Relaxed Chromatin Formation and Weak Suppression of Homologous Pairing by the Testis-Specific Linker Histone H1T

Biochemistry

Volumn 55, Issue 4, 2016, Pages 637-646

  MacHida, Shinichi ^a   Hayashida, Ryota ^a   Takaku, Motoki ^a   Fukuto, Atsuhiko ^b   Sun, Jiying ^b   Kinomura, Aiko ^b   Tashiro, Satoshi ^b   Kurumizaka, Hitoshi ^a,c  

^a WASEDA UNIVERSITY   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; PROTEINS;

GERM CELLS; HIGHER-ORDER; HOMOLOGOUS RECOMBINATION; HUMAN CELLS; IN-VITRO; LINKER HISTONES; NUCLEOSOMES; RECOMBINATION FREQUENCIES;

CHROMOSOMES;

HISTONE; HISTONE H1; HISTONE H1.1; HISTONE H1.2; HISTONE H1.3; HISTONE H1.4; HISTONE H1.5; HISTONE H1T; NUCLEOSOME ASSEMBLY PROTEIN 1; RAD51 PROTEIN; RAD54 PROTEIN; UNCLASSIFIED DRUG; DNA HELICASE; NUCLEAR PROTEIN; NUCLEOSOME; RAD51 PROTEIN, HUMAN; RAD54L PROTEIN, HUMAN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA SEQUENCE; ENZYME REPRESSION; GENE SEQUENCE; GENETIC RECOMBINATION; GERM CELL; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MEIOSIS; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SEDIMENTATION; SOMATIC CELL; CELL LINE; CHEMISTRY; GENETICS; IMMUNOLOGY; METABOLISM;

CELL LINE; DNA HELICASES; HISTONES; HUMANS; NUCLEAR PROTEINS; NUCLEOSOMES; RAD51 RECOMBINASE; RECOMBINATION, GENETIC;

EID: 84957024654     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b01126     Document Type: Article

References (64)

1. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution Nature 389, 251-260 10.1038/38444
2. Davey, C. A., Sargent, D. F., Luger, K., Maeder, A. W., and Richmond, T. J. (2002) Solvent Mediated Interactions in the Structure of the Nucleosome Core Particle at 1.9Å Resolution J. Mol. Biol. 319, 1097-1113 10.1016/S0022-2836(02)00386-8
3. Makde, R. D., England, J. R., Yennawar, H. P., and Tan, S. (2010) Structure of RCC1 chromatin factor bound to the nucleosome core particle Nature 467, 562-566 10.1038/nature09321
4. Luger, K., Dechassa, M. L., and Tremethick, D. J. (2012) New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat. Rev. Mol. Cell Biol. 13, 436-447 10.1038/nrm3382
5. Happel, N. and Doenecke, D. (2009) Histone H1 and its isoforms: Contribution to chromatin structure and function Gene 431, 1-12 10.1016/j.gene.2008.11.003
6. Harshman, S. W., Young, N. L., Parthun, M. R., and Freitas, M. A. (2013) H1 histones: current perspectives and challenges Nucleic Acids Res. 41, 9593-9609 10.1093/nar/gkt700
7. Whitlock, J. P., Jr. and Simpson, R. T. (1976) Removal of histone H1 exposes a fifty base pair DNA segment between nucleosomes Biochemistry 15, 3307-3314 10.1021/bi00660a022
8. Simpson, R. T. (1978) Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones Biochemistry 17, 5524-5531 10.1021/bi00618a030
9. Syed, S. H., Goutte-Gattat, D., Becker, N., Meyer, S., Shukla, M. S., Hayes, J. J., Everaers, R., Angelov, D., Bednar, J., and Dimitrov, S. (2010) Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome Proc. Natl. Acad. Sci. U. S. A. 107, 9620-9625 10.1073/pnas.1000309107
10. Caterino, T. L., Fang, H., and Hayes, J. J. (2011) Nucleosome linker DNA contacts and induces specific folding of the intrinsically disordered H1 carboxyl-terminal domain Mol. Cell. Biol. 31, 2341-2348 10.1128/MCB.05145-11
11. Hartman, P. G., Chapman, G. E., Moss, T., and Bradbury, E. M. (1977) Studies on the role and mode of operation of the very-lysine-rich histone H1 in eukaryote chromatin. The three structural regions of the histone H1 molecule Eur. J. Biochem. 77, 45-51 10.1111/j.1432-1033.1977.tb11639.x
12. Allan, J., Hartman, P. G., Crane-Robinson, C., and Aviles, F. X. (1980) The structure of histone H1 and its location in chromatin Nature 288, 675-679 10.1038/288675a0
13. Song, F., Chen, P., Sun, D., Wang, M., Dong, L., Liang, D., Xu, R. M., Zhu, P., and Li, G. (2014) Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units Science 344, 376-380 10.1126/science.1251413
14. Zhou, B.-R., Jiang, J., Feng, H., Ghirlando, R., Xiao, T. S., and Bai, Y. (2015) Structural mechanisms of nucleosome recognition by linker histones Mol. Cell 59, 628-638 10.1016/j.molcel.2015.06.025
15. Th'ng, J. P. H., Sung, R., Ye, M., and Hendzel, M. J. (2005) H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain J. Biol. Chem. 280, 27809-27814 10.1074/jbc.M501627200
16. Clausell, J., Happel, N., Hale, T. K., Doenecke, D., and Beato, M. (2009) Histone H1 subtypes differentially modulate chromatin condensation without preventing ATP-dependent remodeling by SWI/SNF or NURF PLoS One 4, e0007243 10.1371/journal.pone.0007243
17. Izzo, A., Kamieniarz-Gdula, K., Ramírez, F., Noureen, N., Kind, J., Manke, T., van Steensel, B., and Schneider, R. (2013) The genomic landscape of the somatic linker histone subtypes H1.1 to H1.5 in human cells Cell Rep. 3, 2142-2154 10.1016/j.celrep.2013.05.003
18. DeLucia, F., Faraone-Mennella, M. R., D'Erme, M., Quesada, P., Caiafa, P., and Farina, B. (1994) Histone-induced condensation of rat testis chromatin: testis-specific H1t versus somatic H1 variants Biochem. Biophys. Res. Commun. 198, 32-39 10.1006/bbrc.1994.1005
19. Khadake, J. R. and Rao, M. R. (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 10.1021/bi00048a025
20. Bucci, L. R., Brock, W. A., and Meistrich, M. L. (1982) Distribution and synthesis of histone 1 subfractions during spermatogenesis in the rat Exp. Cell Res. 140, 111-118 10.1016/0014-4827(82)90162-8
21. Grimes, S. R., Wilkersona, D. C., Noss, K. R., and Wolfe, S. A. (2003) Transcriptional control of the testis-specific histone H1t gene Gene 304, 13-21 10.1016/S0378-1119(02)01201-5
22. Govin, J., Caron, C., Lestrat, C., Rousseaux, S., and Khochbin, S. (2004) The role of histones in chromatin remodelling during mammalian spermiogenesis Eur. J. Biochem. 271, 3459-3469 10.1111/j.1432-1033.2004.04266.x
