Histone deacetylase inhibitors enhance the apoptotic activity of insulin-like growth factor binding protein-3 by blocking PKC-induced IGFBP-3 degradation

International Journal of Cancer

Volumn 131, Issue 10, 2012, Pages 2253-2263

  Oh, Seung Hyun ^a,b   Whang, Young Mi ^c   Min, Hye Young ^d   Han, Seung Ho ^c,g   Kang, Ju Hee ^b,e   Song, Ki Hoon ^b   Glisson, Bonnie S ^c   Kim, Yeul Hong ^f   Lee, Ho Young ^d  

^a Gachon University   (South Korea)

^b National Cancer Center   (South Korea)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d Seoul National University   (South Korea)

^e Chung Ang University   (South Korea)

^f Korea University College of Medicine   (South Korea)

^g Eulji University   (South Korea)

Author keywords

Akt; head and neck squamous cell carcinoma; histone deacetylases; insulin like growth factor binding protein 3; Non small cell lung cancer; protein kinase C

Indexed keywords

DEPSIPEPTIDE; HISTONE DEACETYLASE INHIBITOR; PROTEIN KINASE B; PROTEIN KINASE C; RECOMBINANT GROWTH FACTOR; SOMATOMEDIN BINDING PROTEIN 3; VORINOSTAT;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; DRUG EFFICACY; DRUG HALF LIFE; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; TREATMENT RESPONSE;

ANIMALS; APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DRUG SYNERGISM; FEMALE; HEAD AND NECK NEOPLASMS; HISTONE DEACETYLASE INHIBITORS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; MICE; MICE, NUDE; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN STABILITY; PROTEOLYSIS; TRANSCRIPTION, GENETIC; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84867033832     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27509     Document Type: Article

References (50)

