Nuclear activities of basic fibroblast growth factor: Potentiation of low-serum growth mediated by natural or chimeric nuclear localization signals

Molecular Biology of the Cell

Volumn 10, Issue 5, 1999, Pages 1429-1444

  Arese, Marco ^a,b   Chen, Yan ^a   Florkiewicz, Robert Z ^c   Gualandris, Anna ^a   Shen, Bin ^a   Rifkin, Daniel B ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c Ciblex Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; FIBROBLAST GROWTH FACTOR 2; POLYCLONAL ANTIBODY; RECOMBINANT BASIC FIBROBLAST GROWTH FACTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL GROWTH; CELL STRAIN 3T3; CHIMERA; GENE OVEREXPRESSION; MITOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ANIMALIA;

EID: 0032952058     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.5.1429     Document Type: Article

References (82)

1. Abraham, J.A., Mergia, A., Whang, J.L., Tumolo, A., Friedman, J., Hjerrild, K.A., Gospodarowicz, D., and Fiddes, J.C. (1986). Nucleotide sequence of a bovine clone encoding the angiogenic protein, basic fibroblast growth factor. Science 233, 545-548.
2. Acland, P., Dixon, M., Peters, G., and Dickson, C. (1990). Subcellular fate of the Int-2 oncoprotein is determined by choice of initiation codon. Nature 343, 662-665.
3. Albelda, S.M., Oliver, P.D., Romer, L.H., and Buck, C.A. (1990). EndoCAM: a novel endothelial cell-cell adhesion molecule. J. Cell Biol. 110, 1227-1237.
4. Antoine, M., Reimers, K., Dickson, C., and Kiefer, P. (1997). Fibroblast growth factor 3, a protein with dual subcellular localization, is targeted to the nucleus and nucleolus by the concerted action of two nuclear localization signals and a nucleolar retention signal. J. Biol. Chem. 272, 29475-29481.
5. Arnaud, E., Touriol, C., Boutonnet, C., Gensac, M.C., Vagner, S., Prats, H., and Prats, A.C. (1999). A new 34-kilodalton isoform of human fibroblast growth factor 2 is cap dependently synthesized by using a non-AUG start codon and behaves as a survival factor. Mol. Cell. Biol. 19, 505-514.
6. Baird, A. (1994). Potential mechanism regulating the extracellular activities of basic fibroblast growth factor (FGF-2). Mol. Reprod. Dev. 39, 43-48.
7. Baird, A., Esch, F., Gospodarowicz, D., and Guillemin, R. (1985). Retina- and eye-derived endothelial cell growth factors: partial molecular characterization and identity with acidic and basic fibroblast growth factors. Biochemistry 24, 7855-7860.
8. Baldin, V., Roman, A.M., Bosc-Bierne, I., Amalric, F., and Bouche, G. (1990). Translocation of bFGF to the nucleus is G1 phase cell cycle specific in bovine aortic endothelial cells. EMBO J. 9, 1511-1517.
9. Basilico, C., and Moscatelli, D. (1992). The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59, 115-165.
10. Beyer, A.L., Christensen, M.E., Walker, B.W., and LeStourgeon, W.M. (1977). Identification and characterization of the packaging proteins of core 40S hnRNP particles. Cell 11, 127-138.
11. Bikfalvi, A., Klein, S., Pintucci, G., Quarto, N., Mignatti, P., and Rifkin, D.B. (1995). Differential modulation of cell phenotype by different molecular weight forms of basic fibroblast growth factor: possible intracellular signaling by the high molecular weight forms. J. Cell Biol. 129, 233-243.
12. Boeck, R., and Kolakofsky, D. (1994). Positions + 5 and + 6 can be major determinants of the efficiency of non-AUG initiation codons for protein synthesis. EMBO J. 13, 3608-3617.
13. Bouche, G., Gas, N., Prats, H., Baldin, U., 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→G1 transition. Proc. Natl. Acad. Sci. USA 86, 6770-6776.
14. Bugler, B., Amalric, F., and Prats, H. (1991). Alternative initiation of translation determines cytoplasmic or nuclear localization of basic fibroblast growth factor. Mol. Cell. Biol. 11, 573-577.
15. Burgess, W.H., Bizik, J., Mehlman, T., Quarto, N., and Rifkin, D.B. (1991). Direct evidence for methylation of arginine residues in high molecular weight forms of basic fibroblast growth factor. Cell Regul. 2, 87-93.
16. Burgess, W.H., and Maciag, T. (1989). The heparin-binding (fibroblast) growth factor family of proteins. Annu. Rev. Biochem. 58, 575-606.
17. Burwen, S.J., and Jones, A.L. (1987). The association of polypeptide hormones and growth factors with the nuclei of target cells. Trends Biochem. Sci. 12, 159-162.
