Cyclin B3

Last updated
CCNB3
Identifiers
Aliases CCNB3 , cyclin B3, CYCB3
External IDs OMIM: 300456; MGI: 2183443; HomoloGene: 13199; GeneCards: CCNB3; OMA:CCNB3 - orthologs
Orthologs
SpeciesHumanMouse
Entrez

85417

209091

Ensembl

ENSG00000147082

ENSMUSG00000051592

UniProt

Q8WWL7

Q810T2

RefSeq (mRNA)

NM_033031
NM_033670
NM_033671

NM_183015

RefSeq (protein)

NP_149020
NP_391990

NP_898836

Location (UCSC) Chr X: 50.2 – 50.35 Mb Chr X: 6.85 – 6.91 Mb
PubMed search [3] [4]
Wikidata
View/Edit Human View/Edit Mouse

G2/mitotic-specific cyclin-B3 is a protein encoded by the CCNB3 gene located on the X chromosome in humans. [5] Cyclin B3 has features of both A type cyclins and B type cyclins and is a distinct subfamily of B type cyclins conserved across many species. [6] [7] [8] [9] However, human cyclin B3 is considerably larger than all other previously characterized invertebrate or vertebrate cyclin B3s. [10] Unlike cyclin B1 and cyclin B2, it is solely expressed in germ cells in mammals, with a significant role in meiosis and gamete formation. [11]

Contents

Structure

Cyclin B3 was originally identified in chickens from cDNA as a 403 amino acid protein. It has roughly 30% similarity to chicken and Xenopus B and A type cyclins. The cyclin box of chicken cyclin B3 has 15 residues different from the consensus sequence for B type cyclins and 22 residues different from the consensus sequence for A type cyclins. The destruction box sequence for chicken cyclin B3 also differs from the expected sequence: rather than containing a leucine it has a phenylalanine. The nuclear localization sequence (NLS) of chicken cyclin B3 appears to be in the 26 C-terminal residues, consistent with A type cyclins. [6]

Human cyclin B3 is the largest cyclin, 1395 amino acids long, due to large variable domain (contained in exon 8) between the destruction box and cyclin box. There are indications of alternative splicing that alters localization to the cytoplasm. [8] [10] [12]

Expression

Cyclin B3 is nearly entirely localized to the nucleus and cycles similarly to other B cyclins in somatic cells. [6] [8] In humans it is primarily expressed in germ cells in the testis, somewhat contradictory to its observed function in oocyte meiosis in other organisms. [8] [10]

Function

When it was initially characterized, human cyclin B3 was found to associate with CDK2 in HeLa cells but it did not significantly spur histone H1 kinase activity as is common with other cyclin-CDK complexes. However, further research has not shown that cyclin B3 associates with CDK2 but rather CDK1 (as seen with chicken cyclin B3). In HeLa cells, cyclin B3 was observed to degrade during the metaphase-anaphase transition when it had a complete destruction box. Accumulation of cyclin B3 was also shown to induce the beginning of mitosis early and prevent exit from M phase by arresting cells in anaphase. [8]

Role in mitosis

Cyclin B3 has primarily mitotic functionality in Caenorhabditis elegans where it is primarily localized to the nucleus and is necessary for chromatid separation. [13] Cyclin B3 is especially important in early C. elegans embryos where it again governs chromatid separation as well as kinetochore and microtubule assembly. [14] It additionally appears to drive rapid mitosis in early C. elegans embryos, roughly three times faster than mitosis in adult worms. [15]

Role in meiosis and gamete production

Oogenesis

Cyclin B3 has been investigated in the context of oogenesis as its initial mammalian characterization found mRNA expression in fetal ovaries but not adult ovaries. [8] More recent research[ when? ] has shown that female mice with null or severe loss of function mutations to both copies of cyclin B3 (Ccnb3-/-) are sterile: most ccnb3-/- oocytes do not form polar bodies. Cyclin B3-CDK1 complexes promote the degradation of Anaphase Promoting Complex/Cyclosome (APC/C) substrates securin and cyclin B1, which potentially leads to the onset of anaphase I. Cyclin B3 is also degraded as the oocyte leaves meiosis I. [9] [16]

