Effects of an indolocarbazole-derived CDK4 inhibitor on breast cancer cells

Journal of Cancer

Volumn 2, Issue 1, 2011, Pages 36-51

  Sun, Yuan ^a,d   Li, Ying Xia ^b   Wu, Hai Jun ^b   Wu, Si Hung ^a   Wang, Y Alan ^c   Luo, Dian Zhong ^d   Liao, D Joshua ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b FUDAN UNIVERSITY   (China)

^c HARVARD UNIVERSITY   (United States)

^d GUANGXI MEDICAL UNIVERSITY   (China)

Author keywords

Breast cancer cell lines; CDK4 inhibitor; NPCD

Indexed keywords

ANTINEOPLASTIC AGENT; CARBAZOLE DERIVATIVE; CYCLIN D1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; NAPHTHO[2,1 ALPHA]PYRROLO[3,4 C]CARBAZOLE 5,7 (6H,12H)DIONE; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CELL CYCLE; CELL DEATH; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG STRUCTURE; DRUG SYNTHESIS; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 79957873480     PISSN: None     EISSN: 18379664     Source Type: Journal    
DOI: 10.7150/jca.2.36     Document Type: Article

References (87)

1. Liao D, Thakur A, Wu J, Biliran H, Sarkar FH Perspectives on c-Myc, Cyclin D1, and Their Interaction in Cancer Formation, Progression, and Response to Chemotherapy. Crit Rev Oncog. 2007; 13: 93-158.
2. Kim JK, Diehl JA Nuclear cyclin D1: an oncogenic driver in human cancer. J Cell Physiol. 2009; 220: 292-296.
3. Kirkegaard T, Nielsen KV, Jensen LB, Campbell FM, Muller S, Tovey SM et al. Genetic alterations of CCND1 and EMSY in breast cancers. Histopathology. 2008; 52: 698-705.
4. Fernandez V, Hartmann E, Ott G, Campo E, Rosenwald A Pathogenesis of mantle-cell lymphoma: all oncogenic roads lead to dysregulation of cell cycle and DNA damage response pathways. J Clin Oncol. 2005; 23: 6364-6369.
5. Elsheikh S, Green AR, Aleskandarany MA, Grainge M, Paish CE, Lambros MB et al. CCND1 amplification and cyclin D1 expression in breast cancer and their relation with proteomic subgroups and patient outcome. Breast Cancer Res Treat. 2008; 109: 325-335.
6. Weinstat-Saslow D, Merino MJ, Manrow RE, Lawrence JA, Bluth RF, Wittenbel KD et al. Overexpression of cyclin D mRNA distinguishes invasive and in situ breast carcinomas from non-malignant lesions. Nat Med. 1995, 1: 1257-1260.
7. Yu Q, Geng Y, Sicinski P Specific protection against breast cancers by cyclin D1 ablation. Nature. 2001; 411: 1017-1021.
8. Butt AJ, McNeil CM, Musgrove EA, Sutherland RL Downstream targets of growth factor and oestrogen signalling and endocrine resistance: the potential roles of c-Myc, cyclin D1 and cyclin E. Endocr Relat Cancer. 2005; 12 (Suppl 1): S47-S59.
9. Aggarwal BB, Ichikawa H Molecular targets and anticancer potential of indole-3-carbinol and its derivatives. Cell Cycle. 2005; 4: 1201-1215.
10. Alao JP The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Mol Cancer. 2007; 6: 24.
11. Curiel DT Gene therapy for carcinoma of the breast: Genetic ablation strategies. Breast Cancer Res. 2000; 2: 45-49.
12. Malumbres M, Barbacid M Is Cyclin D1-CDK4 kinase a bona fide cancer target? Cancer Cell.2006; 9: 2-4.
13. Mani S, Wang C, Wu K, Francis R, Pestell R Cyclin-dependent kinase inhibitors: novel anticancer agents. Expert Opin Investig Drugs. 2000; 9: 1849-1870.
14. Wang C, Li Z, Fu M, Bouras T, Pestell RG Signal transduction mediated by cyclin D1: from mitogens to cell proliferation: a molecular target with therapeutic potential. Cancer Treat Res. 2004; 119: 217-237.
15. Aubry C, Wilson AJ, Emmerson D, Murphy E, Chan YY, Dickens MP et al. Fascaplysin-inspired diindolyls as selective inhibitors of CDK4/cyclin D1. Bioorg Med Chem. 2009; 17: 6073-6084.
