Abstract
Labeled nuclear proteins were microinjected into the cytoplasm of Tetrahymena thermophila. Macronuclear H1, calf thymus H1, and the SV40 large T antigen nuclear localization signal linked to BSA accumulated specifically in macronuclei, even if cells were in micronuclear S phase or were nonreplicating. The way in which histone H4 localized to either the macronucleus or the micronucleus suggested that it accumulates in whichever nucleus is replicating. The inability of the micronucleus to accumulate Tetrahymena H1 or heterologous nuclear proteins, even at a period in the cell cycle when it is accumulating H4, suggests that it has a specialized transport system. These studies demonstrate that although the mechanism for localizing proteins to nuclei is highly conserved among eukaryotes, it can differ between two porecontaining nuclei lying in the same cytoplasm.
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Selected References
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- Allis C. D., Allen R. L., Wiggins J. C., Chicoine L. G., Richman R. Proteolytic processing of h1-like histones in chromatin: a physiologically and developmentally regulated event in Tetrahymena micronuclei. J Cell Biol. 1984 Nov;99(5):1669–1677. doi: 10.1083/jcb.99.5.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Allis C. D., Bowen J. K., Abraham G. N., Glover C. V., Gorovsky M. A. Proteolytic processing of histone H3 in chromatin: a physiologically regulated event in Tetrahymena micronuclei. Cell. 1980 May;20(1):55–64. doi: 10.1016/0092-8674(80)90234-2. [DOI] [PubMed] [Google Scholar]
 - Allis C. D., Glover C. V., Gorovsky M. A. Micronuclei of Tetrahymena contain two types of histone H3. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4857–4861. doi: 10.1073/pnas.76.10.4857. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Allis C. D., Wiggins J. C. Proteolytic processing of micronuclear H3 and histone phosphorylation during conjugation in Tetrahymena thermophila. Exp Cell Res. 1984 Aug;153(2):287–298. doi: 10.1016/0014-4827(84)90601-3. [DOI] [PubMed] [Google Scholar]
 - Bonner W. M. Protein migration into nuclei. I. Frog oocyte nuclei in vivo accumulate microinjected histones, allow entry to small proteins, and exclude large proteins. J Cell Biol. 1975 Feb;64(2):421–430. doi: 10.1083/jcb.64.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Bonner W. M. Protein migration into nuclei. II. Frog oocyte nuclei accumulate a class of microinjected oocyte nuclear proteins and exclude a class of microinjected oocyte cytoplasmic proteins. J Cell Biol. 1975 Feb;64(2):431–437. doi: 10.1083/jcb.64.2.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Dequin R., Saumweber H., Sedat J. W. Proteins shifting from the cytoplasm into the nuclei during early embryogenesis of Drosophila melanogaster. Dev Biol. 1984 Jul;104(1):37–48. doi: 10.1016/0012-1606(84)90034-4. [DOI] [PubMed] [Google Scholar]
 - Dingwall C., Allan J. Accumulation of the isolated carboxy-terminal domain of histone H1 in the Xenopus oocyte nucleus. EMBO J. 1984 Sep;3(9):1933–1937. doi: 10.1002/j.1460-2075.1984.tb02072.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Dingwall C., Laskey R. A. Protein import into the cell nucleus. Annu Rev Cell Biol. 1986;2:367–390. doi: 10.1146/annurev.cb.02.110186.002055. [DOI] [PubMed] [Google Scholar]
 - Dreyer C., Hausen P. Two-dimensional gel analysis of the fate of oocyte nuclear proteins in the development of Xenopus laevis. Dev Biol. 1983 Dec;100(2):412–425. doi: 10.1016/0012-1606(83)90235-x. [DOI] [PubMed] [Google Scholar]
 - Feldherr C. M. Nucleocytoplasmic exchanges during early interphase. J Cell Biol. 1968 Oct;39(1):49–54. doi: 10.1083/jcb.39.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Gerace L., Burke B. Functional organization of the nuclear envelope. Annu Rev Cell Biol. 1988;4:335–374. doi: 10.1146/annurev.cb.04.110188.002003. [DOI] [PubMed] [Google Scholar]
 - Glover C. V., Vavra K. J., Guttman S. D., Gorovsky M. A. Heat shock and deciliation induce phosphorylation of histone H1 in T. pyriformis. Cell. 1981 Jan;23(1):73–77. doi: 10.1016/0092-8674(81)90271-3. [DOI] [PubMed] [Google Scholar]
 - Goldfarb D. S., Gariépy J., Schoolnik G., Kornberg R. D. Synthetic peptides as nuclear localization signals. Nature. 1986 Aug 14;322(6080):641–644. doi: 10.1038/322641a0. [DOI] [PubMed] [Google Scholar]
 - Gorovsky M. A. Macro- and micronuclei of Tetrahymena pyriformis: a model system for studying the structure and function of eukaryotic nuclei. J Protozool. 1973 Feb;20(1):19–25. doi: 10.1111/j.1550-7408.1973.tb05995.x. [DOI] [PubMed] [Google Scholar]
 - Gorovsky M. A. Studies on nuclear structure and function in Tetrahymena pyriformis. II. Isolation of macro- and micronuclei. J Cell Biol. 1970 Dec;47(3):619–630. doi: 10.1083/jcb.47.3.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Gorovsky M. A., Yao M. C., Keevert J. B., Pleger G. L. Isolation of micro- and macronuclei of Tetrahymena pyriformis. Methods Cell Biol. 1975;9(0):311–327. doi: 10.1016/s0091-679x(08)60080-1. [DOI] [PubMed] [Google Scholar]
 - Gurdon J. B. Nuclear transplantation and the control of gene activity in animal development. Proc R Soc Lond B Biol Sci. 1970 Dec 1;176(1044):303–314. doi: 10.1098/rspb.1970.0050. [DOI] [PubMed] [Google Scholar]
