Activated EGL-15 FGF receptor promotes protein degradation in muscles of Caenorhabditis elegans

EMBO Journal

Volumn 22, Issue 19, 2003, Pages 5058-5067

  Szewczyk, Nathaniel J ^a,b   Jacobson, Lewis A ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b NASA AMES RESEARCH CENTER   (United States)

Author keywords

Oncogene; Proteolysis; Ras; Remodeling; Signal transduction

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN; PHOSPHATASE; PROTEIN EGL 15; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GENETIC CODE; MUSCLE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE PROTEINS; MUSCLES; RAS PROTEINS; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION;

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS;

EID: 0141865502     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg472     Document Type: Article

References (61)

1. 2+-dependent systems. In Rivett, A. (ed.), Advances in Molecular and Cellular Biology: Intracellular Protein Degradation, Vol. 27, JAI Press, Stamford, CT, pp. 235-266.
2. Beitel, G.J., Clark, S.G. and Horvitz, H.R. (1990) Caenorhabditis elegans ras gene let-60 acts as a switch in the pathway of vulval induction. Nature, 348, 503-509.
3. Borland, C.Z., Schutzman, J.L. and Stern, M.J. (2001) Fibroblast growth factor signaling in Caenorhabditis elegans. BioEssays, 23, 1120-1130.
4. Burdine, R.D., Chen, E.B., Kwok, S.F. and Stern, M.J. (1997) egl-17 encodes an invertebrate fibroblast growth factor family member required specifically for sex myoblast migration in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA, 94, 2433-2437.
5. Chang, C., Newman, A.P. and Sternberg, P.W. (1999) Reciprocal EGF signaling back to the uterus from the induced C.elegans vulva coordinates morphogenesis of epithelia. Curr. Biol., 9, 237-246.
6. Chang, C., Hopper, N.A. and Sternberg, P.W. (2000) Caenorhabditis elegans SOS-1 is necessary for multiple RAS-mediated developmental signals. EMBO J., 19, 3283-3294.
7. Clandinin, T.R., DeModena, J.A. and Sternberg, P.W. (1998) Inositol trisphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C.elegans. Cell, 92, 523-533.
8. Clark, S.G., Stern, M.J. and Horvitz, H.R. (1992) C.elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature, 356, 340-344.
9. Dent, J.A. and Han, M. (1998) Post-embryonic expression pattern of C.elegans let-60 ras reporter constructs. Mech. Dev., 72, 179-182.
10. DeVore, D., Horvitz, H. and Stern, M. (1995) An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C.elegans hermaphrodites. Cell, 83, 611-620.
11. Dohm, G.L., Tapscott, E.B. and Kasperek, G.J. (1987) Protein degradation during endurance exercise and recovery. Med. Sci. Sports Exerc., 19, S166-S171.
12. Dourdin, N., Bhatt, A.K., Dutt, P., Greer, P.A., Arthur, J.S., Elce, J.S. and Huttenlocher, A. (2001) Reduced cell migration and disruption of the actin cytoskeleton in calpain-deficient embryonic fibroblasts. J. Biol. Chem., 276, 48382-48388.
13. Eble, D.M., Spragia, M.L., Ferguson, A.G. and Samarel, A.M. (1999) Sarcomeric myosin heavy chain is degraded by the proteasome. Cell Tissue Res., 296, 541-548.
14. Eisenmann, D.M. and Kim, S.K. (1997) Mechanism of activation of the Caenorhabditis elegans ras homologue let-60 by a novel, temperature-sensitive, gain-of-function mutation. Genetics, 146, 553-565.
15. Fire, A. and Waterston, R.H. (1989) Proper expression of myosin genes in transgenic nematodes. EMBO J., 8, 3419-3428.
16. Floss, T., Arnold, H.H. and Braun, T. (1997) A role for FGF-6 in skeletal muscle regeneration. Genes Dev., 11, 2040-2051.
17. Fostel, J.L., Coste, L.B. and Jacobson, L.A. (2003) Degradation of transgene-coded and endogenous proteins in the muscles of Caenorhabditis elegans. Biochem. Biophys. Res. Commun., in press.
18. Han, M. and Sternberg, P.W. (1990) let-60, a gene that specifies cell fates during Caenorhabditis elegans vulval induction, encodes a ras protein. Cell, 63, 921-932.
