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PMID: 8599938 Published · ppublish English Comparative Study Journal Article

Evidence for a shared structural role for HMG1 and linker histones B4 and H1 in organizing chromatin.

The EMBO journal ·Vol. 15 ·No. 3 ·1996-02-01 ·Pages 548-61

Nightingale K, Dimitrov S, Reeves R, Wolffe AP

Abstract

The high mobility group proteins 1 and 2 (HMG1/2) and histone B4 are major components of chromatin within the nuclei assembled during the incubation of Xenopus sperm chromatin in Xenopus egg extract. To investigate their potential structural and functional roles, we have cloned and expressed Xenopus HMG1 and histone B4. Purified histone B4 and HMG1 form stable complexes with nucleosomes including Xenopus 5S DNA. Both proteins associate with linker DNA and stabilize it against digestion with micrococcal nuclease, in a similar manner to histone H1. However, neither histone B4 nor HMG1 influence the DNase I or hydroxyl radical digestion of DNA within the nucleosome core. We suggest that HMG1/2 and histone B4 have a shared structural role in organizing linker DNA in the nucleosome.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Chromatin/chemistry,genetics Cloning, Molecular DNA/chemistry,genetics DNA Primers/genetics Female High Mobility Group Proteins/chemistry,genetics Histones/chemistry,genetics Humans In Vitro Techniques Male Molecular Sequence Data Molecular Structure Nucleosomes/chemistry,genetics Ovum/chemistry Sequence Homology, Amino Acid Spermatozoa/chemistry Xenopus
Chemicals
Chromatin DNA Primers High Mobility Group Proteins Histones Nucleosomes DNA
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Nightingale K
Laboratory of Molecular Embryology, National Institute of Child Health and Human Development, NIH, Bethesda, MD 20892-2710, USA.
Dimitrov S
Reeves R
Wolffe A P
References (98)
98 references, click to expand
  1. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage.
    Cell. 1982 Oct;30(3):675-86 PMID: 6183003
  2. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription.
    Cell. 1982 Oct;30(3):687-96 PMID: 7139712
  3. The binding sites for large and small high-mobility-group (HMG) proteins. Studies on HMG-nucleosome interactions in vitro.
    Eur J Biochem. 1982 Oct;127(2):429-36 PMID: 6216108
  4. Active chromatin of oocytes injected with somatic cell nuclei or cloned DNA.
    Dev Biol. 1982 Nov;94(1):216-29 PMID: 7152104
  5. Formation in vitro of sperm pronuclei and mitotic chromosomes induced by amphibian ooplasmic components.
    Science. 1983 May 13;220(4598):719-21 PMID: 6601299
  6. Genomic organization, DNA sequence, and expression of chicken embryonic histone genes.
    J Biol Chem. 1983 Jul 25;258(14):9005-16 PMID: 6190814
  7. Detection by chemical cross-linking of interaction between high mobility group protein 1 and histone oligomers in free solution.
    J Biol Chem. 1983 Sep 25;258(18):11020-4 PMID: 6224795
  8. 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):838-48 PMID: 6224801
  9. 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):1222-30 PMID: 6609160
  10. Rat liver HMG1: a physiological nucleosome assembly factor.
    EMBO J. 1984 May;3(5):1193-9 PMID: 6329744
  11. Isolation and sequence of cDNA clones coding for a member of the family of high mobility group proteins (HMG-T) in trout and analysis of HMG-T-mRNA's in trout tissues.
    Nucleic Acids Res. 1985 Jul 11;13(13):4871-88 PMID: 4022777
  12. High mobility group proteins 1 and 2 stimulate transcription in vitro by RNA polymerases II and III.
    J Biol Chem. 1986 May 25;261(15):6986-92 PMID: 3700424
  13. Salt-dependent co-operative interaction of histone H1 with linear DNA.
    J Mol Biol. 1986 Feb 20;187(4):569-80 PMID: 3712436
  14. Mechanism of chromatin assembly in Xenopus oocytes.
    J Mol Biol. 1986 Jun 5;189(3):457-76 PMID: 3783682
  15. The globular domain of histone H5 is internally located in the 30 nm chromatin fiber: an immunochemical study.
    EMBO J. 1987 Aug;6(8):2387-92 PMID: 2444434
  16. Nucleotide sequence of rat liver HMG1 cDNA.
    Nucleic Acids Res. 1987 Nov 11;15(21):9077 PMID: 3684582
  17. Primary structure of non-histone protein HMG1 revealed by the nucleotide sequence.
    Biochemistry. 1988 Aug 9;27(16):6159-63 PMID: 3191113
  18. Full length cDNA sequence for bovine high mobility group 1 (HMG1) protein.
    Nucleic Acids Res. 1988 Nov 11;16(21):10375 PMID: 3194213
  19. DNA looping by the HMG-box domains of HMG1 and modulation of DNA binding by the acidic C-terminal domain.
    Nucleic Acids Res. 1994 Mar 25;22(6):1044-51 PMID: 8152909
  20. DNA chaperones: a solution to a persistence problem?
    Cell. 1994 Apr 22;77(2):167-9 PMID: 8168125
  21. HMG-D, the Drosophila melanogaster homologue of HMG 1 protein, is associated with early embryonic chromatin in the absence of histone H1.
