Abstract
We have shown that changes in proportions of the four chicken H-1's during in vitro myogenesis are primarily the result of differential coupling of their synthesis to DNA replication (see the previous paper). We show here that the four major chicken H-1's are encoded by distinct mRNAs which specify primary amino acid sequence variants. Accumulation of the H-1-variant mRNAs is coupled to DNA replication to different extents. The level of mRNA encoding H-1c (the H-1 variant that increases relative to the other H-1's in nondividing muscle cells) is completely uncoupled. In contrast, the level of mRNAs encoding H-1's a, b, and d (which have levels that decrease in nondividing muscle cells) are more tightly coupled. Polyadenylation is not involved in uncoupling H-1c mRNA accumulation from DNA replication.
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Selected References
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- Allan J., Hartman P. G., Crane-Robinson C., Aviles F. X. The structure of histone H1 and its location in chromatin. Nature. 1980 Dec 25;288(5792):675–679. doi: 10.1038/288675a0. [DOI] [PubMed] [Google Scholar]
- Bustin M., Cole R. D. Species and organ specificity in very lysine-rich histones. J Biol Chem. 1968 Sep 10;243(17):4500–4505. [PubMed] [Google Scholar]
- Caplan A. I. A simplified procedure for preparing myogenic cells for culture. J Embryol Exp Morphol. 1976 Aug;36(1):175–181. [PubMed] [Google Scholar]
- Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
- D'Anna J. A., Gurley L. R., Tobey R. A. Syntheses and modulations in the chromatin contents of histones H1 degrees and H1 during G1 and S phases in Chinese hamster cells. Biochemistry. 1982 Aug 17;21(17):3991–4001. doi: 10.1021/bi00260a014. [DOI] [PubMed] [Google Scholar]
- Gjerset R., Gorka C., Hasthorpe S., Lawrence J. J., Eisen H. Developmental and hormonal regulation of protein H1 degrees in rodents. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2333–2337. doi: 10.1073/pnas.79.7.2333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harrison M. F., Wilt F. H. The program of Hl histone synthesis in S. purpuratus embryos and the control of its timing. J Exp Zool. 1982 Nov 1;223(3):245–256. doi: 10.1002/jez.1402230306. [DOI] [PubMed] [Google Scholar]
- Hohmann P., Bern H. A., Cole R. D. Responsiveness of preneoplastic and neoplastic mouse mammary tissues to hormones: casein and histone syntheses. J Natl Cancer Inst. 1972 Aug;49(2):355–360. [PubMed] [Google Scholar]
- Hohmann P., Cole R. D. Hormonal effects on amino acid incorporation into lysine-rich histones in the mouse mammary gland. J Mol Biol. 1971 Jun 14;58(2):533–540. doi: 10.1016/0022-2836(71)90369-x. [DOI] [PubMed] [Google Scholar]
- Hohmann P., Cole R. D. Hormonal effects on amino-acid incorporation into lysine-rich histones. Nature. 1969 Sep 6;223(5210):1064–1066. doi: 10.1038/2231064a0. [DOI] [PubMed] [Google Scholar]
- Isenberg I. Histones. Annu Rev Biochem. 1979;48:159–191. doi: 10.1146/annurev.bi.48.070179.001111. [DOI] [PubMed] [Google Scholar]
- Johns E. W. Studies on histones. 7. Preparative methods for histone fractions from calf thymus. Biochem J. 1964 Jul;92(1):55–59. doi: 10.1042/bj0920055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kessler E., Yaron A. A novel aminopeptidase from Clostridium histolyticum. Biochem Biophys Res Commun. 1973 Jan 23;50(2):405–412. doi: 10.1016/0006-291x(73)90855-3. [DOI] [PubMed] [Google Scholar]
- Kinkade J. M., Jr Qualitative species differences and quantitative tissue differences in the distribution of lysine-rich histones. J Biol Chem. 1969 Jun 25;244(12):3375–3386. [PubMed] [Google Scholar]
- Konigsberg I. R. Diffusion-mediated control of myoblast fusion. Dev Biol. 1971 Sep;26(1):133–152. doi: 10.1016/0012-1606(71)90113-8. [DOI] [PubMed] [Google Scholar]
- Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
- Lennox R. W., Cohen L. H. The histone H1 complements of dividing and nondividing cells of the mouse. J Biol Chem. 1983 Jan 10;258(1):262–268. [PubMed] [Google Scholar]
