Cubilin, a high affinity receptor for fibroblast growth factor 8, is required for cell survival in the developing vertebrate head

Journal of Biological Chemistry

Volumn 288, Issue 23, 2013, Pages 16655-16670

  Cases, Olivier ^a   Perea Gomez, Aitana ^b   Aguiar, Diego P ^c   Nykjaer, Anders ^d   Amsellem, Sabine ^a   Chandellier, Jacqueline ^a   Umbhauer, Muriel ^c   Cereghini, Silvia ^c   Madsen, Mette ^d   Collignon, Jérôme ^b   Verroust, Pierre ^a   Riou, Jean François ^c   Creuzet, Sophie E ^c   Kozyraki, Renata ^a  

^a INSTITUT DE LA VISION   (France)

^b INSTITUT JACQUES MONOD   (France)

^c CNRS   (France)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; GENE INACTIVATION; HIGH AFFINITY LIGANDS; INTESTINAL ABSORPTION; MEMBRANE BINDING; SIGNALING ACTIVITY; SURFACE PLASMONS; TERNARY COMPLEX;

CELL MEMBRANES; LIGANDS; MOLECULAR BIOLOGY;

MAMMALS;

CUBILIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 17; FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR RECEPTOR; FORKHEAD TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN FOXG1; SMAD1 PROTEIN; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANURA; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPORT; CHICK; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOCYTOSIS; FACE HYPOPLASIA; FOREBRAIN HYPOPLASIA; HYPOPLASIA; INTRACELLULAR SIGNALING; MEMBRANE BINDING; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR AFFINITY; SURFACE PLASMON RESONANCE;

CELL DEATH; CUBILIN; DEVELOPMENT; FIBROBLAST GROWTH FACTOR (FGF); MEGALIN; MOLECULAR CELL BIOLOGY; MOUSE; XENOPUS;

ANIMALS; CELL SURVIVAL; ENDOCYTOSIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTORS; GENE SILENCING; HEAD; LIGANDS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, TRANSGENIC; NEURAL CREST; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RECEPTORS, FIBROBLAST GROWTH FACTOR;

ANURA; VERTEBRATA;

EID: 84878769871     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.451070     Document Type: Article

References (58)