19. Hara, M. and Han, M. (1995) Ras farnesyltransferase inhibitors suppress the phenotype resulting from an activated ras mutation in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA, 92, 3333-3337.
20. Hughes, S.M. (2001) Muscle development: reversal of the differentiated state. Curr. Biol., 11, R237-R239.
21. Jagoe, R.T. and Goldberg, A.L. (2001) What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr. Opin. Clin. Nutr. Metab. Care, 4, 183-190.
22. Jiang, Z.S., Padua, R.R., Ju, H., Doble, B.W., Jin, Y., Hao, J., Cattini, P.A., Dixon, I.M. and Kardami, E. (2002) Acute protection of ischemic heart by FGF-2: involvement of FGF-2 receptors and protein kinase C. Am. J. Physiol. Heart Circ. Physiol., 282, H1071-H1080.
23. Johnson, S.E. and Allen, R.E. (1995) Activation of skeletal muscle satellite cells and the role of fibroblast growth factor receptors. Exp. Cell Res., 219, 449-453.
24. Kastner, S., Elias, M.C., Rivera, A.J. and Yablonka-Reuveni, Z. (2000) Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J. Histochem. Cytochem., 48, 1079-1096.
25. Klint, P. and Claesson-Welsh, L. (1999) Signal transduction by fibroblast growth factor receptors. Front. Biosci., 4, D165-D177.
26. Kokel, M., Borland, C.Z., DeLong, L., Horvitz, H.R. and Stern, M.J. (1998) clr-1 encodes a receptor tyrosine phosphatase that negatively regulates an FGF receptor signaling pathway in Caenorhabditis elegans. Genes Dev., 12, 1425-1437.
27. Kouhara, H., Hadari, Y.R., Spivak Kroizman, T., Schilling, J., Bar Sagi, D., Lax, I. and Schlessinger, J. (1997) A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell, 89, 693-702.
28. Li, W., Han, M. and Guan, K.L. (2000) The leucine-rich repeat protein SUR-8 enhances MAP kinase activation and forms a complex with Ras and Raf. Genes Dev., 14, 895-900.
29. Llovera, M., Garcia-Martinez, C., Agell, N., Lopez-Soriano, F.J., Authier, F.J., Gherardi, R.K. and Argiles, J.M. (1998) Ubiquitin and proteasome gene expression is increased in skeletal muscle of slim AIDS patients. Int. J. Mol. Med., 2, 69-73.
30. Mitch, W.E. and Goldberg, A.L. (1996) Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N. Engl. J. Med., 335, 1897-1905.
31. Molkentin, J. and Dorn, I.G. (2001) Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu. Rev. Physiol., 63, 391-426.
32. Moore, J.W., Dionne, C., Jaye, M. and Swain, J.L. (1991) The mRNAs encoding acidic FGF, basic FGF and FGF receptor are coordinately downregulated during myogenic differentiation. Development, 111, 741-748.
33. Odelberg, S.J., Kollhoff, A. and Keating, M.T. (2000) Dedifferentiation of mammalian myotubes induced by msx1. Cell, 103, 1099-1109.
34. Okkema, P.G., Harrison, S.W., Plunger, V., Aryana, A. and Fire, A. (1993) Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics, 135, 385-404.
35. Olfert, I.M., Breen, E.C., Mathieu-Costello, O. and Wagner, P.D. (2001) Skeletal muscle capillarity and angiogenic mRNA levels after exercise training in normoxia and chronic hypoxia. J. Appl. Physiol., 91, 1176-1184.
36. Olwin, B.B. and Hauschka, S.D. (1988) Cell surface fibroblast growth factor and epidermal growth factor receptors are permanently lost during skeletal muscle terminal differentiation in culture. J. Cell Biol., 107, 761-769.
37. Patil, C. and Walter, P. (2001) Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol., 13, 349-355.
38. Rommel, C., Clarke, B.A., Zimmermann, S., Nunez, L., Rossman, R., Reid, K., Moelling, K., Yancopoulos, G.D. and Glass, D.J. (1999) Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science, 286, 1738-1741.
39. Rooyackers, O.E. and Nair, K.S. (1997) Hormonal regulation of human muscle protein metabolism. Annu. Rev. Nutr., 17, 457-485.
40. Roubin, R., Naert, K., Popovici, C., Vatcher, G., Coulier, F., Thierry Mieg, J., Pontarotti, P., Birnbaum, D., Baillie, D. et al. (1999) let-756, a C.elegans fgf essential for worm development. Oncogene, 18, 6741-6747.
41. Ryder, J.W., Fahlman, R., Wallberg Henriksson, H., Alessi, D.R., Krook, A. and Zierath, J.R. (2000) Effect of contraction on mitogen-activated protein kinase signal transduction in skeletal muscle. Involvement o the mitogen- and stress-activated protein kinase 1. J. Biol. Chem., 275, 1457-1462.
