Skip to main content
Log in

Germline-specific H1 variants: the “sexy” linker histones

  • Review
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

The eukaryotic genome is packed into chromatin, a nucleoprotein complex mainly formed by the interaction of DNA with the abundant basic histone proteins. The fundamental structural and functional subunit of chromatin is the nucleosome core particle, which is composed by 146 bp of DNA wrapped around an octameric protein complex formed by two copies of each core histone H2A, H2B, H3, and H4. In addition, although not an intrinsic component of the nucleosome core particle, linker histone H1 directly interacts with it in a monomeric form. Histone H1 binds nucleosomes near the exit/entry sites of linker DNA, determines nucleosome repeat length and stabilizes higher-order organization of nucleosomes into the ∼30 nm chromatin fiber. In comparison to core histones, histone H1 is less well conserved through evolution. Furthermore, histone H1 composition in metazoans is generally complex with most species containing multiple variants that play redundant as well as specific functions. In this regard, a characteristic feature is the presence of specific H1 variants that replace somatic H1s in the germline and during early embryogenesis. In this review, we summarize our current knowledge about their structural and functional properties.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alizadeh Z, Kageyama S, Aoki F (2005) Degradation of maternal mRNA in mouse embryos: selective degradation of specific mRNAs after fertilization. Mol Reprod Dev 72:281–290

    Article  PubMed  CAS  Google Scholar 

  • Becker M, Becker A, Miyara F, Han Z, Kihara M, Brown DT, Hager GL, Latham K, Adashi EY, Misteli T (2005) Differential in vivo binding dynamics of somatic and oocyte-specific linker histones in oocytes and during ES cell nuclear transfer. Mol Biol Cell 16:3887–3895

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Belikov S, Astrand C, Wrange O (2007) Mechanism of histone H1-stimulated glucocorticoid receptor DNA binding in vivo. Mol Cell Biol 27:2398–2410

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Belloc E, Pique M, Mendez R (2008) Sequential waves of polyadenylation and deadenylation define a translation circuit that drives meiotic progression. Biochem Soc Trans 36:665–670

    Article  PubMed  CAS  Google Scholar 

  • Bender LB, Cao R, Zhang Y, Strome S (2004) The MES-2/MES-3/MES-6 complex and regulation of histone H3 methylation in C. elegans. Curr Biol 14:1639–1643

    Article  PubMed  CAS  Google Scholar 

  • Bharath MM, Chandra NR, Rao MR (2002) Prediction of an HMG-box fold in the C-terminal domain of histone H1: insights into its role in DNA condensation. Proteins 49:71–81

    Article  PubMed  CAS  Google Scholar 

  • Bordignon V, Clarke HJ, Smith LC (1999) Developmentally regulated loss and reappearance of immunoreactive somatic histone H1 on chromatin of bovine morula-stage nuclei following transplantation into oocytes. Biol Reprod 61:22–30

    Article  PubMed  CAS  Google Scholar 

  • Bordignon V, Clarke HJ, Smith LC (2001) Factors controlling the loss of immunoreactive somatic histone H1 from blastomere nuclei in oocyte cytoplasm: a potential marker of nuclear reprogramming. Dev Biol 233:192–203

    Article  PubMed  CAS  Google Scholar 

  • Brandt WF, Schwager SU, Rodrigues JA, Busslinger M (1997) Isolation and amino acid sequence analysis reveal an ancient evolutionary origin of the cleavage stage (CS) histones of the sea urchin. Eur J Biochem 247:784–791

    Article  PubMed  CAS  Google Scholar 

  • Catena R, Ronfani L, Sassone-Corsi P, Davidson I (2006) Changes in intranuclear chromatin architecture induce bipolar nuclear localization of histone variant H1T2 in male haploid spermatids. Dev Biol 296:231–238

    Article  PubMed  CAS  Google Scholar 

  • Cavalcanti MC, Rizgalla M, Geyer J, Failing K, Litzke LF, Bergmann M (2009) Expression of histone 1 (H1) and testis-specific histone 1 (H1t) genes during stallion spermatogenesis. Anim Reprod Sci 111:220–234