More recent research[ when? ] has indicated that cyclin B3-CDK1 complexes phosphorylate Emi2, an APC/C inhibitor, which flags it for degradation and maintains APC/C activity. Importantly, cyclin B3 is not present during meiosis II, which allows for arrest in metaphase II. [17] This pattern of degradation, different from cyclins B1 and B2, is potentially the result of its destruction box sequence which does not match cyclins B1 and B2. [11] [6]

Cyclin B3 seems to maintain this key function in oogenesis in other organisms like Drosophila , where Cyclin B3 acts directly on APC/C, and Caenorhabditis elegans. [18] [19] [20] Interestingly, injection of frog (Xenopus laevis), zebrafish (Danio rerio), or fly (Drosophila) cyclin B3 mRNA rescued Ccnb3-/- mutant fertility in mice, suggesting that cyclin B3 is highly conserved amongst all animals. [9]

Spermatogenesis

As its initial mammalian characterization found cyclin B3 is primarily expressed in human testis and implicated in meiosis, its role in spermatogenesis has been studied in mouse models. Cyclin B3 mRNA was observed beginning in prophase I, continuing to accumulate in leptotene and zygotene stages, and decreasing as sperm cells entered the pachytene stage. [8] When cyclin B3 expression was artificially extended until the end of meiosis, spermatogenesis was negatively affected. This extended expression led to decrease in sperm counts, cells in seminiferous tubules with abnormal morphology and increased instances of apoptosis, and resulted in no functional gametes. [21]

Interestingly, male mice and flies with null or severe loss of function mutations of cyclin B3 (Ccbn3-/Y) retain their fertility and exhibit normal spermatogenesis which shows that cyclin B3 is not necessary and has some redundant functionality in males. [22] [18]

Cancer

Despite its primary role in meiosis, cyclin B3 has been implicated in cancer, first described in bone sarcomas as a fusion of BCOR and CCNB3 in undifferentiated sarcomas. Tumors with this mutation are relatively rare but more prevalent in adolescents and young adults as well and significantly more common in men than women; no reasons for this demographic breakdown have been proposed. [23] [24]

Related Research Articles

<span class="mw-page-title-main">Meiosis</span> Cell division producing haploid gametes

Meiosis (; from Ancient Greek μείωσις 'lessening', is a special type of cell division of germ cells in sexually-reproducing organisms that produces the gametes, the sperm or egg cells. It involves two rounds of division that ultimately result in four cells, each with only one copy of each chromosome. Additionally, prior to the division, genetic material from the paternal and maternal copies of each chromosome is crossed over, creating new combinations of code on each chromosome. Later on, during fertilisation, the haploid cells produced by meiosis from a male and a female will fuse to create a zygote, a cell with two copies of each chromosome again.

<span class="mw-page-title-main">Cell division</span> Process by which living cells divide

Cell division is the process by which a parent cell divides into two daughter cells. Cell division usually occurs as part of a larger cell cycle in which the cell grows and replicates its chromosome(s) before dividing. In eukaryotes, there are two distinct types of cell division: a vegetative division (mitosis), producing daughter cells genetically identical to the parent cell, and a cell division that produces haploid gametes for sexual reproduction (meiosis), reducing the number of chromosomes from two of each type in the diploid parent cell to one of each type in the daughter cells. Mitosis is a part of the cell cycle, in which, replicated chromosomes are separated into two new nuclei. Cell division gives rise to genetically identical cells in which the total number of chromosomes is maintained. In general, mitosis is preceded by the S stage of interphase and is followed by telophase and cytokinesis; which divides 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 all together define the M phase of an animal cell cycle—the division of the mother cell into two genetically identical daughter cells. To ensure proper progression through the cell cycle, DNA damage is detected and repaired at various checkpoints throughout the cycle. These checkpoints can halt progression through the cell cycle by inhibiting certain cyclin-CDK complexes. Meiosis undergoes two divisions resulting in four haploid daughter cells. Homologous chromosomes are separated in the first division of meiosis, such that each daughter cell has one copy of each chromosome. These chromosomes have already been replicated and have two sister chromatids which are then separated during the second division of meiosis. Both of these cell division cycles are used in the process of sexual reproduction at some point in their life cycle. Both are believed to be present in the last eukaryotic common ancestor.

