Testis-specific expression of a functional retroposon encoding glucose- 6-phosphate dehydrogenase in the mouse

Genomics

Volumn 41, Issue 3, 1997, Pages 350-359

  Hendriksen, Peter J M ^a,b   Hoogerbrugge, Jos W ^a   Baarends, Willy M ^a   De Boer, Peter ^b   Vreeburg, Jan T M ^a   Vos, Elène A ^b   Van Der Lende, Tette ^b   Grootegoed, J Anton ^a  

^a ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE 6 PHOSPHATE DEHYDROGENASE; RECOMBINANT GLUCOSE 6 PHOSPHATE DEHYDROGENASE 1; RECOMBINANT GLUCOSE 6 PHOSPHATE DEHYDROGENASE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; GENE EXPRESSION; INTRON; MALE; MEIOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROPOSON; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; SPERMATOGENESIS; TISSUE SPECIFICITY; X CHROMOSOME INACTIVATION;

EID: 0031149133     PISSN: 08887543     EISSN: None     Source Type: Journal    
DOI: 10.1006/geno.1997.4673     Document Type: Article

References (62)

1. Aitken, J., and Fisher, H. (1994). Reactive oxygen species generation and human spermatozoa: The balance of benefit and risk. BioEssays 16: 259-267.
2. Ashworth, A., Skene, B., Swift, S., and Lovell-Badge, R. (1990). Zfa is an expressed retroposon derived from an alternative transcript of the Zfx gene. EMBO J. 9: 1529-1534.
3. Auffray, C., and Rougeon, F. (1980). Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur. J. Biochem. 107: 303-314.
4. Bautista, J. M., Mason, P. J., and Luzzatto, L. (1992). Purification and properties of human glucose-6-phosphate dehydrogenase made in E. coli. Biochim. Biophys. Acta 1119: 74-80.
5. Bautista, J. M., Mason, P. J., and Luzzato, L. (1995). Human glucose-6-phosphate dehydrogenase lysine 205 is dispensable for substrate binding but essential for catalysis. FEBS Lett. 366: 61-64.
6. Boer, P. H., Adra, C. N., Lau, Y-F., and McBurney, M. W. (1987). The testis-specific phosphoglycerate kinase gene Pgk-2 is a recruited retroposon. Mol. Cell. Biol. 7: 3107-3112.
7. Bonsignore, A., Cancedda, R., Nicolini, A., Damiani, G., and De Flora, A. (1971). Metabolism of human erythrocyte glucose-6-phosphate dehydrogenase. VI. Interconversion of multiple molecular forms. Arch. Biochem. Biophys. 147: 493-501.
8. Brown, R. M., Dahl, H-H. M., and Brown, G. K. (1990). Pyruvate dehydrogenase E1α subunit genes in the mouse: Mapping and comparison with human homologs. Somatic Cell Mol. Genet. 16: 487-492.
9. Capel, B., Swain, A., Nicolis, S., Hacker, A., Walter, M., Koopman, P., Goodfellow, P. N., and Lovell-Badge, R. (1993). Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 73: 1019-1030.
10. Chakrabarti, R., McCracken, J. B., Chakrabarti, D., and Souba, W. W. (1995). Detection of a functional promoter/enhancer in an intron-less human gene encoding a glutamine synthetase-like enzyme. Gene 153: 163-169.
11. Conway, S. J., Mahadevaiah, S. K., Darling, S. M., Capel, B., Rattigan, A. M., and Burgoyne, P. S. (1994). Y353/B: A candidate multiple-copy spermiogenesis gene on the mouse Y chromosome. Mamm. Genome 5: 203-210.
12. Dahl, H-H. M., Brown, R. M., Hutchison, W. M., Maragos, C., and Brown, G. K. (1990). A testis-specific form of the human pyruvate dehydrogenase E1α subunit is coded for by an intronless gene on chromosome 4. Genomics 8: 225-232.
13. De Boer, P., Searle, A. G., van der Hoeven, F. A., de Rooij, D. G., and Beechey, C. V. (1986). Male pachytene pairing in single and double translocation heterozygotes and spermatogenic impairment in the mouse. Chromosoma 93: 326-336.
14. Eddy, E. M. (1995). 'Chauvinist genes' of male germ cells: Gene expression during mouse spermatogenesis. Reprod. Fertil. Dev. 7: 695-704.
15. Erickson, R. P., Zwingman, T., and Ao, A. (1993). Gene expression, X-inactivation, and methylation during spermatogenesis: The case of Zfa, Zfx, and Zfy in mice. Mol. Reprod. Dev. 35: 114-120.
16. Fitch, W. M., and Margoliash, E. (1967). Construction of phylogenetic trees. Science 155: 279-284.
17. Fitzgerald, J., Hutchison, W. M., and Dahl, H-H. M. (1992). Isolation and characterisation of the mouse pyruvate dehydrogenase E1 alpha genes. Biochim. Biophys. Acta 1131: 83-90.