    Article  PubMed  CAS  Google Scholar 

  • Clare SE, Fantz DA, Kistler WS, Kistler MK (1997a) The testis-specific histone H1t gene is strongly repressed by a G/C-rich region just downstream of the TATA Box. J Biol Chem 272:33028–33036

    Article  PubMed  CAS  Google Scholar 

  • Clare SE, Hatfield WR, Fantz DA, Kistler WS, Kistler MK (1997b) Characterization of the promoter region of the rat testis-specific histone H1t gene. Biol Reprod 56:73–82

    Article  PubMed  CAS  Google Scholar 

  • Couteau F, Guerry F, Muller F, Palladino F (2002) A heterochromatin protein 1 homologue in Caenorhabditis elegans acts in germline and vulval development. EMBO Rep 3:235–241

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dasso M, Dimitrov S, Wolffe AP (1994) Nuclear assembly is independent of linker histones. Proc Natl Acad Sci U S A 91:12477–12481

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • De Lucia F, Faraone-Mennella MR, D’Erme M, Quesada P, Caiafa P, Farina B (1994) Histone-induced condensation of rat testis chromatin: testis-specific H1t versus somatic H1 variants. Biochem Biophys Res Commun 198:32–39

    Article  PubMed  Google Scholar 

  • de Moor CH, Richter JD (1997) The Mos pathway regulates cytoplasmic polyadenylation in Xenopus oocytes. Mol Cell Biol 17:6419–6426

    Article  PubMed Central  PubMed  Google Scholar 

  • Dimitrov S, Wolffe AP (1996) Remodeling somatic nuclei in Xenopus laevis egg extracts: molecular mechanisms for the selective release of histones H1 and H1(0) from chromatin and the acquisition of transcriptional competence. EMBO J 15:5897–5906

    PubMed Central  PubMed  CAS  Google Scholar 

  • Dimitrov S, Dasso MC, Wolffe AP (1994) Remodeling sperm chromatin in Xenopus laevis egg extracts: the role of core histone phosphorylation and linker histone B4 in chromatin assembly. J Cell Biol 126:591–601

    Article  PubMed  CAS  Google Scholar 

  • Drabent B, Kardalinou E, Doenecke D (1991) Structure and expression of the human gene encoding testicular H1 histone (H1t). Gene 103:263–268

  • Drabent B, Bode C, Doenecke D (1993) Structure and expression of the mouse testicular H1 histone gene (H1t). Biochim Biophys Acta 1216:311–313

  • Drabent B, Bode C, Bramlage B, Doenecke D (1996) Expression of the mouse testicular histone gene H1t during spermatogenesis. Histochem Cell Biol 106:247–251

    Article  PubMed  CAS  Google Scholar 

  • Drabent B, Bode C, Miosge N, Herken R, Doenecke D (1998) Expression of the mouse histone gene H1t begins at premeiotic stages of spermatogenesis. Cell Tissue Res 291:127–132

    Article  PubMed  CAS  Google Scholar 

  • Drabent B, Saftig P, Bode C, Doenecke D (2000) Spermatogenesis proceeds normally in mice without linker histone H1t. Histochem Cell Biol 113:433–442

    PubMed  CAS  Google Scholar 

  • Easton D, Chalkley R (1972) High-resolution electrophoretic analysis of the histones from embryos and sperm of Arbacia punctulata. Exp Cell Res 72:502–508

    Article  PubMed  CAS  Google Scholar 

  • Faraone-Mennella MR, De Lucia F, Gentile N, Quesada P, Farina B (1999) In vitro poly(ADP-ribosyl)ated histones H1a and H1t modulate rat testis chromatin condensation differently. J Cell Biochem 76:20–29

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Miranda G, Mendez R (2012) The CPEB-family of proteins, translational control in senescence and cancer. Ageing Res Rev 11:460–472

    Article  PubMed  CAS  Google Scholar 

  • Franks RR, Davis FC (1983) Regulation of histone synthesis during early Urechis caupo (echiura) development. Dev Biol 98:101–109

    Article  PubMed  CAS  Google Scholar 

  • Furuya M, Tanaka M, Teranishi T, Matsumoto K, Hosoi Y, Saeki K, Ishimoto H, Minegishi K, Iritani A, Yoshimura Y (2007) H1foo is indispensable for meiotic maturation of the mouse oocyte. J Reprod Dev 53:895–902

