Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1997 Sep;17(9):5033–5043. doi: 10.1128/mcb.17.9.5033

Identification of mouse histone deacetylase 1 as a growth factor-inducible gene.

S Bartl 1, J Taplick 1, G Lagger 1, H Khier 1, K Kuchler 1, C Seiser 1
PMCID: PMC232354  PMID: 9271381

Abstract

Reversible acetylation of core histones plays an important role in transcriptional regulation, cell cycle progression, and developmental events. The acetylation state of histones is controlled by the activities of acetylating and deacetylating enzymes. By using differential mRNA display, we have identified a mouse histone deacetylase gene, HD1, as an interleukin-2-inducible gene in murine T cells. Sequence alignments revealed that murine HD1 is highly homologous to the yeast RPD3 pleiotropic transcriptional regulator. Indirect immunofluorescence microscopy proved that mouse HD1 is a nuclear protein. When expressed in yeast, murine HD1 was also detected in the nucleus, although it failed to complement the rpd3delta deletion phenotype. HD1 mRNA expression was low in G0 mouse cells but increased when the cells crossed the G1/S boundary after growth stimulation. Immunoprecipitation experiments and functional in vitro assays showed that HD1 protein is associated with histone deacetylase activity. Both HD1 protein levels and total histone deacetylase activity increased upon interleukin-2 stimulation of resting B6.1 cells. When coexpressed with a luciferase reporter construct, HD1 acted as a negative regulator of the Rous sarcoma virus enhancer/promoter. HD1 overexpression in stably transfected Swiss 3T3 cells caused a severe delay during the G2/M phases of the cell cycle. Our results indicate that balanced histone acetylation/deacetylation is crucial for normal cell cycle progression of mammalian cells.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Adamczewski J. P., Gannon J. V., Hunt T. Simian virus 40 large T antigen associates with cyclin A and p33cdk2. J Virol. 1993 Nov;67(11):6551–6557. doi: 10.1128/jvi.67.11.6551-6557.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Almouzni G., Khochbin S., Dimitrov S., Wolffe A. P. Histone acetylation influences both gene expression and development of Xenopus laevis. Dev Biol. 1994 Oct;165(2):654–669. doi: 10.1006/dbio.1994.1283. [DOI] [PubMed] [Google Scholar]
  3. Alonso W. R., Nelson D. A. A novel yeast histone deacetylase: partial characterization and development of an activity assay. Biochim Biophys Acta. 1986 Mar 26;866(2-3):161–169. doi: 10.1016/0167-4781(86)90113-2. [DOI] [PubMed] [Google Scholar]
  4. Annunziato A. T., Seale R. L. Histone deacetylation is required for the maturation of newly replicated chromatin. J Biol Chem. 1983 Oct 25;258(20):12675–12684. [PubMed] [Google Scholar]
  5. Arts J., Lansink M., Grimbergen J., Toet K. H., Kooistra T. Stimulation of tissue-type plasminogen activator gene expression by sodium butyrate and trichostatin A in human endothelial cells involves histone acetylation. Biochem J. 1995 Aug 15;310(Pt 1):171–176. doi: 10.1042/bj3100171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Attisano L., Lewis P. N. Purification and characterization of two porcine liver nuclear histone acetyltransferases. J Biol Chem. 1990 Mar 5;265(7):3949–3955. [PubMed] [Google Scholar]
  7. Ayer D. E., Lawrence Q. A., Eisenman R. N. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell. 1995 Mar 10;80(5):767–776. doi: 10.1016/0092-8674(95)90355-0. [DOI] [PubMed] [Google Scholar]
  8. Ballester R., Michaeli T., Ferguson K., Xu H. P., McCormick F., Wigler M. Genetic analysis of mammalian GAP expressed in yeast. Cell. 1989 Nov 17;59(4):681–686. doi: 10.1016/0092-8674(89)90014-7. [DOI] [PubMed] [Google Scholar]
  9. Belikoff E., Wong L. J., Alberts B. M. Extensive purification of histone acetylase A, the major histone N-acetyl transferase activity detected in mammalian cell nuclei. J Biol Chem. 1980 Dec 10;255(23):11448–11453. [PubMed] [Google Scholar]
