Therapeutic targeting of polo-like kinase 1 using RNA-interfering nanoparticles (iNOPs) for the treatment of non-small cell lung cancer

Oncotarget

Volumn 6, Issue 14, 2015, Pages 12020-12034

  McCarroll, Joshua A ^a,b   Dwarte, Tanya ^a   Baigude, Huricha ^c   Dang, Jason ^c,d   Yang, Lu ^a   Erlich, Rafael B ^a,b   Kimpton, Kathleen ^a   Teo, Joann ^a,b   Sagnella, Sharon M ^a,b   Akerfeldt, Mia C ^a   Liu, Jie ^b   Phillips, Phoebe A ^b   Rana, Tariq M ^c,d   Kavallaris, Maria ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Interfering nanoparticles; Non small cell lung cancer; Orthotopic non small cell lung cancer mouse model; Polo like kinase 1; SiRNA

Indexed keywords

CASPASE 3; CASPASE 7; INTERFERING NANOPARTICLE 7; NANOPARTICLE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; POLO LIKE KINASE 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; ONCOPROTEIN; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL DEATH; DRUG TARGETING; ENZYME ACTIVITY; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR VOLUME; ANIMAL; CARCINOMA, NON-SMALL-CELL LUNG; CELL PROLIFERATION; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; LUNG NEOPLASMS;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE PROTEINS; CELL PROLIFERATION; HUMANS; LUNG NEOPLASMS; MICE; NANOPARTICLES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84931335566     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2664     Document Type: Article

References (40)

