PI3K-targeted therapy can be evaded by gene amplification along the MYC-eukaryotic translation initiation factor 4E (eIF4E) axis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 37, 2011, Pages

  Ilic, Nina ^a   Utermark, Tamara ^a   Widlund, Hans R ^b   Roberts, Thomas M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (1 CYANO 1 METHYLETHYL) 3 METHYL 8 (3 QUINOLINYL)IMIDAZO[4,5 C]QUINOLIN 2(1H,3H) ONE; INITIATION FACTOR 4E; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE;

ALLELE; ARTICLE; BREAST EPITHELIUM; CANCER CELL; CELL PROLIFERATION; COMPARATIVE STUDY; DRUG EFFICACY; DRUG TARGETING; GENE AMPLIFICATION; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EUKARYOTIC INITIATION FACTOR-4E; FEMALE; GENE AMPLIFICATION; GENE DOSAGE; GENOME, HUMAN; HUMANS; IMIDAZOLES; MOLECULAR TARGETED THERAPY; PHOSPHATIDYLINOSITOL 3-KINASES; POINT MUTATION; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-MYC; QUINOLINES; RNA CAPS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; UP-REGULATION;

EUKARYOTA;

EID: 80053070033     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1108237108     Document Type: Article

References (52)

1. Yuan TL, Cantley LC (2008) PI3K pathway alterations in cancer: Variations on a theme. Oncogene 27:5497-5510.
2. Samuels Y, et al. (2005) Mutant PIK3CA promotes cell growth and invasion of human cancer cells. Cancer Cell 7:561-573. (Pubitemid 40799249)
3. Samuels Y, et al. (2004) High frequency of mutations of the PIK3CA gene in human cancers. Science 304:554. (Pubitemid 38541907)
4. Engelman JA, Luo J, Cantley LC (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7:606-619. (Pubitemid 44100518)
5. Sauter G, Maeda T, Waldman FM, Davis RL, Feuerstein BG (1996) Patterns of epidermal growth factor receptor amplification in malignant gliomas. Am J Pathol 148:1047-1053. (Pubitemid 26108242)
6. Tornillo L, Terracciano LM (2006) An update on molecular genetics of gastrointestinal stromal tumours. J Clin Pathol 59:557-563. (Pubitemid 43886037)
7. Moasser MM (2007) The oncogene HER2: Its signaling and transforming functions and its role in human cancer pathogenesis. Oncogene 26:6469-6487.
8. Keniry M, Parsons R (2008) The role of PTEN signaling perturbations in cancer and in targeted therapy. Oncogene 27:5477-5485.
9. Serra V, et al. (2008) NVP-BEZ235, a dual PI3K/mTOR inhibitor, prevents PI3K signaling and inhibits the growth of cancer cells with activating PI3K mutations. Cancer Res 68: 8022-8030.
10. Junttila TT, et al. (2009) Ligand-independent HER2/HER3/PI3K complex is disrupted by trastuzumab and is effectively inhibited by the PI3K inhibitor GDC-0941. Cancer Cell 15:429-440.
11. Kong D, Yamori T (2009) Advances in development of phosphatidylinositol 3-kinase inhibitors. Curr Med Chem 16:2839-2854.
12. Gorre ME, et al. (2001) Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293:876-880. (Pubitemid 32743979)
13. Shah NP, et al. (2002) Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2:117-125. (Pubitemid 41039112)
14. Engelman JA, et al. (2007) MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316:1039-1043. (Pubitemid 46799492)
15. Turke AB, et al. (2010) Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 17:77-88.
16. Nagata Y, et al. (2004) PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 6:117-127. (Pubitemid 39485684)
17. Berns K, et al. (2007) A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 12:395-402. (Pubitemid 47539306)
18. Zhao JJ, et al. (2005) The oncogenic properties of mutant p110alpha and p110beta phosphatidylinositol 3-kinases in human mammary epithelial cells. Proc Natl Acad Sci USA 102:18443-18448. (Pubitemid 43011245)
19. Meyerson M, et al. (1997) hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90:785-795. (Pubitemid 27357969)
20. Shaulian E, Zauberman A, Ginsberg D, Oren M (1992) Identification of a minimal transforming domain of p53: Negative dominance through abrogation of sequence-specific DNA binding. Mol Cell Biol 12:5581-5592.
21. Yun CH, et al. (2008) The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci USA 105:2070-2075. (Pubitemid 351439466)
22. Azam M, Latek RR, Daley GQ (2003) Mechanisms of autoinhibition and STI-571/imatinib resistance revealed by mutagenesis of BCR-ABL. Cell 112:831-843. (Pubitemid 36378885)
23. Zhu J, Blenis J, Yuan J (2008) Activation of PI3K/Akt and MAPK pathways regulates Myc-mediated transcription by phosphorylating and promoting the degradation of Mad1. Proc Natl Acad Sci USA 105:6584-6589. (Pubitemid 351754550)
24. Chen Y, Olopade OI (2008) MYC in breast tumor progression. Expert Rev Anticancer Ther 8:1689-1698.