    EMBO J. 1994 Apr 15;13(8):1817-22 PMID: 8168480
  22. Binding of histones H1 and H5 and their globular domains to four-way junction DNA.
    Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3525-9 PMID: 8170940
  23. HMG domain proteins: architectural elements in the assembly of nucleoprotein structures.
    Trends Genet. 1994 Mar;10(3):94-100 PMID: 8178371
  24. The high mobility group protein HMG1 can reversibly inhibit class II gene transcription by interaction with the TATA-binding protein.
    J Biol Chem. 1994 Jun 24;269(25):17136-40 PMID: 8006019
  25. Remodeling sperm chromatin in Xenopus laevis egg extracts: the role of core histone phosphorylation and linker histone B4 in chromatin assembly.
    J Cell Biol. 1994 Aug;126(3):591-601 PMID: 8045925
  26. Contacts of the globular domain of histone H5 and core histones with DNA in a "chromatosome".
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7817-21 PMID: 8052665
  27. Specific recognition of cruciform DNA by nuclear protein HMG1.
    Science. 1989 Feb 24;243(4894 Pt 1):1056-9 PMID: 2922595
  28. Dominant and specific repression of Xenopus oocyte 5S RNA genes and satellite I DNA by histone H1.
    EMBO J. 1989 Feb;8(2):527-37 PMID: 2721490
  29. Tetrahymena HMG nonhistone chromosomal protein. Isolation and amino acid sequence lacking the N- and C-terminal domains of vertebrate HMG 1.
    J Biochem. 1989 Apr;105(4):577-81 PMID: 2760016
  30. Electrophoretic analyses of nucleosomes and other protein-DNA complexes.
    Methods Enzymol. 1989;170:116-42 PMID: 2770536
  31. High mobility group protein 1 preferentially conserves torsion in negatively supercoiled DNA.
    Biochemistry. 1989 Jun 27;28(13):5658-64 PMID: 2550058
  32. Duplicated NHP6 genes of Saccharomyces cerevisiae encode proteins homologous to bovine high mobility group protein 1.
    J Biol Chem. 1990 Feb 25;265(6):3234-9 PMID: 2406250
  33. Isolation and characterization of a Drosophila hydei histone DNA repeat unit.
    Nucleic Acids Res. 1990 Mar 25;18(6):1573-80 PMID: 2109309
  34. Primary structure of non-histone chromosomal protein HMG2 revealed by the nucleotide sequence.
    Biochemistry. 1990 May 8;29(18):4419-23 PMID: 2350545
  35. DNA and protein determinants of nucleosome positioning on sea urchin 5S rRNA gene sequences in vitro.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5724-8 PMID: 2377610
  36. Structural features of the HMG chromosomal proteins and their genes.
    Biochim Biophys Acta. 1990 Jul 30;1049(3):231-43 PMID: 2200521
  37. The structure of DNA in a nucleosome.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7405-9 PMID: 2170977
  38. New foldback transposable element TFB1 found in histone genes of the midge Chironomus thummi.
    J Mol Biol. 1990 Oct 20;215(4):477-82 PMID: 2172549
  39. Xenopus Y-box transcription factors: molecular cloning, functional analysis and developmental regulation.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):9028-32 PMID: 2247479
  40. Efficient large-scale purification of non-histone chromosomal proteins HMG1 and HMG2 by using Polybuffer-exchanger PBE94.