23. Petronczki, M., Siomos, M. F., and Nasmyth, K. (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis Cell 112, 423-440 10.1016/S0092-8674(03)00083-7
24. Neale, M. J. and Keeney, S. (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination Nature 442, 153-158 10.1038/nature04885
25. Sung, P. (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein Science 265, 1241-1243 10.1126/science.8066464
26. Baumann, P., Benson, F. E., and West, S. C. (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro Cell 87, 757-766 10.1016/S0092-8674(00)81394-X
27. Gupta, R. C., Bazemore, L. R., Golub, E. I., and Radding, C. M. (1997) Activities of human recombination protein Rad51 Proc. Natl. Acad. Sci. U. S. A. 94, 463-468 10.1073/pnas.94.2.463
28. Maeshima, K., Morimatsu, K., and Horii, T. (1996) Purification and characterization of XRad51.1 protein, Xenopus RAD51 homologue: recombinant XRad51.1 promotes strand exchange reaction Genes Cells 1, 1057-1068 10.1046/j.1365-2443.1996.d01-224.x
29. Alexiadis, V. and Kadonaga, J. T. (2002) Strand pairing by Rad54 and Rad51 is enhanced by chromatin Genes Dev. 16, 2767-2771 10.1101/gad.1032102
30. Jaskelioff, M., Van Komen, S., Krebs, J. E., Sung, P., and Peterson, C. L. (2003) Rad54p is a chromatin remodeling enzyme required for heteroduplex DNA joint formation with chromatin J. Biol. Chem. 278, 9212-9218 10.1074/jbc.M211545200
31. Alexeev, A., Mazin, A., and Kowalczykowski, S. C. (2003) Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament Nat. Struct. Biol. 10, 182-186 10.1038/nsb901
32. Zhang, Z., Fan, H.-Y., Goldman, J. A., and Kingston, R. E. (2007) Homology-driven chromatin remodeling by human RAD54 Nat. Struct. Mol. Biol. 14, 397-405 10.1038/nsmb1223
33. Sinha, M. and Peterson, C. L. (2008) A Rad51 presynaptic filament is sufficient to capture nucleosomal homology during recombinational repair of a DNA double-strand break Mol. Cell 30, 803-810 10.1016/j.molcel.2008.04.015
34. Machida, S., Takaku, M., Ikura, M., Sun, J., Suzuki, H., Kobayashi, W., Kinomura, A., Osakabe, A., Tachiwana, H., Horikoshi, Y., Fukuto, A., Matsuda, R., Ura, K., Tashiro, S., Ikura, T., and Kurumizaka, H. (2014) Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1 Sci. Rep. 4, 4863 10.1038/srep04863
35. Ishida, T., Takizawa, Y., Sakane, I., and Kurumizaka, H. (2008) The Lys313 residue of the human Rad51 protein negatively regulates the strand-exchange activity Genes Cells 13, 91-103 10.1111/j.1365-2443.2007.01143.x
36. Tachiwana, H., Osakabe, A., Kimura, H., and Kurumizaka, H. (2008) Nucleosome formation with the testis-specific histone H3 variant, H3t, by human nucleosome assembly proteins in vitro Nucleic Acids Res. 36, 2208-2218 10.1093/nar/gkn060
37. Tachiwana, H., Kagawa, W., Osakabe, A., Kawaguchi, K., Shiga, T., Hayashi-Takanaka, Y., Kimura, H., and Kurumizaka, H. (2010) Structural basis of instability of the nucleosome containing a testis-specific histone variant, human H3T Proc. Natl. Acad. Sci. U. S. A. 107, 10454-10459 10.1073/pnas.1003064107
38. Kagawa, W., Kurumizaka, H., Ikawa, S., Yokoyama, S., and Shibata, T. (2001) Homologous pairing promoted by the human Rad52 protein J. Biol. Chem. 276, 35201-35208 10.1074/jbc.M104938200
39. Lowary, P. T. and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning J. Mol. Biol. 276, 19-42 10.1006/jmbi.1997.1494
40. Arimura, Y., Tachiwana, H., Oda, T., Sato, M., and Kurumizaka, H. (2012) Structural analysis of the hexasome, lacking one histone H2A/H2B dimer from the conventional nucleosome Biochemistry 51, 3302-3309 10.1021/bi300129b
41. Dorigo, B., Schalch, T., Bystricky, K., and Richmond, T. J. (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail J. Mol. Biol. 327, 85-96 10.1016/S0022-2836(03)00025-1
42. Demeler, B. and van Holde, K. E. (2004) Sedimentation velocity analysis of highly heterogeneous systems Anal. Biochem. 335, 279-288 10.1016/j.ab.2004.08.039
43. Pierce, A. J., Johnson, R. D., Thompson, L. H., and Jasin, M. (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells Genes Dev. 13, 2633-2638 10.1101/gad.13.20.2633
44. Kobayashi, J., Kato, A., Ota, Y., Ohba, R., and Komatsu, K. (2010) Bisbenzamidine derivative, pentamidine represses DNA damage response through inhibition of histone H2A acetylation Mol. Cancer 9, e34 10.1186/1476-4598-9-34