 - Horowitz S., Bowen J. K., Bannon G. A., Gorovsky M. A. Unusual features of transcribed and translated regions of the histone H4 gene family of Tetrahymena thermophila. Nucleic Acids Res. 1987 Jan 12;15(1):141–160. doi: 10.1093/nar/15.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Jiang L. W., Schindler M. Nuclear transport in 3T3 fibroblasts: effects of growth factors, transformation, and cell shape. J Cell Biol. 1988 Jan;106(1):13–19. doi: 10.1083/jcb.106.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Johmann C. A., Gorovsky M. A. Purification and characterization of the histones associated with the macronucleus of Tetrahymena. Biochemistry. 1976 Mar 23;15(6):1249–1256. doi: 10.1021/bi00651a012. [DOI] [PubMed] [Google Scholar]
 - Johns E. W. Studies on histones. 7. Preparative methods for histone fractions from calf thymus. Biochem J. 1964 Jul;92(1):55–59. doi: 10.1042/bj0920055. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Karrer K. M. Germ line-specific DNA sequences are present on all five micronuclear chromosomes in Tetrahymena thermophila. Mol Cell Biol. 1983 Nov;3(11):1909–1919. doi: 10.1128/mcb.3.11.1909. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Lanford R. E., Kanda P., Kennedy R. C. Induction of nuclear transport with a synthetic peptide homologous to the SV40 T antigen transport signal. Cell. 1986 Aug 15;46(4):575–582. doi: 10.1016/0092-8674(86)90883-4. [DOI] [PubMed] [Google Scholar]
 - Maihle N. J., Satir B. H. Protein secretion in Tetrahymena thermophila: characterization of the secretory mutant strain SB281. J Cell Sci. 1985 Oct;78:49–65. doi: 10.1242/jcs.78.1.49. [DOI] [PubMed] [Google Scholar]
 - Moreland R. B., Langevin G. L., Singer R. H., Garcea R. L., Hereford L. M. Amino acid sequences that determine the nuclear localization of yeast histone 2B. Mol Cell Biol. 1987 Nov;7(11):4048–4057. doi: 10.1128/mcb.7.11.4048. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Nelson M., Silver P. Context affects nuclear protein localization in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Feb;9(2):384–389. doi: 10.1128/mcb.9.2.384. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Richter J. D., Young P., Jones N. C., Krippl B., Rosenberg M., Ferguson B. A first exon-encoded domain of E1A sufficient for posttranslational modification, nuclear-localization, and induction of adenovirus E3 promoter expression in Xenopus oocytes. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8434–8438. doi: 10.1073/pnas.82.24.8434. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Stevenson I., Lloyd F. P. Ultrastructure of nuclear division in Paramecium aurelia. II. Amitosis of the macronucleus. Aust J Biol Sci. 1971 Oct;24(5):977–987. doi: 10.1071/bi9710977. [DOI] [PubMed] [Google Scholar]
 - Stevenson I., Lloyd F. P. Ultrastructure of nuclear division in Paramecium aurella. I. Mitosis in the micronucleus. Aust J Biol Sci. 1971 Oct;24(5):963–975. doi: 10.1071/bi9710963. [DOI] [PubMed] [Google Scholar]
 - Tondravi M. M., Yao M. C. Transformation of Tetrahymena thermophila by microinjection of ribosomal RNA genes. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4369–4373. doi: 10.1073/pnas.83.12.4369. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Vavra K. J., Allis C. D., Gorovsky M. A. Regulation of histone acetylation in Tetrahymena macro- and micronuclei. J Biol Chem. 1982 Mar 10;257(5):2591–2598. [PubMed] [Google Scholar]
 - White E. M., Shapiro D. L., Allis C. D., Gorovsky M. A. Sequence and properties of the message encoding Tetrahymena hv1, a highly evolutionarily conserved histone H2A variant that is associated with active genes. Nucleic Acids Res. 1988 Jan 11;16(1):179–198. doi: 10.1093/nar/16.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Wolfe J., Hunter B., Adair W. S. A cytological study of micronuclear elongation during conjugation in Tetrahymena. Chromosoma. 1976 Jun 23;55(4):289–308. doi: 10.1007/BF00292827. [DOI] [PubMed] [Google Scholar]
 - Woodard J., Kaneshiro E., Gorovsky M. A. Cytochemical studies on the problem of macronuclear subnuclei in tetrahymena. Genetics. 1972 Feb;70(2):251–260. doi: 10.1093/genetics/70.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Wu L. H., Kuehl L., Rechsteiner M. Dynamic behavior of histone H1 microinjected into HeLa cells. J Cell Biol. 1986 Aug;103(2):465–474. doi: 10.1083/jcb.103.2.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Wu M., Allis C. D., Gorovsky M. A. Cell-cycle regulation as a mechanism for targeting proteins to specific DNA sequences in Tetrahymena thermophila. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2205–2209. doi: 10.1073/pnas.85.7.2205. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Wu M., Allis C. D., Richman R., Cook R. G., Gorovsky M. A. An intervening sequence in an unusual histone H1 gene of Tetrahymena thermophila. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8674–8678. doi: 10.1073/pnas.83.22.8674. [DOI] [PMC free article] [PubMed] [Google Scholar]
 - Wu R. S., Bonner W. M. Separation of basal histone synthesis from S-phase histone synthesis in dividing cells. Cell. 1981 Dec;27(2 Pt 1):321–330. doi: 10.1016/0092-8674(81)90415-3. [DOI] [PubMed] [Google Scholar]
 
