Translation of a testis-specific Cu/Zn superoxide dismutase (SOD-1) mRNA is regulated by a 65-kilodalton protein which binds to its 5' untranslated region

Molecular and Cellular Biology

Volumn 16, Issue 8, 1996, Pages 4535-4543

  Gu, Wei ^a   Hecht, Norman B ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; RNA BINDING PROTEIN;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CROSS LINKING; GERM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; RNA SEQUENCE; RNA TRANSLATION; SPERMATOGENESIS; TESTIS; TRANSLATION REGULATION;

EID: 0029994496     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.8.4535     Document Type: Article

References (70)

1. Aharon, T., and R. J. Schneider. 1993. Selective destabilization of short-lived mRNAs with the granulocyte-macrophage colony-stimulating factor AU-rich 3′ noncoding region is mediated by a cotranslational mechanism. Mol. Cell. Biol. 13:1971-1980.
2. Aitken, R. J., and J. S. Clarkson. 1987. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J. Reprod. Fertil. 81:459-469.
3. Alvarez, J. G., and B. T. Storey. 1992. Evidence for increased lipid peroxidative damage and loss of superoxide dismutase activity as a model of sublethal cryodamage to human sperm during cryopreservation. J. Androl. 13:232-241.
4. Alvarez, J. G., J. C. Touchstone, L. Blasco, and B. T. Storey. 1987. Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa: superoxide dismutase as major enzyme protectant against oxygen toxicity. J. Androl. 8:338-348.
5. Arrick, B. A., A. L. Lee, R. L. Grendell, and R. Derynck. 1991. Inhibition of translation of transforming growth factor-β3 mRNA by its 5′ untranslated region. Mol. Cell. Biol. 121:4306-4311.
6. Avraham, K. B., M. Schickler, D. Sapoznicov, R. Yarom, and V. Groner. 1988. Down's syndrome: abnormal neuromuscular junctions in tongue of transgenic mice with elevated levels of human Cu/Zn superoxide dismutase. Cell 54:823-829.
7. Bauche, F., M. H. Fouchard, and B. Jégou. 1994. Antioxidant system in rat testicular cells. FEBS Lett. 349:392-396.
8. 2+ superoxide dismutase. Gene 99:191-195.
9. Bernstein, P., and J. Ross. 1989. Poly(A), poly(A) binding protein and the regulation of mRNA stability. Trends Biochem. Sci. 14:373-377.
10. Braun, R. E., J. J. Peschon, R. R. Behringer, R. L. Brinster, and R. D. Palmiter. 1989. Protamine 3′-untranslated sequences regulate temporal translational control and subcellular localization of growth hormone in spermatids of transgenic mice. Genes Dev. 3:793-802.
11. Chang, E. C., B. F. Crawford, Z. Hong, T. Bilinski, and D. J. Kosman. 1991. Genetic and biochemical characterization of Cu, Zn superoxide dismutase mutations in Saccharomyces cerevisiae. J. Biol. Chem. 266:4417-4424.
12. Clerch, L. B. 1995. A 3′ untranslated region of catalase mRNA composed of a stem-loop and dinucleotide repeat elements binds a 69-kDa redox-sensitive protein. Arch. Biochem. Biophys. 317:267-274.
13. Crapo, J. D., T. Oury, C. Rabouille, J. W. Slot, and L.-Y. Chang. 1992. Copper, zinc superoxide dismutase is primarily a cytosolic protein in human cells. Proc. Natl. Acad. Sci. USA 89:10405-10409.
14. Cummings, A., and J. Sommerville. 1988. Protein kinase associated with stored messenger ribonucleoprotein particles of Xenopus oocytes. J. Cell Biol. 107:45-56.
15. Deng, H.-X., A. Hentati, J. A. Tainer, Z. Iqbal, A. Cayabyab, W. Y. Hung, E. D. Getzoff, P. Hu, B. Herzfeldt, R. P. Roos, C. Warner, G. Deng, E. Soriano, C. Smyth, H. E. Parge, A. Ahmed, A. D. Roses, R. A. Hollewell, M. A. Pericak-Vouce, and T. Siddique. 1993. Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science 261:1047.
16. Didier, D. K., J. Schiffenbauer, S. L. Woulfe, and M. Zacheis. 1988. Characterization of the cDNA encoding a protein binding to the major histocompatibility complex class II box. Proc. Natl. Acad. Sci. USA 85:7322-7326.
