Targeted Expression of the Class II Phosphoinositide 3-Kinase in Drosophila melanogaster Reveals Lipid Kinase-Dependent Effects on Patterning and Interactions with Receptor Signaling Pathways

REFERENCES

• Akam, M. E., Roberts D. B., Richards G. P., and Ashburner M.. 1978. Drosophila: the genetics of two major larval proteins. Cell 13:215–225.
   PubMed Web of Science ®Google Scholar
• Arcaro, A., Volinia S., Zvelebil M. J., Stein R., Watton S. J., Layton M. J., Gout I., Ahmadi K., Downward J., and Waterfield M. D.. 1998. Human phosphoinositide 3-kinase C2_β—the role of calcium and the C2 domain in enzyme activity. J. Biol. Chem. 273:33082–33090.
   PubMed Web of Science ®Google Scholar
• Arcaro, A., Zvelebil M. J., Wallasch C., Ullrich A., Waterfield M. D., and Domin J.. 2000. Class II phosphoinositide 3-kinases are downstream targets of activated polypeptide growth factor receptors. Mol. Cell. Biol. 20:3817–3830.
   PubMed Web of Science ®Google Scholar
• Arcaro, A., Khanzada U. K., Vanhaesebroeck B., Tetley T. D., Waterfield M. D., and Seckl M. J.. 2002. Two distinct phosphoinositide 3-kinases mediate polypeptide growth factor-stimulated PKB activation. EMBO J. 21:5097–5108.
   PubMed Web of Science ®Google Scholar
• Artavanis-Tsakonas, S., Rand M. D., and Lake R. J.. 1999. Notch signalling: cell fate control and signal integration in development. Science 284:770–776.
   PubMed Web of Science ®Google Scholar
• Baker, N. E., and Rubin G. M.. 1992. Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division and cell death in eye imaginal discs. Dev. Biol. 150:381–396.
   PubMedGoogle Scholar
• Basler, K., Christen B., and Hafen E.. 1991. Ligand-independent activation of the Sevenless receptor tyrosine kinase changes the fate of cells in the developing Drosophila eye. Cell 64:1069–1081.
   PubMedGoogle Scholar
• Berset, T., Hoier E. F., Battu G., Canevascini S., and Hajnal A.. 2001. Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science 291:1055–1058.
   PubMed Web of Science ®Google Scholar
• Brand, A. H., and Perrimon N.. 1993. Targetted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415.
   PubMed Web of Science ®Google Scholar
• Bray, S. 1998. Notch signalling in Drosophila: three ways to use a pathway. Semin. Cell Dev. Biol. 9:591–597.
   PubMed Web of Science ®Google Scholar
• Brown, R., Ho L., Weber-Hall S., Shipley J. M., and Fry M. J.. 1997. Identification and cDNA cloning of a novel mammalian C2 domain-containing phosphoinositide 3-kinase, HsC2-PI3K. Biochem. Biophys. Res. Commun. 233:537–544.
   PubMedGoogle Scholar
• Brown, R., Domin J., Arcaro A., Waterfield M. D., and Shepherd P. R.. 1999. Insulin activates the α isoform of class II phosphoinositide 3-kinase. J. Biol. Chem. 274:14529–14532.
   PubMed Web of Science ®Google Scholar
• Capdevila, J., and Guerrero I.. 1994. Targetted expression of the signalling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13:4459–4468.
   PubMedGoogle Scholar
• Casci, T., and Freeman M.. 1999. Control of EGF receptor signalling: lessons from fruitflies. Cancer Metast. Rev. 18:181–201.
   PubMedGoogle Scholar
• Clifford, R. J., and Shübach T.. 1989. Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homologue of the vertebrate EGF receptor gene. Genetics 123:771–787.
   PubMedGoogle Scholar
• Cohen, S. M. 1993. Imaginal disc development, p. 747–842. In Bate M. and Martinez-Arias A. (ed.), The development of Drosophila melanogaster, vol. 2. Cold Spring Harbor Laboratory Press, New York, N.Y.
   Google Scholar
• Crosby, M. A., and Meyerowitz E. M.. 1986. Lethal mutations flanking the 68C glue gene cluster on chromosome 3 of Drosophila melanogaster. Genetics 112:785–802.
   PubMedGoogle Scholar
• de Celis, J. F., Bray S., and Garcia-Bellido A.. 1997. Notch signalling regulates Veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing. Development 124:1919–1928.
   PubMedGoogle Scholar
• Diaz-Benjumea, F. J., and Garcia-Bellido A.. 1990. Behaviour of cells mutant for an EGF receptor homologue of Drosophila in genetic mosaics. Proc. R. Soc. London Biol. 242:36–44.
