Phosphatidylinositol 4-kinases, phosphatidylinositol 4-phosphate and cancer

Cancer Letters

Volumn 325, Issue 2, 2012, Pages 125-131

  Waugh, Mark G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

4 Kinase; GPCR; PH; Phosphatidylinositol; Phospholipid; PI; PI4P; TGN

Indexed keywords

ELONGATION FACTOR 1ALPHA; EPIDERMAL GROWTH FACTOR RECEPTOR; GEMCITABINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE ALPHA; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE BETA; PHOSPHATIDYLINOSITOL KINASE; PHOSPHOLIPASE C; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ACTIN FILAMENT; APOPTOSIS; CANCER RESISTANCE; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CRYSTAL STRUCTURE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; HIGH THROUGHPUT SCREENING; HUMAN; LIVER CELL CARCINOMA; NEOPLASM; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SHORT SURVEY; SIGNAL TRANSDUCTION;

EID: 84865631981     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.06.009     Document Type: Review

References (103)

1. Di Paolo G., De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006, 443:651-657.
2. De Matteis M.A., Di Campli A., Godi A. The role of the phosphoinositides at the Golgi complex. Biochim. Biophys. Acta 2005, 1744:396-405.
3. Yuan T.L., Cantley L.C. PI3K pathway alterations in cancer: variations on a theme. Oncogene 2008, 27:5497-5510.
4. Balla A., Balla T. Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 2006, 16:351-361.
5. Minogue S., Waugh M.G. The phosphatidylinositol 4-kinases: do not call it a comeback. Subcell Biochem. 2012, 58:1-24.
6. Balla A., Kim Y.J., Varnai P., Szentpetery Z., Knight Z., Shokat K.M., et al. Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase III{alpha}. Mol. Biol. Cell 2008, 19:711-721.
7. Szentpetery Z., Varnai P., Balla T. Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc. Natl. Acad. Sci. USA 2010, 107:8225-8230.
8. Wong K.K., Engelman J.A., Cantley L.C. Targeting the PI3K signaling pathway in cancer. Curr. Opin. Genet. Dev. 2010, 20:87-90.
9. Walker D.H., Pike L.J. Phosphatidylinositol kinase is activated in membranes derived from cells treated with epidermal growth factor. Proc. Natl. Acad. Sci. USA 1987, 84:7513-7517.
10. Walker D.H., Dougherty N., Pike L.J. Purification and characterization of a phosphatidylinositol kinase from A431 cells. Biochemistry (Mosc) 1988, 27:6504-6511.
11. Kauffmann-Zeh A., Thomas G.M., Ball A., Prosser S., Cunningham E., Cockcroft S., et al. Requirement for phosphatidylinositol transfer protein in epidermal growth factor signaling. Science 1995, 268:1188-1190.
12. Kauffmann-Zeh A., Klinger R., Endemann G., Waterfield M.D., Wetzker R., Hsuan J.J. Regulation of human type II phosphatidylinositol kinase activity by epidermal growth factor-dependent phosphorylation and receptor association. J. Biol. Chem. 1994, 269:31243-31251.
13. Cochet C., Filhol O., Payrastre B., Hunter T., Gill G.N. Interaction between the epidermal growth factor receptor and phosphoinositide kinases. J. Biol. Chem. 1991, 266:637-644.
14. Li J., Lu Y., Zhang J., Kang H., Qin Z., Chen C. PI4KIIalpha is a novel regulator of tumor growth by its action on angiogenesis and HIF-1alpha regulation. Oncogene 2010, 29:2550-2559.
15. Roesli C., Borgia B., Schliemann C., Gunthert M., Wunderli-Allenspach H., Giavazzi R., et al. Comparative analysis of the membrane proteome of closely related metastatic and nonmetastatic tumor cells. Cancer Res. 2009, 69:5406-5414.
16. Chuang Y.Y., Tran N.L., Rusk N., Nakada M., Berens M.E., Symons M. Role of synaptojanin 2 in glioma cell migration and invasion. Cancer Res. 2004, 64:8271-8275.
17. Chang-Ileto B., Frere S.G., Chan R.B., Voronov S.V., Roux A., Di Paolo G. Synaptojanin 1-mediated PI(4,5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Dev. Cell 2011, 20:206-218.
