Identification of mutations in distinct regions of p85 alpha in urothelial cancer

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Ross, Rebecca L ^a   Burns, Julie E ^a   Taylor, Claire F ^a   Mellor, Paul ^b   Anderson, Deborah H ^b   Knowles, Margaret A ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 110 ALPHA; MESSENGER RNA; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN P85; PROTEIN P85ALPHA; RAB PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL TYPE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; EXON; FIBROBLAST; GENE DELETION; GENE FUNCTION; GENETIC ANALYSIS; GENETIC IDENTIFICATION; GENETIC SCREENING; HETEROZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MISSENSE MUTATION; MOUSE; NONHUMAN; PIK3CA GENE; PIK3R1 GENE; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UROGENITAL TRACT CANCER; UROTHELIUM CELL;

ANIMALS; CATTLE; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GTP PHOSPHOHYDROLASES; HUMANS; MODELS, MOLECULAR; MUTATION; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; RAB5 GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; URINARY BLADDER NEOPLASMS; UROTHELIUM;

EID: 84893158543     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084411     Document Type: Article

References (49)

1. Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296: 1655-1657. doi:10.1126/science.296.5573.1655. PubMed: 12040186.
2. Askham JM, Platt F, Chambers PA, Snowden H, Taylor CF et al. (2010) AKT1 mutations in bladder cancer: identification of a novel oncogenic mutation that can co-operate with E17K. Oncogene 29: 150-155. doi:10.1038/onc.2009.315. PubMed: 19802009.
3. Aveyard JS, Skilleter A, Habuchi T, Knowles MA (1999) Somatic mutation of PTEN in bladder carcinoma. Br J Cancer 80: 904-908. doi:10.1038/sj.bjc.6690439. PubMed: 10360673. (Pubitemid 29209858)
4. Platt FM, Hurst CD, Taylor CF, Gregory WM, Harnden P et al. (2009) Spectrum of phosphatidylinositol 3-kinase pathway gene alterations in bladder cancer. Clin Cancer Res 15: 6008-6017. doi:10.1158/1078-0432.CCR-09-0898. PubMed: 19789314.
5. López-Knowles E, Hernández S, Malats N, Kogevinas M, Lloreta J et al. (2006) PIK3CA mutations are an early genetic alteration associated with FGFR3 mutations in superficial papillary bladder tumors. Cancer Res 66: 7401-7404. doi:10.1158/0008-5472.CAN-06-1182. PubMed: 16885334. (Pubitemid 44289191)
6. Cairns P, Evron E, Okami K, Halachmi N, Esteller M et al. (1998) Point mutation and homozygous deletion of PTEN/MMAC1 in primary bladder cancers. Oncogene 16: 3215-3218. doi:10.1038/sj.onc.1201855. PubMed: 9671402. (Pubitemid 28318794)
7. Wang DS, Rieger-Christ K, Latini JM, Moinzadeh A, Stoffel J et al. (2000) Molecular analysis of PTEN and MXI1 in primary bladder carcinoma. Int J Cancer 88: 620-625. doi:10.1002/1097-0215(20001115)88:4. PubMed: 11058880.
8. Knowles MA, Habuchi T, Kennedy W, Cuthbert-Heavens D (2003) Mutation Spectrum of the 9q34 Tuberous Sclerosis Gene TSC1 in Transitional Cell Carcinoma of the Bladder. Cancer Res 63: 7652-7656. PubMed: 14633685. (Pubitemid 37466691)
9. Yu J, Wjasow C, Backer JM (1998) Regulation of the p85/p110alpha phosphatidylinositol 3′-kinase. Distinct roles for the n-terminal and c-terminal SH2 domains. J Biol Chem 273: 30199-30203. doi:10.1074/jbc.273.46. 30199. PubMed: 9804776. (Pubitemid 28545483)
10. Miled N, Yan Y, Hon W-C, Perisic O, Zvelebil M et al. (2007) Mechanism of two classes of cancer mutations in the phosphoinositide 3-kinase catalytic subunit. Science 317: 239-242. doi:10.1126/science.1135394. PubMed: 17626883. (Pubitemid 47076198)
11. Jimenez C, Jones DR, Rodríguez-Viciana P, Gonzalez-García A, Leonardo E et al. (1998) Identification and characterization of a new oncogene derived from the regulatory subunit of phosphoinositide 3-kinase. EMBO J 17: 743-753. doi:10.1093/emboj/17.3.743. PubMed: 9450999.
