Kinetics of histone gene expression during early development of Xenopus laevis.

Using literature data for transcriptional and translational rate constants, gene copy numbers, DNA concentrations, and stability constants, we have calculated the expected concentrations of histones and histone mRNA during embryogenesis of Xenopus laevis. The results led us to conclude that: (i) for X. laevis the gene copy number of the histone genes is too low to ensure the synthesis of sufficient histones during very early development, inheritance from the oocyte of either histone protein or histone mRNA (but not necessarily both) is necessary; (ii) from the known storage of histones in the oocyte and the rates of histone synthesis determined by Adamson & Woodland (1977), there would be sufficient histones to structure the newly synthesized DNA up to gastrulation but not thereafter (these empirical rates of histone synthesis may be underestimates); (iii) on the other hand, the amount of H3 mRNA recently observed during early embryogenesis (Koster, 1987, Koster et al., 1988) could direct a higher and sufficient synthesis of H3 protein, also after gastrulation. We present a quantitative model that accounts both for the observed H3 mRNA concentration as a function of time during embryogenesis and for the synthesis of sufficient histones to structure the DNA throughout early embryogenesis. The model suggests that X. laevis exhibits a major (i.e. some 14-fold) reduction in transcription of histone genes approximately 11 hours after fertilization. This reduction could be due to a decrease in the number of transcribed histone genes, a decreased rate constant of transcription with continued transcription of all the histone genes, and/or a reduction in the time during the cell cycle in which histone mRNA synthesis takes place. Alternatively, the histone mRNA stability might decrease approximately 16-fold 11 hours after fertilization.

[1]  J. Ruderman,et al.  Modulations of histone messenger RNA during the early development of Xenopus laevis. , 1979, Developmental biology.

[2]  K. Marcu,et al.  On the existence of polyadenylated histone mRNA in Xenopus laevis oocytes , 1976, Cell.

[3]  J. Gerhart Mechanisms Regulating Pattern Formation in the Amphibian Egg and Early Embryo , 1980 .

[4]  R. W. Morgan,et al.  Changes in the cell cycle during early amphibian development , 1966 .

[5]  M. Pardue,et al.  A portion of all major classes of histone messenger RNA in amphibian oocytes is polyadenylated. , 1978, The Journal of biological chemistry.

[6]  H. Woodland Changes in the polysome content of developing Xenopus laevis embryos. , 1974, Developmental biology.

[7]  S. Elgin,et al.  Chromosomal proteins and chromatin structure. , 1975, Annual review of biochemistry.

[8]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage , 1982, Cell.

[9]  A. Moorman,et al.  Quantitation of the accumulation of histone messenger RNA during oogenesis in Xenopus laevis. , 1981, Developmental biology.

[10]  J. Faber,et al.  Normal Table of Xenopus Laevis (Daudin) , 1958 .

[11]  H. Woodland,et al.  The functional stability of sea urchin histone mRNA injected into oocytes of Xenopus laevis. , 1980, Developmental biology.

[12]  E. Adamson,et al.  Histone synthesis in early amphibian development: histone and DNA syntheses are not co-ordinated. , 1974, Journal of molecular biology.

[13]  K. Shiokawa,et al.  Synthesis of heterogeneous mRNA-like RNA and low-molecular-weight RNA before the midblastula transition in embryos of Xenopus laevis. , 1987, Developmental biology.

[14]  H. Woodland The translational control phase of early development , 1982, Bioscience reports.

[15]  Ru-chih C. Huang,et al.  The Biology of Isolated Chromatin , 1968, Science.

[16]  L. D. Smith,et al.  Conservation of RNA polymerase during maturation of the Rana pipiens oocyte. , 1976, Developmental biology.

[17]  A. Moorman,et al.  The accumulation of the maternal pool of histone H1A during oogenesis in Xenopus laevis. , 1983, Cell differentiation.

[18]  R. Roeder,et al.  Genomic organization and nucleotide sequence of two distinct histone gene clusters from Xenopus laevis. Identification of novel conserved upstream sequence elements. , 1985, Journal of molecular biology.

[19]  J. Dumont Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals , 1972, Journal of morphology.

[20]  L. Kedes,et al.  Expression and organization of histone genes. , 1983, Annual review of genetics.

[21]  R. Chalkley,et al.  Histone segregation on replicating chromatin. , 1985, Biochemistry.

