Developmental Genetics of Secretory Vesicle Acidification During Caenorhabditis elegans Spermatogenesis

Author:

Gleason Elizabeth J1,Hartley Paul D1,Henderson Melissa1,Hill-Harfe Katherine L12,Price Paul W3,Weimer Robby M4,Kroft Tim L1,Zhu Guang-dan1,Cordovado Suzanne15,L’Hernault Steven W125

Affiliation:

1. Department of Biology, Graduate Programs

2. Genetics and Molecular Biology, and

3. Abeome Corp., Athens, Georgia 30605

4. Department of Biology, University of Utah, Salt Lake City, Utah 84112

5. Biochemistry, Cell and Developmental Biology, Emory University, Atlanta, Georgia 30322

Abstract

Abstract Secretory vesicles are used during spermatogenesis to deliver proteins to the cell surface. In Caenorhabditis elegans, secretory membranous organelles (MO) fuse with the plasma membrane to transform spermatids into fertilization-competent spermatozoa. We show that, like the acrosomal vesicle of mammalian sperm, MOs undergo acidification during development. Treatment of spermatids with the V-ATPase inhibitor bafilomycin blocks both MO acidification and formation of functional spermatozoa. There are several spermatogenesis-defective mutants that cause defects in MO morphogenesis, including spe-5. We determined that spe-5, which is on chromosome I, encodes one of two V-ATPase B paralogous subunits. The spe-5 null mutant is viable but sterile because it forms arrested, multi-nucleate spermatocytes. Immunofluorescence with a SPE-5-specific monoclonal antibody shows that SPE-5 expression begins in spermatocytes and is found in all subsequent stages of spermatogenesis. Most SPE-5 is discarded into the residual body during spermatid budding, but a small amount remains in budded spermatids where it localizes to MOs as a discrete dot. The other V-ATPase B subunit is encoded by vha-12, which is located on the X chromosome. Usually, spe-5 mutants are self-sterile in a wild-type vha-12 background. However, an extrachromosomal transgene containing wild-type vha-12 driven by its own promoter allows spe-5 mutant hermaphrodites to produce progeny, indicating that VHA-12 can at least partially substitute for SPE-5. Others have shown that the X chromosome is transcriptionally silent in the male germline, so expression of the autosomally located spe-5 gene ensures that a V-ATPase B subunit is present during spermatogenesis.

Publisher

Oxford University Press (OUP)

Subject

Genetics

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