Meiotic recombination checkpoint

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

Contents

Spo11 catalyzes a double strand break (DSB) in one of the two homologous chromosomes to induce meiotic recombination. The repair of these DSBs are monitored at a DSB-dependent meiotic recombination checkpoint while at the DSB-independent meiotic recombination checkpoint the asynapsis of each homolog pair is examined. Malik meiotic recombination.JPG
Spo11 catalyzes a double strand break (DSB) in one of the two homologous chromosomes to induce meiotic recombination. The repair of these DSBs are monitored at a DSB-dependent meiotic recombination checkpoint while at the DSB-independent meiotic recombination checkpoint the asynapsis of each homolog pair is examined.

Generally speaking, the cell cycle regulation of meiosis is similar to that of mitosis. As in the mitotic cycle, these transitions are regulated by combinations of different gene regulatory factors, the cyclin-Cdk complex and the anaphase-promoting complex (APC). [1] The first major regulatory transition occurs in late G1, when the start of meiotic cycle is activated by Ime1 instead of Cln3/Cdk1 in mitosis. The second major transition occurs at the entry into metaphase I. The main purpose of this step is to make sure that DNA replication has completed without error so that spindle pole bodies can separate. This event is triggered by the activation of M-Cdk in late prophase I. Then the spindle assembly checkpoint examines the attachment of microtubules at kinetochores, followed by initiation of metaphase I by APCCdc20. The special chromosome separation in meiosis, homologous chromosomes separation in meiosis I and chromatids separation in meiosis II, requires special tension between homologous chromatids and non-homologous chromatids for distinguishing microtubule attachment and it relies on the programmed DNA double strand break (DSB) and repair in prophase I. Therefore meiotic recombination checkpoint can be a kind of DNA damage response at specific time spot. On the other hand, the meiotic recombination checkpoint also makes sure that meiotic recombination does happen in every pair of homologs.

DSB-dependent pathway

The abrupt onset of M-Cdk in late prophase I depends on the positive transcription regulation feedback loop consisting of Ime2, Ndt80 and Cdk/cyclin complex. However the activation of M-Cdk is controlled by the general phosphorylation switch Wee1/Cdc25. Wee1 activity is high in early prophase I and the accumulation of Cdc25 activates M-Cdk by direct phosphorylation and marking Wee1 to be degraded. Meiotic recombination may begin with a double-strand break, either induced by Spo11 [2] or by other endogenous or exogenous causes of DNA damage. These DNA breaks must be repaired before metaphase I. and these DSBs must be repaired before metaphase I. The cell monitor these DSBs via ATM pathway, in which Cdc25 is suppressed when DSB lesion is detected. This pathway is the same as classical DNA damage response and is the part we know the best in meiotic recombination checkpoint.

DSB-independent pathway

The DSB-independent pathway was proposed when people studied spo11 mutant cells in some species and found that these Spo11 cells could not process to metaphase I even in the absence of DSB. [3] The direct purpose of these DSBs is to help with the condensation of chromosomes. Even though the initial homolog paring in early leptotene is just random interactions, the further progression into presynaptic alignment depends on the formation of double strand breaks and single strand transfer complexes. [1] [4] Therefore the unsynapsed chromosomes in Spo11 cells can be a target of checkpoint. An AAA–adenosine triphosphatase (AAA-ATPase) was found to be essential in this pathway. [5] but the mechanism is not yet clear. Some other studies also drew sex body formation into attention, and the signaling could be either structure based or transcription regulation such as meiotic sex chromosome inactivation. [6] [7] Under this cascade, failure to synapse will maintain the gene expression from sex chromosomes and some products may inhibit cell cycle progression. Meiotic sex chromosome inactivation only happens in male, which may partially be the reason why only Spo11 mutant spermatocytes but not oocytes fail to transition from prophase I to metaphase I. [3] [8] However the asynapsis does not happen only within sex chromosomes, and such transcription regulation was suspended until it was further expanded to all the chromosomes as meiotic silencing of unsynapsed chromatin, [9] but the effector gene is not found yet.

