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Prophase of meiosis in human spermatocytes analysed by EM microspreading in infertile men and their controls and comparisons with human oocytes

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Summary

Observations at the electron microscope (EM) level have been made on 1883 primary spermatocytes from 40 chromosomally normal subfertile men and 566 spermatocytes from 10 fertile controls, using the technique of microspreading. Spermatocytes of infertile men in general showed greater indications of degeneration including higher levels of background silver deposition, nucleolar organising region — XY associations, fragmentation of synaptonemal complexes and overproduction of XY excrescences. A few oligospermic men also showed an immature morphology of the XY pair and/or a reduced extent of XY synapsis. Dissociation of the sex chromosome axes at prophase was found to occur with a much lower frequency than that recorded for separated X and Y chromosomes at metaphase I. In a single spermatocyte, synaptonemal complex formation was observed between Xqter and Yqter, a situation that could enable rare XqYq interchange. A proteinaceous stalked body exists on the Y axis towards its non-pairing end; this structure might have a functional relationship with the gene for spermatogenesis, (AZF), located at the euchromatin/heterochromatin interface. Compared with human oocytes, spermatocytes show fewer anomalies of synapsis, i.e. asynapsed segments or whole axes, non-homologous associations, interchanges, interlocks. These latter data agree well with findings from the mouse.

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References

  • Beechey CV (1973) X-Y chromosome dissociation and sterility in the mouse. Cytogenet Cell Genet 12:60–67

    Google Scholar 

  • Bobrow M, Pearson PL, Collacott HEAC (1971) Para-nucleolar position of the human Y chromosome in interphase nuclei. Nature 232:556–557

    Google Scholar 

  • Boer P de, Branje HEB (1979) Association of the extra chromosome of tertiary trisomic male mice with the sex chromosomes during first meiotic prophase, and its significance for impairment of spermatogenesis. Chromosoma 73:369–379

    Google Scholar 

  • Bonaccorsi S, Pisano C, Puoti F, Gatti M (1988) Y chromosome loops in Drosophila melanogaster. Genetics 120:1015–1034

    CAS  PubMed  Google Scholar 

  • Bond DJ, Chandley AC (1983) Aneuploidy. (Oxford monographs on medical genetics, no 11) Oxford University Press, Oxford New York Toronto

    Google Scholar 

  • Brandriff B, Gordon L, Ashworth L, Watchmaker G, Moore D II, Wyrobek AJ, Carrano AV (1985) Chromosomes of human sperm: variability among normal individuals. Hum Genet 70:18–24

    Google Scholar 

  • Burgoyne BS, Baker T (1984) Meiotic pairing and gametogenic failure. In: Evans CW, Dickinson HG (eds) Controlling events in meiosis. Company of Biologists, Cambridge, pp 349–362

    Google Scholar 

  • Cameron IT, Buckton KE, Baird DT (1984) X-Y translocation. A case report. Hum Genet 67:457–459

    Google Scholar 

  • Chandley AC (1981) The origin of chromosomal aberrations in man and their potential for survival and reproduction in the adult human population. Ann Génét (Paris) 24:5–11

    Google Scholar 

  • Chandley AC (1982) A pachytene analysis of two male-fertile paracentric inversions in chromosome I of the mouse and in the male-sterile double heterozygote. Chromosoma 85:127–135

    Google Scholar 

  • Chandley AC (1987) Meiotic analysis in germ cells of man and the mouse. In: Monk M (ed) Mammalian development. A practical approach. IRL Press, Oxford Washington, DC, pp 71–91

    Google Scholar 

  • Chandley AC, Edmond PE (1971) Meiotic studies on a subfertile patient with a ring Y chromosome. Cytogenetics 10:295–304

    Google Scholar 

  • Chandley AC, Edmond P, Maclean N, Fletcher J, Watson GS (1976) Cytogenetics and infertility in man: results of a five-year survey of men attending a subfertility clinic. II. Testicular histology and meiosis. Ann Hum Genet 40:165–176