12. Shekar SC, Wu H, Fu Z, Yip SC, Nagajyothi et al. (2005) Mechanism of constitutive phosphoinositide 3-kinase activation by oncogenic mutants of the p85 regulatory subunit. J Biol Chem 280: 27850-27855. doi:10.1074/jbc. M506005200. PubMed: 15932879. (Pubitemid 41076901)
13. Jücker M, Südel K, Horn S, Sickel M, Wegner W et al. (2002) 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: 894-901. doi:10.1038/sj.leu.2402484. PubMed: 11986952. (Pubitemid 34537563)
14. Philp AJ, Campbell IG, Leet C, Vincan E, Rockman SP et al. (2001) The phosphatidylinositol 3′-kinase p85alpha gene is an oncogene in human ovarian and colon tumors. Cancer Res 61: 7426-7429. PubMed: 11606375. (Pubitemid 32995029)
15. Mizoguchi M, Nutt CL, Mohapatra G, Louis DN (2004) Genetic alterations of phosphoinositide 3-kinase subunit genes in human glioblastomas. Brain Pathol 14: 372-377. PubMed: 15605984. (Pubitemid 39524966)
16. Network. TCGAR (2008) Comprehensive genomic characterisation defines human glioblastoma genes and core pathways. Nature 455: 1061-1068
17. Jaiswal BS, Janakiraman V, Kljavin NM, Chaudhuri S, Stern HM et al. (2009) Somatic mutations in p85alpha promote tumorigenesis through class IA PI3K activation. Cancer Cell 16: 463-474. doi:10.1016/j.ccr.2009.10.016. PubMed: 19962665.
18. Sjödahl G, Lauss M, Gudjonsson S, Liedberg F, Halldén C et al. (2011) A systematic study of gene mutations in urothelial carcinoma; inactivating mutations in TSC2 and PIK3R1. PLOS ONE 6: e18583. doi:10.1371/journal.pone.0018583. PubMed: 21533174.
19. Urick ME, Rudd ML, Godwin AK, Sgroi DC, Merino M et al. (2011) PIK3R1 (p85-alpha/p85{alpha}) is Somatically Mutated at High Frequency in Primary Endometrial. Cancer - Cancer Res 71: 4061-4067. doi:10.1158/0008-5472.CAN-11- 0549.
20. Cheung LW, Hennessy BT, Li J, Yu S, Myers AP et al. (2011) High Frequency of PIK3R1 and PIK3R2 Mutations in Endometrial Cancer Elucidates a Novel Mechanism for Regulation of PTEN Protein Stability. Cancer Discov 1: 170-185. Available online at: doi:10.1158/2159-8290.CD-11-0039 PubMed: 21984976.
21. Chamberlain MD, Berry TR, Pastor MC, Anderson DH (2004) The p85alpha subunit of phosphatidylinositol 3′-kinase binds to and stimulates the GTPase activity of Rab proteins. J Biol Chem 279: 48607-48614. doi:10.1074/jbc.M409769200. PubMed: 15377662. (Pubitemid 39625735)
22. Rabinovsky R, Pochanard P, McNear C, Brachmann SM, Duke-Cohan JS et al. (2009) p85 Associates with unphosphorylated PTEN and the PTEN-associated complex. Mol Cell Biol 29: 5377-5388. doi:10.1128/MCB.01649-08. PubMed: 19635806.
23. Chagpar RB, Links PH, Pastor MC, Furber LA, Hawrysh AD et al. (2010) Direct positive regulation of PTEN by the p85 subunit of phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A 107: 5471-5476. doi:10.1073/pnas.0908899107. PubMed: 20212113.
