Co-targeting of the PI3K pathway improves the response of BRCA1 deficient breast cancer cells to PARP1 inhibition

Cancer Letters

Volumn 319, Issue 2, 2012, Pages 232-241

  Kimbung, Siker ^a   Biskup, Ewa ^a,b   Johansson, Ida ^a   Aaltonen, Kristina ^a   Ottosson Wadlund, Astrid ^c   Gruvberger Saal, Sofia ^a   Cunliffe, Heather ^d   Fadeel, Bengt ^c   Loman, Niklas ^a   Berglund, Pontus ^a   Hedenfalk, Ingrid ^a  

^a LUND UNIVERSITY   (Sweden)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c KAROLINSKA INSTITUTE   (Sweden)

^d TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

Author keywords

BRCA1; Breast cancer; PARP1; PI3K; Synergy

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AG 14361; AZD 2881; BRCA1 PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1 INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; RUCAPARIB; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BIOSYNTHESIS; BREAST CANCER; CANCER CELL; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; DRUG POTENTIATION; DRUG TARGETING; ENZYME INHIBITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MACROMOLECULE; PRIORITY JOURNAL;

APOPTOSIS; BRCA1 PROTEIN; BREAST NEOPLASMS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL SURVIVAL; DNA DAMAGE; DRUG THERAPY, COMBINATION; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; POLY(ADP-RIBOSE) POLYMERASES; SIGNAL TRANSDUCTION;

EID: 84859481137     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.01.015     Document Type: Article

References (40)