    Article  PubMed  CAS  Google Scholar 

  • Gajiwala KS, Chen H, Cornille F, Roques BP, Reith W, Mach B, Burley SK (2000) Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature 403:916–921

    Article  PubMed  CAS  Google Scholar 

  • Gao S, Chung YG, Parseghian MH, King GJ, Adashi EY, Latham KE (2004) Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer: evidence for a uniform developmental program in mice. Dev Biol 266:62–75

    Article  PubMed  CAS  Google Scholar 

  • Godde JS, Ura K (2009) Dynamic alterations of linker histone variants during development. Int J Dev Biol 53:215–224

    Article  PubMed  CAS  Google Scholar 

  • Green GR, Poccia DL (1985) Phosphorylation of sea urchin sperm H1 and H2B histones precedes chromatin decondensation and H1 exchange during pronuclear formation. Dev Biol 108:235–245

    Article  PubMed  CAS  Google Scholar 

  • Grimes SR, Wolfe SA, Anderson JV, Stein GS, Stein JL (1990) Structural and functional analysis of the rat testis-specific histone H1t gene. J Cell Biochem 44:1–17

    Article  PubMed  CAS  Google Scholar 

  • Grimes SR, Wolfe SA, Koppel DA (1992a) Temporal correlation between the appearance of testis-specific DNA-binding proteins and the onset of transcription of the testis-specific histone H1t gene. Exp Cell Res 201:216–224

    Article  PubMed  CAS  Google Scholar 

  • Grimes SR, Wolfe SA, Koppel DA (1992b) Tissue-specific binding of testis nuclear proteins to a sequence element within the promoter of the testis-specific histone H1t gene. Arch Biochem Biophys 296:402–409

    Article  PubMed  CAS  Google Scholar 

  • Grimes SR, Prado S, Wolfe SA (2005) Transcriptional activation of the testis-specific histone H1t gene by RFX2 may require both proximal promoter X-box elements. J Cell Biochem 94:317–326

    Article  PubMed  CAS  Google Scholar 

  • Hake LE, Richter JD (1994) CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79:617–627

    Article  PubMed  CAS  Google Scholar 

  • Hayakawa K, Ohgane J, Tanaka S, Yagi S, Shiota K (2012) Oocyte-specific linker histone H1foo is an epigenomic modulator that decondenses chromatin and impairs pluripotency. Epigenetics 7:1029–1036

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Herlands L, Allfrey VG, Poccia D (1982) Translational regulation of histone synthesis in the sea urchin Strongylocentrotus purpuratus. J Cell Biol 94:219–223

    Article  PubMed  CAS  Google Scholar 

  • Horvath GC, Kistler WS, Kistler MK (2004) RFX2 is a potential transcriptional regulatory factor for histone H1t and other genes expressed during the meiotic phase of spermatogenesis. Biol Reprod 71:1551–1559

    Article  PubMed  CAS  Google Scholar 

  • Iguchi N, Tanaka H, Yomogida K, Nishimune Y (2003) Isolation and characterization of a novel cDNA encoding a DNA-binding protein (Hils1) specifically expressed in testicular haploid germ cells. Int J Androl 26:354–365

    Article  PubMed  CAS  Google Scholar 

  • Iguchi N, Tanaka H, Yamada S, Nishimura H, Nishimune Y (2004) Control of mouse hils1 gene expression during spermatogenesis: identification of regulatory element by transgenic mouse. Biol Reprod 70:1239–1245

    Article  PubMed  CAS  Google Scholar 

  • Jayaramaiah Raja S, Renkawitz-Pohl R (2005) Replacement by Drosophila melanogaster protamines and Mst77F of histones during chromatin condensation in late spermatids and role of sesame in the removal of these proteins from the male pronucleus. Mol Cell Biol 25:6165–6177

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jedrusik MA, Schulze E (2001) A single histone H1 isoform (H1.1) is essential for chromatin silencing and germline development in Caenorhabditis elegans. Development 128:1069–1080