16. Corsino P, Horenstein N, Ostrov D, Rowe T, Law M, Barrett A et al. A Novel Class of Cyclin-dependent Kinase Inhibitors Identified by Molecular Docking Act through a Unique Mechanism. J Biol Chem. 2009; 284: 29945-29955.
17. Huang JW, Shiau CW, Yang J, Wang DS, Chiu HC, Chen CY et al. Development of small-molecule cyclin D1-ablative agents. J Med Chem. 2006; 49: 4684-4689.
18. Huang JW, Shiau CW, Yang YT, Kulp SK, Chen KF, Brueggemeier RW et al. Peroxisome proliferator-activated receptor gamma-independent ablation of cyclin D1 by thiazolidinediones and their derivatives in breast cancer cells. Mol Pharmacol. 2005; 67: 1342-1348.
19. Klasa RJ, List AF, Cheson BD Rational approaches to design of therapeutics targeting molecular markers. Hematology Am Soc Hematol Educ Program. 2001;: 443-462.
20. Kakeya H, Onose R, Liu PC, Onozawa C, Matsumura F, Osada H Inhibition of cyclin D1 expression and phosphorylation of retinoblastoma protein by phosmidosine, a nucleotide antibiotic. Cancer Res. 1998; 58: 704-710.
21. Takahashi-Yanaga F, Taba Y, Miwa Y, Kubohara Y, Watanabe Y, Hirata M et al. Dictyostelium differentiation-inducing factor-3 activates glycogen synthase kinase-3beta and degrades cyclin D1 in mammalian cells. J Biol Chem. 2003; 278: 9663-9670.
22. Seo BR, Lee KW, Ha J, Park HJ, Choi JW, Lee KT Saucernetin-7 isolated from Saururus chinensis inhibits proliferation of human promyelocytic HL-60 leukemia cells via G0/G1 phase arrest and induction of differentiation. Carcinogenesis. 2004; 25: 1387-1394.
23. Yang CS, Chin KV, Lambert JD Cancer chemoprevention by targeting proteasomal degradation: commentary re KA Dragnev et al, Specific chemopreventive agents trigger proteasomal degradation of G1 cyclins: implications for combination therapy. Clin Cancer Res, 2004;10:2570-7. Clin Cancer Res. 2004; 10: 2220-2221.
24. Dragnev KH, Pitha-Rowe I, Ma Y, Petty WJ, Sekula D, Murphy B et al. Specific chemopreventive agents trigger proteasomal degradation of G1 cyclins: implications for combination therapy. Clin Cancer Res. 2004; 10: 2570-2577.
25. Hori A, Ikeyama S, Sudo K Suppression of cyclin D1 mRNA expression by the angiogenesis inhibitor TNP-470 (AGM-1470) in vascular endothelial cells. Biochem Biophys Res Commun. 1994; 204: 1067-1073.
26. Senderowicz AM Inhibitors of cyclin-dependent kinase modulators for cancer therapy. Prog Drug Res. 2005; 63: 183-206.
27. Zhai S, Senderowicz AM, Sausville EA, Figg WD: Flavopiridol, a novel cyclin-dependent kinase inhibitor, in clinical development. Ann Pharmacother. 2002; 36: 905-911.
28. Soni R, O'Reilly T, Furet P, Muller L, Stephan C, Zumstein-Mecker S et al. Selective in vivo and in vitro effects of a small molecule inhibitor of cyclin-dependent kinase 4. J Natl Cancer Inst. 2001; 93: 436-446.
29. Zhu G, Conner SE, Zhou X, Chan HK, Shih C, Engler TA et al. Synthesis of 1,7-annulated indoles and their applications in the studies of cyclin dependent kinase inhibitors. Bioorg Med Chem Lett. 2004; 14: 3057-3061.
30. Zhu G, Conner SE, Zhou X, Shih C, Li T, Anderson BD et al. Synthesis, structure-activity relationship, and biological studies of indolocarbazoles as potent cyclin D1-CDK4 inhibitors. J Med Chem. 2003; 46: 2027-2030.
31. Zhu G, Conner S, Zhou X, Shih C, Brooks HB, Considine E et al Synthesis of quinolinyl/isoquinolinyl[a]pyrrolo [3,4-c] carbazoles as cyclin D1/CDK4 inhibitors. Bioorg Med Chem Lett. 2003; 13: 1231-1235.
32. Jeong HW, Kim MR, Son KH, Han MY, Ha JH, Garnier M et al. Cinnamaldehydes inhibit cyclin dependent kinase 4/cyclin D1. Bioorg Med Chem Lett. 2000; 10: 1819-1822.
