Sprouty4, an FGF inhibitor, displays cyclic gene expression under the control of the notch segmentation clock in the mouse PSM

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Hayashi, Shinichi ^a,b   Shimoda, Taiju ^a,b   Nakajima, Masato ^a,b   Tsukada, Yuki ^a,b   Sakumura, Yuichi ^a,b   Dale, J Kim ^c   Maroto, Miguel ^c   Kohno, Kenji ^a   Matsui, Takaaki ^a,b   Bessho, Yasumasa ^a,b  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; NOTCH RECEPTOR; PROTEIN INHIBITOR; SPROUTY PROTEIN; SPROUTY PROTEIN 4; UNCLASSIFIED DRUG; WNT PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GLYCOSYLTRANSFERASE; HES7 PROTEIN, MOUSE; LFNG PROTEIN, MOUSE; NERVE PROTEIN; SPRY4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EXPLANT; GENE EXPRESSION; IN SITU HYBRIDIZATION; MESODERM; MOUSE; MUTANT; NONHUMAN; OSCILLATION; PERIODICITY; PROMOTER REGION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL RHYTHM; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; ZEBRA FISH;

VERTEBRATA;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOLOGICAL CLOCKS; BLOTTING, WESTERN; EMBRYO, MAMMALIAN; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOSYLTRANSFERASES; IN SITU HYBRIDIZATION; MESODERM; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; RECEPTORS, NOTCH; ZEBRAFISH;

EID: 66049115814     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005603     Document Type: Article

References (44)

