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Mouse Y-Encoded Transcription Factor Zfy2 Is Essential for Sperm Formation and Function in Assisted Fertilization.

Yamauchi Y, Riel JM, Ruthig V, Ward MA - PLoS Genet. (2015)

Bottom Line: Spermatogenesis is a key developmental process allowing for a formation of a mature male gamete.During its final phase, spermiogenesis, haploid round spermatids undergo cellular differentiation into spermatozoa, which involves extensive restructuring of cell morphology, DNA, and epigenome.Therefore, only three Y chromosome genes, Sry, Eif2s3y and Zfy2, constitute the minimum Y chromosome complement compatible with successful intracytoplasmic sperm injection in the mouse.

View Article: PubMed Central - PubMed

Affiliation: Institute for Biogenesis Research, John A. Burns School of Medicine, University of Hawaii, Honolulu, Hawaii, United States of America.

ABSTRACT
Spermatogenesis is a key developmental process allowing for a formation of a mature male gamete. During its final phase, spermiogenesis, haploid round spermatids undergo cellular differentiation into spermatozoa, which involves extensive restructuring of cell morphology, DNA, and epigenome. Using mouse models with abrogated Y chromosome gene complements and Y-derived transgene we identified Y chromosome encoded Zfy2 as the gene responsible for sperm formation and function. In the presence of a Zfy2 transgene, mice lacking the Y chromosome and transgenic for two other Y-derived genes, Sry driving sex determination and Eif2s3y initiating spermatogenesis, are capable of producing sperm which when injected into the oocytes yield live offspring. Therefore, only three Y chromosome genes, Sry, Eif2s3y and Zfy2, constitute the minimum Y chromosome complement compatible with successful intracytoplasmic sperm injection in the mouse.

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Sperm headshape analysis.(A) The distribution of specific headshape defect categories among testicular sperm from XE,Z2Y*XSry (n = 41 sperm from 3 males), XESxrbY*X (n = 19 sperm from 2 males), and XY*XSxra (44 sperm from 3 males) males. (B) The categories of headshape defects. Normal: represents a normal shape of testicular sperm head. A ("dolphin"): sperm head is elongated and has some curvature reminiscent of crescent shape typical for mouse sperm, small hooked tip can be differentiated. B ("mushroom"): sperm head is elongated but the curvature is not present, hint of a hooked tip can sometimes be observed. C ("cupcake"): sperm head is no longer elongated, the caudal side is wider than in A and B categories, and opens up to a wide dorsal side; hint of a hooked tip can be sometimes be seen. D ("egg"): sperm head has an oval shape with no mark of a hooked tip. The head is less elongated than in category B; E ("ball"): sperm head has a round shape with no hint of a hooked tip, is smaller than in all other categories, and is strongly stained indicative of high DNA condensation; F ("drumstick"): sperm head is elongated, has no traces of a hooked tip, is longer and thinner than in category A&B but shorter than in G. G ("club"): sperm head is clearly elongated with no hint of a hooked tip, and very poorly condensed. Scale = 5 μm.
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pgen.1005476.g003: Sperm headshape analysis.(A) The distribution of specific headshape defect categories among testicular sperm from XE,Z2Y*XSry (n = 41 sperm from 3 males), XESxrbY*X (n = 19 sperm from 2 males), and XY*XSxra (44 sperm from 3 males) males. (B) The categories of headshape defects. Normal: represents a normal shape of testicular sperm head. A ("dolphin"): sperm head is elongated and has some curvature reminiscent of crescent shape typical for mouse sperm, small hooked tip can be differentiated. B ("mushroom"): sperm head is elongated but the curvature is not present, hint of a hooked tip can sometimes be observed. C ("cupcake"): sperm head is no longer elongated, the caudal side is wider than in A and B categories, and opens up to a wide dorsal side; hint of a hooked tip can be sometimes be seen. D ("egg"): sperm head has an oval shape with no mark of a hooked tip. The head is less elongated than in category B; E ("ball"): sperm head has a round shape with no hint of a hooked tip, is smaller than in all other categories, and is strongly stained indicative of high DNA condensation; F ("drumstick"): sperm head is elongated, has no traces of a hooked tip, is longer and thinner than in category A&B but shorter than in G. G ("club"): sperm head is clearly elongated with no hint of a hooked tip, and very poorly condensed. Scale = 5 μm.