33. Markwalder JA, Arnone MR, Benfield PA, Boisclair M, Burton CR, Chang CH et al. Synthesis and biological evaluation of 1-aryl-4,5-dihydro-1H-pyrazolo[3,4-d]pyrimidin-4-one inhibitors of cyclin-dependent kinases. J Med Chem. 2004; 47: 5894-5911.
34. Kubo A, Kaye FJ Searching for selective cyclin-dependent kinase inhibitors to target the retinoblastoma/p16 cancer gene pathway. J Natl Cancer Inst. 2001; 93: 415-417.
35. Sanchez-Martinez C, Shih C, Faul MM, Zhu G, Paal M, Somoza C et al. Aryl[a]pyrrolo[3,4-c]carbazoles as selective cyclin D1-CDK4 inhibitors. Bioorg Med Chem Lett. 2003; 13: 3835-3839.
36. Sanchez-Martinez C, Faul MM, Shih C, Sullivan KA, Grutsch JL, Cooper JT et al. Synthesis of aryl- and heteroaryl[a]pyrrolo[3,4-c]carbazoles. J Org Chem. 2003; 68: 8008-8014.
37. Senderowicz AM Small-molecule cyclin-dependent kinase modulators. Oncogene. 2003; 22: 6609-6620.
38. Senderowicz AM Novel direct and indirect cyclin-dependent kinase modulators for the prevention and treatment of human neoplasms. Cancer Chemother Pharmacol. 2003; 52 (Suppl 1): S61-S73.
39. Faul MM, Engler TA, Sullivan KA, Grutsch JL, Clayton MT, Martinelli MJ et al. Synthetic approaches to indolo[6,7-a]pyrrolo[3,4-c]carbazoles: potent cyclin D1/CDK4 inhibitors. J Org Chem. 2004; 69: 2967-2975.
40. Engler TA, Furness K, Malhotra S, Sanchez-Martinez C, Shih C, Xie W et al. Novel, potent and selective cyclin D1/CDK4 inhibitors: indolo[6,7-a]pyrrolo[3,4-c]carbazoles. Bioorg Med Chem Lett. 2003; 13: 2261-2267.
41. Toogood PL, Harvey PJ, Repine JT, Sheehan DJ, VanderWel SN, Zhou H et al. Discovery of a potent and selective inhibitor of cyclin-dependent kinase 4/6. J Med Chem. 2005; 48: 2388-2406.
42. VanderWel SN, Harvey PJ, McNamara DJ, Repine JT, Keller PR, Quin JIII, et al. Pyrido[2,3-d]pyrimidin-7-ones as specific inhibitors of cyclin-dependent kinase 4. J Med Chem. 2005; 48: 2371-2387.
43. Fry DW, Harvey PJ, Keller PR, Elliott WL, Meade M, Trachet E et al. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol Cancer Ther. 2004; 3: 1427-1438.
44. Zhang C, Yan Z, Arango ME, Painter CL, Anderes K Advancing bioluminescence imaging technology for the evaluation of anticancer agents in the MDA-MB-435-HAL-Luc mammary fat pad and subrenal capsule tumor models. Clin Cancer Res. 2009; 15: 238-246.
45. Menu E, Garcia J, Huang X, Di LM, Toogood PL, Chen I et al A novel therapeutic combination using PD 0332991 and bortezomib: study in the 5T33MM myeloma model. Cancer Res. 2008; 68: 5519-5523.
46. Wang L, Wang J, Blaser BW, Duchemin AM, Kusewitt DF, Liu T et al. Pharmacologic inhibition of CDK4/6: mechanistic evidence for selective activity or acquired resistance in acute myeloid leukemia. Blood. 2007; 110: 2075-2083.
47. Finn RS, Dering J, Conklin D, Kalous O, Cohen DJ, Desai AJ et al. PD 0332991, a selective cyclin D kinase 4/6 inhibitor, preferentially inhibits proliferation of luminal estrogen receptor-positive human breast cancer cell lines in vitro. Breast Cancer Res. 2009; 11: R77.
48. Sanchez-Martinez C, Shih C, Zhu G, Li T, Brooks HB, Patel BK et al. Studies on cyclin-dependent kinase inhibitors: indolo-[2,3-a]pyrrolo[3,4-c]carbazoles versus bis-indolylmaleimides. Bioorg Med Chem Lett. 2003; 13: 3841-3846.
49. Thoms HC, Dunlop MG, Stark LA CDK4 inhibitors and apoptosis: a novel mechanism requiring nucleolar targeting of RelA. Cell Cycle. 2007; 6: 1293-1297.
50. Thoms HC, Dunlop MG, Stark LA p38-mediated inactivation of cyclin D1/cyclin-dependent kinase 4 stimulates nucleolar translocation of RelA and apoptosis in colorectal cancer cells. Cancer Res. 2007; 67: 1660-1669.