Meiotic checkpoint protein kinases CHEK1 and CHEK2

The central role in meiosis of human and mouse CHEK1 and CHEK2 and their orthologs in Saccharomyces cerevisiae , Caenorhabditis elegans , Schizosaccharomyces pombe and Drosophila has been reviewed by MacQueen and Hochwagen [10] and Subramanian and Hochwagen. [11] During meiotic recombination in human and mouse, CHEK1 protein kinase is important for integrating DNA damage repair with cell cycle arrest. [12] CHEK1 is expressed in the testes and associates with meiotic synaptonemal complexes during the zygonema and pachynema stages. [12] CHEK1 likely acts as an integrator for ATM and ATR signals and in monitoring meiotic recombination. [12] In mouse oocytes CHEK1 appears to be indispensable for prophase I arrest and to function at the G2/M checkpoint. [13]

CHEK2 regulates cell cycle progression and spindle assembly during mouse oocyte maturation and early embryo development. [14] Although CHEK2 is a down stream effector of the ATM kinase that responds primarily to double-strand breaks it can also be activated by ATR (ataxia-telangiectasia and Rad3 related) kinase that responds primarily to single-strand breaks. In mouse, CHEK2 is essential for DNA damage surveillance in female meiosis. The response of oocytes to DNA double-strand break damage involves a pathway hierarchy in which ATR kinase signals to CHEK2 which then activates p53 and p63 proteins. [15]

In the fruitfly Drosophila , irradiation of germ line cells generates double-strand breaks that result in cell cycle arrest and apoptosis. The Drosophila CHEK2 ortholog mnk and the p53 ortholog dp53 are required for much of the cell death observed in early oogenesis when oocyte selection and meiotic recombination occur. [16]

Meiosis-specific Transcription factor Ndt80

Ndt80 is a meiosis-specific transcription factor required for successful completion of meiosis and spore formation. [17] The protein recognizes and binds to the middle sporulation element (MSE) 5'-C[AG]CAAA[AT]-3' in the promoter region of stage-specific genes that are required for progression through meiosis and sporulation. [17] [18] [19] The DNA-binding domain of Ndt80 has been isolated, and the structure reveals that this protein is a member of the Ig-fold family of transcription factors. [20] Ndt80 also competes with the repressor SUM1 for binding to promoters containing MSEs. [21]

Transitions in yeast

When a mutation inactivates Ndt80 in budding yeast, meiotic cells display a prolonged delay in late pachytene, the third stage of prophase. [22] The cells display intact synaptonemal complexes but eventually arrest in the diffuse chromatin stage that follows pachytene. This checkpoint-mediated arrest prevents later events from occurring until earlier events have been executed successfully and prevents chromosome missegregation. [23] [24]

Role in cell cycle progression

NDt80 is crucial for the completion of prophase and entry into meiosis 1, as it stimulates the expression of a large number of middle meiotic genes. Ndt80 is regulated through transcriptional and post-translational mechanisms (i.e. phosphorylation).

Interaction with Clb1

Ndt80 stimulates the expression of the B-type cyclin Clb-1, which greatly interacts with Cdk1 during meiotic divisions. [25] Active complexes of Clb-1 with Cdk1 play a large role in triggering the events of the first meiotic division, and their activity is restricted to meiosis 1. [26]

Interaction with Ime2

Ndt80 stimulates expression of itself and expression of protein kinase Ime2, both of which feedback to further stimulate Ndt80. This increased amount of Ndt80 protein further enhances the transcription of target genes. [24] Early in meiosis 1, Ime2 activity rises and is required for the normal accumulation and activity of Ndt80. However, if Ndt80 is expressed prematurely, it will initially accumulate in an unmodified form. Ime2 can then also act as a meiosis-specific kinase that phosphorylates Ndt80, resulting in fully activated Ndt80. [27]

Expression of Plk

Ndt80 stimulates the expression of the gene that encodes polo-like kinase, Plk. This protein is activated in late pachytene and is needed for crossover formation and partial loss of cohesion from chromosome arms. Plk is also both necessary and sufficient to trigger exit from pachytene points. [28] [29]

Recombination model

The meiotic recombination checkpoint operates in response to defects in meiotic recombination and chromosome synapsis, potentially arresting cells before entry into meiotic divisions. [30] Because recombination is initiated by double stranded breaks (DSBs) at certain regions of the genome, entry into Meiosis 1 must be delayed until the DSBs are repaired. [31] The meiosis-specific kinase Mek1 plays an important role in this and recently, it has been discovered that Mek1 is able to phosphorylate Ndt80 independently of IME2. This phosphorylation, however, is inhibitory and prevents Ndt80 from binding to MSEs in the presence of DSBs. [32]

