|
|
|
|||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Development, Vol 126, Issue 11 2515-2525, Copyright © 1999 by Company of Biologists
JOURNAL ARTICLES |
S Kramer, M Okabe, N Hacohen, MA Krasnow and Y Hiromi
Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA.
Extracellular factors such as FGF and EGF control various aspects of morphogenesis, patterning and cellular proliferation in both invertebrates and vertebrates. In most systems, it is primarily the distribution of these factors that controls the differential behavior of the responding cells. Here we describe the role of Sprouty in eye development. Sprouty is an extracellular protein that has been shown to antagonize FGF signaling during tracheal branching in Drosophila. It is a novel type of protein with a highly conserved cysteine-rich region. In addition to the embryonic tracheal system, sprouty is also expressed in other tissues including the developing eye imaginal disc, embryonic chordotonal organ precursors and the midline glia. In each of these tissues, EGF receptor signaling is known to participate in the control of the correct number of neurons or glia. We show that, in all three tissues, the loss of sprouty results in supernumerary neurons or glia, respectively. Furthermore, overexpression of sprouty in wing veins and ovarian follicle cells, two other tissues where EGF signaling is required for patterning, results in phenotypes that resemble the loss-of-function phenotypes of Egf receptor. These results suggest that Sprouty acts as an antagonist of EGF as well as FGF signaling pathways. These receptor tyrosine kinase-mediated pathways may share not only intracellular signaling components but also extracellular factors that modulate the strength of the signal.
This article has been cited by other articles:
![]() |
K. Sugiura, Y.-Q. Su, Q. Li, K. Wigglesworth, M. M. Matzuk, and J. J. Eppig Fibroblast Growth Factors and Epidermal Growth Factor Cooperate with Oocyte-Derived Members of the TGFbeta Superfamily to Regulate Spry2 mRNA Levels in Mouse Cumulus Cells Biol Reprod, November 1, 2009; 81(5): 833 - 841. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. K. Mardakheh, M. Yekezare, L. M. Machesky, and J. K. Heath Spred2 interaction with the late endosomal protein NBR1 down-regulates fibroblast growth factor receptor signaling J. Cell Biol., October 19, 2009; 187(2): 265 - 277. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. L. Franciscovich, A. D. V. Mortimer, A. A. Freeman, J. Gu, and S. Sanyal Overexpression Screen in Drosophila Identifies Neuronal Roles of GSK-3{beta}/shaggy as a Regulator of AP-1-Dependent Developmental Plasticity Genetics, December 1, 2008; 180(4): 2057 - 2071. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Chandramouli, C. Y. Yu, P. Yusoff, D.-H. Lao, H. F. Leong, K. Mizuno, and G. R. Guy Tesk1 Interacts with Spry2 to Abrogate Its Inhibition of ERK Phosphorylation Downstream of Receptor Tyrosine Kinase Signaling J. Biol. Chem., January 18, 2008; 283(3): 1679 - 1691. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Rottinger, A. Saudemont, V. Duboc, L. Besnardeau, D. McClay, and T. Lepage FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis and regulate gastrulation during sea urchin development Development, January 15, 2008; 135(2): 353 - 365. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Sese, M. Corominas, H. Stocker, T. I. Heino, E. Hafen, and F. Serras The Cdi/TESK1 kinase is required for Sevenless signaling and epithelial organization in the Drosophila eye J. Cell Sci., December 15, 2006; 119(24): 5047 - 5056. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Bundschu, U. Walter, and K. Schuh The VASP-Spred-Sprouty Domain Puzzle J. Biol. Chem., December 1, 2006; 281(48): 36477 - 36481. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Cabrita, F. Jaggi, S. P. Widjaja, and G. Christofori A Functional Interaction between Sprouty Proteins and Caveolin-1 J. Biol. Chem., September 29, 2006; 281(39): 29201 - 2912. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Chi, P. Itaranta, S. Zhang, and S. Vainio Sprouty2 Is Involved in Male Sex Organogenesis by Controlling Fibroblast Growth Factor 9-Induced Mesonephric Cell Migration to the Developing Testis Endocrinology, August 1, 2006; 147(8): 3777 - 3788. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. A. Jarvis, S. J. Toering, M. A. Simon, M. A. Krasnow, and R. K. Smith-Bolton Sprouty proteins are in vivo targets of Corkscrew/SHP-2 tyrosine phosphatases Development, March 15, 2006; 133(6): 1133 - 1142. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. DaSilva, L. Xu, H. J. Kim, W. T. Miller, and D. Bar-Sagi Regulation of sprouty stability by mnk1-dependent phosphorylation. Mol. Cell. Biol., March 1, 2006; 26(5): 1898 - 1907. [Abstract] [Full Text] [PDF] |
||||
![]() |
K.-i. Ozaki, S. Miyazaki, S. Tanimura, and M. Kohno Efficient suppression of FGF-2-induced ERK activation by the cooperative interaction among mammalian Sprouty isoforms J. Cell Sci., December 15, 2005; 118(24): 5861 - 5871. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Anderson, R. Bhandari, and J. P. Kumar A Genetic Screen Identifies Putative Targets and Binding Partners of CREB-Binding Protein in the Developing Drosophila Eye Genetics, December 1, 2005; 171(4): 1655 - 1672. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. A. Pieper, X. Wu, T. W. Han, S. J. Estill, Q. Dang, L. C. Wu, S. Reece-Fincanon, C. A. Dudley, J. A. Richardson, D. J. Brat, et al. The neuronal PAS domain protein 3 transcription factor controls FGF-mediated adult hippocampal neurogenesis in mice PNAS, September 27, 2005; 102(39): 14052 - 14057. [Abstract] [Full Text] [PDF] |
||||
![]() |
B.-Z. Shilo Regulating the dynamics of EGF receptor signaling in space and time Development, September 15, 2005; 132(18): 4017 - 4027. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Nonami, T. Taketomi, A. Kimura, K. Saeki, H. Takaki, T. Sanada, K. Taniguchi, M. Harada, R. Kato, and A. Yoshimura The Sprouty-related protein, Spred-1, localizes in a lipid raft/caveola and inhibits ERK activation in collaboration with caveolin-1 Genes Cells, September 1, 2005; 10(9): 887 - 895. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Haimov-Kochman, A. Ravhon, D. Prus, C. Greenfield, Z. Finci-Yeheskel, D. S.Goldman-Wohl, S. Natanson-Yaron, R. Reich, S. Yagel, and A. Hurwitz Expression and regulation of Sprouty-2 in the granulosa-lutein cells of the corpus luteum Mol. Hum. Reprod., August 1, 2005; 11(8): 537 - 542. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Iwanami, Y. Hiromi, and M. Okabe Cell-type specific utilization of multiple negative feedback loops generates developmental constancy Genes Cells, July 1, 2005; 10(7): 743 - 752. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Takayama, P. May, R. G. W. Anderson, and J. Herz Low Density Lipoprotein Receptor-related Protein 1 (LRP1) Controls Endocytosis and c-CBL-mediated Ubiquitination of the Platelet-derived Growth Factor Receptor {beta} (PDGFR{beta}) J. Biol. Chem., May 6, 2005; 280(18): 18504 - 18510. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Rubin, Y. Zwang, N. Vaisman, D. Ron, and Y. Yarden Phosphorylation of Carboxyl-terminal Tyrosines Modulates the Specificity of Sprouty-2 Inhibition of Different Signaling Pathways J. Biol. Chem., March 11, 2005; 280(10): 9735 - 9744. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Wilson, E. Vogelsang, and M. Leptin FGF signalling and the mechanism of mesoderm spreading in Drosophila embryos Development, February 1, 2005; 132(3): 491 - 501. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Suzuki-Hirano, T. Sato, and H. Nakamura Regulation of isthmic Fgf8 signal by sprouty2 Development, January 15, 2005; 132(2): 257 - 265. [Abstract] [Full Text] [PDF] |
||||
![]() |
