Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1994 Aug 1;126(3):591–601. doi: 10.1083/jcb.126.3.591

Remodeling sperm chromatin in Xenopus laevis egg extracts: the role of core histone phosphorylation and linker histone B4 in chromatin assembly

PMCID: PMC2120139  PMID: 8045925

Abstract

We find that the remodeling of the condensed Xenopus laevis sperm nucleus into the paternal pronucleus in egg extracts is associated with phosphorylation of the core histones H2A, H2A.X and H4, and uptake of a linker histone B4 and a HMG 2 protein. Histone B4 is required for the assembly of chromatosome structures in the pronucleus. However neither B4 nor core histone phosphorylation are required for the assembly of spaced nucleosomal arrays. We suggest that the spacing of nucleosomal arrays is determined by interaction between adjacent histone octamers under physiological assembly conditions.

Full Text

The Full Text of this article is available as a PDF (2.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abé S. Differentiation of spermatogenic cells from vertebrates in vitro. Int Rev Cytol. 1987;109:159–209. doi: 10.1016/s0074-7696(08)61722-2. [DOI] [PubMed] [Google Scholar]
  2. Abé S., Hiyoshi H. Synthesis of sperm-specific basic nuclear proteins (SPs) in cultured spermatids from Xenopus laevis. Exp Cell Res. 1991 May;194(1):90–94. doi: 10.1016/0014-4827(91)90134-g. [DOI] [PubMed] [Google Scholar]
  3. Almouzni G., Clark D. J., Méchali M., Wolffe A. P. Chromatin assembly on replicating DNA in vitro. Nucleic Acids Res. 1990 Oct 11;18(19):5767–5774. doi: 10.1093/nar/18.19.5767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Almouzni G., Méchali M. Assembly of spaced chromatin involvement of ATP and DNA topoisomerase activity. EMBO J. 1988 Dec 20;7(13):4355–4365. doi: 10.1002/j.1460-2075.1988.tb03334.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Almouzni G., Méchali M. Assembly of spaced chromatin promoted by DNA synthesis in extracts from Xenopus eggs. EMBO J. 1988 Mar;7(3):665–672. doi: 10.1002/j.1460-2075.1988.tb02861.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Almouzni G., Méchali M., Wolffe A. P. Transcription complex disruption caused by a transition in chromatin structure. Mol Cell Biol. 1991 Feb;11(2):655–665. doi: 10.1128/mcb.11.2.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Almouzni G., Wolffe A. P. Nuclear assembly, structure, and function: the use of Xenopus in vitro systems. Exp Cell Res. 1993 Mar;205(1):1–15. doi: 10.1006/excr.1993.1051. [DOI] [PubMed] [Google Scholar]
  8. Annunziato A. T. Inhibitors of topoisomerases I and II arrest DNA replication, but do not prevent nucleosome assembly in vivo. J Cell Sci. 1989 Aug;93(Pt 4):593–603. doi: 10.1242/jcs.93.4.593. [DOI] [PubMed] [Google Scholar]
  9. Aubert D., Garcia M., Benchaibi M., Poncet D., Chebloune Y., Verdier G., Nigon V., Samarut J., Mura C. V. Inhibition of proliferation of primary avian fibroblasts through expression of histone H5 depends on the degree of phosphorylation of the protein. J Cell Biol. 1991 May;113(3):497–506. doi: 10.1083/jcb.113.3.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Blow J. J., Laskey R. A. Initiation of DNA replication in nuclei and purified DNA by a cell-free extract of Xenopus eggs. Cell. 1986 Nov 21;47(4):577–587. doi: 10.1016/0092-8674(86)90622-7. [DOI] [PubMed] [Google Scholar]
  11. Bonne-Andrea C., Harper F., Sobczak J., De Recondo A. M. Rat liver HMG1: a physiological nucleosome assembly factor. EMBO J. 1984 May;3(5):1193–1199. doi: 10.1002/j.1460-2075.1984.tb01950.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Camerini-Otero R. D., Sollner-Webb B., Felsenfeld G. The organization of histones and DNA in chromatin: evidence for an arginine-rich histone kernel. Cell. 1976 Jul;8(3):333–347. doi: 10.1016/0092-8674(76)90145-8. [DOI] [PubMed] [Google Scholar]