18. Cochrane, A.W., Perkins, A., and Rosen, C.A. (1990). Identification of sequences important in the nucleolar localization of human immunodeficiency virus Rev: relevance of nucleolar localization to function. Virology 64, 881-885.
19. Coffin, J.D., et al. (1995). Abnormal bone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice. Mol. Biol. Cell 6, 1861-1873.
20. Curtis, B.M., Widmer, M.B., deRoos, P., and Qwarnstrom, E.E. (1990). IL-1 and its receptor are translocated to the nucleus. J. Immunol. 144, 1295-1303.
21. Dang, C.V., and Lee, W.M. (1989). Nuclear and nucleolar targeting sequences of c-erb-A, c-myb, N-myc, p53, HSP70, and HIV tat proteins. J. Biol. Chem. 264, 18019-18023.
22. Davis, M.G., Zhou, M., Ali, S., Coffin, D., Doetschman, T., and Dorn, G.W., II. (1997). Intracrine and autocrine effects of basic fibroblast growth factor in vascular smooth muscle cells. J. Mol. Cardiol. 29, 1061-1072.
23. Dono, R., James, D., and Zeller, R. (1998). A GR-motif functions in nuclear accumulation of the large FGF-2 isoforms and interferes with mitogenic signaling. Oncogene 16, 2151-2158.
24. Dono, R., and Zeller, R. (1994). Cell-type-specific nuclear translocation of fibroblast growth factor-2 isoforms during chicken kidney and limb morphogenesis. Dev. Biol. 163, 316-330.
25. Fantl, W.J., Johnson, D.E., and Williams, L.T. (1993). Signaling by receptor tyrosine kinase. Annu. Rev. Biochem. 62, 453-481.
26. Florkiewicz, R.Z., Majack, R.A., Buechler, R.D., and Florkiewicz, E. (1995). Quantitative export of FGF-2 occurs through an alternative, energy-dependent, non-ER/Golgi pathway. J. Cell. Physiol. 162, 388-399.
27. Florkiewicz, R.Z., and Sommer, A. (1989). Human basic fibroblast growth factor gene encodes four polypeptides: three initiate translation from non-AUG codons. Proc. Natl. Acad. Sci. USA 86, 3978-3981.
28. Garcia-Bustos, J., Heitman, J., and Hall, M.N. (1991). Nuclear protein localization. Biochim. Biophys. Acta 1071, 83-101.
29. Giordano, S., Sherman, L., Lyman, W., and Morrison, R. (1992). Multiple molecular weight forms of basic fibroblast growth factor are developmentally regulated in the CNS. Dev. Biol. 152, 293-303.
30. Grothe, C., Meisinger, C., Holzschuh, J., Wewetzer, K., and Cattini, P. (1998). Overexpression of the 18 kDa and 21/23 kDa fibroblast growth factor-2 isoforms in PC12 cells and Schwann cells results in altered cell morphology and growth. Brain Res. Mol. Brain Res. 57, 97-105.
31. Gualandris, A., Urbinati, C., Rusnati, M., Ziche, M., and Presta, M. (1994). Interaction of high-molecular-weight basic fibroblast growth factor with endothelium: biological activity and intracellular fate of human recombinant M(r) 24,000 bFGF. J. Cell. Physiol. 161, 149-159.
32. Henderson, J.E. (1997). Nuclear targeting of secretory proteins. Mol. Cell. Endocrinol. 129, 1-5.
33. Jans, D.A. (1994). Nuclear signaling pathways for polypeptide ligands and their membrane receptors? FASEB J. 8, 841-847.
34. Jans, D.A., and Hassan, G. (1998). Nuclear targeting by growth factors, cytokines, and their receptors: a role in signaling? Bioassays 20, 400-411.
35. Jaye, M., et al. (1986). Human endothelial cell growth factor: cloning, nucleotide sequence, and chromosome localization. Science 233, 541-545.
36. Jaye, M., Schlessinger, J., and Dionne, C.A. (1992). Fibroblast growth factor receptor tyrosine kinases: molecular analysis and signal transduction. Biochim. Biophys. Acta 1135, 185-199.
37. Jiang, L.W., and Schindler, M. (1988). Nuclear transport in 3T3 fibroblasts: effects of growth factors, transformation, and cell shape. J. Cell Biol. 106, 13-19.
38. Joy, A., Moffet, K., Neary, E., Mordechai, E., Stachoviach, S., Coons, J., Rankin Shapiro, J., Florkiewicz, R.Z., and Stachowiak, M.K. (1997). Nuclear accumulation of FGF-2 is associated with proliferation of human astrocytes and glioma cells. Oncogene 14, 171-183.
39. Kalderon, D., Richardson, W.D., Markham, A.F., and Smith, A.E. (1984). Sequence requirements for nuclear location of SV40 large-T antigen. Nature 311, 33-38.
