Sticky siRNAs targeting survivin and cyclin B1 exert an antitumoral effect on melanoma subcutaneous xenografts and lung metastases

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Kedinger, Valerie ^a   Meulle, Aline ^a   Zounib, Omar ^a   Bonnet, Marie Elise ^a   Gossart, Jean Baptiste ^a   Benoit, Elodie ^a   Messmer, Melanie ^b   Shankaranarayanan, Pattabhiraman ^c   Behr, Jean Paul ^a   Erbacher, Patrick ^a   Bolcato Bellemin, Anne Laure ^d  

^a Polyplus transfection SA   (France)

^b INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d IQVIA   (United States)

Author keywords

Cyclin B1; Delivery; Melanoma; Sticky siRNA; Survivin; Tumor inhibition

Indexed keywords

CYCLIN B1; DOXORUBICIN; POLYETHYLENEIMINE; SMALL INTERFERING RNA; SURVIVIN; BIRC5 PROTEIN, MOUSE; CCNB1 PROTEIN, MOUSE; INHIBITOR OF APOPTOSIS PROTEIN; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG DELIVERY SYSTEM; DRUG DOSE COMPARISON; DRUG POTENTIATION; DRUG TARGETING; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; LUNG METASTASIS; M PHASE CELL CYCLE CHECKPOINT; MELANOMA; METASTASIS INHIBITION; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR GROWTH; TUMOR VOLUME; TUMOR XENOGRAFT; WEIGHT REDUCTION; ANIMAL; DISEASE MODEL; DRUG SCREENING; EXPERIMENTAL MELANOMA; GENE THERAPY; GENE TRANSFER; GENETICS; LUNG TUMOR; METABOLISM; NUDE MOUSE; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECONDARY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CYCLIN B1; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; INHIBITOR OF APOPTOSIS PROTEINS; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, NUDE; POLYETHYLENEIMINE; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84880021823     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-338     Document Type: Article

References (48)

