Functional characterization of human nucleosome assembly protein-2 (NAP1L4) suggests a role as a histone chaperone

Genomics

Volumn 44, Issue 3, 1997, Pages 253-265

  Rodriguez, Pedro ^a   Munroe, David ^b   Prawitt, Dirk ^c   Chu, Lee Lee ^a   Bric, Eva ^b   Kim, Jungho ^a   Reid, Laura H ^d   Davies, Chris ^e   Nakagama, Hitoshi ^f   Loebbert, Ralf ^c   Winterpacht, Andreas ^c   Petruzzi, Mary Jane ^g   Higgins, Michael J ^g   Nowak, Norma ^g   Evans, Glen ^e   Shows, Tom ^f   Weissman, Bernard E ^d   Zabel, Bernhard ^c   Housman, David E ^h   Pelletier, Jerry ^a  

^a MCGILL UNIVERSITY   (Canada)

^b CELERA   (United States)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^g UNIVERSITY AT BUFFALO   (United States)

^h MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEOSOME ASSEMBLY PROTEIN 2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CHROMOSOME 11P; DELETION MUTANT; DNA HISTONE INTERACTION; GENE STRUCTURE; HUMAN; HUMAN CELL; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; TRANSCRIPTION REGULATION;

ESCHERICHIA COLI;

EID: 0031572246     PISSN: 08887543     EISSN: None     Source Type: Journal    
DOI: 10.1006/geno.1997.4868     Document Type: Article

References (59)

1. Albrecht, S., von Schweinitz, D., Waha, A., Kraus, J. A., von Deimling, A., and Pietsch, T. (1994). Loss of maternal alleles on chromosome arm 11p in hepatoblastoma. Cancer Res. 54: 5041-5044.
2. Allende, J. E., and Allende, A. C. (1995). Protein kinases. IV. Protein kinase CK2: An enzyme with multiple substrates and a puzzling regulation. FASEB J. 9: 313-323.
3. Arents, G., and Moudrianakis, E. N. (1993). Topography of the histone octamer surface: Repeating structural motifs utilized in the docking of nucleosomal DNA. Proc. Natl. Acad. Sci. USA 90: 10489-10493.
4. Baffa, R., Negrini, M., Mandes, B., Rugge, M., Ranzani, G. N., Hirohashi, S., and Croce, C. M. (1996). Loss of heterozygosity for chromosome 11 in adenocarcinoma of the stomach. Cancer Res. 56: 268-272.
5. Bepler, G., and Garcia-Blanco, M. A. (1994). Three tumor-suppressor regions on chromosome 11p identified by high-resolution deletion mapping in human non-small-cell lung cancer. Proc. Natl. Acad. Sci. USA 91: 5513-5517.
6. Crevel, G., and Cotterill, S. (1995). DF 31, a sperm decondensation factor from Drosophila melanogaster: Purification and characterization. EMBO J. 14: 1711-1717.
7. Cruzen, M. E., Bengtsson, U., McMahon, J., Wasmuth, J. J., and Arfin, S. M. (1993). Assignment of the cysteinyl-tRNA synthetase gene (CARS) to 11p1S.5. Genomics 15: 692-693.
8. Cullen, K. E., Kladde, M. P., and Seyfred, M. A. (1993). Interaction between transcription regulatory regions of prolactin chromatin. Science 261: 203-206.
9. Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475-1488.
10. Dilworth, S. M., Black, S. J., and Laskey, R. A. (1987). Two complexes that contain histones are required for nucleosome assembly in vitro: Role of nucleoplasmin and N1 in Xenopus egg extracts. Cell 51: 1009-1018.
11. Dilworth, S. M., and Dingwall, C. (1988). Chromatin assembly in vitro and in vivo. Bioessays 9: 44-49.
12. Dingwall, C., and Laskey, R. A. (1991). Nuclear targeting sequences - A consensus? Trends Biochem. Sci. 16: 478-481.
13. Dowdy, S. F., Fasching, C. L., Araujo, D., Lai, K-M., Livanos, E., Weissman, B. E., and Stanbridge, E. J. (1991). Suppression of tumorigenicity in Wilms tumor by the p15.5-p14 region of chromosome 11. Science 254: 293-295.
14. Field, J., Nikawa, J.-I., Broek, D., MacDonald, B., Rodgers, I. A., Wilson, I. A., Lemer, R. A., and Wigler, M. (1988). Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol. 8: 2159-2165.
15. Fujii-Nakata, T., Ishimi, Y., Okuda, A., and Kikuchi, A. (1992). Functional analysis of nucleosome assembly protein, NAP-1. J. Biol. Chem. 267: 20980-20986.
16. Hoovers, J. M. N., Kalikin, L. M., Johnson, L. A., Alders, M., Redeker, B., Law, D. J., Bliek, J., Steenmen, M., Benedict, M., Wiegant, J., Lengauer, C., Taillon-Miller, P., Schlessinger, D., Edwards, M. C., Elledge, S. J., Ivens, A., Westerveld, A., Little, P., Mannens, M., and Feinberg, A. P. (1995). Multiple genetic loci within 11p15 defined by Beckwith-Wiedemann syndrome rearrangement breakpoints and subchromosomal transferable fragments. Proc. Natl. Acad. Sci. USA 92: 12456-12460.
17. KIP2 gene, is biallelically expressed in fetal and adult tissues. Hum. Mol. Genet. 5: 1743-1748.
18. Ishimi, Y., Hirosumi, J., Sato, W., Sugasawa, K., Yokota, S., Hanaoka, F., and Yamada, M. (1984). Purification and initial characterization of a protein which facilitates assembly of nucleosomelike structure from mammalian cells. Eur. J. Biochem. 142: 431-439.
19. Ishimi, Y., and Kikuchi, A. (1991). Identification and molecular cloning of yeast homolog of nucleosome assembly protein I which facilitates nucleosome assembly in vitro. J. Biol. Chem. 266: 7025-7029.
20. Ishimi, Y., Kojima, M., Yamada, M., and Hanaoka, F. (1987). Binding mode of nucleosome-assembly protein (AP-1) and histones. Eur. J. Biochem. 162: 19-24.
21. Ishimi, Y., Yasuda, H., Hirosumi, J., Hanaoka, F., and Yamada, M. (1983). A protein which facilitates assembly of nucleosome-like structures in vitro in mammalian cells. J. Biochem. 94: 735-744.
22. Ito, T., Bulger, M., Kobayashi, R., and Kadonaga, J. T. (1996). Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol. Cell. Biol. 16: 3112-3124.
23. Jantzen, H.-M., Admon, A., Bell, S. P., and Tjian, R. (1990). Nucleolar transcription factor hUBF contains a DNA-binding motif with homology to HMG proteins. Nature 344: 830-836.
24. Kellogg, D. R., Kikuchi, A., Fujii-Nakata, T., Turck, C. W., and Murray, A. W. (1995). Members of the NAP/SET family of proteins interact specifically with B-type cyclins. J. Cell Biol. 130: 661-673.
25. Kellogg, D. R., and Murray, A. W. (1995). NAP1 acts with Clb2 to perform mitotic functions and to suppress polar bud growth in budding yeast. J. Cell Biol. 130: 675-685.
26. Kleinschmidt, J. A., Fortkamp, E., Krohne, G., Zentgraf, H., and Franke, W. W. (1985). Coexistence of two different types of soluble histone complexes in nuclei of Xenopus laevis oocytes. J. Biol. Chem. 260: 1166-1176.
27. Kleinschmidt, J. A., and Franke, W. W. (1982). Soluble acidic complexes containing histones H3 and H4 in nuclei of Xenopus laevis oocytes. Cell 29: 799-809.
28. Koufos, A., Grundy, P., Morgan, K., Aleck, K. A., Hadro, T., Lampkin, B. C., Kalbakji, A., and Cavenee, W. K. (1989). Familial Wiedemann-Beckwith syndrome and a second Wilms' tumor locus both map to 11p15.5. Am. J. Hum. Genet. 44: 711-719.
29. Lapeyre, B., Bourbon, H., and Amalric, F. (1987). Nucleolin, the major nucleolar protein of growing eukaryotic cells: An unusual structure revealed by the nucleotide sequence. Proc. Natl. Acad. Sci. USA 84: 1472-1476.
30. Laskey, R. A., Honda, B. M., Mills, A. D., and Finch, J. T. (1978). Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275: 416-420.