    J Chromatogr. 1990 Aug 24;530(1):39-46 PMID: 2277118
  41. 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):262-7 PMID: 1852137
  42. Isolation and characterization of maize cDNAs encoding a high mobility group protein displaying a HMG-box.
    Nucleic Acids Res. 1991 May 25;19(10):2573-7 PMID: 2041733
  43. Chromatosome positioning on assembled long chromatin. Linker histones affect nucleosome placement on 5 S rDNA.
    J Mol Biol. 1991 Jul 5;220(1):89-100 PMID: 2067021
  44. A negative regulator of HO transcription, SIN1 (SPT2), is a nonspecific DNA-binding protein related to HMG1.
    Mol Cell Biol. 1991 Aug;11(8):4135-46 PMID: 2072912
  45. Histone contributions to the structure of DNA in the nucleosome.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6829-33 PMID: 1650485
  46. Sequence of human HMG2 cDNA.
    Nucleic Acids Res. 1991 Dec 11;19(23):6643 PMID: 1754403
  47. Cooperative binding of the globular domains of histones H1 and H5 to DNA.
    Nucleic Acids Res. 1992 Jan 25;20(2):187-94 PMID: 1741245
  48. Histones H2A/H2B inhibit the interaction of transcription factor IIIA with the Xenopus borealis somatic 5S RNA gene in a nucleosome.
    Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1229-33 PMID: 1741376
  49. 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. 1992 Mar;11(3):1055-63 PMID: 1547772
  50. Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin.
    Science. 1992 Apr 10;256(5054):234-7 PMID: 1566071
  51. A high-mobility-group protein and its cDNAs from Drosophila melanogaster.
    Mol Cell Biol. 1992 May;12(5):1915-23 PMID: 1373803
  52. DNA--protein interactions. HMG has DNA wrapped up.
    Nature. 1992 May 28;357(6376):282-3 PMID: 1589033
  53. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts.
    Cell. 1992 May 29;69(5):759-67 PMID: 1591776
  54. Sequence of a cDNA encoding chicken high-mobility-group protein-2.
    Gene. 1992 May 15;114(2):289-90 PMID: 1601311
  55. Nucleotide sequence of a mouse cDNA encoding the nonhistone chromosomal high mobility group protein-1 (HMG1).
    Nucleic Acids Res. 1992 Jul 11;20(13):3516 PMID: 1630928
  56. Insect proteins homologous to mammalian high mobility group protein 1. Characterization and DNA-binding properties.
    J Biol Chem. 1992 Aug 25;267(24):17170-7 PMID: 1512255
  57. Nucleotide sequence of a mouse cDNA encoding the non-histone chromosomal high mobility group protein-2 (HMG-2)
    Nucleic Acids Res. 1992 Sep 25;20(18):4927 PMID: 1408807
  58. Post-translational cleavage of a histone H1-like protein in the sperm of Mytilus.
    J Biol Chem. 1993 Jan 5;268(1):195-9 PMID: 8416927
  59. Structure of the HMG box motif in the B-domain of HMG1.
    EMBO J. 1993 Apr;12(4):1311-9 PMID: 8467791
  60. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5.
    Nature. 1993 Jul 29;364(6436):412-20 PMID: 8332212
  61. HMG-X, a Xenopus gene encoding an HMG1 homolog, is abundantly expressed in the developing nervous system.
    FEBS Lett. 1994 Sep 26;352(2):191-6 PMID: 7925972
  62. Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA bending.
    EMBO J. 1994 Oct 17;13(20):5002-12 PMID: 7957066
  63. Core histone acetylation does not block linker histone binding to a nucleosome including a Xenopus borealis 5 S rRNA gene.
    J Biol Chem. 1994 Nov 4;269(44):27171-4 PMID: 7961624
  64. Molecular basis of mammalian sexual determination: activation of Müllerian inhibiting substance gene expression by SRY.
    Science. 1994 Dec 2;266(5190):1494-500 PMID: 7985018
  65. The DNA sequence specificity of HMG boxes lies in the minor wing of the structure.
    EMBO J. 1994 Dec 1;13(23):5639-46 PMID: 7988561
  66. Nuclear assembly is independent of linker histones.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12477-81 PMID: 7809061
  67. Prokaryotic HU and eukaryotic HMG1: a kinked relationship.
    Mol Microbiol. 1994 Oct;14(1):1-5 PMID: 7830547
  68. Methylation at CpG sequences does not influence histone H1 binding to a nucleosome including a Xenopus borealis 5 S rRNA gene.