1. Nguyen DX, Bos PD, Massague J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 2009, 9(4):274-284. 10.1038/nrc2622, 19308067.
2. Zheng Y, Fernando HC. Surgical and nonresectional therapies for pulmonary metastasis. The Surg Clin North Am 2010, 90(5):1041-1051.
3. Soengas MS, Lowe SW. Apoptosis and melanoma chemoresistance. Oncogene 2003, 22(20):3138-3151. 10.1038/sj.onc.1206454, 12789290.
4. Ambrosini G, Adida C, Altieri DC. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 1997, 3(8):917-921. 10.1038/nm0897-917, 9256286.
5. Grossman D, McNiff JM, Li F, Altieri DC. Expression and targeting of the apoptosis inhibitor, survivin, in human melanoma. J Invest Dermatol 1999, 113(6):1076-1081. 10.1046/j.1523-1747.1999.00776.x, 10594755.
6. McKenzie JA, Grossman D. Role of the apoptotic and mitotic regulator survivin in melanoma. Anticancer Res 2012, 32(2):397-404.
7. Altieri DC. Validating survivin as a cancer therapeutic target. Nat Rev Cancer 2003, 3(1):46-54. 10.1038/nrc968, 12509766.
8. Gradilone A, Gazzaniga P, Ribuffo D, Scarpa S, Cigna E, Vasaturo F, Bottoni U, Innocenzi D, Calvieri S, Scuderi N, et al. Survivin, bcl-2, bax, and bcl-X gene expression in sentinel lymph nodes from melanoma patients. J Clin Oncol 2003, 21(2):306-312. 10.1200/JCO.2003.08.066, 12525523.
9. Wheatley SP, McNeish IA. Survivin: a protein with dual roles in mitosis and apoptosis. Int Rev Cytol 2005, 247:35-88.
10. Thomas J, Liu T, Cotter MA, Florell SR, Robinette K, Hanks AN, Grossman D. Melanocyte expression of survivin promotes development and metastasis of UV-induced melanoma in HGF-transgenic mice. Cancer Res 2007, 67(11):5172-5178. 10.1158/0008-5472.CAN-06-3669, 2292453, 17545596.
11. Mehrotra S, Languino LR, Raskett CM, Mercurio AM, Dohi T, Altieri DC. IAP regulation of metastasis. Cancer Cell 2010, 17(1):53-64. 10.1016/j.ccr.2009.11.021, 2818597, 20129247.
12. McKenzie JA, Liu T, Goodson AG, Grossman D. Survivin enhances motility of melanoma cells by supporting Akt activation and {alpha}5 integrin upregulation. Cancer Res 2010, 70(20):7927-7937. 10.1158/0008-5472.CAN-10-0194, 2955769, 20807805.
13. Pennati M, Folini M, Zaffaroni N. Targeting survivin in cancer therapy: fulfilled promises and open questions. Carcinogenesis 2007, 28(6):1133-1139. 10.1093/carcin/bgm047, 17341657.
14. Nakahara T, Kita A, Yamanaka K, Mori M, Amino N, Takeuchi M, Tominaga F, Hatakeyama S, Kinoyama I, Matsuhisa A, et al. YM155, a novel small-molecule survivin suppressant, induces regression of established human hormone-refractory prostate tumor xenografts. Cancer Res 2007, 67(17):8014-8021. 10.1158/0008-5472.CAN-07-1343, 17804712.
15. Talbot DC, Ranson M, Davies J, Lahn M, Callies S, Andre V, Kadam S, Burgess M, Slapak C, Olsen AL, et al. Tumor survivin is downregulated by the antisense oligonucleotide LY2181308: a proof-of-concept, first-in-human dose study. Clin Cancer Res 2010, 16(24):6150-6158. 10.1158/1078-0432.CCR-10-1932, 21041181.
16. Pennati M, Colella G, Folini M, Citti L, Daidone MG, Zaffaroni N. Ribozyme-mediated attenuation of survivin expression sensitizes human melanoma cells to cisplatin-induced apoptosis. J Clin Invest 2002, 109(2):285-286. 150847, 11805141.
17. O'Connor DS, Grossman D, Plescia J, Li F, Zhang H, Villa A, Tognin S, Marchisio PC, Altieri DC. Regulation of apoptosis at cell division by p34cdc2 phosphorylation of survivin. Proc Natl Acad Sci USA 2000, 97(24):13103-13107. 10.1073/pnas.240390697, 27185, 11069302.
