Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells

Autophagy

Volumn 4, Issue 5, 2008, Pages 669-679

  Akar, Ugur ^a   Chaves Reyez, Arturo ^a   Barria, Magaly ^a   Tari, Ana ^a   Sanguino, Angela ^a   Kondo, Yasuko ^a   Kondo, Seiji ^a   Arun, Banu ^a   Lopez Berestein, Gabriel ^a   Ozpolat, Bulent ^a  

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

Author keywords

Apoptosis; Autophagy; Bcl 2; Beclin 1; Breast cancer; siRNA

Indexed keywords

ACRIDINE ORANGE; CELL PROTEIN; DOXORUBICIN; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; PROTEIN ATG5; PROTEIN BCL 2; PROTEIN LC3 II; SMALL INTERFERING RNA;

ARTICLE; AUTOPHAGY; BREAST CANCER; CELL DEATH; CELL GROWTH; CELL STRAIN MCF 7; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; IC 50; LIGHT CHAIN; PROTEIN EXPRESSION; PROTEIN INDUCTION;

EID: 48249087666     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.6083     Document Type: Article

References (66)

1. Legha SS, Buzdar AU, Smith TL, Hortobagyi GN, Swenerton KD, Blumenschein GR, Gehan EA, Bodey GP, Freireich EJ. Complete remissions in metastatic breast cancer treated with combination drug therapy. Ann Intern Med 1979; 91:847-52.
2. Valero V, Buzdar AU, McNeese M, Singletary E, Horyobagyi GN. Primary chemotherapy in the treatment of breast cancer: the University of Texas M.D. Anderson Cancer Center experience. Clin Breast Cancer 2002; 3 Suppl 2:S63-8.
3. Hockenbery D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 1990; 348:334-6.
4. Wang CW, Klionsky DJ. The molecular mechanism of autophagy. Mol Med 2003; 8:65-76.
5. Kerr JF, Winterford CM, Harmon BV. Apoptosis. Its significance in cancer and cancer therapy. Cancer 1994; 73:2013-26.
6. Buchholz, T, Davis, D, McConkey, DJ, Symmans, F, Valero, V, Tucker, SL, Pusztai, L, Cristofanilli, M, Esteva, FJ, Hortobagyi, G, Sahin, A. The nuclear transcription factor KB/bcl-2 pathway correlates with pathologic complete response to doxorubicin-based neoadjuvant chemotherapy in human breast cancer. Clinical Cancer Research 2005; 11:8398-402.
7. Reed JC, Cuddy M, Slabiak T, Croce CM, Nowell PC. Oncogenic potential of bcl-2 demonstrated by gene transfer. Nature 1988; 336:259-61.
8. Tsujimoto Y, Cossman J, Jaffe E, Croce CM. Involvement of the bcl-2 gene in human follicular lymphoma. Science 1985; 228:1440-3.
9. Reed JC, Kitada S, Takayama S, Miyashita T. Regulation of chemoresistance by the bcl-2 oncoprotein in non-Hodgkin's lymphoma and lymphocytic leukemia cell lines. Ann Oncol 1994; 5 Suppl 1:61-5.
10. Kitada S, Takayama S, De Riel K, Tanaka S, Reed JC. Reversal of chemoresistance of lymphoma cells by antisense-mediated reduction of bcl-2 gene expression. Antisense Res Dev 1994; 4:71-9.
11. Ohbu M, Saegusa M, Kobayashi N, Tsukamoto H, Mieno H, Kakita A, Okayasu I. Expression of bcl-2 protein in esophageal squamous cell carcinomas and its association with lymph node metastasis. Cancer 1997; 79:1287-93.
12. Pattingre S, Tassa A, Qu XP, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122:927-39.
13. Kroemer G, Jaattela M. Lysosomes and autophagy in cell death control. Nat Rev Cancer 2005; 5:886-97.
14. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6:463-77.
15. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5:726-34.
