Involvement of the linker histone H1Foo in the regulation of oogenesis

in Reproduction
Authors:
Satoshi FunayaDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan

Search for other papers by Satoshi Funaya in
Current site
Google Scholar
PubMed
Close
,
Yuria KawabataDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan

Search for other papers by Yuria Kawabata in
Current site
Google Scholar
PubMed
Close
,
Kenta SugieDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan

Search for other papers by Kenta Sugie in
Current site
Google Scholar
PubMed
Close
,
Ken-ichiro AbeDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan

Search for other papers by Ken-ichiro Abe in
Current site
Google Scholar
PubMed
Close
,
Yutaka SuzukiDepartment of Computational Biology and Medical Sciences, Graduate school of Frontier Sciences, The University of Tokyo, Kashiwa, Japan

Search for other papers by Yutaka Suzuki in
Current site
Google Scholar
PubMed
Close
,
Masataka G SuzukiDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan

Search for other papers by Masataka G Suzuki in
Current site
Google Scholar
PubMed
Close
, and
Fugaku AokiDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan

Search for other papers by Fugaku Aoki in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-7036-4024
View More View Less

Correspondence should be addressed to F Aoki; Email: aokif@edu.k.u-tokyo.ac.jp

*(S Funaya and Y Kawabata contributed equally to this work)

Restricted access

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $1.00
USD  $1.00

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $1.00
USD  $1.00

USD  $1.00
USD  $1.00

In brief

In oocytes, chromatin structure is loosened during their growth, which seems to be essential for the establishment of competence to accomplish the maturation and further development after fertilization. This paper shows that a linker histone variant, H1foo, is involved in the formation of loosened chromatin structure in growing oocytes.

Abstract

During oogenesis, oocytes show a unique mode of division and gene expression patterns. Chromatin structure is thought to be involved in the regulation of these processes. In this study, we investigated the functions of linker histones, which modulate higher-order chromatin structure during oogenesis. Because H1foo is highly expressed in oocytes, we knocked down H1foo using siRNA and observed oocyte growth, maturation, and fertilization. However, H1foo knockdown had no effect on any of these processes. Overexpression of H1b or H1d, which has a high ability to condense chromatin and is expressed at a low level in oocytes, resulting in tightened chromatin and a decreased success rate of oocyte maturation. By contrast, overexpression of H1a, which is expressed at a high level in oocytes and has a low ability to compact chromatin, did not affect growth or maturation. Therefore, H1a, but not other variants, might compensate for the function of H1foo in H1foo-knockdown oocytes. These results implicate H1foo in the formation of loose chromatin structure, which is necessary for oocyte maturation. In addition, the low expression of somatic linker histone variants, for example, H1b and H1d, is important for loosened chromatin and meiotic progression.

 

  • Collapse
  • Expand
  • Abe K, Inoue A, Suzuki MG & Aoki F 2010 Global gene silencing is caused by the dissociation of RNA polymerase II from DNA in mouse oocytes. Journal of Reproduction and Development 56 502507. (https://doi.org/10.1262/jrd.10-068a)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Abe K, Yamamoto R, Franke V, Cao M, Suzuki Y, Suzuki MG, Vlahovicek K, Svoboda P, Schultz RM & Aoki F 2015 The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3’ processing. EMBO Journal 34 15231537. (https://doi.org/10.15252/embj.201490648)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bednar J, Horowitz RA, Grigoryev SA, Carruthers LM, Hansen JC, Koster AJ & Woodcock CL 1998 Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. PNAS 95 1417314178. (https://doi.org/10.1073/pnas.95.24.14173)