<span class="mw-page-title-main">Telophase</span> Final stage of a cell division for eukaryotic cells both in mitosis and meiosis

Telophase is the final stage in both meiosis and mitosis in a eukaryotic cell. During telophase, the effects of prophase and prometaphase are reversed. As chromosomes reach the cell poles, a nuclear envelope is re-assembled around each set of chromatids, the nucleoli reappear, and chromosomes begin to decondense back into the expanded chromatin that is present during interphase. The mitotic spindle is disassembled and remaining spindle microtubules are depolymerized. Telophase accounts for approximately 2% of the cell cycle's duration.

<span class="mw-page-title-main">Anaphase-promoting complex</span> Cell-cycle regulatory complex

Anaphase-promoting complex is an E3 ubiquitin ligase that marks target cell cycle proteins for degradation by the 26S proteasome. The APC/C is a large complex of 11–13 subunit proteins, including a cullin (Apc2) and RING (Apc11) subunit much like SCF. Other parts of the APC/C have unknown functions but are highly conserved.

Maturation-promoting factor (abbreviated MPF, also called mitosis-promoting factor or M-Phase-promoting factor) is the cyclin–Cdk complex that was discovered first in frog eggs. It stimulates the mitotic and meiotic phases of the cell cycle. MPF promotes the entrance into mitosis (the M phase) from the G2 phase by phosphorylating multiple proteins needed during mitosis. MPF is activated at the end of G2 by a phosphatase, which removes an inhibitory phosphate group added earlier.

<span class="mw-page-title-main">Spindle checkpoint</span> Cell cycle checkpoint

The spindle checkpoint, also known as the metaphase-to-anaphase transition, the spindle assembly checkpoint (SAC), the metaphase checkpoint, or the mitotic checkpoint, is a cell cycle checkpoint during metaphase of mitosis or meiosis that prevents the separation of the duplicated chromosomes (anaphase) until each chromosome is properly attached to the spindle. To achieve proper segregation, the two kinetochores on the sister chromatids must be attached to opposite spindle poles. Only this pattern of attachment will ensure that each daughter cell receives one copy of the chromosome. The defining biochemical feature of this checkpoint is the stimulation of the anaphase-promoting complex by M-phase cyclin-CDK complexes, which in turn causes the proteolytic destruction of cyclins and proteins that hold the sister chromatids together.

<span class="mw-page-title-main">Kinetochore</span> Protein complex that allows microtubules to attach to chromosomes during cell division

A kinetochore is a disc-shaped protein structure associated with duplicated chromatids in eukaryotic cells where the spindle fibers attach during cell division to pull sister chromatids apart. The kinetochore assembles on the centromere and links the chromosome to microtubule polymers from the mitotic spindle during mitosis and meiosis. The term kinetochore was first used in a footnote in a 1934 Cytology book by Lester W. Sharp and commonly accepted in 1936. Sharp's footnote reads: "The convenient term kinetochore has been suggested to the author by J. A. Moore", likely referring to John Alexander Moore who had joined Columbia University as a freshman in 1932.

G<sub>2</sub> phase Second growth phase in the eukaryotic cell cycle, prior to mitosis

G2 phase, Gap 2 phase, or Growth 2 phase, is the third subphase of interphase in the cell cycle directly preceding mitosis. It follows the successful completion of S phase, during which the cell’s DNA is replicated. G2 phase ends with the onset of prophase, the first phase of mitosis in which the cell’s chromatin condenses into chromosomes.