1. Aisner DL, Marshall CB. Molecular pathology of non-small cell lung cancer: a practical guide. American journal of clinical pathology. 2012; 138:332-346.
2. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012; 380:2095-2128.
3. Kavallaris M. Microtubules and resistance to tubulin-binding agents. Nature reviews Cancer. 2010; 10:194-204.
4. Medema RH, Lin CC, Yang JC. Polo-like kinase 1 inhibitors and their potential role in anticancer therapy, with a focus on NSCLC. Clinical cancer research: an official journal of the American Association for Cancer Research. 2011; 17:6459-6466.
5. Cholewa BD, Liu X, Ahmad N. The role of polo-like kinase 1 in carcinogenesis: cause or consequence?. Cancer research. 2013; 73:6848-6855.
6. Wang ZX, Xue D, Liu ZL, Lu BB, Bian HB, Pan X, Yin YM. Overexpression of polo-like kinase 1 and its clinical significance in human non-small cell lung cancer. The international journal of biochemistry & cell biology. 2012; 44:200-210.
7. Tan J, Li Z, Lee PL, Guan P, Aau MY, Lee ST, Feng M, Lim CZ, Lee EY, Wee ZN, Lim YC, Karuturi RK, Yu Q. PDK1 signaling toward PLK1-MYC activation confers oncogenic transformation, tumor-initiating cell activation, and resistance to mTOR-targeted therapy. Cancer Discov. 3:1156-1171.
8. Wierer M, Verde G, Pisano P, Molina H, Font-Mateu J, Di Croce L, Beato M. PLK1 signaling in breast cancer cells cooperates with estrogen receptor-dependent gene transcription. Cell Rep. 3:2021-2032.
9. Hu K, Law JH, Fotovati A, Dunn SE. Small interfering RNA library screen identified polo-like kinase-1 (PLK1) as a potential therapeutic target for breast cancer that uniquely eliminates tumor-initiating cells. Breast cancer research: BCR. 2012; 14:R22.
10. Lee C, Fotovati A, Triscott J, Chen J, Venugopal C, Singhal A, Dunham C, Kerr JM, Verreault M, Yip S, Wakimoto H, Jones C, Jayanthan A, Narendran A, Singh SK, Dunn SE. Polo-like kinase 1 inhibition kills glioblastoma multiforme brain tumor cells in part through loss of SOX2 and delays tumor progression in mice. Stem cells (Dayton, Ohio). 2012; 30:1064-1075.
11. Haupenthal J, Bihrer V, Korkusuz H, Kollmar O, Schmithals C, Kriener S, Engels K, Pleli T, Benz A, Canamero M, Longerich T, Kronenberger B, Richter S, Waidmann O, Vogl TJ, Zeuzem S, et al. Reduced efficacy of the Plk1 inhibitor BI 2536 on the progression of hepatocellular carcinoma due to low intratumoral drug levels. Neoplasia. 2012; 14:410-419.
12. Steegmaier M, Hoffmann M, Baum A, Lenart P, Petronczki M, Krssak M, Gurtler U, Garin-Chesa P, Lieb S, Quant J, Grauert M, Adolf GR, Kraut N, Peters JM, Rettig WJ. BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo Curr Biol. 2007; 17:316-322.
13. Lu B, Mahmud H, Maass AH, Yu B, van Gilst WH, de Boer RA, Sillje HH. The Plk1 inhibitor BI 236 temporarily arrests primary cardiac fibroblasts in mitosis and generates aneuploidy in vitro. PloS one. 2010; 5:e12963.
14. Rana TM. Illuminating the silence: understanding the structure and function of small RNAs. Nature reviews Molecular cell biology. 2007; 8:23-36.
15. McCarroll J, Teo J, Boyer C, Goldstein D, Kavallaris M, Phillips PA. Potential applications of nanotechnology for the diagnosis and treatment of pancreatic cancer. Frontiers in physiology. 2014; 5:2.
16. Coelho T, Adams D, Silva A, Lozeron P, Hawkins PN, Mant T, Perez J, Chiesa J, Warrington S, Tranter E, Munisamy M, Falzone R, Harrop J, Cehelsky J, Bettencourt BR, Geissler M, et al. Safety and efficacy of RNAi therapy for transthyretin amyloidosis. The New England journal of medicine. 2013; 369:819-829.
17. Davis ME, Zuckerman JE, Choi CH, Seligson D, Tolcher A, Alabi CA, Yen Y, Heidel JD, Ribas A. Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature. 2010; 464:1067-1070.
18. Tabernero J, Shapiro GI, LoRusso PM, Cervantes A, Schwartz GK, Weiss GJ, Paz-Ares L, Cho DC, Infante JR, Alsina M, Gounder MM, Falzone R, Harrop J, White AC, Toudjarska I, Bumcrot D, et al. First-in-humans trial of an RNA interference therapeutic targeting VEGF and KSP in cancer patients with liver involvement. Cancer Discov. 2013; 3:406-417.
19. Baigude H, McCarroll J, Yang CS, Swain PM, Rana TM. Design and creation of new nanomaterials for therapeutic RNAi. ACS chemical biology. 2007; 2:237-241.
20. Baigude H, Rana TM. Delivery of therapeutic RNAi by nanovehicles. Chembiochem: a European journal of chemical biology. 2009; 10:2449-2454.
21. Baigude H, Rana TM. Interfering nanoparticles for silencing microRNAs. Methods in enzymology. 2012; 509:339-353.
