ERBB3 knockdown induces cell cycle arrest and activation of Bak and Bax-dependent apoptosis in colon cancer cells

Oncotarget

Volumn 5, Issue 13, 2014, Pages 5138-5152

  Lee, Hyunji ^a   Lee, Hyunjung ^a   Chin, Hyunjung ^a   Kim, Kyoungmi ^a   Lee, Daekee ^a  

^a Ewha Womans University   (South Korea)

Author keywords

Apoptosis; Bak; Bax; Cell cycle arrest; ERBB3 targeting

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BH3 PROTEIN; BIM PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; INHIBITOR OF APOPTOSIS PROTEIN; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; K RAS PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN MCL 1; PROTEIN NOXA; PROTEIN P53; PUMA PROTEIN; S6 KINASE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; BAK1 PROTEIN, HUMAN; BAX PROTEIN, HUMAN; CHROMONE DERIVATIVE; ENZYME INHIBITOR; ERBB3 PROTEIN, HUMAN; MORPHOLINE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL LINE; CELL CYCLE ARREST; CELL PROLIFERATION; COLON CANCER; COLON CANCER CELL LINE; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME REPRESSION; G1 PHASE CELL CYCLE CHECKPOINT; GENE MUTATION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; UPREGULATION; ANTAGONISTS AND INHIBITORS; CELL CYCLE CHECKPOINT; COLON TUMOR; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HCT116 CELL LINE; HT 29 CELL LINE; METABOLISM; PATHOLOGY; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; WESTERN BLOTTING;

APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMONES; COLONIC NEOPLASMS; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HT29 CELLS; HUMANS; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, ERBB-3; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84905000100     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2094     Document Type: Article

References (68)

