{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,1]],"date-time":"2025-11-01T09:06:31Z","timestamp":1761987991592},"reference-count":47,"publisher":"The Company of Biologists","issue":"12","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2004,6,15]]},"abstract":"<jats:p>The switch from spermatogenesis to oogenesis in the Caenorhabditis elegans hermaphrodite requires mog-6, which post-transcriptionally represses the fem-3 RNA. In this study, we show that mog-6 codes for a divergent nuclear cyclophilin, in that a conserved domain is not required for its function in the sperm-oocyte switch. MOG-6 binds to the nuclear zinc finger protein MEP-1 through two separate domains that are essential for the role of MOG-6 in the sperm-oocyte switch. We propose that MOG-6 has a function distinct from that of prevailing cyclophilins and that its binding to MEP-1 is essential for germline sex determination. Finally, we found that gld-3 mog-6 mutants develop germline tumors, suggesting that mog-6 might function in the decision between mitosis and meiosis.<\/jats:p>","DOI":"10.1242\/dev.01154","type":"journal-article","created":{"date-parts":[[2004,5,25]],"date-time":"2004-05-25T00:23:43Z","timestamp":1085444623000},"page":"2935-2945","source":"Crossref","is-referenced-by-count":36,"title":["Roles of the<i>C. elegans<\/i>cyclophilin-like protein MOG-6 in MEP-1 binding and germline fates"],"prefix":"10.1242","volume":"131","author":[{"given":"Marco","family":"Belfiore","sequence":"first","affiliation":[{"name":"Department of Biology, Unit of Zoology, University of Fribourg, 1700 Fribourg, Switzerland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paolo","family":"Pugnale","sequence":"additional","affiliation":[{"name":"Department of Biology, Unit of Zoology, University of Fribourg, 1700 Fribourg, Switzerland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zarifja","family":"Saudan","sequence":"additional","affiliation":[{"name":"Department of Biology, Unit of Zoology, University of Fribourg, 1700 Fribourg, Switzerland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alessandro","family":"Puoti","sequence":"additional","affiliation":[{"name":"Department of Biology, Unit of Zoology, University of Fribourg, 1700 Fribourg, Switzerland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","reference":[{"key":"2021042604393072000_REF1","doi-asserted-by":"crossref","unstructured":"Aamodt, E. J., Chung, M. A. and McGhee, J. D.(1991). Spatial control of gut-specific gene expression during Caenorhabditis elegans development. Science252,579-582.","DOI":"10.1126\/science.2020855"},{"key":"2021042604393072000_REF2","doi-asserted-by":"crossref","unstructured":"Ahringer, J. and Kimble, J. (1991). Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3 3\u2032untranslated region. Nature349,346-348.","DOI":"10.1038\/349346a0"},{"key":"2021042604393072000_REF3","doi-asserted-by":"crossref","unstructured":"Ahringer, J., Rosenquist, T. A., Lawson, D. N. and Kimble,J. (1992). The Caenorhabditis elegans sex determining gene fem-3 is regulated post-transcriptionally. EMBO J.11,2303-2310.","DOI":"10.1002\/j.1460-2075.1992.tb05289.x"},{"key":"2021042604393072000_REF4","unstructured":"Bai, C. and Elledge, S. J. (1997). Searching for interacting proteins with the two-hybrid system I. In The Yeast Two-Hybrid System (ed. P. L. Bartel and S. Fields), pp.11-28. Oxford, UK: Oxford University Press."},{"key":"2021042604393072000_REF5","doi-asserted-by":"crossref","unstructured":"Baker, E. K., Colley, N. J. and Zucker, C. S.(1994). The cyclophilin homolog NinaA functions as a chaperone,forming a stable complex in vivo with its protein target rhodopsin. EMBO J.13,4886-4895.","DOI":"10.1002\/j.1460-2075.1994.tb06816.x"},{"key":"2021042604393072000_REF6","doi-asserted-by":"crossref","unstructured":"Bartel, P. L. and Fields, S. (1995). Analyzing protein-protein interactions using two-hybrid system. Methods Enzymol.254,241-263.","DOI":"10.1016\/0076-6879(95)54018-0"},{"key":"2021042604393072000_REF7","doi-asserted-by":"crossref","unstructured":"Barton, M. K., Schedl, T. B. and Kimble, J.