    • Search Google Scholar
    • Export Citation
  • Bednar J, Hamiche A & Dimitrov S 2016 H1-nucleosome interactions and their functional implications. Biochimica et Biophysica Acta 1859 436443. (https://doi.org/10.1016/j.bbagrm.2015.10.012)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chalut KJ, Höpfler M, Lautenschläger F, Boyde L, Chan CJ, Ekpenyong A, martinez-Arias A & Guck J 2012 Chromatin decondensation and nuclear softening accompany Nanog downregulation in embryonic stem cells. Biophysical Journal 103 20602070. (https://doi.org/10.1016/j.bpj.2012.10.015)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Clarke HJ, Bustin M & Oblin C 1997 Chromatin modifications during oogenesis in the mouse: removal of somatic subtypes of histone H1 from oocyte chromatin occurs post-natally through a post-transcriptional mechanism. Journal of Cell Science 110 477487. (https://doi.org/10.1242/jcs.110.4.477)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Clausell J, Happel N, Hale TK, Doenecke D & Beato M 2009 Histone H1 subtypes differentially modulate chromatin condensation without preventing ATP-dependent remodeling by SWI/SNF or NURF. PLoS ONE 4 e0007243. (https://doi.org/10.1371/journal.pone.0007243)

    • Search Google Scholar
    • Export Citation
  • Drabent B, Bode C, Bramlage B & Doenecke D 1996 Expression of the mouse testicular histone gene H1t during spermatogenesis. Histochemistry and Cell Biology 106 247251. (https://doi.org/10.1007/BF02484408)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Evans JP, Schultz RM & Kopf GS 1995 Identification and localization of integrin subunits in oocytes and eggs of the mouse. Molecular Reproduction and Development 40 211220. (https://doi.org/10.1002/mrd.1080400210)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fan Y, Sirotkin A, Russell RG, Ayala J & Skoultchi AI 2001 Individual somatic H1 subtypes are dispensable for mouse development even in mice lacking the H1(0) replacement subtype. Molecular and Cellular Biology 21 79337943. (https://doi.org/10.1128/MCB.21.23.7933-7943.2001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fan Y, Nikitina T, morin-Kensicki EM, Zhao J, Magnuson TR, Woodcock CL & Skoultchi AI 2003 H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Molecular and Cellular Biology 23 45594572. (https://doi.org/10.1128/MCB.23.13.4559-4572.2003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Funaya S, Ooga M, Suzuki MG & Aoki F 2018 Linker histone H1FOO regulates the chromatin structure in mouse zygotes. FEBS Letters 592 24142424. (https://doi.org/10.1002/1873-3468.13175)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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. Journal of Reproduction and Development 53 895902. (https://doi.org/10.1262/jrd.19008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP & Surani MA 2010 Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329 7882. (https://doi.org/10.1126/science.1187945)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Inoue A & Zhang Y 2014 Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nature Structural and Molecular Biology 21 609616. (https://doi.org/10.1038/nsmb.2839)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Inoue A, Nakajima R, Nagata M & Aoki F 2008 Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Human Reproduction 23 13771384. (https://doi.org/10.1093/humrep/den096)

    • Search Google Scholar
    • Export Citation
  • Izzo A, ziegler-Birling C, Hill PWS, Brondani L, Hajkova P, torres-Padilla ME & Schneider R 2017 Dynamic changes in H1 subtype composition during epigenetic reprogramming. Journal of Cell Biology 216 30173028. (https://doi.org/10.1083/jcb.201611012)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lawitts JA & Biggers JD 1993 Culture of preimplantation embryos. Methods in Enzymology 225 153164. (https://doi.org/10.1016/0076-6879(9325012-q)

  • Lennox RW & Cohen LH 1983 The histone H1 complements of dividing and nondividing cells of the mouse. Journal of Biological Chemistry 258 262268. (https://doi.org/10.1016/S0021-9258(1833251-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lin CJ, Conti M & ramalho-Santos M 2013 Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development. Development 140 36243634. (https://doi.org/10.1242/dev.095513)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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. PNAS 102 28082813. (https://doi.org/10.1073/pnas.0406060102)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Martin RM & Cardoso MC 2010 Chromatin condensation modulates access and binding of nuclear proteins. FASEB Journal 24 10661072. (https://doi.org/10.1096/fj.08-128959)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Moore GP, lintern-Moore S, Peters H & Faber M 1974 RNA synthesis in the mouse oocyte. Journal of Cell Biology 60 416422. (https://doi.org/10.1083/jcb.60.2.416)