1. Yarden Y and Sliwkowski MX. Untangling the ErbB signalling network. Nature reviews Molecular cell biology. 2001; 2(2):127-137.
2. Yarden Y and Pines G. The ERBB network: at last, cancer therapy meets systems biology. Nature reviews Cancer. 2012; 12(8):553-563.
3. Moyer JD, Barbacci EG, Iwata KK, Arnold L, Boman B, Cunningham A, DiOrio C, Doty J, Morin MJ, Moyer MP, Neveu M, Pollack VA, Pustilnik LR, Reynolds MM, Sloan D, Theleman A, et al. Induction of apoptosis and cell cycle arrest by CP-358,774, an inhibitor of epidermal growth factor receptor tyrosine kinase. Cancer Res. 1997; 57(21):4838-4848.
4. Ciardiello F, Caputo R, Bianco R, Damiano V, Pomatico G, De Placido S, Bianco AR and Tortora G. Antitumor effect and potentiation of cytotoxic drugs activity in human cancer cells by ZD-1839 (Iressa), an epidermal growth factor receptor-selective tyrosine kinase inhibitor. Clinical cancer research: an official journal of the American Association for Cancer Research. 2000; 6(5):2053-2063.
5. Schoeberl B, Pace EA, Fitzgerald JB, Harms BD, Xu L, Nie L, Linggi B, Kalra A, Paragas V, Bukhalid R, Grantcharova V, Kohli N, West KA, Leszczyniecka M, Feldhaus MJ, Kudla AJ, et al. Therapeutically targeting ErbB3: a key node in ligand-induced activation of the ErbB receptor-PI3K axis. Science signaling. 2009; 2(77):ra31.
6. Chan KC, Knox WF, Gee JM, Morris J, Nicholson RI, Potten CS and Bundred NJ. Effect of epidermal growth factor receptor tyrosine kinase inhibition on epithelial proliferation in normal and premalignant breast. Cancer Res. 2002; 62(1):122-128.
7. Ullrich RT, Zander T, Neumaier B, Koker M, Shimamura T, Waerzeggers Y, Borgman CL, Tawadros S, Li H, Sos ML, Backes H, Shapiro GI, Wolf J, Jacobs AH, Thomas RK and Winkeler A. Early detection of erlotinib treatment response in NSCLC by 3'-deoxy-3'-[F]-fluoro-L-thymidine ([F]FLT) positron emission tomography (PET). PloS one. 2008; 3(12):e3908.
8. Wu X, Fan Z, Masui H, Rosen N and Mendelsohn J. Apoptosis induced by an anti-epidermal growth factor receptor monoclonal antibody in a human colorectal carcinoma cell line and its delay by insulin. The Journal of clinical investigation. 1995; 95(4):1897-1905.
9. Nahta R, Hung MC and Esteva FJ. The HER-2-targeting antibodies trastuzumab and pertuzumab synergistically inhibit the survival of breast cancer cells. Cancer Res. 2004; 64(7):2343-2346.
10. Guy PM, Platko JV, Cantley LC, Cerione RA and Carraway KL, 3rd. Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proceedings of the National Academy of Sciences of the United States of America. 1994; 91(17):8132-8136.
11. Alimandi M, Romano A, Curia MC, Muraro R, Fedi P, Aaronson SA, Di Fiore PP and Kraus MH. Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas. Oncogene. 1995; 10(9):1813-1821.
12. Pinkas-Kramarski R, Soussan L, Waterman H, Levkowitz G, Alroy I, Klapper L, Lavi S, Seger R, Ratzkin BJ, Sela M and Yarden Y. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. The EMBO journal. 1996; 15(10):2452-2467.
13. Kim HH, Sierke SL and Koland JG. Epidermal growth factor-dependent association of phosphatidylinositol 3-kinase with the erbB3 gene product. The Journal of biological chemistry. 1994; 269(40):24747-24755.
14. SoltoffSP, Carraway KL, 3rd, Prigent SA, Gullick WG and Cantley LC. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Molecular and cellular biology. 1994; 14(6):3550-3558.
15. Hennessy BT, Smith DL, Ram PT, Lu Y and Mills GB. Exploiting the PI3K/AKT pathway for cancer drug discovery. Nature reviews Drug discovery. 2005; 4(12):988-1004.
16. Campbell MR, Amin D and Moasser MM. HER3 comes of age: new insights into its functions and role in signaling, tumor biology, and cancer therapy. Clinical cancer research: an official journal of the American Association for Cancer Research. 2010; 16(5):1373-1383.