    PubMed  CAS  Google Scholar 

  • Jedrusik MA, Schulze E (2003) Telomeric position effect variegation in Saccharomyces cerevisiae by Caenorhabditis elegans linker histones suggests a mechanistic connection between germ line and telomeric silencing. Mol Cell Biol 23:3681–3691

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jedrusik MA, Schulze E (2007) Linker histone HIS-24 (H1.1) cytoplasmic retention promotes germ line development and influences histone H3 methylation in Caenorhabditis elegans. Mol Cell Biol 27:2229–2239

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jedrzejczak P, Kempisty B, Bryja A, Mostowska M, Depa-Martynow M, Pawelczyk L, Jagodzinski PP (2007) Quantitative assessment of transition proteins 1, 2 spermatid-specific linker histone H1-like protein transcripts in spermatozoa from normozoospermic and asthenozoospermic men. Arch Androl 53:199–205

    Article  PubMed  CAS  Google Scholar 

  • Jullien J, Astrand C, Halley-Stott RP, Garrett N, Gurdon JB (2010) Characterization of somatic cell nuclear reprogramming by oocytes in which a linker histone is required for pluripotency gene reactivation. Proc Natl Acad Sci U S A 107:5483–5488

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jullien J, Miyamoto K, Pasque V, Allen GE, Bradshaw CR, Garrett NJ, Halley-Stott RP, Kimura H, Ohsumi K, Gurdon JB (2014) Hierarchical molecular events driven by oocyte-specific factors lead to rapid and extensive reprogramming. Mol Cell 55:524–536

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kelly WG, Fire A (1998) Chromatin silencing and the maintenance of a functional germline in Caenorhabditis elegans. Development 125:2451–2456

    PubMed Central  PubMed  CAS  Google Scholar 

  • Khadake JR, Rao MR (1995) DNA- and chromatin-condensing properties of rat testes H1a and H1t compared to those of rat liver H1bdec; H1t is a poor condenser of chromatin. Biochemistry 34:15792–15801

    Article  PubMed  CAS  Google Scholar 

  • Khadake JR, Rao MR (1997) Condensation of DNA and chromatin by an SPKK-containing octapeptide repeat motif present in the C-terminus of histone H1. Biochemistry 36:1041–1051

    Article  PubMed  Google Scholar 

  • Lin Q, Sirotkin A, Skoultchi AI (2000) Normal spermatogenesis in mice lacking the testis-specific linker histone H1t. Mol Cell Biol 20:2122–2128

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lin Q, Inselman A, Han X, Xu H, Zhang W, Handel MA, Skoultchi AI (2004) Reductions in linker histone levels are tolerated in developing spermatocytes but cause changes in specific gene expression. J Biol Chem 279:23525–23535

    Article  PubMed  CAS  Google Scholar 

  • Lu ZH, Sittman DB, Brown DT, Munshi R, Leno GH (1997) Histone H1 modulates DNA replication through multiple pathways in Xenopus egg extract. J Cell Sci 110:2745–2758

    PubMed  CAS  Google Scholar 

  • Lu ZH, Sittman DB, Romanowski P, Leno GH (1998) Histone H1 reduces the frequency of initiation in Xenopus egg extract by limiting the assembly of prereplication complexes on sperm chromatin. Mol Biol Cell 9:1163–1176

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Maeda C, Sato S, Hattori N, Tanaka S, Yagi S, Shiota K (2008) DNA hypomethylation circuit of the mouse oocyte-specific histone H1foo gene in female germ cell lineage. Biol Reprod 78:816–821

    Article  PubMed  CAS  Google Scholar 

  • Maki N, Suetsugu-Maki R, Sano S, Nakamura K, Nishimura O, Tarui H, Del Rio-Tsonis K, Ohsumi K, Agata K, Tsonis PA (2010) Oocyte-type linker histone B4 is required for transdifferentiation of somatic cells in vivo. FASEB J 24:3462–3467

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mandl B, Brandt WF, Superti-Furga G, Graninger PG, Birnstiel ML, Busslinger M (1997) The five cleavage-stage (CS) histones of the sea urchin are encoded by a maternally expressed family of replacement histone genes: functional equivalence of the CS H1 and frog H1M (B4) proteins. Mol Cell Biol 17:1189–1200