    J Biol Chem. 1995 Mar 3;270(9):4197-200 PMID: 7876175
  69. HMG-D is an architecture-specific protein that preferentially binds to DNA containing the dinucleotide TG.
    EMBO J. 1995 Mar 15;14(6):1264-75 PMID: 7720717
  70. Nucleosomal anatomy--where are the histones?
    Bioessays. 1995 Feb;17(2):161-70 PMID: 7748166
  71. Molecular basis of human 46X,Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex.
    Cell. 1995 Jun 2;81(5):705-14 PMID: 7774012
  72. The HMG-1 box protein family: classification and functional relationships.
    Nucleic Acids Res. 1995 May 11;23(9):1604-13 PMID: 7784217
  73. Activation of the TFIID-TFIIA complex with HMG-2.
    Genes Dev. 1995 Jun 1;9(11):1354-65 PMID: 7797075
  74. Heterogeneity of chromatin subunits in vitro and location of histone H1.
    Nucleic Acids Res. 1976 Feb;3(2):477-92 PMID: 1257057
  75. The organization of histones and DNA in chromatin: evidence for an arginine-rich histone kernel.
    Cell. 1976 Jul;8(3):333-47 PMID: 986252
  76. The presence of high mobility group non-histone chromatin proteins in isolated nucleosomes.
    FEBS Lett. 1977 Jan 15;73(1):85-8 PMID: 838051
  77. Two-dimensional electrophoretic analysis of polynucleosomes.
    J Biol Chem. 1977 Jul 10;252(13):4729-38 PMID: 559672
  78. Reconstitution of chromatin core particles.
    Biochemistry. 1977 Nov 29;16(24):5295-303 PMID: 921932
  79. Evidence for the close proximity of histones H1 and H3 in chromatin of intact nuclei.
    FEBS Lett. 1978 Jul 1;91(1):149-52 PMID: 668905
  80. Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones.
    Biochemistry. 1978 Dec 12;17(25):5524-31 PMID: 728412
  81. Chromatin fractionation procedure that yields nucleosomes containing near-stoichiometric amounts of high mobility group nonhistone chromosomal proteins.
    Biochemistry. 1979 Aug 21;18(17):3739-48 PMID: 476083
  82. Points of contact between histone H1 and the histone octamer.
    Proc Natl Acad Sci U S A. 1980 Jan;77(1):127-31 PMID: 6928607
  83. Isolation and separation of chicken erythrocyte high mobility group non-histone chromatin proteins by chromatography on phosphocellulose.
    FEBS Lett. 1980 Oct 6;119(2):337-42 PMID: 7428950
  84. A comparison of histone variants in different rat tissues.
    Cell Differ. 1980 Dec;9(6):339-50 PMID: 7438214
  85. Transcriptional activation of Xenopus class III genes in chromatin isolated from sperm and somatic nuclei.
    Nucleic Acids Res. 1989 Jan 25;17(2):767-80 PMID: 2915929
  86. Nonhistone proteins HMG1 and HMG2 suppress the nucleosome assembly at physiological ionic strength.
    Biochim Biophys Acta. 1989 Mar 1;1007(2):209-14 PMID: 2465778
  87. A human placental cDNA clone that encodes nonhistone chromosomal protein HMG-1.
    Nucleic Acids Res. 1989 Feb 11;17(3):1197-214 PMID: 2922262
  88. The nonspecific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures.
    Genes Dev. 1993 Aug;7(8):1521-34 PMID: 8339930
  89. 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):6415-9 PMID: 8341648
  90. Absence of somatic histone H1 in oocytes and preblastula embryos of Xenopus laevis.
    Dev Biol. 1993 Aug;158(2):510-22 PMID: 8344467
  91. dHMG-Z, a second HMG-1-related protein in Drosophila melanogaster.
    Nucleic Acids Res. 1993 Sep 11;21(18):4369-71 PMID: 8414994
  92. Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type.
    Dev Biol. 1993 Nov;160(1):214-27 PMID: 8224538
  93. Chromosome condensation in Xenopus mitotic extracts without histone H1.
    Science. 1993 Dec 24;262(5142):2033-5 PMID: 8266099
  94. A positive role for nucleosome mobility in the transcriptional activity of chromatin templates: restriction by linker histones.
    EMBO J. 1995 Aug 1;14(15):3752-65 PMID: 7641694
  95. Two mutations in the HMG-box with very different structural consequences provide insights into the nature of binding to four-way junction DNA.
    EMBO J. 1995 Aug 1;14(15):3844-53 PMID: 7641702
  96. The structure of histone H1 and its location in chromatin.
    Nature. 1980 Dec 25;288(5792):675-9 PMID: 7453800
  97. Circular dichroism, thermal denaturation, and deoxyribonuclease I digestion studies of nucleosomes highly enriched in high mobility group proteins HMG 1 and HMG 2.
    Biochemistry. 1981 Feb 17;20(4):1042-6 PMID: 6260136
  98. Domain structure in high molecular weight high mobility group nonhistone chromatin proteins.
    Nature. 1982 Nov 4;300(5887):76-8 PMID: 6215587
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1996-02-01
Pages
548-61
Language
English
Region
England
NLM ID
8208664
PMCID
PMC449973
Subset
IM
Databases
GENBANK
U21933
External Links
PubMed source PMC Full Text View journal details
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