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The distribution of somatic H1 subtypes is non-random on active vs. inactive chromatin: Distribution in human fetal fibroblasts

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Abstract

Chromatin immunoprecipitation was employed to determine whether or not the previously reported depletion of histone H1 on actively transcribed sequences was selective with respect to H1 subtypes. DNA of immunofractionated chromatin was analyzed by slot-blots for repetitive sequences and PCR for single and low-copy sequences. Based on the analysis of a diverse set of sequences, we report distinct differences in subtype distributions. Actively transcribed chromatin, as well as chromatin poised for transcription, is characterized by a relative depletion of somatic H1 subtypes 2 and 4 (H1s-2 and H1s-4), whereas facultative and constitutive heterochromatin contain all four somatic subtypes. These results support a model in which subtypes are selectively depleted upon gene expression. In turn, the data also support the possibility that the somatic subtypes have different functional roles based on their selective depletion from different classes of DNA sequences.

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References

  • Brandt WF, Von Holt C (1986) Variants of wheat histone H1 and N-and C-terminal extensions. FEBS Let 194: 282–286.

    Article  CAS  Google Scholar 

  • Brown DT, Alexander BT, Sittman DB (1996) Differential effect of H1 variant overexpression on cell cycle progression and gene expression. Nucl Acids Res 24: 486–493.

    Article  PubMed  CAS  Google Scholar 

  • Burfeind P, Hoyer-Fender S, Doenecke D, Tsaousidou S, Engel W (1992) Expression of a histone H1 gene (H1.1) in human testis and Hassall's corpuscles of the thymus. Thymus 19: 245–251.

    PubMed  CAS  Google Scholar 

  • Chadee DN, Taylor WR, Hurta RAR, Allis CD, Wright JA, Davie JR (1995) Increased phosphorylation of histone H1 in mouse fibroblasts transformed with oncogenes or constitutively active mitogen-activated protein kinase kinase. J Biol Chem 270: 20098–20105.

    Article  PubMed  CAS  Google Scholar 

  • Chaurasia P, Mukherjee S, Thakur MK (1996) Age-related analysis of EcoRI generated satellite DNA-containing chromatin of rat liver. Biochem Molec Biol Intr 40: 1261–1270.

    CAS  Google Scholar 

  • Cole MD (1986) The myc oncogene: Its role in transformation and differentiation. Ann Rev Genet 20: 361–384.

    Article  PubMed  CAS  Google Scholar 

  • Cole RD (1987) Microheterogeneity in H1 histones and its consequences. Int J Peptide Protein Res 30: 433–449.

    Article  CAS  Google Scholar 

  • D'Erme M, Zardo G, Reale A, Caiafa P (1996) Co-operative interactions of oligonucleosomal DNA with the H1e histone variant and its poly(ADP-ribosyl)ated isoform. Biochem J 316: 475–480.

    PubMed  Google Scholar 

  • Dedon PC, Soults JA, Allis CD, Gorovsky MA (1991a) A simplified formaldehyde fixation and immunoprecipitation technique for studying protein-DNA interactions. Anal Biochem 197: 83–90.

    Article  PubMed  CAS  Google Scholar 

  • Dedon PC, Soults JA, Allis CD, Gorovsky MA (1991b) For-maldehyde cross-linking and immunoprecipitation demon-strate developmental changes in H1 association with transcriptionally active genes. Mol Cell Biol 11: 1729–1733.

    PubMed  CAS  Google Scholar 

  • D'Incalci M, Paola A, Wu RS, Bonner WM (1986) H1 variant synthesis in proliferating and quiescent human cells. Eur J Biochem 154: 273–279.

    Article  PubMed  Google Scholar 

  • Erba HP, Eddy R, Shows T, Kedes L, Gunning P (1988) Structure, chromosome location and expression of the human gamma-actin gene: Differential evolution, location and expression of the cytoskeletal beta-and gamma-actin genes. Mol Cell Biol 8: 1775–1789.

    PubMed  CAS  Google Scholar 

  • Franke K, Drabent B, Doenecke D (1998) Expression of murine H1 histone genes during postnatal development. Biochim Biophys Acta 1389: 232–242.

    Google Scholar 

  • Goldman MA, Holmquist GP, Gray MC, Caston LA, Nag A (1984) Replication timing of genes and middle repetitive sequences. Science 224: 686–692.

    PubMed  CAS  Google Scholar 

  • Gunning P, Ponte P, Okayama H, Engel J, Blau H, Kedes L (1983) Isolation and characterization of full-length cDNA clones for human α-, β-, and γ-actin mRNAs: Skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed. Mol Cell Biol 3: 787–795.