17. Elroy-Stein, O., Y. Bernstein, and Y. Groner. 1986. Overproduction of human Cu/Zn-superoxide dismutase in transfected cells: extenuation of paraquat-mediated cytotoxicity and enhancement of lipid peroxidation. EMBO J. 5:615-622.
18. Fajardo, M. A., K. A. Butner, K. Lee, and R. E. Braun. 1994. Germ cell-specific proteins interact with the 3′ untranslated regions of Prm-1 and Prm-2 mRNA. Dev. Biol. 166:643-653.
19. Gold, B., and N. B. Hecht. 1981. Differential compartmentalization of messenger ribonucleic acid in murine testis. Biochemistry 20:480-487.
20. Gold, B., L. Stern, F. M. Bradlay, and N. B. Hecht. 1983. Gene expression during mammalian spermatogenesis. II. Stage-specific differences in mRNA populations. J. Exp. Zool. 225:123-134.
21. Goossen, B., S. W. Caughman, J. B. Harford, R. D. Klausner, and M. W. Hentze. 1990. Translational repression by a complex between the iron-responsive element of ferritin mRNA and its specific cytoplasmic binding protein is position-dependent in vivo. EMBO J. 9:4127-4133.
22. Goossen, B., and M. W. Hentze. 1992. Position is the critical determinant for function of iron-responsive elements as translational regulators. Mol. Cell. Biol. 12:1959-1966.
23. Grens, A., and I. E. Scheffler. 1990. The 5′- and 3′-untranslated regions of ornithine decarboxylase mRNA affect the translational efficiency. J. Biol. Chem. 265:11810-11816.
24. Gu, W., and N. B. Hecht. 1996. Developmental expression of glutathione peroxidase, catalase and manganese superoxide dismutase mRNAs during spermatogenesis in the mouse. J. Androl. 17:256-262.
25. Gu, W., and N. B. Hecht. Unpublished data.
26. Gu, W., C. Morales, and N. B. Hecht. 1995. In male mouse germ cells Cu/Zn superoxide dismutase (SOD-1) utilizes alternative promoters which produce multiple transcripts with different translational potential. J. Biol. Chem. 270:236-243.
27. Hake, L. E., and J. D. Richter. 1994. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79:617-627.
28. Han, J. R., G. Yiu, and N. B. Hecht. 1995. Testis brain RNA-binding protein attaches translationally repressed and transported mRNAs to microtubules. Proc. Natl. Acad. Sci. USA 92:9550-9554.
29. Harrell, C. M., A. R. McKenzie, M. M. Patino, W. E. Walden, and E. C. Theil. 1991. Ferritin mRNA: interaction of iron regulatory element with translational regulatory protein P-90 and the effect on base-paired flanking regions. Proc. Natl. Acad. Sci. USA 88:4166-4170.
30. Hecht, N. B. 1986. Regulation of gene expression during mammalian spermalogenesis, p. 151-193. In J. Rossant and R. Pedersen (ed.), Experimental approaches to mammalian embryonic development. Cambridge University Press, New York.
31. Hecht, N. B. 1993. Gene expression during male germ cell development, p. 400-432. In C. Desjardins and L. L. Ewing (ed.), Cell and molecular biology of the testis. Oxford University Press, New York.
32. Henderson, B. R., C. Seiser, and L. C. Kuhn. 1993. Characterization of a second RNA-binding protein in rodents with specificity for iron-responsive elements. J. Biol. Chem. 268:27327-27334.
33. Hentze, M. W., S. W. Caughman, T. A. Rouault, J. G. Barriocanal, A. Dancis, J. B. Harford, and R. D. Klausner. 1987. Identification of the iron-responsive element for the translational regulation of human ferritin mRNA. Science 238:1570-1573.
34. Holland, M. K., J. Alvarez, and B. T. Storey. 1982. Production of superoxide and activity of superoxide dismutase in rabbit epididymal spermatozoa. Biol. Reprod. 27:1109-1118.
35. Houman, F., M. R. Diaz-Torres, and A. Wright. 1990. Transcriptional anti-termination in the bgl operon of E. coli is modulated by a specific RNA binding protein. Cell 62:1153-1163.
