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Deficiency Does Not Alleviate Meiotic Arrest Phenotypes of Mutants Defective in Synapsis\nTo determine if TRIP13 deficiency prevents apoptosis triggered by asynapsis as in C. elegans, we analyzed mice that were doubly mutant for Spo11 and Trip13. SPO11 is a transesterase that is essential for the creation of genetically programmed DSB during leptonema of many organisms, including mice [18]. In C. elegans, spo-11 mutant gametes have extensive asynapsis, which triggers PCH-2 dependent apoptosis in pachynema [2]. In mice, Spo11 −/− spermatocytes are severely defective in homologous chromosome synapsis [34,35], and arrest with chromosomes in a state characteristic of the zygotene/pachytene transition (Figure 3H). Spermatocytes in Trip13Gt/Gt Spo11 −/− testes progressed maximally to that point before undergoing death (Figs 3I), well before the spindle checkpoint that eliminates achiasmate spermatocytes [36]. There was no evidence of metaphase I spermatocytes or postmeiotic spermatids in these testes, unlike those seen in Trip13 single mutants (Figure 3G). In contrast to the complete synapsis in Trip13Gt/Gt pachytene spermatocytes (Figure 5A), in which SPO11 is available in leptonema to initiate (via DSB induction, Figure S2A and S2B) a recombination-driven homolog search, chromosome synapsis in doubly mutant spermatocytes was highly disrupted as in Spo11 single mutants (Figure 5B and 5C). Identical studies were performed with mice deficient for Mei1, a vertebrate-specific gene also required for DSB formation and chromosome synapsis [37], with similar results (Figure 3J and 3K; immunocytology not shown).\nFigure 5 Immunocytological Analysis of Trip13 Compound Mutants\nSurface-spread chromosomes were immunolabeled with the indicated antibodies and fluorophores. Genotypes are indicated, as are those panels in which dual staining patterns are merged. Note that (H) and (I) are at lower magnification to show multiple nuclei. In yeast, deletion of PCH2 alleviates the pachytene arrest caused by asynaptic mutants zip1 and zip2 [8]. Although mouse SYCP1 might be a functional equivalent of Zip1p, because Sycp1 mutant spermatocytes arrest at approximately the same point as Trip13 mutants, there would be no opportunity to observe bypass of Sycp1 −/−. Since Zip2p is present at sites of axial associations, even in zip1 mutants, it has been suggested that Zip2p promotes initiation of chromosome synapsis [38]. These observations raise the possibility that in yeast, Pch2p responds to synapsis polymerization rather than initiation. To test this, we performed epistasis analysis with a Rec8 allele (Rec8Mei8, abbreviated as Rec8 −). Meiotic chromosomes of Rec8 mutant spermatocytes undergo apparent homolog pairing and interhomolog synaptic initiation, but are defective in DSB repair and fail to maintain interhomolog synapsis [39,40]. Rather, sister chromatids appear to synapse and are bound by SYCP1 along their axes. Rec8 mutants do not progress to diplonema or metaphase I. Double mutant analysis indicated that Rec8 is epistatic to Trip13. As in the Spo11 and Mei1 experiments, histology of testes deficient for both REC8 and TRIP13 resembled the Rec8 mutant, with no evidence of progression to metaphase I that occurs in Trip13Gt/Gt mice (Figure 3L and 3M). Immunocytological analysis of spread chromosomes showed a failure of homologous chromosome synapsis in both the Rec8 −/− and Rec8 −/− Trip13Gt/Gt spermatocytes, as previously reported for Rec8 mutants (Figure 5D and 5E) [39,40].\nAlthough subsequent reports indicate otherwise [10,12], deletion of PCH2 in yeast was originally reported to alleviate meiotic arrest caused by deficiency for the meiosis-specific RecA homolog DMC1 [8]. To investigate this relationship in mice, we constructed animals doubly mutant for Trip13 and Dmc1. As in Dmc1 −/− mice, in which spermatocytes undergo meiotic arrest from defective DSB repair and failed chromosome synapsis [16], spermatogenesis in Dmc1 −/− Trip13Gt/Gt testes was uniformly arrested at the point where spermatocytes contained chromatin characteristic of zygonema/pachynema (Figure 3N). Immunocytological analysis indicated that both Dmc1 −/− and Dmc1 −/− Trip13Gt/Gt chromosomes had extensive asynapsis compared to Trip13Gt single mutants (Figure 5F–5H), and all had persistent RAD51/DMC1 foci and phosphorylated H2AX (γH2AX; Figure 5I–5L), confirming that Dmc1 is epistatic to Trip13. Doubly mutant females had residual ovaries, phenocopying Dmc1 −/− and Trip13Gt/Gt single mutants (unpublished data)."}

