Abstract
We have analyzed a locus of Drosophila melanogaster located at 98C on chromosome 3, which contains two tandemly arranged genes, named Mst98Ca and Mst98Cb. They are two additional members of the Mst(3)CGP gene family by three criteria. (i) Both genes are exclusively transcribed in the male germ line. (ii) Both transcripts encode a protein with a high proportion of the repetitive motif Cys-Gly-Pro. (iii) Their expression is translationally controlled; while transcripts can be detected in diploid stages of spermatogenesis, association with polysomes can be shown only in haploid stages of sperm development. The genes differ markedly from the other members of the gene family in structure; they do not contain introns, they are of much larger size, and they have the Cys-Gly-Pro motifs clustered at the carboxy-terminal end of the encoded proteins. An antibody generated against the Mst98Ca protein recognizes both Mst98C proteins in D. melanogaster. In a male-sterile mutation in which spermiogenesis is blocked before individualization of sperm, both of these proteins are no longer synthesized. This finding provides proof of late translation for the Mst98C proteins and thereby independent proof of translational control of expression. Northern (RNA) and Western immunoblot analyses indicate the presence of homologous gene families in many other Drosophila species. The Mst98C proteins share sequence homology with proteins of the outer dense fibers in mammalian spermatozoa and can be localized to the sperm tail by immunofluorescence with an anti-Mst98Ca antibody.
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- Baltz J. M., Williams P. O., Cone R. A. Dense fibers protect mammalian sperm against damage. Biol Reprod. 1990 Sep;43(3):485–491. doi: 10.1095/biolreprod43.3.485. [DOI] [PubMed] [Google Scholar]
- Beverley S. M., Wilson A. C. Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J Mol Evol. 1984;21(1):1–13. doi: 10.1007/BF02100622. [DOI] [PubMed] [Google Scholar]
- Braun R. E., Peschon J. J., Behringer R. R., Brinster R. L., Palmiter R. D. Protamine 3'-untranslated sequences regulate temporal translational control and subcellular localization of growth hormone in spermatids of transgenic mice. Genes Dev. 1989 Jun;3(6):793–802. doi: 10.1101/gad.3.6.793. [DOI] [PubMed] [Google Scholar]
- Burfeind P., Hoyer-Fender S. Sequence and developmental expression of a mRNA encoding a putative protein of rat sperm outer dense fibers. Dev Biol. 1991 Nov;148(1):195–204. doi: 10.1016/0012-1606(91)90329-2. [DOI] [PubMed] [Google Scholar]
- Clermont Y., Oko R., Hermo L. Immunocytochemical localization of proteins utilized in the formation of outer dense fibers and fibrous sheath in rat spermatids: an electron microscope study. Anat Rec. 1990 Aug;227(4):447–457. doi: 10.1002/ar.1092270408. [DOI] [PubMed] [Google Scholar]
- DiBenedetto A. J., Lakich D. M., Kruger W. D., Belote J. M., Baker B. S., Wolfner M. F. Sequences expressed sex-specifically in Drosophila melanogaster adults. Dev Biol. 1987 Jan;119(1):242–251. doi: 10.1016/0012-1606(87)90225-9. [DOI] [PubMed] [Google Scholar]
- Erickson R. P. Post-meiotic gene expression. Trends Genet. 1990 Aug;6(8):264–269. doi: 10.1016/0168-9525(90)90209-o. [DOI] [PubMed] [Google Scholar]
- Fawcett D. W. The mammalian spermatozoon. Dev Biol. 1975 Jun;44(2):394–436. doi: 10.1016/0012-1606(75)90411-x. [DOI] [PubMed] [Google Scholar]
- Haidl G., Becker A., Henkel R. Poor development of outer dense fibers as a major cause of tail abnormalities in the spermatozoa of asthenoteratozoospermic men. Hum Reprod. 1991 Nov;6(10):1431–1438. doi: 10.1093/oxfordjournals.humrep.a137283. [DOI] [PubMed] [Google Scholar]
