centriole

The centrosome was discovered jointly by Walther Flemming in 1875Flemming, W. (1875). Studien uber die Entwicklungsgeschichte der Najaden. Sitzungsgeber. Akad. Wiss. Wien 71, 81–147Bloodgood RA. From central to rudimentary to primary: the history of an underappreciated organelle whose time has come. The primary cilium. Methods Cell Biol. 2009;94:3-52. doi: 10.1016/S0091-679X(08)94001-2. Epub 2009 Dec 23. PMID 20362083. and Edouard Van Beneden in 1876.Van Beneden, E. (1876). Contribution a l’histoire de la vesiculaire germinative et du premier noyau embryonnaire. Bull. Acad. R. Belg (2me series) 42, 35–97. Edouard Van Beneden made the first observation of centrosomes as composed of two orthogonal centrioles in 1883.{{Cite journal | year = 2002 | doi = 10.1007/s00109-002-0374-y| pmid = 12226736 | issue = 9 | pages = 545–548| volume = 80| title = JMM - Past and Present| last1 = Wunderlich| journal = Journal of Molecular Medicine| first1 = V.| doi-access = free}} Theodor Boveri introduced the term "centrosome" in 1888Boveri, T. (1888). Zellen-Studien II. Die Befruchtung und Teilung des Eies von Ascaris megalocephala.

Jena. Z. Naturwiss. 22, 685–882.Boveri, T. Ueber das Verhalten der Centrosomen bei der Befruchtung des Seeigel-Eies nebst allgemeinen Bemerkungen über Centrosomen und Verwandtes. Verh. d. Phys.-Med. Ges. zu Würzburg, N. F., Bd. XXIX, 1895. [https://archive.org/details/bub_gb_UYcPAQAAMAAJ link].Boveri, T. (1901). Zellen-Studien: Uber die Natur der Centrosomen. IV. Fischer, Jena. [https://archive.org/details/zellenstudienbe00bovegoog link]. and the term "centriole" in 1895.Boveri, T. (1895). Ueber die Befruchtungs und Entwickelungsfahigkeit kernloser Seeigeleier und uber die Moglichkeit ihrer Bastardierung. Arch. Entwicklungsmech. Org. (Wilhelm Roux) 2, 394–443. The basal body was named by Theodor Wilhelm Engelmann in 1880.Engelmann, T. W. (1880). Zur Anatomie und Physiologie der Flimmerzellen. Pflugers Arch. 23, 505–535. The pattern of centriole duplication was first worked out independently by Étienne de Harven and Joseph G. Gall c. 1950.{{cite book | last = Wolfe | first = Stephen L. | author-link = Stephen L. Wolfe | title = Biology: the foundations | publisher = Wadsworth | year = 1977|edition=First | url =https://archive.org/details/biologyfoundatio00wolf| url-access = registration | isbn = 9780534004903 }}{{Cite book|volume=106 |year=1987 |pages=227–293|doi=10.1016/S0074-7696(08)61714-3 |title=The Centrosome and Its Role in the Organization of Microtubules |first1=I. A. |last1=Vorobjev |first2=E. S. |last2=Nadezhdina |series=International Review of Cytology|isbn=978-0-12-364506-7 |pmid=3294718}}. See also de Harven's own recollections of this work: {{Cite journal|title=Early observations of centrioles and mitotic spindle fibers by transmission electron microscopy|first=Etienne|last=de Harven |journal=Biology of the Cell |year=1994 |volume=80 |pages=107–109 |doi=10.1111/j.1768-322X.1994.tb00916.x|pmid=8087058|issue=2–3|s2cid=84594630|df=dmy-all}}

File:Centriole-en.svg]]

