Crossref journal-article
Cold Spring Harbor Laboratory
Genes & Development (246)
Abstract

Sporulation in Saccharomyces cerevisiae is a highly regulated process wherein a diploid cell gives rise to four haploid gametes. In this study we show that histone H4 Ser1 is phosphorylated (H4 S1ph) during sporulation, starting from mid-sporulation and persisting to germination, and is temporally distinct from earlier meiosis-linked H3 S10ph involved in chromosome condensation. A histone H4 S1A substitution mutant forms aberrant spores and has reduced sporulation efficiency. Deletion of sporulation-specific yeast Sps1, a member of the Ste20 family of kinases, nearly abolishes the sporulation-associated H4 S1ph modification. H4 S1ph may promote chromatin compaction, since deletion of SPS1 increases accessibility to antibody immunoprecipitation; furthermore, either deletion of Sps1 or an H4 S1A substitution results in increased DNA volume in nuclei within spores. We find H4 S1ph present during Drosophila melanogaster and mouse spermatogenesis, and similar to yeast, this modification extends late into sperm differentiation relative to H3 S10ph. Thus, H4 S1ph may be an evolutionarily ancient histone modification to mark the genome for gamete-associated packaging.

Bibliography

Krishnamoorthy, T., Chen, X., Govin, J., Cheung, W. L., Dorsey, J., Schindler, K., Winter, E., Allis, C. D., Guacci, V., Khochbin, S., Fuller, M. T., & Berger, S. L. (2006). Phosphorylation of histone H4 Ser1 regulates sporulation in yeast and is conserved in fly and mouse spermatogenesis. Genes & Development, 20(18), 2580–2592.