  13. Christensen M. E., Rattner J. B., Dixon G. H. Hyperacetylation of histone H4 promotes chromatin decondensation prior to histone replacement by protamines during spermatogenesis in rainbow trout. Nucleic Acids Res. 1984 Jun 11;12(11):4575–4592. doi: 10.1093/nar/12.11.4575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Crippa M. P., Trieschmann L., Alfonso P. J., Wolffe A. P., Bustin M. Deposition of chromosomal protein HMG-17 during replication affects the nucleosomal ladder and transcriptional potential of nascent chromatin. EMBO J. 1993 Oct;12(10):3855–3864. doi: 10.1002/j.1460-2075.1993.tb06064.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dasso M., Nishitani H., Kornbluth S., Nishimoto T., Newport J. W. RCC1, a regulator of mitosis, is essential for DNA replication. Mol Cell Biol. 1992 Aug;12(8):3337–3345. doi: 10.1128/mcb.12.8.3337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Davis D. L., Burch J. B. Isolation of a chicken HMG2 cDNA clone and evidence for an HMG2-specific 3'-untranslated region. Gene. 1992 Apr 15;113(2):251–256. doi: 10.1016/0378-1119(92)90403-c. [DOI] [PubMed] [Google Scholar]
  17. Dilworth S. M., Black S. J., Laskey R. A. Two complexes that contain histones are required for nucleosome assembly in vitro: role of nucleoplasmin and N1 in Xenopus egg extracts. Cell. 1987 Dec 24;51(6):1009–1018. doi: 10.1016/0092-8674(87)90587-3. [DOI] [PubMed] [Google Scholar]
  18. Dimitrov S., Almouzni G., Dasso M., Wolffe A. P. Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type. Dev Biol. 1993 Nov;160(1):214–227. doi: 10.1006/dbio.1993.1299. [DOI] [PubMed] [Google Scholar]
  19. Forbes D. J., Kirschner M. W., Newport J. W. Spontaneous formation of nucleus-like structures around bacteriophage DNA microinjected into Xenopus eggs. Cell. 1983 Aug;34(1):13–23. doi: 10.1016/0092-8674(83)90132-0. [DOI] [PubMed] [Google Scholar]
  20. Glikin G. C., Ruberti I., Worcel A. Chromatin assembly in Xenopus oocytes: in vitro studies. Cell. 1984 May;37(1):33–41. doi: 10.1016/0092-8674(84)90298-8. [DOI] [PubMed] [Google Scholar]
  21. Goodwin G. H., Woodhead L., Johns E. W. The presence of high mobility group non-histone chromatin proteins in isolated nucleosomes. FEBS Lett. 1977 Jan 15;73(1):85–88. [PubMed] [Google Scholar]
  22. Guan K. L., Dixon J. E. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal Biochem. 1991 Feb 1;192(2):262–267. doi: 10.1016/0003-2697(91)90534-z. [DOI] [PubMed] [Google Scholar]
  23. Gurdon J. B. Changes in somatic cell nuclei inserted into growing and maturing amphibian oocytes. J Embryol Exp Morphol. 1968 Nov;20(3):401–414. [PubMed] [Google Scholar]
  24. Hansen J. C., Ausio J., Stanik V. H., van Holde K. E. Homogeneous reconstituted oligonucleosomes, evidence for salt-dependent folding in the absence of histone H1. Biochemistry. 1989 Nov 14;28(23):9129–9136. doi: 10.1021/bi00449a026. [DOI] [PubMed] [Google Scholar]
  25. Hayes J. J., Clark D. J., Wolffe A. P. Histone contributions to the structure of DNA in the nucleosome. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6829–6833. doi: 10.1073/pnas.88.15.6829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hayes J. J., Tullius T. D., Wolffe A. P. The structure of DNA in a nucleosome. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7405–7409. doi: 10.1073/pnas.87.19.7405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hayes J. J., Wolffe A. P. Preferential and asymmetric interaction of linker histones with 5S DNA in the nucleosome. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6415–6419. doi: 10.1073/pnas.90.14.6415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hiyoshi H., Uno S., Yokota T., Katagiri C., Nishida H., Takai M., Agata K., Eguchi G., Abé S. Isolation of cDNA for a Xenopus sperm-specific basic nuclear protein (SP4) and evidence for expression of SP4 mRNA in primary spermatocytes. Exp Cell Res. 1991 May;194(1):95–99. doi: 10.1016/0014-4827(91)90135-h. [DOI] [PubMed] [Google Scholar]
