FGFR4 and its novel splice form in myogenic cells: Interplay of glycosylation and tyrosine phosphorylation

Journal of Cellular Physiology

Volumn 215, Issue 3, 2008, Pages 803-817

  Kwiatkowski, Boguslaw A ^a   Kirillova, Irina ^a   Richard, Robert E ^a   Israeli, David ^b   Yablonka Reuveni, Zipora ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b GÉNÉTHON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 4; MYOD PROTEIN; COMPLEMENTARY DNA; FIBROBLAST GROWTH FACTOR RECEPTOR 3; ISOPROTEIN; PHOSPHOTYROSINE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; ALTERNATIVE RNA SPLICING; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; CYTOLOGY; GENETICS; GLYCOSYLATION; HUMAN; METABOLISM; MUSCLE CELL; PHOSPHORYLATION; SKELETAL MUSCLE SATELLITE CELL; WESTERN BLOTTING;

ALTERNATIVE SPLICING; ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; DNA, COMPLEMENTARY; GLYCOSYLATION; HUMANS; MICE; MICE, INBRED C57BL; MUSCLE CELLS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN ISOFORMS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 4; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 42949127648     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21365     Document Type: Article

References (65)

1. Amara JF, Courage NL, Gilman M. 1999. Cell surface tagging and a suicide mechanism in a single chimeric human protein. Hum Gene Ther 10:2651-2655.
2. Anastasi S, Giordano S, Sthandier O, Gambarotta G, Maione R, Comoglio P, Amati P. 1997. A natural hepatocyte growth factor/scatter factor autocrine loop in myoblast cells and the effect of the constitutive Met kinase activation on myogenic differentiation. J Cell Biol 137:1057-1068.
3. Andres V, Walsh K. 1996. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J Cell Biol 132:657-666.
4. Bergstrom DA, Penn BH, Strand A, Perry RL, Rudnicki MA, Tapscott SJ. 2002. Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol Cell 9:587-600.
5. Boilly B, Vereoutter-Edouart AS, Hondermarck H, Nurcombe V, Le Bourhis X. 2000. FGF signals for cell proliferation and migration through different pathways. Cytokine Growth Factor Rev 11:295-302.
6. Cavallaro U, Niedermeyer J, Fuxa M, Christofori G. 2001. N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nat Cell Biol 3:650-657.
7. Citores L, Khnykin D, Sorensen V, Wesche J, Klingenberg O, Wiedlocha A, Olsnes S. 2001. Modulation of intracellular transport of acidic fibroblast growth factor by mutations in the cytoplasmic receptor domain. J Cell Sci 114:1677-1689.
8. Duchesne L, Tissot B, Rudd TR, Dell A, Fernig DG. 2006. N-glycosylation of fibroblast growth factor receptor I regulates ligand and heparan sulfate co-receptor binding. J Biol Chem 281:27178-27189.
9. Eswarakumar VP, Lax I, Schlessinger J. 2005. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16:139-149.
10. Ezzat S, Zheng L, Yu S, Asa SL. 2001. A soluble dominant negative fibroblast growth factor receptor 4 isoform in human MCF-7 breast cancer cells. Biochem Biophys Res Commun 287:60-65.
11. Ezzat S, Zheng L, Asa SL. 2004. Pituitary tumor-derived fibroblast growth factor receptor 4 isoform disrupts neural cell-adhesion molecule/N-cadherin signaling to diminish cell adhesiveness: A mechanism underlying pituitary neoplasia. Mol Endocrinol 18:2543-2552.
12. Gao G, Goldfarb M. 1995. Heparin can activate a receptor tyrosine kinase. EMBO J 14:2183-2190.
13. Gonzalez AM, Hill DJ, Logan A, Maher PA, Baird A. 1996. Distribution of fibroblast growth factor (FGF)-2 and FGF receptor-1 messenger RNA expression and protein presence in the mid-trimester human fetus. Pediatr Res 39:375-385.
14. Graves DC, Yablonka-Reuveni Z. 2000. Vascular smooth muscle cells spontaneously adopt a skeletal muscle phenotype: A unique Myf5(-)/MyoD(+) myogenic program. J Histochem Cytochem 48:1173-1193.
15. Gutierrez A, Ratliff EP, Andres AM, Huang X, McKeehan WL, Davis RA. 2006. Bile acids decrease hepatic paraoxonase I expression and plasma high-density lipoprotein levels via FXR-mediated signaling of FGFR4. Arterioscler Thromb Vasc Biol 26:301-306.
16. Harmer NJ, Pellegrini L, Chirgadze D, Fernandez-Recio J, Blundell TL. 2004. The crystal structure of fibroblast growth factor (FGF) 19 reveals novel features of the FGF family and offers a structural basis for its unusual receptor affinity. Biochemistry 43:629-640.