18. Fitzgerald, J., Dahl, H-H. M., and Iannello, R. C. (1994). Differential expression of two testis-specific transcripts of the mouse Pdha-2 gene during spermatogenesis. DNA Cell Biol. 13: 531-537.
19. Fraenkel, D. G. (1968). Selection of Escherichia coli mutants lacking glucose-6-phosphate dehydrogenase or gluconate-6-phosphate dehydrogenase. J. Bacteriol. 95: 1267-1271.
20. Fritz, R. S., Dreher, K. L., Jones, E. A., and Kletzien, R. F. (1989). Analysis of the glucose-6-phosphate dehydrogenase gene, pseudogene and cDNA: Implications for amino-terminal heterogeneity of the enzyme. Unpublished. Database Accession No. M24284.
21. Fulcher, K. D., Welch, J. E., Klapper, D. G., O'Brien, D. A., and Eddy, E. M. (1995). Identification of a unique μ-class glutathione S-transferase in mouse spermatogenic cells. Mol. Reprod. Dev. 42: 415-424.
22. Goto, M., Koji, T., Mizuno, K., Tamaru, M., Koikeda, S., Nakane, P. K., Mori, 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.
23. Grigor, M. R. (1984). Multiple molecular forms of rat mammary glucose-6-phosphate dehydrogenase: Proposed role in turn-over of the enzyme. Arch. Biochem. Biophys. 229: 612-622.
24. Grootegoed, J. A., and Den Boer, P. J. (1989). Energy metabolism of spermatids: A review. In "Cellular and Molecular Events in Spermiogenesis as Targets for Fertility Regulations" (D. W. Hamilton and G. H. M. Waites, Eds.), pp. 193-215, Cambridge Univ. Press, Cambridge, UK.
25. Hedrick, J. L., and Smith, A. J. (1968). Size and charge isomer separation and estimation of molecular weights of proteins by disc gel electrophoresis. Arch. Biochem. Biophys. 126: 155-164.
26. Hendriksen, P. J. M., Hoogerbrugge, J. W., Themmen, A. P. N., Koken, M. H. M., Hoeijmakers, J. H. J., Oostra, B. A., van der Lende, T., and Grootegoed, J. A. (1995). Postmeiotic transcription of X and Y chromosomal genes during spermatogenesis in the mouse. Dev. Biol. 170: 730-733.
27. Ho, Y., Howard, A. J., and Crapo, J. D. (1988). Cloning and sequence of a cDNA encoding rat glucose 6-phosphate dehydrogenase. Nucleic Acids Res. 16: 7746.
28. Hultman, T., Ståhl, S., Homes, E., and Uhlén, M. (1989). Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucleic Acids Res. 17: 4973-4946.
29. Iannello, R. C., and Dahl, H. H. (1992). Transcriptional expression of a testis-specific variant of the mouse pyruvate dehydrogenase E1 alpha subunit. Biol. Reprod. 47: 48-58.
30. Iannello, R. C., Young, J. C., and Kola, I. (1994). Pdha-2: A model for studying transcriptional regulation in early spermatocytes. Mol. Reprod. Dev. 39: 194-199.
31. Jeffery, J., Persson, B., Wood, I., Bergman, T., Jeffery, R., and Jörnvall, H. (1993). Glucose-6-phosphate dehydrogenase: Structure-function relationships and the Pichia jadinii enzyme structure. Eur. J. Biochem. 212: 41-49.
32. Kalab, P., Visconti, P., Leclerc, P., and Kopf, G. S. (1994). p95, the major phosphotyrosine-containing protein in mouse spermatozoa, is a hexokinase with unique properties. J. Biol. Chem. 269: 3810-3817.
33. Koopman, P., Ashworth, A., and Lovell-Badge, R. (1991). The ZFY gene family in humans and mice. Trends Genet. 7: 132-136.
34. Kramer, J. M. (1981). Immunofluorescent localization of PGK-1 and PGK-2 isozymes within specific cells of the mouse testis. Dev. Biol. 87: 30-36.
35. Luzzato, L., and Mehta, A. (1995). Glucose-6-phosphate dehydrogenase deficiency. In "The Metabolic and Molecular Bases of Inherited Disease" (C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle, Eds.), pp. 3367-3398, McGraw-Hill, New York.
36. Martins, R. N., Stokes, G. B., and Masters, C. L. (1985). Regulation of the multiple molecular forms of rat liver glucose-6-phosphate dehydrogenase by insulin and dietary restriction. Biochem. Biophys. Res. Commun. 127: 136-142.
37. Mason, P. J., Vulliamy, T. J., Foulkes, N. S., Town, M., Haidar, B., and Luzzato, L. (1988). The production of normal and variant human glucose-6-phosphate dehydrogenase in COS cells. Eur. J. Biochem. 178: 109-113.