18. Castedo M, Perfettini JL, Roumier T, Kroemer G. Cyclin-dependent kinase-1: linking apoptosis to cell cycle and mitotic catastrophe. Cell Death Differ 2002, 9(12):1287-1293. 10.1038/sj.cdd.4401130, 12478465.
19. Soria JC, Jang SJ, Khuri FR, Hassan K, Liu D, Hong WK, Mao L. Overexpression of cyclin B1 in early-stage non-small cell lung cancer and its clinical implication. Cancer Res 2000, 60(15):4000-4004.
20. Hassan KA, Ang KK, El-Naggar AK, Story MD, Lee JI, Liu D, Hong WK, Mao L. Cyclin B1 overexpression and resistance to radiotherapy in head and neck squamous cell carcinoma. Cancer Res 2002, 62(22):6414-6417.
21. Korenaga D, Takesue F, Yasuda M, Honda M, Nozoe T, Inutsuka S. The relationship between cyclin B1 overexpression and lymph node metastasis in human colorectal cancer. Surgery 2002, 131:S114-S120. 10.1067/msy.2002.119362, 11821797.
22. Takeno S, Noguchi T, Kikuchi R, Uchida Y, Yokoyama S, Muller W. Prognostic value of cyclin B1 in patients with esophageal squamous cell carcinoma. Cancer 2002, 94(11):2874-2881. 10.1002/cncr.10542, 12115375.
23. Yasuda M, Takesue F, Inutsuka S, Honda M, Nozoe T, Korenaga D. Overexpression of cyclin B1 in gastric cancer and its clinicopathological significance: an immunohistological study. J Cancer Res Clin Oncol 2002, 128(8):412-416. 10.1007/s00432-002-0359-9, 12200597.
24. Wang A, Yoshimi N, Ino N, Tanaka T, Mori H. Overexpression of cyclin B1 in human colorectal cancers. J Cancer Res Clin Oncol 1997, 123(2):124-127. 10.1007/BF01269891, 9030252.
25. Kallakury BV, Sheehan CE, Rhee SJ, Fisher HA, Kaufman RP, Rifkin MD, Ross JS. The prognostic significance of proliferation-associated nucleolar protein p120 expression in prostate adenocarcinoma: a comparison with cyclins A and B1, Ki-67, proliferating cell nuclear antigen, and p34cdc2. Cancer 1999, 85(7):1569-1576. 10.1002/(SICI)1097-0142(19990401)85:7<1569::AID-CNCR19>3.0.CO;2-M, 10193948.
26. Allan K, Jordan RC, Ang LC, Taylor M, Young B. Overexpression of cyclin A and cyclin B1 proteins in astrocytomas. Arch Pathol Lab Med 2000, 124(2):216-220.
27. Kuhling H, Alm P, Olsson H, Ferno M, Baldetorp B, Parwaresch R, Rudolph P. Expression of cyclins E, A, and B, and prognosis in lymph node-negative breast cancer. J Pathol 2003, 199(4):424-431. 10.1002/path.1322, 12635132.
28. Georgieva J, Sinha P, Schadendorf D. Expression of cyclins and cyclin dependent kinases in human benign and malignant melanocytic lesions. J Clin Pathol 2001, 54(3):229-235. 10.1136/jcp.54.3.229, 1731381, 11253137.
29. Yuan J, Yan R, Kramer A, Eckerdt F, Roller M, Kaufmann M, Strebhardt K. Cyclin B1 depletion inhibits proliferation and induces apoptosis in human tumor cells. Oncogene 2004, 23(34):5843-5852. 10.1038/sj.onc.1207757, 15208674.
30. Ozeki M, Tamae D, Hou DX, Wang T, Lebon T, Spitz DR, Li JJ. Response of cyclin B1 to ionizing radiation: regulation by NF-kappaB and mitochondrial antioxidant enzyme MnSOD. Anticancer Res 2004, 24(5A):2657-2663.
31. Li Z, Xia L, Lee LM, Khaletskiy A, Wang J, Wong JY, Li JJ. Effector genes altered in MCF-7 human breast cancer cells after exposure to fractionated ionizing radiation. Radiat Res 2001, 155(4):543-553. 10.1667/0033-7587(2001)155[0543:EGAIMH]2.0.CO;2, 11260656.
32. Bolcato-Bellemin AL, Bonnet ME, Creusat G, Erbacher P, Behr JP. Sticky overhangs enhance siRNA-mediated gene silencing. Proc Natl Acad Sci USA 2007, 104(41):16050-16055. 10.1073/pnas.0707831104, 2042160, 17913877.
