New negative feedback regulators of Egfr signaling in Drosophila

Genetics

Volumn 191, Issue 4, 2012, Pages 1213-1226

  Butchar, Jonathan P ^a   Cain, Donna ^a   Manivannan, Sathiya N ^a   McCue, Andrea D ^a   Bonanno, Liana ^a   Halula, Sarah ^a   Truesdell, Sharon ^a   Austin, Christina L ^a   Jacobsen, Thomas L ^a   Simcox, Amanda ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAMTS1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; NEU DIFFERENTIATION FACTOR; PROTEOHEPARAN SULFATE; SULF1 PROTEIN; SULFATASE; UNCLASSIFIED DRUG;

ARTICLE; DROSOPHILA; EXTRACELLULAR SPACE; GENE FUNCTION; GENE INTERACTION; GENETIC ANALYSIS; MICROARRAY ANALYSIS; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; BODY PATTERNING; DROSOPHILA; DROSOPHILA PROTEINS; EPISTASIS, GENETIC; FEEDBACK, PHYSIOLOGICAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOTYPE; LIGANDS; PHENOTYPE; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SULFATASES; TRANSCRIPTOME; VEINS; WING;

EID: 84865067902     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.112.141093     Document Type: Article

References (91)

1. Ai, X., A. T. Do, O. Lozynska, M. Kusche-Gullberg, U. Lindahl et al., 2003 QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J. Cell Biol. 162: 341-351.
2. Ai, X., A. T. Do, M. Kusche-Gullberg, U. Lindahl, K. Lu et al., 2006 Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2. J. Biol. Chem. 281: 4969-4976.
3. Ai, X., T. Kitazawa, A. T. Do, M. Kusche-Gullberg, P. A. Labosky et al., 2007 SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development 134: 3327-3338.
4. Alias, Z., and A. G. Clark, 2007 Studies on the glutathione S-transferase proteome of adult Drosophila melanogaster: responsiveness to chemical challenge. Proteomics 7: 3618-3628.
5. Apte, S. S., 2009 A disintegrin-like and metalloprotease (reprolysintype) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J. Biol. Chem. 284: 31493-31497.
6. Asha, H., I. Nagy, G. Kovacs, D. Stetson, I. Ando et al., 2003 Analysis of Ras-induced overproliferation in Drosophila hemocytes. Genetics 163: 203-215.
7. Avraham, R., and Y. Yarden, 2011 Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 12: 104-117.
8. Aza-Blanc, P., F. A. Ramirez-Weber, M. P. Laget, C. Schwartz, and T. B. Kornberg, 1997 Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89: 1043-1053.
9. Baena-Lopez, L. A., J. C. Pastor-Pareja, and J. Resino, 2003 Wg and Egfr signalling antagonise the development of the peripodial epithelium in Drosophila wing discs. Development 130: 6497-6506.
10. Bhambhani, C., J. L. Chang, D. L. Akey, and K. M. Cadigan, 2011 The oligomeric state of CtBP determines its role as a transcriptional co-activator and co-repressor of Wingless targets. EMBO J. 30: 2031-2043.
11. Blair, S. S., 2007 Wing vein patterning in Drosophila and the analysis of intercellular signaling. Annu. Rev. Cell Dev. Biol. 23: 293-319.
12. Bolstad, B. M., R. A. Irizarry, M. Astrand, and T. P. Speed, 2003 A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
13. Brand, A., and N. Perrimon, 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
14. Buff, E., A. Carmena, S. Gisselbrecht, F. Jimenez, and A. M. Michelson, 1998 Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification ofembryonic muscle progenitors. Development 125: 2075-2086.
15. Butler, M. J., T. L. Jacobsen, D. M. Cain, M. G. Jarman, M. Hubank et al., 2003 Discovery of genes with highly restricted expression patterns in the Drosophila wing disc using DNA oligonucleotide microarrays. Development 130: 659-670.