18. Chu K., Minogue S., Hsuan J., Waugh M. Differential effects of the phosphatidylinositol 4-kinases, PI4KIIalpha and PI4KIIIbeta, on Akt activation and apoptosis. Cell Death Dis. 2010, 1.
19. Craige B., Salazar G., Faundez V. Phosphatidylinositol-4-kinase type II alpha contains an AP-3 sorting motif and a kinase domain that are both required for endosome traffic. Mol. Biol. Cell 2008.
20. Wang Y.J., Wang J., Sun H.Q., Martinez M., Sun Y.X., Macia E., et al. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 2003, 114:299-310.
21. Simons J.P., Al-Shawi R., Minogue S., Waugh M.G., Wiedemann C., Evangelou S., et al. Loss of phosphatidylinositol 4-kinase 2alpha activity causes late onset degeneration of spinal cord axons. Proc. Natl. Acad. Sci. USA 2009, 106:11535-11539.
22. Hawkins P.T., Jackson T.R., Stephens L.R. Platelet-derived growth factor stimulates synthesis of PtdIns(3,4,5)P3 by activating a PtdIns(4,5)P2 3-OH kinase. Nature 1992, 358:157-159.
23. Jackson T.R., Stephens L.R., Hawkins P.T. Receptor specificity of growth factor-stimulated synthesis of 3-phosphorylated inositol lipids in Swiss 3T3 cells. J. Biol. Chem. 1992, 267:16627-16636.
24. Panaretou C., Tooze S.A. Regulation and recruitment of phosphatidylinositol 4-kinase on immature secretory granules is independent of ADP-ribosylation factor 1. Biochem. J. 2002, 363:289-295.
25. Banerji S., Ngo M., Lane C.F., Robinson C.A., Minogue S., Ridgway N.D. Oxysterol binding protein-dependent activation of sphingomyelin synthesis in the golgi apparatus requires phosphatidylinositol 4-kinase IIalpha. Mol. Biol. Cell 2010, 21:4141-4150.
26. Burgett A.W., Poulsen T.B., Wangkanont K., Anderson D.R., Kikuchi C., Shimada K., et al. Natural products reveal cancer cell dependence on oxysterol-binding proteins. Nat. Chem. Biol. 2011, 7:639-647.
27. Jiang P., Enomoto A., Jijiwa M., Kato T., Hasegawa T., Ishida M., et al. An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res. 2008, 68:1310-1318.
28. Weng L., Enomoto A., Ishida-Takagishi M., Asai N., Takahashi M. Girding for migratory cues: roles of the Akt substrate Girdin in cancer progression and angiogenesis. Cancer Sci. 2010, 101:836-842.
29. Ghosh P., Beas A.O., Bornheimer S.J., Garcia-Marcos M., Forry E.P., Johannson C., et al. A Gi-GIV molecular complex binds epidermal growth factor receptor and determines whether cells migrate or proliferate. Mol. Cell Biol. 2010.
30. Enomoto A., Murakami H., Asai N., Morone N., Watanabe T., Kawai K., et al. Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev. Cell 2005, 9:389-402.
31. Lin C., Ear J., Pavlova Y., Mittal Y., Kufareva I., Ghassemian M., et al. Tyrosine phosphorylation of the Galpha-interacting protein GIV promotes activation of phosphoinositide 3-kinase during cell migration. Sci. Sig. 2011, 4:ra64.
32. Roy A., Levine T.P. Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p. J. Biol. Chem. 2004, 279:44683-44689.
33. Hammond G.R., Schiavo G., Irvine R.F. Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns(4,5)P(2). Biochem. J. 2009, 422:23-35.
34. Waugh M.G., Minogue S., Blumenkrantz D., Anderson J.S., Hsuan J.J. Identification and characterization of differentially active pools of type IIalpha phosphatidylinositol 4-kinase activity in unstimulated A431 cells. Biochem. J. 2003, 376:497-503.
35. Minogue S., Chu K.M., Westover E.J., Covey D.F., Hsuan J.J., Waugh M.G. Relationship between phosphatidylinositol 4-phosphate synthesis, membrane organization, and lateral diffusion of PI4KIIalpha at the trans-Golgi network. J. Lipid Res. 2010, 51:2314-2324.