[22]  A. Moorman,et al.  The organization of the histone genes in the genome of Xenopus laevis. , 1981, Nucleic acids research.

[23]  R. Chalkley,et al.  Histone synthesis and deposition in the G1 and S phases of hepatoma tissue culture cells. , 1985, Biochemistry.

[24]  F. Kafatos The cocoonase zymogen cells of silk moths: a model of terminal cell differentiation for specific protein synthesis. , 1972, Current topics in developmental biology.

[25]  E. Adamson,et al.  The synthesis and storage of histones during the oogenesis of Xenopus laevis. , 1977, Developmental biology.

[26]  A. Mclaren,et al.  Current problems in germ cell differentiation , 1983 .

[27]  H. Woodland Histone synthesis during the development of Xenopus , 1980, FEBS letters.

[28]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[29]  N. Heintz,et al.  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 , 1983, Molecular and cellular biology.

[30]  H. Westerhoff,et al.  Modern theories of metabolic control and their applications , 1984, Bioscience reports.

[31]  I. Dawid,et al.  Differential gene expression in the gastrula of Xenopus laevis. , 1983, Science.

[32]  E. Adamson,et al.  Changes in the rate of histone synthesis during oocyte maturation and very early development of Xenopus laevis. , 1977, Developmental biology.

[33]  W. Bonner,et al.  Separation of basal histone synthesis from S-phase histone synthesis in dividing cells , 1981, Cell.

[34]  Eric H. Davidson,et al.  Gene activity in early development , 1968 .

[35]  J. Flynn,et al.  The synthesis of histone H1 during early amphibian development. , 1980, Developmental biology.

[36]  I. Dawid,et al.  Gene expression in Xenopus embryogenesis. , 1985, Journal of embryology and experimental morphology.

[37]  L. Kedes,et al.  Distinct organizations and patterns of expression of early and late histone gene sets in the sea urchin , 1983, Nature.

[38]  J. Richter,et al.  The mechanism for increased protein synthesis during Xenopus oocyte maturation. , 1982, Developmental biology.

[39]  Keith R. Yamamoto,et al.  Biological Regulation and Development , 1982, Springer US.

[40]  O. Destrée,et al.  Analysis of histones from different tissues and embryos of Xenopus laevis (Daudin). II. Qualitative and quantitative aspects of nuclear histones during early stages of development. , 1973, Cell differentiation.

[41]  H. Westerhoff,et al.  Thermodynamics and Control of Biological Free-Energy Transduction , 1987 .

[42]  R. Laskey,et al.  Assembly of SV40 chromatin in a cell-free system from Xenopus eggs , 1977, Cell.

[43]  J. Gall,et al.  Histone RNA in amphibian oocytes visualized by in situ hybridization to methacrylate‐embedded tissue sections. , 1984, The EMBO journal.

[44]  R. Simpson Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. , 1978, Biochemistry.

[45]  M. Birnstiel,et al.  The organization and expression of histone gene families , 1981, Cell.

[46]  R. Roeder Multiple forms of deoxyribonucleic acid-dependent ribonucleic acid polymerase in Xenopus laevis. Levels of activity during oocyte and embryonic development. , 1974, The Journal of biological chemistry.

[47]  E. Cronkite,et al.  Histone turnover within nonproliferating cells. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[48]  H. Woodland,et al.  The stability and translation of sea urchin histone messenger RNA molecules injected into Xenopus laevis eggs and developing embryos. , 1980, Developmental biology.

[49]  A. Goustin Two temporal phases for the control of histone gene activity in cleaving sea urchin embryos (S. purpuratus). , 1981, Developmental biology.

[50]  R. Britten,et al.  Molecular biology of the sea urchin embryo. , 1982, Science.

[51]  D. Anderson,et al.  Patterns of synthesis and accumulation of heterogeneous RNA in lampbrush stage oocytes of Xenopus laevis (Daudin). , 1978, Developmental biology.

[52]  I. Dawid,et al.  Deoxyribonucleic acid in amphibian eggs. , 1965, Journal of molecular biology.

[53]  M. Bendig Persistence and expression of histone genes injected into Xenopus eggs in early development , 1981, Nature.

[54]  R. Harland,et al.  Induction of chromosome replication during maturation of amphibian oocytes. , 1983, Ciba Foundation symposium.

[55]  O. Miller,et al.  Visualization of Nucleolar Genes , 1969, Science.

[56]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: II. control of the onset of transcription , 1982, Cell.