Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1989 Mar;9(3):902–913. doi: 10.1128/mcb.9.3.902

Expression of replication-dependent histone genes in avian spermatids involves an alternate pathway of mRNA 3'-end formation.

P B Challoner 1, S B Moss 1, M Groudine 1
PMCID: PMC362679  PMID: 2471062

Abstract

In somatic cells the expression of replication-dependent histone genes is coupled to the S phase of the cell cycle. However, we have found a number of novel H2a, H2b, and H3 poly(A)+ RNA species in avian haploid round spermatids. The spermatid-specific H2a and H2b 0.8-kilobase RNAs are transcribed from a subset of the replication-dependent H2a and H2b gene families. Two cDNAs derived from the spermatid-specific H2b transcripts were isolated and sequenced. The structures of these cDNAs reveal that the spermatid-specific RNAs are identical to the 0.5-kilobase poly(A)- H2b mRNAs expressed in proliferating somatic cells, except for the addition of poly(A) at the 3' ends. The site of poly(A) addition in the spermatid-specific RNAs is located 26 to 28 nucleotides 3' of the poly(A)- H2b mRNA terminus. Thus, the hairpin structures and purine-rich elements required for the U7 small nuclear ribonucleoprotein-mediated cleavage reaction that generates the 3' ends of poly(A)- H2b mRNAs are not utilized in spermatids and are retained in the poly(A)+ H2b RNAs.