40. Kamiguchi, H., Yoshida, K., Wakamoto, H., Inaba, M., Sasaki, H., Otani, M., and Toya, S. (1996). Cytokine-induced selective increase of high molecular-weight bFGF isoforms and their subcellular kinetics in cultured rat hippocampal astrocytes. Neurochem. Res. 21, 701-706.
41. Kimura, H. (1993). Schwannoma-derived growth factor must be transported into the nucleus to exert its mitogenic activity. Proc. Natl. Acad. Sci. USA 90, 2165-2169.
42. Kueng, W., Silber, E., and Eppendberger, U. (1989). Quantification of cells cultured on 96-well plates. Anal. Biochem. 182, 16-19.
43. Lanford, R.E., and Butel, J.S. (1984). Construction and characterization of an SV40 mutant defective in nuclear transport of T antigen. Cell 37, 801-813.
44. Levine, J.E., and Prystowsky, M.B. (1995). Polypeptide growth factors in the nucleus: a review of function and translocation. Neuroimmunomodulation 2, 290-298.
45. G-dimethylarginine in nucleolar proteins C23. Biochemistry 24, 6025-6028.
46. G-dimethylarginine. J. Biol. Chem. 260, 14304-14310.
47. Liu, L., Doble, B.W., and Kardami, E. (1993). Perinatal phenotype and hypothyroidism are associated with elevated levels of 21.5- to 22-kDa basic fibroblast growth factor in cardiac ventricles. Dev. Biol. 157, 507-516.
48. Makkerh, J.P.S., Dingwall, C., and Laskey, R.A. (1996). Comparative mutagenesis of nuclear localization signals reveals the importance of neutral and acidic amino acids. Curr. Biol. 6, 1025-1027.
49. Mason, I.J. (1994). The ins and outs of fibroblast growth factor. Cell 78, 547-552.
50. Mignatti, P., Morimoto, T., and Rifkin, D.B. (1992). Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J. Cell. Physiol. 151, 81-93.
51. Najbauer, J., Johnson, B.A., Young, A., and Aswad, D.W. (1993). Peptides with sequences similar to glycine, arginine rich motifs in proteins interacting with RNA are efficiently recognized by methyltransferases modifying arginine in numerous proteins. J. Biol. Chem. 268, 10501-10509.
52. Nigg, E.A. (1997). Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386, 779-787.
53. Nishimura, T., Utsunomiya Y., Hoshikawa, M., Ohuchi, H., and Itoh, N. (1999). Structure and expression of a novel human FGF, FGF-19, expressed in the fetal brain. Biochim. Biophys. Acta 1444, 148-151.
54. Pasumarthi, K.B., Doble, B.W., Kardami, E., and Cattini, P.A. (1994). Overexpression of CUG- or AUG-initiated forms of basic fibroblast growth factor in cardiac myocytes results in similar effects on mitosis and protein synthesis but distinct nuclear morphologies. J. Mol. Cell. Cardiol. 26, 1045-1060.
55. Pasumarthi, K.B., Kardami, E., and Cattini, P.A. (1996). High and low molecular weight fibroblast growth factor-2 increase proliferation of neonatal rat cardiac myocytes but have differential effects on binucleation and nuclear morphology. Evidence for both paracrine and intracrine actions of fibroblast growth factor-2. Circ. Res. 78, 126-136.
56. 2 terminus in nuclear accumulation. Growth Factors 11, 163-176.
57. Pederson, T. (1998). Growth factors in the nucleolus? J. Cell Biol. 143, 279-281.
58. Pintucci, G., Quarto, N., and Rifkin, D.B. (1996). Methylation of high molecular weight fibroblast growth factor-2 determines posttranslational increases in molecular weight and affects its intracellular distribution. Mol. Biol. Cell 7, 1249-1258.
59. Piotrowicz, R.S., Martin, J.L., Dillman, W.H., and Levin, E.G. (1997). The 27-kDa heat shock protein facilitates basic fibroblast growth factor release from endothelial cells. J. Biol. Chem. 272, 7042-7047.
60. Prats, A.C., Vagner, S., Prats, H., and Amalric, F. (1992). cis-acting elements involved in the alternative translation initiation process of human basic fibroblast growth factor mRNA. Mol. Cell. Biol. 12, 4796-4805.
61. Prats, H., et al. (1989). High molecular mass forms of basic fibroblast growth factor are initiated by alternative CUG codons. Proc. Natl. Acad. Sci. USA 86, 1836-1840.
62. Prochiantz, A., and Theodore, L. (1995). Nuclear/growth factors. BioEssays 17, 39-44.
63. 2-terminal extension of high molecular weight bFGF is a nuclear targeting signal. J. Cell. Physiol. 147, 311-318.