36. Waugh M.G., Minogue S., Anderson J.S., Balinger A., Blumenkrantz D., Calnan D.P., et al. Localization of a highly active pool of type II phosphatidylinositol 4-kinase in a p97/valosin-containing-protein-rich fraction of the endoplasmic reticulum. Biochem. J. 2003, 373:57-63.
37. Waugh M.G., Minogue S., Chotai D., Berditchevski F., Hsuan J.J. Lipid and peptide control of phosphatidylinositol 4-kinase IIalpha activity on Golgi-endosomal rafts. J. Biol. Chem. 2006, 281:3757-3763.
38. Waugh M.G., Chu K.M., Clayton E.L., Minogue S., Hsuan J.J. Detergent-free isolation and characterization of cholesterol-rich membrane domains from trans-Golgi network vesicles. J. Lipid Res. 2011, 52:582-589.
39. Wong K., Meyers dd R., Cantley L.C. Subcellular locations of phosphatidylinositol 4-kinase isoforms. J. Biol. Chem. 1997, 272:13236-13241.
40. Ishikawa S., Egami H., Kurizaki T., Akagi J., Tamori Y., Yoshida N., et al. Identification of genes related to invasion and metastasis in pancreatic cancer by cDNA representational difference analysis. J. Exp. Clin. Cancer Res. 2003, 22:299-306.
41. Ma H., Blake T., Chitnis A., Liu P., Balla T. Crucial role of phosphatidylinositol 4-kinase IIIalpha in development of zebrafish pectoral fin is linked to phosphoinositide 3-kinase and FGF signaling. J. Cell Sci. 2009, 122:4303-4310.
42. Audhya A., Emr S.D. Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev. Cell 2002, 2:593-605.
43. Guerreiro A.S., Fattet S., Kulesza D.W., Atamer A., Elsing A.N., Shalaby T., et al. A sensitized RNA interference screen identifies a novel role for the PI3K p110gamma isoform in medulloblastoma cell proliferation and chemoresistance. Mol. Cancer Res. 2011, 9:925-935.
44. Giroux V., Iovanna J., Dagorn J.C. Probing the human kinome for kinases involved in pancreatic cancer cell survival and gemcitabine resistance. FASEB J. 2006, 20:1982-1991.
45. Godi A., Pertile P., Meyers R., Marra P., Di Tullio G., Iurisci C., et al. ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat. Cell Biol. 1999, 1:280-287.
46. Hausser A., Storz P., Martens S., Link G., Toker A., Pfizenmaier K. Protein kinase D regulates vesicular transport by phosphorylating and activating phosphatidylinositol-4 kinase IIIbeta at the Golgi complex. Nat. Cell Biol. 2005, 7:880-886.
47. Taverna E., Francolini M., Jeromin A., Hilfiker S., Roder J., Rosa P. Neuronal calcium sensor 1 and phosphatidylinositol 4-OH kinase beta interact in neuronal cells and are translocated to membranes during nucleotide-evoked exocytosis. J. Cell Sci. 2002, 115:3909-3922.
48. Zhao X., Varnai P., Tuymetova G., Balla A., Toth Z.E., Oker-Blom C., et al. Interaction of neuronal calcium sensor-1 (NCS-1) with phosphatidylinositol 4-kinase beta stimulates lipid kinase activity and affects membrane trafficking in COS-7 cells. J. Biol. Chem. 2001, 276:40183-40189.
49. Gromada J., Bark C., Smidt K., Efanov A.M., Janson J., Mandic S.A., et al. Neuronal calcium sensor-1 potentiates glucose-dependent exocytosis in pancreatic beta cells through activation of phosphatidylinositol 4-kinase beta. Proc. Natl. Acad. Sci. USA 2005, 102:10303-10308.
50. Haynes L.P., Thomas G.M., Burgoyne R.D. Interaction of neuronal calcium sensor-1 and ADP-ribosylation factor 1 allows bidirectional control of phosphatidylinositol 4-kinase beta and trans-Golgi network-plasma membrane traffic. J. Biol. Chem. 2005, 280:6047-6054.
51. Kapp-Barnea Y., Melnikov S., Shefler I., Jeromin A., Sagi-Eisenberg R. Neuronal calcium sensor-1 and phosphatidylinositol 4-kinase beta regulate IgE receptor-triggered exocytosis in cultured mast cells. J. Immunol. 2003, 171:5320-5327.