17. Baselga J and Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nature reviews Cancer. 2009; 9(7):463-475.
18. Engelman JA, Janne PA, Mermel C, Pearlberg J, Mukohara T, Fleet C, Cichowski K, Johnson BE and Cantley LC. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(10):3788-3793.
19. Sergina NV, Rausch M, Wang D, Blair J, Hann B, Shokat KM and Moasser MM. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature. 2007; 445(7126):437-441.
20. Shi F, Telesco SE, Liu Y, Radhakrishnan R and Lemmon MA. ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(17):7692-7697.
21. Jaiswal BS, Kljavin NM, Stawiski EW, Chan E, Parikh C, Durinck S, Chaudhuri S, Pujara K, Guillory J, Edgar KA, Janakiraman V, Scholz RP, Bowman KK, Lorenzo M, Li H, Wu J, et al. Oncogenic ERBB3 mutations in human cancers. Cancer cell. 2013; 23(5):603-617.
22. Schoeberl B, Faber AC, Li D, Liang MC, Crosby K, Onsum M, Burenkova O, Pace E, Walton Z, Nie L, Fulgham A, Song Y, Nielsen UB, Engelman JA and Wong KK. An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res. 2010; 70(6):2485-2494.
23. Sithanandam G, Fornwald LW, Fields J and Anderson LM. Inactivation of ErbB3 by siRNA promotes apoptosis and attenuates growth and invasiveness of human lung adenocarcinoma cell line A549. Oncogene. 2005; 24(11):1847-1859.
24. Xue C, Liang F, Mahmood R, Vuolo M, WyckoffJ, Qian H, Tsai KL, Kim M, Locker J, Zhang ZY and Segall JE. ErbB3-dependent motility and intravasation in breast cancer metastasis. Cancer Res. 2006; 66(3):1418-1426.
25. Beji A, Horst D, Engel J, Kirchner T and Ullrich A. Toward the prognostic significance and therapeutic potential of HER3 receptor tyrosine kinase in human colon cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2012; 18(4):956-968.
26. Aurisicchio L, Marra E, Roscilli G, Mancini R and Ciliberto G. The promise of anti-ErbB3 monoclonals as new cancer therapeutics. Oncotarget. 2012; 3(8):744-758.
27. Noto A, De Vitis C, Roscilli G, Fattore L, Malpicci D, Marra E, Luberto L, D'Andrilli A, Coluccia P, Giovagnoli MR, Normanno N, Ruco L, Aurisicchio L, Mancini R and Ciliberto G. Combination therapy with anti-ErbB3 monoclonal antibodies and EGFR TKIs potently inhibits non-small cell lung cancer. Oncotarget. 2013; 4(8):1253-1265.
28. Garrett JT, Olivares MG, Rinehart C, Granja-Ingram ND, Sanchez V, Chakrabarty A, Dave B, Cook RS, Pao W, McKinely E, Manning HC, Chang J and Arteaga CL. Transcriptional and posttranslational up-regulation of HER3 (ErbB3) compensates for inhibition of the HER2 tyrosine kinase. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(12):5021-5026.
29. Lee D, Yu M, Lee E, Kim H, Yang Y, Kim K, Pannicia C, Kurie JM and Threadgill DW. Tumor-specific apoptosis caused by deletion of the ERBB3 pseudo-kinase in mouse intestinal epithelium. The Journal of clinical investigation. 2009; 119(9):2702-2713.
30. Kelly PN and Strasser A. The role of Bcl-2 and its pro-survival relatives in tumourigenesis and cancer therapy. Cell death and differentiation. 2011; 18(9):1414-1424.
31. Gilmore AP, Valentijn AJ, Wang P, Ranger AM, Bundred N, O'Hare MJ, Wakeling A, Korsmeyer SJ and Streuli CH. Activation of BAD by therapeutic inhibition of epidermal growth factor receptor and transactivation by insulin-like growth factor receptor. The Journal of biological chemistry. 2002; 277(31):27643-27650.
32. Cragg MS, Kuroda J, Puthalakath H, Huang DC and Strasser A. Gefitinib-induced killing of NSCLC cell lines expressing mutant EGFR requires BIM and can be enhanced by BH3 mimetics. PLoS medicine. 2007; 4(10):1681-1689; discussion 1690.