33. Yuan J, Kramer A, Matthess Y, Yan R, Spankuch B, Gatje R, Knecht R, Kaufmann M, Strebhardt K. Stable gene silencing of cyclin B1 in tumor cells increases susceptibility to taxol and leads to growth arrest in vivo. Oncogene 2006, 25(12):1753-1762. 10.1038/sj.onc.1209202, 16278675.
34. Wolanin K, Magalska A, Mosieniak G, Klinger R, McKenna S, Vejda S, Sikora E, Piwocka K. Curcumin affects components of the chromosomal passenger complex and induces mitotic catastrophe in apoptosis-resistant Bcr-Abl-expressing cells. Mol Cancer Res 2006, 4(7):457-469. 10.1158/1541-7786.MCR-05-0172, 16849521.
35. Shrayer D, Bogaars H, Gersten D, Hearing V, Maizel A, Wanebo H. Nude mouse model to study passive humoral immunotherapy directed against B16 F10 murine melanoma. J Surg Oncol 1994, 57(1):50-56. 10.1002/jso.2930570114, 8065154.
36. Altieri DC. Targeting survivin in cancer. Cancer Lett 2013, 332(2):225-228. 10.1016/j.canlet.2012.03.005, 22410464.
37. Dif F, Djediat C, Alegria O, Demeneix B, Levi G. Transfection of multiple pulmonary cell types following intravenous injection of PEI-DNA in normal and CFTR mutant mice. J Gene Med 2006, 8(1):82-89. 10.1002/jgm.831, 16142827.
38. Zou SM, Erbacher P, Remy JS, Behr JP. Systemic linear polyethylenimine (L-PEI)-mediated gene delivery in the mouse. J Gene Med 2000, 2(2):128-134. 10.1002/(SICI)1521-2254(200003/04)2:2<128::AID-JGM95>3.0.CO;2-W, 10809146.
39. Ge Q, Filip L, Bai A, Nguyen T, Eisen HN, Chen J. Inhibition of influenza virus production in virus-infected mice by RNA interference. Proc Natl Acad Sci USA 2004, 101(23):8676-8681. 10.1073/pnas.0402486101, 423254, 15173599.
40. Gunther M, Lipka J, Malek A, Gutsch D, Kreyling W, Aigner A. Polyethylenimines for RNAi-mediated gene targeting in vivo and siRNA delivery to the lung. Eur J Pharm Biopharm 2011, 77(3):438-449. 10.1016/j.ejpb.2010.11.007, 21093588.
41. Vachtenheim J, Borovansky J. "Transcription physiology" of pigment formation in melanocytes: central role of MITF. Exp Dermatol 2010, 19(7):617-627. 10.1111/j.1600-0625.2009.01053.x, 20201954.
42. Grossman D, Altieri DC. Drug resistance in melanoma: mechanisms, apoptosis, and new potential therapeutic targets. Cancer Metastasis Rev 2001, 20(1-2):3-11.
43. Hortobagyi GN. Anthracyclines in the treatment of cancer. An overview. Drugs 1997, 54(4):1-7.
44. Trabulo S, Cardoso AM, Santos-Ferreira T, Cardoso AL, Simoes S, de Lima MC P. Survivin silencing as a promising strategy to enhance the sensitivity of cancer cells to chemotherapeutic agents. Mol Pharm 2011, 8(4):1120-1131. 10.1021/mp100426e, 21619051.
45. Chen S, Liu X, Gong W, Yang H, Luo D, Zuo X, Li W, Wu P, Liu L, Xu Q, et al. Combination therapy with VEGFR2 and EGFR siRNA enhances the antitumor effect of cisplatin in non-small cell lung cancer xenografts. Oncol Rep 2013, 29(1):260-268.
46. Velculescu VE, Madden SL, Zhang L, Lash AE, Yu J, Rago C, Lal A, Wang CJ, Beaudry GA, Ciriello KM, et al. Analysis of human transcriptomes. Nat Genet 1999, 23(4):387-388.
47. Dutta A, Chandra R, Leiter LM, Lester S. Cyclins as markers of tumor proliferation: immunocytochemical studies in breast cancer. Proc Natl Acad Sci USA 1995, 92(12):5386-5390. 10.1073/pnas.92.12.5386, 41699, 7539916.
48. Bonnet ME, Erbacher P, Bolcato-Bellemin AL. Systemic delivery of DNA or siRNA mediated by linear polyethylenimine (L-PEI) does not induce an inflammatory response. Pharm Res 2008, 25(12):2972-2982. 10.1007/s11095-008-9693-1, 18709489.