16. Casci, T., J. Vinos, and M. Freeman, 1999 Sprouty, an intracellular inhibitor of Ras signaling. Cell 96: 655-665.
17. Clifford, R. J., and T. Schupbach, 1989 Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homolog of the vertebrate EGF receptor gene. Genetics 123: 771-787.
18. Coppey, M., A. N. Boettiger, A.M. Berezhkovskii, and S. Y. Shvartsman, 2008 Nuclear trapping shapes the terminal gradient in the Drosophila embryo. Curr. Biol. 18: 915-919.
19. de Celis, J. F., M. Llimargas, and J. Casanova, 1995 Ventral veinless, the gene encoding the Cf1a transcription factor, links positional information and cell differentiation during embryonic and imaginal development in Drosophila melanogaster. Development 121: 3405-3416.
20. Dhoot, G. K., M. K. Gustafsson, X. Ai, W. Sun, D. M. Standiford et al., 2001 Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293: 1663-1666.
21. Dietzl, G., D. Chen, F. Schnorrer, K. C. Su, Y. Barinova et al., 2007 A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
22. El Hour, M., A. Moncada-Pazos, S. Blacher, A. Masset, S. Cal et al., 2010 Higher sensitivity of Adamts12-deficient mice to tumor growth and angiogenesis. Oncogene 29: 3025-3032.
23. Fang, M., J. Li, T. Blauwkamp, C. Bhambhani, N. Campbell et al., 2006 C-terminal-binding protein directly activates and represses Wnt transcriptional targets in Drosophila. EMBO J. 25: 2735-2745.
24. Firth, L. C., and N. E. Baker, 2007 Spitz from the retina regulates genes transcribed in the second mitotic wave, peripodial epithelium, glia and plasmatocytes of the Drosophila eye imaginal disc. Dev. Biol. 307: 521-538.
25. Gabay, L., H. Scholz, M. Golembo, A. Klaes, B.-Z. Shilo et al., 1996 EGF receptor signaling induces pointed P1 transcription and inactivates Yan protein in the Drosophila embryonic ventral ectoderm. Development 122: 3355-3362.
26. Gabay, L., R. Seger, and B.-Z. Shilo, 1997 In situ activation pattern of Drosophila EGF receptor pathway during development. Science 277: 1103-1106.
27. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling et al., 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80.
28. Ghiglione, C., K. L. R. Carraway, L. T. Amundadottir, R. E. Boswell, N. Perrimon et al., 1999 The transmembrane molecule kekkon 1 acts in a feedback loop to negatively regulate the activity of the Drosophila EGF receptor during oogenesis. Cell 96: 847-856.
29. Golembo, M., R. Schweitzer, M. Freeman, and B.-Z. Shilo, 1996 argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 122: 223-230.
30. Golembo, M., T. Yarnitzky, T. Volk, and B. Z. Shilo, 1999 Vein expression is induced by the EGF receptor pathway to provide a positive feedback loop in patterning the Drosophila embryonic ventral ectoderm. Genes Dev. 13: 158-162.
31. Gomez, A. R., A. Lopez-Varea, C. Molnar, E. de la Calle-Mustienes, M. Ruiz-Gomez et al., 2005 Conserved cross-interactions in Drosophila and Xenopus between Ras/MAPK signaling and the dual-specificity phosphatase MKP3. Dev. Dyn. 232: 695-708.
32. Hacohen, N., S. Kramer, D. Sutherland, Y. Hiromi, and M. A. Krasnow, 1998 sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92: 253-263.
33. Holst, C. R., H. Bou-Reslan, B. B. Gore, K. Wong, D. Grant et al., 2007 Secreted sulfatases Sulf1 and Sulf2 have overlapping yet essential roles in mouse neonatal survival. PLoS ONE 2: e575.
34. Iwamoto, R., N. Mine, T. Kawaguchi, S. Minami, K. Saeki et al., 2010 HB-EGF function in cardiac valve development requires interaction with heparan sulfate proteoglycans. Development 137: 2205-2214.