  10. Bradbury E. M. Reversible histone modifications and the chromosome cell cycle. Bioessays. 1992 Jan;14(1):9–16. doi: 10.1002/bies.950140103. [DOI] [PubMed] [Google Scholar]
  11. Braunstein M., Rose A. B., Holmes S. G., Allis C. D., Broach J. R. Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev. 1993 Apr;7(4):592–604. doi: 10.1101/gad.7.4.592. [DOI] [PubMed] [Google Scholar]
  12. Brosch G., Ransom R., Lechner T., Walton J. D., Loidl P. Inhibition of maize histone deacetylases by HC toxin, the host-selective toxin of Cochliobolus carbonum. Plant Cell. 1995 Nov;7(11):1941–1950. doi: 10.1105/tpc.7.11.1941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brownell J. E., Zhou J., Ranalli T., Kobayashi R., Edmondson D. G., Roth S. Y., Allis C. D. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell. 1996 Mar 22;84(6):843–851. doi: 10.1016/s0092-8674(00)81063-6. [DOI] [PubMed] [Google Scholar]
  14. Egner R., Mahé Y., Pandjaitan R., Kuchler K. Endocytosis and vacuolar degradation of the plasma membrane-localized Pdr5 ATP-binding cassette multidrug transporter in Saccharomyces cerevisiae. Mol Cell Biol. 1995 Nov;15(11):5879–5887. doi: 10.1128/mcb.15.11.5879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Evan G. I., Lewis G. K., Ramsay G., Bishop J. M. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol. 1985 Dec;5(12):3610–3616. doi: 10.1128/mcb.5.12.3610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Futamura M., Monden Y., Okabe T., Fujita-Yoshigaki J., Yokoyama S., Nishimura S. Trichostatin A inhibits both ras-induced neurite outgrowth of PC12 cells and morphological transformation of NIH3T3 cells. Oncogene. 1995 Mar 16;10(6):1119–1123. [PubMed] [Google Scholar]
  17. Garcea R. L., Alberts B. M. Comparative studies of histone acetylation in nucleosomes, nuclei, and intact cells. Evidence for special factors which modify acetylase action. J Biol Chem. 1980 Dec 10;255(23):11454–11463. [PubMed] [Google Scholar]
  18. Georgieva E. I., López-Rodas G., Sendra R., Gröbner P., Loidl P. Histone acetylation in Zea mays. II. Biological significance of post-translational histone acetylation during embryo germination. J Biol Chem. 1991 Oct 5;266(28):18751–18760. [PubMed] [Google Scholar]
  19. Girardot V., Rabilloud T., Yoshida M., Beppu T., Lawrence J. J., Khochbin S. Relationship between core histone acetylation and histone H1(0) gene activity. Eur J Biochem. 1994 Sep 15;224(3):885–892. doi: 10.1111/j.1432-1033.1994.00885.x. [DOI] [PubMed] [Google Scholar]
  20. Grabher A., Brosch G., Sendra R., Lechner T., Eberharter A., Georgieva E. I., López-Rodas G., Franco L., Dietrich H., Loidl P. Subcellular location of enzymes involved in core histone acetylation. Biochemistry. 1994 Dec 13;33(49):14887–14895. doi: 10.1021/bi00253a028. [DOI] [PubMed] [Google Scholar]
  21. Halleck M. S., Pownall S., Harder K. W., Duncan A. M., Jirik F. R., Schlegel R. A. A widely distributed putative mammalian transcriptional regulator containing multiple paired amphipathic helices, with similarity to yeast SIN3. Genomics. 1995 Mar 20;26(2):403–406. doi: 10.1016/0888-7543(95)80229-f. [DOI] [PubMed] [Google Scholar]
  22. Hay C. W., Candido E. P. Histone deacetylase. Association with a nuclease resistant, high molecular weight fraction of HeLa cell chromatin. J Biol Chem. 1983 Mar 25;258(6):3726–3734. [PubMed] [Google Scholar]
  23. Hofbauer R., Müllner E., Seiser C., Wintersberger E. Cell cycle regulated synthesis of stable mouse thymidine kinase mRNA is mediated by a sequence within the cDNA. Nucleic Acids Res. 1987 Jan 26;15(2):741–752. doi: 10.1093/nar/15.2.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hoshikawa Y., Kwon H. J., Yoshida M., Horinouchi S., Beppu T. Trichostatin A induces morphological changes and gelsolin expression by inhibiting histone deacetylase in human carcinoma cell lines. Exp Cell Res. 1994 Sep;214(1):189–197. doi: 10.1006/excr.1994.1248. [DOI] [PubMed] [Google Scholar]
