Functions and mechanisms of receptor tyrosine kinase Torso signaling: Lessons from Drosophila embryonic terminal development

Developmental Dynamics

Volumn 232, Issue 3, 2005, Pages 656-672

  Li, Willis X ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

c Kit; Drosophila; Embryonic development; PDGF receptor; Review; Terminal system; Torso; Type III receptor tyrosine kinase

Indexed keywords

COLONY STIMULATING FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; ONCOPROTEIN; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE TORSO; RAF PROTEIN; RAS PROTEIN; SOS PROTEIN; STEM CELL FACTOR RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR;

CELL FATE; DROSOPHILA; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; GENE EXPRESSION; GENETIC ANALYSIS; GERM CELL; INTERNALIZATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EMBRYONIC INDUCTION; INSECT PROTEINS; MODELS, BIOLOGICAL; PROTEIN STRUCTURE, TERTIARY; RECEPTOR PROTEIN-TYROSINE KINASES; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 14644388169     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.20295     Document Type: Review

References (159)

1. Agazie YM, Movilla N, Ischenko I, Hayman MJ. 2003. The phosphotyrosine phosphatase SHP2 is a critical mediator of transformation induced by the oncogenic fibroblast growth factor receptor 3. Oncogene 22:6909-6918.
2. Ambrosio L, Mahowald AP, Perrimon N. 1989a. l(1)pole hole is required maternally for pattern formation in the terminal regions of the embryo. Development 106:145-158.
3. Ambrosio L, Mahowald AP, Perrimon N, 1989b. Requirement of the Drosophila raf homologue for torso function. Nature 342:288-291.
4. Basler K, Hafen E. 1990. Receptor tyrosine kinases mediate cell-cell interactions during Drosophila development. Prog Growth Factor Res 2:15-27.
5. Bate M, Martinez Arias A. 1993. The development of Drosophila melanogaster. Plainview, NY: Cold Spring Harbor Laboratory Press. Vol. 2. 1558 p.
6. Bellaiche Y, Bandyopadhyay R, Desplan C, Dostatni N. 1996. Neither the homeodomain nor the activation domain of Bicoid is specifically required for its down-regulation by the Torso receptor tyrosine kinase cascade. Development 122:3499-3508.
7. Biggs WH III, Zipursky SL. 1992. Primary structure, expression, and signal-dependent tyrosine phosphorylation of a Drosophila homolog of extracellular signal-regulated kinase. Proc Natl Acad Sci USA 89:6295-6299.
8. Biggs WH III, Zavitz KH, Dickson B, van der Straten A, Brunner D, Hafen E, Zipursky SL. 1994. The Drosophila rolled locus encodes a MAP kinase required in the sevenless signal transduction pathway. EMBO J 13:1628-1635.
9. Bonfini L, Karlovich CA, Dasgupta C, Banerjee U. 1992. The Son of sevenless gene product: a putative activator of Ras. Science 255:603-606.
10. Brand AH, Perrimon N. 1994. Raf acts downstream of the EGF receptor to determine dorsoventral polarity during Drosophila oogenesis. Genes Dev 8:629-639.
11. Brunner D, Oellers N, Szabad J, Biggs WH III, Zipursky SL, Hafen E. 1994. A gain-of-function mutation in Drosophila MAP kinase activates multiple receptor tyrosine kinase signaling pathways. Cell 76:875-888.
12. Campos-Ortega JA, Hartenstein V. 1997. The embryonic development of Drosophila melanogaster. Berlin: Springer, xvii. 405 p.
13. Casali A, Casanova J. 2001. The spatial control of Torso RTK activation: a C-terminal fragment of the Trunk protein acts as a signal for Torso receptor in the Drosophila embryo. Development 128:1709-1715.
14. Casanova J, Struhl G. 1989. Localized surface activity of torso, a receptor tyrosine kinase, specifies terminal body pattern in Drosophila. Genes Dev 3:2025-2038.
15. Casanova J, Struhl G. 1993. The torso receptor localizes as well as transduces the spatial signal specifying terminal body pattern in Drosophila. Nature 362:152-155.
16. Casanova J, Llimargas M, Greenwood S, Struhl G. 1994. An oncogenic form of human raf can specify terminal body pattern in Drosophila. Mech Dev 48:59-64.