Centrioles are involved in the organization of the mitotic spindle and in the completion of cytokinesis.{{Cite journal|doi=10.1016/S0960-9822(02)01019-9|pmid=12176356|year=2002|last1=Salisbury|first1=JL|last2=Suino|first2=KM|last3=Busby|first3=R|last4=Springett|first4=M|title=Centrin-2 is required for centriole duplication in mammalian cells|volume=12|issue=15|pages=1287–92|journal=Current Biology|s2cid=1415623|doi-access=free}} 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.{{Cite journal|pmid=15738265|year=2005|last1=La Terra|first1=S|last2=English|first2=CN|last3=Hergert|first3=P|last4=McEwen|first4=BF|last5=Sluder|first5=G|last6=Khodjakov|first6=A|title=The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation|volume=168|issue=5|pages=713–22|doi=10.1083/jcb.200411126|pmc=2171814|journal=The Journal of Cell Biology}} 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.{{Cite journal|pmid=16814722|year=2006|last1=Basto|first1=R|last2=Lau|first2=J|last3=Vinogradova|first3=T|last4=Gardiol|first4=A|last5=Woods|first5=CG|last6=Khodjakov|first6=A|last7=Raff|first7=JW|title=Flies without centrioles|volume=125|issue=7|pages=1375–86|doi=10.1016/j.cell.2006.05.025|journal=Cell|s2cid=2080684|doi-access=free}}

The centrioles can self replicate during cell division.

Centrioles are a very important part of centrosomes, which are involved in organizing microtubules in the cytoplasm.{{Cite journal|pmid=17518519|year=2007|last1=Feldman|first1=JL|last2=Geimer|first2=S|last3=Marshall|first3=WF|title=The mother centriole plays an instructive role in defining cell geometry|volume=5|issue=6|pages=e149|doi=10.1371/journal.pbio.0050149|pmc=1872036|journal=PLOS Biology |doi-access=free }}{{Cite journal|doi=10.1016/S0955-0674(02)00017-0|pmid=12517710|year=2003|last1=Beisson|first1=J|last2=Wright|first2=M|title=Basal body/centriole assembly and continuity|volume=15|issue=1|pages=96–104|journal=Current Opinion in Cell Biology}} The position of the centriole determines the position of the nucleus and plays a crucial role in the spatial arrangement of the cell.

Sperm centrioles are important for 2 functions:Avidor-Reiss, T., Khire, A., Fishman, E. L., & Jo, K. H. (2015). Atypical centrioles during sexual reproduction. Frontiers in cell and developmental biology, 3, 21.

Chicago (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.{{Cite book|chapter=The biology of fertilization in humans|editor=Patrizio, Pasquale|title=A color atlas for human assisted reproduction: laboratory and clinical insights|publisher=Lippincott Williams & Wilkins|year=2003|isbn=978-0-7817-3769-2|page=3|chapter-url=https://books.google.com/books?id=2SBoQ8H-KMIC&pg=PA3|author1=Hewitson, Laura |author2=Schatten, Gerald P. |name-list-style=amp |access-date=2013-11-09|display-editors=etal}}

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.{{Cite journal|doi=10.1242/dmm.006262|pmc=3008963|pmid= 21045211|year=2011|author1=Cui, Cheng |author2=Chatterjee, Bishwanath |author3=Francis, Deanne |author4=Yu, Qing |author5=SanAgustin, Jovenal T. |author6=Francis, Richard |author7=Tansey, Terry |author8=Henry, Charisse |author9=Wang, Baolin |author10=Lemley, Bethan |author11=Pazour, Gregory J. |author12=Lo, Cecilia W. |title=Disruption of Mks1 localization to the mother centriole causes cilia defects and developmental malformations in Meckel-Gruber syndrome|volume=4|issue=1|pages=43–56|journal=Dis. Models Mech.}}

File:Spindle centriole - embryonic brain mouse - TEM.jpg

Proper orientation of cilia via centriole positioning toward the posterior of embryonic node cells is critical for establishing left-right asymmetry, during mammalian development.{{Cite journal|last1=Babu|first1=Deepak|last2=Roy|first2=Sudipto|date=2013-05-01|title=Left–right asymmetry: cilia stir up new surprises in the node|journal=Open Biology|language=en|volume=3|issue=5|pages=130052|doi=10.1098/rsob.130052|issn=2046-2441|pmc=3866868|pmid=23720541}}

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.{{Cite journal|pmid=16862117|year=2006|last1=Tsou|first1=MF|last2=Stearns|first2=T|title=Mechanism limiting centrosome duplication to once per cell cycle|volume=442|issue=7105|pages=947–51|doi=10.1038/nature04985|journal=Nature|bibcode = 2006Natur.442..947T |s2cid=4413248}}

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.