1. Kozyraki, R., and Gofflot, F. (2007) Multiligand endocytosis and congenital defects: roles of cubilin, megalin, and amnionless. Curr. Pharm. Des. 13, 3038-3046 (Pubitemid 350130969)
2. Amsellem, S., Gburek, J., Hamard, G., Nielsen, R., Willnow, T. E., Devuyst, O., Nexo, E., Verroust, P. J., Christensen, E. I., and Kozyraki, R. (2010) Cubilin is essential for albumin reabsorption in the renal proximal tubule. J. Am. Soc. Nephrol. 21, 1859-1867
3. Kozyraki, R., and Cases, O. (2013) Vitamin B12 absorption: Mammalian physiology and acquired and inherited disorders. Biochimie 95, 1002-1007
4. Reznichenko, A., Snieder, H., van den Born, J., de Borst, M. H., Damman, J., van Dijk, M. C., van Goor, H., Hepkema, B. G., Hillebrands, J.-L., Leuvenink, H. G., Niesing, J., Bakker, S. J., Seelen, M., Navis, G., and REGaTTA (REnal GeneTics TrAnsplantation) Groningen Group (2012) CUBN as a novel locus for end-stage renal disease: insights from renal transplantation. PLoS ONE 7, e36512
5. Franke, B., Vermeulen, S. H., Steegers-Theunissen, R. P., Coenen, M. J., Schijvenaars, M. M., Scheffer, H., den Heijer, M., and Blom, H. J. (2009) An association study of 45 folate-related genes in spina bifida: Involvement of cubilin (CUBN) and tRNA aspartic acid methyltransferase 1 (TRDMT1). Birth Defects Res. Part A Clin. Mol. Teratol. 85, 216-226
6. Pangilinan, F., Molloy, A. M., Mills, J. L., Troendle, J. F., Parle-McDermott, A., Signore, C., O'Leary, V. B., Chines, P., Seay, J. M., Geiler-Samerotte, K., Mitchell, A., VanderMeer, J. E., Krebs, K. M., Sanchez, A., Cornman-Homonoff, J., Stone, N., Conley, M., Kirke, P. N., Shane, B., Scott, J. M., and Brody, L. C. (2012) Evaluation of common genetic variants in 82 candidate genes as risk factors for neural tube defects. BMC Med. Genet. 13, 62
7. Assémat, E., Châtelet, F., Chandellier, J., Commo, F., Cases, O., Verroust, P., and Kozyraki, R. (2005) Overlapping expression patterns of the multiligand endocytic receptors cubilin and megalin in the CNS, sensory organs and developing epithelia of the rodent embryo. Gene Expr. Patterns 6, 69-78 (Pubitemid 41819233)
8. Smith, B. T., Mussell, J. C., Fleming, P. A., Barth, J. L., Spyropoulos, D. D., Cooley, M. A., Drake, C. J., and Argraves, W. S. (2006) Targeted disruption of cubilin reveals essential developmental roles in the structure and function of endoderm and in somite formation. BMC Dev. Biol. 6, 30
9. Assémat, E., Vinot, S., Gofflot, F., Linsel-Nitschke, P., Illien, F., Châtelet, F., Verroust, P., Louvet-Vallée, S., Rinninger, F., and Kozyraki, R. (2005) Expression and role of cubilin in the internalization of nutrients during the peri-implantation development of the rodent embryo. Biol. Reprod. 72, 1079-1086 (Pubitemid 40547970)
10. 12 complex, mediates high density lipoprotein holoparticle endocytosis. Proc. Natl. Acad. Sci. U.S.A. 96, 10158-10163
11. Moestrup, S. K., Kozyraki, R., Kristiansen, M., Kaysen, J. H., Rasmussen, H. H., Brault, D., Pontillon, F., Goda, F. O., Christensen, E. I., Hammond, T. G., and Verroust, P. J. (1998) The intrinsic factor-vitamin B12 receptor and target of teratogenic antibodies is a megalin-binding peripheral membrane protein with homology to developmental proteins. J. Biol. Chem. 273, 5235-5242 (Pubitemid 28108687)
12. Barth, J. L., and Argraves, W. S. (2001) Cubilin and megalin: partners in lipoprotein and vitamin metabolism. Trends Cardiovasc. Med. 11, 26-31 (Pubitemid 32547234)
13. Fyfe, J. C., Madsen, M., Højrup, P., Christensen, E. I., Tanner, S. M., de la Chapelle, A., He, Q., and Moestrup, S. K. (2004) The functional cobalamin (vitamin B12)-intrinsic factor receptor is a novel complex of cubilin and amnionless. Blood 103, 1573-1579 (Pubitemid 38268944)
14. Christ, A., Christa, A., Kur, E., Lioubinski, O., Bachmann, S., Willnow, T. E., and Hammes, A. (2012) LRP2 is an auxiliary SHH receptor required to condition the forebrain ventral midline for inductive signals. Dev. Cell 22, 268-278
15. Spoelgen, R., Hammes, A., Anzenberger, U., Zechner, D., Andersen, O. M., Jerchow, B., and Willnow, T. E. (2005) LRP2/megalin is required for patterning of the ventral telencephalon. Development 132, 405-414 (Pubitemid 40268289)
16. Kozyraki, R., Fyfe, J., Verroust, P. J., Jacobsen, C., Dautry-Varsat, A., Gburek, J., Willnow, T. E., Christensen, E. I., and Moestrup, S. K. (2001) Mega-lin- dependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia. Proc. Natl. Acad. Sci. U.S.A. 98, 12491-12496 (Pubitemid 33019973)