    Google Scholar 

  • Chandley AC, Goetz P, Hargreave TB, Joseph AM, Speed RM (1984) On the nature and extent of XY pairing at meiotic prophase in man. Cytogenet Cell Genet 38:241–247

    Google Scholar 

  • Chandley AC, Speed RM, McBeath S, Hargreave TB (1986) A human 9;20 reciprocal translocation associated with male infertility analyzed at prophase and metaphase I of meiosis. Cytogenet Cell Genet 41:145–153

    Google Scholar 

  • Chandley AC, McBeath S, Speed RM, Yorston L, Hargreave TB (1987a) Pericentric inversion in human chromosome I and the risk for male sterility. J Med Genet 24:325–334

    Google Scholar 

  • Chandley AC, Hargreave TB, McBeath S, Mitchell AR, Speed RM (1987b) Ring XY bivalent: a new phenomenon at metaphase I of meiosis in man. J Med Genet 24:101–106

    Google Scholar 

  • Coerdt W, Rehder H, Gausmann I, Johannisson R, Gropp A (1985) Quantitative histology of human fetal testes in chromosomal disease. Pediatr Pathol 3:245–259

    Google Scholar 

  • Gabriel-Robez O, Ratomponirina C, Dutrillaux B, Carre-Pigeon F, Rumpler Y (1986) Meiotic association between the XY chromosomes and the autosomal quadrivalent of a reciprocal translocation in two infertile men, 46,XY,t(19;22) and 46,XY,t(17;21). Cytogenet Cell Genet 43:154–160

    Google Scholar 

  • Gabriel-Robez O, Rumpler Y, Ratomponirina C, Petit C, Levilliers J, Croquette MF, Coturier J (1990) Deletion of the pseudo autosomal region and lack of sex chromosome pairing at pachytene in two infertile men, carriers of an X;Y translocation. Cytogenet Cell Genet (in press)

  • Forejt N (1974) Nonrandom association between a specific autosome and the X chromosome in meiosis of the male mouse: possible consequence of homologous centromere separation. Cytogenet Cell Genet 13:369–383

    Google Scholar 

  • Forejt J, Gregorová S (1977) Meiotic studies of translocations causing male sterility in the mouse. I. Autosomal reciprocal translocations. Cytogenet Cell Genet 19:159–179

    Google Scholar 

  • Jacobs PA, Hassold TJ, Whittington E, Butler G, Collyer S, Keston M, Lee M (1988) Klinefelter's syndrome: an analysis of the origin of the additional sex chromosome using molecular probes. Ann Hum Genet 52:93–109

    Google Scholar 

  • Johannisson R, Lohrs U, Wolff HH, Schwinger E (1987) Two different XY-quadrivalent associations and impairment of fertility in men. Cytogenet Cell Genet 45:222–230

    Google Scholar 

  • Johannisson R, Froster-Iskenius U, Saadallah N, Hulten MA (1988) Spermatogenesis in two patients with the fragile X syndrome. II. First meiosis: light and electron microscopy. Hum Genet 79:231–234

    Google Scholar 

  • Lifschytz E, Lindsley DL (1972) The role of X-chromosome inactivation during spermatogenesis. Proc Nat Acad Sci USA 69:182–186

    Google Scholar 

  • Luciani JM, Guichaoua MR, Mattei A, Morazzani MR (1984) Pachytene analysis of a man with a 13q∶14q translocation and infertility. Behaviour of the trivalent and non random association with the sex vesicle. Cytogenet Cell Genet 38:14–22

    Google Scholar 

  • Martin RH (1988) Human sperm karyotyping: a tool for the study of aneuploidy. In: Vig BK, Sandberg AA (eds) Aneuploidy, part B: Induction and test systems. Liss, New York, pp 297–316

    Google Scholar 

  • Miklos GLG (1974) Sex chromosome pairing and male fertility. Cytogenet Cell Genet 13:558–577