Authors 12
  1. Thanuja Krishnamoorthy (first)
  2. Xin Chen (additional)
  3. Jerome Govin (additional)
  4. Wang L. Cheung (additional)
  5. Jean Dorsey (additional)
  6. Karen Schindler (additional)
  7. Edward Winter (additional)
  8. C. David Allis (additional)
  9. Vincent Guacci (additional)
  10. Saadi Khochbin (additional)
  11. Margaret T. Fuller (additional)
  12. Shelley L. Berger (additional)
References 70 Referenced 84
  1. 10.1016/j.cell.2004.11.016
  2. 10.4161/cc.4.6.1745 / Cell Cycle / H2B (Ser10) phosphorylation is induced during apoptosis and meiosis in S. cerevisiae by Ahn, (2005)
  3. 10.1007/s00412-004-0281-9
  4. 10.1016/0076-6879(93)25009-Q
  5. 10.1101/gad.1101503
  6. 10.1101/gad.4.10.1775
  7. 10.1073/pnas.96.12.6835
  8. 10.1074/jbc.M006801200
  9. 10.1016/S0092-8674(03)00355-6
  10. 10.1016/j.cub.2005.02.049
  11. 10.1038/88313
  12. 10.1074/jbc.M102531200
  13. 10.1016/S1097-2765(00)80068-4
  14. 10.1126/science.282.5389.699
  15. 10.1128/MCB.15.7.3685 / Mol. Cell. Biol. / Bdf1, a yeast chromosomal protein required for sporulation by Chua, (1995)
  16. 10.1006/dbio.1998.9101
  17. 10.1128/MCB.21.8.2726-2735.2001
  18. 10.1016/S0022-2836(03)00025-1
  19. 10.1101/gad.8.18.2162
  20. Fuller, M.T. (1993) in The development of Drosophila melanogaster, Spermatogenesis, eds Bate M. MartinezArias A. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), pp 71–148.
  21. 10.1074/jbc.274.36.25543
  22. 10.1046/j.1356-9597.2001.00498.x
  23. 10.1111/j.1432-1033.2004.04266.x / Eur. J. Biochem. / The role of histones in chromatin remodelling during mammalian spermiogenesis by Govin, (2004)
  24. 10.1083/jcb.125.3.517
  25. 10.1016/0006-291X(73)91307-7
  26. 10.1007/s004120050256
  27. 10.1101/gad.1144003
  28. 10.1242/jcs.109.12.2779 / J. Cell Sci. / Assembly of ring canals in the male germ line from structural components of the contractile ring by Hime, (1996)
  29. 10.1016/S0092-8674(00)00034-9
  30. 10.1016/S1097-2765(02)00826-2
  31. 10.1128/EC.4.3.536-544.2005
  32. 10.1038/nature03368
  33. 10.1128/jb.124.2.863-869.1975 / J. Bacteriol. / Proteinase activities of Saccharomyces cerevisiae during sporulation by Klar, (1975)
  34. 10.1101/gad.8.18.2151
  35. Kupiec, M. Byers, B. Esposito, R.E. Mitchell, A.P. (1997) in The molecular and cellular biology of the yeast Saccharomyces, Meiosis and sporulation in Saccharomyces cerevisiae ed Pringle J.R. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), pp 889–1036.
  36. {'key': '2021111607424709000_20.18.2580.36', 'first-page': '912', 'article-title': 'The SPS100 gene of Saccharomyces cerevisiae is activated late in the sporulation process and contributes to spore wall maturation', 'volume': '8', 'author': 'Law,', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / The SPS100 gene of Saccharomyces cerevisiae is activated late in the sporulation process and contributes to spore wall maturation by Law, (1988)
  37. 10.1073/pnas.0308721101
  38. 10.1016/S1097-2765(00)80257-9
  39. 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U
  40. 10.1038/38444
  41. 10.1083/jcb.44.3.688
  42. 10.1021/bi0117652
  43. 10.1007/s00412-002-0227-z
  44. 10.1128/mr.58.1.56-70.1994 / Microbiol. Rev. / Control of meiotic gene expression in Saccharomyces cerevisiae by Mitchell, (1994)
  45. 10.1006/bbrc.1996.5903
  46. 10.1091/mbc.8.12.2421
  47. 10.1016/j.tig.2004.02.007
  48. 10.1016/S0079-6603(08)60839-9
  49. 10.1016/S0021-9258(20)65105-5 / J. Biol. Chem. / Phosphorylation of histones 1 and 3 and nonhistone high mobility group 14 by an endogenous kinase in HeLa metaphase chromosomes by Paulson, (1982)
  50. {'key': '2021111607424709000_20.18.2580.50', 'first-page': '2443', 'article-title': 'Characterization and mutational analysis of a cluster of three genes expressed preferentially during sporulation of Saccharomyces cerevisiae', 'volume': '6', 'author': 'Percival-Smith,', 'year': '1986', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Characterization and mutational analysis of a cluster of three genes expressed preferentially during sporulation of Saccharomyces cerevisiae by Percival-Smith, (1986)
  51. 10.1128/MCB.23.15.5354-5365.2003
  52. 10.1016/S0014-5793(04)00060-2
  53. 10.1093/nar/gkg176
  54. 10.1038/82539
  55. 10.1126/science.287.5452.501
  56. 10.1038/33952
  57. 10.1126/science.1070963
  58. 10.1126/science.1124000
  59. 10.1038/sj.emboj.7600204
  60. 10.1073/pnas.67.3.1616
  61. 10.1038/81971
  62. 10.1128/MCB.25.18.8179-8190.2005
  63. 10.1016/S0092-8674(00)80718-7
  64. 10.1016/S1097-2765(02)00802-X
  65. 10.1038/78153
  66. 10.1126/science.1087795
  67. 10.1073/pnas.0400078101
  68. 10.1073/pnas.97.9.4683
  69. 10.1128/MCB.21.21.7243-7255.2001
  70. 10.1002/bip.10303
Dates
Type When
Created 18 years, 11 months ago (Sept. 15, 2006, 7:10 p.m.)
Deposited 3 years, 9 months ago (Nov. 16, 2021, 11:58 a.m.)
Indexed 1 year ago (Aug. 5, 2024, 7:14 p.m.)
Issued 18 years, 11 months ago (Sept. 15, 2006)
Published 18 years, 11 months ago (Sept. 15, 2006)
Published Online 18 years, 11 months ago (Sept. 15, 2006)
Published Print 18 years, 11 months ago (Sept. 15, 2006)
Funders 0

None

@article{Krishnamoorthy_2006, title={Phosphorylation of histone H4 Ser1 regulates sporulation in yeast and is conserved in fly and mouse spermatogenesis}, volume={20}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.1457006}, DOI={10.1101/gad.1457006}, number={18}, journal={Genes &amp; Development}, publisher={Cold Spring Harbor Laboratory}, author={Krishnamoorthy, Thanuja and Chen, Xin and Govin, Jerome and Cheung, Wang L. and Dorsey, Jean and Schindler, Karen and Winter, Edward and Allis, C. David and Guacci, Vincent and Khochbin, Saadi and Fuller, Margaret T. and Berger, Shelley L.}, year={2006}, month=sep, pages={2580–2592} }