Somatic Mutations in p85α Promote Tumorigenesis through Class IA PI3K Activation

Cancer Cell

Volumn 16, Issue 6, 2009, Pages 463-474

  Jaiswal, Bijay S ^a   Janakiraman, Vasantharajan ^a   Kljavin, Noelyn M ^a   Chaudhuri, Subhra ^a   Stern, Howard M ^a   Wang, Weiru ^a   Kan, Zhengyan ^a   Dbouk, Hashem A ^b   Peters, Brock A ^a   Waring, Paul ^a   Dela Vega, Trisha ^a   Kenski, Denise M ^a   Bowman, Krista K ^a   Lorenzo, Maria ^a   Li, Hong ^a   Wu, Jiansheng ^a   Modrusan, Zora ^a   Stinson, Jeremy ^a   Eby, Michael ^a   Yue, Peng ^a   Kaminker, Josh S ^a   de Sauvage, Frederic J ^a   Backer, Jonathan M ^b   Seshagiri, Somasekar ^a   more..

^a GENENTECH INC   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

CELLCYCLE; SIGNALING

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE 1A; PROTEIN KINASE B; PROTEIN P110; PROTEIN P110ALPHA; PROTEIN P85; PROTEIN P85ALPHA; PROTEIN SH2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL GROWTH; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; COLON CANCER; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENE SEQUENCE; HUMAN; HUMAN TISSUE; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SOMATIC MUTATION; ANIMAL; CELL LINE; CELL TRANSFORMATION; CHEMISTRY; COLON TUMOR; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; PATHOLOGY;

MAMMALIA;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; ENZYME ACTIVATION; HUMANS; MICE; MUTATION;

EID: 70749140937     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2009.10.016     Document Type: Article

References (55)

