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Fine Structural Cytochemical Analysis of Homologous Chromosome Recognition, Alignment, and Pairing in Guinea Pig Spermatogonia and Spermatocytes¹

Laboratory of Electron Microscopy,³ Department of Cell Biology, Faculty of Sciences, National Autonomous University of Mexico (UNAM), Mexico D.F., Mexico Center of Electron Microscopy,⁴ University of Lausanne, CH-1005 Lausanne, Switzerland Department of Molecular Genetics and Cell Biology,⁵ University of Chicago, Chicago, Illinois 60637

The nuclei of guinea pig spermatogonia and spermatocytes were studied by means of quantitative autoradiography and electron microscopic methods such as high-resolution cytochemistry, immunocytochemistry, and in situ hybridization. Our observations reveal, in the nucleus of spermatogonia type B, small lampbrush structures of extended chromatin not found in nonmeiotic cells. During meiotic interphase, pairs of parallel lampbrush structures become associated by numerous filaments. The formation of the synaptonemal complex is simultaneous with the extension of chromosomal axes in a continuous leptotene-zygotene stage. Some chromosomes do not recognize their homologs before the onset of the leptotene-zygotene stage and undergo classical leptotene and zygotene stages. The immunocytochemical localization of Dmc1 and Rad51 supports the idea that these proteins are not involved in homology search and final pairing. Immunolocalization of DNA, RNA polymerase II, heterogeneous nuclear ribonucleoproteins, small nuclear ribonucleoproteins, and the trimethyl-guanosin cap of small nuclear RNAs suggests that the chromatin of lampbrush structures transcribe hnRNA and that splicing is scarce. The results of quantitative autoradiography after [³H]uridine labeling show an intense transcription accompanied by a very slow export of RNA. In situ hybridization demonstrates the presence of RNA in the regions of homology recognition and pairing. These results lead us to propose that the RNA synthesized in the lampbrush structures is involved in the process of homology searching and recognition.

¹ Supported by the Swiss National Science Foundation (grant no. 31-53944.98), Volkswagen-Stiftung (grant I/74 348), UNAM, PAPIIT (IN227398 grant), CONACYT 36450-N, and a DGAPA travel grant to G.H.V.N. and O.M.E. Part of this work was carried out during a sabbatical stay of G.H.V.N. and O.M.E. at the University of Lausanne, benefiting from a fellowship of the Fondation du 450e Anniversaire de l'Université de Lausanne. C.S. was the recipient of a fellowship from the Ministero degli Affari Esteri, Roma.

² Correspondence: S. Fakan, Centre of Electron Microscopy, University of Lausanne, Bugnon 27, CH-1005 Lausanne, Switzerland. FAX: 41 21 692 50 55; sfakan{at}cme.unil.ch

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