LECA, the last common ancestor of all eukaryotes was a ciliated cell with centrioles.{{Citation needed|date=April 2024}} 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.{{cite journal | last1 = Marshall | first1 = W.F. | year = 2009 | title = Centriole Evolution | journal = Current Opinion in Cell Biology | volume = 21 | issue = 1| pages = 14–19 | doi = 10.1016/j.ceb.2009.01.008 | pmid=19196504 | pmc=2835302}}

It is unclear if the last common ancestor had one{{Cite book| doi = 10.1007/978-0-387-74021-8_10| last2 = Azimzadeh| pmid = 17977464| isbn = 978-0-387-74020-1| year = 2007| pages = [https://archive.org/details/eukaryoticmembra00gasp/page/119 119–129]| series = Advances in Experimental Medicine and Biology| last1 = Bornens| first2 = J.| chapter = Origin and Evolution of the Centrosome| title = Eukaryotic Membranes and Cytoskeleton| volume = 607| first1 = M.| chapter-url-access = registration| chapter-url = https://archive.org/details/eukaryoticmembra00gasp| url = https://archive.org/details/eukaryoticmembra00gasp/page/119}} or two cilia.{{Cite journal | doi = 10.1093/gbe/evp011 | last1 = Rogozin | first1 = I. B. | last2 = Basu | first2 = M. K. | last3 = Csürös | first3 = M. | last4 = Koonin | first4 = E. V. | title = Analysis of Rare Genomic Changes Does Not Support the Unikont-Bikont Phylogeny and Suggests Cyanobacterial Symbiosis as the Point of Primary Radiation of Eukaryotes | journal = Genome Biology and Evolution | volume = 1 | pages = 99–113 | year = 2009 | pmid = 20333181 | pmc = 2817406}} Important genes such as those coding for centrins, required for centriole growth, are only found in eukaryotes, and not in bacteria or archaea.

The word centriole ({{IPAc-en|ˈ|s|ɛ|n|t|r|i|oʊ|l}}) uses combining forms of centri- and -ole, yielding "little central part", which describes a centriole's typical location near the center of the cell.

Typical centrioles are made of 9 triplets of microtubules organized with radial symmetry.{{cite journal |doi=10.1016/j.ceb.2012.10.016 |pmid=23199753 |pmc=3578074 |title=Building a centriole |journal=Current Opinion in Cell Biology |volume=25 |issue=1 |pages=72–7 |year=2013 |last1=Avidor-Reiss |first1=Tomer |last2=Gopalakrishnan |first2=Jayachandran }} 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,{{cite journal |doi=10.1534/genetics.109.101709 |pmid=19293139 |pmc=2674812 |title=A Proximal Centriole-Like Structure is Present in Drosophila Spermatids and Can Serve as a Model to Study Centriole Duplication |journal=Genetics |volume=182 |issue=1 |pages=133–44 |year=2009 |last1=Blachon |first1=S |last2=Cai |first2=X |last3=Roberts |first3=K. A |last4=Yang |first4=K |last5=Polyanovsky |first5=A |last6=Church |first6=A |last7=Avidor-Reiss |first7=T }} or that have microtubules with no radial symmetry, such as in the distal centriole of human spermatozoon.{{cite journal |doi=10.1038/s41467-018-04678-8 |pmid=29880810 |pmc=5992222 |title=A novel atypical sperm centriole is functional during human fertilization |journal=Nature Communications |volume=9 |issue=1 |pages=2210 |year=2018 |last1=Fishman |first1=Emily L |last2=Jo |first2=Kyoung |last3=Nguyen |first3=Quynh P. H |last4=Kong |first4=Dong |last5=Royfman |first5=Rachel |last6=Cekic |first6=Anthony R |last7=Khanal |first7=Sushil |last8=Miller |first8=Ann L |last9=Simerly |first9=Calvin |last10=Schatten |first10=Gerald |last11=Loncarek |first11=Jadranka |last12=Mennella |first12=Vito |last13=Avidor-Reiss |first13=Tomer |bibcode=2018NatCo...9.2210F }} Atypical centrioles may have evolved at least eight times independently during vertebrate evolution and may evolve in the sperm after internal fertilization evolves.Turner, K., N. Solanki, H.O. Salouha, and T. Avidor-Reiss. 2022. Atypical Centriolar Composition Correlates with Internal Fertilization in Fish. Cells. 11:758, https://www.mdpi.com/2073-4409/11/5/758

It wasn't clear why the centriole became 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 that couples 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.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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Category:Centrosome

Category:Protein complexes

Category:Cell movement