    PubMed  CAS  Google Scholar 

  • Hanauer A, Mandel JL (1984) The glyceraldehyde 3 phosphate dehydrogenase gene family: Structure of a human cDNA and of an X chromosome linked pseudogene; amazing complexity of the gene family in mouse. EMBO J 3: 2627–2633.

    PubMed  CAS  Google Scholar 

  • Hannon R, Bateman E, Allan J, Harborne N, Gould H (1984) Control of RNA polymerase binding to chromatin by variations in linker histone composition. J Mol Biol 180: 131–149.

    Article  PubMed  CAS  Google Scholar 

  • Hebbes TR, Thorne AW, Crane-Robinson C (1988) A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J 7: 1395–1402.

    PubMed  CAS  Google Scholar 

  • Hickey E, Brandon SE, Smale G, Lloyd D, Weber LA (1989) Sequence and regulation of a gene encoding a human 89–kilodalton heat shock protein. Mol Cell Biol 9: 2615–2626.

    PubMed  CAS  Google Scholar 

  • Hieter PA, Max EE, Seidman JG, Maizel JV Jr, Leder P (1980) Cloned human and mouse kappa immunoglobulin constant and J region genes conserve homology in functional segments. Cell 22: 197–207.

    Article  PubMed  CAS  Google Scholar 

  • Higurashi M, Adachi H, Ohba Y (1987) Synthesis and degra-dation of H1 histone subtypes in mouse lymphoma L5178Y cells. J Biol Chem 262: 13075–13080.

    PubMed  CAS  Google Scholar 

  • Huang H-C, Cole RD (1984) The distribution of H1 histone is nonuniform in chromatin and correlates with different degrees of condensation. J Biol Chem 259: 14237–14242.

    PubMed  CAS  Google Scholar 

  • Jackson V, Chalkley R (1981) A new method for the isolation of replicative chromatin: Selective deposition of histone on both new and old DNA. Cell 23: 121–134.

    Article  PubMed  CAS  Google Scholar 

  • Kaludov NK, Pabon-Pena L, Seavy M, Robinson G, Hurt MM (1997) A mouse histone H1 variant, H1b, binds preferentially to a regulatory sequence within a mouse H3.2 replication-dependent histone gene. J Biol Chem 272: 15120–15127.

    Article  PubMed  CAS  Google Scholar 

  • Kamakaka RT, Thomas JO (1990) Chromatin structure of transcriptionally competent and repressed genes. EMBO J 9 3997–4006.

    PubMed  CAS  Google Scholar 

  • Kandolf H (1994) The H1A histone variant is an in-vivo repressor of oocyte-type 5S gene transcription in Xenopus laevis embryos. Proc Natl Acad Sci USA 91: 7257–7261.

    Article  PubMed  CAS  Google Scholar 

  • Khochbin S, Wolffe AP (1994) Developmentally regulated expression of linker-histone variants in vertebrates. Eur J Biochem 225: 501–510.

    Article  PubMed  CAS  Google Scholar 

  • Lennox RW, Cohen LH (1983) The histone H1 complements of dividing and nondividing cells of the mouse. J Biol Chem 258: 262–268.

    PubMed  CAS  Google Scholar 

  • Lennox RW(1984) Differences in evolutionary stability among mammalian H1 subtypes: Implications for the roles of H1 subtypes in chromatin. J Biol Chem 259: 669–672.

    PubMed  CAS  Google Scholar 

  • Liao LW, Cole RD (1981) Condensation of dinucleosomes by individual subfractions of H1 histone. J Biol Chem 256: 10124–10128.

    PubMed  CAS  Google Scholar 

  • Liu AYC, Bae-Lee MS, Choi H-S, Li B (1989) Heat shock induction of HSP89 is regulated in cellular aging. Biochim Biophys Acta 162: 1302–1310.

    CAS  Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Meergans T, Albig W, Doenecke D (1997) Varied expression patterns of human H1 histone genes in different cell lines. DNA Cell Biol 16: 1041–1049.

    Article  PubMed  CAS  Google Scholar 

  • Meyne J, Baker RJ, Hobart HH et al. (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99: 3–10.

    Article  PubMed  CAS  Google Scholar 

  • Mohr E, Trieschmann L, Grossbach U (1989) Histone H1 in two subspecies of Chironomus thummi with different genome sizes: Homologous chromosome sites differ largely in their content of a specific H1 variant. Proc Natl Acad Sci USA 86: 9308–9312.

    Article  PubMed  CAS  Google Scholar 

  • Moyzis RK, Buckingham JM, Cram LS et al. (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA 85: 6622–6626.

    Article  PubMed  CAS  Google Scholar 

  • Orlando V, Paro R (1993) Mapping polycomb-repressed domains in the bithorax complex using in vivo formaldehyde cross-linked chromatin. Cell 75: 1187–1198.