17. Casanova J, Furriols M, McCormick CA, Struhl G. 1995. Similarities between trunk and spatzle, putative extracellular ligands specifying body pattern in Drosophila. Genes Dev 9:2539-2544.
18. Casci T, Vinos J, Freeman M. 1999. Sprouty, an intracellular inhibitor of Ras signaling. Cell 96:655-665.
19. Chang HC, Rubin GM. 1997. 14-3-3 epsilon positively regulates Ras-mediated signaling in Drosophila. Genes Dev 11:1132-1139.
20. Chen YJ, Chiang CS, Weng LC, Lengyel JA, Liaw GJ. 2002. Tramtrack69 is required for the early repression of tailless expression. Mech Dev 116:75-83.
21. Chong H, Vikis HG, Guan KL. 2003. Mechanisms of regulating the Raf kinase family. Cell Signal 15:463-469.
22. Chou TB, Perrimon N. 1992. Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131:643-653.
23. Clark SG, Stern MJ, Horvitz HR. 1992. C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature 356:340-344.
24. Cleghon V, Gayko U, Copeland TD, Perkins LA, Perrimon N, Morrison DK. 1996. Drosophila terminal structure development is regulated by the compensatory activities of positive and negative phosphotyrosine signaling sites on the Torso RTK. Genes Dev 10:566-577.
25. Cleghon V, Feldmann P, Ghiglione C, Copeland TD, Perrimon N, Hughes DA, Morrison DK. 1998. Opposing actions of CSW and RasGAP modulate the strength of Torso RTK signaling in the Drosophila terminal pathway. Mol Cell 2:719-727.
26. Courey AJ, Jia S. 2001. Transcriptional repression: the long and the short of it. Genes Dev 15:2786-2796.
27. Degelmann A, Hardy PA, Perrimon N, Mahowald AP. 1986. Developmental analysis of the torso-like phenotype in Drosophila produced by a maternal-effect locus. Dev Biol 115:479-489.
28. Deshpande G, Calhoun G, Schedl P. 2004. Overlapping mechanisms function to establish transcriptional quiescence in the embryonic Drosophila germline. Development 131:1247-1257.
29. Dhillon AS, Kolch W. 2002. Untying the regulation of the Raf-1 kinase. Arch Biochem Biophys 404:3-9.
30. Dickson BJ, van der Straten A, Dominguez M, Hafen E. 1996. Mutations Modulating Raf signaling in Drosophila eye development. Genetics 142:163-171.
31. Doyle HJ, Bishop JM. 1993. Torso, a receptor tyrosine kinase required for embryonic pattern formation, shares substrates with the sevenless and EGF-R pathways in Drosophila. Genes Dev 7:633-646.
32. Driever W, Nusslein-Volhard C. 1988. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54:95-104.
33. Duffy JB, Perrimon N. 1994. The torso pathway in Drosophila: lessons on receptor tyrosine kinase signaling and pattern formation. Dev Biol 166:380-395.
34. Emori Y, Sugaya R, Akimaru H, Higashijima S, Shishido E, Saigo K, Homma Y. 1994. Drosophila phospholipase C-gamma expressed predominantly in blastoderm cells at cellularization and in endodermal cells during later embryonic stages. J Biol Chem 269:19474-19479.
35. Ephrussi A, St. Johnston D. 2004. Seeing is believing: the bicoid morphogen gradient matures. Cell 116:143-152.
36. Feldmann P, Eicher EN, Leevers SJ, Hafen E, Hughes DA. 1999. Control of growth and differentiation by Drosophila Ras-GAP, a homolog of p120 Ras-GTPase-activating protein. Mol Cell Biol 19:1928-1937.
37. Feller SM. 2001. Crk family adaptors-signalling complex formation and biological roles. Oncogene 20:6348-6371.
38. Finkelstein R, Perrimon N. 1990. The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346:485-488.
39. Flores GV, Duan H, Yan H, Nagaraj R, Fu W, Zou Y, Noll M, Banerjee U. 2000. Combinatorial signaling in the specification of unique cell fates. Cell 103:75-85.
40. Fortini ME, Simon MA, Rubin GM. 1992. Signalling by the sevenless protein tyrosine kinase is mimicked by Ras1 activation. Nature 355:559-561.