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Marcon L, Boissonneault G (2004) Transient DNA strand breaks during mouse and human spermiogenesis: new insights in stage specificity and link to chromatin remodeling. Biol Reprod 70:910–918

    Article  PubMed  CAS  Google Scholar 

  • Martianov I, Brancorsini S, Catena R, Gansmuller A, Kotaja N, Parvinen M, Sassone-Corsi P, Davidson I (2005) Polar nuclear localization of H1T2, a histone H1 variant required for spermatid elongation and DNA condensation during spermiogenesis. Proc Natl Acad Sci U S A 102:2808–2813

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T (2006) Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10:105–116

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Meyer-Ficca ML, Scherthan H, Burkle A, Meyer RG (2005) Poly(ADP-ribosyl)ation during chromatin remodeling steps in rat spermiogenesis. Chromosoma 114:67–74

    Article  PubMed  CAS  Google Scholar 

  • Meyer-Ficca ML, Ihara M, Lonchar JD, Meistrich ML, Austin CA, Min W, Wang ZQ, Meyer RG (2011) Poly(ADP-ribose) metabolism is essential for proper nucleoprotein exchange during mouse spermiogenesis. Biol Reprod 84:218–228

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Miyamoto K, Furusawa T, Ohnuki M, Goel S, Tokunaga T, Minami N, Yamada M, Ohsumi K, Imai H (2007) Reprogramming events of mammalian somatic cells induced by Xenopus laevis egg extracts. Mol Reprod Dev 74:1268–1277

    Article  PubMed  CAS  Google Scholar 

  • Mizusawa Y, Kuji N, Tanaka Y, Tanaka M, Ikeda E, Komatsu S, Kato S, Yoshimura Y (2010) Expression of human oocyte-specific linker histone protein and its incorporation into sperm chromatin during fertilization. Fertil Steril 93:1134–1141

    Article  PubMed  CAS  Google Scholar 

  • Müller K, Thisse C, Thisse B, Raz E (2002) Expression of a linker histone-like gene in the primordial germ cells in zebrafish. Mech Dev 117:253–257

    Article  PubMed  Google Scholar 

  • Newrock KM, Alfageme CR, Nardi RV, Cohen LH (1978) Histone changes during chromatin remodeling in embryogenesis. Cold Spring Harb Symp Quant Biol 42:421–431

  • Nightingale K, Dimitrov S, Reeves R, Wolffe AP (1996) Evidence for a shared structural role for HMG1 and linker histones B4 and H1 in organizing chromatin. EMBO J 15:548–561

    PubMed Central  PubMed  CAS  Google Scholar 

  • Osley MA (1991) The regulation of histone synthesis in the cell cycle. Annu Rev Biochem 60:827–861

    Article  PubMed  CAS  Google Scholar 

  • Paris J, Swenson K, Piwnica-Worms H, Richter JD (1991) Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein. Genes Dev 5:1697–1708

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Montero S, Carbonell A, Morán T, Vaquero A, Azorín F (2013) The embryonic linker histone H1 variant of Drosophila, dBigH1, regulates zygotic genome activation. Dev Cell 26:578–590

    Article  PubMed  Google Scholar 

  • Poccia D (1986) Remodeling of nucleoproteins during gametogenesis, fertilization, and early development. Int Rev Cytol 105:1–65

    Article  PubMed  CAS  Google Scholar 

  • Poccia D, Salik J, Krystal G (1987) Transitions in histone variants of the male pronucleus following fertilization and evidence for a maternal store of cleavage-stage histones in the sera urchin egg. Dev Biol 82:287–296

  • Poccia D, Salik J, Krystal G (1981) Transitions in histone variants of the male pronucleus following fertilization and evidence for a maternal store of cleavage-stage histones in the sea urchin egg. Dev Biol 82(2):287–296

    Article  PubMed  CAS  Google Scholar 

  • Porter DC, Vacquier VD (1988) Extraction of phosphorylated sperm specific histone H1 from sea urchin eggs: analysis of phosphopeptide maps. Biochem Biophys Res Commun 151:1200–1204