33. Costa DB, Halmos B, Kumar A, Schumer ST, Huberman MS, Boggon TJ, Tenen DG and Kobayashi S. BIM mediates EGFR tyrosine kinase inhibitor-induced apoptosis in lung cancers with oncogenic EGFR mutations. PLoS medicine. 2007; 4(10):1669-1679; discussion 1680.
34. Gong Y, Somwar R, Politi K, Balak M, Chmielecki J, Jiang X and Pao W. Induction of BIM is essential for apoptosis triggered by EGFR kinase inhibitors in mutant EGFR-dependent lung adenocarcinomas. PLoS medicine. 2007; 4(10):e294.
35. Sun Q, Ming L, Thomas SM, Wang Y, Chen ZG, Ferris RL, Grandis JR, Zhang L and Yu J. PUMA mediates EGFR tyrosine kinase inhibitor-induced apoptosis in head and neck cancer cells. Oncogene. 2009; 28(24):2348-2357.
36. Henson ES, Hu X and Gibson SB. Herceptin sensitizes ErbB2-overexpressing cells to apoptosis by reducing antiapoptotic Mcl-1 expression. Clin Cancer Res. 2006; 12(3 Pt 1):845-853.
37. Milella M, Trisciuoglio D, Bruno T, Ciuffreda L, Mottolese M, Cianciulli A, Cognetti F, Zangemeister-Wittke U, Del Bufalo D and Zupi G. Trastuzumab down-regulates Bcl-2 expression and potentiates apoptosis induction by Bcl-2/Bcl-XL bispecific antisense oligonucleotides in HER-2 gene-amplified breast cancer cells. Clinical cancer research: an official journal of the American Association for Cancer Research. 2004; 10(22):7747-7756.
38. Bean GR, Ganesan YT, Dong Y, Takeda S, Liu H, Chan PM, Huang Y, Chodosh LA, Zambetti GP, Hsieh JJ and Cheng EH. PUMA and BIM are required for oncogene inactivation-induced apoptosis. Science signaling. 2013; 6(268):ra20.
39. Wild R, Fager K, Flefleh C, Kan D, Inigo I, Castaneda S, Luo FR, Camuso A, McGlinchey K and Rose WC. Cetuximab preclinical antitumor activity (monotherapy and combination based) is not predicted by relative total or activated epidermal growth factor receptor tumor expression levels. Molecular cancer therapeutics. 2006; 5(1):104-113.
40. Jhawer M, Goel S, Wilson AJ, Montagna C, Ling YH, Byun DS, Nasser S, Arango D, Shin J, Klampfer L, Augenlicht LH, Perez-Soler R and Mariadason JM. PIK3CA mutation/PTEN expression status predicts response of colon cancer cells to the epidermal growth factor receptor inhibitor cetuximab. Cancer Res. 2008; 68(6):1953-1961.
41. Pohl M, Stricker I, Schoeneck A, Schulmann K, Klein-Scory S, Schwarte-WaldhoffI, Hasmann M, Tannapfel A, Schmiegel W and Reinacher-Schick A. Antitumor activity of the HER2 dimerization inhibitor pertuzumab on human colon cancer cells in vitro and in vivo. J Cancer Res Clin Oncol. 2009; 135(10):1377-1386.
42. Shirasawa S, Furuse M, Yokoyama N and Sasazuki T. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science. 1993; 260(5104):85-88.
43. Samuels Y, Diaz LA, Jr., Schmidt-Kittler O, Cummins JM, Delong L, Cheong I, Rago C, Huso DL, Lengauer C, Kinzler KW, Vogelstein B and Velculescu VE. Mutant PIK3CA promotes cell growth and invasion of human cancer cells. Cancer cell. 2005; 7(6):561-573.
44. She QB, Halilovic E, Ye Q, Zhen W, Shirasawa S, Sasazuki T, Solit DB and Rosen N. 4E-BP1 is a key effector of the oncogenic activation of the AKT and ERK signaling pathways that integrates their function in tumors. Cancer cell. 2010; 18(1):39-51.
45. Lindsay J, Esposti MD and Gilmore AP. Bcl-2 proteins and mitochondria-specificity in membrane targeting for death. Biochimica et biophysica acta. 2011; 1813(4):532-539.
46. Miyashita T and Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 1995; 80(2):293-299.
47. Silvera D, Formenti SC and Schneider RJ. Translational control in cancer. Nature reviews Cancer. 2010; 10(4):254-266.
48. GraffJR, Konicek BW, Carter JH and Marcusson EG. Targeting the eukaryotic translation initiation factor 4E for cancer therapy. Cancer Res. 2008; 68(3):631-634.
49. Hynes NE and Lane HA. ERBB receptors and cancer: the complexity of targeted inhibitors. Nature reviews Cancer. 2005; 5(5):341-354.