1. Pourquie O (2001) Vertebrate somitogenesis. Annu Rev Cell Dev Biol 17: 311-350.
2. Dequeant ML, Pourquie O (2008) Segmental patterning of the vertebrate embryonic axis. Nat Rev Genet 9: 370-382.
3. Palmeirim I, Henrique D, Ish-Horowicz D, Pourquie O (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91: 639-648.
4. Bessho Y, Kageyama R (2003) Oscillations, clocks and segmentation. Curr Opin Genet Dev 13: 379-384.
5. Bessho Y, Sakata R, Komatsu S, Shiota K, Yamada S, et al. (2001) Dynamic expression and essential functions of Hes7 in somite segmentation. Genes Dev 15: 2642-2647.
6. Holley SA, Geisler R, Nüsslein-Volhard C (2000) Control of her1 expression during zebrafish somitogenesis by a Delta-dependent oscillator and an independent wave-front activity. Genes Dev 14: 1678-1690.
7. Oates AC, Ho RK (2002) Hairy/E(spl)-related (Her) genes are central components of the segmentation oscillator and display redundancy with the Delta/Notch signaling pathway in the formation of anterior segmental boundaries in the zebrafish. Development 129: 2929-2946.
8. Henry CA, Urban MK, Dill KK, Merlie JP, Page MF, et al. (2002) Two linked hairy/Enhancer of split-related zebrafish genes, her1 and her7, function together to refine alternating somite boundaries. Development 129: 3693-3704.
9. Jouve C, Palmeirim I, Henrique D, Beckers J, Gossler A, et al. (2000) Notch signalling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm. Development 127: 1421-1429.
10. McGrew MJ, Dale JK, Fraboulet S, Pourquie O (1998) The lunatic fringe gene is a target of the molecular clock linked to somite segmentation in avian embryos. Curr Biol 8: 979-982.
11. Aulehla A, Johnson RL (1999) Dynamic expression of lunatic fringe suggests a link between notch signaling and an autonomous cellular oscillator driving somite segmentation. Dev Biol 207: 49-61.
12. Forsberg H, Crozet F, Brown NA (1998) Waves of mouse Lunatic fringe expression, in four-hour cycles at two-hour intervals, precede somite boundary formation. Curr Biol 8: 1027-1030.
13. Elmasri H, Liedtke D, Lucking G, Volff JN, Gessler M, et al. (2004) her7 and hey1, but not lunatic fringe show dynamic expression during somitogenesis in medaka (Oryzias latipes). Gene Expr Patterns 4: 553-559.
14. Prince VE, Holley SA, Bally-Cuif L, Prabhakaran B, Oates AC, et al. (2001) Zebrafish lunatic fringe demarcates segmental boundaries. Mech Dev 105: 175-180.
15. Ishikawa A, Kitajima S, Takahashi Y, Kokubo H, Kanno J, et al. (2004) Mouse Nkd1, a Wnt antagonist, exhibits oscillatory gene expression in the PSM under the control of Notch signaling. Mech Dev 121: 1443-1453.
16. Dale JK, Malapert P, Chal J, Vilhais-Neto G, Maroto M, et al. (2006) Oscillations of the snail genes in the presomitic mesoderm coordinate segmental patterning and morphogenesis in vertebrate somitogenesis. Dev Cell 10: 355-366.
17. Aulehla A, Wehrle C, Brand-Saberi B, Kemler R, Gossler A, et al. (2003) Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell 4: 395-406.
18. Niwa Y, Masamizu Y, Liu T, Nakayama R, Deng CX, et al. (2007) The initiation and propagation of Hes7 oscillation are cooperatively regulated by Fgf and notch signaling in the somite segmentation clock. Dev Cell 13: 298-304.
19. Dequeant ML, Glynn E, Gaudenz K, Wahl M, Chen J, et al. (2006) A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314: 1595-1598.
20. Bessho Y, Hirata H, Masamizu Y, Kageyama R (2003) Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock. Genes Dev 17: 1451-1456.
21. Dale JK, Maroto M, Dequeant ML, Malapert P, McGrew M, et al. (2003) Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421: 275-278.
22. Sawada A, Shinya M, Jiang YJ, Kawakami A, Kuroiwa A, et al. (2001) Fgf/ MAPK signalling is a crucial positional cue in somite boundary formation. Development 128: 4873-4880.
23. Dubrulle J, McGrew MJ, Pourquie O (2001) FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106: 219-232.
24. Dubrulle J, Pourquie O (2004) fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427: 419-422.
25. Kawamura A, Koshida S, Hijikata H, Sakaguchi T, Kondoh H, et al. (2005) Zebrafish hairy/enhancer of split protein links FGF signaling to cyclic gene expression in the periodic segmentation of somites. Genes Dev 19: 1156-1161.
26. de Maximy AA, Nakatake Y, Moncada S, Itoh N, Thiery JP, et al. (1999) Cloning and expression pattern of a mouse homologue of drosophila sprouty in the mouse embryo. Mech Dev 81: 213-216.
27. Minowada G, Jarvis LA, Chi CL, Neubuser A, Sun X, et al. (1999) Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126: 4465-4475.
28. Pourquie O, Tam PP (2001) A nomenclature for prospective somites and phases of cyclic gene expression in the presomitic mesoderm. Dev Cell 1: 619-620.
29. Maroto M, Dale JK, Dequeant ML, Petit AC, Pourquie O (2005) Synchronised cycling gene oscillations in presomitic mesoderm cells require cell-cell contact. Int J Dev Biol 49: 309-315.
30. Bessho Y, Miyoshi G, Sakata R, Kageyama R (2001) Hes7: a bHLH-type repressor gene regulated by Notch and expressed in the presomitic mesoderm. Genes Cells 6: 175-185.
31. Zhang N, Gridley T (1998) Defects in somite formation in lunatic fringe-deficient mice. Nature 394: 374-377.
32. Evrard YA, Lun Y, Aulehla A, Gan L, Johnson RL (1998) lunatic fringe is an essential mediator of somite segmentation and patterning. Nature 394: 377-381.
33. Ding W, Bellusci S, Shi W, Warburton D (2004) Genomic structure and promoter characterization of the human Sprouty4 gene, a novel regulator of lung morphogenesis. Am J Physiol Lung Cell Mol Physiol 287: L52-59.
34. Takebayashi K, Sasai Y, Sakai Y, Watanabe T, Nakanishi S, et al. (1994) Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1. Negative autoregulation through the multiple N box elements. J Biol Chem 269: 5150-5156.
35. Ikeda K, Nagano K, Kawakami K (1993) Anomalous interaction of Sp1 and specific binding of an E-box-binding protein with the regulatory elements of the Na,K-ATPase alpha 2 subunit gene promoter. Eur J Biochem 218: 195-204.
36. Holley SA, Julich D, Rauch GJ, Geisler R, Nüsslein-Volhard C (2002) her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. Development 129: 1175-1183.
37. Mason JM, Morrison DJ, Basson MA, Licht JD (2006) Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol 16: 45-54.
38. Sasaki A, Taketomi T, Kato R, Saeki K, Nonami A, et al. (2003) Mammalian Sprouty4 suppresses Ras-independent ERK activation by binding to Raf1. Nat Cell Biol 5: 427-432.
39. Shim K, Minowada G, Coling DE, Martin GR (2005) Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev Cell 8: 553-564.
40. Taketomi T, Yoshiga D, Taniguchi K, Kobayashi T, Nonami A, et al. (2005) Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia. Nat Neurosci 8: 855-857.
41. Klein T, Arias AM (1998) Interactions among Delta, Serrate and Fringe modulate Notch activity during Drosophila wing development. Development 125: 2951-2962.
42. Taniguchi K, Ayada T, Ichiyama K, Kohno R, Yonemitsu Y, et al. (2007) Sprouty2 and Sprouty4 are essential for embryonic morphogenesis and regulation of FGF signaling. Biochem Biophys Res Commun 352: 896-902.
43. Matsui T, Raya A, Kawakami Y, Callol-Massot C, Capdevila J, et al. (2005) Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev 19: 164-175.
44. Sawano A, Miyawaki A (2000) Directed evolution of green fluorescent protein by a new versatile PCR strategy for site-directed and semi-random mutagenesis. Nucleic Acids Res 28: E78.