    Article  PubMed  CAS  Google Scholar 

  • Racki WJ, Richter JD (2006) CPEB controls oocyte growth and follicle development in the mouse. Development 133:4527–4537

    Article  PubMed  CAS  Google Scholar 

  • Ramesh S, Bharath MM, Chandra NR, Rao MR (2006) A K52Q substitution in the globular domain of histone H1t modulates its nucleosome binding properties. FEBS Lett 580:5999–6006

    Article  PubMed  CAS  Google Scholar 

  • Richter JD (2007) CPEB: a life in translation. Trends Biochem Sci 32:279–285

    Article  PubMed  CAS  Google Scholar 

  • Saeki H, Ohsumi K, Aihara H, Ito T, Hirose S, Ura K, Kaneda Y (2005) Linker histone variants control chromatin dynamics during early embryogenesis. Proc Natl Acad Sci U S A 102:5697–5702

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Salik J, Herlands L, Hoffmann HP, Poccia D (1981) Electrophoretic analysis of the stored histone pool in unfertilized sea urchin eggs: quantification and identification by antibody binding. J Cell Biol 90:385–395

    Article  PubMed  CAS  Google Scholar 

  • Sanicola M, Ward S, Childs G, Emmons SW (1990) Identification of a Caenorhabditis elegans histone H1 gene family. Characterization of a family member containing an intron and encoding a poly(A)+ mRNA. J Mol Biol 212:259–268

  • Seyedin SM, Kistler WS (1980) Isolation and characterization of rat testis H1t. An H1 histone variant associated with spermatogenesis. J Biol Chem 255:5949–5954

    PubMed  CAS  Google Scholar 

  • Shang E, Nickerson HD, Wen D, Wang X, Wolgemuth DJ (2007) The first bromodomain of Brdt, a testis-specific member of the BET sub-family of double-bromodomain-containing proteins, is essential for male germ cell differentiation. Development 134:3507–3515

    Article  PubMed  CAS  Google Scholar 

  • Shechter D, Nicklay JJ, Chitta RK, Shabanowitz J, Hunt DF, Allis CD (2009) Analysis of histones in Xenopus laevis. I. A distinct index of enriched variants and modifications exists in each cell type and is remodeled during developmental transitions. J Biol Chem 284:1064–1074

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shintomi K, Iwabuchi M, Saeki H, Ura K, Kishimoto T, Ohsumi K (2005) Nucleosome assembly protein-1 is a linker histone chaperone in Xenopus eggs. Proc Natl Acad Sci U S A 102:8210–8215

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Simpson RT, Bergman LW (1980) Structure of sea urchin sperm chromatin core particle. J Biol Chem 255:10702–10709

    PubMed  CAS  Google Scholar 

  • Smith A, Haaf T (1998) DNA nicks and increased sensitivity of DNA to fluorescence in situ end labeling during functional spermiogenesis. Biotechniques 25:496–502

    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

    Article  PubMed  CAS  Google Scholar 

  • Spadafora C, Bellard M, Compton JL, Chambon P (1976) The DNA repeat lengths in chromatins from sea urchin sperm and gastrula cells are markedly different. FEBS Lett 69:281–285

    Article  PubMed  CAS  Google Scholar 

  • Stebbins-Boaz B, Hake LE, Richter JD (1996) CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J 15:2582–2592

    PubMed Central  PubMed  CAS  Google Scholar 

  • Steger K, Klonisch T, Gavenis K, Drabent B, Doenecke D, Bergmann M (1998) Expression of mRNA and protein of nucleoproteins during human spermiogenesis. Mol Hum Reprod 4:939–945

    Article  PubMed  CAS  Google Scholar 

  • Steinbach OC, Wolffe AP, Rupp RA (1997) Somatic linker histones cause loss of mesodermal competence in Xenopus. Nature 389:395–399

    Article  PubMed  CAS  Google Scholar 

  • Strickland WN, Strickland M, Brandt WF, Von Holt C, Lehmann A, Wittmann-Liebold B (1980) The primary structure of histone H1 from sperm of the sea urchin Parechinus angulosus. 2. Sequence of the C-terminal CNBr peptide and the entire primary structure. Eur J Biochem 104:567–578

