Conditional activation of Pik3ca H1047R in a knock-in mouse model promotes mammary tumorigenesis and emergence of mutations

Oncogene

Volumn 32, Issue 3, 2013, Pages 318-326

  Yuan, W ^a   Stawiski, E ^a   Janakiraman, V ^a   Chan, E ^a   Durinck, S ^a   Edgar, K A ^a   Kljavin, N M ^a   Rivers, C S ^a   Gnad, F ^a   Roose Girma, M ^a   Haverty, P M ^a   Fedorowicz, G ^a   Heldens, S ^a   Soriano, R H ^a   Zhang, Z ^a   Wallin, J J ^a   Johnson, L ^a   Merchant, M ^a   Modrusan, Z ^a   Stern, H M ^a   Seshagiri, S ^a   more..

^a GENENTECH INC   (United States)

Author keywords

exome sequencing; H1047R; knock in; mammary gland; Pik3ca; Trp53

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PICTILISIB;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST ADENOCARCINOMA; CARCINOGENESIS; CONTROLLED STUDY; EXOME; FEMALE; GENE ACTIVATION; GENE MUTATION; GENE TARGETING; HISTOPATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADENOCARCINOMA; ALLELES; ANIMALS; BASE SEQUENCE; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCK-IN TECHNIQUES; GENOMICS; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MUTATION; ORGAN SPECIFICITY; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84872613150     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.53     Document Type: Article

References (53)

1. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002; 296: 1655-1657.
2. Hawkins PT, Anderson KE, Davidson K, Stephens LR. Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans 2006; 34: 647-662.
3. Vanhaesebroeck B, Ali K, Bilancio A, Geering B, Foukas LC. Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem Sci 2005; 30: 194-204.
4. Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 2004; 304: 554.
5. Bachman KE, Argani P, Samuels Y, Silliman N, Ptak J, Szabo S et al. The PIK3CA gene is mutated with high frequency in human breast cancers. Cancer Biol Ther 2004; 3: 772-775.
6. Lee JW, Soung YH, Kim SY, Lee HW, Park WS, Nam SW et al. PIK3CA gene is frequently mutated in breast carcinomas and hepatocellular carcinomas. Oncogene 2004; 24: 1477-1480.
7. Bader AG, Kang S, Zhao L, Vogt PK. Oncogenic PI3K deregulates transcription and translation. Nat Rev Cancer 2005; 5: 921-929.
8. Zhao L, Vogt PK. Helical domain and kinase domain mutations in p110alpha of phosphatidylinositol 3-kinase induce gain of function by different mechanisms. Proc Natl Acad Sci USA 2008; 105: 2652-2657.
9. Zhao L, Vogt PK. Class I PI3K in oncogenic cellular transformation. Oncogene 2008; 27: 5486-5496.
10. Isakoff SJ. Breast cancer-associated PIK3CA mutations are oncogenic in mammary epithelial cells. Cancer Res 2005; 65: 10992-11000.
11. Bader AG. Cancer-specific mutations in PIK3CA are oncogenic in vivo. Proc Natl Acad Sci USA 2006; 103: 1475-1479.
12. Horn S, Bergholz U, Jücker M, McCubrey JA, Trümper L, Stocking C et al. Mutations in the catalytic subunit of class IA PI3K confer leukemogenic potential to hematopoietic cells. Oncogene 2008; 27: 4096-4106.
13. Walrath JC, Hawes JJ, Van Dyke T, Reilly KM. Genetically engineered mouse models in cancer research. Adv Cancer Res 2010; 106: 113-164.
14. Singh M, Lima A, Molina R, Hamilton P, Clermont AC, Devasthali V et al. Assessing therapeutic responses in Kras mutant cancers using genetically engineered mouse models. Nat Biotechnol 2010; 28: 585-593.
15. Engelman JA, Chen L, Tan X, Crosby K, Guimaraes AR, Upadhyay R et al. Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers. Nat Med 2008; 14: 1351-1356.
16. Adams JR, Xu K, Liu JC, Agamez NMR, Loch AJ, Wong RG et al. Cooperation between Pik3ca and p53 mutations in mouse mammary tumor formation. Cancer Res 2011; 71: 2706-2717.
17. Meyer DS, Brinkhaus H, Muller U, Muller M, Cardiff RD, Bentires-Alj M. Luminal expression of PIK3CA mutant H1047R in the mammary gland induces heterogeneous tumors. Cancer Res 2011; 71: 4344-4351.
18. Liu P, Cheng H, Santiago S, Raeder M, Zhang F, Isabella A et al. Oncogenic PIK3CAdriven mammary tumors frequently recur via PI3K pathway-dependent and PI3K pathway-independent mechanisms. Nat Med 2011; 17: 1116-1120.
19. Shah SP, Morin RD, Khattra J, Prentice L, Pugh T, Burleigh A et al. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 2009; 461: 809-813.
20. Ding L, Ellis MJ, Li S, Larson DE, Chen K, Wallis JW et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010; 464: 999-1005.
21. Bi L, Okabe I, Bernard DJ, Wynshaw-Boris A, Nussbaum RL. Proliferative defect and embryonic lethality in mice homozygous for a deletion in the p110alpha subunit of phosphoinositide 3-kinase. J Biol Chem 1999; 274: 10963-10968.
22. Wagner KU, Wall RJ, St-Onge L, Gruss P, Wynshaw-Boris A, Garrett L et al. Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res 1997; 25: 4323-4330.
23. Wagner KU, McAllister K, Ward T, Davis B, Wiseman R, Hennighausen L. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res 2001; 10: 545-553.
24. Li G, Robinson GW, Lesche R, Martinez-Diaz H, Jiang Z, Rozengurt N et al. Conditional loss of PTEN leads to precocious development and neoplasia in the mammary gland. Development 2002; 129: 4159-4170.
25. Fishler T, Li YY, Wang RH, Kim HS, Sengupta K, Vassilopoulos A et al. Genetic instability and mammary tumor formation in mice carrying mammary-specific disruption of Chk1 and p53. Oncogene 2010; 29: 4007-4017.
26. Tiede B, Kang Y. From milk to malignancy: the role of mammary stem cells in development, pregnancy and breast cancer. Cell Res 2011; 21: 245-257.
27. Khan H. Spindle cell carcinoma of the breast: a case series of a rare histological subtype. Eur J Surg Oncol 2003; 29: 600-603.
28. Carter MR, Hornick JL, Lester S, Fletcher CD. Spindle cell (sarcomatoid) carcinoma of the breast: a clinicopathologic and immunohistochemical analysis of 29 cases. Am J Surg Pathol 2006; 30: 300-309.
29. Weigelt B, Reis-Filho JS. Histological and molecular types of breast cancer: is there a unifying taxonomy? Nat Rev Clin Oncol 2009; 6: 718-730.
30. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J et al. Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci USA 2010; 107: 15449-15454.
31. Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011; 469: 539-542.
32. Olivier M, Hollstein M, Hainaut P. TP53 mutations in human cancers: origins, consequences, and clinical use. Cold Spring Harb Perspect Biol 2010; 2: a001008.
33. Amikura T, Sekine M, Hirai Y, Fujimoto S, Hatae M, Kobayashi I et al. Mutational analysis of TP53 and p21 in familial and sporadic ovarian cancer in Japan. Gynecol Oncol 2006; 100: 365-371.
34. Grochova D, Vankova J, Damborsky J, Ravcukova B, Smarda J, Vojtesek B et al. Analysis of transactivation capability and conformation of p53 temperaturedependent mutants and their reactivation by amifostine in yeast. Oncogene 2007; 27: 1243-1252.
35. Ng PC, Henikoff S. Accounting for human polymorphisms predicted to affect protein function. Genome Res 2002; 12: 436-446.
36. Ramensky V, Bork P, Sunyaev S. Human non-synonymous SNPs: server and survey. Nucleic Acids Res 2002; 30: 3894-3900.
37. Stephens P, Edkins S, Davies H, Greenman C, Cox C, Hunter C et al. A screen of the complete protein kinase gene family identifies diverse patterns of somatic mutations in human breast cancer. Nat Genet 2005; 37: 590-592.
38. Folkes A, Shuttleworth S, Chuckowree I, Oxenford S, Wan NC, Castanedo G et al. Preparation of thienopyrimidines and furopyrimidines as lipid kinase inhibitors for treating cancer and other diseases. PCT Int Appl 2007; 206. CODEN: PIXXD2 WO 2007127175. A2 20071108.
39. Salphati L, Wong H, Belvin M, Bradford D, Edgar KA, Prior WW et al. Pharmacokinetic-pharmacodynamic modeling of tumor growth inhibition and biomarker modulation by the novel phosphatidylinositol 3-kinase inhibitor GDC-0941. Drug Metab Dispos 2010; 38: 1436-1442.
40. Tuveson D, Hanahan D. Translational medicine: cancer lessons from mice to humans. Nature 2011; 471: 316-317.
41. Hennessy BT, Gonzalez-Angulo AM, Stemke-Hale K, Gilcrease MZ, Krishnamurthy S, Lee JS et al. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res 2009; 69: 4116-4124.
42. Stratton MR, Campbell PJ, Futreal PA. The cancer genome. Nature 2009; 458: 719-724.
43. Boyault S, Drouet Y, Navarro C, Bachelot T, Lasset C, Treilleux I et al. Mutational characterization of individual breast tumors: TP53 and PI3K pathway genes are frequently and distinctively mutated in different subtypes. Breast Cancer Res Treat 2011; 132: 29-39.
44. Hynes NE, Dey JH. PI3K inhibition overcomes trastuzumab resistance: blockade of ErbB2/ErbB3 is not always enough. Cancer Cell 2009; 15: 353-355.
45. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001; 15: 3243-3248.
46. Ullman-Cullere MH, Foltz CJ. Body condition scoring: a rapid and accurate method for assessing health status in mice. Lab Anim Sci 1999; 49: 319-323.
47. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3: Article 3.
48. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods 2003; 31: 265-273.
49. Hupe P, Stransky N, Thiery JP, Radvanyi F, Barillot E. Analysis of array CGH data: from signal ratio to gain and loss of DNA regions. Bioinformatics 2004; 20: 3413-3422.
50. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25: 1754-1760.
51. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011; 43: 491-498.
52. Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM et al. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res 2001; 29: 308-311.
53. Pinheiro J, Bates D, DebRoy S, Sarkar D. nlme: linear and nonlinear mixed effects models. R Package Version 2008; 3: 1-89.