Mentions: Sperm from XE,Z2Y*XSry males were also observed in live epididymal and testicular cell suspension, with and on silver stained testicular cell spreads (S4 Fig). The epididymal sperm were extremely rare; only few immotile sperm were noted in 4 out of 5 males. The headshape of both testicular and epididymal sperm was abnormal, as expected from males lacking Y chromosome long arm [19]. To characterize structural sperm defects in more detail we performed the analysis of sperm headshape on silver stained testicular cell spreads (Fig 3). Only sperm with fully developed tails were included in this analysis. In XY males, the great majority of testicular sperm were normal (84%, 31/37), with remaining having slight headshape defects, comparable to those noted earlier in epididymal sperm [19]. In XY*XSxra, XESxrbY*X and XE,Z2Y*XSry males all sperm were morphologically abnormal. We divided the observable headshape defects into 7 categories (A-G) (Fig 3B) and quantified their incidence (Fig 3A). In XE,Z2Y*XSry males sperm heads were either oval or rounded in shape, with no hint of a hooked tip, and frequently highly condensed (categories D and E, 61%), or were elongated with no curvature reminiscent of crescent shape typical for mouse sperm, and occasional hint of a hooked tip (category B, 39%). Sperm in XY*XSxra males, which similarly as XE,Z2Y*XSry lack Y chromosome long arm, had better developed heads than in XE,Z2Y*XSry males, with predominance of sperm with clear head elongation with or without curvature, and with and without a marked hooked tip (category A and B, 66%), suggesting that presence of additional Y genes within Sxra facilitates head restructuring. In XESxrbY*X males the great majority of sperm were scored as elongated but poorly condensed (category G, 74%; this category was specific for this genotype). The tail development in all examined genotypes was normal (see S4 Fig for images of whole testicular sperm from XE,Z2Y*XSry males).


Mouse Y-Encoded Transcription Factor Zfy2 Is Essential for Sperm Formation and Function in Assisted Fertilization.

Yamauchi Y, Riel JM, Ruthig V, Ward MA - PLoS Genet. (2015)

Sperm headshape analysis.(A) The distribution of specific headshape defect categories among testicular sperm from XE,Z2Y*XSry (n = 41 sperm from 3 males), XESxrbY*X (n = 19 sperm from 2 males), and XY*XSxra (44 sperm from 3 males) males. (B) The categories of headshape defects. Normal: represents a normal shape of testicular sperm head. A ("dolphin"): sperm head is elongated and has some curvature reminiscent of crescent shape typical for mouse sperm, small hooked tip can be differentiated. B ("mushroom"): sperm head is elongated but the curvature is not present, hint of a hooked tip can sometimes be observed. C ("cupcake"): sperm head is no longer elongated, the caudal side is wider than in A and B categories, and opens up to a wide dorsal side; hint of a hooked tip can be sometimes be seen. D ("egg"): sperm head has an oval shape with no mark of a hooked tip. The head is less elongated than in category B; E ("ball"): sperm head has a round shape with no hint of a hooked tip, is smaller than in all other categories, and is strongly stained indicative of high DNA condensation; F ("drumstick"): sperm head is elongated, has no traces of a hooked tip, is longer and thinner than in category A&B but shorter than in G. G ("club"): sperm head is clearly elongated with no hint of a hooked tip, and very poorly condensed. Scale = 5 μm.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4697804&req=5