24. UICC (1978) TNM classification of malignant tumors, bladder. 3 ed: Union Internationale Contre le Cancer, Geneva. pp. 113-117
25. WHO (1973) Histological typing of urinary bladder tumours; Mostofi Fk, Geneva, editor. World Health Organisation.
26. Chapman EJ, Williams SV, Platt FM, Hurst CD, Chambers P et al. (2009) Integrated genomic and transcriptional analysis of the in vitro evolution of telomerase-immortalized urothelial cells (TERT-NHUC). Genes Chromosomes Cancer 48: 694-710. doi:10.1002/gcc.20672. PubMed: 19405089.
27. Taylor CF (2009) Mutation scanning using high-resolution melting. Biochem Soc Trans 37: 433-437. doi:10.1042/BST0370433. PubMed: 19290876.
28. Tomlinson DC, L'Hôte CG, Kennedy W, Pitt E, Knowles MA (2005) Alternative splicing of fibroblast growth factor receptor 3 produces a secreted isoform that inhibits fibroblast growth factor-induced proliferation and is repressed in urothelial carcinoma cell lines. Cancer Res 65: 10441-10449. doi:10.1158/0008-5472.CAN-05-1718. PubMed: 16288035. (Pubitemid 41743738)
29. Ross RL, Askham JM, Knowles MA (2013) PIK3CA mutation spectrum in urothelial carcinoma reflects cell context-dependent signaling and phenotypic outputs. Oncogene 32: 768-776. PubMed: 22430209.
30. Sanchez-Carbayo M, Socci ND, Lozano J, Saint F, Cordon-Cardo C (2006) Defining molecular profiles of poor outcome in patients with invasive bladder cancer using oligonucleotide microarrays. J Clin Oncol 24: 778-789. doi:10.1200/JCO.2005.03.2375. PubMed: 16432078. (Pubitemid 46622045)
31. Antonetti DA, Algenstaedt P, Kahn CR (1996) Insulin receptor substrate 1 binds two novel splice variants of the regulatory subunit of phosphatidylinositol 3-kinase in muscle and brain. Mol Cell Biol 16: 2195-2203. PubMed: 8628286. (Pubitemid 26123740)
32. Mandelker D, Gabelli SB, Schmidt-Kittler O, Zhu J, Cheong I et al. (2009) A frequent kinase domain mutation that changes the interaction between PI3Kalpha and the membrane. Proc Natl Acad Sci U S A 106: 16996-17001. doi:10.1073/pnas.0908444106. PubMed: 19805105.
33. Wu H, Shekar SC, Flinn RJ, El-Sibai M, Jaiswal BS et al. (2009) Regulation of Class IA PI 3-kinases: C2 domain-iSH2 domain contacts inhibit p85/p110alpha and are disrupted in oncogenic p85 mutants. Proc Natl Acad Sci U S A 106: 20258-20263. doi:10.1073/pnas.0902369106. PubMed: 19915146.
34. Parsons DW, Jones S, Zhang X, Lin JC-H, Leary RJ et al. (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321: 1807-1812. doi:10.1126/science.1164382. PubMed: 18772396.
35. Huang C-H, Mandelker D, Schmidt-Kittler O, Samuels Y, Velculescu VE et al. (2007) The structure of a human p110alpha/p85alpha complex elucidates the effects of oncogenic PI3Kalpha mutations. Science 318: 1744-1748. doi:10.1126/science.1150799. PubMed: 18079394. (Pubitemid 350274378)
36. Sun M, Hillmann P, Hofmann BT, Hart JR, Vogt PK (2010) Cancer-derived mutations in the regulatory subunit p85alpha of phosphoinositide 3-kinase function through the catalytic subunit p110alpha. Proc Natl Acad Sci U S A 107: 15547-15552. doi:10.1073/pnas.1009652107. PubMed: 20713702.