- Kaltschmidt B., Glätzer K. H., Michiels F., Leiss D., Renkawitz-Pohl R. During Drosophila spermatogenesis beta 1, beta 2 and beta 3 tubulin isotypes are cell-type specifically expressed but have the potential to coassemble into the axoneme of transgenic flies. Eur J Cell Biol. 1991 Feb;54(1):110–120. [PubMed] [Google Scholar]
- Kloetzel P. M., Falkenburg P. E., Hössl P., Glätzer K. H. The 19S ring-type particles of Drosophila. Cytological and biochemical analysis of their intracellular association and distribution. Exp Cell Res. 1987 May;170(1):204–213. doi: 10.1016/0014-4827(87)90130-3. [DOI] [PubMed] [Google Scholar]
- Kuhn R., Kuhn C., Börsch D., Glätzer K. H., Schäfer U., Schäfer M. A cluster of four genes selectively expressed in the male germ line of Drosophila melanogaster. Mech Dev. 1991 Sep;35(2):143–151. doi: 10.1016/0925-4773(91)90064-d. [DOI] [PubMed] [Google Scholar]
- Kuhn R., Schäfer U., Schäfer M. Cis-acting regions sufficient for spermatocyte-specific transcriptional and spermatid-specific translational control of the Drosophila melanogaster gene mst(3)gl-9. EMBO J. 1988 Feb;7(2):447–454. doi: 10.1002/j.1460-2075.1988.tb02832.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kwon Y. K., Hecht N. B. Cytoplasmic protein binding to highly conserved sequences in the 3' untranslated region of mouse protamine 2 mRNA, a translationally regulated transcript of male germ cells. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3584–3588. doi: 10.1073/pnas.88.9.3584. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Michiels F., Falkenburg D., Müller A. M., Hinz U., Otto U., Bellmann R., Glätzer K. H., Brand R., Bialojan S., Renkawitz-Pohl R. Testis-specific beta 2 tubulins are identical in Drosophila melanogaster and D. hydei but differ from the ubiquitous beta 1 tubulin. Chromosoma. 1987;95(6):387–395. doi: 10.1007/BF00333989. [DOI] [PubMed] [Google Scholar]
- Michiels F., Gasch A., Kaltschmidt B., Renkawitz-Pohl R. A 14 bp promoter element directs the testis specificity of the Drosophila beta 2 tubulin gene. EMBO J. 1989 May;8(5):1559–1565. doi: 10.1002/j.1460-2075.1989.tb03540.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Myers E. W., Miller W. Optimal alignments in linear space. Comput Appl Biosci. 1988 Mar;4(1):11–17. doi: 10.1093/bioinformatics/4.1.11. [DOI] [PubMed] [Google Scholar]
- Oko R. J., Clermont Y. Biogenesis of specialized cytoskeletal elements of rat spermatozoa. Ann N Y Acad Sci. 1991;637:203–223. doi: 10.1111/j.1749-6632.1991.tb27311.x. [DOI] [PubMed] [Google Scholar]
- Oko R. Comparative analysis of proteins from the fibrous sheath and outer dense fibers of rat spermatozoa. Biol Reprod. 1988 Aug;39(1):169–182. doi: 10.1095/biolreprod39.1.169. [DOI] [PubMed] [Google Scholar]
- Olivieri G., Olivieri A. Autoradiographic study of nucleic acid synthesis during spermatogenesis in Drosophila melanogaster. Mutat Res. 1965 Aug;2(4):366–380. doi: 10.1016/0027-5107(65)90072-2. [DOI] [PubMed] [Google Scholar]
- Schäfer M., Kuhn R., Bosse F., Schäfer U. A conserved element in the leader mediates post-meiotic translation as well as cytoplasmic polyadenylation of a Drosophila spermatocyte mRNA. EMBO J. 1990 Dec;9(13):4519–4525. doi: 10.1002/j.1460-2075.1990.tb07903.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vera J. C., Brito M., Zuvic T., Burzio L. O. Polypeptide composition of rat sperm outer dense fibers. A simple procedure to isolate the fibrillar complex. J Biol Chem. 1984 May 10;259(9):5970–5977. [PubMed] [Google Scholar]