1. Jemal A, Siegel R, Xu J, Ward E,. Cancer statistics, 2010. CA Cancer J Clin 2010; 60: 277-300.
2. Siesling S, van Dijck JA, Visser O, Coebergh JW,. Trends in incidence of and mortality from cancer in The Netherlands in the period 1989-1998. Eur J Cancer 2003; 39: 2521-30.
3. Thun MJ, Henley SJ, Burns D, Jemal A, Shanks TG, Calle EE,. Lung cancer death rates in lifelong nonsmokers. J Natl Cancer Inst 2006; 98: 691-9.
4. Pollak MN, Schernhammer ES, Hankinson SE,. Insulin-like growth factors and neoplasia. Nat Rev Cancer 2004; 4: 505-18.
5. Silha JV, Sheppard PC, Mishra S, Gui Y, Schwartz J, Dodd JG, Murphy LJ,. Insulin-like growth factor (IGF) binding protein-3 attenuates prostate tumor growth by IGF-dependent and IGF-independent mechanisms. Endocrinology 2006; 147: 2112-21.
6. Yokota T, Shimokawa H, Shibata S, Itoh K, Baba Y, Ohya K, Ohyama K, Suzuki S,. Insulin-like growth factor I regulates apoptosis in condylar cartilage. J Dent Res 2008; 87: 159-63.
7. Mishra S, Murphy LJ,. The effects of insulin-like growth factor binding protein-3 (IGFBP-3) on T47D breast cancer cells enriched for IGFBP-3 binding sites. Mol Cell Biochem 2004; 267: 83-9.
8. Lewitt MS, Scott FP, Clarke NM, Wu T, Sinosich MJ, Baxter RC,. Regulation of insulin-like growth factor-binding protein-3 ternary complex formation in pregnancy. J Endocrinol 1998; 159: 265-74.
9. Oh SH, Kim WY, Kim JH, Younes MN, El-Naggar AK, Myers JN, Kies M, Cohen P, Khuri F, Hong WK, Lee HY,. Identification of insulin-like growth factor binding protein-3 as a farnesyl transferase inhibitor SCH66336-induced negative regulator of angiogenesis in head and neck squamous cell carcinoma. Clin Cancer Res 2006; 12: 653-61.
10. Oh SH, Lee OH, Schroeder CP, Oh YW, Ke S, Cha HJ, Park RW, Onn A, Herbst RS, Li C, Lee HY,. Antimetastatic activity of insulin-like growth factor binding protein-3 in lung cancer is mediated by insulin-like growth factor-independent urokinase-type plasminogen activator inhibition. Mol Cancer Ther 2006; 5: 2685-95.
11. Lee KW, Ma L, Yan X, Liu B, Zhang XK, Cohen P,. Rapid apoptosis induction by IGFBP-3 involves an insulin-like growth factor-independent nucleomitochondrial translocation of RXRalpha/Nur77. J Biol Chem 2005; 280: 16942-8.
12. Aishima S, Basaki Y, Oda Y, Kuroda Y, Nishihara Y, Taguchi K, Taketomi A, Maehara Y, Hosoi F, Maruyama Y, Fotovati A, Oie S, et al. High expression of insulin-like growth factor binding protein-3 is correlated with lower portal invasion and better prognosis in human hepatocellular carcinoma. Cancer Sci 2006; 97: 1182-90.
13. Chang YS, Kong G, Sun S, Liu D, El-Naggar AK, Khuri FR, Hong WK, Lee HY,. Clinical significance of insulin-like growth factor-binding protein-3 expression in stage I non-small cell lung cancer. Clin Cancer Res 2002; 8: 3796-802.
14. Chang YS, Wang L, Liu D, Mao L, Hong WK, Khuri FR, Lee HY,. Correlation between insulin-like growth factor-binding protein-3 promoter methylation and prognosis of patients with stage I non-small cell lung cancer. Clin Cancer Res 2002; 8: 3669-75.
15. Lee CT, Park KH, Yanagisawa K, Adachi Y, Ohm JE, Nadaf S, Dikov MM, Curiel DT, Carbone DP,. Combination therapy with conditionally replicating adenovirus and replication defective adenovirus. Cancer Res 2004; 64: 6660-5.
16. Martin JL, Baxter RC,. Oncogenic ras causes resistance to the growth inhibitor insulin-like growth factor binding protein-3 (IGFBP-3) in breast cancer cells. J Biol Chem 1999; 274: 16407-11.
17. Lee HY, Moon H, Chun KH, Chang YS, Hassan K, Ji L, Lotan R, Khuri FR, Hong WK,. Effects of insulin-like growth factor binding protein-3 and farnesyltransferase inhibitor SCH66336 on Akt expression and apoptosis in non-small-cell lung cancer cells. J Natl Cancer Inst 2004; 96: 1536-48.