  25. Inoue A., Fujimoto D. Histone deacetylase from calf thymus. Biochim Biophys Acta. 1970 Nov 11;220(2):307–316. doi: 10.1016/0005-2744(70)90015-x. [DOI] [PubMed] [Google Scholar]
  26. Jeppesen P., Turner B. M. The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell. 1993 Jul 30;74(2):281–289. doi: 10.1016/0092-8674(93)90419-q. [DOI] [PubMed] [Google Scholar]
  27. Jones J. S., Prakash L. Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast. 1990 Sep-Oct;6(5):363–366. doi: 10.1002/yea.320060502. [DOI] [PubMed] [Google Scholar]
  28. Kaufman P. D. Nucleosome assembly: the CAF and the HAT. Curr Opin Cell Biol. 1996 Jun;8(3):369–373. doi: 10.1016/s0955-0674(96)80012-3. [DOI] [PubMed] [Google Scholar]
  29. Kayne P. S., Kim U. J., Han M., Mullen J. R., Yoshizaki F., Grunstein M. Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. Cell. 1988 Oct 7;55(1):27–39. doi: 10.1016/0092-8674(88)90006-2. [DOI] [PubMed] [Google Scholar]
  30. Kijima M., Yoshida M., Sugita K., Horinouchi S., Beppu T. Trapoxin, an antitumor cyclic tetrapeptide, is an irreversible inhibitor of mammalian histone deacetylase. J Biol Chem. 1993 Oct 25;268(30):22429–22435. [PubMed] [Google Scholar]
  31. Kleff S., Andrulis E. D., Anderson C. W., Sternglanz R. Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem. 1995 Oct 20;270(42):24674–24677. doi: 10.1074/jbc.270.42.24674. [DOI] [PubMed] [Google Scholar]
  32. Lechner T., Lusser A., Brosch G., Eberharter A., Goralik-Schramel M., Loidl P. A comparative study of histone deacetylases of plant, fungal and vertebrate cells. Biochim Biophys Acta. 1996 Sep 5;1296(2):181–188. doi: 10.1016/0167-4838(96)00069-6. [DOI] [PubMed] [Google Scholar]
  33. Liang P., Pardee A. B. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992 Aug 14;257(5072):967–971. doi: 10.1126/science.1354393. [DOI] [PubMed] [Google Scholar]
  34. Loidl P. Histone acetylation: facts and questions. Chromosoma. 1994 Dec;103(7):441–449. doi: 10.1007/BF00337382. [DOI] [PubMed] [Google Scholar]
  35. Loidl P. Towards an understanding of the biological function of histone acetylation. FEBS Lett. 1988 Jan 25;227(2):91–95. doi: 10.1016/0014-5793(88)80874-3. [DOI] [PubMed] [Google Scholar]
  36. López-Rodas G., Brosch G., Golderer G., Lindner H., Gröbner P., Loidl P. Enzymes involved in the dynamic equilibrium of core histone acetylation of Physarum polycephalum. FEBS Lett. 1992 Jan 13;296(1):82–86. doi: 10.1016/0014-5793(92)80408-9. [DOI] [PubMed] [Google Scholar]
  37. López-Rodas G., Georgieva E. I., Sendra R., Loidl P. Histone acetylation in Zea mays.I. Activities of histone acetyltransferases and histone deacetylases. J Biol Chem. 1991 Oct 5;266(28):18745–18750. [PubMed] [Google Scholar]
  38. López-Rodas G., Tordera V., Sánchez del Pino M. M., Franco L. Yeast contains multiple forms of histone acetyltransferase. J Biol Chem. 1989 Nov 15;264(32):19028–19033. [PubMed] [Google Scholar]
  39. McKenzie E. A., Kent N. A., Dowell S. J., Moreno F., Bird L. E., Mellor J. The centromere and promoter factor, 1, CPF1, of Saccharomyces cerevisiae modulates gene activity through a family of factors including SPT21, RPD1 (SIN3), RPD3 and CCR4. Mol Gen Genet. 1993 Sep;240(3):374–386. doi: 10.1007/BF00280389. [DOI] [PubMed] [Google Scholar]
  40. Megee P. C., Morgan B. A., Mittman B. A., Smith M. M. Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science. 1990 Feb 16;247(4944):841–845. doi: 10.1126/science.2106160. [DOI] [PubMed] [Google Scholar]
  41. Megee P. C., Morgan B. A., Smith M. M. Histone H4 and the maintenance of genome integrity. Genes Dev. 1995 Jul 15;9(14):1716–1727. doi: 10.1101/gad.9.14.1716. [DOI] [PubMed] [Google Scholar]
  42. Miyashita T., Yamamoto H., Nishimune Y., Nozaki M., Morita T., Matsushiro A. Activation of the mouse cytokeratin A (endo A) gene in teratocarcinoma F9 cells by the histone deacetylase inhibitor Trichostatin A. FEBS Lett. 1994 Oct 17;353(2):225–229. doi: 10.1016/0014-5793(94)01034-x. [DOI] [PubMed] [Google Scholar]
