Synergistic effects of eukaryotic coexpression plasmid carrying LKB1 and FUS1 genes on lung cancer in vitro and in vivo

Journal of Cancer Research and Clinical Oncology

Volumn 140, Issue 6, 2014, Pages 895-907

  Li, Lingdong ^a   Yu, Chuanjiang ^a   Ren, Jiang ^a   Ye, Sujuan ^a   Ou, Wenjing ^a   Wang, Yu ^a   Yang, Weihan ^a   Zhong, Guoxing ^a   Chen, Xiang ^a   Shi, Huashan ^a   Su, Xiaolan ^a   Chen, Lijuan ^a   Zhu, Wen ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

Combination gene therapy; Eukaryotic coexpression; FUS1; LKB1; Lung cancer

Indexed keywords

ANTINEOPLASTIC AGENT; LIPOSOME; LIVER KINASE B1; PLASMID VECTOR; TUMOR SUPPRESSOR CANDIDATE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER GENE THERAPY; CANCER GROWTH; CANCER MORTALITY; CANCER SURVIVAL; CELL CYCLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DRUG POTENTIATION; FEMALE; FLOW CYTOMETRY; GENE TRANSFER; IN VITRO STUDY; IN VIVO STUDY; LIPOSOMAL GENE DELIVERY SYSTEM; LUNG CANCER; LUNG CANCER CELL LINE; LUNG METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; TUMOR INVASION; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CELL ADHESION; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; DRUG SYNERGISM; FEMALE; GENETIC THERAPY; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; PROTEIN-SERINE-THREONINE KINASES; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901330434     PISSN: 01715216     EISSN: 14321335     Source Type: Journal    
DOI: 10.1007/s00432-014-1607-5     Document Type: Article

References (41)