  29. Hock R., Moorman A., Fischer D., Scheer U. Absence of somatic histone H1 in oocytes and preblastula embryos of Xenopus laevis. Dev Biol. 1993 Aug;158(2):510–522. doi: 10.1006/dbio.1993.1209. [DOI] [PubMed] [Google Scholar]
  30. Isackson P. J., Debold W. A., Reeck G. R. Isolation and separation of chicken erythrocyte high mobility group non-histone chromatin proteins by chromatography on phosphocellulose. FEBS Lett. 1980 Oct 6;119(2):337–342. doi: 10.1016/0014-5793(80)80284-5. [DOI] [PubMed] [Google Scholar]
  31. Jackson J. B., Pollock J. M., Jr, Rill R. L. Chromatin fractionation procedure that yields nucleosomes containing near-stoichiometric amounts of high mobility group nonhistone chromosomal proteins. Biochemistry. 1979 Aug 21;18(17):3739–3748. doi: 10.1021/bi00584a015. [DOI] [PubMed] [Google Scholar]
  32. Jackson V. In vivo studies on the dynamics of histone-DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both. Biochemistry. 1990 Jan 23;29(3):719–731. doi: 10.1021/bi00455a019. [DOI] [PubMed] [Google Scholar]
  33. Kay B. K. Xenopus laevis: Practical uses in cell and molecular biology. Injections of oocytes and embryos. Methods Cell Biol. 1991;36:663–669. [PubMed] [Google Scholar]
  34. Kleinschmidt J. A., Scheer U., Dabauvalle M. C., Bustin M., Franke W. W. High mobility group proteins of amphibian oocytes: a large storage pool of a soluble high mobility group-1-like protein and involvement in transcriptional events. J Cell Biol. 1983 Sep;97(3):838–848. doi: 10.1083/jcb.97.3.838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kleinschmidt J. A., Seiter A., Zentgraf H. Nucleosome assembly in vitro: separate histone transfer and synergistic interaction of native histone complexes purified from nuclei of Xenopus laevis oocytes. EMBO J. 1990 Apr;9(4):1309–1318. doi: 10.1002/j.1460-2075.1990.tb08240.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kleinschmidt J. A., Steinbeisser H. DNA-dependent phosphorylation of histone H2A.X during nucleosome assembly in Xenopus laevis oocytes: involvement of protein phosphorylation in nucleosome spacing. EMBO J. 1991 Oct;10(10):3043–3050. doi: 10.1002/j.1460-2075.1991.tb07855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Laskey R. A., Honda B. M., Mills A. D., Finch J. T. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature. 1978 Oct 5;275(5679):416–420. doi: 10.1038/275416a0. [DOI] [PubMed] [Google Scholar]
  39. Lohka M. J., Masui Y. Formation in vitro of sperm pronuclei and mitotic chromosomes induced by amphibian ooplasmic components. Science. 1983 May 13;220(4598):719–721. doi: 10.1126/science.6601299. [DOI] [PubMed] [Google Scholar]
  40. Lohka M. J., Masui Y. Roles of cytosol and cytoplasmic particles in nuclear envelope assembly and sperm pronuclear formation in cell-free preparations from amphibian eggs. J Cell Biol. 1984 Apr;98(4):1222–1230. doi: 10.1083/jcb.98.4.1222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Louters L., Chalkley R. Exchange of histones H1, H2A, and H2B in vivo. Biochemistry. 1985 Jun 18;24(13):3080–3085. doi: 10.1021/bi00334a002. [DOI] [PubMed] [Google Scholar]
  42. Mahadevan L. C., Willis A. C., Barratt M. J. Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell. 1991 May 31;65(5):775–783. doi: 10.1016/0092-8674(91)90385-c. [DOI] [PubMed] [Google Scholar]
  43. Mannironi C., Bonner W. M., Hatch C. L. H2A.X. a histone isoprotein with a conserved C-terminal sequence, is encoded by a novel mRNA with both DNA replication type and polyA 3' processing signals. Nucleic Acids Res. 1989 Nov 25;17(22):9113–9126. doi: 10.1093/nar/17.22.9113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Merriam R. W. Movement of cytoplasmic proteins into nuclei induced to enlarge and initiate DNA or RNA synthesis. J Cell Sci. 1969 Sep;5(2):333–349. doi: 10.1242/jcs.5.2.333. [DOI] [PubMed] [Google Scholar]