<span class="mw-page-title-main">Separase</span> Mammalian protein found in Homo sapiens

Separase, also known as separin, is a cysteine protease responsible for triggering anaphase by hydrolysing cohesin, which is the protein responsible for binding sister chromatids during the early stage of anaphase. In humans, separin is encoded by the ESPL1 gene.

<span class="mw-page-title-main">Cell cycle checkpoint</span> Control mechanism in the eukaryotic cell cycle

Cell cycle checkpoints are control mechanisms in the eukaryotic cell cycle which ensure its proper progression. Each checkpoint serves as a potential termination point along the cell cycle, during which the conditions of the cell are assessed, with progression through the various phases of the cell cycle occurring only when favorable conditions are met. There are many checkpoints in the cell cycle, but the three major ones are: the G1 checkpoint, also known as the Start or restriction checkpoint or Major Checkpoint; the G2/M checkpoint; and the metaphase-to-anaphase transition, also known as the spindle checkpoint. Progression through these checkpoints is largely determined by the activation of cyclin-dependent kinases by regulatory protein subunits called cyclins, different forms of which are produced at each stage of the cell cycle to control the specific events that occur therein.

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

Aurora kinase A also known as serine/threonine-protein kinase 6 is an enzyme that in humans is encoded by the AURKA gene.

Polo-like kinases (Plks) are regulatory serine/threonine kinases of the cell cycle involved in mitotic entry, mitotic exit, spindle formation, cytokinesis, and meiosis. Only one Plk is found in the genomes of the fly Drosophila melanogaster (Polo), budding yeast (Cdc5) and fission yeast (Plo1). Vertebrates and other animals, however, have many Plk family members including Plk1, Plk2/Snk, Plk3/Prk/FnK, Plk4/Sak and Plk5. Of the vertebrate Plk family members, the mammalian Plk1 has been most extensively studied. During mitosis and cytokinesis, Plks associate with several structures including the centrosome, kinetochores, and the central spindle.

<span class="mw-page-title-main">CDC20</span> Protein-coding gene in humans

The cell division cycle protein 20 homolog is an essential regulator of cell division that is encoded by the CDC20 gene in humans. To the best of current knowledge its most important function is to activate the anaphase promoting complex (APC/C), a large 11-13 subunit complex that initiates chromatid separation and entrance into anaphase. The APC/CCdc20 protein complex has two main downstream targets. Firstly, it targets securin for destruction, enabling the eventual destruction of cohesin and thus sister chromatid separation. It also targets S and M-phase (S/M) cyclins for destruction, which inactivates S/M cyclin-dependent kinases (Cdks) and allows the cell to exit from mitosis. A closely related protein, Cdc20homologue-1 (Cdh1) plays a complementary role in the cell cycle.

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

MASTL is an official symbol provided by HGNC for human gene whose official name is micro tubule associated serine/threonine kinase like. This gene is 32,1 kbps long. This gene is also known as GW, GWL, THC2, MAST-L, GREATWALL. This is present in mainly mammalian cells like human, house mouse, cattle, monkey, etc. It is in the 10th chromosome of the mammalian nucleus. Recent studies have been carried on zebrafish and frogs. This gene encodes for the protein micro tubule associated serine/threonine kinase and its sub-classes.

<span class="mw-page-title-main">Meiotic recombination checkpoint</span>

The meiotic recombination checkpoint monitors meiotic recombination during meiosis, and blocks the entry into metaphase I if recombination is not efficiently processed.

A series of biochemical switches control transitions between and within the various phases of the cell cycle. The cell cycle is a series of complex, ordered, sequential events that control how a single cell divides into two cells, and involves several different phases. The phases include the G1 and G2 phases, DNA replication or S phase, and the actual process of cell division, mitosis or M phase. During the M phase, the chromosomes separate and cytokinesis occurs.