36. Jow, W. W., P. N. Schlegel, Z. Cichon, D. Philips, M. Goldstein, and C. W. Bardin. 1993. Identification and localization of copper-zinc superoxide dismutase gene expression in rat testicular development. J. Androl. 14:439-447.
37. Kennedy, M. C., M. M. Lione, G. A. Blondin, and H. Beinert 1992. Purification and characterization of cytosolic aconitase from beef liver and its relationship to the iron-responsive element binding protein. Proc. Natl. Acad. Sci. USA 89:11730-11734.
38. Kick, D., P. Barrett, A., Cummings, and J. Sommerville. 1987. Phosphorylation of a 60 kDa polypeptide from Xenopus oocytes blocks messenger RNA translation. Nucleic Acids Res. 15:4009-4019.
39. Kilk, A., M. Laan, and A. Torp. 1995. Human Cu/Zn superoxide dismutase enzymatic activity in cells is regulated by the length of the mRNA. FEBS Lett. 362:323-327.
40. Kim, S. J., K. Park, K. Y. Koeller, L. M. Wakefield, M. B. Sporn, and A. B. Roberts. 1992. Post-transcriptional regulation of the human transforming growth factor-β1 gene. J. Biol. Chem. 267:13702-13707.
41. Koeller, D. M., J. L. Cassey, M. W. Hentze, E. M. Gerhardt, L.-N. Chan, R. D. Klausner, and J. B. Harford. 1989. A cytosolic protein binds to a structural element within the iron regulatory region of the transferrin receptor mRNA. Proc. Natl. Acad. Sci. USA 86:3574-3578.
42. Kozak, M. 1978. How do eukaryotic ribosomes select initiation regions of messenger RNA? Cell 15:1109-1123.
43. Kwon, Y. K., and N. B. Hecht. 1991. Cytoplasmic protein binding to highly conserved sequences in the 3′ untranslated region of mouse protamine 2 mRNA, a translationally regulated gene of male germ cells. Proc. Natl. Acad. Sci. USA 88:3584-3588.
44. Kwon, Y. K., and N. B. Hecht. 1993. Binding of a phosphoprotein to the 3′ untranslated region of the mouse protamine 2 mRNA temporally represses its translation. Mol. Cell. Biol. 13:6547-6557.
45. Kwon, Y. K., M. T. Murray, and B. N. Hecht. 1993. Proteins homologous to the Xenopus germ cell-specific RNA-binding proteins p54/p56 are temporally expressed in mouse male germ cells. Dev. Biol. 158:90-100.
46. Lasso, J. L., E. E. Hoiles, J. G. Alvarez, and B. T. Storey. 1994. Mechanism of superoxide dismutase loss from human sperm cells during cryopreservation. J. Androl. 15:255-265.
47. Levanon, D., J. Lieman-Hurwitz, N. Dafni, M. Wigderson, L. Sherman, Y. Bernstein, Z. Laver-Rudich, E. Danciger, O. Stein, and Y. Groner. 1985. Architecture and anatomy of the chromosomal locus in human chromosome 21 encoding the Cu/Zn superoxide dismutase. EMBO J. 4:77-84.
48. Liu, X. F., I. Flashvili, E. B. Gralla, J. S. Valentine, P. Lapinskas, and V. C. Culotta. 1992. Yeast lacking superoxide dismutase. J. Biol. Chem. 267:18298-18302.
49. Manzella, J. M., and P. J. Blackshear. 1992. Specific protein binding to a conserved region of the ornithine decarboxylase mRNA 5′-untranslated region. J. Biol. Chem. 267:7077-7082.
50. Marello, K., J. LaRovere, and J. Sommerville. 1992. Binding of Xenopus oocyte masking protein to mRNA sequences. Nucleic Acids Res. 20:5593-5600.
51. Murray, M. T., G. Krohne, and W. W. Franke. 1991. Different forms of soluble cytoplasmic mRNA binding proteins and particles in Xenopus laevis oocytes and embryos. J. Biol. Chem. 112:1-11.
52. Murray, M. T., D. L. Schiller, and W. W. Franke. 1992. Sequence analysis of cytoplasmic mRNA-binding protein of Xenopus oocytes identifies a family of RNA-binding proteins. Proc. Natl. Acad. Sci. USA 89:11-15.