    Article  PubMed  CAS  Google Scholar 

  • Studencka M, Konzer A, Moneron G, Wenzel D, Opitz L, Salinas-Riester G, Bedet C, Kruger M, Hell SW, Wisniewski JR, Schmidt H, Palladino F, Schulze E, Jedrusik-Bode M (2011) Novel roles of Caenorhabditis elegans heterochromatin protein HP1 and linker histone in the regulation of innate immune gene expression. Mol Cell Biol 32:251–265

    Article  PubMed  CAS  Google Scholar 

  • Studencka M, Wesolowski R, Opitz L, Salinas-Riester G, Wisniewski JR, Jedrusik-Bode M (2012) Transcriptional repression of Hox genes by C. elegans HP1/HPL and H1/HIS-24. PLoS Genet 8:e1002940

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Su Y, Wub D, Zhoub W, Irwin DM, Zhang Y (2013) Rapid evolution of the mammalian HILS1 gene and the nuclear condensation process during mammalian spermiogenesis. J Genet Genom 40:55–59

    Article  CAS  Google Scholar 

  • Tanaka M, Hennebold JD, Macfarlane J, Adashi EY (2001) A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. Development 128:655–664

    PubMed  CAS  Google Scholar 

  • Tanaka Y, Kato S, Tanaka M, Kuji N, Yoshimura Y (2003) Structure and expression of the human oocyte-specific histone H1 gene elucidated by direct RT-nested PCR of a single oocyte. Biochem Biophys Res Commun 304:351–357

    Article  PubMed  CAS  Google Scholar 

  • Tanaka H, Iguchi N, Isotani A, Kitamura K, Toyama Y, Matsuoka Y, Onishi M, Masai K, Maekawa M, Toshimori K, Okabe M, Nishimune Y (2005) HANP1/H1T2, a novel histone H1-like protein involved in nuclear formation and sperm fertility. Mol Cell Biol 25:7107–7119

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Teranishi T, Tanaka M, Kimoto S, Ono Y, Miyakoshi K, Kono T, Yoshimura Y (2004) Rapid replacement of somatic linker histones with the oocyte-specific linker histone H1foo in nuclear transfer. Dev Biol 266:76–86

    Article  PubMed  CAS  Google Scholar 

  • Tsunemoto K, Anzai M, Matsuoka T, Tokoro M, Shin SW, Amano T, Mitani T, Kato H, Hosoi Y, Saeki K, Iritani A, Matsumoto K (2008) Cis-acting elements (E-box and NBE) in the promoter region of three maternal genes (Histone H1oo, Nucleoplasmin 2, and Zygote Arrest 1) are required for oocyte-specific gene expression in the mouse. Mol Reprod Dev 75:1104–1108

    Article  PubMed  CAS  Google Scholar 

  • Ura K, Nightingale K, Wolffe AP (1996) Differential association of HMG1 and linker histones B4 and H1 with dinucleosomal DNA: structural transitions and transcriptional repression. EMBO J 15:4959–4969

    PubMed Central  PubMed  CAS  Google Scholar 

  • vanWert JM, Panek HR, Wolfe SA, Grimes SR (1998) The TE promoter element of the histone H1t gene is essential for transcription in transgenic mouse primary spermatocytes. Biol Reprod 59:704–710

    Article  PubMed  CAS  Google Scholar 

  • Vanfleteren JR, Van Bun SM, Van Beeumen JJ (1988) The primary structure of the major isoform (H1.1) of histone H1 from the nematode Caenorhabditis elegans. Biochem J 255:647–652

  • VanWert JM, Wolfe SA, Grimes SR (2008) Binding of RFX2 and NF-Y to the testis-specific histone H1t promoter may be required for transcriptional activation in primary spermatocytes. J Cell Biochem 104(3):1087–1101

    Article  PubMed  CAS  Google Scholar 

  • Wibrand K, Olsen LC (2002) Linker histone H1M transcripts mark the developing germ line in zebrafish. Mech Dev 117:249–252