Cdc14 and Cdc14 are a gene and its protein product respectively. Cdc14 is found in most of the eukaryotes. Cdc14 was defined by Hartwell in his famous screen for loci that control the cell cycle of Saccharomyces cerevisiae. Cdc14 was later shown to encode a protein phosphatase. Cdc14 is dual-specificity, which means it has serine/threonine and tyrosine-directed activity. A preference for serines next to proline is reported. Many early studies, especially in the budding yeast Saccharomyces cerevisiae, demonstrated that the protein plays a key role in regulating late mitotic processes. However, more recent work in a range of systems suggests that its cellular function is more complex.

<span class="mw-page-title-main">APC/C activator protein CDH1</span> Fungal protein found in Saccharomyces cerevisiae S288c

Cdh1 is one of the substrate adaptor proteins of the anaphase-promoting complex (APC) in the budding yeast Saccharomyces cerevisiae. Functioning as an activator of the APC/C, Cdh1 regulates the activity and substrate specificity of this ubiquitin E3-ligase. The human homolog is encoded by the FZR1 gene, which is not to be confused with the CDH1 gene.

Mitotic exit is an important transition point that signifies the end of mitosis and the onset of new G1 phase for a cell, and the cell needs to rely on specific control mechanisms to ensure that once it exits mitosis, it never returns to mitosis until it has gone through G1, S, and G2 phases and passed all the necessary checkpoints. Many factors including cyclins, cyclin-dependent kinases (CDKs), ubiquitin ligases, inhibitors of cyclin-dependent kinases, and reversible phosphorylations regulate mitotic exit to ensure that cell cycle events occur in correct order with fewest errors. The end of mitosis is characterized by spindle breakdown, shortened kinetochore microtubules, and pronounced outgrowth of astral (non-kinetochore) microtubules. For a normal eukaryotic cell, mitotic exit is irreversible.

<span class="mw-page-title-main">Motifs targeted by APC/C</span>

The anaphase- promoting complex or cyclosome (APC/C) is a highly specific ubiquitin protein ligase responsible for triggering events of late mitosis. In early mitosis, Cdc20 levels rise and APC/C binds to form active APC/CCdc20. This then leads to the destruction of mitotic cyclins, securin, and other proteins to trigger chromosome separation in anaphase. In early anaphase, Cdk1 is inactivated, leading to the activation of Cdh1, the other activator subunit of APC/C. This then triggers the degradation of Cdc20 and leads to the activation of APC/CCdh1 through G1 to suppress S- phase cyclin-Cdk activity. At the end of G1, APC/CCdh1 is inactivated and S- phase and mitotic cyclins gets reaccumulate as the cell progresses to S phase.