  43. Mold D. E., McCarty K. S., Sr A Chinese hamster ovary cell histone deacetylase that is associated with a unique class of mononucleosomes. Biochemistry. 1987 Dec 15;26(25):8257–8262. doi: 10.1021/bi00399a036. [DOI] [PubMed] [Google Scholar]
  44. Morgenstern J. P., Land H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 1990 Jun 25;18(12):3587–3596. doi: 10.1093/nar/18.12.3587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Nasmyth K., Stillman D., Kipling D. Both positive and negative regulators of HO transcription are required for mother-cell-specific mating-type switching in yeast. Cell. 1987 Feb 27;48(4):579–587. doi: 10.1016/0092-8674(87)90236-4. [DOI] [PubMed] [Google Scholar]
  46. O'Neill L. P., Turner B. M. Histone H4 acetylation distinguishes coding regions of the human genome from heterochromatin in a differentiation-dependent but transcription-independent manner. EMBO J. 1995 Aug 15;14(16):3946–3957. doi: 10.1002/j.1460-2075.1995.tb00066.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Pear W. S., Nolan G. P., Scott M. L., Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8392–8396. doi: 10.1073/pnas.90.18.8392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Perry C. A., Annunziato A. T. Histone acetylation reduces H1-mediated nucleosome interactions during chromatin assembly. Exp Cell Res. 1991 Oct;196(2):337–345. doi: 10.1016/0014-4827(91)90269-z. [DOI] [PubMed] [Google Scholar]
  49. Pesis K. H., Matthews H. R. Histone acetylation in replication and transcription: turnover at specific acetylation sites in histone H4 from Physarum polycephalum. Arch Biochem Biophys. 1986 Dec;251(2):665–673. doi: 10.1016/0003-9861(86)90376-0. [DOI] [PubMed] [Google Scholar]
  50. Ramanathan B., Smerdon M. J. Enhanced DNA repair synthesis in hyperacetylated nucleosomes. J Biol Chem. 1989 Jul 5;264(19):11026–11034. [PubMed] [Google Scholar]
  51. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  52. Rundlett S. E., Carmen A. A., Kobayashi R., Bavykin S., Turner B. M., Grunstein M. HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14503–14508. doi: 10.1073/pnas.93.25.14503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Schreiber-Agus N., Chin L., Chen K., Torres R., Rao G., Guida P., Skoultchi A. I., DePinho R. A. An amino-terminal domain of Mxi1 mediates anti-Myc oncogenic activity and interacts with a homolog of the yeast transcriptional repressor SIN3. Cell. 1995 Mar 10;80(5):777–786. doi: 10.1016/0092-8674(95)90356-9. [DOI] [PubMed] [Google Scholar]
  54. Seiser C., Teixeira S., Kühn L. C. Interleukin-2-dependent transcriptional and post-transcriptional regulation of transferrin receptor mRNA. J Biol Chem. 1993 Jun 25;268(18):13074–13080. [PubMed] [Google Scholar]
  55. Shimizu M., Roth S. Y., Szent-Gyorgyi C., Simpson R. T. Nucleosomes are positioned with base pair precision adjacent to the alpha 2 operator in Saccharomyces cerevisiae. EMBO J. 1991 Oct;10(10):3033–3041. doi: 10.1002/j.1460-2075.1991.tb07854.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Sternberg P. W., Stern M. J., Clark I., Herskowitz I. Activation of the yeast HO gene by release from multiple negative controls. Cell. 1987 Feb 27;48(4):567–577. doi: 10.1016/0092-8674(87)90235-2. [DOI] [PubMed] [Google Scholar]
  57. Strebhardt K., Mullins J. I., Bruck C., Rübsamen-Waigmann H. Additional member of the protein-tyrosine kinase family: the src- and lck-related protooncogene c-tkl. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8778–8782. doi: 10.1073/pnas.84.24.8778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Strich R., Slater M. R., Esposito R. E. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10018–10022. doi: 10.1073/pnas.86.24.10018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sugita K., Koizumi K., Yoshida H. Morphological reversion of sis-transformed NIH3T3 cells by trichostatin A. Cancer Res. 1992 Jan 1;52(1):168–172. [PubMed] [Google Scholar]
