Abstract
At zygotene/pachytene stage of meiosis in mammalian testis, the X—Y heterobivalent is sequesterd into a heterochromatinized body whose genetic inactivity is shown by lack of uridine incorporation. For the genic level evaluation of the X-inactivation, activities of three X-linked genes were assayed in testicular cell types in the laboratory mouse. While hypoxanthine phosphoribosyl transferase is functional at least up to pachytene stage of primary spermatocytes, glucose-6-phosphate dehydrogenase appears to be active only in the Sertoli cells. No transcript of the muscle specific muscular dystrophin gene was obtained from its regular 5′ promoter. Thus, inactivation of X-linked genes in testis occurs at different stages during spermatogenesis, independently of heterochrornatinizati on of the XY-body. We propose that Xist transcript, the putative regulator of X-inactivation in female soma, is also the regulator in testis. However, due to its extremely low level in testis the transcript may regulate by “spreading” in a gradient and affect the genes in a temporal order. Thus, besides other factors, physical proximity of the genes to Xist may determine the stage of their inactivation.
Similar content being viewed by others
References
Adams A and Harkness A 1976 DevelopmentaI changes in purine phosphoribosyltransferases in human and rat tissues;Biochem. J. 160 565–576
Ailsop.J and Watts RWE 1985 Purine Synthesis and salvage in the testis;Cline. Ski. 69 45–46
Ailsop J and Watts RWE 1986 Purine phosphoribosyl transferase (EC 2.4.2.7 and 2.4.2.8) and purine de novo synthesis activity in rat testicular tissue at different stages of development and their correlation with the circulating levels of gonadotrophins and testosterone and with structural changes;Differentiation 32 144–147
Barr M L and Bertram E G 1949 A morphological distinction between neurons of the male and female, and the behaviour of the nucleolus satellite during acceIerated nucleoprotein synthesis;Nature (London) 163 676–677
Blair H J, Reed V, Laval S H and Boyd Y 1993 The locus for Pyruvate dehydrogenase El subunit (Pdhal) lies between Plop and Amg on the mouse X-chromosome;Mammalian Genome 4 230–233
Borsani G, Tonlorenzi R, Simmler M C, Dandolo L, Arnaud D, Capra V, Grompe M, Pizzuti A, Muzny D, Lawrence C, Willard H F, Avner P and Ballabio A 1991 Characterization of a muiine gene expressed from the inactive X Chromosome;Nature (London) 351 325–329
Brinster R L 1966 Glucose-6-phosphate dehydrogenase activity in the preimplantation mouse embryo;Biochetn. J. 101 161–163
Brock W A 1977 Evidence against gene expression after meiosis in the male mice;J. Exp. Zool. 202 69–80
Brockdorf N, Ashworth A, Kay G F, McCabe V M, Norris D P and Rastan S 1992 The product of the mouse Xist gene is a 15 Kb inactive X-specific transcript containing no conserved ORF and located in the nucleus;Cell 71 515–526
Bnsekdorf N, Ashworth A, Kay G F, Cooper P, Smith S, McCabe V M, Norris D P, Penny G D, Patel D and Rastan S 1991 Conservation of position and exclusive expression of mouse Xist from the inactive X-chromosome;Nature (London) 351 329–331
Brown A. 1, Ballabio A, Rupert J L, Lafreniere R G, Grompe M, TonIorenzi R and Willard H F 1991 A gene from the region of the human X-inactivation centre is expressed exclusiveIy from the inactive X-chromosome;Nature (London) 349 38–44
Brown A. 1, Hendrich B D, Rupert I L, Lafrenierc Y X, Lawrence J and WilIard H F 1992 The human XIST gene: Analysis of a 17 Kb inactive X-specific RNA that contains conserved repeats and is highly Iocalized within the nucleus;Cell 71 527–542