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Deficiency Does Not Alleviate Meiotic Arrest Phenotypes of Mutants Defective in Synapsis\nTo determine if TRIP13 deficiency prevents apoptosis triggered by asynapsis as in C. elegans, we analyzed mice that were doubly mutant for Spo11 and Trip13. SPO11 is a transesterase that is essential for the creation of genetically programmed DSB during leptonema of many organisms, including mice [18]. In C. elegans, spo-11 mutant gametes have extensive asynapsis, which triggers PCH-2 dependent apoptosis in pachynema [2]. In mice, Spo11 −/− spermatocytes are severely defective in homologous chromosome synapsis [34,35], and arrest with chromosomes in a state characteristic of the zygotene/pachytene transition (Figure 3H). Spermatocytes in Trip13Gt/Gt Spo11 −/− testes progressed maximally to that point before undergoing death (Figs 3I), well before the spindle checkpoint that eliminates achiasmate spermatocytes [36]. There was no evidence of metaphase I spermatocytes or postmeiotic spermatids in these testes, unlike those seen in Trip13 single mutants (Figure 3G). In contrast to the complete synapsis in Trip13Gt/Gt pachytene spermatocytes (Figure 5A), in which SPO11 is available in leptonema to initiate (via DSB induction, Figure S2A and S2B) a recombination-driven homolog search, chromosome synapsis in doubly mutant spermatocytes was highly disrupted as in Spo11 single mutants (Figure 5B and 5C). Identical studies were performed with mice deficient for Mei1, a vertebrate-specific gene also required for DSB formation and chromosome synapsis [37], with similar results (Figure 3J and 3K; immunocytology not shown).\nFigure 5 Immunocytological Analysis of Trip13 Compound Mutants\nSurface-spread chromosomes were immunolabeled with the indicated antibodies and fluorophores. Genotypes are indicated, as are those panels in which dual staining patterns are merged. Note that (H) and (I) are at lower magnification to show multiple nuclei. In yeast, deletion of PCH2 alleviates the pachytene arrest caused by asynaptic mutants zip1 and zip2 [8]. Although mouse SYCP1 might be a functional equivalent of Zip1p, because Sycp1 mutant spermatocytes arrest at approximately the same point as Trip13 mutants, there would be no opportunity to observe bypass of Sycp1 −/−. Since Zip2p is present at sites of axial associations, even in zip1 mutants, it has been suggested that Zip2p promotes initiation of chromosome synapsis [38]. These observations raise the possibility that in yeast, Pch2p responds to synapsis polymerization rather than initiation. To test this, we performed epistasis analysis with a Rec8 allele (Rec8Mei8, abbreviated as Rec8 −). Meiotic chromosomes of Rec8 mutant spermatocytes undergo apparent homolog pairing and interhomolog synaptic initiation, but are defective in DSB repair and fail to maintain interhomolog synapsis [39,40]. Rather, sister chromatids appear to synapse and are bound by SYCP1 along their axes. Rec8 mutants do not progress to diplonema or metaphase I. Double mutant analysis indicated that Rec8 is epistatic to Trip13. As in the Spo11 and Mei1 experiments, histology of testes deficient for both REC8 and TRIP13 resembled the Rec8 mutant, with no evidence of progression to metaphase I that occurs in Trip13Gt/Gt mice (Figure 3L and 3M). Immunocytological analysis of spread chromosomes showed a failure of homologous chromosome synapsis in both the Rec8 −/− and Rec8 −/− Trip13Gt/Gt spermatocytes, as previously reported for Rec8 mutants (Figure 5D and 5E) [39,40].\nAlthough subsequent reports indicate otherwise [10,12], deletion of PCH2 in yeast was originally reported to alleviate meiotic arrest caused by deficiency for the meiosis-specific RecA homolog DMC1 [8]. To investigate this relationship in mice, we constructed animals doubly mutant for Trip13 and Dmc1. As in Dmc1 −/− mice, in which spermatocytes undergo meiotic arrest from defective DSB repair and failed chromosome synapsis [16], spermatogenesis in Dmc1 −/− Trip13Gt/Gt testes was uniformly arrested at the point where spermatocytes contained chromatin characteristic of zygonema/pachynema (Figure 3N). Immunocytological analysis indicated that both Dmc1 −/− and Dmc1 −/− Trip13Gt/Gt chromosomes had extensive asynapsis compared to Trip13Gt single mutants (Figure 5F–5H), and all had persistent RAD51/DMC1 foci and phosphorylated H2AX (γH2AX; Figure 5I–5L), confirming that Dmc1 is epistatic to Trip13. Doubly mutant females had residual ovaries, phenocopying Dmc1 −/− and Trip13Gt/Gt single mutants (unpublished data)."}