    Article  PubMed  CAS  Google Scholar 

  • Ozawa K, Murakami Y, Eki T, Soeda E, Yokoyama K (1992) Mapping of the gene family for human heat-shock protein 90α to chromosomes 1, 4, 11, and 14. Genomics 12: 214–220.

    Article  PubMed  CAS  Google Scholar 

  • Panetta G, Buttinelli M, Flaus A, Richmond TJ, Rhodes D (1998) Differential nucleosome positioning on Xenopus oocyte and somatic 5S RNA genes determines both TFIIIA and H1 binding: A mechanism for selective H1 repression. J Mol Biol 282: 683–697.

    Article  PubMed  CAS  Google Scholar 

  • Parseghian MH, Clark RF, Hauser LJ, Dvorkin N, Harris DA, Hamkalo BA (1993) Fractionation of human H1 subtypes and characterization of a subtype-specific antibody exhibiting non-uniform nuclear staining. Chromosome Res 1: 127–139.

    Article  PubMed  CAS  Google Scholar 

  • Parseghian MH, Henschen AH, Krieglstein KG, Hamkalo BA (1994a) A proposal for a coherent mammalian histone H1 nomenclature correlated with amino acid sequences. Protein Sci 3: 575–587.

    Article  PubMed  CAS  Google Scholar 

  • Parseghian MH, Harris DA, Rishwain DR, Hamkalo BA (1994b) Characterization of a set of antibodies specific for three human histone H1 subtypes. Chromosoma 103: 198–208.

    PubMed  CAS  Google Scholar 

  • Pehrson JR, Cole RD (1982) Histone H1 subfractions and H1° turnover at different rates in nondividing cells. Biochemistry 21: 456–460.

    Article  PubMed  CAS  Google Scholar 

  • Pina B, Martinez P, Suau P (1987) Changes in H1 complement in differentiating rat-brain cortical neurons. Eur J Biochem 164: 71–76.

    Article  PubMed  CAS  Google Scholar 

  • Ponte I, Vidal-Taboada JM, Suau P (1998) Evolution of the vertebrate H1 histone class: Evidence for the functional differentiation of the subtypes. Mol Biol Evol 15: 702–708.

    PubMed  CAS  Google Scholar 

  • Riquelme PT, Burzio LO, Koide SS (1979) ADP ribosylation of rat liver lysine-rich histone in vitro. J Biol Chem 254: 3018–3028.

    PubMed  CAS  Google Scholar 

  • Roche J, Gorka C, Goeltz P, Lawrence JJ (1985) Association of histone H1° with a gene repressed during liver development. Nature 314: 197–198.

    Article  PubMed  CAS  Google Scholar 

  • Schlissel MS, Brown DD (1984) The transcriptional regulation of Xenopus 5S RNA genes in chromatin: The roles of active stable transcription complexes and histone H1. Cell 37: 903–913.

    Article  PubMed  CAS  Google Scholar 

  • Schulze E, Trieschmann L, Schulze B et al. (1993) Structural and functional differences between histone H1 sequence variants with differential intranuclear distribution. Proc Natl Acad Sci USA 90: 2481–2485.

    Article  PubMed  CAS  Google Scholar 

  • Schulze E, Nagel S, Gavenis K, Grossbach U (1994) Structurally divergent histone H1 variants in chromosomes containing highly condensed interphase chromatin. J Cell Biol 127: 1789–1798.

    Article  PubMed  CAS  Google Scholar 

  • Seguchi K, Takami Y, Nakayama T (1995) Targeted disruption of 01H1 encoding a particular H1 histone variant causes changes in protein patterns in the DT40 chicken B cell line. J Mol Biol 254: 869–880.

    Article  PubMed  CAS  Google Scholar 

  • Sera T, Wolffe AP (1998) Role of histone H1 as an architectural determinant of chromatin structure and as a specific repressor of transcription on Xenopus oocyte 5S rRNA genes. Mol Cell Biol 18: 3668–3680.

    PubMed  CAS  Google Scholar 

  • Seyedin SM, Cole RD, Kistler WS (1981) Histones from mammalian testes: The widespread occurrence of H1t. Exp Cell Res 136: 399–405.

    Article  PubMed  CAS  Google Scholar 

  • Sirotkin AM, Edelmann W, Cheng G, Klein-Szanto A, Kucherlapati R, Skoultchi AI (1995) Mice develop normally without the H1° linker histone. Proc Natl Acad Sci USA 92: 6434–6438.

    Article  PubMed  CAS  Google Scholar 

  • Smith RC, Dworkin-Rastl E, Dworkin MB (1988) Expression of a histone H1–like protein is restricted to early Xenopus development. Genes Dev 2: 1284–1295.

    PubMed  CAS  Google Scholar 

  • Solomon MJ, Larsen PL, Varshavsky AJ (1988) Mapping protein-DNA interactions in vivo with formaldehyde: Evidence that histone H4 is retained on a highly transcribed gene. Cell 53: 937–947.