  • Ooga M, Fulka H, Hashimoto S, Suzuki MG & Aoki F 2016 Analysis of chromatin structure in mouse preimplantation embryos by fluorescent recovery after photobleaching. Epigenetics 11 8594. (https://doi.org/10.1080/15592294.2015.1136774)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ooga M, Funaya S, Hashioka Y, Fujii W, Naito K, Suzuki MG & Aoki F 2018 Chd9 mediates highly loosened chromatin structure in growing mouse oocytes. Biochemical and Biophysical Research Communications 500 583588. (https://doi.org/10.1016/j.bbrc.2018.04.105)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Orrego M, Ponte I, Roque A, Buschati N, Mora X & Suau P 2007 Differential affinity of mammalian histone H1 somatic subtypes for DNA and chromatin. BMC Biology 5 22. (https://doi.org/10.1186/1741-7007-5-22)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pan C & Fan Y 2016 Role of H1 linker histones in mammalian development and stem cell differentiation. Biochimica et Biophysica Acta 1859 496509. (https://doi.org/10.1016/j.bbagrm.2015.12.002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Popova EY, Grigoryev SA, Fan Y, Skoultchi AI, Zhang SS & Barnstable CJ 2013 Developmentally regulated linker histone H1c promotes heterochromatin condensation and mediates structural integrity of rod photoreceptors in mouse retina. Journal of Biological Chemistry 288 1789517907. (https://doi.org/10.1074/jbc.M113.452144)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Quinn P & Begley AJ 1984 Effect of human seminal plasma and mouse accessory gland extracts on mouse fertilization in vitro. Australian Journal of Biological Sciences 37 14752. (https://doi.org/10.1071/bi9840147)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rabini S, Franke K, Saftig P, Bode C, Doenecke D & Drabent B 2000 Spermatogenesis in mice is not affected by histone H1.1 deficiency. Experimental Cell Research 255 114124. (https://doi.org/10.1006/excr.1999.4767)

    • Search Google Scholar
    • Export Citation
  • Sirotkin AM, Edelmann W, Cheng G, klein-Szanto A, Kucherlapati R & Skoultchi AI 1995 Mice develop normally without the H1(0) linker histone. PNAS 92 64346438. (https://doi.org/10.1073/pnas.92.14.6434)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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 655664. (https://doi.org/10.1242/dev.128.5.655)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Th’ng JP, Sung R, Ye M & Hendzel MJ 2005 H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. Journal of Biological Chemistry 280 2780927814. (https://doi.org/10.1074/jbc.M501627200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Thoma F, Koller T & Klug A 1979 Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. Journal of Cell Biology 83 403427. (https://doi.org/10.1083/jcb.83.2.403)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Thomas FH & Vanderhyden BC 2006 Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reproductive Biology and Endocrinology 4 19. (https://doi.org/10.1186/1477-7827-4-19)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang ZF, Sirotkin AM, Buchold GM, Skoultchi AI & Marzluff WF 1997 The mouse histone H1 genes: gene organization and differential regulation. Journal of Molecular Biology 271 124138. (https://doi.org/10.1006/jmbi.1997.1166)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yamagata K, Yamazaki T, Yamashita M, Hara Y, Ogonuki N & Ogura A 2005 Noninvasive visualization of molecular events in the mammalian zygote. Genesis 43 7179. (https://doi.org/10.1002/gene.20158)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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. PNAS 100 1054610551. (https://doi.org/10.1073/pnas.1837812100)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zuccotti M, Ponce RH, Boiani M, Guizzardi S, Govoni P, Scandroglio R, Garagna S & Redi CA 2002 The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote 10 7378. (https://doi.org/10.1017/s0967199402002101)

    • PubMed
    • Search Google Scholar
    • Export Citation