41. Fragale A, Tartaglia M, Wu J, Gelb BD. 2004. Noonan syndrome-associated SHP2/PTPN11 mutants cause EGF-dependent prolonged GAB1 binding and sustained ERK2/MAPK1 activation. Hum Mutat 23:267-277.
42. Freeman M. 2000. Feedback control of intercellular signalling in development. Nature 408:313-319.
43. Furriols M, Casanova J. 2003. New EMBO member's review: in and out of Torso RTK signalling. EMBO J 22:1947-1952.
44. Garrity PA, Rao Y, Salecker I, McGlade J, Pawson T, Zipursky SL. 1996. Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 85:639-650.
45. Gayko U, Cleghon V, Copeland T, Morrison DK, Perrimon N. 1999. Synergistic activities of multiple phosphotyrosine residues mediate full signaling from the Drosophila Torso receptor tyrosine kinase. Proc Natl Acad Sci U S A 96:523-528.
46. Ghiglione C, Perrimon N, Perkins LA. 1999. Quantitative variations in the level of MAPK activity control patterning of the embryonic termini in Drosophila. Dev Biol 205:181-193.
47. Greenwood S, Struhl G. 1997. Different levels of Ras activity can specify distinct transcriptional and morphological consequences in early Drosophila embryos. Development 124:4879-4886.
48. Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow MA. 1998. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92:253-263.
49. Halfon MS, Carmena A, Gisselbrecht S, Sackerson CM, Jimenez F, Baylies MK, Michelson AM. 2000. Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103:63-74.
50. Hamilton TG, Klinghoffer RA, Corrin PD, Soriano P. 2003. Evolutionary divergence of platelet-derived growth factor alpha receptor signaling mechanisms. Mol Cell Biol 23:4013-4025.
51. Han DC, Shen TL, Guan JL. 2001. The Grb7 family proteins: structure, interactions with other signaling molecules and potential cellular functions. Oncogene 20:6315-6321.
52. Hanafusa H, Torii S, Yasunaga T, Nishida E. 2002. Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat Cell Biol 4:850-858.
53. Hanafusa H, Torii S, Yasunaga T, Matsumoto K, Nishida E. 2004. Shp2, an SH2-containing protein-tyrosine phosphatase, positively regulates receptor tyrosine kinase signaling by dephosphorylating and inactivating the inhibitor Sprouty. J Biol Chem 279:22992-22995.
54. Hanks SK, Hunter T. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9:576-596.
55. Heldin CH, Westermark B. 1999. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79:1283-1316.
56. Herbst R, Carroll PM, Allard JD, Schilling J, Raabe T, Simon MA. 1996. Daughter of sevenless is a substrate of the phosphotyrosine phosphatase Corkscrew and functions during sevenless signaling. Cell 85:899-909.
57. Heuchel R, Berg A, Tallquist M, Ahlen K, Reed RK, Rubin K, Claesson-Welsh L, Heldin CH, Soriano P. 1999. Platelet-derived growth factor beta receptor regulates interstitial fluid homeostasis through phosphatidylinositol-3′ kinase signaling. Proc Natl Acad Sci U S A 96:11410-11415.
58. Hou XS, Chou TB, Melnick MB, Perrimon N. 1995. The torso receptor tyrosine kinase can activate Raf in a Ras-independent pathway. Cell 81:63-71.
59. Janody F, Sturny R, Schaeffer V, Azou Y, Dostatni N. 2001. Two distinct domains of Bicoid mediate its transcriptional downregulation by the Torso pathway. Development 128:2281-2290.
60. Jhiang SM. 2000. The RET proto-oncogene in human cancers. Oncogene 19:5590-5597.
61. Jimenez G, Guichet A, Ephrussi A, Casanova J. 2000. Relief of gene repression by torso RTK signaling: role of capicua in Drosophila terminal and dorsoventral patterning. Genes Dev 14:224-231.
62. Jones S, Vignais ML, Broach JR. 1991. The CDC25 protein of Saccharomyces cerevisiae promotes exchange of guanine nucleotides bound to ras. Mol Cell Biol 11:2641-2646.
63. Karim FD, Chang HC, Therrien M, Wassarman DA, Laverty T, Rubin GM. 1996. A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics 143:315-329.
64. Klinghoffer RA, Hamilton TG, Hoch R, Soriano P. 2002. An allelic series at the PDGFalphaR locus indicates unequal contributions of distinct signaling pathways during development. Dev Cell 2:103-113.