    Article  PubMed  CAS  Google Scholar 

  • Stathakis DG, Hoover KB, You Z, Bryant PJ (1997) Human postsynaptic density-95 (PSD95): Location of the gene (DLG4) and possible function in nonneural, as well as in neural tissues. Genomics 44: 71–82.

    Article  PubMed  CAS  Google Scholar 

  • Takami Y, Nakayama T (1997) A single copy of linkerH1 genes is enough for proliferation of the DT40 chicken B cell line, and linker H1 variants participate in regulation of gene expression. Genes Cells 2: 711–723.

    Article  PubMed  CAS  Google Scholar 

  • Takami Y, Takeda S, Nakayama T (1997) An approximately half set of histone genes is enough for cell proliferation and a lack of several histone variants causes protein pattern changes in the DT40 chicken B cell line. J Mol Biol 265: 394–408.

    Article  PubMed  CAS  Google Scholar 

  • Talasz H, Helliger W, Puschendorf B, Lindner H (1996) In vivo phosphorylation of histone H1 variants during the cell cycle. Biochemistry 35: 1761–1767.

    Article  PubMed  CAS  Google Scholar 

  • Talasz H, Sapojnikova N, Helliger W, Lindner H, Puschendorf B (1998) In vitro binding of H1 histone subtypes to nucleosomal organized mouse mammary tumor virus long terminal repeat promotor. J Biol Chem 273: 32236–32243.

    Article  PubMed  CAS  Google Scholar 

  • Thompson LM, Plummer S, Schalling M et al. (1991) A gene encoding a fibroblast growth factor receptor isolated from the Huntington disease gene region of human chromosome 4. Genomics 11: 1133–1142.

    Article  PubMed  CAS  Google Scholar 

  • Tischfield J, Schafer IA, Dickerman LH et al. (1979) Lesch-Nyhan syndrome. Cytogenet Cell Genet 24: 199–200.

    PubMed  CAS  Google Scholar 

  • Travis A, Amsterdam A, Belanger C, Grosschedl R (1991) Lef-1, a gene encoding a lymphoid-specific protein, with an HMG domain, regulates T-cell receptor Cα enhancer function. Genes Dev 5: 880–894.

    PubMed  CAS  Google Scholar 

  • Vam vakopoulos NC, Griffin CA, Hawkins AL, Lee C, Chrousos GP, Wang-Jabs E (1993) Mapping the intron-containing human hsp 90α (HSPCAL4) gene to chromosome band 14p32. Cytogenet Cell Genet 64: 224–226.

    Article  CAS  Google Scholar 

  • van Deutekom JCT, Wijmenga C, van Tienhoven EAE et al. (1993) FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit. Hum Mol Genet 2: 2037–2042.

    PubMed  CAS  Google Scholar 

  • Vermaak D, Steinbach OC, Dimitrov S, Rupp RAW, Wolffe AP (1998) The globular domain of histone H1 is sufficient to direct specific gene repression in early Xenopus embryos. Curr Biol 8: 533–536.

    Article  PubMed  CAS  Google Scholar 

  • Wang Z-F, Sirotkin AM, Buchold GM, Skoultchi AI, Marzluff WF (1997) The mouse histone H1 genes: Gene organization and differential regulation. J Mol Biol 271: 124–138.

    Article  PubMed  CAS  Google Scholar 

  • Waterman ML, Fischer WH, Jones KA (1991) A thymus-specific member of the HMG protein family regulates the human T-cell receptor CCα enhancer. Genes Dev 5: 656–669.

    PubMed  CAS  Google Scholar 

  • Weintraub H (1984) Histone-H1–dependent chromatin superstructures and the suppression of gene activity. Cell 38: 17–27.

    Article  PubMed  CAS  Google Scholar 

  • Winokur ST, Bengtsson U, Feddersen J et al. (1994) The DNA rearrangement associated with facioscapulohumeral muscular dystrophy involves a heterochromatin-associated repetitive element: Implications for a role of chromatin structure in the pathogenesis of the disease. Chromosome Res 2: 225–234.

    Article  PubMed  CAS  Google Scholar 

  • Yang TP, Hansen SK, Oishi KK, Ryder OA, Hamkalo BA (1982) Characterization of a cloned repetitive DNA sequence concentrated on the human X chromosome. Proc Natl Acad Sci USA 79: 6593–6597.

    Article  PubMed  CAS  Google Scholar 

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Parseghian, M.H., Newcomb, R.L., Winokur, S.T. et al. The distribution of somatic H1 subtypes is non-random on active vs. inactive chromatin: Distribution in human fetal fibroblasts. Chromosome Res 8, 405–424 (2000). https://doi.org/10.1023/A:1009262819961

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