Skip to main content
Protein Science : A Publication of the Protein Society logoLink to Protein Science : A Publication of the Protein Society
. 1994 Apr;3(4):575–587. doi: 10.1002/pro.5560030406

A proposal for a coherent mammalian histone H1 nomenclature correlated with amino acid sequences.

M H Parseghian 1, A H Henschen 1, K G Krieglstein 1, B A Hamkalo 1
PMCID: PMC2142865  PMID: 8003976

Abstract

Bio-Rex 70 chromatography was combined with reverse-phase (RP) HPLC to fractionate histone H1 zero and 4 histone H1 subtypes from human placental nuclei as previously described (Parseghian MH et al., 1993, Chromosome Res 1:127-139). After proteolytic digestion of the subtypes with Staphylococcus aureus V8 protease, peptides were fractionated by RP-HPLC and partially sequenced by Edman degradation in order to correlate them with human spleen subtypes (Ohe Y, Hayashi H, Iwai K, 1986, J Biochem (Tokyo) 100:359-368; 1989, J Biochem (Tokyo) 106:844-857). Based on comparisons with the sequence data available from other mammalian species, subtypes were grouped. These groupings were used to construct a coherent nomenclature for mammalian somatic H1s. Homologous subtypes possess characteristic patterns of growth-related and cAMP-dependent phosphorylation sites. The groupings defined by amino acid sequence also were used to correlate the elution profiles and electrophoretic mobilities of subtypes derived from different species. Previous attempts at establishing an H1 nomenclature by chromatographic or electrophoretic fractionations has resulted in several misidentifications. We present here, for the first time, a nomenclature for somatic H1s based on amino acid sequences that are analogous to those for H1 zero and H1t. The groupings defined should be useful in correlating the many observations regarding H1 subtypes in the literature.

Full Text

The Full Text of this article is available as a PDF (5.0 MB).

