Abstract
Proportions of the four major chicken H-1 histones (referred to as H- 1's a-d) change during in vitro skeletal myogenesis. As myoblasts fuse and differentiate into myotubes, the relative amount of H-1c increases dramatically. The change occurs primarily because synthesis of the H-1 species is coupled to DNA synthesis to different extents. H-1c synthesis is least tightly coupled to DNA replication in precursor myoblasts and in differentiated myotubes. Thus H-1c synthesis predominates after dividing myoblasts fuse into postmitotic myotubes. This results in the replacement of pre-existing H-1 and therefore increases the relative amount of H-1c. Differences in the stability of the H-1's are also involved in changing H-1 proportions. The results show that changes in H-1 proportions during myogenesis are a consequence of withdrawal from the cell cycle. The data provides a general mechanistic explanation of how tissue-specific H-1 proportions are established.
Full Text
The Full Text of this article is available as a PDF (1.5 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Allan J., Cowling G. J., Harborne N., Cattini P., Craigie R., Gould H. Regulation of the higher-order structure of chromatin by histones H1 and H5. J Cell Biol. 1981 Aug;90(2):279–288. doi: 10.1083/jcb.90.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Bakayev V. V., Bakayeva T. G., Varshavsky A. J. Nucleosomes and subnucleosomes: heterogeneity and composition. Cell. 1977 Jul;11(3):619–629. doi: 10.1016/0092-8674(77)90079-4. [DOI] [PubMed] [Google Scholar]
- Boulikas T., Wiseman J. M., Garrard W. T. Points of contact between histone H1 and the histone octamer. Proc Natl Acad Sci U S A. 1980 Jan;77(1):127–131. doi: 10.1073/pnas.77.1.127. [DOI] [PMC free article] [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]
- Carpenter B. G., Baldwin J. P., Bradbury E. M., Ibel K. Organisation of subunits in chromatin. Nucleic Acids Res. 1976 Jul;3(7):1739–1746. doi: 10.1093/nar/3.7.1739. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiu I. M., Marzluff W. F. Uncoordinate synthesis of histone H1 in cells arrested in the G1 phase. Biochim Biophys Acta. 1982 Dec 31;699(3):173–182. doi: 10.1016/0167-4781(82)90105-1. [DOI] [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]
- Finch J. T., Klug A. Solenoidal model for superstructure in chromatin. Proc Natl Acad Sci U S A. 1976 Jun;73(6):1897–1901. doi: 10.1073/pnas.73.6.1897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gooderham K., Naha P. M. Biochemical controls of the G1 phase of a mammalian cell cycle. II. Synthesis of H1 histones in temperature sensitive mouse cells, arrested in G1 phase. Cell Biol Int Rep. 1981 Dec;5(12):1105–1114. doi: 10.1016/s0309-1651(81)80020-3. [DOI] [PubMed] [Google Scholar]
- Gordon J. S., Kaufman R., Rosenfeld B. I. Independent control during myogenesis of histone and high-mobility-group (HMGs) chromosomal protein heterogeneity. Arch Biochem Biophys. 1981 Oct 15;211(2):709–721. doi: 10.1016/0003-9861(81)90507-5. [DOI] [PubMed] [Google Scholar]
- Gurley L. R., Hardin J. M. The metabolism of histone fractions. II. Conservation and turnover of histone fractions in mammalian cells. Arch Biochem Biophys. 1969 Mar;130(1):1–6. doi: 10.1016/0003-9861(69)90002-2. [DOI] [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]
- Hentschel C. C., Birnstiel M. L. The organization and expression of histone gene families. Cell. 1981 Aug;25(2):301–313. doi: 10.1016/0092-8674(81)90048-9. [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]
- Hohmann P. Species- and cell-specific expression of H1 histones in tissue culture cells. Arch Biochem Biophys. 1980 Nov;205(1):198–209. doi: 10.1016/0003-9861(80)90099-5. [DOI] [PubMed] [Google Scholar]
- Hohmann P. The H1 class of histone and diversity in chromosomal structure. Subcell Biochem. 1978;5:87–127. doi: 10.1007/978-1-4615-7942-7_2. [DOI] [PubMed] [Google Scholar]
- Igo-Kemenes T., Hörz W., Zachau H. G. Chromatin. Annu Rev Biochem. 1982;51:89–121. doi: 10.1146/annurev.bi.51.070182.000513. [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]