References

  1. 1 2 3 GRCh38: Ensembl release 89: ENSG00000147082 – Ensembl, May 2017
  2. 1 2 3 GRCm38: Ensembl release 89: ENSMUSG00000051592 – Ensembl, May 2017
  3. ↑ "Human PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  4. ↑ "Mouse PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  5. ↑ "CCNB3 cyclin B3 [Homo sapiens (human)] - Gene - NCBI". www.ncbi.nlm.nih.gov. Retrieved 2024-12-16.
  6. 1 2 3 4 Gallant, P.; Nigg, E. A. (1994-02-01). "Identification of a novel vertebrate cyclin: cyclin B3 shares properties with both A- and B-type cyclins". The EMBO Journal. 13 (3): 595–605. doi:10.1002/j.1460-2075.1994.tb06297.x. ISSN   0261-4189. PMC   394849 . PMID   8313904.
  7. ↑ Gunbin, Konstantin V.; Suslov, Valentin V.; Turnaev, Igor I.; Afonnikov, Dmitry A.; Kolchanov, Nikolay A. (2011-07-28). "Molecular evolution of cyclin proteins in animals and fungi". BMC Evolutionary Biology. 11 (1): 224. Bibcode:2011BMCEE..11..224G. doi: 10.1186/1471-2148-11-224 . ISSN   1471-2148. PMC   3162929 . PMID   21798004.
  8. 1 2 3 4 5 6 7 Nguyen, Thomas B.; Manova, Katia; Capodieci, Paola; Lindon, Catherine; Bottega, Steve; Wang, Xiang-Yuan; Refik-Rogers, Jale; Pines, Jonathon; Wolgemuth, Debra J.; Koff, Andrew (2002-11-01). "Characterization and expression of mammalian cyclin b3, a prepachytene meiotic cyclin". The Journal of Biological Chemistry. 277 (44): 41960–41969. doi: 10.1074/jbc.M203951200 . ISSN   0021-9258. PMID   12185076.
  9. 1 2 3 Karasu, Mehmet E.; Bouftas, Nora; Keeney, Scott; Wassmann, Katja (2019-04-01). "Cyclin B3 promotes anaphase I onset in oocyte meiosis". The Journal of Cell Biology. 218 (4): 1265–1281. doi:10.1083/jcb.201808091. ISSN   1540-8140. PMC   6446836 . PMID   30723090.
  10. 1 2 3 Lozano, Jean-Claude; Perret, Eric; Schatt, Philippe; Arnould, Cécile; Peaucellier, Gérard; Picard, André (2002-02-22). "Molecular cloning, gene localization, and structure of human cyclin B3". Biochemical and Biophysical Research Communications. 291 (2): 406–413. doi:10.1006/bbrc.2002.6458. ISSN   0006-291X. PMID   11846420.
  11. 1 2 Kim, Hye Min; Kang, Min Kook; Seong, Se Yoon; Jo, Jun Hyeon; Kim, Min Ju; Shin, Eun Kyeong; Lee, Chang Geun; Han, Seung Jin (2023-09-04). "Meiotic Cell Cycle Progression in Mouse Oocytes: Role of Cyclins". International Journal of Molecular Sciences. 24 (17): 13659. doi: 10.3390/ijms241713659 . ISSN   1422-0067. PMC   10487953 . PMID   37686466.
  12. ↑ Tschöp, Katrin; Müller, Gerd A.; Grosche, Jens; Engeland, Kurt (April 2006). "Human cyclin B3. mRNA expression during the cell cycle and identification of three novel nonclassical nuclear localization signals". The FEBS Journal. 273 (8): 1681–1695. doi:10.1111/j.1742-4658.2006.05184.x. ISSN   1742-464X. PMID   16623705.
  13. ↑ van der Voet, Monique; Lorson, Monique A.; Srinivasan, Dayalan G.; Bennett, Karen L.; van den Heuvel, Sander (2009-12-15). "C. elegans mitotic cyclins have distinct as well as overlapping functions in chromosome segregation". Cell Cycle (Georgetown, Tex.). 8 (24): 4091–4102. doi:10.4161/cc.8.24.10171. ISSN   1551-4005. PMC   3614003 . PMID   19829076.
  14. ↑ Deyter, Gary M. R.; Furuta, Tokiko; Kurasawa, Yasuhiro; Schumacher, Jill M. (2010-11-24). "Caenorhabditis elegans cyclin B3 is required for multiple mitotic processes including alleviation of a spindle checkpoint-dependent block in anaphase chromosome segregation". PLOS Genetics. 6 (11): e1001218. doi: 10.1371/journal.pgen.1001218 . ISSN   1553-7404. PMC   2991249 . PMID   21124864.