42. Saito, A., Higuchi, I., Nakagawa, M., Saito, M., Uchida, Y., Inose, M., Kasai, T., Niiyama, T., Fukunaga, H. et al. (2000) An overexpression of fibroblast growth factor (FGF) and FGF receptor 4 in a severe clinical phenotype of facioscapulohumeral muscular dystrophy. Muscle Nerve, 23, 490-497.
43. Schafer, W. R., Kim, R., Sterne, R., Thorner, J., Kim, S.H. and Rine, J. (1989) Genetic and pharmacological suppression of oncogenic mutations in ras genes of yeast and humans. Science, 245, 379-385.
44. Schultz, E. and McCormick, K.M. (1994) Skeletal muscle satellite cells. Rev. Physiol. Biochem. Pharmacol., 123, 213-257.
45. Schutzman, J.L., Borland, C.Z., Newman, J.C., Robinson, M.K., Kokel, M. and Stern, M.J. (2001) The Caenorhabditis elegans EGL-15 signaling pathway implicates a DOS-like multisubstrate adaptor protein in fibroblast growth factor signal transduction. Mol. Cell. Biol., 21, 8104-8116.
46. Selfors, L.M., Schutzman, J.L., Borland, C.Z. and Stern, M.J. (1998) soc-2 encodes a leucine-rich repeat protein implicated in fibroblast growth factor receptor signaling. Proc. Natl Acad. Sci. USA, 95, 6903-6908.
47. Shen, X. et al. (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C.elegans development. Cell, 107, 893-903.
48. Sieburth, D.S., Sun, Q. and Han, M. (1998) SUR-8, a conserved Ras-binding protein with leucine-rich repeats, positively regulates Ras-mediated signaling in C.elegans. Cell, 94, 119-130.
49. Sogos, V., Balaci, L., Ennas, M.G., Dell'era, P., Presta, M. and Gremo, F. (1998) Developmentally regulated expression and localization of fibroblast growth factor receptors in the human muscle. Dev. Dyn., 211, 362-373.
50. Solomon, V. and Goldberg, A.L. (1996) Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J. Biol. Chem., 271, 26690-26697.
51. Stern, M.J. and Horvitz, H.R. (1991) A normally attractive cell interaction is repulsive in two C.elegans mesodermal cell migration mutants. Development, 113, 797-803.
52. Sternberg, P.W. and Han, M. (1998) Genetics of RAS signaling in C.elegans. Trends Genet., 14, 466-472.
53. Sternberg, P.W., Lesa, G., Lee, J., Katz, W.S., Yoon, C., Clandinin, T.R., Huang, L.S., Chamberlin, H.M. and Jongeward, G. (1995) LET-23-mediated signal transduction during Caenorhabditis elegans development. Mol. Reprod. Dev., 42, 523-528.
54. Suzuki, J., Yamazaki, Y., Guang, L., Kaziro, Y. and Koide, H. (2000) Involvement of Ras and Ral in chemotactic migration of skeletal myoblasts. Mol. Cell. Biol., 20, 4658-4665.
55. Szewczyk, N.J., Hartman, J.J., Barmada, S.J. and Jacobson, L.A. (2000) Genetic defects in acetylcholine signalling promote protein degradation in muscle cells of Caenorhabditis elegans. J. Cell Sci., 113, 2003-2010.
56. Szewczyk, N.J., Peterson, B.K. and Jacobson, L.A. (2002) Activation of Ras and the MAP kinase pathway promotes protein degradation in muscle cells of Caenorhabditis elegans. Mol. Cell. Biol., 22, 4181-4188.
57. Tan, P.B. and Kim, S.K. (1999) Signaling specificity: the RTK/RAS/MAP kinase pathway in metazoans. Trends Genet., 15, 145-149.
58. Tisdale, M.J. (2001) Loss of skeletal muscle in cancer: biochemical mechanisms. Front. Biosci., 6, D164-D174.
59. Wolkow, C.A., Kimura, K.D., Lee, M.S. and Ruvkun, G. (2000) Regulation of C.elegans life-span by insulinlike signaling in the nervous system. Science, 290, 147-150.
60. Yusoff, P., Lao, D.H., Ong, S.H., Wong, E.S., Lim, J., Lo, T.L., Leong, H.F., Fong, C.W. and Guy, G.R. (2002) Sprouty2 inhibits the Ras/MAP kinase pathway by inhibiting the activation of Raf. J. Biol. Chem., 277, 3195-3201.
61. Zdinak, L.A., Greenberg, I.B., Szewczyk, N.J., Barmada, S.J., Cardamone Rayner, M., Hartman, J.J. and Jacobson, L.A. (1997) Transgene-coded chimeric proteins as reporters of intracellular proteolysis: starvation-induced catabolism of a lacZ fusion protein in muscle cells of Caenorhabditis elegans. J. Cell. Biochem., 67, 143-153.