The formation of the sex vesicle, or XY body, during male meiosis and pairing of the sex chromosomes are thought to be essential for successful spermatogenesis. Despite its cytological discovery a century ago, the mechanism of XY body formation, particularly heterochromatinization of the sex chromosomes, has remained unclear. The HP1 class of chromobox genes are thought to encode proteins involved in the packaging of chromosomal DNA into repressive heterochromatin domains, as seen, for example, in position-effect variegation. Study of the distribution of a murine HP1-like chromodomain protein, M31, during spermatogenesis revealed spreading from the tip of the XY body in mid-stage pachytene spermatocytes to include the whole of the XY body in late-pachytene spermatocytes. We also demonstrate that the formation of the XY body during spermatogenic progression in neonatal mice coincides with the expression of a novel nuclear isoform of M31, M31p21. These results support the view that a common mechanistic basis exists for heterochromatin-induced repression, homeotic gene silencing, and sex-chromosome inactivation during mammalian spermatogenesis.

1.
Armstrong SJ, Húlten MA, Keohane AM, Turner BM: Different strategies of X-inactivation in germinal and somatic cells: histone H4 underacetylation does not mark the inactive X chromosome in the mouse male germline. Expl Cell Res 230:399–402 (1997).
2.
Ayoub N, Richler C, Wahrman J: Xist RNA is associated with the transcriptionally inactive XY body in mammalian male meiosis. Chromosoma 106:1–10 (1997).
3.
Bunick D, Johnson PA, Johnson TR, Hecht NB: Transcription of the testis-specific mouse protamine 2 gene in a homologous in vitro transcription system. Proc natl Acad Sci, USA 87:891–895 (1990).
4.
Burgoyne PS, Mahadevaiah SK, Sutcliffe MJ, Palmer SJ: Fertility in mice requires X-Y pairing and a Y-chromosomal “spermiogenesis” gene mapping to the long arm. Cell 71:391–398 (1992).
5.
Calenda A, Allenet B, Escalier D, Bach J-F, Garchon H-J: The meiosis-specific Xmr gene product is homologous to the lymphocyte Xlr protein and is a component of the XY body. EMBO J 13:100–109 (1994).
6.
Dreesen TD, Henikoff S, Loughney KA: A pairing-sensitive element that mediates trans- inactivation is associated with the Drosophila brown gene. Genes Dev 5:331–340 (1991).
7.
Handel MA, Park C, Kot M: Genetic control of sex-chromosome inactivation during male meiosis. Cytogenet Cell Genet 66:83–88 (1994).
8.
Henikoff S, Dreesen TD: Trans- inactivation of the Drosophila brown gene: evidence for transcriptional repression and somatic pairing dependence. Proc natl Acad Sci, USA 86:6704–6708 (1989).
9.
Horsley D, Hutchings A, Butcher GW, Singh PB: M32, a murine homologue of Drosophila heterochromatin protein 1 (HP1), localises to euchromatin within interphase nuclei and is largely excluded from constitutive heterochromatin. Cytogenet Cell Genet 73:308–311 (1996.).
10.
Jaafar H, Gabriel-Robez O, Rumpler Y: Pattern of ribonucleic acid synthesis in vitro in primary spermatocytes from mouse testis carrying an X-autosome translocation. Chromosoma 98:330–334 (1989).
11.
Kierszenbaum AL, Tres LL: Transcription sites in spread meiotic prophase chromosomes from mouse spermatocytes. J Cell Biol 63:923–935 (1974).
12.
Kofman-Alfaro S, Chandley AC: Meiosis in the male mouse: an autoradiographic investigation. Chromosoma 31:404–420 (1970).
13.
Kralewski M, Novello A, Benavente R: A novel Mr 77,000 protein of the XY body of mammalian spermatocytes: its localisation in normal animals and in Searle’s translocation carriers. Chromosoma 106:160–167 (1997).
14.
Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 (1970).
15.
Latos-Bielenska A, Vogel W: Demonstration of replication patterns in the last premeiotic S-phase of male Chinese hamsters after BrdU pulse labeling. Chromosoma 101:279–283 (1992).
16.
Lee JT, Jaenisch R: The (epi)genetic control of mammalian X-chromosome inactivation. Curr Op Genet Dev 7:274–280 (1997).
17.