Brown A. J and Willard H F 1994 The human X inactivation centre is not required for maintenance of X-chromosome inactivation;Nature (London) 368 154–156
Brown S W and Chandra S 1973 Inactivation system of the mammalian X-chromosome;Proc. Natl. Acad. Sci. USA 70 195–199
Burgoyne P S 1982 Genetic homoIogy and crossing over in the X and Y chromosomes of mammals;Hum. Genet. 61 S5–90
Chomczynski P and Sacchi N 1957 Single-step method of RNA isoIation by acid guanidium thiocyanate-phenol-chloroform extraction;Anal. Biochem. 162 156–159
Comings D E 1966 Uridine-5-H3 radioautography of the human sex chromatin body;J. Cell Biol. 28 437–441
Cooper D W 1971 Directed genetic change model for X-chromosome inactivation in eutherian mammaIs;Nature (London) 230 292–294
Erickson R P, Zwingman T and Asangla A 0 1993 Gene expression, X-inactivation, and methylalion during spermatogenesis: The case of Zfa, Zfx and Zfy in Mice;Mol. Reprod. Derv. 35 114–120
Erickson R P 1976 Glucose-6-phosphate dehydrogenase activity changes during spermatogenesis: possible relevance to X-chromosome inactivation;Derv. Biol. 53 134–137
Goto M, Koji T, Mizuno K, Tamaru M, Koikeda S, Nakane P K, Morin N, Masamune Y and Nakanishi Y 1990 Transcription switch of two phosphoglycerate kinase genes during spermatogenesis as determined with mouse testis sections in situ;Exp. Cell Res. 186 273–278
Graham A, Papalopulu N and Krumlavf R 1959 The murine andDrosophila homeobox gene complexes have common features of organization and expression;Cell 57 367–378
Grant M, Zuccotti M and Monk M 1992 Methylation of CpG sites of two X-linked genes coincides with X-inactivation in the female mouse embryo but not in the germ line;Nature Genet. 2 161–165
Handel M A, Prak C and Kot M 1994 Genetic control of sex chromosome inactivation during maIe meiosis;Cytogenet. Cell Genet. (in press)
Hoffman E P, Monaco A P and Feener A. C 1957 Conservation of the Duchenne muscular dystrophy gene in mice and humans;Science 238 347–350
Hotta Y and Chandley A C 1982 Activities of X-linked enzymes in spermatocytes of mice rendered sterile by chromosomal alterations;Gamete Res. 6 65–72
Hotta Y, Chandley A C, Stern H, Searle A G and Beechey A. V 1979 A disruption of pachytene DNA metabolism in maIe mice with chromosomally derived sterility;Chromosama 73 287–300
Jablonka E and Lamb M J 1958 Meiotic pairing constrains and the activity of sex chromosomes;J. Theor. Biol. 133 23–36
Jones J T and Andrews S J 1978 Glucose-6-phosphate dehydrogenase activity in somatic and germinal cells of the mouse testis;J. Reprod. Bert. 54 357–362
Kay G F, Pehny G D, PateI D, Ashworth A, Brockdorf N and Rastan S 1993 Expression of Xist during mouse development suggests a role in the initiation of X chromosome inactivation;Cell 72 171–182
Konecki D S, Brennand J, Ftiscoe J C, Caskey A. T and Chinault C 1982 Flypoxanthine phasphoribasyl transfernse genes of mouse and chinese hamster: construction and sequence analysis of cDNA recombinants;Nucleic Acids Res. 10 6763–6775
Kramer J M 1981 Immunofluorescent localization of PGK-2 and PGK-2 isozymes within specific cells of the mouse testis;Derv. Biol. 87 30–36
Kramer J M and Erickson R P 1951 Developmental program of PGK-l and PGK-2 spermatogenic cells of the mouse: specific activities and rates of synthesis;Dev. Biol. 87 37–45
Lederfein D, Levy Z, Augier N, Mopnet T, Mosis G, Fuchs O, Yaffe D and Nudel 1992 A 71-kilodalton protein is a major product of the Duchenne muscular dystrophy gene in brain and other nonmuscle tissues;Proc. Natl. Acad. Sci. USA 89 5346–5350