64. Quarto, N., Talarico, D., Florkiewicz, R., and Rifkin, D.B. (1991b). Selective expression of high molecular weight basic fibroblast growth factor confers a unique phenotype to NIH 3T3 cells. Cell Regul. 2, 699-708.
65. Renko, M., Quarto, N., Morimoto, T., and Rifkin, D.B. (1990). Nuclear and cytoplasmic localization of different basic fibroblast growth factor species. J. Cell. Physiol. 144, 108-114.
66. Riese, J., Zeller, R., and Dono, R. (1995). Nucleo-cytoplasmic translocation and secretion of fibroblast growth factor-2 during avian gastrulation. Mech. Dev. 49, 13-22.
67. Rifkin, D.B., and Moscatelli, D. (1989). Recent developments in the cell biology of basic fibroblast growth factor. J. Cell Biol. 109, 1-6.
68. Robbins, J., Dilworth, S.M., Laskey, R.A., and Dingwall, C. (1991). Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64, 615-623.
69. Scheer, U., and Benavente, R. (1990). Functional and dynamic aspects of the mammalian nucleolus. Bioessays 12, 14-21.
70. Shi, J., Friedman, S., and Maciag, T. (1997). A carboxyl-terminal domain in fibroblast growth factor (FGF)-2 inhibits FGF-1 release in response to heat shock in vitro. J. Biol. Chem. 272, 1142-1147.
71. Shin, S.I., Freedman, V.H., Risser, R., and Pollack, R. (1975). Tumorigenicity of virus-transformed cells in nude mice is correlated specifically with anchorage independent growth in vitro. Proc. Natl. Acad. Sci. USA 72, 4435-4439.
72. Siomi, H., Shida, H., Nam, S.H., Nosaka, T., Maki, M., and Hatanaka, M. (1988). Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing. Cell 55, 197-209.
73. Stachowiak, M.K., Moffett, J., Joy, I., Puchacz, E., Florkiewicz, R., and Stachowiak, E.K. (1996). Regulation of bFGF gene expression and subcellular distribution of bFGF protein in adrenal medullary cells. J. Cell Biol. 127, 203-223.
74. Stachowiak, M.K., Moffett, J., Maher, P., Tucholski, J., and Stachowiak, E.K. (1997). Growth factor regulation of cell growth and proliferation in the nervous system. A new intracrine nuclear mechanism. Mol. Neurobiol. 15, 257-283.
75. Vagner, S., Gensac, M.C., Maret, A., Bayard, F., Amalric, F., Prats, H., and Prats, A.C. (1995). Alternative translation of human fibroblast growth factor 2 mRNA occurs by internal entry of ribosomes. Mol. Cell. Biol. 15, 35-44.
76. Vagner, S., Touriol, C., Galy, B., Audigier, S., Gensac, M.-C., Amalric, F., Bayard, F., Prats, H., and Prats, A.-C. (1996). Translation of CUG-but not AUG-initiated forms of human fibroblast growth factor 2 is activated in transformed and stressed cells. J. Cell Biol. 135, 1391-1402.
77. Vilgrain, I., and Baird, A. (1991). Phosphorylation of basic fibroblast growth factor by a protein kinase associated with the outer surface of a target cell. Mol. Endocrinol. 5, 1003-1012.
78. Vilgrain, I., Gonzalez, A.M., and Baird, A. (1993). Phosphorylation of basic fibroblast growth factor (FGF-2) in the nuclei of SK-Hep-1 cells. FEBS Lett. 331, 228-232.
79. Wiedlocha, A., Falnes, P.O., Rapak, A., Munoz, R., Klingenberg, O., and Olsnes, S. (1996). Stimulation of proliferation of a human osteosarcoma cell line by exogenous acidic fibroblast growth factor requires both activation of receptor tyrosine kinase and growth factor internalization. Mol. Cell. Biol. 16, 270-280.
80. Yu, Z-X., Biro, S., Fu, Y.-M., Sanchez, J., Smale, G., Sasse, J., Ferrans, V.J., and Casscells, W. (1993). Localization of basic fibroblast growth factor in bovine endothelial cells: immunohistochemical and biochemical studies. Exp. Cell Res. 204, 247-259.
81. Zhan, X., Hu, X., Friedman, S., and Maciag, T. (1992). Analysis of endogenous and exogenous nuclear translocation of fibroblast growth factor-1 in NIH3T3 cells. Biochem. Biophys. Res. Commun. 188, 982-991.
82. Zirwes, R.F., Kouzmenko, A.P., Peters, J.M., Franke, W.W., and Schmidt-Zachmann, M.S. (1997). Topogenesis of a nucleolar protein: determination of molecular segments directing nucleolar association. Mol. Biol. Cell 8, 231-248.