pgen.1005476.g003: Sperm headshape analysis.(A) The distribution of specific headshape defect categories among testicular sperm from XE,Z2Y*XSry (n = 41 sperm from 3 males), XESxrbY*X (n = 19 sperm from 2 males), and XY*XSxra (44 sperm from 3 males) males. (B) The categories of headshape defects. Normal: represents a normal shape of testicular sperm head. A ("dolphin"): sperm head is elongated and has some curvature reminiscent of crescent shape typical for mouse sperm, small hooked tip can be differentiated. B ("mushroom"): sperm head is elongated but the curvature is not present, hint of a hooked tip can sometimes be observed. C ("cupcake"): sperm head is no longer elongated, the caudal side is wider than in A and B categories, and opens up to a wide dorsal side; hint of a hooked tip can be sometimes be seen. D ("egg"): sperm head has an oval shape with no mark of a hooked tip. The head is less elongated than in category B; E ("ball"): sperm head has a round shape with no hint of a hooked tip, is smaller than in all other categories, and is strongly stained indicative of high DNA condensation; F ("drumstick"): sperm head is elongated, has no traces of a hooked tip, is longer and thinner than in category A&B but shorter than in G. G ("club"): sperm head is clearly elongated with no hint of a hooked tip, and very poorly condensed. Scale = 5 μm.
Mentions: Sperm from XE,Z2Y*XSry males were also observed in live epididymal and testicular cell suspension, with and on silver stained testicular cell spreads (S4 Fig). The epididymal sperm were extremely rare; only few immotile sperm were noted in 4 out of 5 males. The headshape of both testicular and epididymal sperm was abnormal, as expected from males lacking Y chromosome long arm [19]. To characterize structural sperm defects in more detail we performed the analysis of sperm headshape on silver stained testicular cell spreads (Fig 3). Only sperm with fully developed tails were included in this analysis. In XY males, the great majority of testicular sperm were normal (84%, 31/37), with remaining having slight headshape defects, comparable to those noted earlier in epididymal sperm [19]. In XY*XSxra, XESxrbY*X and XE,Z2Y*XSry males all sperm were morphologically abnormal. We divided the observable headshape defects into 7 categories (A-G) (Fig 3B) and quantified their incidence (Fig 3A). In XE,Z2Y*XSry males sperm heads were either oval or rounded in shape, with no hint of a hooked tip, and frequently highly condensed (categories D and E, 61%), or were elongated with no curvature reminiscent of crescent shape typical for mouse sperm, and occasional hint of a hooked tip (category B, 39%). Sperm in XY*XSxra males, which similarly as XE,Z2Y*XSry lack Y chromosome long arm, had better developed heads than in XE,Z2Y*XSry males, with predominance of sperm with clear head elongation with or without curvature, and with and without a marked hooked tip (category A and B, 66%), suggesting that presence of additional Y genes within Sxra facilitates head restructuring. In XESxrbY*X males the great majority of sperm were scored as elongated but poorly condensed (category G, 74%; this category was specific for this genotype). The tail development in all examined genotypes was normal (see S4 Fig for images of whole testicular sperm from XE,Z2Y*XSry males).

Bottom Line: Spermatogenesis is a key developmental process allowing for a formation of a mature male gamete.During its final phase, spermiogenesis, haploid round spermatids undergo cellular differentiation into spermatozoa, which involves extensive restructuring of cell morphology, DNA, and epigenome.Therefore, only three Y chromosome genes, Sry, Eif2s3y and Zfy2, constitute the minimum Y chromosome complement compatible with successful intracytoplasmic sperm injection in the mouse.

View Article: PubMed Central - PubMed

Affiliation: Institute for Biogenesis Research, John A. Burns School of Medicine, University of Hawaii, Honolulu, Hawaii, United States of America.

ABSTRACT
Spermatogenesis is a key developmental process allowing for a formation of a mature male gamete. During its final phase, spermiogenesis, haploid round spermatids undergo cellular differentiation into spermatozoa, which involves extensive restructuring of cell morphology, DNA, and epigenome. Using mouse models with abrogated Y chromosome gene complements and Y-derived transgene we identified Y chromosome encoded Zfy2 as the gene responsible for sperm formation and function. In the presence of a Zfy2 transgene, mice lacking the Y chromosome and transgenic for two other Y-derived genes, Sry driving sex determination and Eif2s3y initiating spermatogenesis, are capable of producing sperm which when injected into the oocytes yield live offspring. Therefore, only three Y chromosome genes, Sry, Eif2s3y and Zfy2, constitute the minimum Y chromosome complement compatible with successful intracytoplasmic sperm injection in the mouse.

Show MeSH
Related in: MedlinePlus