Lifschytz E and Lindsley D L 1972 The role of X-chromosome inactivation during spermatogenesis;Proc. Natl. Acad. Ski. USA 69 182–186
Luzzato L and Battistuzzi G 1985 Glucose-6-phosphate dehydrogenase; inAdvances in thuman genetics (ads) S Harris and K Hirschhorn (New York, London: Plenum Press) Vol 14, pp 217–329
Lyon M F 1992 Some milestones in the history of X-chromosome inactivation;Annu. Rev. Genet. 26 17–28
Maniatis T, Fritsch E F and Sambrook J 1982Molecular cloning: A laboratory manual (New York: Cold Spring Harbor Laboratory)
Martini G, Toniolo D, Vulliamy G, Paonessa G, Urso M D and Persica M G 1986 Structural analysis of the X-linked gene encoding human glucose-6-phosphate dehydrogenase;EMBO J. 5 1849–1855
McCarrey J R, Berg W M, Paragioudakis S J, Zhang P L, Dilworth D D, ArnoId B L and Ross J J 1992 Differential transcription of Pgk genes during spermatogenesis in the mouse;Dev. Biol. 154 160–168
McCarrey J R and Dilworth D D 1992 Expression of Dist in mouse germ cells correlates with X-chromosome inactivation;Nature Genet. 2 200–203
McKee B D and Handel M A 1993 Sex chromosomes, recombination, and chromatin conformation;Chromosoma 102 71–80
Meistrich M L 1977 Separation of spermatogenic cells and nuclei from rodent testes; inMethods in cell biology (ed.) D M Prescott (New York, San Francisco, London: Academic Press) pp 15–54
Monesi V 1965 Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse;Chromosoma 17 11–21
Nadeau J H Davidson M T, Doolittle D P, Grant P, Hillyard A L, Kosowsky M R and Roderick T H 1992 Comparative map for mice and humans;Mammalian Genome 3 480–536
Ninfali P and Palma F 1990 Comparative study on gIucose-6-phosphate dehydrogenase from rabbit tissues;J. Exp. Zool. 254 6–12
Polani P E 19S2 Pairing of the X and Y chromosomes, noninactivation of X-linked genes, and the maleness factors;Hum. Genet. 60 207–211
Rappold G A 1993 The pseudoautosomal regions of the human sex chromosomes;Hum. Genet. 92 315–324
Raman R and Das P 1991 Mammalian sex chromosomes III. Activity of pseudoautosomal steroid sulfatase enzyme during spermatogenesis in Mus nisculus;Somatic Cell Mal. Genet. 17 429–433
Salida E C, Yen P H, Mohandas T K and Shapiro L J 1992 Expression of the X-inactivation associated gene XIST during spermatogenesis;Nature Genet. 2 196–199
Selander R K, Smith M H, Yang S Y, Johnson W E and Gentry J B 1971 Biochemical polymorphism and systematics in the genusPeromyscus. 1. Variation in the old-field mouse;Stud. Genet. 6 50–90
Shannon M and Handel M A 1993 Expression of the Bpi/ gene during spermatogenesis: implications for sex-chromosome inactivation;Biol. Reprod. 49 770–778
Shen R S and Lee I P 1976 Developmental patterns of enzymes in mouse testis;J. Reprod. Fert. 48 301–305
Singer-Sam J, Robinson M D, Beilve A R, Simon M 1 and Riggs A D 1990 Measurement by quantitative PCR of changes in HPRT, PGK-1, PGK-2, APRT, MTase, and Zfy gene transcripts during mouse spermatogenesis;Nucleic Acids Res. 18 1255–1259
Solari A J 1974 The behaviour of the XY pair in mammals;Int. Rev. Cytol. 38 273–317
Takakubo F and Dahl H-HM 1992 The expression pattern of the Ayruvate Dehydrogenase El subunit genes during spermatogenesis in adult mouse;Exp. Cell Res. 199 39–49
Tanaka S and Fujimoto H 19S6 A postmeiotically expressed clone encodes lactate dehydrogenase isozyme X;Biochem, Biophys. Res. Commun. 136 760–766
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Das, P., Raman, R. Inactivation of mammalian X-chromosome during spermatogenesis: Temporal expression of genes in the laboratory mouse. J Biosci 19, 513–528 (1994). https://doi.org/10.1007/BF02703199
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02703199