    Google Scholar 

  • Moses MJ, Counce SJ, Paulson DF (1975) Synaptonemal complex complement of man in spreads of spermatocytes, with details of the sex chromosome pair. Science 187:363–365

    Google Scholar 

  • Moyzis RK, Buckingham JM, Scott Cram L, Dani M, Deaven LL, Jones MD, Meyne J, Ratliff RL, Wu J-R (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA 85:6622–6626

    CAS  PubMed  Google Scholar 

  • Quack B, Speed RM, Luciani JM, Noel B, Guichaoua M, Chandley AC (1988) Meiotic analysis of two human reciprocal X-autosome translocations. Cytogenet Gell Genet 48:43–47

    Google Scholar 

  • Rasmussen SW, Holm PB (1978) Human meiosis. II. Chromosome pairing and recombination nodules in human spermatocytes. Carlsberg Res Commun 43:275–327

    Google Scholar 

  • Rosenmann A, Wahrman J, Richler C, Voss R, Persitz A, Goldman B (1985) Meiotic association between the XY chromosomes and unpaired autosomal elements as a cause of human male sterility. Cytogenet Cell Genet 39:19–29

    Google Scholar 

  • Rosenmann A, Wahrman J, Richler C, Madgar I, Weissenberg R, Chaki R (1987) Under what circumstances is the human XY bivalent tangled? A note on chromosomally-derived sterility. Cytogenet Cell Genet 45:58–61

    Google Scholar 

  • Setterfield LA, Mahadevaiah S, Mittwoch U (1988) Pachytene pairing in relation to sperm and oocyte numbers in a malefertile reciprocal translocation in the mouse. Cytogenet Cell Genet 49:293–299

    Google Scholar 

  • Solari AJ (1980) Synaptonemal complexes and associated structures in microspread human spermatocytes. Chromosoma 81:315–337

    Google Scholar 

  • Sotomayor RE, Gumming RB (1977) XY dissociation in mice: a model that may account for sex aneuploidy in humans (abstract)? Genetics 86:60–61

    Google Scholar 

  • Speed RM (1985) The prophase stages in human foetal oocytes studied by light and electron microscope. Hum Genet 69:69–75

    Google Scholar 

  • Speed RM (1986a) Oocyte development in XO foetuses of man and mouse: the possible role of heterologous X-chromosome pairing in germ cell survival. Chromosoma 94:115–124

    Google Scholar 

  • Speed RM (1986b) Prophase pairing in a mosaic 18p-;iso18q human female foetus studied by surface spreading. Hum Genet 72:256–259

    Google Scholar 

  • Speed RM (1988) The possible role of meiotic pairing anomalies in the atresia of human fetal oocytes. Hum Genet 78:260–266

    Google Scholar 

  • Stahl A, Hartung M, Devictor M, Berge-Lefranc JL (1984) The association of the nucleolus and the short arm of acrocentric chromosomes with the XY pair in human spermatocytes: its possible role in facilitating sex-chromosome acrocentric translocation. Hum Genet 68:173–180

    Google Scholar 

  • Tiepolo L, Zuffardi O (1976) Localization of factors controlling spermatogenesis in the nonfluorescent portion of the human Y chromosome long arm. Hum Genet 34:119–124

    Google Scholar 

  • Vogt P, Hennig W (1986) Molecular structure of the lampbrush loop nooses of the Y chromosome of Drosophila hydei. I. The Y chromosome-specific repetitive DNA sequence family ay I is dispersed in the loop DNA. Chromosoma 94:449–458

    Google Scholar 

  • Weir BJ, Rowlands IW (1977) Ovulation and atresia. In: Zuckerman S, Weir BJ (eds) The ovary, vol 1, 2nd edn. Academic Press, New York London, pp 265–301

    Google Scholar 

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Speed, R.M., Chandley, A.C. Prophase of meiosis in human spermatocytes analysed by EM microspreading in infertile men and their controls and comparisons with human oocytes. Hum Genet 84, 547–554 (1990). https://doi.org/10.1007/BF00210808

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