17. Zucker, R. M., Hunter, S., and Rogers, J. M. (1998) Confocal laser scanning microscopy of apoptosis in organogenesis-stage mouse embryos. Cytometry 33, 348-354 (Pubitemid 28492379)
18. Le Panse, S., Galceran, M., Pontillon, F., Lelongt, B., van de Putte, M., Ronco, P. M., and Verroust, P. J. (1995) Immunofunctional properties of a yolk sac epithelial cell line expressing two proteins gp280 and gp330 of the intermicrovillar area of proximal tubule cells: inhibition of endocytosis by the specific antibodies. Eur. J. Cell Biol. 67, 120-129
19. Colas, A., Cartry, J., Buisson, I., Umbhauer, M., Smith, J. C., and Riou, J.-F. (2008) Mix. 1/2-dependent control of FGF availability during gastrulation is essential for pronephros development in Xenopus. Dev. Biol. 320, 351-365
20. Kristiansen, M., Kozyraki, R., Jacobsen, C., Nexø, E., Verroust, P. J., and Moestrup, S. K. (1999) Molecular dissection of the intrinsic factor-vitamin B12 receptor, cubilin, discloses regions important for membrane association and ligand binding. J. Biol. Chem. 274, 20540-20544
21. Nykjaer, A., Lee, R., Teng, K. K., Jansen, P., Madsen, P., Nielsen, M. S., Jacobsen, C., Kliemannel, M., Schwarz, E., Willnow, T. E., Hempstead, B. L., and Petersen, C. M. (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848 (Pubitemid 38297746)
22. Creuzet, S. E. (2009) Regulation of pre-otic brain development by the cephalic neural crest. Proc. Natl. Acad. Sci. U.S.A. 106, 15774-15779
23. 12 malabsorption with proteinuria). Orphanet J. Rare Dis. 1, 17
24. Hayashi, S., Lewis, P., Pevny, L., and McMahon, A. P. (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Gene Expr. Patterns 2, 93-97 (Pubitemid 36356020)
25. Paek, H., Gutin, G., and Hébert, J. M. (2009) FGF signaling is strictly required to maintain early telencephalic precursor cell survival. Development 136, 2457-2465
26. Anderson, R. M., Stottmann, R. W., Choi, M., and Klingensmith, J. (2006) Endogenous bone morphogenetic protein antagonists regulate mammalian neural crest generation and survival. Dev. Dyn. 235, 2507-2520 (Pubitemid 44325264)
27. Ohkubo, Y., Chiang, C., and Rubenstein, J. L. (2002) Coordinate regulation and synergistic actions of BMP4, SHH, and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111, 1-17 (Pubitemid 34310447)
28. Mason, I. (2007) Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat. Rev. Neurosci. 8, 583-596
29. Geng, X., and Oliver, G. (2009) Pathogenesis of holoprosencephaly. J. Clin. Invest. 119, 1403-1413
30. Hébert, J. M., and Fishell, G. (2008) The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci. 9, 678-685
31. Hoch, R. V., Rubenstein, J. L., and Pleasure, S. (2009) Genes and signaling events that establish regional patterning of the mammalian forebrain. Semin. Cell Dev. Biol. 20, 378-386
32. Klingensmith, J., Matsui, M., Yang, Y.-P., and Anderson, R. M. (2010) Roles of bone morphogenetic protein signaling and its antagonism in holoprosencephaly. Am. J. Med. Genet. C Semin. Med. Genet. 154C, 43-51
33. Le Douarin, N. M., Couly, G., and Creuzet, S. E. (2012) The neural crest is a powerful regulator of pre-otic brain development. Dev. Biol. 366, 74-82
34. Geng, X., Speirs, C., Lagutin, O., Inbal, A., Liu, W., Solnica-Krezel, L., Jeong, Y., Epstein, D. J., and Oliver, G. (2008) Haploinsufficiency of Six3 fails to activate Sonic hedgehog expression in the ventral forebrain and causes holoprosencephaly. Dev. Cell 15, 236-247
35. Liu, W., Lagutin, O., Swindell, E., Jamrich, M., and Oliver, G. (2010) Neuroretina specification in mouse embryos requires Six3-mediated suppression of Wnt8b in the anterior neural plate. J. Clin. Invest. 120, 3568-3577
36. Itasaki, N., and Hoppler, S. (2010) Cross-talk between Wnt and bone morphogenic protein signaling: a turbulent relationship. Dev. Dyn. 239, 16-33
37. Eswarakumar, V. P., Lax, I., and Schlessinger, J. (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 16, 139-149 (Pubitemid 40616112)
38. Turner, N., and Grose, R. (2010) Fibroblast growth factor signalling: from development to cancer. Nat. Rev. Cancer 10, 116-129
39. Sapkota, G., Alarcón, C., Spagnoli, F. M., Brivanlou, A. H., and Massagué, J. (2007) Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol. Cell 25, 441-454 (Pubitemid 46199289)