1. Amzel L.M., Huang C.H., Mandelker D., Lengauer C., Gabelli S.B., and Vogelstein B. Structural comparisons of class I phosphoinositide 3-kinases. Nat. Rev. Cancer 8 (2008) 665-669
2. Backer J.M., Myers Jr. M.G., Shoelson S.E., Chin D.J., Sun X.J., Miralpeix M., Hu P., Margolis B., Skolnik E.Y., Schlessinger J., et al. Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11 (1992) 3469-3479
3. Bader A.G., Kang S., Zhao L., and Vogt P.K. Oncogenic PI3K deregulates transcription and translation. Nat. Rev. Cancer 5 (2005) 921-929
4. Borlado L.R., Redondo C., Alvarez B., Jimenez C., Criado L.M., Flores J., Marcos M.A., Martinez A.C., Balomenos D., and Carrera A.C. Increased phosphoinositide 3-kinase activity induces a lymphoproliferative disorder and contributes to tumor generation in vivo. FASEB J. 14 (2000) 895-903
5. Brachmann S.M., Yballe C.M., Innocenti M., Deane J.A., Fruman D.A., Thomas S.M., and Cantley L.C. Role of phosphoinositide 3-kinase regulatory isoforms in development and actin rearrangement. Mol. Cell. Biol. 25 (2005) 2593-2606
6. Cantley L.C. The phosphoinositide 3-kinase pathway. Science 296 (2002) 1655-1657
7. Carpenter C.L., Auger K.R., Chanudhuri M., Yoakim M., Schaffhausen B., Shoelson S., and Cantley L.C. Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J. Biol. Chem. 268 (1993) 9478-9483
8. Chan T.O., Rodeck U., Chan A.M., Kimmelman A.C., Rittenhouse S.E., Panayotou G., and Tsichlis P.N. Small GTPases and tyrosine kinases coregulate a molecular switch in the phosphoinositide 3-kinase regulatory subunit. Cancer Cell 1 (2002) 181-191
9. Chantry D., Vojtek A., Kashishian A., Holtzman D.A., Wood C., Gray P.W., Cooper J.A., and Hoekstra M.F. p110delta, a novel phosphatidylinositol 3-kinase catalytic subunit that associates with p85 and is expressed predominantly in leukocytes. J. Biol. Chem. 272 (1997) 19236-19241
10. Dhand R., Hara K., Hiles I., Bax B., Gout I., Panayotou G., Fry M.J., Yonezawa K., Kasuga M., and Waterfield M.D. PI 3-kinase: structural and functional analysis of intersubunit interactions. EMBO J. 13 (1994) 511-521
11. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
12. Engelman J.A., Luo J., and Cantley L.C. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7 (2006) 606-619
13. Folkes, A., Shuttleworth, S., Chuckowree, I., Oxenford, S., Wan, N.C., Castanedo, G., Goldsmith, R., Gunzner, J., Heffron, T., Mathieu, S., et al. August 2007. Preparation of thienopyrimidines and furopyrimidines as lipid kinase inhibitors for treating cancer and other diseases. Patent PIXXD2 WO 2007127175.
14. Fruman D.A., Meyers R.E., and Cantley L.C. Phosphoinositide kinases. Annu. Rev. Biochem. 67 (1998) 481-507
15. Garcia Z., Silio V., Marques M., Cortes I., Kumar A., Hernandez C., Checa A.I., Serrano A., and Carrera A.C. A PI3K activity-independent function of p85 regulatory subunit in control of mammalian cytokinesis. EMBO J. 25 (2006) 4740-4751
16. Gymnopoulos M., Elsliger M.A., and Vogt P.K. Rare cancer-specific mutations in PIK3CA show gain of function. Proc. Natl. Acad. Sci. USA 104 (2007) 5569-5574
17. Hartmann C., Bartels G., Gehlhaar C., Holtkamp N., and von Deimling A. PIK3CA mutations in glioblastoma multiforme. Acta Neuropathol. 109 (2005) 639-642
18. Hawkins P.T., Anderson K.E., Davidson K., and Stephens L.R. Signalling through Class I PI3Ks in mammalian cells. Biochem. Soc. Trans. 34 (2006) 647-662
19. Hennessy B.T., Smith D.L., Ram P.T., Lu Y., and Mills G.B. Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat. Rev. Drug Discov. 4 (2005) 988-1004
20. Hoedemaeker F.J., Siegal G., Roe S.M., Driscoll P.C., and Abrahams J.P. Crystal structure of the C-terminal SH2 domain of the p85alpha regulatory subunit of phosphoinositide 3-kinase: an SH2 domain mimicking its own substrate. J. Mol. Biol. 292 (1999) 763-770
21. Holt K.H., Olson L., Moye-Rowley W.S., and Pessin J.E. Phosphatidylinositol 3-kinase activation is mediated by high-affinity interactions between distinct domains within the p110 and p85 subunits. Mol. Cell. Biol. 14 (1994) 42-49
22. Horn S., Bergholz U., Jucker M., McCubrey J.A., Trumper L., Stocking C., and Basecke J. Mutations in the catalytic subunit of class IA PI3K confer leukemogenic potential to hematopoietic cells. Oncogene 27 (2008) 4096-4106
23. Hu P., Mondino A., Skolnik E.Y., and Schlessinger J. Cloning of a novel, ubiquitously expressed human phosphatidylinositol 3-kinase and identification of its binding site on p85. Mol. Cell. Biol. 13 (1993) 7677-7688
24. Huang C.H., Mandelker D., Schmidt-Kittler O., Samuels Y., Velculescu V.E., Kinzler K.W., Vogelstein B., Gabelli S.B., and Amzel L.M. The structure of a human p110alpha/p85alpha complex elucidates the effects of oncogenic PI3Kalpha mutations. Science 318 (2007) 1744-1748
25. Huang C.H., Mandelker D., Gabelli S.B., and Amzel L.M. Insights into the oncogenic effects of PIK3CA mutations from the structure of p110alpha/p85alpha. Cell Cycle 7 (2008) 1151-1156
26. Huang J., Wei W., Zhang J., Liu G., Bignell G.R., Stratton M.R., Futreal P.A., Wooster R., Jones K.W., and Shapero M.H. Whole genome DNA copy number changes identified by high density oligonucleotide arrays. Hum. Genomics 1 (2004) 287-299
27. Ikenoue T., Kanai F., Hikiba Y., Obata T., Tanaka Y., Imamura J., Ohta M., Jazag A., Guleng B., Tateishi K., et al. Functional analysis of PIK3CA gene mutations in human colorectal cancer. Cancer Res. 65 (2005) 4562-4567
