Intracellular trafficking of LET-756, a fibroblast growth factor of C. elegans, is controlled by a balance of export and nuclear signals

Experimental Cell Research

Volumn 312, Issue 9, 2006, Pages 1484-1495

  Popovici, Cornel ^a   Fallet, Mathieu ^b   Marguet, Didier ^b   Birnbaum, Daniel ^a   Roubin, Régine ^a  

^a INSTITUT PAOLI CALMETTES   (France)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

C. elegans; FGF; Nuclear speckles; Nucleolus; Nucleus

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; FIBROBLAST GROWTH FACTOR; GLUTAMINE; LET 756 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL STRAIN COS1; CONTROLLED STUDY; MOLECULE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA SPLICING; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 33646160429     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.01.012     Document Type: Article

References (39)

1. Popovici C., Roubin R., Coulier F., and Birnbaum D. An evolutionary history of the FGF superfamily. Bioessays 27 (2005) 849-857
2. Olsen S.K., Garbi M., Zampieri N., Eliseenkova A.V., Ornitz D.M., Goldfarb M., and Mohammadi M. FHFs share structural but not functional homology to FGFs. J. Biol. Chem. 278 (2003) 34226-34236
3. Green P.J., Walsh F.S., and Doherty P. Promiscuity of fibroblast growth factor receptors. Bioessays 18 (1996) 639-646
4. Huang P., and Stern M.J. FGF signaling in flies and worms: more and more relevant to vertebrate biology. Cytokine Growth Factor Rev. 16 (2005) 151-158
5. DeVore D.L., Horvitz H.R., and Stern M.J. An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites. Cell 83 (1995) 611-620
6. Goodman S.J., Branda C.S., Robinson M.K., Burdine R.D., and Stern M.J. Alternative splicing affecting a novel domain in the C. elegans EGL-15 FGF receptor confers functional specificity. Development 130 (2003) 3757-3766
7. Birnbaum D., Popovici C., and Roubin R. A pair as a minimum: the two fibroblast growth factors of the nematode Caenorhabditis elegans. Dev. Dyn. 232 (2005) 247-255
8. Burdine R.D., Chen E.B., Kwok S.F., and Stern M.J. egl-17 encodes an invertebrate fibroblast growth factor family member required specifically for sex myoblast migration in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 2433-2437
9. Burdine R.D., Branda C.S., and Stern M.J. EGL-17(FGF) expression coordinates the attraction of the migrating sex myoblasts with vulval induction in C. elegans. Development 125 (1998) 1083-1093
10. Roubin R., Naert K., Popovici C., Vatcher G., Coulier F., Thierry-Mieg J., Pontarotti P., Birnbaum D., Baillie D., and Thierry-Mieg D. let-756, a C. elegans fgf essential for worm development. Oncogene 18 (1999) 6741-6747
11. Huang P., and Stern M.J. FGF signaling functions in the hypodermis to regulate fluid balance in C. elegans. Development 131 (2004) 2595-2604
12. Bülow H.E., Boulin T., and Hobert O. Differential functions of the C. elegans FGF receptor in axon outgrowth and maintenance of axon position. Neuron 42 (2004) 367-374
13. Popovici C., Conchonaud F., Birnbaum D., and Roubin R. Functional phylogeny relates LET-756 to FGF9. J. Biol. Chem. 279 (2004) 40146-40152
14. Wood W.B., and and the community of C. elegans Researchers. The Nematode Caenorhabditis elegans (1998), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
15. Klonis N., Rug M., Harper I., Wickham M., Cowman A., and Tilley L. Fluorescence photobleaching analysis for the study of cellular dynamics. Eur. Biophys. J. 31 (2002) 36-51
16. Carmo-Fonseca M., Mendes-Soares L., and Campos I. To be or not to be in the nucleolus. Nat. Cell Biol. 2 (2000) E107-E112
17. Lamond A.I., and Spector D.L. Nuclear speckles: a model for nuclear organelles. Nat. Rev., Mol. Cell Biol. 4 (2003) 605-612
18. Johnson H.M., Subramaniam P.S., Olsnes S., and Jans D.A. Trafficking and signaling pathways of nuclear localizing protein ligands and their receptors. Bioessays 26 (2004) 993-1004
19. Sorokin A., Mohammadi M., Huang J., and Schlessinger J. Internalization of fibroblast growth factor receptor is inhibited by a point mutation at tyrosine 766. J. Biol. Chem. 269 (1994) 17056-17061