    Article  PubMed  CAS  Google Scholar 

  • Wilkerson DC, Wolfe SA, Grimes SR (2002a) H1t/GC-box and H1t/TE1 element are essential for promoter activity of the testis-specific histone H1t gene. Biol Reprod 67:1157–1164

    Article  PubMed  CAS  Google Scholar 

  • Wilkerson DC, Wolfe SA, Grimes SR (2002b) Sp1 and Sp3 activate the testis-specific histone H1t promoter through the H1t/GC-box. J Cell Biochem 86:716–725

    Article  PubMed  CAS  Google Scholar 

  • Wirth M, Jedrusik-Bode MA (2009) Interplay between histone deacetylase SIR-2, linker histone H1 and histone methyltransferases in heterochromatin formation. Epigenetics 4:353–356

    Article  PubMed  CAS  Google Scholar 

  • Wirth M, Paap F, Fischle W, Wenzel D, Agafonov DE, Samatov TR, Wisniewski JR, Jedrusik-Bode M (2009) HIS-24 linker histone and SIR-2.1 deacetylase induce H3K27me3 in the Caenorhabditis elegans germ line. Mol Cell Biol 29:3700–3709

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wolfe SA, Grimes SR (1999) Binding of nuclear proteins to an upstream element involved in transcriptional regulation of the testis-specific histone H1t gene. J Cell Biochem 75:555–565

    Article  PubMed  CAS  Google Scholar 

  • Wolfe SA, Grimes SR (2003a) Specific binding of nuclear proteins to a bifunctional promoter element upstream of the H1/AC box of the testis-specific histone H1t gene. Biol Reprod 68:2267–2273

    Article  PubMed  CAS  Google Scholar 

  • Wolfe SA, Grimes SR (2003b) Transcriptional repression of the testis-specific histone H1t gene mediated by an element upstream of the H1/AC box. Gene 308:129–138

    Article  PubMed  CAS  Google Scholar 

  • Wolfe SA, van Wert JM, Grimes SR (1995) Expression of the testis-specific histone H1t gene: evidence for involvement of multiple cis-acting promoter elements. Biochemistry 34:12461–12469

    Article  PubMed  CAS  Google Scholar 

  • Wolfe SA, Wilkerson DC, Prado S, Grimes SR (2004) Regulatory factor X2 (RFX2) binds to the H1t/TE1 promoter element and activates transcription of the testis-specific histone H1t gene. J Cell Biochem 91:375–383

    Article  PubMed  CAS  Google Scholar 

  • Wolfe SA, van Wert J, Grimes SR (2006) Transcription factor RFX2 is abundant in rat testis and enriched in nuclei of primary spermatocytes where it appears to be required for transcription of the testis-specific histone H1t gene. J Cell Biochem 99:735–746

    Article  PubMed  CAS  Google Scholar 

  • Wolfe SA, Vanwert JM, Grimes SR (2008) Transcription factor RFX4 binding to the testis-specific histone H1t promoter in spermatocytes may be important for regulation of H1t gene transcription during spermatogenesis. J Cell Biochem 105:61–69

    Article  PubMed  CAS  Google Scholar 

  • Yan W, Ma L, Burns KH, Matzuk MM (2003) HILS1 is a spermatid-specific linker histone H1-like protein implicated in chromatin remodeling during mammalian spermiogenesis. Proc Natl Acad Sci U S A 100:10546–10551

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yun Y, Zhao GM, Wu SJ, Li W, Lei AM (2012) Replacement of H1 linker histone during bovine somatic cell nuclear transfer. Theriogenology 78:1371–1380

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We apologize to colleagues whose work could not be cited here due to space limitations. Work in the authors’ laboratory is supported by grants from MINECO (BFU2012-30724) and the Generalitat de Catalunya (SGR2014-204).

Compliance with ethical standards

All authors declare that they have no conflict of interest. This article does not contain any studies with human participants performed by any of the authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fernando Azorín.

Additional information

Salvador Pérez-Montero and Albert Carbonell contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez-Montero, S., Carbonell, A. & Azorín, F. Germline-specific H1 variants: the “sexy” linker histones. Chromosoma 125, 1–13 (2016). https://doi.org/10.1007/s00412-015-0517-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-015-0517-x

Keywords

Navigation