28. Isakoff S.J., Engelman J.A., Irie H.Y., Luo J., Brachmann S.M., Pearline R.V., Cantley L.C., and Brugge J.S. Breast cancer-associated PIK3CA mutations are oncogenic in mammary epithelial cells. Cancer Res. 65 (2005) 10992-11000
29. Jackson S.P., Schoenwaelder S.M., Goncalves I., Nesbitt W.S., Yap C.L., Wright C.E., Kenche V., Anderson K.E., Dopheide S.M., Yuan Y., et al. PI 3-kinase p110beta: a new target for antithrombotic therapy. Nat. Med. 11 (2005) 507-514
30. Jimenez C., Hernandez C., Pimentel B., and Carrera A.C. The p85 regulatory subunit controls sequential activation of phosphoinositide 3-kinase by Tyr kinases and Ras. J. Biol. Chem. 277 (2002) 41556-41562
31. Jimenez C., Jones D.R., Rodriguez-Viciana P., Gonzalez-Garcia A., Leonardo E., Wennstrom S., von Kobbe C., Toran J.L., R-Borlado L., Calvo V., et al. Identification and characterization of a new oncogene derived from the regulatory subunit of phosphoinositide 3-kinase. EMBO J. 17 (1998) 743-753
32. Jucker M., Sudel K., Horn S., Sickel M., Wegner W., Fiedler W., and Feldman R.A. Expression of a mutated form of the p85alpha regulatory subunit of phosphatidylinositol 3-kinase in a Hodgkin's lymphoma-derived cell line (CO). Leukemia 16 (2002) 894-901
33. Kang S., Bader A.G., and Vogt P.K. Phosphatidylinositol 3-kinase mutations identified in human cancer are oncogenic. Proc. Natl. Acad. Sci. USA 102 (2005) 802-807
34. Kang S., Denley A., Vanhaesebroeck B., and Vogt P.K. Oncogenic transformation induced by the p110beta, -gamma, and -delta isoforms of class I phosphoinositide 3-kinase. Proc. Natl. Acad. Sci. USA 103 (2006) 1289-1294
35. Knight Z.A., Feldman M.E., Balla A., Balla T., and Shokat K.M. A membrane capture assay for lipid kinase activity. Nat. Protoc. 2 (2007) 2459-2466
36. Kodaki T., Woscholski R., Hallberg B., Rodriguez-Viciana P., Downward J., and Parker P.J. The activation of phosphatidylinositol 3-kinase by Ras. Curr. Biol. 4 (1994) 798-806
37. Lambert C., Leonard N., De Bolle X., and Depiereux E. ESyPred3D: Prediction of proteins 3D structures. Bioinformatics 18 (2002) 1250-1256
38. Lin M., Wei L.J., Sellers W.R., Lieberfarb M., Wong W.H., and Li C. dChipSNP: significance curve and clustering of SNP-array-based loss-of-heterozygosity data. Bioinformatics 20 (2004) 1233-1240
39. Miled N., Yan Y., Hon W.C., Perisic O., Zvelebil M., Inbar Y., Schneidman-Duhovny D., Wolfson H.J., Backer J.M., and Williams R.L. Mechanism of two classes of cancer mutations in the phosphoinositide 3-kinase catalytic subunit. Science 317 (2007) 239-242
40. Otsu M., Hiles I., Gout I., Fry M.J., Ruiz-Larrea F., Panayotou G., Thompson A., Dhand R., Hsuan J., Totty N., et al. Characterization of two 85 kd proteins that associate with receptor tyrosine kinases, middle-T/pp60c-src complexes, and PI3-kinase. Cell 65 (1991) 91-104
41. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 321 (2008) 1807-1812
42. Philp A.J., Campbell I.G., Leet C., Vincan E., Rockman S.P., Whitehead R.H., Thomas R.J., and Phillips W.A. The phosphatidylinositol 3′-kinase p85alpha gene is an oncogene in human ovarian and colon tumors. Cancer Res. 61 (2001) 7426-7429
43. Samuels Y., Wang Z., Bardelli A., Silliman N., Ptak J., Szabo S., Yan H., Gazdar A., Powell S.M., Riggins G.J., et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 304 (2004) 554
44. Shekar S.C., Wu H., Fu Z., Yip S.C., Nagajyothi, Cahill S.M., Girvin M.E., and Backer J.M. Mechanism of constitutive phosphoinositide 3-kinase activation by oncogenic mutants of the p85 regulatory subunit. J. Biol. Chem. 280 (2005) 27850-27855
45. Starr T.K., Allaei R., Silverstein K.A., Staggs R.A., Sarver A.L., Bergemann T.L., Gupta M., O'Sullivan M.G., Matise I., Dupuy A.J., et al. A transposon-based genetic screen in mice identifies genes altered in colorectal cancer. Science 323 (2009) 1747-1750
46. Taniguchi C.M., Tran T.T., Kondo T., Luo J., Ueki K., Cantley L.C., and Kahn C.R. Phosphoinositide 3-kinase regulatory subunit p85alpha suppresses insulin action via positive regulation of PTEN. Proc. Natl. Acad. Sci. USA 103 (2006) 12093-12097
47. TCGA. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455 (2008) 1061-1068
48. Vanhaesebroeck B., and Waterfield M.D. Signaling by distinct classes of phosphoinositide 3-kinases. Exp. Cell Res. 253 (1999) 239-254
49. 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
50. Vaughn J.L., Goodwin R.H., Tompkins G.J., and McCawley P. The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In Vitro 13 (1977) 213-217
51. Wang Z.J., Taylor F., Churchman M., Norbury G., and Tomlinson I. Genetic pathways of colorectal carcinogenesis rarely involve the PTEN and LKB1 genes outside the inherited hamartoma syndromes. Am. J. Pathol. 153 (1998) 363-366
52. Wood L.D., Parsons D.W., Jones S., Lin J., Sjoblom T., Leary R.J., Shen D., Boca S.M., Barber T., Ptak J., et al. The genomic landscapes of human breast and colorectal cancers. Science 318 (2007) 1108-1113
53. Yin Y., and Shen W.H. PTEN: a new guardian of the genome. Oncogene 27 (2008) 5443-5453
54. Yu J., Zhang Y., McIlroy J., Rordorf-Nikolic T., Orr G.A., and Backer J.M. Regulation of the p85/p110 phosphatidylinositol 3′-kinase: stabilization and inhibition of the p110alpha catalytic subunit by the p85 regulatory subunit. Mol. Cell. Biol. 18 (1998) 1379-1387
55. Zhao L., and Vogt P.K. Class I PI3K in oncogenic cellular transformation. Oncogene 27 (2008) 5486-5496