- Levenson R. G., Marcu K. B. On the existence of polyadenylated histone mRNA in Xenopus laevis oocytes. Cell. 1976 Oct;9(2):311–322. doi: 10.1016/0092-8674(76)90121-5. [DOI] [PubMed] [Google Scholar]
- Molgaard H. V., Perucho M., Ruiz-Carrillo A. Histone H5 messenger RNA is polyadenylated. Nature. 1980 Jan 31;283(5746):502–504. doi: 10.1038/283502a0. [DOI] [PubMed] [Google Scholar]
- Palatnik C. M., Wilkins C., Jacobson A. Translational control during early Dictyostelium development: possible involvement of poly(A) sequences. Cell. 1984 Apr;36(4):1017–1025. doi: 10.1016/0092-8674(84)90051-5. [DOI] [PubMed] [Google Scholar]
- Palmiter R. D. Prevention of NH2-terminal acetylation of proteins synthesized in cell-free systems. J Biol Chem. 1977 Dec 25;252(24):8781–8783. [PubMed] [Google Scholar]
- Panyim S., Chalkley R. High resolution acrylamide gel electrophoresis of histones. Arch Biochem Biophys. 1969 Mar;130(1):337–346. doi: 10.1016/0003-9861(69)90042-3. [DOI] [PubMed] [Google Scholar]
- Pehrson J. R., Cole R. D. Histone H1 subfractions and H10 turnover at different rates in nondividing cells. Biochemistry. 1982 Feb 2;21(3):456–460. doi: 10.1021/bi00532a006. [DOI] [PubMed] [Google Scholar]
- Pehrson J., Cole R. D. Histone H10 accumulates in growth-inhibited cultured cells. Nature. 1980 May 1;285(5759):43–44. doi: 10.1038/285043a0. [DOI] [PubMed] [Google Scholar]
- Peterkofsky B., Diegelmann R. Use of a mixture of proteinase-free collagenases for the specific assay of radioactive collagen in the presence of other proteins. Biochemistry. 1971 Mar 16;10(6):988–994. doi: 10.1021/bi00782a009. [DOI] [PubMed] [Google Scholar]
- Pieler C., Adolf G. R., Swetly P. Accumulation of histone H1(0) during chemically induced differentiation of murine neuroblastoma cells. Eur J Biochem. 1981 Apr;115(2):329–333. doi: 10.1111/j.1432-1033.1981.tb05242.x. [DOI] [PubMed] [Google Scholar]
- Poccia D. L., Hinegardner R. T. Developmental changes in chromatin proteins of the sea urchin from blastula to mature larva. Dev Biol. 1975 Jul;45(1):81–89. doi: 10.1016/0012-1606(75)90243-2. [DOI] [PubMed] [Google Scholar]
- Protter A. A., Wang S. Y., Shelness G. S., Ostapchuk P., Williams D. L. Isolation and characterization of a cDNA clone specific for avian vitellogenin II. Nucleic Acids Res. 1982 Aug 25;10(16):4935–4950. doi: 10.1093/nar/10.16.4935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruderman J. V., Gross P. R. Histones and histone synthesis in sea urchin development. Dev Biol. 1974 Feb;36(2):286–298. doi: 10.1016/0012-1606(74)90052-9. [DOI] [PubMed] [Google Scholar]
- Ruderman J. V., Pardue M. L. A portion of all major classes of histone messenger RNA in amphibian oocytes is polyadenylated. J Biol Chem. 1978 Mar 25;253(6):2018–2025. [PubMed] [Google Scholar]
- Switzer R. C., 3rd, Merril C. R., Shifrin S. A highly sensitive silver stain for detecting proteins and peptides in polyacrylamide gels. Anal Biochem. 1979 Sep 15;98(1):231–237. doi: 10.1016/0003-2697(79)90732-2. [DOI] [PubMed] [Google Scholar]
- Tan K. B., Borun T. W., Charpentier R., Cristofalo V. J., Croce C. M. Normal and neoplastic human cells have different histone H1 compositions. J Biol Chem. 1982 May 25;257(10):5337–5338. [PubMed] [Google Scholar]
- Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Winter E., Levy D., Gordon J. S. Changes in the H-1 histone complement during myogenesis. I. Establishment by differential coupling of H-1 species synthesis to DNA replication. J Cell Biol. 1985 Jul;101(1):167–174. doi: 10.1083/jcb.101.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wray W., Boulikas T., Wray V. P., Hancock R. Silver staining of proteins in polyacrylamide gels. Anal Biochem. 1981 Nov 15;118(1):197–203. doi: 10.1016/0003-2697(81)90179-2. [DOI] [PubMed] [Google Scholar]
- Zlatanova J. S. Synthesis of histone H1(0) is not inhibited in hydroxyurea-treated Friend cells. FEBS Lett. 1980 Apr 7;112(2):199–202. doi: 10.1016/0014-5793(80)80179-7. [DOI] [PubMed] [Google Scholar]