16. Daido, S, Kanzawa, T, Yamamoto, A, Takeuchi, H, Kondo, Y, Kondo S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res 2004; 64:4286-93.
17. Edinger AL, Thompson, CB. Defective autophagy leads to cancer. Cancer Cell 2003; 4:422-4.
18. Toth S, Nagy K, Palfia Z, Rez G. Cellular autophagic capacity changes during azaserine-induced tumour progression in the rat pancreas. Up-regulation in all premalignant stages and down-regulation with loss of cycloheximide sensitivity of segregation along with malignant transformation. Cell Tissue Res 2002; 309:409-16.
19. Liang XH, Jackson S, Seaman M, Brown K, Kemplex B, Hibshoos H, Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin1. Nature 1999; 402;672-77.
20. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen E-L, Mizushima N, Ohsumi Y, Levine B. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003; 112:1809-20.
21. Futreal PA., Söderkvist P, Marks JR, Iglehart JD, Cochran C, Barrett JC, Wiseman RW. Detection of frequent allelic loss on proximal chromosome 17q in sporadic breast carcinoma using microsatellite length polymorphisms. Cancer Res 1992; 52:2624-7.
22. Saito H, Inazawa S, Kasmuni F, Koi S, Sagae S, Kudo R, Saito J, Noda K, Nakamura Y. Detailed deletion mapping of chromosome 17q in ovarian and breast cancers: 2-cM region on 17q21.3 often and commonly deleted in tumors. Cancer Res 1993; 53:3382-5.
23. Fire A, et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391:806-11.
24. Elbashir SM, et al. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001; 411:494-8.
25. Yin JQ, Gao J, Shao R, Tian WN, Wang J, Wan Y. siRNA agents inhibit oncogene expression and attenuate human tumor cell growth. J Exp Ther Oncol 2003; 3:194-204.
26. Ryther RC, Flynt AS, Phillips JA 3rd, Patton JG. siRNA therapeutics: big potential from small RNAs. Gene Ther 2005;12:5-11.
27. Uchida H, et al. Adenovirus-mediated transfer of siRNA against survivin induced apoptosis and attenuated tumor cell growth in vitro and in vivo. Mol Ther 2004; 10:162-71.
28. Reich SJ, et al. Small interfering RNA (siRNA) targeting VEGF effectively inhibits ocular neovascularization in a mouse model. Mol Vis 2003; 9:210-6.
29. Landen CN, Chavez-Reyes A, Bucana C, Schmandt R, Deavers MT, Lopez-Berestein G, Sood AK. Therapeutic EphA2 gene targeting in vivo using neutral liposomal small interfering RNA delivery. Cancer Res 2005; 65:6910-518.
30. Halder JB, Kamat AA, Landen CN, Han LY, Lutgendorf SK, Lin YG, Merritt WM, Jennings NB, Chavez-Reyes A, Coleman RL, Gershenson DM, Schmandt R, Cole SW, Lopez-Berestein G, Sood AK. Focal adhesion kinase targeting for therapy of ovarian carcinoma using in vivo siRNA delivery in neutral liposomes. Clin Cancer Res 2006; 12:4916-24.
31. Akar U, Ozpolat O, Mehta K, Fok J, Kondo Y, Lopez-Berestein G. Tissue transglutaminase inhibits autophagy in pancreatic cancer cells. Mol Cancer Res 2007; 5:241-49
32. Ozpolat B, Akar U, Steiner M, Zorilla-Calancho I, Tirado-Gomez M, Colburn N, Danilenko M, Lopez Berestein G. Programmed cell death-4 tumor suppressor protein contributes to retinoic acid induced terminal granulocytic differentiation of human myeloid leukemia cells. Mol Cancer Res 2007; 5:95-108.
