The testis-specific high-mobility-group protein, a phosphorylation-dependent DNA-packaging factor of elongating and condensing spermatids

Molecular and Cellular Biology

Volumn 16, Issue 7, 1996, Pages 3720-3729

  Alami Ouahabi, Naïma ^a   Veilleux, Stéphane ^a   Meistrich, Marvin L ^b   Boissonneault, Guylain ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; MAMMALIA; TETRAHYMENA THERMOPHILA;

DNA BINDING PROTEIN; DNA TOPOISOMERASE; HIGH MOBILITY GROUP PROTEIN; PROTEIN KINASE C; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA METABOLISM; DNA PACKAGING; DNA SUPERCOILING; DNA TRANSCRIPTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; SPERMATID; SPERMATOGENESIS; TESTIS; TISSUE SPECIFICITY;

ANIMALS; DNA, SUPERHELICAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HIGH MOBILITY GROUP PROTEINS; HUMANS; MALE; MICE; MITOCHONDRIAL PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PLASMIDS; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; SPERMATOGONIA; TETRAHYMENA THERMOPHILA; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0030014597     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.7.3720     Document Type: Article

References (58)

1. Alexander-Bridges, M., L. Ercolani, X. F. Kong, and N. Nasrin. 1992. Identification of a core motif that is recognized by three members of the HMG class of transcriptional regulators: IRE-ABP, SRY, and TCF-1 alpha. J. Cell. Biochem. 48:129-135.
2. Balasubramanian, B., C. V. Lowry, and R. S. Zitomer. 1993. The Rox1 repressor of the Saccharomyces cerevisiae hypoxic genes is a specific DNA-binding protein with a high-mobility-group motif. Mol. Cell. Biol. 13:6071-5078.
3. Barone, J. G., J. De Lara, K. B. Cummings, and W. S. Ward. 1994. DNA organization in human spermatozoa. J. Androl. 15:139-144.
4. Baskaran, R., and M. R. Rao. 1991 Mammalian spermatid specific protein, TP2, is a zinc metalloprotein with two finger motifs. Biochem. Biophys. Res. Commun. 179:1491-1499.
5. Bhorjee, J. S. 1981. Differential phosphorylation of nuclear nonhistone high mobility group proteins HMG 14 and HMG 17 during the cell cycle. Proc. Natl. Acad. Sci. USA 78:6944-6948.
6. Bianchi, M. E., M. Beltrame, and G. Paonessa. 1989. Specific recognition of cruciform DNA by nuclear protein HMG1. Science 243:1056-1059.
7. Bianchi, M. E., L. Falciola, S. Ferrari, and D. M. Lilley. 1992. The DNA binding site of HMG1 protein is composed of two similar segments (HMG boxes), both of which have counterparts in other eukaryotic regulatory proteins. EMBO J. 11:1055-1063.
8. Boissonneault, G., and V. F. Lau. 1993. A testis-specific gene encoding a nuclear high-mobility-group box protein located in elongating spermatids. Mol. Cell. Biol. 13:4323-4330.
9. Bucci, L. R., W. A. Brock, I. L. Goldknopf, and M. L. Meistrich. 1984. Characterization of high mobility group protein levels during spermatogenesis in the rat. J. Biol. Chem. 259:8840-8846.
10. Bucci, L. R., W. A. Brock, and M. L. Meistrich. 1985. Heterogeneity of high-mobility-group protein 2. Enrichment of a rapidly migrating form in testis. Biochem. J. 229:233-240.
11. Bustin, M., M. P. Crippa, and J. M. Pash. 1992. Expression of HMG chromosomal proteins during cell cycle and differentiation. Crit. Rev. Eukaryotic Gene Expression 2:137-143.
12. Bustin, M., D. A. Lehn, and D. Landsman. 1990. Structural features of the HMG chromosomal proteins and their genes. Biochim. Biophys. Acta 1049: 231-243.
13. 3H-thymidine and radioautography. Fertil. Steril. 28:805-817.
14. Diffley, J. F., and B. Stillman. 1992. DNA binding properties of an HMG1-related protein from yeast mitochondria. J. Biol. Chem. 267:3368-3374.
15. Dimov, S. I., E. A. Alexandrova, and B. G. Beltchev. 1990. Differences between some properties of acetylated and nonacetylated forms of HMG1 protein. Biochem. Biophys. Res. Commun. 166:819-826.