17. Hart KC, Robertson SC, Donoghue DJ. 2001. Identification of tyrosine residues in constitutlvely activated fibroblast growth factor receptor 3 involved in mitogenesis, Stat activation, and phosphatidylinositol 3-kinase activation. Mol Biol Cell 12:931-942.
18. Hatch NE, Hudson M, Seto ML, Cunningham ML, Bothwell M. 2006. Intracellular retention, degradation, and signaling of glycosylation-deficient FGFR2 and craniosynostosis syndrome-associated FGFR2C278F. J Biol Chem 281:27292-27305.
19. Haugsten EM, Sorensen V, Brech A, Olsnes S, Wesche J. 2005. Different intracellular trafficking of FGF1 endocytosed by the four homologous FGF receptors. J Cell Sci 118:3869-3881.
20. Hollenberg SM, Cheng PF, Weintraub H. 1993. Use of a conditional MyoD transcription factor in studies of MyoD trans-activation and muscle determination. Proc Natl Acad Sci U S A 90:8028-8032.
21. Itoh N, Mima T, Mikawa T. 1996. Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122:291-300.
22. Jin L, Zeng H, Chien S, Otto KG, Richard RE, Emery DW, Blau CA. 2000. In vivo selection using a cell-growth switch. Nat Genet 26:64-66.
23. Johnson SE, Allen RE. 1995. Activation of skeletal muscle satellite cells and the role of fibroblast growth factor receptors. Exp Cell Res 219:449-453.
24. Johnson DE, Williams LT. 1993. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 60:1-41.
25. Kastner S, Elias MC, Rivera AJ, 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.
26. Kinsella TM, Nolan GP. 1996. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum Gene Ther 7:1405-1413.
27. Korhonen J, Partanen J, Alitalo K. 1992. Expression of FGFR-4 mRNA in developing mouse tissues. Int J Dev Biol 36:323-329.
28. Lin HY, Xu J, Ischenko I, Ornitz DM, Halegoua S, Hayman MJ. 1998. Identification of the cytoplasmic regions of fibroblast growth factor (FGF) receptor I which play important roles in induction of neurite outgrowth in PC12 cells by FGF-1. Mo1 Cell Biol 18:3762-3770.
29. Mangasarian K, Li Y, Mansukhani A, Basilico C. 1997. Mutation associated with Crouzon syndrome causes ligand-independent dimerization and activation of FGF receptor-2. J Cell Physiol 172:117-125.
30. Marics I, Padilla F, Guillemot JF, Scaal M, Marcelle C. 2002. FGFR4 signaling is a necessary step in limb muscle differentiation. Development 129:4559-4569.
31. Marks JL, McLellan MD, Zakowski MF, Lash AE, Kasai Y, Broderick S, Sarkaria IS, Pham D, Singh B, Miner TL, Fewell GA, Fulton LL, Mardis ER, Wilson RK, Kris MG, Rusch VW, Varmus H, Pao W. 2007. Mutational analysis of EGFR and related signaling pathway genes in lung adenocarcinomas identifies a novel somatic kinase domain mutation in FGFR4. PLoS ONE 2:e426.
32. Mohammadi M, McMahon G, Sun L, Tang C, Hirth P, Yeh BK, Hubbard SR, Schlessinger J. 1997. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276:955-960.
33. Mohammadi M, Olsen SK, Goetz R. 2005. A protein canyon in the FGF-FGF receptor dimer selects from an a la carte menu of heparan sulfate motifs. Curr Opin Struct Biol 15:506-516.
34. Olwin BB, Arthur K, Hannon K, Hein P, McFall A, Riley B, Szebenyi G, Zhou Z, Zuber ME, Rapraeger AC, et al. 1994. Role of FGFs in skeletal muscle and limb development. Mol Reprod Dev 39:90-100 (discussion, 100-101).
35. Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M. 1996. Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292-15297.
36. Plotnikov AN, Schlessinger J, Hubbard SR, Mohammadi M. 1999. Structural basis for FGF receptor dimerization and activation. Cell 98:641-650.
37. Powell PP, Wang CC, Horinouchi H, Shepherd K, Jacobson M, Lipson M, Jones R. 1998. Differential expression of fibroblast growth factor receptors 1 to 4 and ligand genes in late fetal and early postnatal rat lung. Am J Respir Cell Mol Biol 19:563-572.
38. Raffioni S, Thomas D, Foehr ED, Thompson LM, Bradshaw RA. 1999. Comparison of the intracellular signaling responses by three chimeric fibroblast growth factor receptors in PC12 cells. Proc Natl Acad Sci U S A 96:7178-7183.
39. Rappolee DA, Patel Y, Jacobson K. 1998. Expression of fibroblast growth factor receptors in peri-implantation mouse embryos. Mol Reprod Dev 51:254-264.
40. Shaoul E, Reich-Slotky R, Berman B, Ron D. 1995. Fibroblast growth factor receptors display both common and distinct signaling pathways. Oncogene 10:1553-1561.
41. Shefer G, Yablonka-Reuveni Z. 2008. The ins and outs of satellite cell myogenesis: The role of the ruling growth factors. In: Schiaffino S, Partridge T, editors. Skeletal muscle repair and regeneration. Series: Advances in Muscle research, Vol 3. Heidelberg, Germany: Springer. pp 107-143.
42. Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z. 2006. Satellite-cell pool size does matter: Defining the myogenic potency of aging skeletal muscle. Dev Biol 294:50-66.
43. Sorensen V, Wiedlocha A, Haugsten EM, Khnykin D, Wesche J, Olsnes S. 2006. Different abilities of the four FGFRs to mediate FGF-1 translocation are linked to differences in the receptor C-terminal tail. J Cell Sci 119:4332-4341.
44. Stark KL, McMahon JA, McMahon AP. 1991. FGFR-4, a new member of the fibroblast growth factor receptor family, expressed in the definitive endoderm and skeletal muscle lineages of the mouse. Development 113:641-651.
45. Takaishi S, Sawada M, Morita Y, Seno H, Fukuzawa H, Chiba T. 2000. Identification of a novel alternative splicing of human FGF receptor 4: Soluble-form splice variant expressed in human gastrointestinal epithelial cells. Biochem Biophys Res Commun 267:658-662.
46. Tuominen H, Heikinheimo P, Loo BM, Kataja K, Oker-Blom C, Uutela M, Jalkanen M, Goldman A. 2001. Expression and glycosylation studies of human FGF receptor 4. Protein Expr Purif 21:275-285.
47. Vainikka S, Joukov V, Wennstrom S, Bergman M, Pelicci PG, Alitalo K. 1994. Signal transduction by fibroblast growth factor receptor-4 (FGFR-4). Comparison with FGFR-1. J Biol Chem 269:18320-18326.
48. van Heumen WR, Claxton C, Pickles JO. 1999. Fibroblast growth factor receptor-4 splice variants cause deletion of a critical tyrosine. IUBMB Life 48:73-78.
49. Wang JK, Goldfarb M. 1997. Amino acid residues which distinguish the mitogenic potentials of two FGF receptors. Oncogene 14:1767-1778.
50. Wang JK, Gao G, Goldfarb M. 1994. Fibroblast growth factor receptors have different signaling and mitogenic potentials. Mol Cell Biol 14:181-188.
51. Weinstein M, Xu X, Ohyama K, Deng CX. 1998. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 125:3615-3623.
52. Welm BE, Freeman KW, Chen M, Contreras A, Spencer DM, Rosen JM. 2002. Inducible dimerization of FGF R1: Development of a mouse model to analyze progressive transformation of the mammary gland. J Cell Biol 157:703-714.
53. Whitney ML, Otto KG, Blau CA, Reinecke H, Murry CE. 2001. Control of myoblast proliferation with a synthetic ligand. J Biol Chem 276:41191-41196.
54. Winterpacht A, Hilbert K, Stelzer C, Schweikardt T, Decker H, Segerer H, Spranger J, Zabel B. 2000. A novel mutation in FGFR-3 disrupts a putative N-glycosylation site and results in hypochondroplasia. Physiol Genomics 2:9-12.
55. Xie MH, Holcomb I, Deuel B, Dowd P, Huang A, Vagts A, Foster J, Liang J, Brush J, Gu Q, Hillan K, Goddard A, Gurney AL. 1999. FGF-19, a novel fibroblast growth factor with unique specificity for FGFR4. Cytokine 11:729-735.
56. Xu X, Weinstein M, Li C, Deng C. 1999. Fibroblast growth factor receptors (FGFRs) and their roles in limb development. Cell Tissue Res 296:33-43.
57. Yablonka-Reuveni Z, Rivera AJ. 1997. Influence of PDGF-BB on proliferation and transition through the MyoD-myogenin-MEF2A expression program during myogenesis in mouse C2 myoblasts. Growth Factors 15:1-27.
58. Yablonka-Reuveni Z, Balestreri TM, Bowen-Pope DF. 1990. Regulation of proliferation and differentiation of myoblasts derived from adult mouse skeletal muscle by specific isoforms of PDGF. J Cell Biol 111:1623-1629.
59. Yaffe D, Saxel O. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270:725-727.
60. Yoon SJ, Seiler SH, Kucherlapati R, Leinwand L. 1992. Organization of the human skeletal myosin heavy chain gene cluster. Proc Natl Acad Sci U S A 89:12078-12082.
61. Yu C, Wang F, Kan M, Jin C, Jones RB, Weinstein M, Deng CX, McKeehan WL. 2000. Elevated cholesterol metabolism and bile acid synthesis in mice lacking membrane tyrosine kinase receptor FG FR4. J Biol Chem 275:15482-15489.
62. Yu S, Asa SL, Weigel RJ, Ezzat S. 2003. Pituitary tumor AP-2alpha recognizes a cryptic promoter in intron 4 of fibroblast growth factor receptor 4. J Biol Chem 278:19597-19602.
63. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. 2006. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281:15694-15700.
64. Zhao P, Hoffman EP. 2004. Embryonic myogenesis pathways in muscle regeneration. Dev Dyn 229:380-392.
65. Zhao P, Caretti G, Mitchell S, McKeehan WL, Boskey AL, Pachman LM, Sartorelli V, Hoffman EP. 2006. Fgfr4 is required for effective muscle regeneration in vivo. Delineation of a MyoD-Tead2-Fgfr4 transcriptional pathway. J Biol Chem 281:429-438.