45. Saeki, H., Ohsumi, K., Aihara, H., Ito, T., Hirose, S., Ura, K., and Kaneda, Y. (2005) Linker histone variants control chromatin dynamics during early embryogenesis Proc. Natl. Acad. Sci. U. S. A. 102, 5697-5702 10.1073/pnas.0409824102
46. Shintomi, K., Iwabuchi, M., Saeki, H., Ura, K., Kishimoto, T., and 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 10.1073/pnas.0500822102
47. San Filippo, J., Sung, P., and Klein, H. (2008) Mechanism of eukaryotic homologous recombination Annu. Rev. Biochem. 77, 229-257 10.1146/annurev.biochem.77.061306.125255
48. Heyer, W. D., Ehmsen, K. T., and Liu, J. (2010) Regulation of homologous recombination in eukaryotes Annu. Rev. Genet. 44, 113-139 10.1146/annurev-genet-051710-150955
49. Krejci, L., Altmannova, V., Spirek, M., and Zhao, X. (2012) Homologous recombination and its regulation Nucleic Acids Res. 40, 5795-5818 10.1093/nar/gks270
50. Steger, K., Klonisch, T., Gavenis, K., Drabent, B., Doenecke, D., and Bergmann, M. (1998) Expression of mRNA and protein of nucleoproteins during human spermiogenesis Mol. Hum. Reprod. 4, 939-945 10.1093/molehr/4.10.939
51. Drabent, B., Saftig, P., Bode, C., and Doenecke, D. (2000) Spermatogenesis proceeds normally in mice without linker histone H1t Histochem. Cell Biol. 113, 433-442
52. Lin, Q., Sirotkin, A., and Skoultchi, A. I. (2000) Normal spermatogenesis in mice lacking the testis-specific linker histone H1t Mol. Cell. Biol. 20, 2122-2128 10.1128/MCB.20.6.2122-2128.2000
53. Fantz, D. A., Hatfield, W. R., Horvath, G., Kistler, M. K., and Kistler, W. S. (2001) Mice with a targeted disruption of the H1t gene are fertile and undergo normal changes in structural chromosomal proteins during spermiogenesis Biol. Reprod. 64, 425-431 10.1095/biolreprod64.2.425
54. Tanaka, H., Matsuoka, Y., Onishi, M., Kitamura, K., Miyagawa, Y., Nishimura, H., Tsujimura, A., Okuyama, A., and Nishimune, Y. (2006) Expression profiles and single-nucleotide polymorphism analysis of human HANP1/H1T2 encoding a histone H1-like protein Int. J. Androl. 29, 353-359 10.1111/j.1365-2605.2005.00600.x
55. Yan, W., Ma, L., Burns, K. H., and Matzuk, M. M. (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 10.1073/pnas.1837812100
56. Tanaka, Y., Kato, S., Tanaka, M., Kuji, N., and 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 10.1016/S0006-291X(03)00610-7
57. Maze, I., Noh, K.-M., Soshnev, A. A., and Allis, C. D. (2014) Every amino acid matters: essential contributions of histone variants to mammalian development and disease Nat. Rev. Genet. 15, 259-271 10.1038/nrg3673
58. Bao, Y., Konesky, K., Park, Y. J., Rosu, S., Dyer, P. N., Rangasamy, D., Tremethick, D. J., Laybourn, P. J., and Luger, K. (2004) Nucleosomes containing the histone variant H2A.Bbd organize only 118 base pairs of DNA EMBO J. 23, 3314-3324 10.1038/sj.emboj.7600316
59. Gautier, T., Abbott, D. W., Molla, A., Verdel, A., Ausio, J., and Dimitrov, S. (2004) Histone variant H2ABbd confers lower stability to the nucleosome EMBO Rep. 5, 715-720 10.1038/sj.embor.7400182
60. Urahama, T., Horikoshi, N., Osakabe, A., Tachiwana, H., and Kurumizaka, H. (2014) Structure of human nucleosome containing the testis-specific histone variant TSH2B Acta Crystallogr., Sect. F: Struct. Biol. Commun. 70, 444-449 10.1107/S2053230X14004695
61. Arimura, Y., Kimura, H., Oda, T., Sato, K., Osakabe, A., Tachiwana, H., Sato, Y., Kinugasa, Y., Ikura, T., Sugiyama, M., Sato, M., and Kurumizaka, H. (2013) Structural basis of a nucleosome containing histone H2A.B/H2A.Bbd that transiently associates with reorganized chromatin Sci. Rep. 3, 3510 10.1038/srep03510
62. Sansoni, V., Casas-Delucchi, C. S., Rajan, M., Schmidt, A., Bonisch, C., Thomae, A. W., Staege, M. S., Hake, S. B., Cardoso, M. C., and Imhof, A. (2014) The histone variant H2A.Bbd is enriched at sites of DNA synthesis Nucleic Acids Res. 42, 6405-6420 10.1093/nar/gku303
63. Ishibashi, T., Li, A., Eirin-Lopez, J. M., Zhao, M., Missiaen, K., Abbott, D. W., Meistrich, M., Hendzel, M. J., and Ausió, J. (2010) H2A.Bbd: an X-chromosome-encoded histone involved in mammalian spermiogenesis Nucleic Acids Res. 38, 1780-1789 10.1093/nar/gkp1129
64. Padavattan, S., Shinagawa, T., Hasegawa, K., Kumasaka, T., Ishii, S., and Kumarevel, T. (2015) Structural and functional analyses of nucleosome complexes with mouse histone variants TH2a and TH2b, involved in reprogramming Biochem. Biophys. Res. Commun. 464, 929-935 10.1016/j.bbrc.2015.07.070