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A novel C. elegans gene interfaces cell cycle and development in spermatogenesis

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Author: Presler, Marc S.
Advisor: Shakes, Diane C.
Committee Members: Allison, Lizabeth; Kerscher, Oliver; Potkay, Monica Brzezinski
Issued Date: 2010-05-17
Subjects: C. elegans
Cell cycle
Worm sperm
Residual body
Novel protein
Sister gene
URI: http://hdl.handle.net/10288/2037
Description: The last thing one discovers in composing a work is what to put first. -TS Eliot Abstract The spermatogenesis pathway in the model organism Caenorhabditis elegans offers an excellent opportunity to study the interplay between the meiotic cell cycle and the developmental program of cellular differentiation. While these two parallel processes cooperate to produce highly specialized gametes, the intricate mechanisms enabling that coordination are not yet fully understood. To further investigate how the cell cycle can integrate with the cellular differentiation program in C. elegans, we characterized the sterile, spermatogenesis-defective mutant spe7, whose primary spermatocytes arrest at Anaphase I while failing to either divide into secondary spermatocytes or bud to form individual spermatids. Here we show that the spindles regress to an interphase/G2-like pattern following the Anaphase I arrest by reorganizing into a network pattern. PLK-1 (polo-like kinase), a protein required for the G2/M-phase transition, ceases to localize the centrosomes after the arrest point, but properly localizes to the Metaphase I plate and jumps off the chromosomes at Anaphase 1. Despite the interphase/G2-like tubulin and PLK-1 configuration in the arrested primary spermatocytes, cyclin B levels remain elevated and the nuclear envelope stays vesiculated. Although the events of pre-division chromatin modifications progress normally, aberrant chromosome configurations are seen following Metaphase I. The molecular identity of spe7 is F32A11.3, which is listed as a spermatogenesis-enriched protein in whole genome microarray studies. In homology searches, F32A11.3 is most similar to a second C. elegans gene and to single genes in other Caenorhabditis species; it also exhibits weak homology to the vertebrate sperm protein, zonadhesion. SPE-7 antibody staining shows a dynamic localization pattern, with the active form likely functioning at Metaphase I. These findings suggest potential necessity of an intact spindle for the budding division, implying cell cycle components are required not just for chromosome segregation, but for early spermiogenesis as well. Furthermore, the mutant phenotype and dynamics patterns of SPE-7 reflect not only the modular and dynamic nature of the spermatogenesis, but SPE-7's likely role as a key linker between the cell cycle and developmental pathways as well. The possible gene duplication event points to an evolutionary pressure for innovation in the germline.
Degree: Bachelors of Science in Biology

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