51. Shen KC, Miller F, Tait L, Santner SJ, Pauley R, Raz A et al. Isolation and characterization of a breast progenitor epithelial cell line with robust DNA damage responses. Breast Cancer Res Treat. 2006; 98: 357-364.
52. Rae JM, Creighton CJ, Meck JM, Haddad BR, Johnson MDMDA-MB-435 cells are derived from M14 Melanoma cells--a loss for breast cancer, but a boon for melanoma research. Breast Cancer Res Treat. 2007; 104: 13-19.
53. Andrews NC, Faller DV A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 1991; 19: 2499.
54. Banerjee S, Zhang Y, Ali S, Bhuiyan M, Wang Z, Chiao PJ et al. Molecular evidence for increased antitumor activity of gemcitabine by genistein in vitro and in vivo using an orthotopic model of pancreatic cancer. Cancer Res. 2005; 65: 9064-9072.
55. Banerjee S, Zhang Y, Wang Z, Che M, Chiao PJ, Abbruzzese JL et al In vitro and in vivo molecular evidence of genistein action in augmenting the efficacy of cisplatin in pancreatic cancer. Int J Cancer. 2007; 120: 906-917.
56. Grafstrom RH, Pan W, Hoess RH Defining the substrate specificity of cdk4 kinase-cyclin D1 complex. Carcinogenesis. 1999; 20: 193-198.
57. Pan W, Cox S, Hoess RH, Grafstrom RH A cyclin D1/cyclin-dependent kinase 4 binding site within the C domain of the retinoblastoma protein. Cancer Res 2001, 61: 2885-2891.
58. Dai Y, Grant S Small molecule inhibitors targeting cyclin-dependent kinases as anticancer agents. Curr Oncol Rep. 2004; 6: 123-130.
59. Graf F, Koehler L, Kniess T, Wuest F, Mosch B, Pietzsch J Cell Cycle Regulating Kinase Cdk4 as a Potential Target for Tumor Cell Treatment and Tumor Imaging. J Oncol. 2009;: 106378.
60. Bukanov NO, Smith LA, Klinger KW, Ledbetter SR, Ibraghimov-Beskrovnaya O Long-lasting arrest of murine polycystic kidney disease with CDK inhibitor roscovitine. Nature. 2006; 444: 949-952.
61. Dawson SJ, Provenzano E, Caldas C Triple negative breast cancers: clinical and prognostic implications. Eur J Cancer. 2009; 45 (Suppl 1): 27-40.
62. Gauthier ML, Berman HK, Miller C, Kozakeiwicz K, Chew K, Moore D et al. Abrogated response to cellular stress identifies DCIS associated with subsequent tumor events and defines basal-like breast tumors. Cancer Cell. 2007; 12: 479-491.
63. Michaud K, Solomon DA, Oermann E, Kim JS, Zhong WZ, Prados MD et al. Pharmacologic inhibition of cyclin-dependent kinases 4 and 6 arrests the growth of glioblastoma multiforme intracranial xenografts. Cancer Res. 2010; 70: 3228-3238.
64. Rivadeneira DB, Mayhew CN, Thangavel C, Sotillo E, Reed CA, Grana X et al. Proliferative suppression by CDK4/6 inhibition: complex function of the retinoblastoma pathway in liver tissue and hepatoma cells. Gastroenterology. 2010; 138: 1920-1930.
65. Dai Y, Hamm TE, Dent P, Grant S Cyclin D1 overexpression increases the susceptibility of human U266 myeloma cells to CDK inhibitors through a process involving p130-, p107- and E2F-dependent S phase entry. Cell Cycle. 2006; 5: 437-446.
66. Baughn LB, Di LM, Wu K, Toogood PL, Louie T, Gottschal k R et al. A novel orally active small molecule potently induces G1 arrest in primary myeloma cells and prevents tumor growth by specific inhibition of cyclin-dependent kinase 4/6. Cancer Res. 2006; 66: 7661-7667.
67. Wei S, Yang HC, Chuang HC, Yang J, Kulp SK, Lu PJ et al. A novel mechanism by which thiazolidinediones facilitate the proteasomal degradation of cyclin D1 in cancer cells. J Biol Chem. 2008; 283: 26759-26770.
68. Kaur M, Velmurugan B, Tyagi A, Deep G, Katiyar S, Agarwal C et al. Silibinin suppresses growth and induces apoptotic death of human colorectal carcinoma LoVo cells in culture and tumor xenograft. Mol Cancer Ther. 2009; 8: 2366-2374.
