Abstract
By selective dissociation of histones with the ionic detergent sodium deoxycholate, we have demonstrated that these basic chromosomal polypeptides, which are effective inhibitors of transcription, are more tenaciously bound to DNA in mitotic than in S-phase chromatin. Evidence is presented which suggests that cell-cycle-stage-specific non-histone chromosomal proteins can account for such variations in the association of histones with DNA. When chromatin is reconstituted with DNA and histones are pooled from S-phase and mitotic cells and either S-phase or mitotic non-histone chromosomal proteins, a preferential extraction of histones with sodium deoxycholate from chromatin reconstituted with S-phase rather than mitotic non-histone chromosomal proteins is observed. In contrast, the extractability of histones with sodium deoxycholate from nucleohistone complexes reconstituted with DNA pooled from S-phase and mitotic cells and either S-phase or mitotic histones is identical. Since non-histone chromosomal proteins rather than histones are responsible for the differences in chromatin template activity during S-phase and mitosis, we propose that non-histone chromosomal proteins may modify gene expression during the cell cycle by mediating the binding of histones to DNA.
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- ALLFREY V. G., LITTAU V. C., MIRSKY A. E. On the role of of histones in regulation ribonucleic acid synthesis in the cell nucleus. Proc Natl Acad Sci U S A. 1963 Mar 15;49:414–421. doi: 10.1073/pnas.49.3.414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BASERGA R. A study of nucleic acid synthesis in ascites tumor cells by two-emulsion autoradiography. J Cell Biol. 1962 Mar;12:633–637. doi: 10.1083/jcb.12.3.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bekhor I., Kung G. M., Bonner J. Sequence-specific interaction of DNA and chromosomal protein. J Mol Biol. 1969 Jan;39(2):351–364. doi: 10.1016/0022-2836(69)90322-2. [DOI] [PubMed] [Google Scholar]
- Borun T. W., Stein G. S. The synthesis of acidic chromosomal proteins during the cell cycle of HeLa S-3 cells. II. The kinetics of residual protein synthesis and transport. J Cell Biol. 1972 Feb;52(2):308–315. doi: 10.1083/jcb.52.2.308. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilmour R. S., Paul J. Role of non-histone components in determining organ specificity of rabbit chromatins. FEBS Lett. 1970 Aug 17;9(4):242–244. doi: 10.1016/0014-5793(70)80366-0. [DOI] [PubMed] [Google Scholar]
- Huang R. C., Bonner J. Histone-bound RNA, a component of native nucleohistone. Proc Natl Acad Sci U S A. 1965 Sep;54(3):960–967. doi: 10.1073/pnas.54.3.960. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson T. C., Holland J. J. Ribonucleic acid and protein synthesis in mitotic HeLa cells. J Cell Biol. 1965 Dec;27(3):565–574. doi: 10.1083/jcb.27.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kostraba N. C., Wang T. Y. Differential activation of transcription of chromatin by non-histone fractions. Biochim Biophys Acta. 1972 Mar 14;262(2):169–180. doi: 10.1016/0005-2787(72)90230-4. [DOI] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Levy R., Levy S., Rosenberg S. A., Simpson R. T. Selective stimulation of nonhistone chromatin protein synthesis in lymphoid cells by phytohemagglutinin. Biochemistry. 1973 Jan 16;12(2):224–228. doi: 10.1021/bi00726a008. [DOI] [PubMed] [Google Scholar]
- Maizel J. V., Jr Acrylamide-gel electrophorograms by mechanical fractionation: radioactive adenovirus proteins. Science. 1966 Feb 25;151(3713):988–990. doi: 10.1126/science.151.3713.988. [DOI] [PubMed] [Google Scholar]
- Marushige K., Bonner J. Template properties of liver chromatin. J Mol Biol. 1966 Jan;15(1):160–174. doi: 10.1016/s0022-2836(66)80218-8. [DOI] [PubMed] [Google Scholar]
- PRESCOTT D. M., BENDER M. A. Synthesis of RNA and protein during mitosis in mammalian tissue culture cells. Exp Cell Res. 1962 Mar;26:260–268. doi: 10.1016/0014-4827(62)90176-3. [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]
- Paul J., Gilmour R. S. Organ-specific restriction of transcription in mammalian chromatin. J Mol Biol. 1968 Jul 14;34(2):305–316. doi: 10.1016/0022-2836(68)90255-6. [DOI] [PubMed] [Google Scholar]
- Paul J., Gilmour R. S. Restriction of deoxyribonucleic acid template activity in chromatin is organ-specific. Nature. 1966 Jun 4;210(5040):992–993. doi: 10.1038/210992a0. [DOI] [PubMed] [Google Scholar]
- Paul J., Gilmour R. S. Template activity of DNA is restricted in chromatin. J Mol Biol. 1966 Mar;16(1):242–244. doi: 10.1016/s0022-2836(66)80276-0. [DOI] [PubMed] [Google Scholar]