37. Musacchio A, Cantley LC, Harrison SC (1996) Crystal structure of the breakpoint cluster region-homology domain from phosphoinositide 3-kinase p85 alpha subunit. Proc Natl Acad Sci U S A 93: 14373-14378. doi:10.1073/pnas.93.25. 14373. PubMed: 8962058. (Pubitemid 26418973)
38. Dhand R, Hara K, Hiles I, Bax B, Gout I et al. (1994) PI 3-kinase: structural and functional analysis of intersubunit interactions. EMBO J 13: 511-521. PubMed: 8313896. (Pubitemid 24050665)
39. Chamberlain MD, Chan T, Oberg JC, Hawrysh AD, James KM et al. (2008) Disrupted RabGAP function of the p85 subunit of phosphatidylinositol 3-kinase results in cell transformation. J Biol Chem 283: 15861-15868. doi:10.1074/jbc.M800941200. PubMed: 18387942.
40. Brachmann SM, Yballe CM, Innocenti M, Deane JA, Fruman DA et al. (2005) Role of phosphoinositide 3-kinase regulatory isoforms in development and actin rearrangement. Mol Cell Biol 25: 2593-2606. doi:10.1128/MCB.25.7.2593-2606.2005. PubMed: 15767666. (Pubitemid 40381624)
41. Zieger K, Wiuf C, Jensen KM, Ørntoft TF, Dyrskjøt L (2009) Chromosomal imbalance in the progression of high-risk non-muscle invasive bladder cancer. BMC Cancer 9: 149. doi:10.1186/1471-2407-9-149. PubMed: 19445696.
42. Simon R, Burger H, Semjonow A, Hertle L, Terpe HJ et al. (2000) Patterns of chromosomal imbalances in muscle invasive bladder cancer. Int J Oncol 17: 1025-1029. PubMed: 11029508.
43. Hurst CD, Platt FM, Taylor CF, Knowles MA (2012) Novel tumor subgroups of urothelial carcinoma of the bladder defined by integrated genomic analysis. Clin Cancer Res 18: 5865-5877. doi:10.1158/1078-0432.CCR-12-1807. PubMed: 22932667.
44. Chen PI, Kong C, Su X, Stahl PD (2009) Rab5 isoforms differentially regulate the trafficking and degradation of epidermal growth factor receptors. J Biol Chem 284: 30328-30338. doi:10.1074/jbc.M109.034546. PubMed: 19723633.
45. Chamberlain MD, Oberg JC, Furber LA, Poland SF, Hawrysh AD et al. (2010) Deregulation of Rab5 and Rab4 proteins in p85R274A-expressing cells alters PDGFR trafficking. Cell Signal 22: 1562-1575. doi:10.1016/j.cellsig.2010.05.025. PubMed: 20570729.
46. Geering B, Cutillas PR, Nock G, Gharbi SI, Vanhaesebroeck B (2007) Class IA phosphoinositide 3-kinases are obligate p85-p110 heterodimers. Proc Natl Acad Sci U S A 104: 7809-7814. doi:10.1073/pnas.0700373104. PubMed: 17470792. (Pubitemid 47185833)
47. Taniguchi CM, Winnay J, Kondo T, Bronson RT, Guimaraes AR et al. (2010) The phosphoinositide 3-kinase regulatory subunit p85alpha can exert tumor suppressor properties through negative regulation of growth factor signaling. Cancer Res 70: 5305-5315. doi:10.1158/0008-5472.CAN-09-3399. PubMed: 20530665.
48. Luo J, Sobkiw CL, Logsdon NM, Watt JM, Signoretti S et al. (2005) Modulation of epithelial neoplasia and lymphoid hyperplasia in PTEN+/-mice by the p85 regulatory subunits of phosphoinositide 3-kinase. Proc Natl Acad Sci U S A 102: 10238-10243. doi:10.1073/pnas.0504378102. PubMed: 16006513. (Pubitemid 41023356)
49. Mellor P, Furber LA, Nyarko JN, Anderson DH (2012) Multiple roles for the p85alpha isoform in the regulation and function of PI3K signalling and receptor trafficking. Biochem J 441: 23-37. doi:10.1042/BJ20111164. PubMed: 22168437.