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SPO11 is a transesterase that is essential for the creation of genetically programmed DSB during leptonema of many organisms, including mice [18]. In C. elegans, spo-11 mutant gametes have extensive asynapsis, which triggers PCH-2 dependent apoptosis in pachynema [2]. In mice, Spo11 −/− spermatocytes are severely defective in homologous chromosome synapsis [34,35], and arrest with chromosomes in a state characteristic of the zygotene/pachytene transition (Figure 3H). Spermatocytes in Trip13Gt/Gt Spo11 −/− testes progressed maximally to that point before undergoing death (Figs 3I), well before the spindle checkpoint that eliminates achiasmate spermatocytes [36]. There was no evidence of metaphase I spermatocytes or postmeiotic spermatids in these testes, unlike those seen in Trip13 single mutants (Figure 3G). In contrast to the complete synapsis in Trip13Gt/Gt pachytene spermatocytes (Figure 5A), in which SPO11 is available in leptonema to initiate (via DSB induction, Figure S2A and S2B) a recombination-driven homolog search, chromosome synapsis in doubly mutant spermatocytes was highly disrupted as in Spo11 single mutants (Figure 5B and 5C). Identical studies were performed with mice deficient for Mei1, a vertebrate-specific gene also required for DSB formation and chromosome synapsis [37], with similar results (Figure 3J and 3K; immunocytology not shown).\nFigure 5 Immunocytological Analysis of Trip13 Compound Mutants\nSurface-spread chromosomes were immunolabeled with the indicated antibodies and fluorophores. Genotypes are indicated, as are those panels in which dual staining patterns are merged. Note that (H) and (I) are at lower magnification to show multiple nuclei. In yeast, deletion of PCH2 alleviates the pachytene arrest caused by asynaptic mutants zip1 and zip2 [8]. Although mouse SYCP1 might be a functional equivalent of Zip1p, because Sycp1 mutant spermatocytes arrest at approximately the same point as Trip13 mutants, there would be no opportunity to observe bypass of Sycp1 −/−. Since Zip2p is present at sites of axial associations, even in zip1 mutants, it has been suggested that Zip2p promotes initiation of chromosome synapsis [38]. These observations raise the possibility that in yeast, Pch2p responds to synapsis polymerization rather than initiation. To test this, we performed epistasis analysis with a Rec8 allele (Rec8Mei8, abbreviated as Rec8 −). Meiotic chromosomes of Rec8 mutant spermatocytes undergo apparent homolog pairing and interhomolog synaptic initiation, but are defective in DSB repair and fail to maintain interhomolog synapsis [39,40]. Rather, sister chromatids appear to synapse and are bound by SYCP1 along their axes. Rec8 mutants do not progress to diplonema or metaphase I. Double mutant analysis indicated that Rec8 is epistatic to Trip13. As in the Spo11 and Mei1 experiments, histology of testes deficient for both REC8 and TRIP13 resembled the Rec8 mutant, with no evidence of progression to metaphase I that occurs in Trip13Gt/Gt mice (Figure 3L and 3M). Immunocytological analysis of spread chromosomes showed a failure of homologous chromosome synapsis in both the Rec8 −/− and Rec8 −/− Trip13Gt/Gt spermatocytes, as previously reported for Rec8 mutants (Figure 5D and 5E) [39,40].\nAlthough subsequent reports indicate otherwise [10,12], deletion of PCH2 in yeast was originally reported to alleviate meiotic arrest caused by deficiency for the meiosis-specific RecA homolog DMC1 [8]. To investigate this relationship in mice, we constructed animals doubly mutant for Trip13 and Dmc1. As in Dmc1 −/− mice, in which spermatocytes undergo meiotic arrest from defective DSB repair and failed chromosome synapsis [16], spermatogenesis in Dmc1 −/− Trip13Gt/Gt testes was uniformly arrested at the point where spermatocytes contained chromatin characteristic of zygonema/pachynema (Figure 3N). Immunocytological analysis indicated that both Dmc1 −/− and Dmc1 −/− Trip13Gt/Gt chromosomes had extensive asynapsis compared to Trip13Gt single mutants (Figure 5F–5H), and all had persistent RAD51/DMC1 foci and phosphorylated H2AX (γH2AX; Figure 5I–5L), confirming that Dmc1 is epistatic to Trip13. Doubly mutant females had residual ovaries, phenocopying Dmc1 −/− and Trip13Gt/Gt single mutants (unpublished data)."}