Selected References

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

  1. Ajiro K., Borun T. W., Cohen L. H. Phosphorylation states of different histone 1 subtypes and their relationship to chromatin functions during the HeLa S-3 cell cycle. Biochemistry. 1981 Mar 17;20(6):1445–1454. doi: 10.1021/bi00509a007. [DOI] [PubMed] [Google Scholar]
  2. Ajiro K., Borun T. W., Shulman S. D., McFadden G. M., Cohen L. H. Comparison of the structures of human histone 1A and 1B and their intramolecular phosphorylation sites during the HeLa S-3 cell cycle. Biochemistry. 1981 Mar 17;20(6):1454–1464. doi: 10.1021/bi00509a008. [DOI] [PubMed] [Google Scholar]
  3. Ajiro K., Shibata K., Nishikawa Y. Subtype-specific cyclic AMP-dependent histone H1 phosphorylation at the differentiation of mouse neuroblastoma cells. J Biol Chem. 1990 Apr 15;265(11):6494–6500. [PubMed] [Google Scholar]
  4. Albig W., Kardalinou E., Drabent B., Zimmer A., Doenecke D. Isolation and characterization of two human H1 histone genes within clusters of core histone genes. Genomics. 1991 Aug;10(4):940–948. doi: 10.1016/0888-7543(91)90183-f. [DOI] [PubMed] [Google Scholar]
  5. Allis C. D., Allen R. L., Wiggins J. C., Chicoine L. G., Richman R. Proteolytic processing of h1-like histones in chromatin: a physiologically and developmentally regulated event in Tetrahymena micronuclei. J Cell Biol. 1984 Nov;99(5):1669–1677. doi: 10.1083/jcb.99.5.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bartley J., Chalkley R. Further studies of a thymus nucleohistone-associated protease. J Biol Chem. 1970 Sep 10;245(17):4286–4292. [PubMed] [Google Scholar]
  7. Baubichon-Cortay H., Mallet L., Denoroy L., Roux B. Histone H1a subtype presents structural differences compared to other histone H1 subtypes. Evidence for a specific motif in the C-terminal domain. Biochim Biophys Acta. 1992 Jul 31;1122(2):167–177. doi: 10.1016/0167-4838(92)90320-d. [DOI] [PubMed] [Google Scholar]
  8. Burfeind P., Hoyer-Fender S., Doenecke D., Tsaousidou S., Engel W. Expression of a histone H1 gene (H1.1) in human testis and Hassall's corpuscles of the thymus. Expression of a histone H1 gene (H1.1). Thymus. 1992 Jun;19(4):245–251. [PubMed] [Google Scholar]
  9. Carozzi N., Marashi F., Plumb M., Zimmerman S., Zimmerman A., Coles L. S., Wells J. R., Stein G., Stein J. Clustering of human H1 and core histone genes. Science. 1984 Jun 8;224(4653):1115–1117. doi: 10.1126/science.6719136. [DOI] [PubMed] [Google Scholar]
  10. Chae C. B., Godski R. A., Carter D. B., Efird P. H. Integrity of proteins in reconstituted chromatin. Biochem Biophys Res Commun. 1975 Dec 15;67(4):1459–1465. doi: 10.1016/0006-291x(75)90190-4. [DOI] [PubMed] [Google Scholar]
  11. Cheng G. H., Nandi A., Clerk S., Skoultchi A. I. Different 3'-end processing produces two independently regulated mRNAs from a single H1 histone gene. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7002–7006. doi: 10.1073/pnas.86.18.7002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Churchill M. E., Travers A. A. Protein motifs that recognize structural features of DNA. Trends Biochem Sci. 1991 Mar;16(3):92–97. doi: 10.1016/0968-0004(91)90040-3. [DOI] [PubMed] [Google Scholar]
  13. Clark R. F., Cho K. W., Weinmann R., Hamkalo B. A. Preferential distribution of active RNA polymerase II molecules in the nuclear periphery. Gene Expr. 1991 Apr;1(1):61–70. [PMC free article] [PubMed] [Google Scholar]
  14. Cole K. D., Kandala J. C., Kremer E., Kistler W. S. Isolation of a genomic clone encoding the rat histone variant, H1d. Gene. 1990 May 14;89(2):265–269. doi: 10.1016/0378-1119(90)90015-j. [DOI] [PubMed] [Google Scholar]
  15. Cole R. D. A minireview of microheterogeneity in H1 histone and its possible significance. Anal Biochem. 1984 Jan;136(1):24–30. doi: 10.1016/0003-2697(84)90303-8. [DOI] [PubMed] [Google Scholar]
