Inhibition of Id proteins by a peptide aptamer induces cell-cycle arrest and apoptosis in ovarian cancer cells

British Journal of Cancer

Volumn 103, Issue 8, 2010, Pages 1237-1244

  Mern, D S ^a   Hasskarl, J ^b   Burwinkel, B ^a,c  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Id proteins; peptide aptamer; cell cycle arrest; apoptosis; ovarian cancer

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; CYCLIN DEPENDENT KINASE INHIBITOR; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 3; INHIBITOR OF DIFFERENTIATION PROTEIN; PEPTIDE APTAMER; ANTINEOPLASTIC AGENT; ID3 PROTEIN, HUMAN; TUMOR PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; E BOX ELEMENT; HUMAN; HUMAN CELL; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CARCINOMA; CELL CYCLE; DRUG EFFECTS; DRUG SCREENING; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OVARY TUMOR; PATHOLOGY; TISSUE DISTRIBUTION; TUMOR CELL CULTURE; TUMOR SUPPRESSOR GENE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APTAMERS, PEPTIDE; CARCINOMA; CELL CYCLE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, P16; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INHIBITOR OF DIFFERENTIATION PROTEINS; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; TISSUE DISTRIBUTION; TUMOR CELLS, CULTURED;

EID: 77957984394     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605897     Document Type: Article

References (44)