(1987). Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans.Genetics115,107-119.","DOI":"10.1093\/genetics\/115.1.107"},{"key":"2021042604393072000_REF8","unstructured":"Belfiore, M., Mathies, L. D., Pugnale, P., Moulder, G.,Barstead, R., Kimble, J. and Puoti, A. (2002). The MEP-1 Zn-finger protein acts with MOG DEAH-box proteins to control gene expression via the fem-3 3\u2032UTR in C. elegans.RNA8, 725-739."},{"key":"2021042604393072000_REF9","unstructured":"Bettinger, J. C., Lee, K. and Rougvie, A. E.(1996). Stage-specific accumulation of the terminal differentiation factor LIN-29 during Caenorhabditis elegansdevelopment. Development122,2517-2527."},{"key":"2021042604393072000_REF10","doi-asserted-by":"crossref","unstructured":"Bourquin, J.-P., Stagljar, I., Meyer, P., Moosbaum, P., Silke,J., Baechi, T., Georgiev, O. and Schaffner, W. (1997). A Serine\/arginine-rich nuclear matrix cyclophilin interacts with the C-terminal domain of RNA polymerase II. Nucleic Acids Res.25,2055-2061.","DOI":"10.1093\/nar\/25.11.2055"},{"key":"2021042604393072000_REF11","doi-asserted-by":"crossref","unstructured":"Crittenden, S. L., Bernstein, D. S., Bachorik, J. L., Thompson,B. E., Gallegos, M., Petcherski, A. G., Moulder, G., Barstead, R., Wickens, M. and Kimble, J. (2002). A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans.Nature417,660-663.","DOI":"10.1038\/nature754"},{"key":"2021042604393072000_REF12","doi-asserted-by":"crossref","unstructured":"Eckmann, C. R., Kraemer, B., Wickens, M. and Kimble, J.(2002). GLD-3, a Bicaudal-C Homolog that Inhibits FBF to Control Germline Sex Determination in C. elegans.Dev. Cell3, 697-710.","DOI":"10.1016\/S1534-5807(02)00322-2"},{"key":"2021042604393072000_REF13","doi-asserted-by":"crossref","unstructured":"Fields, S. and Song, O. (1989). A novel genetic system to detect protein-protein interactions. Nature340,245-246.","DOI":"10.1038\/340245a0"},{"key":"2021042604393072000_REF14","doi-asserted-by":"crossref","unstructured":"Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T. and Schmid, F. X. (1989). 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Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development131,93-104."},{"key":"2021042604393072000_REF21","unstructured":"Horowitz, D. S., Kobayashi, R. and Krainer, A. R.(1997). A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4\/U6 snRNPs. RNA3,1374-1387."},{"key":"2021042604393072000_REF22","doi-asserted-by":"crossref","unstructured":"Jones, A. R., Francis, R. and Schedl, T.(1996). GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol.180,165-183.","DOI":"10.1006\/dbio.1996.0293"},{"key":"2021042604393072000_REF23","doi-asserted-by":"crossref","unstructured":"Kallen, J., Spitzfaden, C., Zurini, M. G., Wider, G., Widmer,H., Wuthrich, K. and Walkinshaw, M. (1991). 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(1999). nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans.Development126,4861-4871.","DOI":"10.1242\/dev.126.21.4861"},{"key":"2021042604393072000_REF40","unstructured":"Subramaniam, K. and Seydoux, G. (2003). Dedifferentiation of primary spermatocytes into germ cell tumors in C. elegans lacking the pumilio-like protein PUF-8. Curr. Biol.13,134-139."},{"key":"2021042604393072000_REF41","unstructured":"Teigelkamp, S., Achsel, T., Mundt, C., Go\u0308thel, S.-F.,Cronshagen, U., Lane, W. S., Mahariel, M. and Lu\u0308hrmann, R.(1998). The 20kD protein of human [U4\/U6.U5] tri-snRNPs is a novel cyclophilin that forms a ternary complex with the U4\/U6-specific 60kD and 90kD proteins. RNA4, 127-141."},{"key":"2021042604393072000_REF42","doi-asserted-by":"crossref","unstructured":"Timmons, L. and Fire, A. (1998). Specific interference by ingested dsRNA. 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