50. Yamaguchi H, Chang SS, Hsu JL and Hung MC. Signaling cross-talk in the resistance to HER family receptor targeted therapy. Oncogene. 2014; 33(9):1073-1081.
51. Amado RG, Wolf M, Peeters M, Van Cutsem E, Siena S, Freeman DJ, Juan T, Sikorski R, Suggs S, Radinsky R, Patterson SD and Chang DD. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J Clin Oncol. 2008; 26(10):1626-1634.
52. Misale S, Yaeger R, Hobor S, Scala E, Janakiraman M, Liska D, Valtorta E, Schiavo R, Buscarino M, Siravegna G, Bencardino K, Cercek A, Chen CT, Veronese S, Zanon C, Sartore-Bianchi A, et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature. 2012; 486(7404):532-536.
53. Diaz LA, Jr., Williams RT, Wu J, Kinde I, Hecht JR, Berlin J, Allen B, Bozic I, Reiter JG, Nowak MA, Kinzler KW, Oliner KS and Vogelstein B. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature. 2012; 486(7404):537-540.
54. Yu K, Toral-Barza L, Shi C, Zhang WG and 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(2):307-315.
55. Wee S, Jagani Z, Xiang KX, Loo A, Dorsch M, Yao YM, Sellers WR, Lengauer C and Stegmeier F. PI3K pathway activation mediates resistance to MEK inhibitors in KRAS mutant cancers. Cancer Res. 2009; 69(10):4286-4293.
56. She QB, Solit DB, Ye Q, O'Reilly KE, Lobo J and Rosen N. The BAD protein integrates survival signaling by EGFR/MAPK and PI3K/Akt kinase pathways in PTEN-deficient tumor cells. Cancer cell. 2005; 8(4):287-297.
57. Westphal D, Dewson G, Czabotar PE and Kluck RM. Molecular biology of Bax and Bak activation and action. Biochimica et biophysica acta. 2011; 1813(4):521-531.
58. Wang C and Youle RJ. Predominant requirement of Bax for apoptosis in HCT116 cells is determined by Mcl-1's inhibitory effect on Bak. Oncogene. 2012; 31(26):3177-3189.
59. Beckerman R and Prives C. Transcriptional regulation by p53. Cold Spring Harbor perspectives in biology. 2010; 2(8):a000935.
60. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M and Green DR. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 2004; 303(5660):1010-1014.
61. Graupner V, Alexander E, Overkamp T, Rothfuss O, De Laurenzi V, Gillissen BF, Daniel PT, Schulze-OsthoffK and Essmann F. Differential regulation of the proapoptotic multidomain protein Bak by p53 and p73 at the promoter level. Cell death and differentiation. 2011; 18(7):1130-1139.
62. Semba S, Itoh N, Ito M, Harada M and Yamakawa M. The in vitro and in vivo effects of 2-(4-morpholinyl)-8-phenyl-chromone (LY294002), a specific inhibitor of phosphatidylinositol 3'-kinase, in human colon cancer cells. Clinical cancer research: an official journal of the American Association for Cancer Research. 2002; 8(6):1957-1963.
63. Hay N and Sonenberg N. Upstream and downstream of mTOR. Genes & development. 2004; 18(16):1926-1945.
64. Martin-Fernandez C, Bales J, Hodgkinson C, Welman A, Welham MJ, Dive C and Morrow CJ. Blocking phosphoinositide 3-kinase activity in colorectal cancer cells reduces proliferation but does not increase apoptosis alone or in combination with cytotoxic drugs. Molecular cancer research: MCR. 2009; 7(6):955-965.
65. Jiang Z, Liu JC, Chung PE, Egan S and Zacksenhaus E. Targeting Her2+ breast cancer: TBK1/IKKe axis. Oncoscience. 2014; 1(2):180-182.
66. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, Kinzler KW and Vogelstein B. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science. 1998; 282(5393):1497-1501.
67. Zhang L, Yu J, Park BH, Kinzler KW and Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science. 2000; 290(5493):989-992.
68. Kim K, Lee H, Threadgill DW and Lee D. Epiregulin-dependent amphiregulin expression and ERBB2 signaling are involved in luteinizing hormone-induced paracrine signaling pathways in mouse ovary. Biochemical and biophysical research communications. 2011; 405(2):319-324.