52. Kapp-Barnea Y., Ninio-Many L., Hirschberg K., Fukuda M., Jeromin A., Sagi-Eisenberg R. Neuronal calcium sensor-1 and phosphatidylinositol 4-kinase beta stimulate extracellular signal-regulated kinase 1/2 signaling by accelerating recycling through the endocytic recycling compartment. Mol. Biol. Cell 2006, 17:4130-4141.
53. Koizumi S., Rosa P., Willars G.B., Challiss R.A., Taverna E., Francolini M., et al. Mechanisms underlying the neuronal calcium sensor-1-evoked enhancement of exocytosis in PC12 cells. J. Biol. Chem. 2002, 277:30315-30324.
54. Mora S., Durham P.L., Smith J.R., Russo A.F., Jeromin A., Pessin J.E. NCS-1 inhibits insulin-stimulated GLUT4 translocation in 3T3L1 adipocytes through a phosphatidylinositol 4-kinase-dependent pathway. J. Biol. Chem. 2002, 277:27494-27500.
55. 2+ sensor-1 in bovine chromaffin cells. J. Neurosci. 2002, 22:2427-2433.
56. Rajebhosale M., Greenwood S., Vidugiriene J., Jeromin A., Hilfiker S. Phosphatidylinositol 4-OH kinase is a downstream target of neuronal calcium sensor-1 in enhancing exocytosis in neuroendocrine cells. J. Biol. Chem. 2003, 278:6075-6084.
57. de Barry J., Janoshazi A., Dupont J.L., Procksch O., Chasserot-Golaz S., Jeromin A., et al. Functional implication of neuronal calcium sensor-1 and phosphoinositol 4-kinase-beta interaction in regulated exocytosis of PC12 cells. J. Biol. Chem. 2006, 281:18098-18111.
58. Zheng Q., Bobich J.A., Vidugiriene J., McFadden S.C., Thomas F., Roder J., et al. Neuronal calcium sensor-1 facilitates neuronal exocytosis through phosphatidylinositol 4-kinase. J. Neurochem. 2005, 92:442-451.
59. Toth B., Balla A., Ma H., Knight Z.A., Shokat K.M., Balla T. Phosphatidylinositol 4-kinase IIIbeta regulates the transport of ceramide between the endoplasmic reticulum and Golgi. J. Biol. Chem. 2006, 281:36369-36377.
60. Pinke D.E., Lee J.M. The lipid kinase PI4KIIIbeta and the eEF1A2 oncogene co-operate to disrupt three-dimensional in vitro acinar morphogenesis. Exp. Cell Res. 2011, 317:2503-2511.
61. Tomlinson V.A., Newbery H.J., Wray N.R., Jackson J., Larionov A., Miller W.R., et al. Translation elongation factor eEF1A2 is a potential oncoprotein that is overexpressed in two-thirds of breast tumours. BMC Cancer 2005, 5:113.
62. Kulkarni G., Turbin D.A., Amiri A., Jeganathan S., Andrade-Navarro M.A., Wu T.D., et al. Expression of protein elongation factor eEF1A2 predicts favorable outcome in breast cancer. Breast Cancer Res. Treat 2007, 102:31-41.
63. Anand N., Murthy S., Amann G., Wernick M., Porter L.A., Cukier I.H., et al. Protein elongation factor EEF1A2 is a putative oncogene in ovarian cancer. Nat. Genet. 2002, 31:301-305.
64. Balla A., Tuymetova G., Barshishat M., Geiszt M., Balla T. Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J. Biol. Chem. 2002, 277:20041-20050.
65. Wei Y.J., Sun H.Q., Yamamoto M., Wlodarski P., Kunii K., Martinez M., et al. Type II phosphatidylinositol 4-kinase beta is a cytosolic and peripheral membrane protein that is recruited to the plasma membrane and activated by Rac-GTP. J. Biol. Chem. 2002, 277:46586-46593.
66. Drabikowski W., Dabrowska R., Barylko B. Separation and characterization of the constituents of troponin. FEBS Lett. 1971, 12:148-152.
67. Jung G., Wang J., Wlodarski P., Barylko B., Binns D.D., Shu H., et al. Molecular determinants of activation and membrane targeting of phosphoinositol 4-kinase IIbeta. Biochem. J. 2008, 409:501-509.