1. Sorlie T., Tibshirani R., Parker J., Hastie T., Marron J.S., Nobel A., Deng S., Johnsen H., Pesich R., Geisler S., Demeter J., Perou C.M., Lonning P.E., Brown P.O., Borresen-Dale A.L., Botstein D. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl Acad. Sci. USA 2003, 100:8418-8423.
2. Hedenfalk I., Duggan D., Chen Y., Radmacher M., Bittner M., Simon R., Meltzer P., Gusterson B., Esteller M., Kallioniemi O.P., Wilfond B., Borg A., Trent J., Raffeld M., Yakhini Z., Ben-Dor A., Dougherty E., Kononen J., Bubendorf L., Fehrle W., Pittaluga S., Gruvberger S., Loman N., Johannsson O., Olsson H., Sauter G. Gene-expression profiles in hereditary breast cancer. N. Engl. J. Med. 2001, 344:539-548.
3. Teschendorff A.E., Miremadi A., Pinder S.E., Ellis I.O., Caldas C. An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol. 2007, 8:R157.
4. Ame J.C., Spenlehauer C., de Murcia G. The PARP superfamily. BioEssays 2004, 26:882-893.
5. Sandhu S.K., Yap T.A., de Bono J.S. Poly(ADP-ribose) polymerase inhibitors in cancer treatment: a clinical perspective. Eur. J. Cancer 2010, 46:9-20.
6. Bryant H.E., Schultz N., Thomas H.D., Parker K.M., Flower D., Lopez E., Kyle S., Meuth M., Curtin N.J., Helleday T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
7. Farmer H., McCabe N., Lord C.J., Tutt A.N., Johnson D.A., Richardson T.B., Santarosa M., Dillon K.J., Hickson I., Knights C., Martin N.M., Jackson S.P., Smith G.C., Ashworth A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
8. Audeh M.W., Carmichael J., Penson R.T., Friedlander M., Powell B., Bell-McGuinn K.M., Scott C., Weitzel J.N., Oaknin A., Loman N., Lu K., Schmutzler R.K., Matulonis U., Wickens M., Tutt A. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet 2010, 376:245-251.
9. Fong P.C., Boss D.S., Yap T.A., Tutt A., Wu P., Mergui-Roelvink M., Mortimer P., Swaisland H., Lau A., O'Connor M.J., Ashworth A., Carmichael J., Kaye S.B., Schellens J.H., de Bono J.S. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 2009, 361:123-134.
10. Tutt A., Robson M., Garber J.E., Domchek S.M., Audeh M.W., Weitzel J.N., Friedlander M., Arun B., Loman N., Schmutzler R.K., Wardley A., Mitchell G., Earl H., Wickens M., Carmichael J. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet 2010, 376:235-244.
11. Arslan C., Dizdar O., Altundag K. Pharmacotherapy of triple-negative breast cancer. Expert Opin. Pharmacother. 2009, 10:2081-2093.
12. Paez J., Sellers W.R. PI3K/PTEN/AKT pathway. A critical mediator of oncogenic signaling. Cancer Treat. Res. 2003, 115:145-167.
13. Yap T.A., Sandhu S.K., Carden C.P., de Bono J.S. Poly(ADP-ribose) polymerase (PARP) inhibitors: exploiting a synthetic lethal strategy in the clinic. CA Cancer J. Clin. 2011, 61:31-49.
14. Shen W.H., Balajee A.S., Wang J., Wu H., Eng C., Pandolfi P.P., Yin Y. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 2007, 128:157-170.
15. Mendes-Pereira A.M., Martin S.A., Brough R., McCarthy A., Taylor J.R., Kim J.S., Waldman T., Lord C.J., Ashworth A. Synthetic lethal targeting of PTEN mutant cells with PARP inhibitors. EMBO Mol. Med. 2009, 1:315-322.
16. Saal L.H., Gruvberger-Saal S.K., Persson C., Lovgren K., Jumppanen M., Staaf J., Jonsson G., Pires M.M., Maurer M., Holm K., Koujak S., Subramaniyam S., Vallon-Christersson J., Olsson H., Su T., Memeo L., Ludwig T., Ethier S.P., Krogh M., Szabolcs M., Murty V.V., Isola J., Hibshoosh H., Parsons R., Borg A. Recurrent gross mutations of the PTEN tumor suppressor gene in breast cancers with deficient DSB repair. Nat. Genet. 2008, 40:102-107.
17. Xiang T., Ohashi A., Huang Y., Pandita T.K., Ludwig T., Powell S.N., Yang Q. Negative regulation of AKT activation by BRCA1. Cancer Res. 2008, 68:10040-10044.
18. Xiang T., Jia Y., Sherris D., Li S., Wang H., Lu D., Yang Q. Targeting the Akt/mTOR pathway in Brca1-deficient cancers. Oncogene 2011.
19. Elstrodt F., Hollestelle A., Nagel J.H., Gorin M., Wasielewski M., van den Ouweland A., Merajver S.D., Ethier S.P., Schutte M. BRCA1 mutation analysis of 41 human breast cancer cell lines reveals three new deleterious mutants. Cancer Res. 2006, 66:41-45.