- KISSANE J. M., ROBINS E. The fluorometric measurement of deoxyribonucleic acid in animal tissues with special reference to the central nervous system. J Biol Chem. 1958 Jul;233(1):184–188. [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]
- Klenow S. Inhibition of DNA synthesis does not influence the H1 histone synthesis in Tetrahymena pyriformis. Biochim Biophys Acta. 1982 Oct 29;699(1):49–52. doi: 10.1016/0167-4781(82)90170-1. [DOI] [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]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [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]
- McGhee J. D., Felsenfeld G. Nucleosome structure. Annu Rev Biochem. 1980;49:1115–1156. doi: 10.1146/annurev.bi.49.070180.005343. [DOI] [PubMed] [Google Scholar]
- McGhee J. D., Rau D. C., Charney E., Felsenfeld G. Orientation of the nucleosome within the higher order structure of chromatin. Cell. 1980 Nov;22(1 Pt 1):87–96. doi: 10.1016/0092-8674(80)90157-9. [DOI] [PubMed] [Google Scholar]
- Moss B. A., Joyce W. G., Ingram V. M. Histones in chick embryonic erythropoiesis. J Biol Chem. 1973 Feb 10;248(3):1025–1031. [PubMed] [Google Scholar]
- Noll M., Kornberg R. D. Action of micrococcal nuclease on chromatin and the location of histone H1. J Mol Biol. 1977 Jan 25;109(3):393–404. doi: 10.1016/s0022-2836(77)80019-3. [DOI] [PubMed] [Google Scholar]
- Panyim S., Bilek D., Chalkley R. An electrophoretic comparison of vertebrate histones. J Biol Chem. 1971 Jul 10;246(13):4206–4215. [PubMed] [Google Scholar]
- Panyim S., Chalkley R. A new histone found only in mammalian tissues with little cell division. Biochem Biophys Res Commun. 1969 Dec 4;37(6):1042–1049. doi: 10.1016/0006-291x(69)90237-x. [DOI] [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]
- Perucho M., Molgaard H. V., Ruiz-Carrillo A. Enrichment of histone H5-synthesizing polysomes by indirect immunoadsorption. Purification of H5 mRNA. J Biol Chem. 1982 Jan 25;257(2):958–963. [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]
- Renz M., Nehls P., Hozier J. Involvement of histone H1 in the organization of the chromosome fiber. Proc Natl Acad Sci U S A. 1977 May;74(5):1879–1883. doi: 10.1073/pnas.74.5.1879. [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]
- SANTOIANNI P., AYALA M. FLUOROMETRIC ULTRAMICROANALYSIS OF DEOXYRIBONUCLEIC ACID IN HUMAN SKIN. J Invest Dermatol. 1965 Aug;45:99–103. doi: 10.1038/jid.1965.100. [DOI] [PubMed] [Google Scholar]
- Schlissel M. S., Brown D. D. The transcriptional regulation of Xenopus 5s RNA genes in chromatin: the roles of active stable transcription complexes and histone H1. Cell. 1984 Jul;37(3):903–913. doi: 10.1016/0092-8674(84)90425-2. [DOI] [PubMed] [Google Scholar]
- Smerdon M. J., Lieberman M. W. Removal of histone H1 from intact nuclei alters the digestion of nucleosome core DNA by staphylococcal nuclease. J Biol Chem. 1981 Mar 10;256(5):2480–2483. [PubMed] [Google Scholar]
- Smith B. J., Cook Y., Johns E. W., Weiss R. A. Absence of H1 degree from quiescent chicken cells. FEBS Lett. 1981 Nov 30;135(1):77–80. doi: 10.1016/0014-5793(81)80947-7. [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]
- Tarnowka M. A., Baglioni C., Basilico C. Synthesis of H1 histones by BHK cells in G1. Cell. 1978 Sep;15(1):163–171. doi: 10.1016/0092-8674(78)90092-2. [DOI] [PubMed] [Google Scholar]
- Thoma F., Koller T., Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol. 1979 Nov;83(2 Pt 1):403–427. doi: 10.1083/jcb.83.2.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whitlock J. P., Jr, Simpson R. T. Removal of histone H1 exposes a fifty base pair DNA segment between nucleosomes. Biochemistry. 1976 Jul 27;15(15):3307–3314. doi: 10.1021/bi00660a022. [DOI] [PubMed] [Google Scholar]
- Wu R. S., Bonner W. M. Separation of basal histone synthesis from S-phase histone synthesis in dividing cells. Cell. 1981 Dec;27(2 Pt 1):321–330. doi: 10.1016/0092-8674(81)90415-3. [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]