33. Tormo M, Tari AM, McDonnell TJ, Cabanillas F, Garcia-Conde J, Lopez-Berestein G. Apoptotic induction in transformed follicular lymphoma cells by bcl-2 downregulation. Leuk Lymphoma 1998; 30:367-79.
34. Konopleva M, Tari AM, Esrrov Z, Harris D, Xie Z, Zhao S, Lopez-Berestein G, Andreeff M. Liposomal Bcl-2 antisense oligonucleotides sensitize acute myeloid leukemia to cytosine-arabinoside, and induce apoptosis independent of other antiapoptotic proteins. Blood 2000; 95:3929-38.
35. Yde CW, Issinger OG. Enhancing cisplatin sensitivity in MCF-7 human breast cancer cells by down-regulation of Bcl-2 and cyclin D1. Int J Oncol 2006; 29:1397-404.
36. Lima RT, Martins LM, Guimaraes JE, Sambade C, Vasconcelos MH. Specific downregulation of bcl-2 and XIAP by RNAi enhances the effects of chemotherapeutic agents in MCF-7 human breast cancer cells. Cancer Gene Ther 2004; 11:309-16.
37. Lu L, Osmond DG. Apoptosis during B lymphopoiesis in mouse bone marrow. J Immunol 1997; 158:5136-45.
38. Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, et al. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol 1999; 147:435-46.
39. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720-8.
40. Teixeira C, Reed JC, Pratt MA. Estrogen promotes chemotherapeutic drug resistance by a mechanism involving Bcl-2 proto-oncogene expression in human breast cancer cells. Cancer Res 1995; 55:3902-7.
41. Herod JJ, Eliopoulos AG, Warwick J, Niedobitek G, Young LS, Kerr DJ. The prognostic significance of Bcl-2 and p53 expression in ovarian carcinoma. Cancer Res 1996; 56:2178-84.
42. Karakas T, Maurer U, Weidman E, Miething CC, Hoelzer D, Bergmann L. High expression of bcl-2 mRNA as a determinant of poor prognosis in acute myeloid leukemia. Ann Oncol 1998; 9:159-65.
43. Reed JC. Regulation of apoptosis by bcl-2 family proteins and its role in cancer and chemoresistance. Curr Opin Oncol 1995; 7:541-6.
44. Nunez G, Seto M, Seremetis S, Ferrero D, Grignani F, Korsmeyer SJ, Dalla-Favera R. Growth- and tumor-promoting effects of deregulated BCL2 in human B-lymphoblastoid cells. Proc Nat Acad Sci USA 1989; 86:4589-93.
45. Cotter FE, Johnson P, Hall P, Pocock C, al Mahdi N, Cowell JK, Morgan G. Antisense oligonucleotides suppress B-cell lymphoma growth in a SCID-hu mouse model. Oncogene 1994; 9:3049-55.
46. Emi M, Kim R, Tanabe K, Uchida Y, Toge T. Targeted therapy against Bcl-2-related proteins in breast cancer cells. Breast Cancer Res 2005; 7: R940-52.
47. Bartholomeusz C, Itamochi H, Yuan XH, Esteva FJ, Wood CG, Terakawa N, Hung MC, Ueno NT. Bcl-2 antisense oligonucleotide overcomes resistance to E1A gene therapy in a low-HER2-expressing ovarian cancer xenograft model. Cancer Res 2005; 65;8406-13.
48. Basma H, El-Refaey H, Sgagias MK, Cowan K, Luo X, Cheng P-W. Bcl-2 antisense and cisplatin combination treatment of MCF-7 breast cancer cells with or without functional p53. J Biomed Sci 2005; 12:999-1011.
49. Dorsett Y, Tuschl T. siRNAs: applications in functional genomics and potential as therapeutics. Nat Rev Drug Discov 2004; 3:318-29.
50. Anderson EM, Miller P, Ilsley D, Marshall W, Khvarova A, Stein CA, Benimetskaya L. Gene profiling study of G3139- and Bcl-2-targeting siRNAs identifies a unique G3139 molecular signature. Cancer Gene Ther 2006; 13:406-14.