68. Mazzocca A., Liotta F., Carloni V. Tetraspanin CD81-regulated cell motility plays a critical role in intrahepatic metastasis of hepatocellular carcinoma. Gastroenterology 2008, 135(244-56):e1.
69. Carloni V., Mazzocca A., Ravichandran K.S. Tetraspanin CD81 is linked to ERK/MAPKinase signaling by Shc in liver tumor cells. Oncogene 2004, 23:1566-1574.
70. Hemler M.E. Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 2005, 6:801-811.
71. Berditchevski F. Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 2001, 114:4143-4151.
72. Yauch R.L., Hemler M.E. Specific interactions among transmembrane 4 superfamily (TM4SF) proteins and phosphoinositide 4-kinase. Biochem. J. 2000, 351(Pt 3):629-637.
73. Pan W., Choi S.C., Wang H., Qin Y., Volpicelli-Daley L., Swan L., et al. Wnt3a-mediated formation of phosphatidylinositol 4,5-bisphosphate regulates LRP6 phosphorylation. Science 2008, 321:1350-1353.
74. Qin Y., Li L., Pan W., Wu D. Regulation of phosphatidylinositol kinases and metabolism by Wnt3a and Dvl. J. Biol. Chem. 2009, 284:22544-22548.
75. Minogue S., Waugh M.G., De Matteis M.A., Stephens D.J., Berditchevski F., Hsuan J.J. Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor. J. Cell Sci. 2006, 119:571-581.
76. Weixel K.M., Blumental-Perry A., Watkins S.C., Aridor M., Weisz O.A. Distinct Golgi populations of phosphatidylinositol 4-phosphate regulated by phosphatidylinositol 4-kinases. J. Biol. Chem. 2005, 280:10501-10508.
77. Salazar G., Craige B., Wainer B.H., Guo J., De Camilli P., Faundez V. Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles. Mol. Biol. Cell 2005, 16:3692-3704.
78. Guo J., Wenk M.R., Pellegrini L., Onofri F., Benfenati F., De Camilli P. Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl. Acad. Sci. USA 2003, 100:3995-4000.
79. Xu Z., Huang G., Kandror K.V. Phosphatidylinositol 4-kinase type IIalpha is targeted specifically to cellugyrin-positive glucose transporter 4 vesicles. Mol. Endocrinol. 2006, 20:2890-2897.
80. Knight Z.A., Gonzalez B., Feldman M.E., Zunder E.R., Goldenberg D.D., Williams O., et al. A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling. Cell 2006, 125:733-747.
81. Borawski J., Troke P., Puyang X., Gibaja V., Zhao S., Mickanin C., et al. Class III phosphatidylinositol 4-kinase alpha and beta are novel host factor regulators of hepatitis C virus replication. J. Virol. 2009, 83:10058-10074.
82. Arita M., Kojima H., Nagano T., Okabe T., Wakita T., Shimizu H. Phosphatidylinositol 4-kinase III beta is a target of enviroxime-like compounds for antipoliovirus activity. J. Virol. 2011, 85:2364-2372.
83. Greninger A.L., Knudsen G.M., Betegon M., Burlingame A.L., Derisi J.L. The 3A protein from multiple picornaviruses utilizes the Golgi adaptor protein ACBD3 to recruit PI4KIIIbeta. J. Virol. 2012, 86:3605-3616.
84. Yang N., Ma P., Lang J., Zhang Y., Deng J., Ju X., et al. Phosphatidylinositol 4-kinase IIIbeta is required for severe acute respiratory syndrome coronavirus spike-mediated cell entry. J. Biol. Chem. 2012, 287:8457-8467.
85. Bianco A., Reghellin V., Donnici L., Fenu S., Alvarez R., Baruffa C., et al. Metabolism of phosphatidylinositol 4-kinase IIIalpha-dependent PI4P Is subverted by HCV and is targeted by a 4-anilino quinazoline with antiviral activity. PLoS Pathog. 2012, 8:e1002576.
86. Waugh M.G., Minogue S., Hsuan J.J. Quantification of multiple phosphatidylinositol 4-kinase isozyme activities in cell extracts. Meth. Mol. Biol. 2009, 462:279-289.
87. Tai A.W., Bojjireddy N., Balla T. A homogeneous and nonisotopic assay for phosphatidylinositol 4-kinases. Anal. Biochem. 2011, 417:97-102.