  60. Sutterluety H., Bartl S., Karlseder J., Wintersberger E., Seiser C. Carboxy-terminal residues of mouse thymidine kinase are essential for rapid degradation in quiescent cells. J Mol Biol. 1996 Jun 14;259(3):383–392. doi: 10.1006/jmbi.1996.0327. [DOI] [PubMed] [Google Scholar]
  61. Talasz H., Weiss G., Puschendorf B. Replication-linked histone acetylation in rat liver tissue is sensitive to alkylating agents. FEBS Lett. 1990 May 7;264(1):141–144. doi: 10.1016/0014-5793(90)80785-h. [DOI] [PubMed] [Google Scholar]
  62. Taunton J., Hassig C. A., Schreiber S. L. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science. 1996 Apr 19;272(5260):408–411. doi: 10.1126/science.272.5260.408. [DOI] [PubMed] [Google Scholar]
  63. Travis G. H., Colavito-Shepanski M., Grunstein M. Extensive purification and characterization of chromatin-bound histone acetyltransferase from Saccharomyces cerevisiae. J Biol Chem. 1984 Dec 10;259(23):14406–14412. [PubMed] [Google Scholar]
  64. Turner B. M., Birley A. J., Lavender J. Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell. 1992 Apr 17;69(2):375–384. doi: 10.1016/0092-8674(92)90417-b. [DOI] [PubMed] [Google Scholar]
  65. Venter U., Svaren J., Schmitz J., Schmid A., Hörz W. A nucleosome precludes binding of the transcription factor Pho4 in vivo to a critical target site in the PHO5 promoter. EMBO J. 1994 Oct 17;13(20):4848–4855. doi: 10.1002/j.1460-2075.1994.tb06811.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Verreault A., Kaufman P. D., Kobayashi R., Stillman B. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell. 1996 Oct 4;87(1):95–104. doi: 10.1016/s0092-8674(00)81326-4. [DOI] [PubMed] [Google Scholar]
  67. Vidal M., Gaber R. F. RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Dec;11(12):6317–6327. doi: 10.1128/mcb.11.12.6317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wolffe A. P. Transcription: in tune with the histones. Cell. 1994 Apr 8;77(1):13–16. doi: 10.1016/0092-8674(94)90229-1. [DOI] [PubMed] [Google Scholar]
  69. Yang W. M., Inouye C., Zeng Y., Bearss D., Seto E. Transcriptional repression by YY1 is mediated by interaction with a mammalian homolog of the yeast global regulator RPD3. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):12845–12850. doi: 10.1073/pnas.93.23.12845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Yang X. J., Ogryzko V. V., Nishikawa J., Howard B. H., Nakatani Y. A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A. Nature. 1996 Jul 25;382(6589):319–324. doi: 10.1038/382319a0. [DOI] [PubMed] [Google Scholar]
  71. Yoshida H., Sugita K. A novel tetracyclic peptide, trapoxin, induces phenotypic change from transformed to normal in sis-oncogene-transformed NIH3T3 cells. Jpn J Cancer Res. 1992 Apr;83(4):324–328. doi: 10.1111/j.1349-7006.1992.tb00109.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Yoshida M., Beppu T. Reversible arrest of proliferation of rat 3Y1 fibroblasts in both the G1 and G2 phases by trichostatin A. Exp Cell Res. 1988 Jul;177(1):122–131. doi: 10.1016/0014-4827(88)90030-4. [DOI] [PubMed] [Google Scholar]
  73. Yoshida M., Horinouchi S., Beppu T. Trichostatin A and trapoxin: novel chemical probes for the role of histone acetylation in chromatin structure and function. Bioessays. 1995 May;17(5):423–430. doi: 10.1002/bies.950170510. [DOI] [PubMed] [Google Scholar]
  74. Yoshida M., Nomura S., Beppu T. Effects of trichostatins on differentiation of murine erythroleukemia cells. Cancer Res. 1987 Jul 15;47(14):3688–3691. [PubMed] [Google Scholar]
  75. de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. von Boehmer H., Hengartner H., Nabholz M., Lernhardt W., Schreier M. H., Haas W. Fine specificity of a continuously growing killer cell clone specific for H-Y antigen. Eur J Immunol. 1979 Aug;9(8):592–597. doi: 10.1002/eji.1830090804. [DOI] [PubMed] [Google Scholar]

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

RESOURCES