18. Oh SH, Woo JK, Yazici YD, Myers JN, Kim WY, Jin Q, Hong SS, Park HJ, Suh YG, Kim KW, Hong WK, Lee HY,. Structural basis for depletion of heat shock protein 90 client proteins by deguelin. J Natl Cancer Inst 2007; 99: 949-61.
19. Oh SH, Jin Q, Kim ES, Khuri FR, Lee HY,. Insulin-like growth factor-I receptor signaling pathway induces resistance to the apoptotic activities of SCH66336 (lonafarnib) through Akt/mammalian target of rapamycin-mediated increases in survivin expression. Clin Cancer Res 2008; 14: 1581-9.
20. Condorelli F, Gnemmi I, Vallario A, Genazzani AA, Canonico PL,. Inhibitors of histone deacetylase (HDAC) restore the p53 pathway in neuroblastoma cells. Br J Pharmacol 2008; 153: 657-68.
21. Dai Y, Rahmani M, Dent P, Grant S,. Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-kappaB activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation. Mol Cell Biol 2005; 25: 5429-44.
22. Edwards A, Li J, Atadja P, Bhalla K, Haura EB,. Effect of the histone deacetylase inhibitor LBH589 against epidermal growth factor receptor-dependent human lung cancer cells. Mol Cancer Ther 2007; 6: 2515-24.
23. Imre G, Gekeler V, Leja A, Beckers T, Boehm M,. Histone deacetylase inhibitors suppress the inducibility of nuclear factor-kappaB by tumor necrosis factor-alpha receptor-1 downregulation. Cancer Res 2006; 66: 5409-18.
24. Moody TW, Nakagawa T, Kang Y, Jakowlew S, Chan D, Jensen RT,. Bombesin/gastrin-releasing peptide receptor antagonists increase the ability of histone deacetylase inhibitors to reduce lung cancer proliferation. J Mol Neurosci 2006; 28: 231-8.
25. Park H, Im JY, Kim J, Choi WS, Kim HS,. Effects of apicidin, a histone deacetylase inhibitor, on the regulation of apoptosis in H-ras-transformed breast epithelial cells. Int J Mol Med 2008; 21: 325-33.
26. Klampfer L, Huang J, Shirasawa S, Sasazuki T, Augenlicht L,. Histone deacetylase inhibitors induce cell death selectively in cells that harbor activated kRasV12: The role of signal transducers and activators of transcription 1 and p21. Cancer Res 2007; 67: 8477-85.
27. Kobayashi Y, Ohtsuki M, Murakami T, Kobayashi T, Sutheesophon K, Kitayama H, Kano Y, Kusano E, Nakagawa H, Furukawa Y,. Histone deacetylase inhibitor FK228 suppresses the Ras-MAP kinase signaling pathway by upregulating Rap1 and induces apoptosis in malignant melanoma. Oncogene 2006; 25: 512-24.
28. Chun KH, Kosmeder JW, II, Sun S, Pezzuto JM, Lotan R, Hong WK, Lee HY,. Effects of deguelin on the phosphatidylinositol 3-kinase/Akt pathway and apoptosis in premalignant human bronchial epithelial cells. J Natl Cancer Inst 2003; 95: 291-302.
29. Morgillo F, Woo JK, Kim ES, Hong WK, Lee HY,. Heterodimerization of insulin-like growth factor receptor/epidermal growth factor receptor and induction of survivin expression counteract the antitumor action of erlotinib. Cancer Res 2006; 66: 10100-11.
30. Bae MK, Kwon YW, Kim MS, Bae SK, Bae MH, Lee YM, Kim YJ, Kim KW,. Identification of genes differentially expressed by hypoxia in hepatocellular carcinoma cells. Biochem Biophys Res Commun 1998; 243: 158-62.
31. Chang YS, Wang L, Suh YA, Mao L, Karpen SJ, Khuri FR, Hong WK, Lee HY,. Mechanisms underlying lack of insulin-like growth factor-binding protein-3 expression in non-small-cell lung cancer. Oncogene 2004; 23: 6569-80.
32. Granata R, Trovato L, Garbarino G, Taliano M, Ponti R, Sala G, Ghidoni R, Ghigo E,. Dual effects of IGFBP-3 on endothelial cell apoptosis and survival: Involvement of the sphingolipid signaling pathways. FASEB J 2004; 18: 1456-8.
33. McIntosh J, Dennison G, Holly JM, Jarrett C, Frankow A, Foulstone EJ, Winters ZE, Perks CM,. IGFBP-3 can either inhibit or enhance EGF-mediated growth of breast epithelial cells dependent upon the presence of fibronectin. J Biol Chem 2010; 285: 38788-800.