  15. ↑ Lara-Gonzalez, Pablo; Variyar, Smriti; Budrewicz, Jacqueline; Schlientz, Aleesa; Varshney, Neha; Bellaart, Andrew; Moghareh, Shabnam; Nguyen, Anh Cao Ngoc; Oegema, Karen; Desai, Arshad (2023-08-11). "Cyclin B3 is a dominant fast-acting cyclin that drives rapid early embryonic mitoses". BioRxiv: The Preprint Server for Biology: 2023.08.11.553011. doi:10.1101/2023.08.11.553011. ISSN   2692-8205. PMC   10441424 . PMID   37609212.
  16. ↑ Li, Yufei; Wang, Leyun; Zhang, Linlin; He, Zhengquan; Feng, Guihai; Sun, Hao; Wang, Jiaqiang; Li, Zhikun; Liu, Chao; Han, Jiabao; Mao, Junjie; Li, Pengcheng; Yuan, Xuewei; Jiang, Liyuan; Zhang, Ying (2019-05-06). "Cyclin B3 is required for metaphase to anaphase transition in oocyte meiosis I". The Journal of Cell Biology. 218 (5): 1553–1563. doi:10.1083/jcb.201808088. ISSN   1540-8140. PMC   6504906 . PMID   30770433.
  17. ↑ Bouftas, Nora; Schneider, Lena; Halder, Marc; Demmig, Rebecca; Baack, Martina; Cladière, Damien; Walter, Melanie; Al Abdallah, Hiba; Kleinhempel, Camilla; Messaritaki, Ria; Müller, Janina; Passarelli, Francesca; Wehrle, Patrick; Heim, Andreas; Wassmann, Katja (2022-10-10). "Cyclin B3 implements timely vertebrate oocyte arrest for fertilization". Developmental Cell. 57 (19): 2305–2320.e6. doi:10.1016/j.devcel.2022.09.005. ISSN   1878-1551. PMID   36182686.
  18. 1 2 Jacobs, H. W.; Knoblich, J. A.; Lehner, C. F. (1998-12-01). "Drosophila Cyclin B3 is required for female fertility and is dispensable for mitosis like Cyclin B". Genes & Development. 12 (23): 3741–3751. doi:10.1101/gad.12.23.3741. ISSN   0890-9369. PMC   317254 . PMID   9851980.
  19. ↑ Garrido, Damien; Bourouh, Mohammed; Bonneil, Éric; Thibault, Pierre; Swan, Andrew; Archambault, Vincent (November 2020). "Cyclin B3 activates the Anaphase-Promoting Complex/Cyclosome in meiosis and mitosis". PLOS Genetics. 16 (11): e1009184. doi: 10.1371/journal.pgen.1009184 . ISSN   1553-7404. PMC   7660922 . PMID   33137813.
  20. ↑ Tarailo-Graovac, Maja; Chen, Nansheng (August 2012). "Proper cyclin B3 dosage is important for precision of metaphase-to-anaphase onset timing in Caenorhabditis elegans". G3. 2 (8): 865–871. doi:10.1534/g3.112.002782. ISSN   2160-1836. PMC   3411242 . PMID   22908035.
  21. ↑ Refik-Rogers, Jale; Manova, Katia; Koff, Andrew (2006-08-11). "Misexpression of cyclin B3 leads to aberrant spermatogenesis". Cell Cycle (Georgetown, Tex.). 5 (17): 1966–1973. doi:10.4161/cc.5.17.3137. ISSN   1551-4005. PMID   16929180.
  22. ↑ Karasu, Mehmet E.; Keeney, Scott (2019-08-24). "Cyclin B3 is dispensable for mouse spermatogenesis". Chromosoma. 128 (3): 473–487. doi:10.1007/s00412-019-00725-5. ISSN   1432-0886. PMC   6824995 . PMID   31446450.
  23. ↑ Krskova, L.; Kabickova, E.; Drahokoupilova, E.; Kopeckova, K.; Plank, L.; Vitkova, P.; Mrhalova, M.; Zamecnik, J.; Kodet, R. (2018). "An undifferentiated sarcoma with BCOR-CCNB3 fusion transcript - pathological and clinical retrospective study". Neoplasma. 65 (4): 630–636. doi:10.4149/neo_2018_171107N716. ISSN   0028-2685. PMID   30064235.
  24. ↑ Pierron, Gaëlle; Tirode, Franck; Lucchesi, Carlo; Reynaud, Stéphanie; Ballet, Stelly; Cohen-Gogo, Sarah; Perrin, Virginie; Coindre, Jean-Michel; Delattre, Olivier (2012-03-04). "A new subtype of bone sarcoma defined by BCOR-CCNB3 gene fusion". Nature Genetics. 44 (4): 461–466. doi:10.1038/ng.1107. ISSN   1546-1718. PMID   22387997.
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