38. Mason, P. J., Stevens, D. J., Luzzato, L., Brenner, S., and Aparicio, S. (1995). Genomic structure and sequence of the Fugu rubripes glucose-6-phosphate dehydrogenase gene (G6PD). Genomics 26: 587-591.
39. McBurney, M. W., Staines, W. A., Boekelheide, K., Parry, D., Jardine, K., and Pickavance, L. (1994). Murine PGK-1 promoter drives widespread but not uniform expression in transgenic mice. Dev. Dyn. 200: 278-293.
40. McCarrey, J. R. (1990). Molecular evolution of the human PGK-2 retroposon. Nucleic Acids Res. 18: 949-955.
41. McCarrey, J. R., and Thomas, K. (1987). Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326: 501-505.
42. McCarrey, J. R., Berg, W. M., Paragioudakis, S. J., Zhang, P. L., Dilworth, D. D., Arnold, B. L., and Rossi, J. J. (1992a). Differential transcription of Pgk genes during spermatogenesis in the mouse. Dev. Biol. 154: 160-168.
43. McCarrey, J. R., Dilworth, D. D., and Sharp, R. M. (1992b). Semi-quantitative analysis of X-linked gene expression during spermatogenesis in the mouse: Ethidium bromide staining of RT-PCR products. Genet. Anal. Tech. Appl. 9: 117-123.
44. 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.
45. Nagamine, C. M., Chan, K., Hake, L. E., and Lau, Y-F. C. (1990). The two candidate testis-determining Y genes (Zfy-1 and Zfy-2) are differentially expressed in fetal and adult mouse tissues. Genes Dev. 4: 63-74.
46. Neifer, S., Jung, A., and Bienzle, U. (1991). Characterization of erythrocytic glucose-6-phosphate dehydrogenase in a mouse strain with reduced G6PD activity. Biomed. Biochim. Acta 50: 233-238.
47. Ninfali, P., and Palma, F. (1990). Comparative study on glucose-6-phosphate dehydrogenase from rabbit tissues. J. Exp. Zool. 254: 6-12.
48. Nouvel, P. (1994). The mammalian genome shaping activity of reverse transcriptase. Genetica 93: 191-201.
49. Ohno, S., Payne, H. W., Morrison, M., and Beutler, E. (1966). Hexose-6-phosphate dehydrogenase found in human liver. Science 153: 1015-1016.
50. Pretch, W., Charles, D. J., and Merkle, S. (1988). X-linked glucose-6-phosphate dehydrogenase deficiency in Mus musculus. Biochem. Genet. 26: 89-103.
51. Rowley, D. L., and Wolf, R. E. (1991). Molecular characterization of the Escherichia coli K-12 zwf gene encoding glucose 6-phosphate dehydrogenase. J. Bacteriol. 172: 968-977.
52. Sachs, L. (1954). Sex-linkage and the sex chromosomes in man. Ann. Eugen. 18: 255-261.
53. Shannon, M., and Handel, M. A. (1993). Expression of the Hprt gene during spermatogenesis: Implications for sex-chromosome inactivation. Biol. Reprod. 49: 770-778.
54. Shaw, C. R. (1966). Glucose-6-phosphate dehydrogenase: Homologous molecules in deer mouse and man. Science 153: 1013-1015.
55. Soares, M. B., Schon, E., Henderson, A., Karathanasis, S. K., Cate, R., Zeitlin, S., Chirgwin, J., and Efstratiadis, A. (1985). RNA-mediated gene duplication: The rat preproinsulin gene is a functional retroposon. Mol. Cell. Biol. 5: 2090-2103.
56. Solari, A. J. (1974). The behavior of the XY pair in mammals. Int. Rev. Cytol. 38: 273-317.
57. Takakubo, F., and Dahl, H-H. M. (1992). The expression pattern of the pyruvate dehydrogenase E1α subunit genes during spermatogenesis in adult mouse. Exp. Cell Res. 199: 39-49.
58. Town, M., Bautista, J. M., Mason, P. J., and Luzzato, L. (1992). Both mutations in G6PD A-are necessary to produce the G6PD deficient phenotype. Hum. Mol. Genet. 1: 171-174.
59. Vanin, E. F. (1985). Processed pseudogenes: Characteristics and evolution. Annu. Rev. Genet. 19: 253-272.
60. Welch, J. E., Schatte, E. C., O'Brien, D. A., and Eddy, E. M. (1992). Expression of a glyceraldehyde 3-phosphate dehydrogenase gene specific to mouse spermatogenic cells. Biol. Reprod. 46: 869-878.
61. Zimmermann, J., Voss, H., Schwager, C., Stegemann, J., Erfle, H., Stucky, K., Kristensen, T., and Ansorge, W. (1990). A simplified protocol for fast plasmid DNA sequencing. Nucleic Acids Res. 18: 1067.
62. Zollo, M., D'Urso, M., Schlessinger, D., and Chen, E. Y. (1993). Sequence of mouse glucose-6-phosphate dehydrogenase cDNA. J. DNA Seq. Map. 3: 319-322.