B Kwabi-Addo, M Ozen, and M Ittmann The role of fibroblast growth factors and their receptors in prostate cancer Endocr. Relat. Cancer, December 1, 2004; 11(4): 709 - 724. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Torii, K. Nakayama, T. Yamamoto, and E. Nishida Regulatory Mechanisms and Function of ERK MAP Kinases J. Biochem., November 1, 2004; 136(5): 557 - 561. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. L. Lo, P. Yusoff, C. W. Fong, K. Guo, B. J. McCaw, W. A. Phillips, H. Yang, E. S. M. Wong, H. F. Leong, Q. Zeng, et al. The Ras/Mitogen-Activated Protein Kinase Pathway Inhibitor and Likely Tumor Suppressor Proteins, Sprouty 1 and Sprouty 2 Are Deregulated in Breast Cancer Cancer Res., September 1, 2004; 64(17): 6127 - 6136. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Kwabi-Addo, J. Wang, H. Erdem, A. Vaid, P. Castro, G. Ayala, and M. Ittmann The Expression of Sprouty1, an Inhibitor of Fibroblast Growth Factor Signal Transduction, Is Decreased in Human Prostate Cancer Cancer Res., July 15, 2004; 64(14): 4728 - 4735. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. Ding, S. Bellusci, W. Shi, and D. Warburton Genomic structure and promoter characterization of the human Sprouty4 gene, a novel regulator of lung morphogenesis Am J Physiol Lung Cell Mol Physiol, July 1, 2004; 287(1): L52 - L59. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Alvarado, A. H. Rice, and J. B. Duffy Bipartite Inhibition of Drosophila Epidermal Growth Factor Receptor by the Extracellular and Transmembrane Domains of Kekkon1 Genetics, May 1, 2004; 167(1): 187 - 202. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. M. Mason, D. J. Morrison, B. Bassit, M. Dimri, H. Band, J. D. Licht, and I. Gross Tyrosine Phosphorylation of Sprouty Proteins Regulates Their Ability to Inhibit Growth Factor Signaling: A Dual Feedback Loop Mol. Biol. Cell, May 1, 2004; 15(5): 2176 - 2188. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Yamada, M. Okabe, and Y. Hiromi EDL/MAE regulates EGF-mediated induction by antagonizing Ets transcription factor Pointed Development, September 1, 2003; 130(17): 4085 - 4096. [Abstract] [Full Text] [PDF] |
||||
![]() |
R.-B. Yang, C. K. D. Ng, S. M. Wasserman, L. G. Komuves, M. E. Gerritsen, and J. N. Topper A Novel Interleukin-17 Receptor-like Protein Identified in Human Umbilical Vein Endothelial Cells Antagonizes Basic Fibroblast Growth Factor-induced Signaling J. Biol. Chem., August 29, 2003; 278(35): 33232 - 33238. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. R. Guy, E. S. M. Wong, P. Yusoff, S. Chandramouli, T. L. Lo, J. Lim, and C. W. Fong Sprouty: how does the branch manager work? J. Cell Sci., August 1, 2003; 116(15): 3061 - 3068. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Sudarsan, S. Pasalodos-Sanchez, S. Wan, A. Gampel, and H. Skaer A genetic hierarchy establishes mitogenic signalling and mitotic competence in the renal tubules of Drosophila Development, March 4, 2003; 129(4): 935 - 944. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. E. Egan, A. B. Hall, B. A. Yatsula, and D. Bar-Sagi The bimodal regulation of epidermal growth factor signaling by human Sprouty proteins PNAS, April 30, 2002; 99(9): 6041 - 6046. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Kheradmand, K. Rishi, and Z. Werb Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2 J. Cell Sci., February 15, 2002; 115(4): 839 - 848. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Gross, B. Bassit, M. Benezra, and J. D. Licht Mammalian Sprouty Proteins Inhibit Cell Growth and Differentiation by Preventing Ras Activation J. Biol. Chem., November 30, 2001; 276(49): 46460 - 46468. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. P. Kumar and K. Moses The EGF receptor and notch signaling pathways control the initiation of the morphogenetic furrow during Drosophila eye development Development, July 15, 2001; 128(14): 2689 - 2697. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Furthauer, F. Reifers, M. Brand, B. Thisse, and C. Thisse sprouty4 acts in vivo as a feedback-induced antagonist of FGF signaling in zebrafish Development, June 15, 2001; 128(12): 2175 - 2186. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. L. Nutt, K. S. Dingwell, C. E. Holt, and E. Amaya Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning Genes & Dev., May 1, 2001; 15(9): 1152 - 1166. [Abstract] [Full Text] |