25. Bild AH, et al. (2006) Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 439:353-357. (Pubitemid 43128862)
26. Wolfer A, et al. (2010) MYC regulation of a "poor-prognosis" metastatic cancer cell state. Proc Natl Acad Sci USA 107:3698-3703.
27. Obaya AJ, Mateyak MK, Sedivy JM (1999) Mysterious liaisons: The relationship between c-Myc and the cell cycle. Oncogene 18:2934-2941. (Pubitemid 29276534)
28. Zunder ER, Knight ZA, Houseman BT, Apsel B, Shokat KM (2008) Discovery of drugresistant and drug-sensitizing mutations in the oncogenic PI3K isoform p110 alpha. Cancer Cell 14:180-192.
29. Folkes AJ, et al. (2008) The identification of 2-(1H-indazol-4-yl)-6-(4- methanesulfonyl-piperazin- 1-ylmethyl)-4-morpholin-4-yl-thieno[3,2-d]pyrimidine (GDC-0941) as a potent, selective, orally bioavailable inhibitor of class I PI3 kinase for the treatment of cancer. J Med Chem 51:5522-5532.
30. García-Martínez JM, et al. (2009) Ku-0063794 is a specific inhibitor of the mammalian target of rapamycin (mTOR). Biochem J 421:29-42.
31. Martin KA, Blenis J (2002) Coordinate regulation of translation by the PI 3-kinase and mTOR pathways. Adv Cancer Res 86:1-39.
32. Jones RM, et al. (1996) An essential E box in the promoter of the gene encoding the mRNA cap-binding protein (eukaryotic initiation factor 4E) is a target for activation by c-myc. Mol Cell Biol 16:4754-4764. (Pubitemid 26272129)
33. Schmidt EV (2004) The role of c-myc in regulation of translation initiation. Oncogene 23:3217-3221.
34. Rosenwald IB, Rhoads DB, Callanan LD, Isselbacher KJ, Schmidt EV (1993) Increased expression of eukaryotic translation initiation factors eIF-4E and eIF-2 alpha in response to growth induction by c-myc. Proc Natl Acad Sci USA 90:6175-6178. (Pubitemid 23191477)
35. Watson JD, Oster SK, Shago M, Khosravi F, Penn LZ (2002) Identifying genes regulated in a Myc-dependent manner. J Biol Chem 277:36921-36930.
36. Krüger M, et al. (2001) Involvement of proteasome alpha-subunit PSMA7 in hepatitis C virus internal ribosome entry site-mediated translation. Mol Cell Biol 21:8357-8364. (Pubitemid 33108596)
37. Druker BJ, et al. (2001) Activity of a specific inhibitor of the BCR-ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome. N Engl J Med 344:1038-1042. (Pubitemid 32267973)
38. Demetri GD, et al. (2002) Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 347:472-480. (Pubitemid 34879334)
39. Inoue A, et al. (2006) Prospective phase II study of gefitinib for chemotherapy-naive patients with advanced non-small-cell lung cancer with epidermal growth factor receptor gene mutations. J Clin Oncol 24:3340-3346. (Pubitemid 46638887)
40. Sequist LV, et al. (2008) First-line gefitinib in patients with advanced non-small-cell lung cancer harboring somatic EGFR mutations. J Clin Oncol 26:2442-2449.
41. Mok TS, et al. (2009) Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 361:947-957.
42. Lazaris-Karatzas A, Sonenberg N (1992) The mRNA 5′ cap-binding protein, eIF-4E, cooperates with v-myc or E1A in the transformation of primary rodent fibroblasts. Mol Cell Biol 12:1234-1238.
43. Ruggero D, et al. (2004) The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat Med 10:484-486. (Pubitemid 38667906)
44. Johnston LA, Prober DA, Edgar BA, Eisenman RN, Gallant P (1999) Drosophila myc regulates cellular growth during development. Cell 98:779-790. (Pubitemid 29446895)
45. Smith MR, et al. (1990) Translation initiation factors induce DNA synthesis and transform NIH 3T3 cells. New Biol 2:648-654. (Pubitemid 20330918)
46. Rosenwald IB, Lazaris-Karatzas A, Sonenberg N, Schmidt EV (1993) Elevated levels of cyclin D1 protein in response to increased expression of eukaryotic initiation factor 4E. Mol Cell Biol 13:7358-7363. (Pubitemid 23354259)
47. Shantz LM, Pegg AE (1994) Overproduction of ornithine decarboxylase caused by relief of translational repression is associated with neoplastic transformation. Cancer Res 54:2313-2316. (Pubitemid 24138716)
48. Sorrells DL, et al. (1998) Detection of eIF4E gene amplification in breast cancer by competitive PCR. Ann Surg Oncol 5:232-237. (Pubitemid 28249313)
49. Kiyono T, et al. (1998) Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 396:84-88. (Pubitemid 28520454)
50. Zhao JJ, et al. (2003) Human mammary epithelial cell transformation through the activation of phosphatidylinositol 3-kinase. Cancer Cell 3:483-495. (Pubitemid 38340295)
51. WhitmanM, Downes CP, Keeler M, Keller T, Cantley L (1988) Type I phosphatidylinositol kinase makes a novel inositol phospholipid, phosphatidylinositol-3-phosphate. Nature 332:644-646.
52. Li C, Wong WH (2003) DNA-Chip Analyzer (dChip) (Springer, New York).