- Paul J., More I. R. Properties of reconstituted chromatin and nucleohistone complexes. Nat New Biol. 1972 Oct 4;239(92):134–135. doi: 10.1038/newbio239134a0. [DOI] [PubMed] [Google Scholar]
- Platz R. D., Stein G. S., Kleinsmith L. J. Changes in the phosphorylation of non-histone chromatin proteins during the cell cycle of HeLa S 3 cells. Biochem Biophys Res Commun. 1973 Apr 2;51(3):735–740. doi: 10.1016/0006-291x(73)91377-6. [DOI] [PubMed] [Google Scholar]
- Robbins E., Borun T. W. The cytoplasmic synthesis of histones in hela cells and its temporal relationship to DNA replication. Proc Natl Acad Sci U S A. 1967 Feb;57(2):409–416. doi: 10.1073/pnas.57.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rovera G., Baserga R. Early changes in the synthesis of acidic nuclear proteins in human diploid fibroblasts stimulated to synthesize DNA by changing the medium. J Cell Physiol. 1971 Apr;77(2):201–211. doi: 10.1002/jcp.1040770211. [DOI] [PubMed] [Google Scholar]
- Shea M., Kleinsmith L. J. Template-specific stimulation of RNA synthesis by phosphorylated non-histone chromatin proteins. Biochem Biophys Res Commun. 1973 Jan 23;50(2):473–477. doi: 10.1016/0006-291x(73)90864-4. [DOI] [PubMed] [Google Scholar]
- Smart J. E., Bonner J. Selective dissociation of histones from chromatin by sodium deoxycholate. J Mol Biol. 1971 Jun 28;58(3):651–659. doi: 10.1016/0022-2836(71)90030-1. [DOI] [PubMed] [Google Scholar]
- Spalding J., Kajiwara K., Mueller G. C. The metabolism of basic proteins in HeLa cell nuclei. Proc Natl Acad Sci U S A. 1966 Nov;56(5):1535–1542. doi: 10.1073/pnas.56.5.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spelsberg T. C., Hnilica L. S. Deoxyribonucleoproteins and the tissue-specific restriction of the deoxyribonucleic acid in chromatin. Biochem J. 1970 Nov;120(2):435–437. doi: 10.1042/bj1200435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spelsberg T. C., Hnilica L. S. The effects of acidic proteins and RNA on the histone inhibition of the DNA-dependent RNA synthesis in vitro. Biochim Biophys Acta. 1969 Nov 19;195(1):63–75. doi: 10.1016/0005-2787(69)90603-0. [DOI] [PubMed] [Google Scholar]
- Stein G. S., Borun T. W. The synthesis of acidic chromosomal proteins during the cell cycle of HeLa S-3 cells. I. The accelerated accumulation of acidic residual nuclear protein before the initiation of DNA replication. J Cell Biol. 1972 Feb;52(2):292–307. doi: 10.1083/jcb.52.2.292. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stein G. S., Matthews D. E. Nonhistone chromosomal protein synthesis: utilization of preexisting and newly transcribed messenger RNA's. Science. 1973 Jul 6;181(4094):71–73. doi: 10.1126/science.181.4094.71. [DOI] [PubMed] [Google Scholar]
- Stein G. S., Thrall C. L. Evidence for the presence of nonhistone chromosomal proteins in the nucleoplasm of HeLa S 3 cells. FEBS Lett. 1973 May 15;32(1):41–45. doi: 10.1016/0014-5793(73)80732-x. [DOI] [PubMed] [Google Scholar]
- Stein G., Baserga R. Nuclear proteins and the cell cycle. Adv Cancer Res. 1972;15:287–330. doi: 10.1016/s0065-230x(08)60378-4. [DOI] [PubMed] [Google Scholar]
- Stein G., Baserga R. The synthesis of acidic nuclear proteins in the prereplicative phase of the isoproterenol-stimulated salivary gland. J Biol Chem. 1970 Nov 25;245(22):6097–6105. [PubMed] [Google Scholar]
- Stein G., Chaudhuri S., Baserga R. Gene activation in WI-38 fibroblasts stimulated to proliferate. Role of non-histone chromosomal proteins. J Biol Chem. 1972 Jun 25;247(12):3918–3922. [PubMed] [Google Scholar]
- Stein G., Farber J. Role of nonhistone chromosomal proteins in the restriction of mitotic chromatin template activity. Proc Natl Acad Sci U S A. 1972 Oct;69(10):2918–2921. doi: 10.1073/pnas.69.10.2918. [DOI] [PMC free article] [PubMed] [Google Scholar]
- TAYLOR J. H. Nucleic acid synthesis in relation to the cell division cycle. Ann N Y Acad Sci. 1960 Oct 7;90:409–421. doi: 10.1111/j.1749-6632.1960.tb23259.x. [DOI] [PubMed] [Google Scholar]
- Teng C. S., Teng C. T., Allfrey V. G. Studies of nuclear acidic proteins. Evidence for their phosphorylation, tissue specificity, selective binding to deoxyribonucleic acid, and stimulation effects on transcription. J Biol Chem. 1971 Jun 10;246(11):3597–3609. [PubMed] [Google Scholar]
- Tsuboi A., Baserga R. Synthesis of nuclear acidic proteins in density-inhibited fibroblasts stimulated to proliferate. J Cell Physiol. 1972 Aug;80(1):107–118. doi: 10.1002/jcp.1040800112. [DOI] [PubMed] [Google Scholar]
- Wang T. Y. Restoration of histone-inhibited DNA-dependent RNA synthesis by acidic chromatin proteins. Exp Cell Res. 1968 Oct;53(1):288–291. doi: 10.1016/0014-4827(68)90377-7. [DOI] [PubMed] [Google Scholar]