16. Fisher, R. P., T. Lisowsky, M. A. Parisi, and D. A. Clayton. 1992. DNA wrapping and bending by a mitochondrial high mobility group-like transcriptional activator protein. J. Biol. Chem. 267:3358-3367.
17. Geremia, R., C. Boitani, M. Conti, and V. Monesi. 1977. RNA synthesis in spermatocytes and spermatids and preservation of meiotic RNA during spermiogenesis in the mouse. Cell Differ. 5:343-355.
18. Giese, K., J. Cox, and R. Grosschedl. 1992. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69:185-195.
19. Green, G. R., R. Balhorn, D. L. Poccia, and N. B. Hecht. 1994. Synthesis and processing of mammalian protamines and transition proteins. Mol. Reprod. Dev. 37:255-263.
20. Grimes, S. R., Jr., and P. G. Smart. 1985. Changes in the structural organization of chromatin during spermatogenesis in the rat. Biochim. Biophys. Acta 824:128-139.
21. Grosschedl, R., K. Giese, and J. Pagel. 1994. HMG domain proteins: architectural elements in the assembly of nucleoprotein structures. Trends Genet. 10:94-100.
22. Hu, C. H., B. McStay, S. W. Jeong, and R. H. Reeder. 1994. xUBF, an RNA polymerase I transcription factor, binds crossover DNA with low sequence specificity. Mol. Cell. Biol. 14:2871-2882.
23. Kimura, K., S. Kubo, K. Sakurada, K. Abe, and N. Katoh. 1987. Protein kinase C phosphorylation of protamine is Ca2+ independent, but the addition of DNA renders it Ca2+ dependent. Biochim. Biophys. Acta 929:203-207.
24. King, C. Y., and M. A. Weiss. 1993. The SRY high-mobility-group box recognizes DNA by partial intercalation in the minor groove: a topological mechanism of sequence specificity. Proc. Natl. Acad. Sci. USA 90:11990-11994.
25. Kohlstaedt, L. A., and R. D. Cole. 1994. Specific interaction between H1 histone and high mobility protein HMG1. Biochemistry 33:570-575.
26. Lawrence, D. L., B. N. Engelsberg, R. S. Farid, E. N. Hughes, and P. C. Billings. 1993. Localization of the binding region of high mobility group protein 2 to cisplatin-damaged DNA. J. Biol. Chem. 268:23940-23945.
27. Lilley, D. M. 1992. DNA-protein interactions. HMG has DNA wrapped up. Nature (London) 357:282-283.
28. Lima, C. D., J. C. Wang, and A. Mondragon. 1994. Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature (London) 367:138-145.
29. Marushige, Y., and K. Marushige. 1994. Phosphorylation of sperm histone during spermiogenesis in mammals. Biochim. Biophys. Acta 518:440-449.
30. McPherson, S., and F. J. Longo. 1993. Chromatin structure-function alterations during mammalian spermatogenesis: DNA nicking and repair in elongating spermatids. Eur. J. Histochem. 37:109-128.
31. McPherson, S. M., and F. J. Longo. 1992. Localization of DNase I-hypersensitive regions during rat spermatogenesis: stage-dependent patterns and unique sensitivity of elongating spermatids. Mol. Reprod. Dev. 31:268-279.
32. McPherson, S. M., and F. J. Longo. 1993. Nicking of rat spermatid and spermatozoa DNA: possible involvement of DNA topoisomerase II. Dev. Biol. 158:122-130.
33. Meistrich, M. L., B. O. Reid, and W. J. Barcellona. 1976. Changes in sperm nuclei during spermatogenesis and epididymal maturation. Exp. Cell Res. 99:72-78.
34. Meistrich, M. L., P. K. Trostle, M. Frapart, and R. P. Erickson. 1977. Biosynthesis and localization of lactate dehydrogenase X in pachytene spermatocytes and spermatids of mouse testes. Dev. Biol. 60:428-441.
35. Meistrich, M. L., P. K. Trostle-Weige, and M. E. A. B. Van Beek. 1994. Separation of specific stages of spermatids from vitamin A synchronized rat testes for assessment of nucleoprotein changes during spermiogenesis. Biol. Reprod. 51:334-344.