31. Looijenga, L. H., Abraham, M., Gillis, A. J., Saunders, G. F., and Oosterhuis, J. W. (1994). Testicular germ cell tumors of adults show deletions of chromosomal bands 11p13 and 11p15.5, but no abnormalities within the zinc-finger regions and exons 2 and 6 of the Wilms' tumor 1 gene. Genes Chromosomes Cancer 9: 153-160.
32. n repeats and heat shock elements have distinct roles in chromatin structure and transcriptional activation of the Drosophila hsp26 gene. Mol. Cell. Biol. 13: 2802-2814.
33. Mannens, M., Slater, R. M., Heyting, C., Bliek, J., de Kraker, J., Goad, N., de Pagter-Holthuizen, P., and Pearson, P. L. (1988). Molecular nature of genetic changes resulting in loss of heterozygosity of chromosome 11 in Wilms' tumors. Hum. Genet. 81: 41-48.
34. Marsolier, M.-C., Tanaka, S., Livingstone-Zatchej, M., Grunstein, M., Thoma, F., and Sentenac, A. (1995). Reciprocal interferences between nucleosomal organization and transcriptional activity of the yeast SNR6 gene. Genes Dev. 9: 410-422.
35. KIP2, a structurally distinct member of the p21CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev. 9: 650-662.
36. Nelson, T., Wiegand, R., and Brutlag, D. (1981). Ribonucleic acid and other polyanions facilitate chromatin assembly in vitro. Biochemistry 20: 2594-2601.
37. Ping, A. J., Reeve, A. E., Law, D. J., Young, M. R., Boehnke, M., and Feinberg, A. P. (1989). Genetic linkage of Beckwith-Wiedemann syndrome to 11p15. Am. J. Hum. Genet. 44: 720-723.
38. Prawitt, D., Munroe, D. J., Pelletier, J., Loebbert, R., Bric, E., Hermanns, P., Housman, D., Winterpacht, A., and Zabel, B. U. (1996). Identification of a NAP related gene in the Wilms' tumor candidate region at 11p15.5. Am. J. Hum. Genet. 59: A79.
39. Reeve, A. E., Sih, S. A., Raizis, A. M., and Feinberg, A. P. (1989). Loss of allelic heterozygosity at a second locus on chromosome 11 in sporadic Wilms' tumor cells. Mol. Cell. Biol. 9: 1799-1803.
40. Reid, L. H., West, A., Gioeli, D. G., Phillips, K. K., Kelleher, K. F., Araujo, D., Stanbridge, E. J., Dowdy, S. F., Gerhard, D. S., and Weissman, B. E. (1996). Localization of a tumor suppressor gene in 11p15.5 using the G401 Wilms' tumor assay. Hum. Mol. Genet. 5: 239-247.
41. Richmond, T. J., Rechsteiner, T., and Luger, K. (1993). Studies on nucleosome structure. Cold Spring Harbor Symp. Quant. Biol. 58: 265-272.
42. Sanger, F., Nicklen, S., and Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463-5467.
43. Schild, C., Claret, F. X., Wahli, W., and Wollfe, A. P. (1993). A nucleosome-dependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro. EMBO J. 12: 423-433.
44. Schmidt Zachmann, M. S., Hugle-Dorr, B., and Franke, W. W. (1987). A constitutive nucleolar protein identified as a member of the nucleoplasmin family. EMBO J. 6: 1881-1890.
45. Shen, X., Yu, L., Weir, J. W., and Gorovsky, M. A. (1995). Linker histones are not essential and affect chromatin condensation in vivo. Cell 82: 47-56.
46. Simon, H.-U., Mills, G. B., Kozlowski, M., Hogg, D., Branch, D., Ishimi, Y., and Siminovitch, K. A. (1994). Molecular characterization of hNRP, a cDNA encoding a human nucleosome-assembly-protein-1-related gene product involved in the induction of cell proliferation. Biochem. J. 297: 389-397.
47. Sirotkin, A. M., Edelmann, W., Cheng, G., Klein-Szanto, A., Kucherlapati, R., and Skoultchi, A. I. (1995). Mice develop normally without the H1(0) histone. Proc. Natl. Acad. Sci. USA 92: 6434-6438.
48. Smith, M. W., Holmsen, A. L., Wei, Y. H., Peterson, M., and Evans, G. A. (1994). Genomic sequence sampling: A strategy for high resolution sequence-based physical mapping of complex genomes. Nature Genet. 7: 40-47.
49. Stein, A., Whitlock, J. P. Jr., and Bina, M. (1979). Acidic polypeptides can assemble both histones and chromatin in vitro at physiological ionic strength. Proc. Natl. Acad. Sci. USA 76: 5000-5004.
50. Sonoda, Y., Iizuka, M., Yasuda, J., Makino, R., Ono, T., Kayama, T., Yoshimoto, T., and Sekiya, T. (1995). Loss of heterozygosity at llplS in malignant glioma. Cancer Res. 55: 2166-2168.
51. Svaren, J., and Chalkley, R. (1990). The structure and assembly of active chromatin. Trends Genet. 6: 52-56.
52. Thomas, G. H., and Elgin, S. C. R. (1988). Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter. EMBO J. 7: 2191-2201.
53. van Holde, K. E. (1989). "Chromatin," Springer-Verlag, New York.
54. von Lindern, M., van Baal, S., Wiegant, J., Raap, A., Hagemeijer, A., and Grosveld, G. (1992). can, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3′ half to different genes: characterization of the set gene. Mol. Cell. Biol. 12: 3346-3355.
55. Walter, P. P., Owen-Hughes, T. A., Coté, J., and Workman, J. L. (1995). Stimulation of transcription factor binding and histone displacement by nucleosome assembly protein 1 and nucleoplasmin requires disruption of the histone octamer. Mol. Cell. Biol. 15: 6178-6187.
56. Wen, L., Huang, J.-K, Johnson, B. H., and Reeck, G. R. (1989). A human placental cDNA that encodes nonhistone chromosomal protein HMG-1. Nucleic Acids Res. 17: 1197-1214.
57. Winqvist, R., Hampton, G. M., Mannermaa, A., Blanco, G., Alavaikko, M., Kiviniemi, H., Taskinen, P. J., Evans, G. A., Wright, F. A., Newsham, I., and Cavenee, W. K. (1995). Loss of heterozygosity for chromosome 11 in primary human breast tumors is associated with poor survival after metastasis. Cancer Res. 55: 2660-2664.
58. Wolffe, A. P. (1995). "Chromatin: Structure and Function," Academic Press, San Diego.
59. Worcel, A., Han, S., and Wong, M. L. (1978). Assembly of newly replicated chromatin. Cell 15: 969-977.