Homologous pairing and chromosome dynamics in meiosis and mitosis

McKee, Bruce D.

doi:10.1016/j.bbaexp.2003.11.017

Cited by 185 publications

(167 citation statements)

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“…Such pairing at first might appear to be a striking novelty. Yet, widespread pairing of homologs in somatic (nonmeiotic) cells has been found both in Drosophila (McKee 2004) and in yeast (Burgess et al 1999). Such somatic pairing differs from meiotic synapsis in three respects: (1) it is not as extensive (McKee 2004); (2) it does not lead to the levels of genetic recombination seen in meiosis; and (3) it terminates in either interphase or prophase, allowing each chromosome to proceed to the metaphase plate independently of its homolog.…”

Section: Identifying a Key Step In The Evolution Of Meiosis From Mitosismentioning

confidence: 97%

“…Yet, widespread pairing of homologs in somatic (nonmeiotic) cells has been found both in Drosophila (McKee 2004) and in yeast (Burgess et al 1999). Such somatic pairing differs from meiotic synapsis in three respects: (1) it is not as extensive (McKee 2004); (2) it does not lead to the levels of genetic recombination seen in meiosis; and (3) it terminates in either interphase or prophase, allowing each chromosome to proceed to the metaphase plate independently of its homolog. Nevertheless, if such homolog pairing in mitotic cells is an ancestral eukaryotic property, then the origins of meiotic synapsis need have involved only its temporal extension into metaphase and more intimate or extensive apposition of homologs, especially at the kinetochores.…”

Section: Identifying a Key Step In The Evolution Of Meiosis From Mitosismentioning

confidence: 97%

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The Evolution of Meiosis From Mitosis

2009

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Section: Identifying a Key Step In The Evolution Of Meiosis From Mitosismentioning

confidence: 97%

Section: Identifying a Key Step In The Evolution Of Meiosis From Mitosismentioning

confidence: 97%

The Evolution of Meiosis From Mitosis

2009

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“…These results imply that 240-bp repeats function to mediate association of sex chromosomes with SNM and MNM. P AIRING of homologous chromosomes is an essential step in meiosis, setting the stage for the segregation of homologs to opposite poles (Page and Hawley 2003;McKee 2004). In most eukaryotes, pairing is accompanied by high frequencies of recombination and by formation of synaptonemal complexes, proteinaceous structures that connect homologs from end to end during the pachytene stage of meiotic prophase.…”

Section: Introductionmentioning

confidence: 99%

Meiotic Pairing and Disjunction of Mini-X Chromosomes in Drosophila Is Mediated by 240-bp rDNA Repeats and the Homolog Conjunction Proteins SNM and MNM

Thomas

McKee

2007

Genetics

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In most eukaryotes, segregation of homologous chromosomes during meiosis is dependent on crossovers that occur while the homologs are intimately paired during early prophase. Crossovers generate homolog connectors known as chiasmata that are stabilized by cohesion between sister-chromatid arms. In Drosophila males, homologs pair and segregate without recombining or forming chiasmata. Stable pairing of homologs is dependent on two proteins, SNM and MNM, that associate with chromosomes throughout meiosis I until their removal at anaphase I. SNM and MNM localize to the rDNA region of the X-Y pair, which contains 240-bp repeats that have previously been shown to function as cis-acting chromosome pairing/segregation sites. Here we show that heterochromatic mini-X chromosomes lacking native rDNA but carrying transgenic 240-bp repeat arrays segregate preferentially from full-length sex chromosomes and from each other. Mini-X pairs do not form autonomous bivalents but do associate at high frequency with the X-Y bivalent to form trivalents and quadrivalents. Both disjunction of mini-X pairs and multivalent formation are dependent on the presence of SNM and MNM. These results imply that 240-bp repeats function to mediate association of sex chromosomes with SNM and MNM. P AIRING of homologous chromosomes is an essential step in meiosis, setting the stage for the segregation of homologs to opposite poles (Page and Hawley 2003;McKee 2004). In most eukaryotes, pairing is accompanied by high frequencies of recombination and by formation of synaptonemal complexes, proteinaceous structures that connect homologs from end to end during the pachytene stage of meiotic prophase. Segregation of homologs requires not only that they pair but also that they undergo at least one crossover. Crossovers generate cytologically visible linkers known as chiasmata, which are essential to maintaining bivalent integrity throughout late prophase I and metaphase I (Hawley 1988).However, synaptonemal complexes, crossing over, and chiasmata are not universal prerequisites for meiotic chromosome segregation. Achiasmate segregation, i.e., segregation of homologs without chiasmata, is found in one sex or the other in several groups of eukaryotes (Wolf 1994). In Drosophila male meiosis, crossing over is normally completely absent and the homologs fail to form either synaptonemal complexes or chiasmata, yet homologs are stably conjoined during late prophase I and metaphase I and segregate from one another with great regularity during anaphase I.Recent data show that stable conjunction and accurate segregation of all four homolog pairs in Drosophila male meiosis depends upon two proteins: stromalin in meiosis (SNM), a homolog of the SCC3/SA cohesin proteins, and Mod(mdg4) in meiosis (MNM), a BTB domain protein (Thomas et al. 2005). SNM and MNM colocalize to meiotic chromosomes throughout prophase I and metaphase I but disappear at the onset of anaphase I, suggesting that they function directly in stabilization of pairing, i.e., as substitutes for ch...

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“…In Drosophila, homologous chromosomes are stably paired from end to end in virtually all cells of the organism (reviewed by McKee 2004). The potential for communication between Drosophila homologs was first postulated .100 years ago by Nettie Stevens (Stevens 1908) and was demonstrated genetically in 1954 by Ed Lewis, who coined the term transvection to describe the phenomenon of pairing-dependent gene regulation (Lewis 1954).…”

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confidence: 99%

Comparing Enhancer Action in Cis and in Trans

2012

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Studies from diverse systems have shown that distinct interchromosomal interactions are a central component of nuclear organization. In some cases, these interactions allow an enhancer to act in trans, modulating the expression of a gene encoded on a separate chromosome held in close proximity. Despite recent advances in uncovering such phenomena, our understanding of how a regulatory element acts on another chromosome remains incomplete. Here, we describe a transgenic approach to better understand enhancer action in trans in Drosophila melanogaster. Using phiC31-based recombinase-mediated cassette exchange (RMCE), we placed transgenes carrying combinations of the simple enhancer GMR, a minimal promoter, and different fluorescent reporters at equivalent positions on homologous chromosomes so that they would pair via the endogenous somatic pairing machinery of Drosophila. Our data demonstrate that the enhancer GMR is capable of activating a promoter in trans and does so in a variegated pattern, suggesting stochastic interactions between the enhancer and the promoter when they are carried on separate chromosomes. Furthermore, we quantitatively assessed the impact of two concurrent promoter targets in cis and in trans to GMR, demonstrating that each promoter is capable of competing for the enhancer's activity, with the presence of one negatively affecting expression from the other. Finally, the single-cell resolution afforded by our approach allowed us to show that promoters in cis and in trans to GMR can both be activated in the same nucleus, implying that a single enhancer can share its activity between multiple promoter targets carried on separate chromosomes.

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Homologous pairing and chromosome dynamics in meiosis and mitosis

Cited by 185 publications

References 158 publications

The Evolution of Meiosis From Mitosis

The Evolution of Meiosis From Mitosis

Meiotic Pairing and Disjunction of Mini-X Chromosomes in Drosophila Is Mediated by 240-bp rDNA Repeats and the Homolog Conjunction Proteins SNM and MNM

Comparing Enhancer Action in Cis and in Trans

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