20. Stachowiak M.K., Fang X., Myers J.M., Dunham S.M., Berezney R., Maher P.A., and Stachowiak E.K. Integrative nuclear FGFR1 signaling (INFS) as a part of a universal "feed-forward-and-gate" signaling module that controls cell growth and differentiation. J. Cell. Biochem. 90 (2003) 662-691
21. Kokel M., Borland C.Z., DeLong L., Horvitz H.R., and Stern M.J. clr-1 encodes a receptor tyrosine phosphatase that negatively regulates an FGF receptor signaling pathway in Caenorhabditis elegans. Genes Dev. 12 (1998) 1425-1437
22. Coulier F., Batoz M., Marics I., de Lapeyriere O., and Birnbaum D. Putative structure of the FGF6 gene product and role of the signal peptide. Oncogene 6 (1991) 1437-1444
23. Goldfarb M. Signaling by fibroblast growth factors: the inside story. Sci. STKE 106 (2001) 37
24. Skjerpen C.S., Nilsen T., Wesche J., and Olsnes S. Binding of FGF-1 variants to protein kinase CK2 correlates with mitogenicity. EMBO J. 21 (2002) 4058-4069
25. Kolpakova E., Wiedlocha A., Stenmark H., Klingenberg O., Falnes P.O., and Olsnes S. Cloning of an intracellular protein that binds selectively to mitogenic acidic fibroblast growth factor. J. Biochem. 336 (1998) 213-222
26. Skjerpen C.S., Wesche J., and Olsnes S. Identification of ribosome-binding protein p34 as an intracellular protein that binds acidic fibroblast growth factor. J. Biol. Chem. 277 (2002) 23864-23871
27. Mizukoshi E., Suzuki M., Loupatov A., Uruno T., Hayashi H., Misono T., Kaul S.C., Wadhwa R., and Imamura T. Fibroblast growth factor-1 interacts with the glucose-regulated protein GRP75/mortalin. J. Biochem. 343 (1999) 461-466
28. Bonnet H., Filhol O., Truchet I., Brethenou P., Cochet C., Amalric F., and Bouche G. Fibroblast growth factor-2 binds to the regulatory beta subunit of CK2 and directly stimulates CK2 activity toward nucleolin. J. Biol. Chem. 271 (1996) 24781-24787
29. Soulet F., Al Saati T., Roga S., Amalric F., and Bouche G. Fibroblast growth factor-2 interacts with free ribosomal protein S19. Biochem. Biophys. Res. Commun. 289 (2001) 591-596
30. Da Costa L., Tchernia G., Gascard P., Lo A., Meerpohl J., Niemeyer C., Chasis J.A., Fixler J., and Mohandas N. Ribosomal protein S19 expression during erythroid differentiation. Blood 101 (2003) 5039-5045
31. Claus P., Doring F., Gringel S., Muller-Ostermeyer F., Fuhlrott J., Kraft T., and Grothe C. Differential intranuclear localization of fibroblast growth factor-2 isoforms and specific interaction with the survival of motoneuron protein. J. Biol. Chem. 278 (2003) 479-485
32. Bossard C., Laurell H., Van den Berghe L., Meunier S., Zanibellato C., and Prats H. Translokin is an intracellular mediator of FGF-2 trafficking. Nat. Cell Biol. 5 (2003) 433-439
33. Reimers K., Antoine M., Zapatka M., Blecken V., Dickson C., and Kiefer P. NoBP, a nuclear fibroblast growth factor 3 binding protein, is cell cycle regulated and promotes cell growth. Mol. Cell. Biol. 21 (2001) 4996-5007
34. Schoorlemmer J., and Goldfarb M. Fibroblast growth factor homologous factors and the islet brain-2 scaffold protein regulate activation of a stress-activated protein kinase. J. Biol. Chem. 277 (2002) 49111-49119
35. Claus P., Doring F., Gringel S., Muller-Ostermeyer F., Fuhlrott J., Kraft T., and Grothe C. Differential intranuclear localization of fibroblast growth factor-2 isoforms and specific interaction with the survival of motoneuron protein. J. Biol. Chem. 278 (2003) 479-485
36. Zaidi S.K., Young D.W., Choi J.Y., Pratap J., Javed A., Montecino M., Stein J.L., Lian J.B., van Wijnen A., and Stein G.S. Intranuclear trafficking: organization and assembly of regulatory machinery for combinatorial biological control. J. Biol. Chem. 279 (2004) 43363-43366
37. Alvarez M., Estivill X., and de la Luna S. DYRK1A accumulates in splicing speckles through a novel targeting signal and induces speckle disassembly. J. Cell Sci. 116 (2003) 3099-3107
38. Chen D., and Huang S. Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J. Cell Biol. 153 (2001) 169-176
39. Misteli T., Gunjan A., Hock R., Bustin M., and Brown D.T. Dynamic binding of histone H1 to chromatin in living cells. Nature 408 (2000) 877-881