  16. Cole R. D. Microheterogeneity in H1 histones and its consequences. Int J Pept Protein Res. 1987 Oct;30(4):433–449. doi: 10.1111/j.1399-3011.1987.tb03352.x. [DOI] [PubMed] [Google Scholar]
  17. Cole R. D. Purification and analysis of H1 histones. Methods Enzymol. 1989;170:524–532. doi: 10.1016/0076-6879(89)70062-8. [DOI] [PubMed] [Google Scholar]
  18. D'Incalci M., Allavena P., Wu R. S., Bonner W. M. H1 variant synthesis in proliferating and quiescent human cells. Eur J Biochem. 1986 Jan 15;154(2):273–279. doi: 10.1111/j.1432-1033.1986.tb09393.x. [DOI] [PubMed] [Google Scholar]
  19. Doenecke D., Tönjes R. Differential distribution of lysine and arginine residues in the closely related histones H1 and H5. Analysis of a human H1 gene. J Mol Biol. 1986 Feb 5;187(3):461–464. doi: 10.1016/0022-2836(86)90446-8. [DOI] [PubMed] [Google Scholar]
  20. Domínguez V., Piña B., Suau P. Histone H1 subtype synthesis in neurons and neuroblasts. Development. 1992 May;115(1):181–185. doi: 10.1242/dev.115.1.181. [DOI] [PubMed] [Google Scholar]
  21. Eick S., Nicolai M., Mumberg D., Doenecke D. Human H1 histones: conserved and varied sequence elements in two H1 subtype genes. Eur J Cell Biol. 1989 Jun;49(1):110–115. [PubMed] [Google Scholar]
  22. Gabrielli F., Tsugita A. H1(0) histones of normal and cancer human cells. Amino acid composition of H1 purified by polyacrylamide gel electrophoresis. Mol Cell Biochem. 1986 Aug;71(2):129–134. doi: 10.1007/BF00214771. [DOI] [PubMed] [Google Scholar]
  23. Giancotti V., Bandiera A., Ciani L., Santoro D., Crane-Robinson C., Goodwin G. H., Boiocchi M., Dolcetti R., Casetta B. High-mobility-group (HMG) proteins and histone H1 subtypes expression in normal and tumor tissues of mouse. Eur J Biochem. 1993 Apr 15;213(2):825–832. doi: 10.1111/j.1432-1033.1993.tb17825.x. [DOI] [PubMed] [Google Scholar]
  24. Goldman M. A., Holmquist G. P., Gray M. C., Caston L. A., Nag A. Replication timing of genes and middle repetitive sequences. Science. 1984 May 18;224(4650):686–692. doi: 10.1126/science.6719109. [DOI] [PubMed] [Google Scholar]
  25. Helliger W., Lindner H., Grübl-Knosp O., Puschendorf B. Alteration in proportions of histone H1 variants during the differentiation of murine erythroleukaemic cells. Biochem J. 1992 Dec 15;288(Pt 3):747–751. doi: 10.1042/bj2880747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Higurashi M., Adachi H., Ohba Y. Synthesis and degradation of H1 histone subtypes in mouse lymphoma L5178Y cells. J Biol Chem. 1987 Sep 25;262(27):13075–13080. [PubMed] [Google Scholar]
  27. Hill C. S., Rimmer J. M., Green B. N., Finch J. T., Thomas J. O. Histone-DNA interactions and their modulation by phosphorylation of -Ser-Pro-X-Lys/Arg- motifs. EMBO J. 1991 Jul;10(7):1939–1948. doi: 10.1002/j.1460-2075.1991.tb07720.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hoyer-Fender S., Grossbach U. Histone H1 heterogeneity in the midge, Chironomus thummi. Structural comparison of the H1 variants in an organism where their intrachromosomal localization is possible. Eur J Biochem. 1988 Sep 1;176(1):139–152. doi: 10.1111/j.1432-1033.1988.tb14261.x. [DOI] [PubMed] [Google Scholar]
  29. Hutchison N., Weintraub H. Localization of DNAase I-sensitive sequences to specific regions of interphase nuclei. Cell. 1985 Dec;43(2 Pt 1):471–482. doi: 10.1016/0092-8674(85)90177-1. [DOI] [PubMed] [Google Scholar]
  30. Kinkade J. M., Jr, Cole R. D. The resolution of four lysine-rich histones derived from calf thymus. J Biol Chem. 1966 Dec 25;241(24):5790–5797. [PubMed] [Google Scholar]
  31. Krystosek A., Puck T. T. The spatial distribution of exposed nuclear DNA in normal, cancer, and reverse-transformed cells. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6560–6564. doi: 10.1073/pnas.87.17.6560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. La Bella F., Zhong R., Heintz N. Cell type-specific expression of a human histone H1 gene. J Biol Chem. 1988 Feb 15;263(5):2115–2118. [PubMed] [Google Scholar]