88. Jovic M., Kean M.J., Szentpetery Z., Polevoy G., Gingras A.C., Brill J.A., et al. Two phosphatidylinositol 4-kinases control lysosomal delivery of the Gaucher disease enzyme, beta-glucocerebrosidase. Mol. Biol. Cell 2012, 23:1533-1545.
89. Barylko B., Gerber S.H., Binns D.D., Grichine N., Khvotchev M., Sudhof T.C., et al. A novel family of phosphatidylinositol 4-kinases conserved from yeast to humans. J. Biol. Chem. 2001, 276:7705-7708.
90. Barylko B., Mao Y.S., Wlodarski P., Jung G., Binns D.D., Sun H.Q., et al. Palmitoylation controls the catalytic activity and subcellular distribution of phosphatidylinositol 4-kinase II{alpha}. J. Biol. Chem. 2009, 284:9994-10003.
91. Rajendran L., Schneider A., Schlechtingen G., Weidlich S., Ries J., Braxmeier T., et al. Efficient inhibition of the Alzheimer's disease beta-secretase by membrane targeting. Science 2008, 320:520-523.
92. Foukas L.C., Berenjeno I.M., Gray A., Khwaja A., Vanhaesebroeck B. Activity of any class IA PI3K isoform can sustain cell proliferation and survival. Proc. Natl. Acad. Sci. USA 2010, 107:11381-11386.
93. Chaussade C., Rewcastle G.W., Kendall J.D., Denny W.A., Cho K., Gronning L.M., et al. Evidence for functional redundancy of class IA PI3K isoforms in insulin signalling. Biochem. J. 2007, 404:449-458.
94. Jo H., Lo P.K., Li Y., Loison F., Green S., Wang J., et al. Deactivation of Akt by a small molecule inhibitor targeting pleckstrin homology domain and facilitating Akt ubiquitination. Proc. Natl. Acad. Sci. USA 2011, 108:6486-6491.
95. Mak L.H., Georgiades S.N., Rosivatz E., Whyte G.F., Mirabelli M., Vilar R., et al. A small molecule mimicking a phosphatidylinositol (4,5)-bisphosphate binding pleckstrin homology domain. ACS Chem. Biol. 2011, 6:1382-1390.
96. Gustin J.P., Karakas B., Weiss M.B., Abukhdeir A.M., Lauring J., Garay J.P., et al. Knockin of mutant PIK3CA activates multiple oncogenic pathways. Proc. Natl. Acad. Sci. USA 2009, 106:2835-2840.
97. Yuan W., Stawiski E., Janakiraman V., Chan E., Durinck S., Edgar K.A., et al. Conditional activation of Pik3ca(H1047R) in a knock-in mouse model promotes mammary tumorigenesis and emergence of mutations. Oncogene 2012.
98. Adams J.R., Xu K., Liu J.C., Agamez N.M., Loch A.J., Wong R.G., et al. Cooperation between Pik3ca and p53 mutations in mouse mammary tumor formation. Cancer Res. 2011, 71:2706-2717.
99. She Q.B., Chandarlapaty S., Ye Q., Lobo J., Haskell K.M., Leander K.R., et al. Breast tumor cells with PI3K mutation or HER2 amplification are selectively addicted to Akt signaling. PLoS One 2008, 3:e3065.
100. Pang H., Flinn R., Patsialou A., Wyckoff J., Roussos E.T., Wu H., et al. Differential enhancement of breast cancer cell motility and metastasis by helical and kinase domain mutations of class IA phosphoinositide 3-kinase. Cancer Res. 2009, 69:8868-8876.
101. Nilsson P., Paavilainen L., Larsson K., Odling J., Sundberg M., Andersson A.C., et al. Towards a human proteome atlas: high-throughput generation of mono-specific antibodies for tissue profiling. Proteomics 2005, 5:4327-4337.
102. Ponten F., Schwenk J.M., Asplund A., Edqvist P.H. The human protein atlas as a proteomic resource for biomarker discovery. J. Intern. Med. 2011, 270:428-446.
103. Uhlen M., Oksvold P., Fagerberg L., Lundberg E., Jonasson K., Forsberg M., et al. Towards a knowledge-based human protein atlas. Nat. Biotechnol. 2010, 28:1248-1250.