PRKACA mediates resistance to HER2-targeted therapy in breast cancer cells and restores anti-apoptotic signaling

Oncogene

Volumn 34, Issue 16, 2014, Pages 2061-2071

  Moody, S E ^a,b,c   Schinzel, A C ^a   Singh, S ^a   Izzo, F ^a   Strickland, M R ^a   Luo, L ^a,b   Thomas, S R ^c   Boehm, J S ^c   Kim, S Y ^d   Wang, Z C ^a,b   Hahn, W C ^a,b,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BAD PROTEIN, HUMAN; BCL2L1 PROTEIN, HUMAN; CYCLIC AMP DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; LAPATINIB; MITOGEN ACTIVATED PROTEIN KINASE; MONOCLONAL ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; PIM1 PROTEIN, HUMAN; PRKACA PROTEIN, HUMAN; PROTEIN BAD; PROTEIN BCL X; PROTEIN KINASE INHIBITOR; PROTEIN KINASE PIM 1; QUINAZOLINE DERIVATIVE; TRASTUZUMAB;

ANTAGONISTS AND INHIBITORS; APOPTOSIS; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION PROFILING; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; OPEN READING FRAME; PHOSPHORYLATION; PHYSIOLOGY;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; BCL-X PROTEIN; BREAST NEOPLASMS; CYCLIC AMP-DEPENDENT PROTEIN KINASE CATALYTIC SUBUNITS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION PROFILING; HEK293 CELLS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; OPEN READING FRAMES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-PIM-1; QUINAZOLINES; RECEPTOR, ERBB-2; TRASTUZUMAB;

EID: 84939885519     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.153     Document Type: Article

References (42)

1. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987; 235: 177-182.
2. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989; 244: 707-712.
3. Blackwell KL, Pegram MD, Tan-Chiu E, Schwartzberg LS, Arbushites MC, Maltzman JD et al. Single-agent lapatinib for HER2-overexpressing advanced or metastatic breast cancer that progressed on first- or second-line trastuzumab-containing regimens. Ann Oncol 2009; 20: 1026-1031.
4. Cobleigh MA, Vogel CL, Tripathy D, Robert NJ, Scholl S, Fehrenbacher L et al. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J Clin Oncol 1999; 17: 2639-2648.
5. Vogel C, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L et al. First-line, single-agent Herceptin(R) (trastuzumab) in metastatic breast cancer. a preliminary report. Eur J Cancer 2001; 37: 25-29.
6. Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L et al. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 2002; 20: 719-726.
7. Piccart-Gebhart MJ, Procter M, Leyland-Jones B, Goldhirsch A, Untch M, Smith I et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 2005; 353: 1659-1672.
8. Xia W, Liu LH, Ho P, Spector NL. Truncated ErbB2 receptor (p95ErbB2) is regulated by heregulin through heterodimer formation with ErbB3 yet remains sensitive to the dual EGFR/ErbB2 kinase inhibitor GW572016. Oncogene 2004; 23: 646-653.
9. Wehrman TS, Raab WJ, Casipit CL, Doyonnas R, Pomerantz JH, Blau HM. A system for quantifying dynamic protein interactions defines a role for Herceptin in modulating ErbB2 interactions. Proc Natl Acad Sci USA 2006; 103: 19063-19068.
10. Nahta R, Yuan LX, Du Y, Esteva FJ. Lapatinib induces apoptosis in trastuzumabresistant breast cancer cells: effects on insulin-like growth factor I signaling. Mol Cancer Ther 2007; 6: 667-674.
11. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA et al. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 2004; 6: 117-127.
12. Berns K, Horlings HM, Hennessy BT, Madiredjo M, Hijmans EM, Beelen K et al. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 2007; 12: 395-402.
13. Kataoka Y, Mukohara T, Shimada H, Saijo N, Hirai M, Minami H. Association between gain-of-function mutations in PIK3CA and resistance to HER2-targeted agents in HER2-amplified breast cancer cell lines. Ann Oncol 2010; 21: 255-262.
14. Esteva FJ, Guo H, Zhang S, Santa-Maria C, Stone S, Lanchbury JS et al. PTEN, PIK3CA, p-AKT, and p-p70S6K status: association with trastuzumab response and survival in patients with HER2-positive metastatic breast cancer. Am J Pathol 2010; 177: 1647-1656.
15. Dave B, Migliaccio I, Gutierrez MC, Wu MF, Chamness GC, Wong H et al. Loss of phosphatase and tensin homolog or phosphoinositol-3 kinase activation and response to trastuzumab or lapatinib in human epidermal growth factor receptor 2-overexpressing locally advanced breast cancers. J Clin Oncol 2011; 29: 166-173.
16. Scaltriti M, Eichhorn PJ, Cortes J, Prudkin L, Aura C, Jimenez J et al. Cyclin E amplification/overexpression is a mechanism of trastuzumab resistance in HER2+ breast cancer patients. Proc Natl Acad Sci USA 2011; 108: 3761-3766.
17. Zhang S, Huang WC, Li P, Guo H, Poh SB, Brady SW et al. Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat Med 2011; 17: 461-469.
18. Eichhorn PJ, Gili M, Scaltriti M, Serra V, Guzman M, Nijkamp W et al. Phosphatidylinositol 3-kinase hyperactivation results in lapatinib resistance that is reversed by the mTOR/phosphatidylinositol 3-kinase inhibitor NVP-BEZ235. Cancer Res 2008; 68: 9221-9230.
19. Jegg AM, Ward TM, Iorns E, Hoe N, Zhou J, Liu X et al. PI3K independent activation of mTORC1 as a target in lapatinib-resistant ERBB2+ breast cancer cells. Breast Cancer Res Treat 2012; 136: 683-692.
20. Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 2010; 468: 968-972.
21. Wu C, Miloslavskaya I, Demontis S, Maestro R, Galaktionov K. Regulation of cellular response to oncogenic and oxidative stress by Seladin-1. Nature 2004; 432: 640-645.
22. Vegran F, Boidot R, Coudert B, Fumoleau P, Arnould L, Garnier J et al. Gene expression profile and response to trastuzumab-docetaxel-based treatment in breast carcinoma. Br J Cancer 2009; 101: 1357-1364.
23. Baselga J, Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 2009; 9: 463-475.
24. Hino S, Tanji C, Nakayama KI, Kikuchi A. Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase stabilizes beta-catenin through inhibition of its ubiquitination. Mol Cell Biol 2005; 25: 9063-9072.
25. Taurin S, Sandbo N, Qin Y, Browning D, Dulin NO. Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase. J Biol Chem 2006; 281: 9971-9976.
26. Harada H, Becknell B, Wilm M, Mann M, Huang LJ, Taylor SS et al. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol Cell 1999; 3: 413-422.
27. Lizcano JM, Morrice N, Cohen P. Regulation of BAD by cAMP-dependent protein kinase is mediated via phosphorylation of a novel site, Ser155. Biochem J 2000; 349: 547-557.
28. Danial NN. BAD: undertaker by night, candyman by day. Oncogene 2008; 27: S53-S70.
29. Fang X, Yu SX, Lu Y, Bast RC Jr., Woodgett JR, Mills G. Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci USA 2000; 97: 11960-11965.
30. Iyer GH, Moore MJ, Taylor SS. Consequences of lysine 72 mutation on the phosphorylation and activation state of cAMP-dependent kinase. J Biol Chem 2005; 280: 8800-8807.
31. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 2006; 355: 2733-2743.
32. Baselga J, Cortes J, Kim SB, Im SA, Hegg R, Im YH et al. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med 2012; 366: 109-119.
33. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001; 344: 783-792.
34. Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012; 367: 1783-1791.
35. Fleming GF, Ma CX, Huo D, Sattar H, Tretiakova M, Lin L et al. Phase II trial of temsirolimus in patients with metastatic breast cancer. Breast Cancer Res Treat 2012; 136: 355-363.
36. Morrow PK, Wulf GM, Ensor J, Booser DJ, Moore JA, Flores PR et al. Phase I/II study of trastuzumab in combination with everolimus (RAD001) in patients with HER2-overexpressing metastatic breast cancer who progressed on trastuzumab-based therapy. J Clin Oncol 2011; 29: 3126-3132.
37. Gu L, Lau SK, Loera S, Somlo G, Kane SE. Protein kinase A activation confers resistance to trastuzumab in human breast cancer cell lines. Clin Cancer Res 2009; 15: 7196-7206.
38. Beristain AG, Molyneux SD, Joshi PA, Pomroy NC, Di Grappa MA, Chang MC et al. PKA signaling drives mammary tumorigenesis through Src. Oncogene 2015; 34: 1160-1173.
39. Beuschlein F, Fassnacht M, Assie G, Calebiro D, Stratakis CA, Osswald A et al. Constitutive activation of PKA catalytic subunit in adrenal Cushing's syndrome. N Engl J Med 2014; 370: 1019-1028.
40. Cao Y, He M, Gao Z, Peng Y, Li Y, Li L et al. Activating Hotspot L205R Mutation in PRKACA and Adrenal Cushing's Syndrome. Science 2014; 344: 913-917.
41. Honeyman JN, Simon EP, Robine N, Chiaroni-Clarke R, Darcy DG, Lim II et al. Detection of a recurrent DNAJB1-PRKACA chimeric transcript in fibrolamellar hepatocellular carcinoma. Science 2014; 343: 1010-1014.
42. Vaillant F, Merino D, Lee L, Breslin K, Pal B, Ritchie ME et al. Targeting BCL-2 with the BH3 mimetic ABT-199 in estrogen receptor-positive breast cancer. Cancer Cell 2013; 24: 120-129.