65. Klingler M, Erdelyi M, Szabad J, Nusslein-Volhard C. 1988. Function of torso in determining the terminal anlagen of the Drosophila embryo. Nature 335:275-277.
66. Kockel L, Vorbruggen G, Jackle H, Mlodzik M, Bohmann D. 1997. Requirement for Drosophila 14-3-3 zeta in Raf-dependent photoreceptor development. Genes Dev 11:1140-1147.
67. Lai KM, Olivier JP, Gish GD, Henkemeyer M, McGlade J, Pawson T. 1995. A Drosophila shc gene product is implicated in signaling by the DER receptor tyrosine kinase. Mol Cell Biol 15:4810-4818.
68. Lechleider RJ, Sugimoto S, Bennett AM, Kashishian AS, Cooper JA, Shoelson SE, Walsh CT, Neel BG. 1993. Activation of the SH2-containing phosphotyrosine phosphatase SH-PTP2 by its binding site, phosphotyrosine 1009, on the human platelet-derived growth factor receptor. J Biol Chem 268:21478-21481.
69. Leevers SJ, Paterson HF, Marshall CJ. 1994. Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature 369:411-414.
70. LeMosy EK. 2003. Pattern formation: the eggshell holds the cue. Curr Biol 13:R508-R510.
71. Li J, Li WX. 2003. Drosophila gain-of-function mutant RTK Torso triggers ectopic Dpp and STAT signaling. 164:247-248.
72. Li W, Perrimon N. 1997. Specificity of receptor tyrosine kinase signaling pathways: lessons from Drosophila. Genet Eng 19:167-182.
73. Li W, Skoulakis EM, Davis RL, Perrimon N. 1997. The Drosophila 14-3-3 protein Leonardo enhances Torso signaling through D-Raf in a Ras 1-dependent manner. Development 124:4163-4171.
74. Li W, Melnick M, Perrimon N. 1998. Dual function of Ras in Raf activation. Development 125:4999-5008.
75. Li W, Noll E, Perrimon N. 2000. Identification of autosomal regions involved in Drosophila Raf function. Genetics 156:763-774.
76. Li WX, Agaisse H, Mathey-Prevot B, Perrimon N. 2002. Differential requirement for STAT by gain-of-function and wild-type receptor tyrosine kinase Torso in Drosophila. Development 129:4241-4248.
77. Li J, Xia F, Li WX. 2003. Coactivation of STAT and Ras is required for germ cell proliferation and invasive migration in Drosophila. Dev Cell 5:787-798.
78. Liaw GJ, Rudolph KM, Huang JD, Dubnicoff T, Courey AJ, Lengyel JA. 1995. The torso response element binds GAGA and NTF-1/Elf-1, and regulates tailless by relief of repression. Genes Dev 9:3163-3176.
79. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ. 2002. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108:261-269.
80. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, Lammers R, Ullrich A, Skolnik EY, Bar-Sagi D, Schlessinger J. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70:431-442.
81. Lu X, Chou TB, Williams NG, Roberts T, Perrimon N. 1993a. Control of cell fate determination by p21ras/Ras1, an essential component of torso signaling in Drosophila. Genes Dev 7:621-632.
82. Lu X, Perkins LA, Perrimon N. 1993b. The torso pathway in Drosophila: a model system to study receptor tyrosine kinase signal transduction. Dev Suppl:47-56.
83. Lu X, Melnick MB, Hsu JC, Perrimon N. 1994. Genetic and molecular analyses of mutations involved in Drosophila raf signal transduction. EMBO J 13:2592-2599.
84. Luschnig S, Krauss J, Bohmann K, Desjeux I, Nusslein-Volhard C. 2000. The Drosophila SHC adaptor protein is required for signaling by a subset of receptor tyrosine kinases. Mol Cell 5:231-241.
85. Marmor MD, Yarden Y. 2004. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23:2057-2070.
86. Marshall CJ. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
87. Martinho RG, Kunwar PS, Casanova J, Lehmann R. 2004. A noncoding RNA is required for the repression of RNApolII-dependent transcription in primordial germ cells. Curr Biol 14:159-165.
88. Melnick MB, Perkins LA, Lee M, Ambrosio L, Perrimon N. 1993. Developmental and molecular characterization of mutations in the Drosophila-raf serine/threonine protein kinase. Development 118:127-138.
89. Morisato D, Anderson KV. 1994. The spatzle gene encodes a component of the extracellular signaling pathway establishing the dorsal-ventral pattern of the Drosophila embryo. Cell 76:677-688.
90. Morrison DK. 2001. KSR: a MAPK scaffold of the Ras pathway? J Cell Sci 114:1609-1612.
91. Morrison DK, Davis RJ. 2003. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 19:91-118.
92. Nusslein-Volhard CN. 2004. The bicoid morphogen papers. I. Account from CNV. Cell 116(Suppl):S1-S5, 2 p following S9.
93. Nusslein-Volhard C, Frohnhofer HG, Lehmann R. 1987. Determination of anteroposterior polarity in Drosophila. Science 238:1675-1681.
94. Olivier JP, Raabe T, Henkemeyer M, Dickson B, Mbamalu G, Margolis B, Schlessinger J, Hafen E, Pawson T. 1993. A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73:179-191.
95. Paroush Z, Wainwright SM, Ish-Horowicz D. 1997. Torso signalling regulates terminal patterning in Drosophila by antagonising Groucho-mediated repression. Development 124:3827-3834.
96. Pawson T, Scott JD. 1997. Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075-2080.
97. Perkins LA, Larsen I, Perrimon N. 1992. corkscrew encodes a putative protein tyrosine phosphatase that functions to transduce the terminal signal from the receptor tyrosine kinase torso. Cell 70:225-236.
98. Perkins LA, Johnson MR, Melnick MB, Perrimon N. 1996. The nonreceptor protein tyrosine phosphatase corkscrew functions in multiple receptor tyrosine kinase pathways in Drosophila. Dev Biol 180:63-81.
99. Perrimon N. 1994. Signalling pathways initiated by receptor protein tyrosine kinases in Drosophila. Curr Opin Cell Biol 6:260-266.
100. Perrimon N, Engstrom L, Mahowald AP. 1985. A pupal lethal mutation with a paternally influenced maternal effect on embryonic development in Drosophila melanogaster. Dev Biol 110:480-491.
101. Perrimon N, Mohler D, Engstrom L, Mahowald AP. 1986. X-linked female-sterile loci in Drosophila melanogaster. Genetics 113:695-712.
102. Perrimon N, Engstrom L, Mahowald AP. 1989. Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics 121:333-352.
103. Perrimon N, Lu X, Hou XS, Hsu JC, Melnick MB, Chou TB, Perkins LA. 1995. Dissection of the Torso signal transduction pathway in Drosophila. Mol Reprod Dev 42:515-522.
104. Perrimon N, Lanjuin A, Arnold C, Noll E. 1996. Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations. Genetics 144:1681-1692.
105. Pignoni F, Baldarelli RM, Steingrimsson E, Diaz RJ, Patapoutian A, Merriam JR, Lengyel JA. 1990. The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell 62:151-163.
106. Pignoni F, Steingrimsson E, Lengyel JA. 1992. bicoid and the terminal system activate tailless expression in the early Drosophila embryo. Development 115:239-251.
107. Porter AC, Vaillancourt RR. 1998. Tyrosine kinase receptor-activated signal transduction pathways which lead to oncogenesis. Oncogene 17:1343-1352.
108. Raabe T, Riesgo-Escovar J, Liu X, Bausenwein BS, Deak P, Maroy P, Hafen E. 1996. DOS, a novel pleckstrin homology domain-containing protein required for signal transduction between sevenless and Ras1 in Drosophila. Cell 85:911-920.
109. Rao Y, Zipursky SL. 1998. Domain requirements for the Dock adapter protein in growth-cone signaling. Proc Natl Acad Sci U S A 95:2077-2082.
110. Rebay I. 2002. Keeping the receptor tyrosine kinase signaling pathway in check: lessons from Drosophila. Dev Biol 251:1-17.
111. Roberts WM, Look AT, Roussel MF, Sherr CJ. 1988. Tandem linkage of human CSF-1 receptor (c-fms) and PDGF receptor genes. Cell 55:655-661.
112. Robertson SC, Tynan JA, Donoghue DJ. 2000. RTK mutations and human syndromes: when good receptors turn bad [published erratum appears in Trends Genet 2000;16:368]. Trends Genet 16:265-271.
113. Robertson SC, Tynan JA, Donoghue DJ. 2000. RTK mutations and human syndromes: when good receptors turn bad [published erratum appears in Trends Genet 2000;16:368]. Trends Genet 16:265-271.
114. Rogge RD, Karlovich CA, Banerjee U. 1991. Genetic dissection of a neurodevelopmental pathway: Son of sevenless functions downstream of the sevenless and EGF receptor tyrosine kinases. Cell 64:39-48.
115. Ronchi E, Treisman J, Dostatni N, Struhl G, Desplan C. 1993. Down-regulation of the Drosophila morphogen bicoid by the torso receptor-mediated signal transduction cascade. Cell 74:347-355.
116. Rozakis-Adcock M, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W, Batzer A, Thomas S, Brugge J, Pelicci PG, et al. 1992. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360:689-692.
117. Savant-Bhonsale S, Montell DJ. 1993. torso-like encodes the localized determinant of Drosophila terminal pattern formation. Genes Dev 7:2548-2555.
118. Schmidt-Ott U. 2001. Different ways to make a head. Bioessays 23:8-11.
119. Schupbach T, Wieschaus E. 1986. Germ-line autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev Biol 113:443-448.
120. Schupbach T, Wieschaus E. 1989. Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics 121:101-117.
121. Sewing A, Wiseman B, Lloyd AC, Land H. 1997. High-intensity Raf signal causes cell cycle arrest mediated by p21Cip1. Mol Cell Biol 17:5588-5597.
122. Shilo BZ. 2003. Signaling by the Drosophila epidermal growth factor receptor pathway during development. Exp Cell Res 284:140-149.
123. Simon MA. 2000. Receptor tyrosine kinases: specific outcomes from general signals. Cell 103:13-15.
124. Simon MA, Bowtell DD, Dodson GS, Laverty TR, Rubin GM. 1991. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67:701-716.
125. Simon MA, Dodson GS, Rubin GM. 1993. An SH3-SH2-SH3 protein is required for p21Ras1 activation and binds to sevenless and Sos proteins in vitro. Cell 73:169-177.
126. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, King F, Roberts T, Ratnofsky S, Lechleider RJ, et al. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778.
127. Sprenger F, Nusslein-Volhard C. 1992. Torso receptor activity is regulated by a diffusible ligand produced at the extracelular terminal regions of the Drosophila egg. Cell 71:987-1001.
128. Sprenger F, Stevens LM, Nusslein-Volhard C. 1989. The Drosophila gene torso encodes a putative receptor tyrosine kinase. Nature 338:478-483.
129. Sprenger F, Trosclair MM, Morrison DK. 1993. Biochemical analysis of torso and D-raf during Drosophila embryogenesis: implications for terminal signal transduction. Mol Cell Biol 13:1163-1172.
130. St. Johnston D, Nusslein-Volhard C. 1992. The origin of pattern and polarity in the Drosophila embryo. Cell 68:201-219.
131. Starz-Gaiano M, Lehmann R. 2001. Moving towards the next generation. Mech Dev 105:5-18.
132. Steingrimsson E, Pignoni F, Liaw GJ, Lengyel JA. 1991. Dual role of the Drosophila pattern gene tailless in embryonic termini. Science 254:418-421.
133. Stevens LM, Frohnhofer HG, Klingler M, Nusslein-Volhard C. 1990. Localized requirement for torso-like expression in follicle cells for development of terminal anlagen of the Drosophila embryo. Nature 346:660-663.
134. Stevens LM, Beuchle D, Jurcsak J, Tong X, Stein D. 2003. The Drosophila embryonic patterning determinant torsolike is a component of the eggshell. Curr Biol 13:1058-1063.
135. Stokoe D, Macdonald SG, Cadwallader K, Symons M, Hancock JF. 1994. Activation of Raf as a result of recruitment to the plasma membrane [see comments] [published erratum appears in Science 1994;266:1792-1793]. Science 264:1463-1467.
136. Stokoe D, Macdonald SG, Cadwallader K, Symons M, Hancock JF. 1994. Activation of Raf as a result of recruitment to the plasma membrane [see comments] [published erratum appears in Science 1994;266:1792-1793]. Science 264:1463-1467.
137. Strecker TR, Kongsuwan K, Lengyel JA, Merriam JR. 1986. The zygotic mutant tailless affects the anterior and posterior ectodermal regions of the Drosophila embryo. Dev Biol 113:64-76.
138. Strecker TR, Halsell SR, Fisher WW, Lipshitz HD. 1989. Reciprocal effects of hyper- and hypoactivity mutations in the Drosophila pattern gene torso. Science 243:1062-1066.
139. Szabad J, Erdelyi M, Hoffmann G, Szidonya J, Wright TR. 1989. Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. II. Mutations on the second chromosome. Genetics 122:823-835.
140. Tallquist M, Kazlauskas A. 2004. PDGF signaling in cells and mice. Cytokine Growth Factor Rev 15:205-213.
141. Tallquist MD, Klinghoffer RA, Heuchel R, Mueting-Nelsen PF, Corrin PD, Heldin CH, Johnson RJ, Soriano P. 2000. Retention of PDGFR-beta function in mice in the absence of phosphatidylinositol 3′-kinase and phospholipase Cgamma signaling pathways. Genes Dev 14:3179-3190.
142. Tan PB, Kim SK. 1999. Signaling specificity: the RTK/RAS/MAP kinase pathway in metazoans. Trends Genet 15:145-149.
143. Tang TL, Freeman RM Jr, O'Reilly AM, Neel BG, Sokol SY. 1995. The SH2-containing protein-tyrosine phosphatase SH-PTP2 is required upstream of MAP kinase for early Xenopus development. Cell 80:473-483.
144. Themen M, Chang HC, Solomon NM, Karim FD, Wassarman DA, Rubin GM. 1995. KSR, a novel protein kinase required for RAS signal transduction. Cell 83:879-888.
145. Therrien M, Wong AM, Rubin GM. 1998. CNK, a RAF-binding multidomain protein required for RAS signaling. Cell 95:343-353.
146. Therrien M, Morrison DK, Wong AM, Rubin GM. 2000. A genetic screen for modifiers of a kinase suppressor of Ras-dependent rough eye phenotype in Drosophila. Genetics 156:1231-1242.
147. Tsuda L, Inoue YH, Yoo MA, Mizuno M, Hata M, Lim YM, Adachi-Yamada T, Ryo H, Masamune Y, Nishida Y. 1993. A protein kinase similar to MAP kinase activator acts downstream of the raf kinase in Drosophila. Cell 72:407-414.
148. van der Geer P, Hunter T, Lindberg RA. 1994. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 10:251-337.
149. van der Geer P, Wiley S, Lai VK, Olivier JP, Gish GD, Stephens R, Kaplan D, Shoelson S, Pawson T. 1995. A conserved amino-terminal Shc domain binds to phosphotyrosine motifs in activated receptors and phosphopeptides. Curr Biol 5:404-412.
150. van der Straten A, Rommel C, Dickson B, Hafen E. 1997. The heat shock protein 83 (Hsp83) is required for Raf-mediated signalling in Drosophila. EMBO J 16:1961-1969.
151. Wassarman DA, Therrien M, Rubin GM. 1995. The Ras signaling pathway in Drosophila. Curr Opin Genet Dev 5:44-50.
152. Weigel D, Jurgens G, Klingler M, Jackle H. 1990. Two gap genes mediate maternal terminal pattern information in Drosophila. Science 248:495-498.
153. Williams H, Brenner S, Venkatesh B. 2002. Identification and analysis of additional copies of the platelet-derived growth factor receptor and colony stimulating factor 1 receptor genes in fugu. Gene 295:255-264.
154. Wolpert L. 1996. One hundred years of positional information. Trends Genet 12:359-364.
155. Woods D, Parry D, Cherwinski H, Bosch E, Lees E, McMahon M. 1997. Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol Cell Biol 17:5598-5611.
156. Wylie C. 1999. Germ cells. Cell 96:165-174.
157. Wylie C. 2000. Germ cells. Curr Opin Genet Dev 10:410-413.
158. Xu C, Kauffmann RC, Zhang J, Kladny S, Carthew RW. 2000. Overlapping activators and repressers delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell 103:87-97.
159. Zhang SQ, Yang W, Kontaridis MI, Bivona TG, Wen G, Araki T, Luo J, Thompson JA, Schraven BL, Philips MR, Neel BG. 2004. Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol Cell 13:341-355.