35. Jordan, K. C., S. D. Hatfield, M. Tworoger, E. J. Ward, K. A. Fischer et al., 2005 Genome wide analysis of transcript levels after perturbation of the EGFR pathway in the Drosophila ovary. Dev. Dyn. 232: 709-724.
36. Kamimura, K., T. Koyama, H. Habuchi, R. Ueda, M. Masu et al., 2006 Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J. Cell Biol. 174: 773-778.
37. Kim, S. E., S. H. Kim, and K. Y. Choi, 2003 Regulation of Drosophila MKP-3 by Drosophila ERK. Ann. N. Y. Acad. Sci. 1010: 51-61.
38. Klein, D. E., V. M. Nappi, G. T. Reeves, S. Y. Shvartsman, and M. A. Lemmon, 2004 Argos inhibits epidermal growth factor receptor signalling by ligand sequestration. Nature 430: 1040-1044.
39. Kleinschmit, A., T. Koyama, K. Dejima, Y. Hayashi, K. Kamimura et al., 2010 Drosophila heparan sulfate 6-O endosulfatase regulates Wingless morphogen gradient formation. Dev. Biol. 345: 204-214.
40. Lai, J. P., D. S. Sandhu, A. M. Shire, and L. R. Roberts, 2008 The tumor suppressor function of human sulfatase 1 (SULF1) in carcinogenesis. J. Gastrointest. Cancer 39: 149-158.
41. Lamanna, W. C., R. J. Baldwin, M. Padva, I. Kalus, G. Ten Dam et al., 2006 Heparan sulfate 6-O-endosulfatases: discrete in vivo activities and functional co-operativity. Biochem. J. 400: 63-73.
42. Le Goff, C., and V. Cormier-Daire, 2011 The ADAMTS(L) family and human genetic disorders. Hum. Mol. Genet. 20: R163-R167.
43. Li, Q., and J. A. Loeb, 2001 Neuregulin-heparan-sulfate proteoglycan interactions produce sustained erbB receptor activation required for the induction of acetylcholine receptors in muscle. J. Biol. Chem. 276: 38068-38075.
44. Li, X., and R. W. Carthew, 2005 A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123: 1267-1277.
45. Lin, E. A., and C. J. Liu, 2010 The role of ADAMTSs in arthritis. Protein Cell 1: 33-47.
46. Liu, Y. J., Y. Xu, and Q. Yu, 2006 Full-length ADAMTS-1 and the ADAMTS-1 fragments display pro-and antimetastatic activity, respectively. Oncogene 25: 2452-2467.
47. Llimargas, M., and J. Casanova, 1997 Ventral veinless, a POU domain transcription factor, regulates different transduction pathways required for tracheal branching in Drosophila. Development 124: 3273-3281.
48. Lu, X., Q. Wang, G. Hu, C. Van Poznak, M. Fleisher et al., 2009 ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis. Genes Dev. 23: 1882-1894.
49. Lum, D. H., J. Tan, S. D. Rosen, and Z. Werb, 2007 Gene trap disruption of the mouse heparan sulfate 6-O-endosulfatase gene, Sulf2. Mol. Cell. Biol. 27: 678-688.
50. Mahtouk, K., F. W. Cremer, T. Reme, M. Jourdan, M. Baudard et al., 2006 Heparan sulphate proteoglycans are essential for the myeloma cell growth activity of EGF-family ligands in multiple myeloma. Oncogene 25: 7180-7191.
51. Molnar, C., A. Lopez-Varea, R. Hernandez, and J. F. de Celis, 2006 A gain-of-function screen identifying genes required for vein formation in the Drosophila melanogaster wing. Genetics 174: 1635-1659.
52. Molokwu, C. N., O. O. Adeniji, S. Chandrasekharan, F. C. Hamdy, and D. J. Buttle, 2010 Androgen regulates ADAMTS15 gene expression in prostate cancer cells. Cancer Invest. 28: 698-710.