   Google Scholar
• Diaz-Benjumea, F. J., and Hafen E.. 1994. The sevenless signalling cassette mediates Drosophila EGF receptor function during epidermal development. Development 120:569–578.
   PubMedGoogle Scholar
• Domin, J., Pages F., Volinia S., Rittenhouse S. E., Zvelebil M. J., Stein R. C., and Waterfield M. D.. 1997. Cloning of a human phosphoinositide 3-kinase with a C2 domain that displays reduced sensitivity to the inhibitor wortmannin. Biochem. J. 326:139–147.
   PubMed Web of Science ®Google Scholar
• Domínguez, M., Wasserman J. D., and Freeman M.. 1998. Multiple functions of the EGF receptor in Drosophila eye development. Curr. Biol. 8:1039–1048.
   PubMedGoogle Scholar
• Dove, S. P., Cooke F. T., Douglas M. R., Sayers L. G., Parker P. J., and Michell R. H.. 1997. Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature 390:187–192.
   PubMed Web of Science ®Google Scholar
• Evan, G. I., Lewis G. K., Ramsay G., and Bishop G. M.. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610–3616.
   PubMed Web of Science ®Google Scholar
• Feldmann, P., Eischer E. N., Leevers S. J., Hafen E., and Hughes D. A.. 1999. Control of growth and differentiation by Drosophila RasGAP, a homolog of p120 Ras-GTPase-activating protein. Mol. Cell. Biol. 19:1928–1937.
   PubMedGoogle Scholar
• Feller, S. M., Wecklein H., Lewitzky M., Kibler E., and Raabe T.. 2002. SH3 domain-mediated binding of the Drk protein to Dos is an important step in signalling of Drosophila receptor tyrosine kinases. Mech. Dev. 116:129–139.
   PubMedGoogle Scholar
• Guan, K. L., and Dixon J. E.. 1991. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192:262–267.
   PubMed Web of Science ®Google Scholar
• Guichard, A., Bergeret E., and Griffin-Shea R.. 1997. Overexpression of Rn RacGAP in Drosophila melanogaster deregulates cytoskeletal organisation in cellular embryos and induces discrete imaginal phenotypes. Mech. Dev. 61:49–62.
   PubMedGoogle Scholar
• Herman, P. K., and Emr S. D.. 1990. Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:6742–6754.
   PubMedGoogle Scholar
• Hinz, U., Giebel B., and Campos-Ortega J. A.. 1994. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76:77–87.
   PubMedGoogle Scholar
• Ho, S. N., Hunt H. D., Horton R. M., Pullen J. K., and Pease L. R.. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51–59.
   PubMed Web of Science ®Google Scholar
• Hoogwerf, A. M., Akam M., and Roberts D.. 1988. A genetic analysis of the rose-gespleten region (68C8-69B5) of Drosophila melanogaster. Genetics 118:665–670.
   PubMedGoogle Scholar
• Hopper, N. A., Lee J., and Sternberg P. W.. 2000. Ark-1 inhibits EGFR signalling in C. elegans. Mol. Cell 6:65–75.
   PubMedGoogle Scholar
• Johnson, R. L., Grenier J. K., and Scott M. P.. 1995. Patched overexpression alters wing disc size and pattern: transcriptional and post-transcriptonal effects on Hedgehog targets. Development 121:4161–4170.
   PubMedGoogle Scholar
• Kay, B. R., Williamson M. P., and Sudol M.. 2000. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14:231–241.
   PubMed Web of Science ®Google Scholar
• Kispert, A., Herrmann B. G., Leptin M., and Reuter R.. 1994. Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium, and Locusta. Genes Dev. 8:2137–2150.
   PubMed Web of Science ®Google Scholar
• Lee, J. R., Urban S., Garvey C. F., and Freeman M.. 2001. Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107:161–171.
   PubMedGoogle Scholar
• Leevers, S. J., Weinkove D., MacDougall L. K., Hafen E., and Waterfield M. D.. 1996. The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J. 15:6584–6594.
   PubMed Web of Science ®Google Scholar
• Lesokhin, A. M., Yu S. Y., Katz J., and Baker N. E.. 1999. Several levels of EGF receptor signalling during photoreceptor specification in wild-type, Ellipse, and null mutant Drosophila. Dev. Biol. 205:129–144.
   PubMedGoogle Scholar
• Linassier, C., MacDougall L. K., Domin J., and Waterfield M. D.. 1997. Molecular cloning and biochemical characterisation of a Drosophila PI-specific phosphoinositide 3-kinase. Biochem. J. 321:849–856.
   PubMedGoogle Scholar
• MacDougall, L. K., Domin J., and Waterfield M. D.. 1995. A family of phosphoinositide 3-kinases in Drosophila identifies a new mediator of intracellular signalling. Curr. Biol. 5:1404–1415.
   PubMed Web of Science ®Google Scholar
• Martín-Blanco, E., Roch F., Noll E., Baonza A., Duffy J. B., and Perrimon N.. 1999. A temporal switch in DER signalling controls the specification and differentiation of veins and interveins in the Drosophila wing. Development 126:5739–5747.
   PubMedGoogle Scholar
• Milan, M., Diaz-Benjumea F. J., and Cohen S. M.. 1998. Beadex encodes an LMO protein that regulates Apterous LIM-homeodomain activity in Drosophila wing development: a model for LMO oncogene function. Genes Dev. 12:2912–2920.
   PubMed Web of Science ®Google Scholar
• Misawa, H., Ohtsubo M., Copeland N., Gilbert D., Jenkins N., and Yoshimura A.. 1998. Cloning and characterisation of a novel class II phosphoinositide 3-kinase containing a C2 domain. Biochem. Biophys. Res. Commun. 244:531–539.
   PubMed Web of Science ®Google Scholar
• Molz, L., Chen Y., and Williams L. T.. 1996. Cpk is a novel class of Drosophila PtdIns 3-kinase containing a C2 domain. J. Biol. Chem. 271:13892–13899.
   PubMedGoogle Scholar
• Moscatello, D. K., Holgado-Madruga M., Emlet D. R., Montgomery R. B., and Wong A. J.. 1998. Constitutive activation of phosphatidylinositol 3-kinase by a naturally occurring mutant epidermal growth factor receptor. J. Biol. Chem. 273:200–206.
   PubMed Web of Science ®Google Scholar
• Olivier J.-P., Raabe T., Henkemeyer M., Dickson B., Mbamalu G., Margolis B., Schlessinger J., Hafen E., and 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.
   PubMed Web of Science ®Google Scholar
• Ono, F., Nakagawa T., Saito S., Owada Y., Sakagami H., Goto K., Suzuki M., Matsuno S., and Kondo H.. 1998. A novel class II phosphoinositide 3-kinase predominantly expressed in liver and its enhanced expression during liver regeneration. J. Biol. Chem. 273:7731–7736.
   PubMedGoogle Scholar
• Ponting, C. P. 1996. Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains? Protein Sci. 5:2353–2357.
   PubMed Web of Science ®Google Scholar
• Price, J. V., Savenye E. D., Lum D., and Breitkreutz A.. 1997. Dominant enhancers of Egfr in Drosophila melanogaster: genetic links between the Notch and EGFR signalling pathways. Genetics 147:1139–1153.
   PubMed Web of Science ®Google Scholar
• Raabe, T., Olivier J. P., Dickson B., Liu X., Gish G. D., Pawson T., and Hafen E.. 1995. Biochemical and genetic analysis of the Drk SH2/SH3 adaptor protein of Drosophila. EMBO J. 14:2509–2518.
   PubMedGoogle Scholar
• Rebay, I., Fehon R. G., and Artavanis-Tsakonas S.. 1993. Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74:319–329.
   PubMed Web of Science ®Google Scholar
• Rebay, I. 2002. Keeping the receptor tyrosine kinase signalling pathway in check: lessons from Drosophila. Dev. Biol. 251:1–17.
   PubMedGoogle Scholar
• Rohrbaugh, M., Ramos E., Nguyen D., Price M., Wen Y., and Lai Z. C.. 2002. Notch activation of yan expression is antagonized by RTK/pointed signaling in the Drosophila eye. Curr. Biol. 12:576–581.
   PubMedGoogle Scholar
• Schnepp, B., Donaldon T., Grumbling G., Ostrowski S., Schweitzer R., Shilo B.-Z., and Simcox A.. 1998. EGF domain swap converts a Drosophila EGF receptor activator into an inhibitor. Genes Dev. 12:908–913.
   PubMedGoogle Scholar
• Schweitzer, R., and Shilo B.-Z.. 1997. A thousand and one roles for the Drosophila EGF receptor. Trends Genet. 13:191–196.
   PubMedGoogle Scholar
• Seto, E. S., Bellen H. J., and Lloyd T. E.. 2002. When cell biology meets development: endocytic regulation of signalling pathways. Genes Dev. 16:1314–1336.
   PubMedGoogle Scholar
• Seugnet, L., Simpson P., and Haenlin M.. 1997. Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev. Biol. 192:585–598.
   PubMedGoogle Scholar
• Shao, X., Li C., Fernandez I., Zhang X., Südhof T. C., and Rizo J.. 1997. Synaptotagmin-syntaxin interaction: the C2 domain as a Ca2+-dependent electrostatic switch. Neuron 18:133–142.
   PubMedGoogle Scholar
• Simon, M. A., Bowtell D. D., Dodson G. S., Laverty T. R., and Rubin G. M.. 1991. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67:701–716.
   PubMedGoogle Scholar
• Simon, M. A., Dodson G. S., and Rubin G. M.. 1993. An SH3-SH2-SH3 protein is required for p21Ras1 activation and binds to sevenless and Sos proteins in vitro. Cell 73:169–177.
   PubMed Web of Science ®Google Scholar
• Simpson, P., Woehl R., and Usui K.. 1999. The development and evolution of bristle patterns in Diptera. Development 126:1349–1364.
   PubMedGoogle Scholar
• Soltoff, S. P., Carraway S. A., Prigent S. A., Gullick W. G., and Cantley L. C.. 1994. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol. Cell. Biol. 14:3550–3558.
   PubMed Web of Science ®Google Scholar
• Stephens, L. R., Eguinoa A., Erdjument-Bromage H., Lui M., Cooke F., Coadwell J., Smrcka A. S., Thelen M., Cadwallader K., Tempst P., and Hawkins P. T.. 1997. The Gβγ sensitivity of a PI3K is dependent upon a tightly associated adaptor, p101. Cell 89:105–114.
   PubMed Web of Science ®Google Scholar
• Sturtevant, M. A., Roark M., and Bier E.. 1993. The Drosophila Rhomboid gene mediates the localised formation of wing veins and interacts genetically with components of the EGF-R signalling pathway. Genes Dev. 7:961–973.
   PubMedGoogle Scholar
• Tsuda, L., Nagaraj R., Zipursky S., and Banerjee U.. 2002. An EGFR/Ebi/Sno pathway promotes delta expression by inactivating Su(H)/SMRTER repression during inductive Notch signaling. Cell 110:625–637.
   PubMed Web of Science ®Google Scholar
• Turner, S. J., Domin J., Waterfield M. D., Ward S. G., and Westwick J.. 1998. The CC chemokine monocyte chemotactic peptide-1 activates both the class I p85/p110 phosphatidylinositol 3-kinase and the class II PI3K-C2α. J. Biol. Chem. 273:25987–25995.
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck, B., Leevers S. J., Ahmadi K., Timms J., Katso R., Driscoll P. C., Woscholski R., Parker P. J., and Waterfield M. D.. 2001. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70:535–602.
   PubMed Web of Science ®Google Scholar
• Virbasius, J. V., Guilherme A., and Czech M. P.. 1996. Mouse p170 is a novel phosphatidylinositol 3-kinase containing a C2 domain. J. Biol. Chem. 271:13304–13307.
   PubMedGoogle Scholar
• Volinia, S., Dhand R., Vanhaesebroeck B., MacDougall L. K., Stein R., Zvelebil M. J., Domin J., Panaretou C., and Waterfield M. D.. 1995. A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system. EMBO J. 14:3339–3348.
   PubMed Web of Science ®Google Scholar
• Walker, E. H., Perisic O., Ried C., Stephens L., and Williams R. L.. 1999. Structural insights into phosphoinositide 3-kinase signalling. Nature 402:313–320.
   PubMed Web of Science ®Google Scholar
• Waterman, H., Katz M., Rubin C., Shtiegman K., Lavi S., Elson A., Jovin T., and Yarden Y.. 2002. A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signalling. EMBO J. 21:303–313.
   PubMed Web of Science ®Google Scholar
• Weinkove, D., Neufeld T. P., Twardzik T., Waterfield M. D., and Leevers S. J.. 1999. Regulation of imaginal disc cell size, cell number and organ size by Drosophila class IA phosphoinositide 3-kinase and its adaptor. Curr. Biol. 9:1019–1029.
   PubMed Web of Science ®Google Scholar
• Wheeler, M., and Domin J.. 2001. Recruitment of the class II phosphoinositide 3-kinase C2β to the epidermal growth factor receptor: role of Grb2. Mol. Cell. Biol. 21:6660–6667.
   PubMedGoogle Scholar
• Zhang, J., Banfic H., Straforini F., Tosi L., Volinia S., and Rittenhouse S.. 1998. A type II phosphoinositide 3-kinase is stimulated via activated integrin in platelets. A source of phosphatidylinositol 3-phosphate. J. Biol. Chem. 273:14081–14084.
   PubMed Web of Science ®Google Scholar