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Deficiency Does Not Alleviate Meiotic Arrest Phenotypes of Mutants Defective in Synapsis\nTo determine if TRIP13 deficiency prevents apoptosis triggered by asynapsis as in C. elegans, we analyzed mice that were doubly mutant for Spo11 and Trip13. SPO11 is a transesterase that is essential for the creation of genetically programmed DSB during leptonema of many organisms, including mice [18]. In C. elegans, spo-11 mutant gametes have extensive asynapsis, which triggers PCH-2 dependent apoptosis in pachynema [2]. In mice, Spo11 −/− spermatocytes are severely defective in homologous chromosome synapsis [34,35], and arrest with chromosomes in a state characteristic of the zygotene/pachytene transition (Figure 3H). Spermatocytes in Trip13Gt/Gt Spo11 −/− testes progressed maximally to that point before undergoing death (Figs 3I), well before the spindle checkpoint that eliminates achiasmate spermatocytes [36]. There was no evidence of metaphase I spermatocytes or postmeiotic spermatids in these testes, unlike those seen in Trip13 single mutants (Figure 3G). In contrast to the complete synapsis in Trip13Gt/Gt pachytene spermatocytes (Figure 5A), in which SPO11 is available in leptonema to initiate (via DSB induction, Figure S2A and S2B) a recombination-driven homolog search, chromosome synapsis in doubly mutant spermatocytes was highly disrupted as in Spo11 single mutants (Figure 5B and 5C). Identical studies were performed with mice deficient for Mei1, a vertebrate-specific gene also required for DSB formation and chromosome synapsis [37], with similar results (Figure 3J and 3K; immunocytology not shown).\nFigure 5 Immunocytological Analysis of Trip13 Compound Mutants\nSurface-spread chromosomes were immunolabeled with the indicated antibodies and fluorophores. Genotypes are indicated, as are those panels in which dual staining patterns are merged. Note that (H) and (I) are at lower magnification to show multiple nuclei. In yeast, deletion of PCH2 alleviates the pachytene arrest caused by asynaptic mutants zip1 and zip2 [8]. Although mouse SYCP1 might be a functional equivalent of Zip1p, because Sycp1 mutant spermatocytes arrest at approximately the same point as Trip13 mutants, there would be no opportunity to observe bypass of Sycp1 −/−. Since Zip2p is present at sites of axial associations, even in zip1 mutants, it has been suggested that Zip2p promotes initiation of chromosome synapsis [38]. These observations raise the possibility that in yeast, Pch2p responds to synapsis polymerization rather than initiation. To test this, we performed epistasis analysis with a Rec8 allele (Rec8Mei8, abbreviated as Rec8 −). Meiotic chromosomes of Rec8 mutant spermatocytes undergo apparent homolog pairing and interhomolog synaptic initiation, but are defective in DSB repair and fail to maintain interhomolog synapsis [39,40]. Rather, sister chromatids appear to synapse and are bound by SYCP1 along their axes. Rec8 mutants do not progress to diplonema or metaphase I. Double mutant analysis indicated that Rec8 is epistatic to Trip13. As in the Spo11 and Mei1 experiments, histology of testes deficient for both REC8 and TRIP13 resembled the Rec8 mutant, with no evidence of progression to metaphase I that occurs in Trip13Gt/Gt mice (Figure 3L and 3M). Immunocytological analysis of spread chromosomes showed a failure of homologous chromosome synapsis in both the Rec8 −/− and Rec8 −/− Trip13Gt/Gt spermatocytes, as previously reported for Rec8 mutants (Figure 5D and 5E) [39,40].\nAlthough subsequent reports indicate otherwise [10,12], deletion of PCH2 in yeast was originally reported to alleviate meiotic arrest caused by deficiency for the meiosis-specific RecA homolog DMC1 [8]. To investigate this relationship in mice, we constructed animals doubly mutant for Trip13 and Dmc1. As in Dmc1 −/− mice, in which spermatocytes undergo meiotic arrest from defective DSB repair and failed chromosome synapsis [16], spermatogenesis in Dmc1 −/− Trip13Gt/Gt testes was uniformly arrested at the point where spermatocytes contained chromatin characteristic of zygonema/pachynema (Figure 3N). Immunocytological analysis indicated that both Dmc1 −/− and Dmc1 −/− Trip13Gt/Gt chromosomes had extensive asynapsis compared to Trip13Gt single mutants (Figure 5F–5H), and all had persistent RAD51/DMC1 foci and phosphorylated H2AX (γH2AX; Figure 5I–5L), confirming that Dmc1 is epistatic to Trip13. Doubly mutant females had residual ovaries, phenocopying Dmc1 −/− and Trip13Gt/Gt single mutants (unpublished data)."}