  45. Newport J. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell. 1987 Jan 30;48(2):205–217. doi: 10.1016/0092-8674(87)90424-7. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Ohsumi K., Katagiri C., Kishimoto T. Chromosome condensation in Xenopus mitotic extracts without histone H1. Science. 1993 Dec 24;262(5142):2033–2035. doi: 10.1126/science.8266099. [DOI] [PubMed] [Google Scholar]
  48. Ohsumi K., Katagiri C. Occurrence of H1 subtypes specific to pronuclei and cleavage-stage cell nuclei of anuran amphibians. Dev Biol. 1991 Sep;147(1):110–120. doi: 10.1016/s0012-1606(05)80011-9. [DOI] [PubMed] [Google Scholar]
  49. Panyim S., Chalkley R. The heterogeneity of histones. I. A quantitative analysis of calf histones in very long polyacrylamide gels. Biochemistry. 1969 Oct;8(10):3972–3979. doi: 10.1021/bi00838a013. [DOI] [PubMed] [Google Scholar]
  50. Philpott A., Leno G. H., Laskey R. A. Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell. 1991 May 17;65(4):569–578. doi: 10.1016/0092-8674(91)90089-h. [DOI] [PubMed] [Google Scholar]
  51. Philpott A., Leno G. H. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell. 1992 May 29;69(5):759–767. doi: 10.1016/0092-8674(92)90288-n. [DOI] [PubMed] [Google Scholar]
  52. Poccia D. Remodeling of nucleoproteins during gametogenesis, fertilization, and early development. Int Rev Cytol. 1986;105:1–65. doi: 10.1016/s0074-7696(08)61061-x. [DOI] [PubMed] [Google Scholar]
  53. Pruss D., Wolffe A. P. Histone-DNA contacts in a nucleosome core containing a Xenopus 5S rRNA gene. Biochemistry. 1993 Jul 13;32(27):6810–6814. doi: 10.1021/bi00078a002. [DOI] [PubMed] [Google Scholar]
  54. Risley M. S., Eckhardt R. A. H1 histone variants in Xenopus laevis. Dev Biol. 1981 May;84(1):79–87. doi: 10.1016/0012-1606(81)90372-9. [DOI] [PubMed] [Google Scholar]
  55. Rodríguez-Campos A., Shimamura A., Worcel A. Assembly and properties of chromatin containing histone H1. J Mol Biol. 1989 Sep 5;209(1):135–150. doi: 10.1016/0022-2836(89)90177-0. [DOI] [PubMed] [Google Scholar]
  56. Roth S. Y., Allis C. D. Chromatin condensation: does histone H1 dephosphorylation play a role? Trends Biochem Sci. 1992 Mar;17(3):93–98. doi: 10.1016/0968-0004(92)90243-3. [DOI] [PubMed] [Google Scholar]
  57. Ruiz-Carrillo A., Wangh L. J., Allfrey V. G. Processing of newly synthesized histone molecules. Science. 1975 Oct 10;190(4210):117–128. doi: 10.1126/science.1166303. [DOI] [PubMed] [Google Scholar]
  58. Russanova V., Stephanova E., Pashev I., Tsanev R. Histone variants in mouse centromeric chromatin. Mol Cell Biochem. 1989 Oct 5;90(1):1–7. doi: 10.1007/BF00225215. [DOI] [PubMed] [Google Scholar]
  59. Russanova V., Venkov C., Tsanev R. A comparison of histone variants in different rat tissues. Cell Differ. 1980 Dec;9(6):339–350. doi: 10.1016/0045-6039(80)90033-0. [DOI] [PubMed] [Google Scholar]
  60. Ryoji M., Worcel A. Chromatin assembly in Xenopus oocytes: in vivo studies. Cell. 1984 May;37(1):21–32. doi: 10.1016/0092-8674(84)90297-6. [DOI] [PubMed] [Google Scholar]
  61. Sealy L., Cotten M., Chalkley R. Xenopus nucleoplasmin: egg vs. oocyte. Biochemistry. 1986 May 20;25(10):3064–3072. doi: 10.1021/bi00358a049. [DOI] [PubMed] [Google Scholar]
  62. Shimamura A., Worcel A. The assembly of regularly spaced nucleosomes in the Xenopus oocyte S-150 extract is accompanied by deacetylation of histone H4. J Biol Chem. 1989 Aug 25;264(24):14524–14530. [PubMed] [Google Scholar]
  63. Shirakawa H., Tsuda K., Yoshida M. Primary structure of non-histone chromosomal protein HMG2 revealed by the nucleotide sequence. Biochemistry. 1990 May 8;29(18):4419–4423. doi: 10.1021/bi00470a022. [DOI] [PubMed] [Google Scholar]
  64. Simpson R. T. Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. Biochemistry. 1978 Dec 12;17(25):5524–5531. doi: 10.1021/bi00618a030. [DOI] [PubMed] [Google Scholar]
  65. Smith R. C., Dworkin-Rastl E., Dworkin M. B. Expression of a histone H1-like protein is restricted to early Xenopus development. Genes Dev. 1988 Oct;2(10):1284–1295. doi: 10.1101/gad.2.10.1284. [DOI] [PubMed] [Google Scholar]