Lenhossek M: Untersuchungen über Spermatogenese. Arch Mikrosk Anat Entwicklungsmech 51:215–318 (1898).
18.
Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R: Xist- deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev 11:156–166 (1997).
19.
Matsuda Y, Hirobe T, Chapman VM: Genetic basis of X-Y chromosome dissociation and male sterility in interspecific hybrids. Proc natl Acad Sci, USA 88:4850–4854 (1991).
20.
McCarrey JR, Dilworth DD: Expression of Xist in mouse germ cells correlates with X-chromosome inactivation. Nature Genet 2:200–203 (1992).
21.
McKee BD, Handel MA: Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102:71–80 (1993).
22.
McKee BD, Karpen GH: Drosophila ribosomal RNA genes function as an X-Y pairing site during male meiosis. Cell 61:61–72 (1990).
23.
Monesi V: Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse. Chromosoma 17:11–21 (1965).
24.
Nebel BR, Amarose AP, Hackett EM: Calendar of gametogenic development in the prepuberal male mouse. Science 134:832–833 (1961).
25.
Oakberg EF: A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am J Anat 99:391–413 (1956).
26.
Odartchenko N, Pavillard M: Late DNA replication in male mouse meiotic chromosomes. Science 167:1133–1134 (1970).
27.
Odorisio T, Rodriguez TA, Evans EP, Clarke AR, Burgoyne PS: The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nature Genet 18:257–261 (1998).
28.
Pardue, ML, Gall JG: Chromosomal localisation of mouse satellite DNA. Science 168:1356–1358 (1970).
29.
Paro R, Hogness D: The polycomb protein shares a homologous domain with a heterochromatin associated protein of Drosophila. Proc natl Acad Sci, USA 88:263–267 (1991).
30.
Peterson K, Wang G, Horsley D, Richardson JC, Sapienza C, Latham KE, Singh PB: The M31 gene has a complex developmentally regulated expression profile and may encode alternative protein products that possess diverse subcellular localisation patterns. J exp Zool 280:288–303 (1998).
31.
Singer-Sam J, Robinson MO, Bellvé AR, Simon MI, Riggs AD: Measurement by quantitative PCR of changes in HPRT, PGK-1, APRT, MTase, and Zfy gene transcripts during mouse spermatogenesis. Nucl Acids Res 18:1255–1259 (1990).
32.
Singh PB: Molecular mechanisms of cellular determination: their relation to chromatin structure and parental imprinting. J Cell Sci 107:2653–2668 (1994).
33.
Singh PB, Huskisson NS: Chromatin complexes as aperiodic microcrystalline arrays that regulate genome organisation and expression. Dev Genet 22:85–99 (1998).
34.
Singh PB, James TC: Chromobox genes and the molecular mechanisms of cellular determination, in Ohlsson R, Hall K, Ritzen M (eds): Genomic Imprinting: Causes and Consequences, pp 71–108 (Cambridge University Press, Cambridge 1995).
35.
Singh PB, Miller JR, Pearce JJ, Burton RD, Paro R, James TC, Gaunt SJ: A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants. Nucl Acids Res 19:789–793 (1991).
36.
Smith A, Benavente R: Meiosis-specific protein selectively associated with sex chromosomes of rat pachytene spermatocytes. Proc natl Acad Sci, USA 98:6938–6942 (1992).
37.
Smith A, Benavente R: An Mr 51,000 protein of mammalian spermatogenic cells that is common to the whole XY body and centromeric heterochromatin of autosomes. Chromosoma 103:591–596 (1995).
38.
Solari AJ: The behavior of the XY pair in mammals. Int J Cytol 38:273–317 (1974).
39.
Tartof KD, Hobbs C, Jones M: A structural basis for variegating position effects. Cell 37:869–878 (1984).
40.
Tease C, Cattanach BM: Sex chromosome pairing patterns in male mice of novel Sxr genotypes. Chromosoma 97:390–395 (1989).
41.
Towbin H, Staehelin T, Gordon J: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc natl Acad Sci, USA 76:4350–4354 (1979).
42.
Wettstein D von, Rasmussen SW, Holm PB: The synaptonemal complex in genetic segregation. A Rev Genet 18:331–413 (1984).
43.
Wreggett KA, Hill F, James PS, Hutchings A, Butcher GW, Singh PB: A mammalian homolog of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet Cell Genet 66:99–103 (1994).
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