34. Choi HS, Lee JH, Park JG, Lee YI,. Trichostatin A, a histone deacetylase inhibitor, activates the IGFBP-3 promoter by upregulating Sp1 activity in hepatoma cells: Alteration of the Sp1/Sp3/HDAC1 multiprotein complex. Biochem Biophys Res Commun 2002; 296: 1005-12.
35. Walker GE, Wilson EM, Powell D, Oh Y,. Butyrate, a histone deacetylase inhibitor, activates the human IGF binding protein-3 promoter in breast cancer cells: Molecular mechanism involves an Sp1/Sp3 multiprotein complex. Endocrinology 2001; 142: 3817-27.
36. Mitsudomi T, Steinberg SM, Nau MM, Carbone D, D'Amico D, Bodner S, Oie HK, Linnoila RI, Mulshine JL, Minna JD, Gazdar AF,. p53 gene mutations in non-small-cell lung cancer cell lines and their correlation with the presence of ras mutations and clinical features. Oncogene 1992; 7: 171-80.
37. Coverley JA, Baxter RC,. Phosphorylation of insulin-like growth factor binding proteins. Mol Cell Endocrinol 1997; 128: 1-5.
38. Schedlich LJ, Nilsen T, John AP, Jans DA, Baxter RC,. Phosphorylation of insulin-like growth factor binding protein-3 by deoxyribonucleic acid-dependent protein kinase reduces ligand binding and enhances nuclear accumulation. Endocrinology 2003; 144: 1984-93.
39. Baxter RC,. Signalling pathways involved in antiproliferative effects of IGFBP-3: A review. Mol Pathol 2001; 54: 145-8.
40. Lee HY, Chun KH, Liu B, Wiehle SA, Cristiano RJ, Hong WK, Cohen P, Kurie JM,. Insulin-like growth factor binding protein-3 inhibits the growth of non-small cell lung cancer. Cancer Res 2002; 62: 3530-7.
41. Jerome L, Alami N, Belanger S, Page V, Yu Q, Paterson J, Shiry L, Pegram M, Leyland-Jones B,. Recombinant human insulin-like growth factor binding protein 3 inhibits growth of human epidermal growth factor receptor-2- overexpressing breast tumors and potentiates herceptin activity in vivo. Cancer Res 2006; 66: 7245-52.
42. Collard TJ, Guy M, Butt AJ, Perks CM, Holly JM, Paraskeva C, Williams AC,. Transcriptional upregulation of the insulin-like growth factor binding protein IGFBP-3 by sodium butyrate increases IGF-independent apoptosis in human colonic adenoma-derived epithelial cells. Carcinogenesis 2003; 24: 393-401.
43. Firth SM, Baxter RC,. Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 2002; 23: 824-54.
44. Wang SC, Nakajima Y, Yu YL, Xia W, Chen CT, Yang CC, McIntush EW, Li LY, Hawke DH, Kobayashi R, Hung MC,. Tyrosine phosphorylation controls PCNA function through protein stability. Nat Cell Biol 2006; 8: 1359-68.
45. Wind M, Wegener A, Kellner R, Lehmann WD,. Analysis of CheA histidine phosphorylation and its influence on protein stability by high-resolution element and electrospray mass spectrometry. Anal Chem 2005; 77: 1957-62.
46. Hung PS, Kao SY, Shih YH, Chiou SH, Liu CJ, Chang KW, Lin SC,. Insulin-like growth factor binding protein-5 (IGFBP-5) suppresses the tumourigenesis of head and neck squamous cell carcinoma. J Pathol 2008; 214: 368-76.
47. Shen L, Glazer RI,. Induction of apoptosis in glioblastoma cells by inhibition of protein kinase C and its association with the rapid accumulation of p53 and induction of the insulin-like growth factor-1-binding protein-3. Biochem Pharmacol 1998; 55: 1711-9.
48. Blobe GC, Sachs CW, Khan WA, Fabbro D, Stabel S, Wetsel WC, Obeid LM, Fine RL, Hannun YA,. Selective regulation of expression of protein kinase C (PKC) isoenzymes in multidrug-resistant MCF-7 cells. Functional significance of enhanced expression of PKC alpha. J Biol Chem 1993; 268: 658-64.
49. Cobb LJ, Liu B, Lee KW, Cohen P,. Phosphorylation by DNA-dependent protein kinase is critical for apoptosis induction by insulin-like growth factor binding protein-3. Cancer Res 2006; 66: 10878-84.
50. Lee MJ, Kim YS, Kummar S, Giaccone G, Trepel JB,. Histone deacetylase inhibitors in cancer therapy. Curr Opin Oncol 2008; 20: 639-49.