  66. Sung M. T., Dixon G. H. Modification of histones during spermiogenesis in trout: a molecular mechanism for altering histone binding to DNA. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1616–1623. doi: 10.1073/pnas.67.3.1616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Tremethick D. J., Drew H. R. High mobility group proteins 14 and 17 can space nucleosomes in vitro. J Biol Chem. 1993 May 25;268(15):11389–11393. [PubMed] [Google Scholar]
  68. Tremethick D. J., Frommer M. Partial purification, from Xenopus laevis oocytes, of an ATP-dependent activity required for nucleosome spacing in vitro. J Biol Chem. 1992 Jul 25;267(21):15041–15048. [PubMed] [Google Scholar]
  69. Tsuda K., Kikuchi M., Mori K., Waga S., Yoshida M. Primary structure of non-histone protein HMG1 revealed by the nucleotide sequence. Biochemistry. 1988 Aug 9;27(16):6159–6163. doi: 10.1021/bi00416a050. [DOI] [PubMed] [Google Scholar]
  70. Wakefield L., Gurdon J. B. Cytoplasmic regulation of 5S RNA genes in nuclear-transplant embryos. EMBO J. 1983;2(9):1613–1619. doi: 10.1002/j.1460-2075.1983.tb01632.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Weisbrod S., Wickens M. P., Whytock S., Gurdon J. B. Active chromatin of oocytes injected with somatic cell nuclei or cloned DNA. Dev Biol. 1982 Nov;94(1):216–229. doi: 10.1016/0012-1606(82)90085-9. [DOI] [PubMed] [Google Scholar]
  72. Wells D., McBride C. A comprehensive compilation and alignment of histones and histone genes. Nucleic Acids Res. 1989;17 (Suppl):r311–r346. doi: 10.1093/nar/17.suppl.r311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. West M. H., Bonner W. M. Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res. 1980 Oct 24;8(20):4671–4680. doi: 10.1093/nar/8.20.4671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Wolffe A. P., Andrews M. T., Crawford E., Losa R., Brown D. D. Negative supercoiling is not required for 5S RNA transcription in vitro. Cell. 1987 May 8;49(3):301–303. doi: 10.1016/0092-8674(87)90279-0. [DOI] [PubMed] [Google Scholar]
  75. Wolffe A. P. Dominant and specific repression of Xenopus oocyte 5S RNA genes and satellite I DNA by histone H1. EMBO J. 1989 Feb;8(2):527–537. doi: 10.1002/j.1460-2075.1989.tb03407.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Wolffe A. P. Replication timing and Xenopus 5S RNA gene transcription in vitro. Dev Biol. 1993 May;157(1):224–231. doi: 10.1006/dbio.1993.1126. [DOI] [PubMed] [Google Scholar]
  77. Wolffe A. P. Transcriptional activation of Xenopus class III genes in chromatin isolated from sperm and somatic nuclei. Nucleic Acids Res. 1989 Jan 25;17(2):767–780. doi: 10.1093/nar/17.2.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Woodland H. R., Adamson E. D. The synthesis and storage of histones during the oogenesis of Xenopus laevis. Dev Biol. 1977 May;57(1):118–135. doi: 10.1016/0012-1606(77)90359-1. [DOI] [PubMed] [Google Scholar]
  79. Woodland H. R. The modification of stored histones H3 and H4 during the oogenesis and early development of Xenopus laevis. Dev Biol. 1979 Feb;68(2):360–370. doi: 10.1016/0012-1606(79)90210-0. [DOI] [PubMed] [Google Scholar]
  80. Worcel A., Han S., Wong M. L. Assembly of newly replicated chromatin. Cell. 1978 Nov;15(3):969–977. doi: 10.1016/0092-8674(78)90280-5. [DOI] [PubMed] [Google Scholar]
  81. 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]
  82. Wyllie A. H., Laskey R. A., Finch J., Gurdon J. B. Selective DNA conservation and chromatin assembly after injection of SV40 DNA into Xenopus oocytes. Dev Biol. 1978 May;64(1):178–188. doi: 10.1016/0012-1606(78)90069-6. [DOI] [PubMed] [Google Scholar]
  83. Young D., Carroll D. Regular arrangement of nucleosomes on 5S rRNA genes in Xenopus laevis. Mol Cell Biol. 1983 Apr;3(4):720–730. doi: 10.1128/mcb.3.4.720. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES