Molecular dissection of nucleolin's role in growth and cell proliferation: New insights

FASEB Journal

Volumn 13, Issue 14, 1999, Pages 1911-1922

  Srivastava, Meera ^a   Pollard, Harvey B ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Apoptosis; Binding proteins; Cell cycle; Ligands; Nucleolin; Phosphorylation; Proteolysis; Ribosome biogenesis

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BINDING PROTEIN; HELICASE; MESSENGER RNA; NUCLEOLIN; RIBOSOME DNA;

APOPTOSIS; AUTOIMMUNE DISEASE; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; DISEASE ACTIVITY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REVIEW; VIRUS INFECTION;

DNA VIRUSES; EUKARYOTA;

EID: 0032754311     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.13.14.1911     Document Type: Review

References (145)

1. Sommerville, J. (1986) Nucleolar structure and ribosome biogenesis. Trends Biochem. Sci. 11, 438-442
2. Warner, J. R. (1990) the nucleolus and ribosome formation. Curr. Opin. Cell Biol. 2, 521-527
3. Scheer, U., and Benavente, R. (1990) Functional and dynamic aspects of mammalian nucleolus. Bioassays 12, 14-21
4. Bugler, B, Caizergues-Ferrer, M., Bouche, G., Bourbon, H., and Amalric, F. (1982) Detection and localization of a class of proteins immunologically related to a 100-kDa nucleolar protein. Eur. J. Biochem. 128, 475-480
5. Shaw, P. J., and Jordan, E. G. (1995) The nucleolus. Annu. Rev. Cell Div. Biol. 11, 93-121
6. Lapeyre, B., Bourbon, H., and Amalric, F. (1987) Nucleolin, the major nucleolar protein of eukaryotic cells: an unusual protein structure revealed by the nucleotide sequence. Proc. Natl. Acad. Sci. USA 84, 1472-1476
7. Chen, C. M., Chiang, S. Y., and Yeh, N. H. (1991) Increased stability of nucleolin in proliferating cells by inhibition of its self-cleaving activity. J. Biol. Chem. 266, 7754-7758
8. Fang, S. H., and Yeh, N. H. (1993) The self-cleaving activity of nucleolin determines its molecular dynamics in relation to cell proliferation. Exp. Cell Res. 208, 48-53
9. Olson, M. O., Kirstein, M. N., and Wallace, M. O. (1990) Limited proteolysis as a probe of the conformation and nucleic acid binding regions of nucleolin. Biochemistry 29, 5682-5686
10. Jordon, G. (1987) At the heart of the nucleolus. Nature (London) 329, 489-490
11. Herrera, A. H., and Olson, M. O. J. (1986) Association od protein C23 with rapidly labeled nucleolar RNA. Biochemistry 25, 6258-6264
12. Borer, R. A., Lehner, C. F., Eppenberger, H. M., and Nigg, E. A. (1989) Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56, 379-390
13. Bouche, G., Gas, N., Prats, H., Baldin, V., Tauber, J. P., Teissie, J., and Amalric, F. (1987) Basic fibroblast growth factor enters the nucleolus and stimulates the transcription of ribosomal genes in ABAE cells undergoing Go-Gl transition. Proc. Natl. Acad. Sci. 84, 6770-6774
14. Caizergues-Ferrer, M., Mariottini, P., Curie, C., Lapeyre, B., Gas, N., Amalric, F., and Amaldi, F. (1989) Nucleolin from Xenopus laevis: cDNA cloning and expression during development. Genes Dev. 3, 324-333
15. Erard, M., Lakhdar-Ghazal, F., and Amalric, F. (1990) Repeat peptide motifs which contain beta-turns and modulate DNA condensation into chromatin. Eur. J. Biochem. 191, 19-26
16. Hanakahi, L. A., Dempsey, L. A., Li, M.-J., and Maizels, N. (1997) Nucleolin is one component of the B-cell specific transcription factor and switch region binding protein, LR1. Proc. Natl. Acad. Sci. USA 94, 3605-3610
17. Borggrefe, T., WabI, M., Akhmedov, A. T., and Jessberger, R. (1998) A B-cell-specific DNA recombination complex. J. Biol. Chem. 273, 17025-17035
18. Minota, S., Jarjour, W. N., Suzuki, N., Nojima, Y., Roubey, R. A., Mimura, T., Yamada, A., Hosoya, T., Takaku, F., and Winfield, J. B. (1991) Autoantibodies to nucleolin in systemic lupus erythematosus and other diseases. J. Immunol. 146, 2249-2252
19. Valdez, B. C., Henning, D., Busch, R. K., Srivastava, M., and Busch, H. (1995) Immunodominant RNA recognition motifs of human nucleolin/C23. Mol. Immunol. 32, 1207-1213
20. Tuteja, N., Huang, N. W., Skopac, D., Tuteja, R., Hrvatic, S., Zhang, J., Ponger, S., Joself, G., Faucher, C., and Amalric, F. (1995) Human DNA helicase IV is nucleolin, an RNA helicase modulated by phosphorylation. Gene 160, 143-148
21. Tuteja, N., Phan, T.-N, Tuteja, R., Ochem, A., and Falaschi, A. (1997) Inhibition of DNA unwinding and ATPase activities of human DNA helicase II by chemotherapeutic agents. Biochem. Biophys. Res. Commun. 236, 636-640
22. Yang, T. H., Tsai, W. H., Lei, H. Y., Lai, M. Y., Chen, D. S., Yeh, N. H., and Lee, S. C. (1994) Purification and characterization of nucleolin and its identification as a transcription repressor. Mol. Cell. Biol. 14, 6068-6074
23. Chan, E. K., Sullivan, K. F., and Tan, E. M. (1989) Ribonucleoprotein SS-B/La belongs to a protein family with consensus sequences for RNA-binding. Nucleic Acids Res. 17, 2233-2244
24. Ge, H., Zuo, P., and Manley, J. L. (1991) Primary structure of the human splicing factor ASF reveals similarities with Drosophila regulators. Cell 66, 373-382
25. Kranier, A. R., Mayeda, A., Kozak, D., and Binns, G. (1991) Functional expression of cloned human splicing factor SF2: homology to RNA-binding proteins, U1 70K, Drosophila splicing regulators. Cell 66, 383-394
26. Fu, X. D., and Maniates, T. (1992) Isolation of a complementary DNA that encodes the mammalian splicing factor SC35. Science 256, 535-538
27. Zamore, P. D., Patton, J. G., and Green, M. R. (1992) Cloning and domain structure of the mammalian splicing factor U2Af. Nature (London) 355, 609-614
28. Srivastava, M., Fleming, P. J., Pollard, H. B., and Burns, A. L. (1984) Cloning and sequencing of the human nucleolin cDNA. FEBS Lett. 250, 99-105
29. Goyette, M., Petropoulos, C. J., Shank, P. R., and Fausto, N. (1984) Regulated transcription of c-Ki-ras and c-myc during compensatory growth of rat liver. Mol. Cell. Biol. 4, 1493-1498
30. Bourbon, H. M., Lapeyre, B., and Amalric, F. (1988) Structure of the mouse nucleolin gene. The complete sequence reveals each RNA binding domain is encoded by two independent exons. J. Mol. Biol. 200, 627-638
31. Olson, M. O., and Thompson, B. A. (1983) Distribution of proteins among chromatin components of nucleoli. Biochemistry 22, 3187-3193
32. Ghisolfi-Nieto, L., Joseph, G., Puvion-Dutilleul, F., Amalric, F., and Bouvet, P. (1996) Nucleolin is a sequence-specific RNA-binding protein: characterization of targets on pre-ribosomal RNA. J. Mol. Biol. 260, 34-53
33. Egyhazi, E., Pigon, A., Chang, J. H., Ghaffari, S. H., Dressen, T. D., Wellman, S. E., Case, S. T., and Olson, M. O. (1988) Effects of anti-C23 (nucleolin) antibody on transcription of ribosomal DNA in Chironomus salivary gland cells. Exp. Cell Res. 178, 264-272
34. Bouche, G., Caizergues-Ferrer, M., Bugler, B., and Amalric, F. (1984) Interrelations between the maturation of a 100 kDa nucleolar protein and pre rRNA synthesis in CHO cells. Nuc. Acids Res. 12, 3025-3035
35. Belenguer, P., Caizergues-Ferrer, M., Labbe, J. C., Doree, M., and Amalric, F. (1990) Mitosis-specific phosphorylation of nucleolin by p34cdc2 protein kinase. Mol. Cell. Biol. 10, 3607-3618
36. Peter, M., Nakagawa, J., Doree, M., Labbe, J. C., and Nigg, E. A. (1990) Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase. Cell 60, 791-801
37. Warrener, P., and Petryshyn, R. (1991) Phosphorylation and proteolytic degradation of nucleolin from 3T3-F442A cells. Biochem. Biophys. Res. Commun. 180, 716-723
38. Tawfic, S., Goueli, S. A., Olson, M. O., and Ahmed, K. (1994) Androgenic regulation of phosphorylation and stability of nucleolin in rat ventral prostate. Prostate 24, 101-106
39. Kass, S., Tyc, K., Steitz, J. A., and Sollner-Webb, B. (1990) The U3 small nuclear ribonuclear protein functions at the first step of pre-ribosomal RNA processing. Cell 60, 897-908
40. Azum-Gelade, M. C., Noaillac-Depeyre, J., Caizergures-Ferrer, M., and Gas, N. (1994) Cell cycle redistribution of U3 snRNA and fibrillarin. Presence in the cytoplasmic nucleus remnant and in the prenucleolar bodies at telophase. J. Cell Sci. 107, 463-475
41. Caville J., Nicoloso, M., and Bachellerie, J.-P. (1996) Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature (London) 383, 732-736
42. Ginisty, H., Amalric, F., and Bouvet, P. (1998) Nucleolin functions in the first step of ribosomal RNA processing. EMBO J. 17, 1476-1486
43. Sapp, M., Richter, A., Weisshart, K., Caizergues-Ferrer, M., Amalric, F., Wallace, M. O. Kirstein, M. N., and Olson, M. O. J. (1989) Characterization of a 48-kDa nucleic acid binding fragment of nucleolin. Eur. J. Biochem. 179, 541-548
44. Ghizolfi, L., Kharrat, A., Joseph, G., Amalric, F., and Erard, M. (1992) Concerted activities of the RNA recognition and the glycine rich C-terminal domains of nucleolin are required for efficient complex formation with preribosomal RNA. Eur. J. Biochem. 209, 541-548
45. Creancier, L., Prats, H., Zanibellato, C., Amalric, F., and Bugler, B. (1993) Determination of the functional domains involved in nucleolar targeting of nucleolin. Mol. Biol. Cell 4, 1239-1250
46. Bugler, B., Bourbon, H., Lapeyre, B., Wallace, M. O., Chang, J. H., Amalric, F., and Olson, M. O. J. (1987) RNA binding fragments from nucleolin contain the ribonucleoprotein consensus sequence. J. Biol. Chem. 262, 10922-10925
47. Query, C. C., Bently, R. C., and Keene, J. D. (1989) A common RNA recognition motif identified within the defined U1 RNA binding domain of the 70K U1-snRNP protein. Cell 57, 89-101
48. Bouvet, P., Jain, C., Belasco, J. G., and Ama Amalric, F. (1997) RNA recognition by joint action of two nucleolin RNA-binding domains: genetic analysis and structural modeling. EMBO J. 16, 5235-5246
49. Ghisolfi-Nieto, L., Joseph, G., Puvion-Dutilleul, F., Amalric, F., and Bouvet, P. (1996) Nucleolin is a sequence-specific RNA-binding protein: Characterization of targets on pre-ribosomal RNA. J. Idol. Biol. 260, 34-53
50. Miranda, G. A., Chokler, I., and Aguilera, R. J. (1995) The murine nucleolin protein is an inducible DNA and ATP binding protein which is readily detected in nuclear extracts of lipopolysaccharide-treated plenocytes. Exp. Cell Res. 217, 294-308
51. Noaillac-Depeyre, J., Dupont, M. A., Tichadou, J. L., and Gas, N. (1989) The effect of adenosine analogue (DRB) on a major nucleolar phosphoprotein nucleolin. Biol. Cell 67, 27-35
52. Sipos, K., and Olson, M. O. (1991) Nucleolin promotes secondary structure in ribosomal RNA. Biochem. Biophys. Res. Commun. 177, 673-678
53. Heine, M. A., Rankin, M. L., and DiMario, P. J. (1993) The Gly/Arg-rich (GAR) domain of Xenopus nucleolin facilitates in vitro nucleic acid binding and in vivo nucleolar localization. Mol. Biol. Cell 4, 1189-1204
54. Ghistolfi, L., Joseph, G., Amalric, F., and Erard, M. (1992) The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties. J. Biol. Chem. 267, 2955-2959
55. Najbauer, J., Johnson, B. A., Young, A. L., and Aswad, D. W. (1993) Peptides with sequences similar to glycine, arginine-rich motifs in proteins interacting with RNA are efficiently recognized by methyltransferase (s) modifying arginine in numerous proteins. J. Biol. Chem. 268, 10501-10509
56. Schmidt-Zachmann, M. S., Dargemont, C., Kuhn, L. C., and Nigg, E. A. (1993) Nuclear export of proteins: the role of nuclear retention. Cell 74, 493-504
57. Kondo, K., and Inouye, M. (1992) Yeast NSR1 that has structural similarity to mammalian nucleolin is involved in pre-RNA processing. J. Biol. Chem. 267, 16252-16258
58. Gulli, M. P., Girard, J. P., Zapetakis, D., Lapeyre, B., Melese, T., and Caizergues-Ferrrer, M. (1995) gar2 is a nucleolar protein from Schizosaccharomyces pombe required for 18S rRNA and 40S ribosomal subunit accumulation. Nucleic Acids Res. 23, 1912-1918
59. Kondo, K., Kowalski, L. R., and Inouye, M. (1992) Cold shock induction of yeast NSR1 protein and its role in pre-RNA processing. J. Biol. Chem. 267, 16259-16265
60. Bandziulis, R. J., Swanson, M. S., and Dreyfuss, G. (1989) RNA-binding proteins as developmental regulators. Genes Dev. 3, 431-437
61. Bouvet, P., Diaz, J. J., Kindbeiter, K., Madjar, J. J., and Amalric, F. (1998) Nucleolin interacts with several ribosomal proteins through its RGG domain. J. Biol. Chem. 273, 19025-19029
62. Nigg, E. A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature (London) 386, 779-787
63. Xue, Z., and Melese, T. (1994) Nucleolar proteins that bind NLSs: A role in nuclear import or ribosome biogenesis. Trends Cell Biol. 4, 414-417
64. Xue, Z., Shan, X., Lapryre, B., and Melese, T. (1993) The amino terminus of mammalian nucleolin specifically recognizes SV40 T-antigen type nuclear localization sequences. Eur. J. Cell Biol. 62, 13-21
65. Messmer, B., and Dreyer, C. (1993) Requirements for nuclear translocation and nucleolar accumulation of nucleolin of Xenopus laevis. Eur. J. Cell 61, 369-382
66. Schwab, M. S., and Dreyer, C. (1997) Protein phosphorylation sites regulate the function of the bipartite NLS of nucleolin. Eur. J. Cell Biol. 73, 287-297
67. Yu, D., Schwartz, M. Z., and Petryshyn, Ru (1998) Effect of laminin on the nuclear localization of nucleolin in rat intestinal epithelial IEC-6 cells. Biochem. Biophys. Res. Commun. 247I, 86-192
68. Lee, W. C., Zabetakis, D., and Melese, T. (1992) NSR1 is required for pre-RNA processing and for the maintenance of steady-state levels of ribosome subunits. Mol. Cell. Biol., 12, 3865-3871
69. Srivastava, M., McBride, O. W., Fleming, P. J., Pollard, H. B., and Burns, A. L. (1990) Genomic organization and chromosomal localization of the human nucleolin gene. J. Biol. Chem. 265, 14922-14931
70. Bachellerie, J. P., Michot, B., Nicoloso, M., Balakin, A., Ni, J., and Fournier, M. J. (1995) Antisense snoRNAs: a family of nucleolar RNAs with long complementarities to rRNA. Trends Biochem. Sci. 20, 261-264
71. Nicoloso, M., Caizergues-Ferrer, M., Michot, B., Azum, M. C., and Bachellerie, J. P. (1994) U20, a novel small nucleolar RNA, is encoded in an intron of the nucleolin gene in mammals. Mol. Cell. Biol. 14, 5766-5776
72. Schneider, H. R., Reichert, G. U., and Issinger, O. G. (1986) Enhanced casein kinase II activity during mouse embryogenesis. Eur. J. Biochem. 161, 733-738
73. Bourbon, H. M., Bugler, B., Caizergues-Ferrer, M., and Amalric, F. (1983) Role of phosphorylation on the maturation pathways of a 100 kDa nucleolar protein. FEBS Lett. 155, 218-222
74. Leitinger, N., and Wesierska-Gadek, J. (1993) ADP-ribosylation of nucleolar proteins in HeLa tumor cells. J. Cell. Biochem. 52, 153-158
75. Geahlen, R. L., and Harrison, M. L. (1984) Induction of a substrate for casein kinase II during lymphocyte mitogenesis. Biochim. Biophys. Acta 804, 169-175
76. Schneider, H. R., Mieskes, G., and Issinger, O. G. (1989) Specific dephosphorylation by phosphatases 1 and 2A of a nuclear protein structurally and immunologically related to nucleolin. Possible influence on the regulation of rRNA synthesis. Eur. J. Biochem. 180, 449-455
77. Suzuki, N., Matsui, H., and Hosoya, T. (1985) Effects of androgen and polyamines on the phosphorylation of nucleolar proteins from rat ventral prostates with particular reference to 110-kDa phosphoprotein. J. Biol. Chem. 260, 8050-8055
78. Suzuki, N., Saito, T., and Hosoya, T. (1987) In vivo effects of dexamethasone and cycloheximide on the phosphorylation of 110-kDa proteins and protein kinase activities of rat liver nucleoli. J. Biol. Chem. 262, 4696-4700
79. Suganuma, M., Fujiki, H., Furuya-Suguri, H., Yoshizawa, S., Yasumoto, S., Kato, Y., Fusetani, N., and Sugimura, T. (1990) Calyculin A, an inhibitor of protein phosphatases, a potent tumor promoter on CD-1 mouse skin. Cancer Res. 50, 3521-3525
80. Fujiki, H., Suganuma, M., Yoshizawa, S., Nishiwaki, S., Winyar, B., and Sugimura, T. (1991) Mechanisms of action of okadaic acid class tumor promoters on mouse skin. Environ. Health Perspect. 93, 211-214
81. Guy, G. R., Cao, X., Chua, S. P., and Tan, Y. H. (1992) Okadaic acid mimics multiple changes in early protein phosphorylation and gene expression induced by tumor necrosis factor or interleukin-1. J. Biol. Chem. 267, 1846-1652
82. Suzuki, N., Suzuki, T., and Hosoya, T. (1993) Limited proteolysis of rat liver nucleolin by endogenous proteases: effects of polyamines and histones. Biochem. J. 289, 109-115
83. Luscher, B., Kuenzel, E. A., Krebs, E. G., and Eisenman, R. N. (1989) Myc oncoproteins are phosphorylated by casein kinase II. EMBO J., 8, 1111-1119
84. Glineur, C., Bailly, M., and Ghysdael, J. (1989) The c-erbA-encoded thyroid hormone receptor is phosphorylated in its amino terminal domain by casein kinase II. Oncogene 4, 1247-1254
85. Meek, D., Simon, S., Kikkawa, U., and Eckhart, W. (1990) The p53 tumor suppressor protein is phosphorylated at serine 389 by casein kinase II. EMBO J. 9, 3253-3260
86. Schneider, H. R., and Issinger, O. G. (1988) Nucleolin (23), a physiological substrate for casein kinase II. Biochem. Biophys. Res. Commun. 156, 1390-1397
87. Caizergues-Ferrer, M., Belenguer, P., Lapeyre, B., Amalric, F., Wallace, M. O., and Olson, M. O. J. (1987) Phosphorylation of nucleolin by a nucleolar type NII protein kinase. Biochemistry 26, 7876-7883
88. Ballal, W. R., Kung, Y. J., Olson, M. O. J., and Busch, H. (1975) changes in nucleolar proteins and their phosphorylation patterns during liver regeneration. J. Biol. Chem. 250, 5921-5925
89. Suzuki, N., Suzuki, T., Uchida, A., Thompson, E. A., and Hosoya, T. (1992) Effect of dexamethasone on nucleolar casein kinase II activity and phosphorylation of nucleolin in lymphosarcoma P1798 cells. J. Steroid Biochem. Mol. Biol. 42, 305-312
90. Suzuki, N., Kobayashi, M., Sakata, K., Suzuki, T., and Hosoya, T. (1992) Synergetic stimulatory effect of glucocorticoid, EGF and insulin on the synthesis of ribosomal RNA and phosphorylation of nucleolin in primary cultured rat hepatocytes. Biochim. Biophys. Acta 1092, 367-375
91. Bouche, G., Baldin, V., Belenger, P., Prats, H., and Amalric, F. (1994) Activation of rDNA transcription by FGF-2: key role of protein kinase II. Cell Mol. Biol. 40, 547-554
92. Csermely, P., Schnaider, T., Cheatham, B., Olson, M. O., and Kagn, C. R. (1993) Insulin induces the phosphorylation of nucleolin. A possible mechanism of insulin-induced RNA efflux from nuclei. J. Biol. Chem. 268, 9747-9752
93. Jin, Y. J., and Burakoff, S. J. (1993) The 25-kDa FK506-binding protein is localized in the nucleus and associates with casein kinase II and nucleolin. Proc. Natl. Acad. Sci. USA 90, 7769-7773
94. Kharrat, A., Derancourt, J., Doree, M., Amalric, F., and Erard, M. Synergistic effect of histone H1, and nucleolin on chromatin condensation in mitosis: role of a phosphorylated heteromer. Biochemistry 30, 10329-10336
95. Weisenberger, D., and Scheer, U. (1995) A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis. J. Cell Biol. 129, 561-575
96. Xu, X., Cooper, L. G., DiMario, P. J., and Nelson, J.W, (1995) Helix formation in model peptides based on nucleolin TPAKK motifs. Biopolymers 35, 93-102
97. Erard, M. S., Belenguer, P., Caizergues-Ferrer, M., Pantaloni, A., and Amalric, F. (1988) A major nucleolar protein, nucleolin, induces chromatin decondensation by binding to histone H1. Eur. J. Biochem. 175, 525-530
98. Hoffman, J., and Schwoch, G. (1989) Co-ordinated changes in the cyclic AMP signalling system and the phosphorylation of two nuclear proteins of Mr 130,000 and 110,000 during proliferative stimulation of the rat parotid gland by isoprenaline. Possible identity of the two proteins with pp135 and nucleolin. Biochem. J. 263, 785-793
99. Zhou, G., Seiberhener, M. L., and Wooten, M. W. (1997) Nucleolin is a protein kinase C-zeta substrate: Connection between cell surface signaling and nucleus in PC12 cells. J. Biol. Chem. 272, 31130-31137
100. Jordon, P., Heid, H., Kinzel, V., and Kubler, D. (1994) Major cell surface-located protein substrates of an ecto-protein kinase are homologs of known nuclear proteins. Biochemistry 33, 14696-14706
101. Semenkovich, C. F., Ostlund, R. E., Jr., Olson, M. O., and Yang, J. W. (1990) A protein partially expressed on the surface of HepG2 cells that binds lipoproteins specifically is nucleolin. Biochemistry 29, 9708-9713
102. Tuteja, N., Huang, N. W., Skopac, D., Tuteja, R., Hrvatic, S., Zhang, J., Pongor, S., Joseph, G., Faucher, C., Amalric, F., and Falaschi, A. (1995) Human DNA helicase IV is nucleolin, an RNA helicase modulated by phosphorylation. Gene 160, 143-148
103. Pasternack, M. S., Bleier, K. J., and McInerney, T. N. (1991) Granzyme A binding to target cell proteins. Granzyme A binds to and cleave nucleolin in vitro. J. Biol. Chem. 266, 14703-14708
104. Arends, M. J., Morris, R. G., and Wyllie, A. H. (1990) Apoptosis: the role of the endonuclease. Am. J. Pathol. 136, 593-608
105. Smith, M. J., Browne, K. A., Thia, K. Y., Apostolidis, V. A., Kershaw, M. H., and Trapani, J. A. (1994) Hypothesis: cytotic lymphocyte granule serine proteases activate target cell endonucleases to trigger apoptosis. Clin. Exp. Pharmacol. Physiol. 21, 67-70
106. Brockstedt, E., Rickers, A., Kostka, S., Laubersheimer, A., Dorken, B., Wittmann-Liebold, B., Bommert, K., and Otto, A. (1998) Identification of apoptosis-associated proteins in a human Burkitt lymphoma cell line. Cleavage of heterogeneous nuclear ribonucleoprotein A1 by caspase 3.J. Biol. Chem. 273, 28057-28064
107. Belenguer, P., Baldin, V., Mathieu, C., Prats, H., Bensaid, M., Bouche, G., and Amalric, F. (1989) Protein kinase NII and regulation of rDNA transcription in mammalian cells. Nucleic Acids Res. 17, 6625-6635
108. Ohmori, H., Murakami, T., Furutani, A., Higashi, K., Hirano, H., Gotoh, S., Kuroiwa, A., Masui, A., Nakamura, T., and Amalric, F. (1990) Simultaneous activation of heat shock protein (hsp 70) and nucleolin genes during in vivo and in vitro prereplicative stages of rat hepatocytes. Exp. Cell Res. 189, 227-232
109. Shi, Y., and Thomas, J. O. (1992) The transport of proteins into the nucleus requires the 70-kilodalton heat shock protein or its cytosolic cognate. Mol. Cell. Biol. 12, 2186-2192
110. Dang, C. V., and Lee, W. M. F. (1989) Nuclear and nucleolar targeting sequences of c-erb-A, c-myc, N-myc, p53, HSP70, and HIV tat proteins. J. Biol. Chem. 264, 18019-18023
111. Callebaut, C., Blanco, J., Benkirane, N., Krust, B., Jacotot, E., Guichard, G., Seddiki, N., Svab, J., Dam, E., Muller, S., Briand, J. P., and Hovenessian, A. G. (1998) Identification of V3 loop-binding proteins as potential receptors implicated in the binding of HIV particles to CD4(+) cells. J. Biol. Chem. 273, 21988-21997
112. Becker, J., and Craig, E. A. (1994) Heat-shock proteins as molecular chaperones. Eur. J. Biochem. 219, 11-23
113. Derenzini, M., Sirri, V., Trere, D., and Ochs, R. S. (1995) The quantity of nucleolar proteins nucleolin and protein B23 is related to cell doubling time in human cancer cells. Lab. Invest. 73, 497-502
114. De Verdugo, U. R., Selinkga, H. C., Huber, M., Kramer, B., Kellermann, J., Hofschneider, P. H., and Kandolf, R. (1995) characterization of a 100-kilodalton binding protein for the six serotypes of Coxsackie B viruses. J. Virol. 69, 6751-6757
115. Roussel, P., and Hernandez-Verdun, D. (1994) Identification of Ag-NOR proteins, markers of proliferation related to ribosomal gene activity. Exp. Cell Res. 214, 465-472
116. Roussel, P., Sirri, V., and Hernandez-Verdun, D. (1994) Quantification of Ag-NOR proteins using Ag-NOR staining on Western blots. J. Histochem. Cytochem. 42, 1513-1517
117. Sirri, V., Roussel, P., Trere, D., Derenzini, M., and Hernandez-Verdun, D. (1995) Amount variability of total and individual Ag-NOR proteins in cells stimulated to proliferate. J. Histochem. Cytochem. 43, 887-893
118. Gillet, G., Michel, D., Crisanti, P., Guerin, M., Herault, Y., Pessac, B., Calothy, G., Brun, G., and Volovitch, M. (1993) Serum factors and v-src control two complementary mitogenic pathways in quail neuroretinal cells in culture. Oncogene 8, 564-574
119. Bogre, L., Jonak, C., Mink, M., Meskiene, I., Trass, J., Ha, D. T., Swoboda, I., Plank, C., Wagner, E., Heberle-Bors, E., and Hirt, H. (1996) Developmental and cell cycle regulation of alfalfa nucMs1, a plant homolog of the yeast Nsr1 and mammalian nucleolin. Plant Cell 8, 417-428
120. Murakami, T., Ohmari, H., Tsuda, T., and Higashi, K. (1991) The effect of changes of N-myc products on the gene expression of heat-shock protein (hsp 70) and nucleolin during differentiation of neuroblastoma cells. Prog. Clin. Biol. Res. 366, 65-70
121. Biggiogera, M., Kaufmann, S. H., Shaper, J. H., Gas, N., Amalric, F., and Fakan, S. (1991) Distribution of nucleolar proteins B23 and nucleolin during mouse spermatogenesis. Chromosoma 100, 162-172
122. Maridor, G., Krek, W., and Nigg, E. A. (1990) Structure and developmental expression of chicken nucleolin and NO38: coordinate expression of two abundant non-ribosomal nucleolar proteins. Biochim. Biophys. Acta 1049, 126-133
123. Mehes, G., and Pajor, L. (1995) Nucleolin and fibrillarin expression in stimulated lymphocytes and differentiating HL-60 cells. Cell Prolif. 28, 329-336
124. Li, D., Dobrowolska, G., and Krebs, E. G. (1996) The physical association of casein kinase 2 with nucleolin. J Biol. Chem. 271, 15662-15668
125. Li, Y. P., Busch, R. K., Valdez, B. C., and Busch, H, (1996) C23 interacts with B23, a putative nucleolar-localization-signal-binding protein. Eur J. Biochem. 237, 153-158
126. Bharti, A. K., Olson, M. O. J., Kufe, D. W., and Rubin, E. H. (1996) Identification of a nucleolin binding site in human topoisomerase 1. J. Biol. Chem. 271, 1993-1997
127. Leger-Silvestre, I., Guelli, M. P., Noaillac-Depeyre, J., Faubladier, M., Sicar, H., Caizergues-Ferrer, M., and Gas, N. (1997) Ultrastructural changes in the Schizosaccharomyces pombe nucleolus following the disruption of the gar2+ gene, which encodes a nucleolar protein structurally related to nucleolin. Chromosoma 105, 542-552
128. Zaidi, S. H. E., and Malter, J. (1995) Nucleolin and heterogeneous nuclear ribonucleoprotein C proteins specifically interact with the 3′-untranslated region of amyloid protein precursor mRNA. J. Biol. Chem. 270, 17292-17298