1. Alani RM, Young AZ, Shifflett CB (2001) Id1 regulation of cellular senescence through transcriptional repression of p16Ink4a. PNAS 98: 7812-7816
2. Bartel P, Chien CT, Sternglanz R, Fields S (1993) Elimination of false positives that arise in using the two-hybrid system. BioTechniques 14: 920-924
3. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H (1990) The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61: 49-59
4. Chen C, Okayama H (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7: 2745-2752
5. Chien CT, Bartel PL, Sternglanz R, Fields S (1991) The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc Natl Acad Sci USA 88: 9578-9582
6. Coppe JP, Smith AP, Desprez PY (2003) Id proteins in epithelial cells. Exp Cell Res 285: 131-145
7. de Candia P, Solit DB, Giri D, Brogi E, Siegel PM, Olshen AB, Muller WJ, Rosen N, Benezra R (2003) Angiogenesis impairment in Id-deficient mice cooperates with an Hsp90 inhibitor to completely suppress HER2/neu-dependent breast tumours. Proc Natl Acad.Sci USA 100: 12337-12342
8. Elliott G, O'Hare P (1997) Intercellular trafficking and protein delivery by a herpes virus structural protein. Cell 88: 223-233
9. Fields S, Song O (1989) A novel genetic system to detect protein-protein interactions. Nature 340: 245-246
10. Fong S, Debs RJ, Desprez PY (2000) Id genes and proteins as promising targets in cancer therapy. Trends Mol Med 10: 387-392
11. Han S, Guo C, Hong L, Liu J, Han Z, Liu C, Wang J, Wu K, Ding J, Fan D (2004) Expression and significances of Id1 helix-loop-helix protein overexpression in gastric cancer. Cancer Lett 216: 63-71
12. Henke E, Perk J, Vider J, de Candia P, Chin Y, Solit DB, Ponomarev V, Cartegni L, Manova K, Rosen N, Benezra R (2008) Peptide-conjugated antisense oligonucleotides for targeted inhibition of a transcriptional regulator in vivo. Nat Biotechnol 26: 91-100
13. Iavarone A, Garg P, Lasorella A, Hsu J, Israel MA (1994) The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev 8: 1270-1284
14. Israel MA, Hernandez MC, Florio M, Andres-Barguin PJ, Mantani A, Carter JH, Julin CM (1999) Id gene expression as a key mediator of tumour cell biology. Cancer Res 59: 1726-1730
15. Kamb A, Gruis NA, Weaver-Feldhaus J, Liu Q, Harshman K, Tavtigian SV, Stockert E, Day RS, Johnson BE, Skolnick MH (1994) A cell cycle regulator potentially involved in genesis of many tumor types. Science 264: 436-440
16. Koh K, Masafumi K, Futoshi U, Takayoshi M, Tadashi K, Jack AR, Noriaki T, Toshiyoshi F (2002) Activation of caspase-3 and cleavage of Rb are associated with p16-mediated apoptosis in human non-small cell lung cancer cells. Oncogene 21: 2108-2113
17. Kusume T, Tsuda H, Kawabata M, Inoue T, Umesaki N, Suzuki T, Yamamoto K (1999) The p16-cyclin D1/CDK4-pRb pathway and clinical outcome in epithelial ovarian cancer. Clin Cancer Res 5: 4152-4157
18. Lee TK, Man K, Ling M, Wang X, Wong Y, Lo C, Poon RT, Ng IO, Fan S (2003) Over-expression of Id-1 induces cell proliferation in hepato-cellular carcinoma through inactivation of p16INK4a/RB pathway. Carcinogenesis 24: 1729-1736
19. Lin CQ, Singh J, Murata K, Itahana Y, Parrinello S, Liang SH, Gillett CE, Campisi J, Desprez, PY (2000) Role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res 60: 1332-1340
20. Ling MT, Wang X, Lee DT, Tam PC, Tsao SW, Wong YC (2004) Id-1 expression induces androgen-independent prostate cancer cell growth through activation of epidermal growth factor receptor (EGF-R). Carcinogenesis 25: 517-525
21. Ling MT, Wang X, Ouyang XS, Xu K, Tsao SW, Wong YC (2003) Id-1 expression promotes cell survival through activation of NF-kappaB signalling pathway in prostate cancer cells. Oncogene 22: 4498-4508
22. Ling MT, Wang X, Zhang X, Wong YC (2006) The multiple roles of Id-1 in cancer progression. Differentiation 74: 481-487
23. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumor xenografts. Nature 401: 670-677
24. Mern DS, Hoppe-Seyler K, Hoppe-Seyler F, Hasskarl J, Burwinkel B (2010) Targeting Id1 and Id3 by a specific peptide aptamer induces E-box promoter activity, cell cycle arrest, and apoptosis in breast cancer cells. Breast Cancer Res Treat, doi: 10.1007/s10549-010-0810-6
25. Narita K, Choudhury A, Dobrenis K (2001) Protein transduction of Rab9 in Niemann- Pick C cells reduces cholesterol storage. FASEB 10: 1558-1560
26. Norton JD (2000) ID helix-loop-helix proteins in cell growth, differentiation and tumourigenesis. J Cell Sci 113: 3897-3905
27. Norton JD, Atherton GT (1998) Coupling of cell growth control and apoptosis functions of Id proteins. Mol Cell Biol 18: 2371-2381
28. Ohtani N, Zebedee Z, Huot TJ, Stinson JA, Sugimoto M, Ohashi Y, Sharrocks AD, Peters G, Hara E (2001) Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 409: 1067-1070
29. Ouyang XS, Wang X, Lee DT, Tsao SW, Wong YC (2002a) Over expression of ID-1 in prostate cancer. J Urol 167: 2598-2602
30. Ouyang XS, Wang X, Ling MT, Wong HL, Tsao SW, Wong YC (2002b) Id-1 stimulates serum independent prostate cancer cell proliferation through inactivation of p16 (INK4a)/pRB) pathway. Carcinogenesis 23: 721-725 (Pubitemid 34567509)
31. Perk J, Iavarone A, Benezra R (2005) Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 5: 603-614
32. Phelan A, Elliott G, O'Hare, P (1998) Intercellular delivery of functional p53 by the herpes virus protein VP22. Nat Biotechnol 16: 440-443
33. Polsky D, Young AZ, Busan KJ, Alani RM (2001) The transcriptional repressor of p16/Ink4a, Id1, is up-regulated in early melanomas. Cancer Res 61: 6008-6011
34. Prabhu S, Ignatova A, Park ST, Sun XH (1997) Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and Id proteins. Mol Cell Biol 17: 5888-5896
35. Ruas M, Peters G (1998) The p16INK4a/CDKN2A tumour suppressor and its relatives. Biochim Biophys Acta 1378: 115-117
36. Ruzinova MB, Benezra R (2003) Id proteins in development, cell cycle and cancer. Trends Cell Biol 13: 410-418
37. Schindl M, Oberhuber G, Obermair A, Schoppmann SF, Karner B, Birner P (2001) Overexpression of Id-1 protein is a marker for unfavourable prognosis in early-stage cervical cancer. Cancer Res 61: 5703-5706
38. Schindl M, Schoppmann SF, Ströbel T, Heinzl H, Leisser C, Horvat R, Birner P (2003) Level of Id-1 protein expression correlates with poor differentiation, enhanced malignant potential, and more aggressive clinical behavior of epithelial ovarian tumours. Clin Cancer Res 9: 779-785
39. Schoppmann SF, Schindl M, Bayer G, Aumayr K, Dienes J, Horvat R, Rudas M, Gnant M, Jakesz R, Birner P (2003) Overexpression of Id-1 isassociated with poor clinical outcome in node negative breast cancer. Int J Cancer 104: 677-682
40. Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1- phase progression. Genes Dev 13: 1501-1512
41. Wang Q, Tsao SW, Fu S, Xue W, Meng X, Feng H, Wong YC, Wang X (2004) Overexpression of Id-1 in gastric adenocarcinoma: implication for a novel diagnostic marker. Anticancer Res 24: 881-886
42. Weintraub H, Davis R, Lockshon D, Lassar A (1990) Muscle-specific transcriptional activation by MyoD. Proc Natl Acad Sci USA 87: 5623-5627
43. Zhang X, Ling MT, Wong YC, Wang X (2007) Evidence of a novel antiapoptotic factor: role of inhibitor of differentiation or DNA binding (Id-1) in anticancer drug-induced apoptosis. Cancer Sci 98: 308-314
44. Zhang X, Ling MT, Feng H, Wong YC, Tsao SW, Wang X (2004) Id-1 stimulates cell proliferation through activation of EGFR in ovarian cancer cells. BJC 91: 2042-2047