Abstract
Mutations in the gene encoding the p110α subunit of PI3K (PIK3CA) that result in enhanced PI3K activity are frequently observed in human cancers. To better understand the role of mutant PIK3CA in the initiation or progression of tumorigenesis, we generated mice in which a PIK3CA mutation commonly detected in human cancers (the H1047R mutation) could be conditionally knocked into the endogenous Pik3ca locus. Activation of this mutation in the mouse ovary revealed that alone, Pik3caH1047R induced premalignant hyperplasia of the ovarian surface epithelium but no tumors. Concomitantly, we analyzed several human ovarian cancers and found PIK3CA mutations coexistent with KRAS and/or PTEN mutations, raising the possibility that a secondary defect in a co-regulator of PI3K activity may be required for mutant PIK3CA to promote transformation. Consistent with this notion, we found that Pik3caH1047R mutation plus Pten deletion in the mouse ovary led to the development of ovarian serous adenocarcinomas and granulosa cell tumors. Both mutational events were required for early, robust Akt activation. Pharmacological inhibition of PI3K/mTOR in these mice delayed tumor growth and prolonged survival. These results demonstrate that the Pik3caH1047R mutation with loss of Pten is enough to promote ovarian cell transformation and that we have developed a model system for studying possible therapies.
MeSH Terms
Animals
Cell Transformation, Neoplastic/genetics
Class I Phosphatidylinositol 3-Kinases
Female
Humans
Mice
Mice, Inbred BALB C
Mice, Inbred C57BL
Mutation
Ovarian Neoplasms/genetics,pathology
Ovary/anatomy & histology,pathology
PTEN Phosphohydrolase/deficiency,genetics,metabolism
Phosphatidylinositol 3-Kinases/genetics,metabolism
Survival Rate
Chemicals
Phosphatidylinositol 3-Kinases
Class I Phosphatidylinositol 3-Kinases
PIK3CA protein, human
Pik3ca protein, mouse
PTEN Phosphohydrolase
PTEN protein, human
Pten protein, mouse
Authors & Affiliations
21 authors, click to expand affiliations / ORCID
Kinross Kathryn M
Cancer Research Division, Peter MacCallum Cancer Centre (Peter Mac), East Melbourne, Victoria, Australia.
Montgomery Karen G
Kleinschmidt Margarete
Waring Paul
Ivetac Ivan
Tikoo Anjali
Saad Mirette
Hare Lauren
Roh Vincent
Mantamadiotis Theo
Sheppard Karen E
Ryland Georgina L
Campbell Ian G
Gorringe Kylie L
Christensen James G
Cullinane Carleen
Hicks Rodney J
Pearson Richard B
Johnstone Ricky W
McArthur Grant A
Phillips Wayne A
References (28)
28 references, click to expand
-
Identification of candidate growth promoting genes in ovarian cancer through integrated copy number and expression analysis.
PLoS One. 2010 Apr 08;5(4):e9983
PMID: 20386695
-
PIK3CA is implicated as an oncogene in ovarian cancer.
Nat Genet. 1999 Jan;21(1):99-102
PMID: 9916799
-
Conditional inactivation of Brca1, p53 and Rb in mouse ovaries results in the development of leiomyosarcomas.
PLoS One. 2009 Dec 31;4(12):e8534
PMID: 20046869
-
Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo.
Science. 2001 Dec 7;294(5549):2186-9
PMID: 11691952
-
Mutation of the PIK3CA gene in ovarian and breast cancer.
Cancer Res. 2004 Nov 1;64(21):7678-81
PMID: 15520168
-
Integrated genomic analyses of ovarian carcinoma.
Nature. 2011 Jun 29;474(7353):609-15
PMID: 21720365
-
PI3K pathway alterations in cancer: variations on a theme.
Oncogene. 2008 Sep 18;27(41):5497-510
PMID: 18794884
-
Expression of activated PIK3CA in ovarian surface epithelium results in hyperplasia but not tumor formation.
PLoS One. 2009;4(1):e4295
PMID: 19172191
-
Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice.
Cell. 2007 Jun 1;129(5):957-68
PMID: 17540175
-
AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth.
Oncogene. 2004 Jul 29;23(34):5853-7
PMID: 15208673
-
High frequency of mutations of the PIK3CA gene in human cancers.
Science. 2004 Apr 23;304(5670):554
PMID: 15016963
-
The biology of ovarian cancer: new opportunities for translation.
Nat Rev Cancer. 2009 Jun;9(6):415-28
PMID: 19461667
-
The molecular genetic basis of ovarian cancer and its roadmap towards a better treatment.
Gynecol Oncol. 2010 May;117(2):358-65
PMID: 20207398
-
Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium.
Cancer Res. 2003 Jul 1;63(13):3459-63
PMID: 12839925
-
Cooperation between Pik3ca and p53 mutations in mouse mammary tumor formation.
Cancer Res. 2011 Apr 1;71(7):2706-17
PMID: 21324922
-
Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene.
Science. 1997 Oct 3;278(5335):120-3
PMID: 9311916
-
Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers.
Nat Med. 2008 Dec;14(12):1351-6
PMID: 19029981
-
Large-scale genomic analysis of ovarian carcinomas.
Mol Oncol. 2009 Apr;3(2):157-64
PMID: 19383377
-
In vivo activity of combined PI3K/mTOR and MEK inhibition in a Kras(G12D);Pten deletion mouse model of ovarian cancer.
Mol Cancer Ther. 2011 Aug;10(8):1440-9
PMID: 21632463
-
Mouse model of human ovarian endometrioid adenocarcinoma based on somatic defects in the Wnt/beta-catenin and PI3K/Pten signaling pathways.
Cancer Cell. 2007 Apr;11(4):321-33
PMID: 17418409
-
Class I PI3K in oncogenic cellular transformation.
Oncogene. 2008 Sep 18;27(41):5486-96
PMID: 18794883
-
Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer.
Nat Med. 2005 Jan;11(1):63-70
PMID: 15619626
-
Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras.
Cell. 1997 May 2;89(3):457-67
PMID: 9150145
-
Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras.
Genes Dev. 2001 Dec 15;15(24):3243-8
PMID: 11751630
-
Luminal expression of PIK3CA mutant H1047R in the mammary gland induces heterogeneous tumors.
Cancer Res. 2011 Jul 1;71(13):4344-51
PMID: 21482677
-
Oncogenic PIK3CA-driven mammary tumors frequently recur via PI3K pathway-dependent and PI3K pathway-independent mechanisms.
Nat Med. 2011 Aug 07;17(9):1116-20
PMID: 21822287
-
PTEN expression in clear cell adenocarcinoma of the ovary.
Gynecol Oncol. 2006 Apr;101(1):71-5
PMID: 16290000
-
PI(3)king apart PTEN's role in cancer.
Clin Cancer Res. 2010 Sep 1;16(17):4325-30
PMID: 20622047