36. Nissen, M. S., and R. Reeves. 1995. Changes in superhelicity are introduced into closed circular DNA by binding of high mobility group protein I/Y. J. Biol. Chem. 270:4355-4360.
37. Oliva, R., and G. H. Dixon. 1991. Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog. Nucleic Acid Res. Mol. Biol. 40:25-94.
38. Oosterwegel, M., M. van de Wetering, and H. Clevers. 1993. HMG box proteins in early T-cell differentiation. Thymus 22:67-81.
39. Parisi, M. A., and D. A. Clayton. 1991. Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 252:965-969.
40. Pil, P. M., and S. J. Lippard. 1992. Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin. Science 256:234-237.
41. Pirhonen, A., P. Valtonen, A. Linnala-Kankkunen, and P. H. Maenpaa. 1993. In vitro phosphorylation sites of stallion and bull P1-protamines for cyclic adenosine 3′,5′ monophosphate-dependent protein kinase and protein kinase C. Biol. Reprod. 48:821-827.
42. Reeves, R., T. A. Langan, and M. S. Nissen. 1991. Phosphorylation of the DNA-binding domain of nonhistone high-mobility group I protein by cdc2 kinase: reduction of binding affinity. Proc. Natl. Acad. Sci. USA 88:1671-1675.
43. Reeves, R., and M. S. Nissen. 1993. Interaction of high mobility group-I (Y) nonhistone proteins with nucleosome core particles. J. Biol. Chem. 268: 21137-21146.
44. Roca, J., and C. Mezquita. 1989. DNA topoisometase II activity in nonreplicating, transcriptionally inactive, chicken late spermatids. EMBO J. 8:1855-1860.
45. Russell, L. D., R. A. Ettlin, A. P. S. Hikim, and E. D. Clegg. 1990. Histological and histopathological evaluation of the testis. Cache River Press, Clearwater, Fla.
46. Sheflin, L. G., N. W. Fucile, and S. W. Spaulding. 1993. The specific interactions of HMG 1 and 2 with negatively supercoiled DNA are modulated by their acidic C-terminal domains and involve cysteine residues in their HMG 1/2 boxes. Biochemistry 32:3238-3248.
47. Sheflin, L. G., and S. W. Spaulding. 1989. High mobility group protein I preferentially conserves torsion in negatively supercoiled DNA. Biochemistry 28:5658-5664.
48. Studier, F. W., and B. A. Moffat. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
49. Toullec, D., P. Pianetti, H. Coste, P. Bellevergue, T. Grand-Perret, M. Ajakane, V. Baudet, P. Boissin, E. Boursier, F. Loriolle, L. Duhame, D. Charon, and J. Kirilovsky. 1994. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266:15771-15781.
50. Trostle-Weige, P. K., M. L. Meistrich, W. A. Brock, and K. Nishioka. 1984. Isolation and characterization of TH3, a germ cell-specific variant of histone 3 in rat testis. J. Biol. Chem. 259:8769-8776.
51. Unni, E., A. Mayerhofer, Y. Zhang, Y. M. Bhatnagar, L. D. Russell, and M. L. Meistrich. 1995. Increased accessibility of the N-terminus of testis-specific histone TH2B to antibodies in elongating spermatids. Mol. Reprod. Dev. 42:210-219.
52. Unni, E., and M. L. Meistrich. 1992. Purification and characterization of the rat spermatid basic nuclear protein TP4. J. Biol. Chem. 267:25359-25363.
53. van de Wetering, M., and H. Clevers. 1992. Sequence-specific interaction of the HMG box proteins TCF-1 and SRY occurs within the minor groove of a Watson-Crick double helix. EMBO J. 11:3039-3044.
54. Van Holde, K. E. 1989. Chromatin. Springer-Verlag, New York.
55. Wampler, S. L., C. M. Tyree, and J. T. Kadonaga. 1990. Fractionation of the general RNA polymerase II transcription factors from Drosophila embryos. J. Biol. Chem. 265:21223-21231.
56. Ward, W. S., and D. S. Coffey. 1991. DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol. Reprod. 44: 569-574.
57. cdc2 sites, and contain protein kinase A sites. Mol. Cell. Biol. 14:10-20.
58. Zechiedrich, E. L., and N. Osheroff. 1990. Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA cross-overs. EMBO J. 9:4555-4562.