Full text

PDF
902

Images in this article

905Image
on p.905
905Image
on p.905
907Image
on p.907
909Image
on p.909

Selected References

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

  1. Alterman R. B., Sprecher C., Graves R., Marzluff W. F., Skoultchi A. I. Regulated expression of a chimeric histone gene introduced into mouse fibroblasts. Mol Cell Biol. 1985 Sep;5(9):2316–2324. doi: 10.1128/mcb.5.9.2316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ballantine J. E., Woodland H. R. Polyadenylation of histone mRNA in Xenopus oocytes and embryos. FEBS Lett. 1985 Jan 28;180(2):224–228. doi: 10.1016/0014-5793(85)81075-9. [DOI] [PubMed] [Google Scholar]
  3. Birchmeier C., Folk W., Birnstiel M. L. The terminal RNA stem-loop structure and 80 bp of spacer DNA are required for the formation of 3' termini of sea urchin H2A mRNA. Cell. 1983 Dec;35(2 Pt 1):433–440. doi: 10.1016/0092-8674(83)90176-9. [DOI] [PubMed] [Google Scholar]
  4. Birchmeier C., Grosschedl R., Birnstiel M. L. Generation of authentic 3' termini of an H2A mRNA in vivo is dependent on a short inverted DNA repeat and on spacer sequences. Cell. 1982 Apr;28(4):739–745. doi: 10.1016/0092-8674(82)90053-8. [DOI] [PubMed] [Google Scholar]
  5. Birchmeier C., Schümperli D., Sconzo G., Birnstiel M. L. 3' editing of mRNAs: sequence requirements and involvement of a 60-nucleotide RNA in maturation of histone mRNA precursors. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1057–1061. doi: 10.1073/pnas.81.4.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blobel G. Release, identification, and isolation of messenger RNA from mammalian ribosomes. Proc Natl Acad Sci U S A. 1971 Apr;68(4):832–835. doi: 10.1073/pnas.68.4.832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blobel G., Sabatini D. Dissociation of mammalian polyribosomes into subunits by puromycin. Proc Natl Acad Sci U S A. 1971 Feb;68(2):390–394. doi: 10.1073/pnas.68.2.390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brock W. A., Trostle P. K., Meistrich M. L. Meiotic synthesis of testis histones in the rat. Proc Natl Acad Sci U S A. 1980 Jan;77(1):371–375. doi: 10.1073/pnas.77.1.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brush D., Dodgson J. B., Choi O. R., Stevens P. W., Engel J. D. Replacement variant histone genes contain intervening sequences. Mol Cell Biol. 1985 Jun;5(6):1307–1317. doi: 10.1128/mcb.5.6.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chambers A., Old R. RNA 3' cleavage and polyadenylation in oocytes and unfertilized eggs of Xenopus laevis. Dev Biol. 1988 Feb;125(2):237–245. doi: 10.1016/0012-1606(88)90207-2. [DOI] [PubMed] [Google Scholar]
  11. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  12. Chodchoy N., Levine B. J., Sprecher C., Skoultchi A. I., Marzluff W. F. Expression of mouse histone genes: transcription into 3' intergenic DNA and cryptic processing sites downstream from the 3' end of the H3 gene. Mol Cell Biol. 1987 Mar;7(3):1039–1047. doi: 10.1128/mcb.7.3.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cleveland D. W., Lopata M. A., MacDonald R. J., Cowan N. J., Rutter W. J., Kirschner M. W. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell. 1980 May;20(1):95–105. doi: 10.1016/0092-8674(80)90238-x. [DOI] [PubMed] [Google Scholar]
  14. Cole K. D., Kandala J. C., Kistler W. S. Isolation of the gene for the testis-specific H1 histone variant H1t. J Biol Chem. 1986 Jun 5;261(16):7178–7183. [PubMed] [Google Scholar]
  15. Cotten M., Gick O., Vasserot A., Schaffner G., Birnstiel M. L. Specific contacts between mammalian U7 snRNA and histone precursor RNA are indispensable for the in vitro 3' RNA processing reaction. EMBO J. 1988 Mar;7(3):801–808. doi: 10.1002/j.1460-2075.1988.tb02878.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. D'Andrea R. J., Coles L. S., Lesnikowski C., Tabe L., Wells J. R. Chromosomal organization of chicken histone genes: preferred associations and inverted duplications. Mol Cell Biol. 1985 Nov;5(11):3108–3115. doi: 10.1128/mcb.5.11.3108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dalton S., Wells J. R. A gene-specific promoter element is required for optimal expression of the histone H1 gene in S-phase. EMBO J. 1988 Jan;7(1):49–56. doi: 10.1002/j.1460-2075.1988.tb02782.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. DeLisle A. J., Graves R. A., Marzluff W. F., Johnson L. F. Regulation of histone mRNA production and stability in serum-stimulated mouse 3T6 fibroblasts. Mol Cell Biol. 1983 Nov;3(11):1920–1929. doi: 10.1128/mcb.3.11.1920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dugaiczyk A., Haron J. A., Stone E. M., Dennison O. E., Rothblum K. N., Schwartz R. J. Cloning and sequencing of a deoxyribonucleic acid copy of glyceraldehyde-3-phosphate dehydrogenase messenger ribonucleic acid isolated from chicken muscle. Biochemistry. 1983 Mar 29;22(7):1605–1613. doi: 10.1021/bi00276a013. [DOI] [PubMed] [Google Scholar]