  33. 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]
  34. Langan T. A. Characterization of highly phosphorylated subcomponents of rat thymus H1 histone. J Biol Chem. 1982 Dec 25;257(24):14835–14846. [PubMed] [Google Scholar]
  35. Langan T. A. Phosphorylation of liver histone following the administration of glucagon and insulin. Proc Natl Acad Sci U S A. 1969 Dec;64(4):1276–1283. doi: 10.1073/pnas.64.4.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Lennox R. W. Differences in evolutionary stability among mammalian H1 subtypes. Implications for the roles of H1 subtypes in chromatin. J Biol Chem. 1984 Jan 10;259(1):669–672. [PubMed] [Google Scholar]
  38. Lennox R. W., Oshima R. G., Cohen L. H. The H1 histones and their interphase phosphorylated states in differentiated and undifferentiated cell lines derived from murine teratocarcinomas. J Biol Chem. 1982 May 10;257(9):5183–5189. [PubMed] [Google Scholar]
  39. Liao L. W., Cole R. D. Condensation of dinucleosomes by individual subfractions of H1 histone. J Biol Chem. 1981 Oct 10;256(19):10124–10128. [PubMed] [Google Scholar]
  40. Liao L. W., Cole R. D. Differences among H1 histone subfractions in binding to linear and superhelical DNA. Sedimentation velocity studies. J Biol Chem. 1981 Nov 10;256(21):11145–11150. [PubMed] [Google Scholar]
  41. Liao L. W., Cole R. D. Differences among subfractions of H1 histone in their interactions with linear and superhelical DNA. Circular dichroism. J Biol Chem. 1981 Jul 10;256(13):6751–6755. [PubMed] [Google Scholar]
  42. Lindner H., Helliger W., Puschendorf B. Separation of rat tissue histone H1 subtypes by reverse-phase h.p.l.c. Identification and assignment to a standard H1 nomenclature. Biochem J. 1990 Jul 15;269(2):359–363. doi: 10.1042/bj2690359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Macleod A. R., Wong N. C., Dixon G. H. The amino-acid sequence of trout-testis histone H1. Eur J Biochem. 1977 Aug 15;78(1):281–291. doi: 10.1111/j.1432-1033.1977.tb11739.x. [DOI] [PubMed] [Google Scholar]
  44. Ogata N., Ueda K., Kagamiyama H., Hayaishi O. ADP-ribosylation of histone H1. Identification of glutamic acid residues 2, 14, and the COOH-terminal lysine residue as modification sites. J Biol Chem. 1980 Aug 25;255(16):7616–7620. [PubMed] [Google Scholar]
  45. Ohba Y., Higurashi M., Hayashi Y. Phosphorylation of H1 subtypes in regenerating rat liver. J Biol Chem. 1984 Mar 10;259(5):2942–2948. [PubMed] [Google Scholar]
  46. Ohe Y., Hayashi H., Iwai K. Human spleen histone H1. Isolation and amino acid sequences of three minor variants, H1a, H1c, and H1d. J Biochem. 1989 Nov;106(5):844–857. doi: 10.1093/oxfordjournals.jbchem.a122941. [DOI] [PubMed] [Google Scholar]
  47. Parseghian M. H., Clark R. F., Hauser L. J., Dvorkin N., Harris D. A., Hamkalo B. A. Fractionation of human H1 subtypes and characterization of a subtype-specific antibody exhibiting non-uniform nuclear staining. Chromosome Res. 1993 Jul;1(2):127–139. doi: 10.1007/BF00710036. [DOI] [PubMed] [Google Scholar]
  48. Pehrson J. R., Cohen L. H. Distribution of histone H1 alpha among cells of the sea urchin embryo. Dev Biol. 1985 Oct;111(2):530–533. doi: 10.1016/0012-1606(85)90506-8. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Piña B., Martínez P., Suau P. Changes in H1 complement in differentiating rat-brain cortical neurons. Eur J Biochem. 1987 Apr 1;164(1):71–76. doi: 10.1111/j.1432-1033.1987.tb10994.x. [DOI] [PubMed] [Google Scholar]
  51. Puck T. T., Bartholdi M., Krystosek A., Johnson R., Haag M. Confocal microscopy of genome exposure in normal, cancer, and reverse-transformed cells. Somat Cell Mol Genet. 1991 Sep;17(5):489–503. doi: 10.1007/BF01233173. [DOI] [PubMed] [Google Scholar]