53. Moncada-Pazos, A., A. J. Obaya, M. F. Fraga, C. G. Viloria, G. Capella et al., 2009 The ADAMTS12 metalloprotease gene is epigenetically silenced in tumor cells and transcriptionally activated in the stroma during progression of colon cancer. J. Cell Sci. 122: 2906-2913.
54. Morimoto-Tomita, M., K. Uchimura, Z. Werb, S. Hemmerich, and S. D. Rosen, 2002 Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J. Biol. Chem. 277: 49175-49185.
55. Nicholson, A. C., S. B. Malik, J. M. Logsdon, Jr., and E. G. Van Meir, 2005 Functional evolution of ADAMTS genes: evidence from analyses of phylogeny and gene organization. BMCEvol. Biol. 5:11.
56. O'Connor, M. B., D. Umulis, H. G. Othmer, and S. S. Blair, 2006 Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133: 183-193.
57. O'Neill, E. M., I. Rebay, R. Tijan, and G. M. Rubin, 1994 The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78: 137-147.
58. Ozdowski, E. F., Y. M. Mowery, and C. Cronmiller, 2009 Stall encodes an ADAMTS metalloprotease and interacts genetically with Delta in Drosophila ovarian follicle formation. Genetics 183: 1027-1040.
59. Pai, L. M., G. Barcelo, and T. Schupbach, 2000 D-cbl, a negative regulator of the Egfr pathway, is required for dorsoventral patterning in Drosophila oogenesis. Cell 103: 51-61.
60. Pallavi, S. K., and L. S. Shashidhara, 2003 Egfr/Ras pathway mediates interactions between peripodial and disc proper cells in Drosophila wing discs. Development 130: 4931-4941.
61. Pankonin, M. S., J. T. Gallagher, and J. A. Loeb, 2005 Specific structural features of heparan sulfate proteoglycans potentiate neuregulin-1 signaling. J. Biol. Chem. 280: 383-388.
62. Porter, S., I. M. Clark, L. Kevorkian, and D. R. Edwards, 2005 The ADAMTS metalloproteinases. Biochem. J. 386: 15-27.
63. Porter, S., P. N. Span, F. C. Sweep, V. C. Tjan-Heijnen, C. J. Pennington et al., 2006 ADAMTS8 and ADAMTS15 expression predicts survival in human breast carcinoma. Int. J. Cancer 118: 1241-1247.
64. Queenan, A. M., A. Ghabrial, and T. Schupbach, 1997 Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development 124: 3871-3880.
65. Ricciardelli, C., K. M. Frewin, A. Tan Ide, E. D. Williams, K. Opeskin et al., 2011 The ADAMTS1 protease gene is required for mammary tumor growth and metastasis. Am. J. Pathol. 179: 3075-3085.
66. Rintelen, F., E. Hafen, and K. Nairz, 2003 The Drosophila dualspecificity ERK phosphatase DMKP3 cooperates with the ERK tyrosine phosphatase PTP-ER. Development 130: 3479-3490.
67. Rosen, S. D., and H. Lemjabbar-Alaoui, 2010 Sulf-2: an extracellular modulator of cell signaling and a cancer target candidate. Expert Opin. Ther. Targets 14: 935-949.
68. Salter, R. C., T. G. Ashlin, A. P. Kwan, and D. P. Ramji, 2010 ADAMTS proteases: Key roles in atherosclerosis? J. Mol. Med. (Berl.) 88: 1203-1211.
69. Sarrazin, S., W. C. Lamanna, and J. D. Esko, 2011 Heparan sulfate proteoglycans. Cold Spring Harb. Perspect. Biol. 3: 1-33.
70. Schnepp, B., G. Grumbling, T. Donaldson, and A. Simcox, 1996 Vein is a novel component in the Drosophila epidermal growth factor receptor pathway with similarity to the neuregulins. Genes Dev. 10: 2302-2313.
71. Schnepp, B., T. Donaldson, G. Grumbling, S. Ostrowski, R. Schweitzer et al., 1998 EGF domain swap converts a Drosophila EGFreceptor activator into an inhibitor. Genes Dev. 12: 908-913.
72. Schweitzer, R., R. Howes, R. Smith, B.-Z. Shilo, and M. Freeman, 1995 Inhibition of Drosophila EGF receptor activation by the secreted protein Argos. Nature 376: 699-702.
73. Shilatifard, A., and R. D. Cummings, 1994 Purification and characterization of N-acetylglucosamine-6-sulfate sulfatase from bovine kidney: evidence for the presence of a novel endosulfatase activity. Biochemistry 33: 4273-4282.
74. Shilo, B. Z., 2005 Regulating the dynamics of EGF receptor signaling in space and time. Development 132: 4017-4027.
75. Simcox, A. A., G. Grumbling, B. Schnepp, C. Bennington-Mathias, E. Hersperger et al., 1996 Molecular, phenotypic, and expression analysis of vein, a gene required for growth of the Drosophila wing disc. Dev. Biol. 177: 475-489.
76. Simon, M. A., D. D. Bowtell, G. S. Dodson, T. R. Laverty, and G. M. Rubin, 1991 Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67: 701-716.
77. Smith, R. K., P. M. Carroll, J. D. Allard, and M. A. Simon, 2002 MASK, a large ankyrin repeat and KH domain-containing protein involved in Drosophila receptor tyrosine kinase signaling. Development 129: 71-82.
78. Stanton, H., J. Melrose, C. B. Little, and A. J. Fosang, 2011 Proteoglycan degradation by the ADAMTS family of proteinases. Biochim. Biophys. Acta 1812: 1616-1629.
79. Sturtevant, M. A., and E. Bier, 1995 Analysis of the genetic hierarchy guiding wing vein development in Drosophila. Development 121: 785-801.
80. Sturtevant, M. A., M. Roark, and E. Bier, 1993 The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway. Genes Dev. 7: 961-973.
81. Urban, S., J. R. Lee, and M. Freeman, 2001 Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107: 173-182.
82. Urban, S., J. R. Lee, and M. Freeman, 2002 A family of Rhomboid intramembrane proteases activates all Drosophila membranetethered EGF ligands. EMBO J. 21: 4277-4286.
83. Viloria, C. G., A. J. Obaya, A. Moncada-Pazos, M. Llamazares, A. Astudillo et al., 2009 Genetic inactivation of ADAMTS15 metalloprotease in human colorectal cancer. Cancer Res. 69: 4926-4934.
84. Vivekanand, P., T. L. Tootle, and I. Rebay, 2004 MAE, a dual regulator of the EGFR signaling pathway, is a target of the Ets transcription factors PNT and YAN. Mech. Dev. 121: 1469-1479.
85. Wagstaff, L., R. Kelwick, J. Decock, and D. R. Edwards, 2011 The roles of ADAMTS metalloproteinases in tumorigenesis and metastasis. Front. Biosci. 16: 1861-1872.
86. Wang, S. H., A. Simcox, and G. Campbell, 2000 Dual role for Drosophila epidermal growth factor receptor signaling in early wing disc development. Genes Dev. 14: 2271-2276.
87. Wasserman, J. D., and M. Freeman, 1998 An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell 95: 355-364.
88. Wessells, R. J., G. Grumbling, T. Donaldson, S. H. Wang, and A. Simcox, 1999 Tissue-specific regulation of vein/EGF receptor signaling in Drosophila. Dev. Biol. 216: 243-259.
89. Wojcinski, A., H. Nakato, C. Soula, and B. Glise, 2011 DSulfatase-1 fine-tunes Hedgehog patterning activity through a novel regulatory feedback loop. Dev. Biol. 358: 168-180.
90. You, J., T. Belenkaya, and X. Lin, 2011 Sulfated is a negative feedback regulator of wingless in Drosophila. Dev. Dyn. 240: 640-648.
91. Zak, N. B., and B. Z. Shilo, 1990 Biochemical properties of the Drosophila EGF receptor homolog (DER) protein. Oncogene 5: 1589-1593.