  20. Engel J. D., Sugarman B. J., Dodgson J. B. A chicken histone H3 gene contains intervening sequences. Nature. 1982 Jun 3;297(5865):434–436. doi: 10.1038/297434a0. [DOI] [PubMed] [Google Scholar]
  21. Fletcher C., Heintz N., Roeder R. G. Purification and characterization of OTF-1, a transcription factor regulating cell cycle expression of a human histone H2b gene. Cell. 1987 Dec 4;51(5):773–781. doi: 10.1016/0092-8674(87)90100-0. [DOI] [PubMed] [Google Scholar]
  22. Gick O., Krämer A., Vasserot A., Birnstiel M. L. Heat-labile regulatory factor is required for 3' processing of histone precursor mRNAs. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8937–8940. doi: 10.1073/pnas.84.24.8937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Grandy D. K., Dodgson J. B. Structure and organization of the chicken H2B histone gene family. Nucleic Acids Res. 1987 Feb 11;15(3):1063–1080. doi: 10.1093/nar/15.3.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Grandy D. K., Engel J. D., Dodgson J. B. Complete nucleotide sequence of a chicken H2b histone gene. J Biol Chem. 1982 Aug 10;257(15):8577–8580. [PubMed] [Google Scholar]
  25. Groudine M., Peretz M., Weintraub H. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol Cell Biol. 1981 Mar;1(3):281–288. doi: 10.1128/mcb.1.3.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Harvey R. P., Robins A. J., Wells J. R. Independently evolving chicken histone H2B genes: identification of a ubiquitous H2B-specific 5' element. Nucleic Acids Res. 1982 Dec 11;10(23):7851–7863. doi: 10.1093/nar/10.23.7851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Harvey R. P., Whiting J. A., Coles L. S., Krieg P. A., Wells J. R. H2A.F: an extremely variant histone H2A sequence expressed in the chicken embryo. Proc Natl Acad Sci U S A. 1983 May;80(10):2819–2823. doi: 10.1073/pnas.80.10.2819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hattori M., Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. doi: 10.1016/0003-2697(86)90403-3. [DOI] [PubMed] [Google Scholar]
  29. Heintz N., Sive H. L., Roeder R. G. Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol Cell Biol. 1983 Apr;3(4):539–550. doi: 10.1128/mcb.3.4.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kim Y. J., Hwang I., Tres L. L., Kierszenbaum A. L., Chae C. B. Molecular cloning and differential expression of somatic and testis-specific H2B histone genes during rat spermatogenesis. Dev Biol. 1987 Nov;124(1):23–34. doi: 10.1016/0012-1606(87)90455-6. [DOI] [PubMed] [Google Scholar]
  31. Krieg P. A., Melton D. A. Formation of the 3' end of histone mRNA by post-transcriptional processing. Nature. 1984 Mar 8;308(5955):203–206. doi: 10.1038/308203a0. [DOI] [PubMed] [Google Scholar]
  32. Krieg P. A., Robins A. J., Colman A., Wells J. R. Chicken histone H5 mRNA: the polyadenylated RNA lacks the conserved histone 3' terminator sequence. Nucleic Acids Res. 1982 Nov 11;10(21):6777–6785. doi: 10.1093/nar/10.21.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Levine B. J., Chodchoy N., Marzluff W. F., Skoultchi A. I. Coupling of replication type histone mRNA levels to DNA synthesis requires the stem-loop sequence at the 3' end of the mRNA. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6189–6193. doi: 10.1073/pnas.84.17.6189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Linial M., Gunderson N., Groudine M. Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science. 1985 Dec 6;230(4730):1126–1132. doi: 10.1126/science.2999973. [DOI] [PubMed] [Google Scholar]