Roles outside of cell cycle progression

Heterokaryon Incompatibility

Heterokaryon Incompatibility (HI) has been likened to a fungal immune system; [33] it is a non-self recognition mechanism that is ubiquitous among filamentous members of the Asomycota phylum of the Fungi kingdom. [34] Vib-1 is an Ndt80 homologue in Neurospora crassa and is required for HI in this species. It has been found that mutations at the vib1 locus suppress non-self recognition, and VIB-1 is required for the production of downstream effectors associated with HI, such as extracellular proteases. [35] [36]

Female sexual development

Studies have indicated that Ndt80 homologues also play a role in female sexual development in fungi species other than the more commonly studied Saccharomyces cerevisiae. [35] [37] Mutations in vib-1 have been found to affect the timing and development of female reproductive structures prior to fertilization. [37]

Role in Cancer

Although usually characterized in yeast and other fungi, the DNA-binding domain of Ndt80 is homologous to a number of proteins in higher eukaryotes and the residues used for binding are highly conserved. In humans, the Ndt80 homologue C11orf9 is highly expressed in invasive or metastatic tumor cells, suggesting potential usage as a target molecule in cancer treatment. [38] However, not much progress has been made on this front in recent years.

See also

Related Research Articles

Cell cycle Series of events and stages that result in cell division

The cell cycle, or cell-division cycle, is the series of events that take place in a cell that cause it to divide into two daughter cells. These events include the duplication of its DNA and some of its organelles, and subsequently the partitioning of its cytoplasm and other components into two daughter cells in a process called cell division.

Meiosis Type of cell division in sexually-reproducing organisms used to produce gametes

Meiosis is a special type of cell division of germ cells in sexually-reproducing organisms used to produce the gametes, such as sperm or egg cells. It involves two rounds of division that ultimately result in four cells with only one copy of each chromosome (haploid). 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 female will fuse to create a cell with two copies of each chromosome again, the zygote.

Cell division The process resulting in division and partitioning of components of a cell to form more cells; may or may not be accompanied by the physical separation of a cell into distinct, individually membrane-bounded daughter cells.

Cell division is the process by which a parent cell divides into two or more daughter cells. Cell division usually occurs as part of a larger cell cycle. In eukaryotes, there are two distinct types of cell division; a vegetative division, whereby each daughter cell is genetically identical to the parent cell (mitosis), and a reproductive cell division, whereby the number of chromosomes in the daughter cells is reduced by half to produce haploid gametes (meiosis). In cell biology, mitosis (/maɪˈtoʊsɪs/) 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 often 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 mitotic (M) phase of an animal cell cycle—the division of the mother cell into two genetically identical daughter cells. Meiosis results in four haploid daughter cells by undergoing one round of DNA replication followed by two divisions. Homologous chromosomes are separated in the first division, and sister chromatids are separated in the second division. 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.

Chromosomal crossover Cellular process

Chromosomal crossover, or crossing over, is the exchange of genetic material during sexual reproduction between two homologous chromosomes' non-sister chromatids that results in recombinant chromosomes. It is one of the final phases of genetic recombination, which occurs in the pachytene stage of prophase I of meiosis during a process called synapsis. Synapsis begins before the synaptonemal complex develops and is not completed until near the end of prophase I. Crossover usually occurs when matching regions on matching chromosomes break and then reconnect to the other chromosome.

Prophase First phase of cell division in both mitosis and meiosis

Prophase (from the Greek πρό, "before" and φάσις, "stage") is the first stage of cell division in both mitosis and meiosis. Beginning after interphase, DNA has already been replicated when the cell enters prophase. The main occurrences in prophase are the condensation of the chromatin reticulum and the disappearance of the nucleolus.

Genetic recombination Production of offspring with combinations of traits that differ from those found in either parent

Genetic recombination is the exchange of genetic material between different organisms which leads to production of offspring with combinations of traits that differ from those found in either parent. In eukaryotes, genetic recombination during meiosis can lead to a novel set of genetic information that can be passed on from the parents to the offspring. Most recombination is naturally occurring.

Oogenesis

Oogenesis, ovogenesis, or oögenesis is the differentiation of the ovum into a cell competent to further develop when fertilized. It is developed from the primary oocyte by maturation. Oogenesis is initiated in the embryonic stage.

Synaptonemal complex Protein structure

The synaptonemal complex (SC) is a protein structure that forms between homologous chromosomes during meiosis and is thought to mediate synapsis and recombination during meiosis I in eukaryotes. It is currently thought that the SC functions primarily as a scaffold to allow interacting chromatids to complete their crossover activities.

Endoreduplication is replication of the nuclear genome in the absence of mitosis, which leads to elevated nuclear gene content and polyploidy. Endoreplication can be understood simply as a variant form of the mitotic cell cycle (G1-S-G2-M) in which mitosis is circumvented entirely, due to modulation of cyclin-dependent kinase (CDK) activity. Examples of endoreplication characterized in arthropod, mammalian, and plant species suggest that it is a universal developmental mechanism responsible for the differentiation and morphogenesis of cell types that fulfill an array of biological functions. While endoreplication is often limited to specific cell types in animals, it is considerably more widespread in plants, such that polyploidy can be detected in the majority of plant tissues.

Synapsis Biological phenomenon in meiosis

Synapsis is the pairing of two chromosomes that occurs during meiosis. It allows matching-up of homologous pairs prior to their segregation, and possible chromosomal crossover between them. Synapsis takes place during prophase I of meiosis. When homologous chromosomes synapse, their ends are first attached to the nuclear envelope. These end-membrane complexes then migrate, assisted by the extranuclear cytoskeleton, until matching ends have been paired. Then the intervening regions of the chromosome are brought together, and may be connected by a protein-RNA complex called the synaptonemal complex. Autosomes undergo synapsis during meiosis, and are held together by a protein complex along the whole length of the chromosomes called the synaptonemal complex. Sex chromosomes also undergo synapsis; however, the synaptonemal protein complex that holds the homologous chromosomes together is only present at one end of each sex chromosome.

Cell cycle checkpoint

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.

Bivalent (genetics)

A bivalent is one pair of chromosomes in a tetrad. A tetrad is the association of a pair of homologous chromosomes physically held together by at least one DNA crossover. This physical attachment allows for alignment and segregation of the homologous chromosomes in the first meiotic division.

CHEK2

CHEK2 is a tumor suppressor gene that encodes the protein CHK2, a serine-threonine kinase. CHK2 is involved in DNA repair, cell cycle arrest or apoptosis in response to DNA damage. Mutations to the CHEK2 gene have been linked to a wide range of cancers.

Chromosome segregation is the process in eukaryotes by which two sister chromatids formed as a consequence of DNA replication, or paired homologous chromosomes, separate from each other and migrate to opposite poles of the nucleus. This segregation process occurs during both mitosis and meiosis. Chromosome segregation also occurs in prokaryotes. However, in contrast to eukaryotic chromosome segregation, replication and segregation are not temporally separated. Instead segregation occurs progressively following replication.

CHEK1

Checkpoint kinase 1, commonly referred to as Chk1, is a serine/threonine-specific protein kinase that, in humans, is encoded by the CHEK1 gene. Chk1 coordinates the DNA damage response (DDR) and cell cycle checkpoint response. Activation of Chk1 results in the initiation of cell cycle checkpoints, cell cycle arrest, DNA repair and cell death to prevent damaged cells from progressing through the cell cycle.

REC8

Meiotic recombination protein REC8 homolog is a protein that in humans is encoded by the REC8 gene.

HORMAD1

HORMA domain-containing protein 1 (HORMAD1) also known as cancer/testis antigen 46 (CT46) is a protein that in humans is encoded by the HORMAD1 gene.

The leptotene stage, also known as the leptonema, is the first of five substages of prophase I in meiosis. The term leptonema derives from Greek words meaning "thin threads". A cell destined to become a gamete enters the leptotene stage after its chromosomes are duplicated during interphase. During the leptotene stage those duplicated chromosomes—each consisting of two sister chromatids—condense from diffuse chromatin into long, thin strands that are more visible within the nucleoplasm. The next stage of prophase I in meiosis is the zygotene stage.

The origin and function of meiosis are currently not well understood scientifically, and would provide fundamental insight into the evolution of sexual reproduction in eukaryotes. There is no current consensus among biologists on the questions of how sex in eukaryotes arose in evolution, what basic function sexual reproduction serves, and why it is maintained, given the basic two-fold cost of sex. It is clear that it evolved over 1.2 billion years ago, and that almost all species which are descendants of the original sexually reproducing species are still sexual reproducers, including plants, fungi, and animals.

Resumption of meiosis occurs as a part of oocyte meiosis after meiotic arrest has occurred. In females, meiosis of an oocyte begins during embryogenesis and will be completed after puberty. A primordial follicle will arrest, allowing the follicle to grow in size and mature. Resumption of meiosis will resume following an ovulatory surge (ovulation) of luteinising hormone (LH).

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