69. Das SK, Hashimoto T, Kanazawa K Growth inhibition of human hepatic carcinoma HepG2 cells by fucoxanthin is associated with down-regulation of cyclin D. Biochim Biophys Acta. 2008; 1780: 743-749.
70. Liu B, Fan Z, Edgerton SM, Deng XS, Alimova IN, Lind SE et al Metformin induces unique biological and molecular responses in triple negative breast cancer cells. Cell Cycle. 2009; 8: 2031-2040.
71. Alimova IN, Liu B, Fan Z, Edgerton SM, Dillon T, Lind SE et al. Metformin inhibits breast cancer cell growth, colony formation and induces cell cycle arrest in vitro. Cell Cycle. 2009; 8: 909-915.
72. Appleyard MV, O'Neill MA, Murray KE, Paulin FE, Bray SE, Kernohan NM et al Seliciclib (CYC202, R-roscovitine) enhances the antitumor effect of doxorubicin in vivo in a breast cancer xenograft model. Int J Cancer. 2009; 124: 465-472.
73. Roy S, Gu M, Ramasamy K, Singh RP, Agarwal C, Siriwardana S et al. p21/Cip1 and p27/Kip1 Are essential molecular targets of inositol hexaphosphate for its antitumor efficacy against prostate cancer. Cancer Res. 2009; 69: 1166-1173.
74. Yabuuchi S, Katayose Y, Oda A, Mizuma M, Shirasou S, Sasaki T et al. ZD1839 (IRESSA) stabilizes p27Kip1 and enhances radiosensitivity in cholangiocarcinoma cell lines. Anticancer Res. 2009; 29: 1169-1180.
75. Bertagnolli MM, Warren RS, Niedzwiecki D, Mueller E, Compton CC, Redston M et al. p27Kip1 in stage III colon cancer: implications for outcome following adjuvant chemotherapy in cancer and leukemia group B protocol 89803. Clin Cancer Res. 2009; 15: 2116-2122.
76. Bedard PL, de AE, Cardoso F Beyond trastuzumab: overcoming resistance to targeted HER-2 therapy in breast cancer. Curr Cancer Drug Targets. 2009; 9: 148-162.
77. Cheng M, Olivier P, Diehl JA, Fero M, Roussel MF, Roberts JM et al. The p21(Cip1) and p27(Kip1) CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 1999; 18: 1571-1583.
78. Murakami H, Horihata M, Andojo S, Yoneda-Kato N, Kato JY Isolation and characterization of cytoplasmic cyclin D1 mutants. FEBS Lett. 2009; 583: 1575-1580.
79. Gartel AL p21(WAF1/CIP1) and cancer: a shifting paradigm? Biofactors. 2009; 35: 161-164.
80. Abukhdeir AM, Park BH P21 and p27: roles in carcinogenesis and drug resistance. Expert Rev Mol Med. 2008; 10: e19.
81. Blain SW: Switching cyclin D-Cdk4 kinase activity on and off. Cell Cycle. 2008; 7: 892-898.
82. Chu IM, Hengst L, Slingerland JM The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nat Rev Cancer. 2008; 8: 253-267.
83. Wesierska-Gadek J, Krystof V Selective cyclin-dependent kinase inhibitors discriminating between cell cycle and transcriptional kinases: future reality or utopia? Ann N Y Acad Sci. 2009; 1171: 228-241.
84. Banerjee S, Zhang Y, Ali S, Bhuiyan M, Wang Z, Chiao PJ et al. Molecular evidence for increased antitumor activity of gemcitabine by genistein in vitro and in vivo using an orthotopic model of pancreatic cancer. Cancer Res. 2005; 65: 9064-9072.
85. Banerjee S, Zhang Y, Wang Z, Che M, Chiao PJ, Abbruzzese JL et al In vitro and in vivo molecular evidence of genistein action in augmenting the efficacy of cisplatin in pancreatic cancer. Int J Cancer. 2007; 120: 906-917.
86. Banerjee S, Zhang Y, Ali S, Bhuiyan M, Wang Z, Chiao PJ et al. Molecular evidence for increased antitumor activity of gemcitabine by genistein in vitro and in vivo using an orthotopic model of pancreatic cancer. Cancer Res. 2005; 65: 9064-9072.
87. Banerjee S, Zhang Y, Wang Z, Che M, Chiao PJ, Abbruzzese JL et alIn vitro and in vivo molecular evidence of genistein action in augmenting the efficacy of cisplatin in pancreatic cancer. Int J Cancer. 2007; 120: 906-917.