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Overexpression of the nucleolar protein nucleophosmin/B23 in collagen lattice-cultured fibroblasts: Potential role in the control of protein synthesis

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Abstract

Fibroblasts cultivated in tridimensional collagen lattices exhibit a downregulation of protein synthesis, related to decreased ribosomal RNA (rRNA) content and half life, when compared to monolayer cultivated cells. The involvement in this process of nucleophosmin/B23, a nucleolar phosphoprotein with ribonuclease properties, was checked. We compared production of nucleophosmin/B23 in monolayer and collagen lattice cultured fibroblasts. A significant increase of nucleophosmin/B23 mRNA levels was noticed in lattice-cultured fibroblasts vs monolayers (+154%, p < 0.05). A concomitant enhancement of nucleolar nucleophosmin/B23 content was found (+112%, p < 0.001). Simultaneously, ribonuclease activity contained in nucleolar extracts from collagen lattice-cultured fibroblasts was significantly increased (+54%, p < 0.01). These data demonstrate that extracellular collagen matrix induces the overexpression of nucleophosmin/B23, and suggest that the regulation of protein syntheses in collagen lattice cultures may be explained, at least partly, by an increased degradation of neosynthesized rRNAs dependent on nucleophosmin.

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References

  1. Juliano RL, Haskill S: Signal transduction from the extracellular matrix. J Cell Biol 120: 577–585, 1993

    Google Scholar 

  2. Gillery P, Bellon G, Coustry F, Borel JP: Cultures of fibroblasts in fibrin lattices: Models for the study of metabolic activities of the cells in physiological conditions. J Cell Physiol 140: 483–490, 1989

    Google Scholar 

  3. Vernon RB, Sage EH: Between molecules and morphology. Extracellular matrix and creation of vascular form. Am J Pathol 147: 873–883, 1995

    Google Scholar 

  4. Gillery P, Leperre A, Coustry F, Maquart F, Borel JP: Different regulation of collagen I gene transcription in three-dimensional lattice cultures. FEBS Lett 296: 297–299, 1992

    Google Scholar 

  5. Nishiyama T, Tsunenaga M, Nakayama Y, Adachi E, Hayashi T: Growth rate of human fibroblasts is repressed by the culture within reconstituted collagen matrix but not by the culture on the matrix. Matrix 9: 193–199, 1989

    Google Scholar 

  6. Gillery P, Georges N, Wegrowski J, Randoux A, Borel JP: Protein synthesis in collagen lattice-cultured fibroblasts is controllled at the ribosomal level. FEBS Lett 357: 287–289, 1995

    Google Scholar 

  7. Gillery P, Georges N, Randoux A, Lefèvre F, Maquart FX, Borel JP: Modulation of protein synthesis by extracellular matrix: Potential involvement of two nucleolar proteins, nucleolin and fibrillarin. Biochem Biophys Res Commun 228: 94–99, 1996

    Google Scholar 

  8. Lefèvre L, Lorenzato M, Georges N, Clavel C, Birembaut P, Gillery P: Decreased number of nucleolar organizing regions in collagen lattice cultured fibroblasts. CR Acad Sci Paris 321: 991–997, 1998

    Google Scholar 

  9. Schmidt-Zachmann MS, Franke WW: DNA cloning and amino acid sequence determination of a major constituent protein of mammalian nucleoli. Correspondence of the nucleophosmin-related protein NO38 to mammalian protein B23. Chromosoma 96: 417–426, 1998

    Google Scholar 

  10. Zatsepina OV, Rousselet A, Chan PK, Olson MOJ, Jordan EG, Bornens M: The nucleolar phosphoprotein B23 redistributes in part to the spindle poles during mitosis. J Cell Sci 112: 455–466, 1999

    Google Scholar 

  11. Savkur RS, Olson MOJ: Preferential cleavage in pre-ribosomal RNA by protein B23 endoribonuclease. Nucleic Acids Res 26: 4508–4515, 1998

    Google Scholar 

  12. Zatsepina OV, Todorov IT, Philipova RN, Krachmarov CP, Trendelenburg MF, Jordan EG: Cell cycle-dependent translocations of a major nucleolar phosphoprotein, B23, and some characteristics of its variants. Eur J Cell Biol 73: 58–70, 1997

    Google Scholar 

  13. Hale TK, Mansfield BC: Nucleotide sequence of a cDNA clone representing a third allele of human protein B23. Nucleic Acids Res 17: 10112, 1989

    Google Scholar 

  14. Chan WY, Liu QR, Borjigin J, Busch H, Rennert OM, Tease LA, Chan PK: Characterization of the cDNA encoding human nucleophosmin and studies of its role in normal and abnormal growth. Biochemistry 28: 1033–1039, 1989

    Google Scholar 

  15. Tokunaga K, Nakamura Y, Sakata K, Fujimori K, Ohkubo M, Sawada K, Sakiyama S: Enhanced expression of a glyceraldehyde-3-phosphate dehydrogenase gene in human lung cancers. Cancer Res 47: 5616–5619, 1987

    Google Scholar 

  16. Muramatsu M, Hayashi Y, Onish, T, Sakai M, Takai K: Rapid isolation of nucleoli from detergent purified of various tumor and tissue culture cells. Exp Cell Res 88: 345–351, 1974

    Google Scholar 

  17. Herrera JE, Savkur R, Olson MO: The ribonuclease activity of nucleolar protein B23. Nucleic Acids Res 23: 3974–3979, 1995

    Google Scholar 

  18. Langholz O, Röckel D, Mauch C, Kozlowska E, Bank I, Krieg T, Eckes B: Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by α1β1 and α2β1 integrins. J Cell Biol 131: 1903–1915, 1995

    Google Scholar 

  19. Fluck J, Querfeld C, Cremer A, Niland S, Krieg T, Sollberg S: Normal human primary fibroblasts undergo apoptosis in three-dimensional contractile collagen gels. J Invest Dermatol 110: 153–157, 1998

    Google Scholar 

  20. Pederson T: The plurifunctional nucleolus. Nucleic Acids Res 26: 3871–3876, 1998

    Google Scholar 

  21. Rossi JJ: Ribozymes in the nucleolus. Science 285: 1685, 1999

    Google Scholar 

  22. Szebeni A, Olson MOJ: Nucleolar protein B23 has molecular chaperone activities. Protein Sci 8: 905–912, 1999

    Google Scholar 

  23. Hingorani K, Szebeni A, Olson MOJ: Mapping the functional domains of nucleolar protein B23. J Biol Chem 275: 24451–24457, 2000

    Google Scholar 

  24. Jiang PS, Yung BYM: Down-regulation of nucleophosmin/B23 mRNA delays the entry of cells into mitosis. Biochem Biophys Res Commun 257: 865–870, 1999

    Google Scholar 

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Correspondence to Philippe Gillery.

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Lefèvre, F., Garnotel, R., Georges, N. et al. Overexpression of the nucleolar protein nucleophosmin/B23 in collagen lattice-cultured fibroblasts: Potential role in the control of protein synthesis. Mol Cell Biochem 229, 45–50 (2002). https://doi.org/10.1023/A:1017995111734

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