22. Su J, Baigude H, McCarroll J, Rana TM. Silencing microRNA by interfering nanoparticles in mice. Nucleic acids research. 2011; 39:e38.
23. Stella GM, Luisetti M, Pozzi E, Comoglio PM. Oncogenes in non-small-cell lung cancer: emerging connections and novel therapeutic dynamics. Lancet Respir Med. 1:251-261.
24. Cheng MW, Wang BC, Weng ZQ, Zhu XW. Clinicopathological significance of Polo-like kinase 1 (PLK1) expression in human malignant glioma. Acta histochemica. 2012; 114:503-509.
25. He ZL, Zheng H, Lin H, Miao XY, Zhong DW. Overexpression of polo-like kinase1 predicts a poor prognosis in hepatocellular carcinoma patients. World journal of gastroenterology: WJG. 2009; 15:4177-4182.
26. King SI, Purdie CA, Bray SE, Quinlan PR, Jordan LB, Thompson AM, Meek DW. Immunohistochemical detection of Polo-like kinase-1 (PLK1) in primary breast cancer is associated with TP53 mutation and poor clinical outcom. Breast cancer research: BCR. 2012; 14:R40.
27. Triscott J, Lee C, Foster C, Manoranjan B, Pambid MR, Berns R, Fotovati A, Venugopal C, O'Halloran K, Narendran A, Hawkins C, Ramaswamy V, Bouffet E, Taylor MD, Singhal A, Hukin J, et al. Personalizing the treatment of pediatric medulloblastoma: Polo-like kinase 1 as a molecular target in high-risk children. Cancer research. 2013; 73:6734-6744.
28. Zhang Z, Zhang G, Kong C. High expression of polo-like kinase 1 is associated with the metastasis and recurrence in urothelial carcinoma of bladder. Urologic oncology. 2013; 31:1222-1230.
29. Guan R, Tapang P, Leverson JD, Albert D, Giranda VL, Luo Y. Small interfering RNA-mediated Polo-like kinase 1 depletion preferentially reduces the survival of p53-defective, oncogenic transformed cells and inhibits tumor growth in animals. Cancer research. 2005; 65:2698-2704.
30. Luo J, Emanuele MJ, Li D, Creighton CJ, Schlabach MR, Westbrook TF, Wong KK, Elledge SJ. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell. 2009; 137:835-848.
31. Onn A, Isobe T, Itasaka S, Wu W, O'Reilly MS, Ki Hong W, Fidler IJ, Herbst RS. Development of an orthotopic model to study the biology and therapy of primary human lung cancer in nude mice. Clinical cancer research: an official journal of the American Association for Cancer Research. 2003; 9:5532-5539.
32. Mukherjee SP, Byrne HJ. Polyamidoamine dendrimer nanoparticle cytotoxicity, oxidative stress, caspase activation and inflammatory response: experimental observation and numerical simulation. Nanomedicine. 9:202-211.
33. Baigude H, Su J, McCarroll J, Rana TM. In Vivo Delivery of RNAi by Reducible Interfering Nanoparticles (iNOPs). ACS Med Chem Lett. 4:720-723.
34. Boyer C, Teo J, Phillips P, Erlich RB, Sagnella S, Sharbeen G, Dwarte T, Duong HT, Goldstein D, Davis TP, Kavallaris M, McCarroll J. Effective delivery of siRNA into cancer cells and tumors using well-defined biodegradable cationic star polymers. Molecular pharmaceutics. 2013; 10:2435-2444.
35. Byrne FL, Yang L, Phillips PA, Hansford LM, Fletcher JI, Ormandy CJ, McCarroll JA, Kavallaris M. RNAi-mediated stathmin suppression reduces lung metastasis in an orthotopic neuroblastoma mouse model. Oncogene. 2014; 33:882-890.
36. McCarroll JA, Gan PP, Liu M, Kavallaris M. betaIII-tubulin is a multifunctional protein involved in drug sensitivity and tumorigenesis in non-small cell lung cancer. Cancer research. 2010; 70:4995-5003.
37. Phillips PA, Dudeja V, McCarroll JA, Borja-Cacho D, Dawra RK, Grizzle WE, Vickers SM, Saluja AK. Triptolide induces pancreatic cancer cell death via inhibition of heat shock protein 70. Cancer research. 2007; 67:9407-9416.
38. Phillips PA, Sangwan V, Borja-Cacho D, Dudeja V, Vickers SM, Saluja AK. Myricetin induces pancreatic cancer cell death via the induction of apoptosis and inhibition of the phosphatidylinositol 3-kinase (PI3K) signaling pathway. Cancer letters. 2011; 308:181-188.
39. Ponomarev V, Doubrovin M, Serganova I, Vider J, Shavrin A, Beresten T, Ivanova A, Ageyeva L, Tourkova V, Balatoni J, Bornmann W, Blasberg R, Gelovani Tjuvajev J. A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging. European journal of nuclear medicine and molecular imaging. 2004; 31:740-751.
40. Shibuya K, Komaki R, Shintani T, Itasaka S, Ryan A, Jurgensmeier JM, Milas L, Ang K, Herbst RS, O'Reilly MS. Targeted therapy against VEGFR and EGFR with ZD6474 enhances the therapeutic efficacy of irradiation in an orthotopic model of human non-small-cell lung cancer. International journal of radiation oncology, biology, physics. 2007; 69:1534-1543.