40. Eivers, E., Demagny, H., and De Robertis, E. M. (2009) Integration of BMP and Wnt signaling via vertebrate Smad1/5/8 and Drosophila Mad. Cytokine Growth Factor Rev. 20, 357-365
41. Shinya, M., Koshida, S., Sawada, A., Kuroiwa, A., and Takeda, H. (2001) Fgf signalling through MAPK cascade is required for development of the subpallial telencephalon in zebrafish embryos. Development 128, 4153-4164 (Pubitemid 33077028)
42. Regad, T., Roth, M., Bredenkamp, N., Illing, N., and Papalopulu, N. (2007) The neural progenitor-specifying activity of FoxG1 is antagonistically regulated by CKI and FGF. Nat. Cell Biol. 9, 531-540 (Pubitemid 46696534)
43. Guillemot, F., and Zimmer, C. (2011) From cradle to grave: the multiple roles of fibroblast growth factors in neural development. Neuron 71, 574-588
44. Guo, Q., Li, K., Sunmonu, N. A., and Li, J. Y. (2010) Fgf8b-containing spliceforms, but not Fgf8a, are essential for Fgf8 function during development of the midbrain and cerebellum. Dev. Biol. 338, 183-192
45. Olsen, S. K., Li, J. Y., Bromleigh, C., Eliseenkova, A. V., Ibrahimi, O. A., Lao, Z., Zhang, F., Linhardt, R. J., Joyner, A. L., and Mohammadi, M. (2006) Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain. Genes Dev. 20, 185-198 (Pubitemid 43112937)
46. Nykjaer, A., Fyfe, J. C., Kozyraki, R., Leheste, J. R., Jacobsen, C., Nielsen, M. S., Verroust, P. J., Aminoff, M., de la Chapelle, A., Moestrup, S. K., Ray, R., Gliemann, J., Willnow, T. E., and Christensen, E. I. (2001) Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D3. Proc. Natl. Acad. Sci. U.S.A. 98, 13895-13900 (Pubitemid 33115995)
47. Mohammadi, M., Olsen, S. K., and Goetz, R. (2005) A protein canyon in the FGF-FGF receptor dimer selects from an à la carte menu of heparan sulfate motifs. Curr. Opin. Struct. Biol. 15, 506-516 (Pubitemid 41393481)
48. Creuzet, S. E., Martinez, S., and Le Douarin, N. M. (2006) The cephalic neural crest exerts a critical effect on forebrain and midbrain development. Proc. Natl. Acad. Sci. U.S.A. 103, 14033-14038 (Pubitemid 44452975)
49. Creuzet, S., Schuler, B., Couly, G., and Le Douarin, N. M. (2004) Reciprocal relationships between Fgf8 and neural crest cells in facial and forebrain development. Proc. Natl. Acad. Sci. U.S.A. 101, 4843-4847 (Pubitemid 38469165)
50. Lunn, J. S., Fishwick, K. J., Halley, P. A., and Storey, K. G. (2007) A spatial and temporal map of FGF/Erk1/2 activity and response repertoires in the early chick embryo. Dev. Biol. 302, 536-552 (Pubitemid 46216273)
51. Walshe, J., and Mason, I. (2000) Expression of FGFR1, FGFR2 and FGFR3 during early neural development in the chick embryo. Mech. Dev. 90, 103-110
52. Storm, E. E., Garel, S., Borello, U., Hebert, J. M., Martinez, S., McConnell, S. K., Martin, G. R., and Rubenstein, J. L. (2006) Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 133, 1831-1844 (Pubitemid 43810989)
53. Bai, C. B., Auerbach, W., Lee, J. S., Stephen, D., and Joyner, A. L. (2002) Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129, 4753-4761 (Pubitemid 35277202)
54. Sheng, N., Xie, Z., Wang, C., Bai, G., Zhang, K., Zhu, Q., Song, J., Guillemot, F., Chen, Y.-G., Lin, A., and Jing, N. (2010) Retinoic acid regulates bone morphogenic protein signal duration by promoting the degradation of phosphorylated Smad1. Proc. Natl. Acad. Sci. U.S.A. 107, 18886-18891
55. Fuentealba, L. C., Eivers, E., Ikeda, A., Hurtado, C., Kuroda, H., Pera, E. M., and De Robertis, E. M. (2007) Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131, 980-993 (Pubitemid 350138081)
56. Gutin, G., Fernandes, M., Palazzolo, L., Paek, H., Yu, K., Ornitz, D. M., McConnell, S. K., and Hébert, J. M. (2006) FGF signalling generates ventral telencephalic cells independently of SHH. Development 133, 2937-2946 (Pubitemid 44314271)
57. Olsen, S. K., Ibrahimi, O. A., Raucci, A., Zhang, F., Eliseenkova, A. V., Yayon, A., Basilico, C., Linhardt, R. J., Schlessinger, J., and Mohammadi, M. (2004) Insights into the molecular basis for fibroblast growth factor receptor autoinhibition and ligand-binding promiscuity. Proc. Natl. Acad. Sci. U.S.A. 101, 935-940 (Pubitemid 38160562)
58. Tomihara-Newberger, C., Haub, O., Lee, H. G., Soares, V., Manova, K., and Lacy, E. (1998) The amn gene product is required in extraembryonic tissues for the generation of middle primitive streak derivatives. Dev. Biol. 204, 34-54 (Pubitemid 28563863)