51. Saeki K, Yuo A, Okuma E, Yazaki Y, Susin SA, Kroemer G, Takaku F. Bcl-2 down-regulation causes autophagy in a caspase-independent manner in human leukemic HL60 cells. Cell Death Differ 2000; 7:1263-9.
52. Høyer-Hansen M, Bastholm L, Mathiasen IS, Elling F, Jäättelä M. Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ 2005; 12:1297-309.
53. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, Domingo D, Yahalom J. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 2001; 61: 439-44.
54. Kottke TJ, Blajeski AL, Meng XW, Svingen PA, Ruchaud S, Mesner Jr PW, et al. Lack of correlation between caspase activation and caspase activity assays in paclitaxel-treated MCF-7 breast cancer cells. J Biol Chem 2002; 277:804-15.
55. Wang D, McDonnell MA, Kelekar A. Multi-probe RPA template sets to study RNA modulation and transcriptional control of BH3-only members of the Bcl-2 family. Cancer Detect Prev 2005; 29:189-200.
56. Bursch W, Ellinger A, Kienzl H, Torok L, Pandey S, Sikorska M, Walker R, Hermann RS. Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 1996; 17:1595-607.
57. Opipari AW Jr, Tan L, Boitano AE, Sorenson DR, Aurora A, Liu JR. Resveratrol-induced autophagocytosis in ovarian cancer cells. Cancer Res2004; 64:696-703.
58. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ 2004; 11:448-57.
59. Jia L, Dourmashkin RR, Allen PD, Gray AB, Newland AC, Kelsey SM. Inhibition of autophagy abrogates tumour necrosis factor alpha induced apoptosis in human T-lymphoblastic leukaemic cells. Br J Haematol 1997; 98:673-85.
60. Komata T, Kanzawa T, Nashimoto T, Aoki H, Endo S, Nameta M, Takahashi H, Yamamoto T, Kondo S, Tanaka R. Mild heat shock induces autophagic growth arrest, but not apoptosis in U251-MG and U87-MG human malignant glioma cells. J Neurooncol 2004; 68:101-11.
61. Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 2004; 7:167-78.
62. Tanabe K, Kim R, Inoue H, Emi M, Uchida Y, Toge T. Antisense Bcl-2 and HER-2 oligonucleotide Treatment of breast cancer cells enhances their sensitivity to anticancer drugs. Int J Oncol 2003; 22:875-81.
63. Chi KC, Wallis AE, Lee CH, De Menezes DL, Sartor J, Dragowska WH, Mayer LD. Effects of Bcl-2 modulation with G3139 antisense oligonucleotide on human breast cancer cells are independent of inherent Bcl-2 protein expression. Breast Cancer Res Treat 2000; 63:199-212.
64. Buchholz T, Davis D, McConkey DJ, Symmans F, Valero V, Tucker SL, Pusztai L, Cristofanilli M, Esteva FJ, Hortobagyi G, Sahin A. Chemotherapy-induced apoptosis and Bcl-2 levels correlate with breast cancer response to chemotherapy. Cancer J 2003; 9:33-41.
65. Pusztai L, Krishnamurti S, Perez Cardona J, Sneige N, Esteva FJ, Volchenok M, Breitenfelder P, Kau SW, Takayama S, Krajewski S, Reed JC, Bast RC Jr, Hortobagyi GN. Expression of BAG-1 and BcL-2 proteins before and after neoadjuvant chemotherapy of locally advanced breast cancer. Cancer Invest 2004; 22:248-56.
66. Ozpolat B, Akar, U Steiner M, Zorrilla-Calancha, I , SanguinoA, Tirado-Gomez M, Nancy Colburn,Danilenko M,and Lopez Beresrein G. Programmed Cell death 4 (PDCD4) tumor suppressor protein is involved in granulocytic differentiation of myeloid leukemia cells. Mol Cancer Res 2007; 5:95-108