  52. Rasheed B. K., Whisenant E. C., Ghai R. D., Papaioannou V. E., Bhatnagar Y. M. Biochemical and immunocytochemical analysis of a histone H1 variant from the mouse testis. J Cell Sci. 1989 Sep;94(Pt 1):61–71. doi: 10.1242/jcs.94.1.61. [DOI] [PubMed] [Google Scholar]
  53. Riquelme P. T., Burzio L. O., Koide S. S. ADP ribosylation of rat liver lysine-rich histone in vitro. J Biol Chem. 1979 Apr 25;254(8):3018–3028. [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. 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]
  56. Seyedin S. M., Kistler W. S. H1 histone subfractions of mammalian testes. 1. Organ specificity in the rat. Biochemistry. 1979 Apr 3;18(7):1371–1375. doi: 10.1021/bi00574a038. [DOI] [PubMed] [Google Scholar]
  57. Seyedin S. M., Kistler W. S. H1 histone subfractions of mammalian testes. 2. Organ specificity in mice and rabbits. Biochemistry. 1979 Apr 3;18(7):1376–1379. doi: 10.1021/bi00574a039. [DOI] [PubMed] [Google Scholar]
  58. Seyedin S. M., Kistler W. S. Isolation and characterization of rat testis H1t. An H1 histone variant associated with spermatogenesis. J Biol Chem. 1980 Jun 25;255(12):5949–5954. [PubMed] [Google Scholar]
  59. Shetty K. T., Link W. T., Pant H. C. cdc2-like kinase from rat spinal cord specifically phosphorylates KSPXK motifs in neurofilament proteins: isolation and characterization. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6844–6848. doi: 10.1073/pnas.90.14.6844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Shibata K., Ajiro K. Cell cycle-dependent suppressive effect of histone H1 on mitosis-specific H3 phosphorylation. J Biol Chem. 1993 Sep 5;268(25):18431–18434. [PubMed] [Google Scholar]
  61. Sizemore S. R., Cole R. D. Asynchronous appearance of newly synthesized histone H1 subfractions in HeLa chromatin. J Cell Biol. 1981 Aug;90(2):415–417. doi: 10.1083/jcb.90.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Smerdon M. J., Isenberg I. Conformational changes in subfractions of calf thymus histone H1. Biochemistry. 1976 Sep 21;15(19):4233–4242. doi: 10.1021/bi00664a016. [DOI] [PubMed] [Google Scholar]
  63. Suzuki M. SPKK, a new nucleic acid-binding unit of protein found in histone. EMBO J. 1989 Mar;8(3):797–804. doi: 10.1002/j.1460-2075.1989.tb03440.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Talasz H., Helliger W., Puschendorf B., Lindner H. G1- and S-phase synthesis of histone H1 subtypes from mouse NIH fibroblasts and rat C6 glioma cells. Biochemistry. 1993 Feb 2;32(4):1188–1193. doi: 10.1021/bi00055a025. [DOI] [PubMed] [Google Scholar]
  65. 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]
  66. Wells D. E. Compilation analysis of histones and histone genes. Nucleic Acids Res. 1986;14 (Suppl):r119–r149. doi: 10.1093/nar/14.suppl.r119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. 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]
  68. Winter E., Levy D., Gordon J. S. Changes in the H-1 histone complement during myogenesis. I. Establishment by differential coupling of H-1 species synthesis to DNA replication. J Cell Biol. 1985 Jul;101(1):167–174. doi: 10.1083/jcb.101.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. 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]
  70. Yang Y. S., Brown D. T., Wellman S. E., Sittman D. B. Isolation and characterization of a mouse fully replication-dependent H1 gene within a genomic cluster of core histone genes. J Biol Chem. 1987 Dec 15;262(35):17118–17125. [PubMed] [Google Scholar]
  71. de Murcia G., Huletsky A., Lamarre D., Gaudreau A., Pouyet J., Daune M., Poirier G. G. Modulation of chromatin superstructure induced by poly(ADP-ribose) synthesis and degradation. J Biol Chem. 1986 May 25;261(15):7011–7017. [PubMed] [Google Scholar]

Articles from Protein Science : A Publication of the Protein Society are provided here courtesy of The Protein Society

RESOURCES