  35. Lüscher B., Schümperli D. RNA 3' processing regulates histone mRNA levels in a mammalian cell cycle mutant. A processing factor becomes limiting in G1-arrested cells. EMBO J. 1987 Jun;6(6):1721–1726. doi: 10.1002/j.1460-2075.1987.tb02423.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. McLauchlan J., Gaffney D., Whitton J. L., Clements J. B. The consensus sequence YGTGTTYY located downstream from the AATAAA signal is required for efficient formation of mRNA 3' termini. Nucleic Acids Res. 1985 Feb 25;13(4):1347–1368. doi: 10.1093/nar/13.4.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Meijer D., Hermans A., von Lindern M., van Agthoven T., de Klein A., Mackenbach P., Grootegoed A., Talarico D., Della Valle G., Grosveld G. Molecular characterization of the testis specific c-abl mRNA in mouse. EMBO J. 1987 Dec 20;6(13):4041–4048. doi: 10.1002/j.1460-2075.1987.tb02749.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Moore C. L., Sharp P. A. Accurate cleavage and polyadenylation of exogenous RNA substrate. Cell. 1985 Jul;41(3):845–855. doi: 10.1016/s0092-8674(85)80065-9. [DOI] [PubMed] [Google Scholar]
  39. Mowry K. L., Steitz J. A. Identification of the human U7 snRNP as one of several factors involved in the 3' end maturation of histone premessenger RNA's. Science. 1987 Dec 18;238(4834):1682–1687. doi: 10.1126/science.2825355. [DOI] [PubMed] [Google Scholar]
  40. Pandey N. B., Marzluff W. F. The stem-loop structure at the 3' end of histone mRNA is necessary and sufficient for regulation of histone mRNA stability. Mol Cell Biol. 1987 Dec;7(12):4557–4559. doi: 10.1128/mcb.7.12.4557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Propst F., Rosenberg M. P., Vande Woude G. F. Proto-oncogene expression in germ cell development. Trends Genet. 1988 Jul;4(7):183–187. doi: 10.1016/0168-9525(88)90073-x. [DOI] [PubMed] [Google Scholar]
  42. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
  43. Ross J., Kobs G. H4 histone messenger RNA decay in cell-free extracts initiates at or near the 3' terminus and proceeds 3' to 5'. J Mol Biol. 1986 Apr 20;188(4):579–593. doi: 10.1016/s0022-2836(86)80008-0. [DOI] [PubMed] [Google Scholar]
  44. Ruiz-Carrillo A., Affolter M., Renaud J. Genomic organization of the genes coding for the six main histones of the chicken: complete sequence of the H5 gene. J Mol Biol. 1983 Nov 15;170(4):843–859. doi: 10.1016/s0022-2836(83)80191-0. [DOI] [PubMed] [Google Scholar]
  45. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Schümperli D. Cell-cycle regulation of histone gene expression. Cell. 1986 May 23;45(4):471–472. doi: 10.1016/0092-8674(86)90277-1. [DOI] [PubMed] [Google Scholar]
  47. Sittman D. B., Graves R. A., Marzluff W. F. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1849–1853. doi: 10.1073/pnas.80.7.1849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sive H. L., Heintz N., Roeder R. G. Multiple sequence elements are required for maximal in vitro transcription of a human histone H2B gene. Mol Cell Biol. 1986 Oct;6(10):3329–3340. doi: 10.1128/mcb.6.10.3329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Soldati D., Schümperli D. Structural and functional characterization of mouse U7 small nuclear RNA active in 3' processing of histone pre-mRNA. Mol Cell Biol. 1988 Apr;8(4):1518–1524. doi: 10.1128/mcb.8.4.1518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Sturm R. A., Dalton S., Wells J. R. Conservation of histone H2A/H2B intergene regions: a role for the H2B specific element in divergent transcription. Nucleic Acids Res. 1988 Sep 12;16(17):8571–8586. doi: 10.1093/nar/16.17.8571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Sugarman B. J., Dodgson J. B., Engel J. D. Genomic organization, DNA sequence, and expression of chicken embryonic histone genes. J Biol Chem. 1983 Jul 25;258(14):9005–9016. [PubMed] [Google Scholar]
  52. Thompson C. B., Challoner P. B., Neiman P. E., Groudine M. Expression of the c-myb proto-oncogene during cellular proliferation. 1986 Jan 30-Feb 5Nature. 319(6052):374–380. doi: 10.1038/319374a0. [DOI] [PubMed] [Google Scholar]
  53. Vogelstein B., Gillespie D. Preparative and analytical purification of DNA from agarose. Proc Natl Acad Sci U S A. 1979 Feb;76(2):615–619. doi: 10.1073/pnas.76.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Wang S. W., Robins A. J., d'Andrea R., Wells J. R. Inverted duplication of histone genes in chicken and disposition of regulatory sequences. Nucleic Acids Res. 1985 Feb 25;13(4):1369–1387. doi: 10.1093/nar/13.4.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES