Binding of Ras to Phosphoinositide 3-Kinase p110α Is Required for Ras- Driven Tumorigenesis in Mice

Cell

Volumn 129, Issue 5, 2007, Pages 957-968

  Gupta, Surbhi ^a   Ramjaun, Antoine R ^a   Haiko, Paula ^b   Wang, Yihua ^a   Warne, Patricia H ^a   Nicke, Barbara ^a   Nye, Emma ^a   Stamp, Gordon ^a   Alitalo, Kari ^b   Downward, Julian ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

CELLBIO; HUMDISEASE; SIGNALING

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P110; PROTEIN P110ALPHA; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CHYLOUS ASCITES; CONTROLLED STUDY; ENZYME ACTIVATION; GENE MUTATION; MOUSE; NONHUMAN; ONCOGENE K RAS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; VASCULARIZATION;

MUS;

EID: 34249026448     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.03.051     Document Type: Article

References (43)

1. Alessi D.R., Andjelkovic M., Caudwell B., Cron P., Morrice N., Cohen P., and Hemmings B.A. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15 (1996) 6541-6551
2. Bai Y., Edamatsu H., Maeda S., Saito H., Suzuki N., Satoh T., and Kataoka T. Crucial role of phospholipase Cepsilon in chemical carcinogen-induced skin tumor development. Cancer Res. 64 (2004) 8808-8810
3. Collado M., Gil J., Efeyan A., Guerra C., Schuhmacher A.J., Barradas M., Benguria A., Zaballos A., Flores J.M., Barbacid M., et al. Tumour biology: senescence in premalignant tumours. Nature 436 (2005) 642
4. Cully M., You H., Levine A.J., and Mak T.W. Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat. Rev. Cancer 6 (2006) 184-192
5. Dajee M., Tarutani M., Deng H., Cai T., and Khavari P.A. Epidermal Ras blockade demonstrates spatially localized Ras promotion of proliferation and inhibition of differentiation. Oncogene 21 (2002) 1527-1538
6. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3 (2003) 11-22
7. Dumont D.J., Jussila L., Taipale J., Lymboussaki A., Mustonen T., Pajusola K., Breitman M., and Alitalo K. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282 (1998) 946-949
8. Foukas L.C., Claret M., Pearce W., Okkenhaug K., Meek S., Peskett E., Sancho S., Smith A.J., Withers D.J., and Vanhaesebroeck B. Critical role for p110alpha phosphoinositide-3-OH kinase in growth and metabolic regulation. Nature 441 (2006) 366-370
9. Fruman D.A., Mauvais-Jarvis F., Pollard D.A., Yballe C.M., Brazil D., Bronson R.T., Kahn C.R., and Cantley L.C. Hypoglycaemia, liver necrosis and perinatal death in mice lacking all isoforms of phosphoinositide 3-kinase p85 alpha. Nat. Genet. 26 (2000) 379-382
10. Gale N.W., Thurston G., Hackett S.F., Renard R., Wang Q., McClain J., Martin C., Witte C., Witte M.H., Jackson D., et al. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev. Cell 3 (2002) 411-423
11. Gonzalez-Garcia A., Pritchard C.A., Paterson H.F., Mavria G., Stamp G., and Marshall C.J. RalGDS is required for tumor formation in a model of skin carcinogenesis. Cancer Cell 7 (2005) 219-226
12. Johnson L., Mercer K., Greenbaum D., Bronson R.T., Crowley D., Tuveson D.A., and Jacks T. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410 (2001) 1111-1116
13. Joukov V., Pajusola K., Kaipainen A., Chilov D., Lahtinen I., Kukk E., Saksela O., Kalkkinen N., and Alitalo K. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J. 15 (1996) 1751
14. Kaipainen A., Korhonen J., Mustonen T., van Hinsbergh V.W., Fang G.H., Dumont D., Breitman M., and Alitalo K. Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc. Natl. Acad. Sci. USA 92 (1995) 3566-3570
15. Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., Jeltsch M., Jackson D.G., Talikka M., Rauvala H., et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 5 (2004) 74-80
16. Kazlauskas A., and Cooper J.A. Autophosphorylation of the PDGF receptor in the kinase insert region regulates interactions with cell proteins. Cell 58 (1989) 1121-1133
17. Makinen T., Jussila L., Veikkola T., Karpanen T., Kettunen M.I., Pulkkanen K.J., Kauppinen R., Jackson D.G., Kubo H., Nishikawa S., et al. Inhibition of lymphangiogenesis with resulting lymphadema in transgenic mice expressing soluble VEGF receptor-3. Nat. Med. 7 (2001) 199-205
18. Makinen T., Veikkola T., Mustjoki S., Karpanen T., Catimel B., Nice E.C., Wise L., Mercer A., Kowalski H., Kerjaschki D., et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 20 (2001) 4762-4773
19. Malliri A., van der Kammen R.A., Clark K., van der Valk M., Michiels F., and Collard J.G. Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours. Nature 417 (2002) 867-871
20. Mattoon D.R., Lamothe B., Lax I., and Schlessinger J. The docking protein Gab1 is the primary mediator of EGF-stimulated activation of the PI-3K/Akt cell survival pathway. BMC Biol. 2 (2004) 24
21. Nakahara R., Yokose T., Nagai K., Nishiwaki Y., and Ochiai A. Atypical adenomatous hyperplasia of the lung: a clinicopathological study of 118 cases including cases with multiple atypical adenomatous hyperplasia. Thorax 56 (2001) 302-305
22. Ong S.H., Hadari Y.R., Gotoh N., Guy G.R., Schlessinger J., and Lax I. Stimulation of phosphatidylinositol 3-kinase by fibroblast growth factor receptors is mediated by coordinated recruitment of multiple docking proteins. Proc. Natl. Acad. Sci. USA 98 (2001) 6074-6079
23. Orme M.H., Alrubaie S., Bradley G.L., Walker C.D., and Leevers S.J. Input from Ras is required for maximal PI(3)K signalling in Drosophila. Nat. Cell Biol. 8 (2006) 1298-1302
24. Pacold M.E., Suire S., Perisic O., Lara-Gonzalez S., Davis C.T., Walker E.H., Hawkins P.T., Stephens L., Eccleston J.F., and Williams R.L. Crystal structure and functional analysis of Ras binding to its effector phosphoinositide 3-kinase gamma. Cell 103 (2000) 931-943
25. Press O.W., Press N.O., and Kaufman S.D. Evaluation and management of chylous ascites. Ann. Intern. Med. 96 (1982) 358-364
26. Prober D.A., and Edgar B.A. Interactions between Ras1, dMyc, and dPI3K signaling in the developing Drosophila wing. Genes Dev. 16 (2002) 2286-2299
27. Quintanilla M., Brown K., Ramsden M., and Balmain A. Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 322 (1986) 78-80
28. Repasky G.A., Chenette E.J., and Der C.J. Renewing the conspiracy theory debate: does Raf function alone to mediate Ras oncogenesis?. Trends Cell Biol. 14 (2004) 639-647
29. Rodriguez-Viciana P., Warne P.H., Dhand R., Vanhaesebroeck B., Gout I., Fry M.J., Waterfield M.D., and Downward J. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370 (1994) 527-532
30. Rodriguez-Viciana P., Warne P.H., Vanhaesebroeck B., Waterfield M.D., and Downward J. Activation of phosphoinositide 3-kinase by interaction with Ras and by point mutation. EMBO J. 15 (1996) 2442-2451
31. Rodriguez-Viciana P., Warne P.H., Khwaja A., Marte B.M., Pappin D., Das P., Waterfield M.D., Ridley A., and Downward J. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell 89 (1997) 457-467
32. Saharinen P., Tammela T., Karkkainen M.J., and Alitalo K. Lymphatic vasculature: development, molecular regulation and role in tumor metastasis and inflammation. Trends Immunol. 25 (2004) 387-395
33. Schulze A., Lehmann K., Jefferies H.B., McMahon M., and Downward J. Analysis of the transcriptional program induced by Raf in epithelial cells. Genes Dev. 15 (2001) 981-994
34. Soltoff S.P., Carraway III K.L., Prigent S.A., Gullick W.G., and Cantley L.C. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol. Cell. Biol. 14 (1994) 3550-3558
35. Suire S., Hawkins P., and Stephens L. Activation of phosphoinositide 3-kinase gamma by Ras. Curr. Biol. 12 (2002) 1068-1075
36. Suire S., Condliffe A.M., Ferguson G.J., Ellson C.D., Guillou H., Davidson K., Welch H., Coadwell J., Turner M., Chilvers E.R., et al. Gbetagammas and the Ras binding domain of p110gamma are both important regulators of PI(3)Kgamma signalling in neutrophils. Nat. Cell Biol. 8 (2006) 1303-1309
37. van Weering D.H., de Rooij J., Marte B., Downward J., Bos J.L., and Burgering B.M. Protein kinase B activation and lamellipodium formation are independent phosphoinositide 3-kinase-mediated events differentially regulated by endogenous Ras. Mol. Cell. Biol. 18 (1998) 1802-1811
38. Vanhaesebroeck B., and Waterfield M.D. Signaling by distinct classes of phosphoinositide 3-kinases. Exp. Cell Res. 253 (1999) 239-254
39. Vanhaesebroeck B., Ali K., Bilancio A., Geering B., and Foukas L.C. Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem. Sci. 30 (2005) 194-204
40. Weir B., Zhao X., and Meyerson M. Somatic alterations in the human cancer genome. Cancer Cell 6 (2004) 433-438
41. Wellbrock C., Karasarides M., and Marais R. The RAF proteins take centre stage. Nat. Rev. Mol. Cell Biol. 5 (2004) 875-885
42. Whitman M., Kaplan D.R., Schaffhausen B., Cantley L., and Roberts T.M. Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315 (1985) 239-242
43. Zhao J.J., Cheng H., Jia S., Wang L., Gjoerup O.V., Mikami A., and Roberts T.M. The p110alpha isoform of PI3K is essential for proper growth factor signaling and oncogenic transformation. Proc. Natl. Acad. Sci. USA 103 (2006) 16296-16300