20. Johannsson O.T., Staff S., Vallon-Christersson J., Kytola S., Gudjonsson T., Rennstam K., Hedenfalk I.A., Adeyinka A., Kjellen E., Wennerberg J., Baldetorp B., Petersen O.W., Olsson H., Oredsson S., Isola J., Borg A. Characterization of a novel breast carcinoma xenograft and cell line derived from a BRCA1 germ-line mutation carrier. Lab. Invest. 2003, 83:387-396.
21. Turner N., Tutt A., Ashworth A. Hallmarks of 'BRCAness' in sporadic cancers. Nat. Rev. Cancer 2004, 4:814-819.
22. Saal L.H., Holm K., Maurer M., Memeo L., Su T., Wang X., Yu J.S., Malmstrom P.O., Mansukhani M., Enoksson J., Hibshoosh H., Borg A., Parsons R. PIK3CA mutations correlate with hormone receptors, node metastasis, and ERBB2, and are mutually exclusive with PTEN loss in human breast carcinoma. Cancer Res. 2005, 65:2554-2559.
23. Yamatodani T., Ekblad L., Kjellen E., Johnsson A., Mineta H., Wennerberg J. Epidermal growth factor receptor status and persistent activation of Akt and p44/42 MAPK pathways correlate with the effect of cetuximab in head and neck and colon cancer cell lines. J. Cancer Res. Clin. Oncol. 2009, 135:395-402.
24. Chou T.C. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 2006, 58:621-681.
25. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273:5858-5868.
26. Thornthwaite J.T., Sugarbaker E.V., Temple W.J. Preparation of tissues for DNA flow cytometric analysis. Cytometry 1980, 1:229-237.
27. Sun Y., Ottosson A., Pervaiz S., Fadeel B. Smac-mediated sensitization of human B-lymphoma cells to staurosporine- and lactacystin-triggered apoptosis is apoptosome-dependent. Leukemia 2007, 21:1035-1043.
28. Vallon-Christersson J., Nordborg N., Svensson M., Hakkinen J. BASE - 2nd generation software for microarray data management and analysis. BMC Bioinf. 2009, 10:330.
29. The R Project for Statistical Computing . http://www.r-project.org.
30. Workman C., Jensen L.J., Jarmer H., Berka R., Gautier L., Nielser H.B., Saxild H.H., Nielsen C., Brunak S., Knudsen S. A new non-linear normalization method for reducing variability in DNA microarray experiments. Genome Biol. 2002, 3. research0048.
31. Huang da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
32. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
33. Marty B., Maire V., Gravier E., Rigaill G., Vincent-Salomon A., Kappler M., Lebigot I., Djelti F., Tourdes A., Gestraud P., Hupe P., Barillot E., Cruzalegui F., Tucker G.C., Stern M.H., Thiery J.P., Hickman J.A., Dubois T. Frequent PTEN genomic alterations and activated phosphatidylinositol 3-kinase pathway in basal-like breast cancer cells. Breast Cancer Res. 2008, 10:R101.
34. Yu K., Toral-Barza L., Shi C., Zhang W.G., Zask A. Response and determinants of cancer cell susceptibility to PI3K inhibitors: combined targeting of PI3K and Mek1 as an effective anticancer strategy. Cancer Biol. Ther. 2008, 7:307-315.
35. Szanto A., Hellebrand E.E., Bognar Z., Tucsek Z., Szabo A., Gallyas F., Sumegi B., Varbiro G. PARP-1 inhibition-induced activation of PI-3-kinase-Akt pathway promotes resistance to taxol. Biochem. Pharmacol. 2009, 77:1348-1357.
36. Wang Y.A., Johnson S.K., Brown B.L., McCarragher L.M., Al-Sakkaf K., Royds J.A., Dobson P.R. Enhanced anti-cancer effect of a phosphatidylinositol-3 kinase inhibitor and doxorubicin on human breast epithelial cell lines with different p53 and oestrogen receptor status. Int. J. Cancer 2008, 123:1536-1544.
37. Drew Y., Mulligan E.A., Vong W.T., Thomas H.D., Kahn S., Kyle S., Mukhopadhyay A., Los G., Hostomsky Z., Plummer E.R., Edmondson R.J., Curtin N.J. Therapeutic potential of poly(ADP-ribose) polymerase inhibitor AG014699 in human cancers with mutated or methylated BRCA1 or BRCA2. J. Natl Cancer Inst. 2010, 103:334-346.
38. Lehmann B.D., Bauer J.A., Chen X., Sanders M.E., Chakravarthy A.B., Shyr Y., Pietenpol J.A. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Invest. 2011, 121:2750-2767.
39. Turner N.C., Ashworth A. Biomarkers of PARP inhibitor sensitivity. Breast Cancer Res. Treat. 2011, 127:283-286.
40. Rottenberg S., Jaspers J.E., Kersbergen A., van der Burg E., Nygren A.O., Zander S.A., Derksen P.W., de Bruin M., Zevenhoven J., Lau A., Boulter R., Cranston A., O'Connor M.J., Martin N.M., Borst P., Jonkers J. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc. Natl. Acad. Sci. USA 2008, 105:17079-17084.