129. Take, M., Tsutsui, J., Obama, H., Ozawa, M., Nakayama, T., Maruyama, I., Arima, T., and Muramatsu, T. (1994) Identification of nucleolin as a binding protein for midkine (MK) and heparin-binding growth associated molecule (HB-GAM). J. Biochem. 116, 1063-1068
130. Dickinson, L. A., and Kohwi-Shigematsu, T. (1995) Nucleolin is a matrix attachment region DNA-binding protein that specifically recognizes a region with high base-unpairing potential. Mol. Cell. Biol. 15, 456-465
131. Barrijal, S., Perros, M., Gu, Z., Avalosse, B. L., Belenguer, P., Amalric, F., and Rommelaere, J. (1992) Nucleolin forms a specific complex with a fragment of the virus (minus) strand of minute virus of mice DNA. Nucleic Acids Res. 20, 5053-5060
132. Pfeiffe, J., and Anderer, F. A. (1983) Isolation and characterization of phosphoprotein pp105 from simian virus 40-transformed mouse fibroblasts. Biochim. Biophys. Acta762, 86-93
133. Kleinman, H. K., Weeks, B. S., Cannon, F, B., Sweeney, T. M., Sephel, G. C., Clement, B., Zain, M., Olson, M. O. J., Jucker, M., and Burrous, B. A. (1991) Identification of a 110-kDa nonintegrin cell surface laminin-binding protein which recognizes an A chain neurite-promoting peptide. Arch. Biochem. Biophys. 290, 320-325
134. Kibbey, M. C., Johnson, B., Petryshyn, R., Jucker, M., and Kleinman, H. K. (1995) A 110-hD nuclear shuttling protein, nucleolin, binds to the neurite-promoting IKVAV site of laminin-1. J. Neurosci. Res. 42, 314-322
135. Lee, C. H., Chang, S. C., Chen, C. J., and Chang, M. F. (1998) The nucleolin binding activity of hepatitis delta antigen is associated with nucleolus targeting. J. Biol. Chem. 273, 7650-7656
136. Krantz, S., Salazar, R., Brandt, R., Kellerman, J., and Lottspeich, F. (1995) Purification and partial amino acid sequencing of a fructosyllysine-specific binding protein from cell membranes of the monocyte-like cell line U937. Biochim. Biophys. Acta 1266, 109-112
137. Zhang, J., Bottaro, A., Li, S., Stewart, V., and Alt, F. W. (1993) A selective defect in IgG2b switching as a result of targeted mutation of the Ig 2b promoter and exon EMBO J. 12, 3529-3537
138. Bottaro, A., Lansford, R., Xu, L., Zhang, J., Rothman, P., and Alt, F. W. (1994) S region transcription per se promotes basal IgE class switch recombination but additional factors regulate the efficiency of the process. EMBO J. 13, 665-674
139. Ishikawa, F., Matunis, M. J., Dreyfuss, G., and Cech, T. R. (1993) Nuclear proteins that bind the pre-mRNA 3′ splice site sequence r(UUAG/G) and the human telomeric DNA sequence d(TTAGGG)n. Mol. Cell. Biol. 13, 4301-4310
140. Jarjour, W. N., Minota, S., Roubey, R. A., Mimura, T., and Winfield, J. B. (1992) Autoantibodies to nucleolin cross-react with histone H1 in systematic lupus erythematosus. Mol. Biol. 16, 263-266
141. 141. Soulard, M., Lagaye, S., Della Valle, V., Danon, F., Larsen, C. J., and Barque, J. P. (1989) Nucleolar proteins identified in human cells as antigens by sera from dogs with autoimmune disorders. Exp. Cell Res. 182, 482-498
142. Bell, S. A., Faust, H., Mittermuller, J., Kolb, H. J., and Meurer, M. (1996) Specificity of antinuclear antibodies in scleroderma-like chronic graft-versus-host disease: clinical correlation and histocompatibility locus antigen association. Br. J. Dermatol 134, 848-854
143. Tan, E. M. (1989) Antinuclear autoantibodies: diagnostic markers for autoimmune diseases and probes for cell biology. Adv. Immunol. 44, 93
144. Bautz, E. K. F., Kalden, J. R., Homma, M., and Tan, E. M. (1989) Molecular and Cell Biology of Autoantibodies and Autoimmunity, Vol. 118, Springer-Verlag, Berlin Heidelberg
145. McDonald, H., Smailus, D., Jenkins, H., Adam, K., Simpson, N. E., and Goodfellow, P. J. (1992) Identification and characterization of a gene at D10S94 in the MEN2A region. Genomics 13, 344-348