composed of two orthogonal cylindrical protein assemblies, called centrioles, which are surrounded by a protein dense amorphous cloud of pericentriolar material (PCM). The PCM is essential for nucleation and organization of microtubules. The centrosome cycle is important to ensure that daughter cells receive a centrosome after cell division. As the cell cycle progresses, the centrosome undergoes a series of morphological and functional changes. Initiation of the centrosome cycle occurs early in the cell cycle in order to have two centrosomes by the time mitosis occurs.

<span class="mw-page-title-main">TUBE1</span> Protein-coding gene in the species Homo sapiens

Tubulin, epsilon 1 is a protein in humans that is encoded by the TUBE1 gene. This gene encodes a member of the tubulin superfamily. This protein localizes to the centriolar sub-distal appendages that are associated with the older of the two centrioles after centrosome duplication. This protein plays a central role in organization of the microtubules during centriole duplication

<span class="mw-page-title-main">SFI1</span> Protein-coding gene in the species Homo sapiens

Sfi1 homolog, spindle assembly associated (yeast) is a protein that in humans is encoded by the SFI1 gene. It localizes to the centriole, and its S. pombe ortholog has been shown to be involved in spindle pole body duplication. SFI1 forms a complex with centrin 2.

A proximal centriole-like or PCL is an atypical type of centriole found in the sperm cells of insects. The PCL name is due to some similarity to the proximal centriole found in vertebrate sperm and the hypothesis that the two structures are homologous. The PCL is an atypical type of centriole because it does not have microtubules, a defining feature of centrioles. However, the PCL is a type of centriole for several reasons. (1) the PCL formation is dependent upon the same genetic pathway that mediates the initiation of centriole formation. (2) The PCL is composed of centriolar proteins. (3) After fertilization, the sperm PCL function like a centriole. The PCL recruits pericentriolar material (PCM) forming a centrosome that acts as a microtubule-organizing center (MTOC). The PCL also serves as a platform to form a typical centriole in the zygote, as expected from a centriole. Also, the PCL is essential to form one of the two spindle poles of the dividing zygote.

Renata Homem de Gouveia Xavier de Basto is a researcher in cell and developmental biology. She is currently a team leader at the Institut Curie in Paris. She is also the deputy director of the CNRS research Unit UMR144 'Cell biology and cancer' at the Institut Curie which, comprises 14 research teams.

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  36. ↑ Khanal, S., M.R. Leung, A. Royfman, E.L. Fishman, B. Saltzman, H. Bloomfield-Gadelha, T. Zeev-Ben-Mordehai, and T. Avidor-Reiss. 2021. A dynamic basal complex modulates mammalian sperm movement. Nat Commun. 12:3808.. https://doi.org/10.1038/s41467-021-24011-0

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