||||
![]() |
M.-A. Impagnatiello, S. Weitzer, G. Gannon, A. Compagni, M. Cotten, and G. Christofori Mammalian Sprouty-1 and -2 Are Membrane-Anchored Phosphoprotein Inhibitors of Growth Factor Signaling in Endothelial Cells J. Cell Biol., March 5, 2001; 152(5): 1087 - 1098. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Rusten, R Cantera, J Urban, G Technau, F. Kafatos, and R Barrio Spalt modifies EGFR-mediated induction of chordotonal precursors in the embryonic PNS of Drosophila promoting the development of oenocytes Development, January 3, 2001; 128(5): 711 - 722. [Abstract] [PDF] |
||||
![]() |
L. Firth, J. Manchester, J. A. Lorenzen, M. Baron, and L. A. Perkins Identification of Genomic Regions That Interact With a Viable Allele of the Drosophila Protein Tyrosine Phosphatase Corkscrew Genetics, October 1, 2000; 156(2): 733 - 748. [Abstract] [Full Text] |
||||
![]() |
D. C. Goldman, G. R. Martin, and P. P. Tam Fate and function of the ventral ectodermal ridge during mouse tail development Development, May 15, 2000; 127(10): 2113 - 2123. [Abstract] [PDF] |
||||
![]() |
A. Taguchi, K. Sawamoto, and H. Okano Mutations Modulating the Argos-Regulated Signaling Pathway in Drosophila Eye Development Genetics, April 1, 2000; 154(4): 1639 - 1648. [Abstract] [Full Text] |
||||
![]() |
M.-h. Jin, K. Sawamoto, M. Ito, and H. Okano The Interaction between the Drosophila Secreted Protein Argos and the Epidermal Growth Factor Receptor Inhibits Dimerization of the Receptor and Binding of Secreted Spitz to the Receptor Mol. Cell. Biol., March 15, 2000; 20(6): 2098 - 2107. [Abstract] [Full Text] |
||||
![]() |
A. Trumpp, M. J. Depew, J. L.R. Rubenstein, J. M. Bishop, and G. R. Martin Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch Genes & Dev., December 1, 1999; 13(23): 3136 - 3148. [Abstract] [Full Text] |
||||
![]() |
G Minowada, L. Jarvis, C. Chi, A Neubuser, X Sun, N Hacohen, M. Krasnow, and G. Martin Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed Development, January 10, 1999; 126(20): 4465 - 4475. [Abstract] [PDF] |
||||
![]() |
A Reich, A Sapir, and B Shilo Sprouty is a general inhibitor of receptor tyrosine kinase signaling Development, January 9, 1999; 126(18): 4139 - 4147. [Abstract] [PDF] |
||||
![]() |
A. Sasaki, T. Taketomi, T. Wakioka, R. Kato, and A. Yoshimura Identification of a Dominant Negative Mutant of Sprouty That Potentiates Fibroblast Growth Factor- but Not Epidermal Growth Factor-induced ERK Activation J. Biol. Chem., September 21, 2001; 276(39): 36804 - 36808. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Lim, E. S. M. Wong, S. H. Ong, P. Yusoff, B. C. Low, and G. R. Guy Sprouty Proteins Are Targeted to Membrane Ruffles upon Growth Factor Receptor Tyrosine Kinase Activation. IDENTIFICATION OF A NOVEL TRANSLOCATION DOMAIN J. Biol. Chem., October 13, 2000; 275(42): 32837 - 32845. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. H. Lee, D. J. Schloss, L. Jarvis, M. A. Krasnow, and J. L. Swain Inhibition of Angiogenesis by a Mouse Sprouty Protein J. Biol. Chem., February 2, 2001; 276(6): 4128 - 4133. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. S. M. Wong, J. Lim, B. C. Low, Q. Chen, and G. R. Guy Evidence for Direct Interaction between Sprouty and Cbl J. Biol. Chem., February 16, 2001; 276(8): 5866 - 5875. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Yigzaw, L. Cartin, S. Pierre, K. Scholich, and T. B. Patel The C Terminus of Sprouty Is Important for Modulation of Cellular Migration and Proliferation J. Biol. Chem., June 15, 2001; 276(25): 22742 - 22747. [Abstract] [Full Text] [PDF] |
||||