53. Neupert, B., N. A. Thompson, C. Meyer, and L. C. Kuhn. 1990. A high yield affinity purification method for specific RNA-binding proteins: isolation of the iron regulatory factor from human placenta. Nucleic Acids Res. 18:51-55.
54. Nikolajczyk, B. S., M. T. Murray, and N. B. Hecht. 1995. A mouse homologue of the Xenopus germ cell-specific ribonucleic acid/deoxyribonucleic acid-binding protein p54/p56 interacts with the protamine 2 promoter. Biol. Reprod. 52:524-530.
55. Paris, J., K. Swenson, H. Piwnica-Worms, and J. D. Richter. 1991. Maturation-specific polyadenylation: in vitro activation by p34cdc2 kinase and phosphorylation of a 58 kD CPE-binding protein. Genes Dev, 5:1697-1708.
56. Parkin, N. T., and N. Sonenberg. 1989. Identification of a protein that binds specifically to RNA from the first exon of c-myc. Oncogene 4:815-822.
57. Pearson, W. R. 1990. Rapid and sensitive sequence comparison with FASTP and FASTA. Methods Enzymol. 183:63-98.
58. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
59. Pelletier, J., and N. Sonenberg. 1985. Insertion mutagenesis to increase secondary structure within the 5′ noncoding region of a eukaryotic mRNA reduces translation efficiency. Cell 40:515-526.
60. Ray, B. K., T. G. Lawson, J. C. Kramer, M. H. Cladaras, J. A. Grifo, R. D. Abramson, W. C. Merrick, and R. E. Thach. 1985. ATP-dependent unwinding of messenger RNA structure by eukaryotic initiation factors. J. Biol. Chem. 260:7651-7658.
61. Richter, J. D., and L. D. Smith. 1984. Reversible inhibition of translation by Xenopus oocyte specific proteins. Nature (London) 309:378-380.
62. Rosen, D. R., T. Siddique, P. David, D. A. Figlewicz, P. Sapp, A. Hentati, D. Donaldson, J. P. Goto, H.-X. Deng, Z. Rahmani, A. Krizus, D. McKenna-Yasek, A. Cayabyab, S. M. Gaston, R. Berger, R. E. Tanzi, J. J. Halperin, B. Herzfeldt, R. Van der Bergh, W. Y. Hong, T. Bird, G. Deng, D. W. Mulder, C. Smyth, N. G. Laing, J. S. Gusella, H. R. Horvitz, and R. H. Brown, Jr. 1993. Mutations in Cu/Zn superoxide dismutase are associated with familial amyotrophic lateral sclerosis. Nature (London) 362:59.
63. Sachs, A. B., and E. Wahle. 1993. Poly(A) tail metabolism and function in eukaryotes. J. Biol. Chem. 268:22955-22958.
64. Sherman, L., N. Dafni, J. Lieman-Hurwitz, and Y. Groner. 1983. Nucleotide sequence and expression of human chromosome 21-encoded superoxide dismutase mRNA. Proc. Natl. Acad. Sci. USA 80:5465-5469.
65. Sherman, L., D. Levanon, J. Lieman-Hurwitz, J. Dafni, and Y. Groner. 1984. Human Cu/Zn superoxide dismutase gene: molecular characterization of its two mRNA species. Nucleic Acids Res. 12:9349-9365.
66. Sonenberg, N. 1991. Picornavirus RNA translation continues to surprise. Trends Genet. 7:105-106.
67. Tafuri, S. R., M. Familiari, and A. P. Wolffe. 1993. A mouse Y box protein, MSY1, is associated with paternal mRNA in spermatocytes. J. Biol. Chem. 268:12213-12220.
68. Van Loon, A. A. W. M., P. J. Den Boer, G. P. Van Der Schans, P. Mackenbach, J. A. Grootegoed, R. A. Baan, and P. H. M. Lohman. 1991. Immunochemical detection of DNA damage induction and repair at different cellular stages of spermatogenesis of hamster after in vitro or in vivo exposure to ionizing radiation. Exp. Cell Res. 193:303-309.
69. Wray, W., T. Boulikas, V. P. Wray, and R. Hancock. 1981. Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118:197-203.
70. Yu, Y., E. Radisky, and E. A. Leibold. 1992. The iron-responsive element binding protein, purification, cloning, and regulation in rat liver. J. Biol. Chem. 267:19005-19010.