1. Baker CH, Kedar D, McCarty MF, Tsan R, Weber KL, Bucana CD, Fidler IJ (2002) Blockade of epidermal growth factor receptor signaling on tumor cells and tumor-associated endothelial cells for therapy of human carcinomas. Am J Pathol 161(3):929-938. doi:10.1016/S0002-9440(10)64253-8 (Pubitemid 34988380)
2. Baylin SB, Ohm JE (2006) Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 6(2):107-116. doi:10.1038/nrc1799 (Pubitemid 43361543)
3. Carretero J, Shimamura T, Rikova K, Jackson AL, Wilkerson MD, Borgman CL, Buttarazzi MS, Sanofsky BA, McNamara KL, Brandstetter KA, Walton ZE, Gu TL, Silva JC, Crosby K, Shapiro GI, Maira SM, Ji H, Castrillon DH, Kim CF, García-Echeverría C, Bardeesy N, Sharpless NE, Hayes ND, Kim WY, Engelman JA, Wong KK (2010) Integrative genomic and proteomic analyses identify targets for Lkb1-deficient metastatic lung tumors. Cancer Cell 17(6):547-559. doi:10.1016/j.ccr.2010.04.026
4. Chen X, Wang X, Wang Y, Yang L, Hu J, Xiao W, Fu A, Cai L, Li X, Ye X, Liu Y, Wu W, Shao X, Mao Y, Wei Y, Chen L (2010) Improved tumor-targeting drug delivery and therapeutic efficacy by cationic liposome modified with truncated bFGF peptide. J Control Release 145(1):17-25. doi:10.1016/j.jconrel.2010.03.007
5. Deng WG, Wu G, Ueda K, Xu K, Roth JA, Ji L (2007a) Enhancement of antitumor activity of cisplatin in human lung cancer cells by tumor suppressor FUS1. Cancer Gene Ther 15(1):29-39. doi:10.1038/sj.cgt.7701094
6. Deng WG, Kawashima H, Wu G, Jayachandran G, Xu K, Minna JD, Roth JA, Ji L (2007b) Synergistic tumor suppression by coexpression of FUS1 and p53 is associated with down-regulation of murine double minute-2 and activation of the apoptotic protease- activating factor 1-dependent apoptotic pathway in human non-small cell lung cancer cells. Cancer Res 67(2):709-717. doi:10.1158/0008- 5472.CAN-06-3463 (Pubitemid 46192211)
7. Dings RP, Yokoyama Y, Ramakrishnan S, Griffioen AW, Mayo KH (2003) The designed angiostatic peptide anginex synergistically improves chemotherapy and antiangiogenesis therapy with angiostatin. Cancer Res 63(2):382-385 (Pubitemid 36152496)
8. Garinis GA, Gorgoulis VG, Mariatos G, Zacharatos P, Kotsinas A, Liloglou T, Foukas P, Kanavaros P, Kastrinakis NG, Vassilakopoulos T, Vogiatzi T, Field JK, Kittas C (2001) Association of allelic loss at the FHIT locus and p53 alterations with tumour kinetics and chromosomal instability in non-small cell lung carcinomas (NSCLCs). J Pathol 193(1):55-65. doi:10.1002/1096-9896(2000) 9999:9999<::AID-PATH 731>3.0.CO;2-#
9. Ghaffar H, Sahin F, Sanchez-Cepedes M, Su GH, Zahurak M, Sidransky D, Westra WH (2003) LKB1 protein expression in the evolution of glandular neoplasia of the lung. Clin Cancer Res 9(8):2998-3003 (Pubitemid 36993259)
10. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30(2):214-226. doi:10.1016/j.molcel.2008.03.003 (Pubitemid 351626684)
11. Halpin C, Barakate A, Askari BM, Abbott JC, Ryan MD (2001) Enabling technologies for manipulating multiple genes on complex pathways. Plant Mol Biol 47(1-2):295-310 (Pubitemid 32804508)
12. Inoki K, Li Y, Zhu T, Wu J, Guan KL (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signaling. Nat Cell Biol 4(9):648-657. doi:10.1038/ncb839 (Pubitemid 34993700)
13. Ito I, Ji L, Tanaka F, Saito Y, Gopalan B, Branch CD, Xu K, Atkinson EN, Bekele BN, Stephens LC, Minna JD, Roth JA, Ramesh R (2004) Liposomal vector mediated delivery of the 3p FUS1 gene demonstrates potent antitumor activity against human lung cancer in vivo. Cancer Gene Ther 11(11):733-739. doi:10.1038/sj.cgt.7700756 (Pubitemid 39488471)
14. Ivanova AV, Ivanov SV, Pascal V, Lumsden JM, Ward JM, Morris N, Tessarolo L, Anderson SK, Lerman MI (2007) Autoimmunity, spontaneous tumourigenesis, and IL-15 insufficiency in mice with a targeted disruption of the tumour suppressor gene Fus1. J Pathol 211(5):591-601. doi:10.1002/path.2146 (Pubitemid 46502436)
15. Jansen M, Ten Klooster JP, Offerhaus GJ, Clevers H (2009) LKB1 and AMPK family signaling: the intimate link between cell polarity and energy metabolism. Physiol Rev 89(3):777-798. doi:10.1152/physrev.00026.2008
16. Ji L, Roth JA (2008) Tumor suppressor FUS1 signaling pathway. J Thorac Oncol 3(4):327-330. doi:10.1097/JTO.0b013e31816bce65 (Pubitemid 351489470)
17. Ji H, Ramsey MR, Hayes DN, Fan C, McNamara K, Kozlowski P, Torrice C, Wu MC, Shimamura T, Perera SA, Liang MC, Cai D, Naumov GN, Bao L, Contreras CM, Li D, Chen L, Krishnamurthy J, Koivunen J, Chirieac LR, Padera RF, Bronson RT, Lindeman NI, Christiani DC, Lin X, Shapiro GI, Jänne PA, Johnson BE, Meyerson M, Kwiatkowski DJ, Castrillon DH, Bardeesy N, Sharpless NE, Wong KK (2007) LKB1 modulates lung cancer differentiation and metastasis. Nature 448(7155):807-810. doi:10.1038/nature06030 (Pubitemid 47266337)
18. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, Birnbaum MJ, Thompson CB (2005) AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 18(3):283-293. doi:10.1016/j.molcel.2005.03.027 (Pubitemid 41350534)
19. Kitaura J, Asai K, Maeda-Yamamoto M, Kawakami Y, Kikkawa U, Kawakami T (2000) Akt-dependent cytokine production in mast cells. J Exp Med 192(5):729-740. doi:10.1084/jem.192.5.729
20. Koivunen JP, Kim J, Lee J, Rogers AM, Park JO, Zhao X, Naoki K, Okamoto I, Nakagawa K, Yeap BY, Meyerson M, Wong KK, Richards WG, Sugarbaker DJ, Johnson BE, Jänne PA (2008) Mutations in the LKB1 tumour suppressor are frequently detected in tumours from Caucasian but not Asian lung cancer patients. Br J Cancer 99(2):245-252. doi:10.1038/sj.bjc.6604469
21. Lechanteur C, Delvenne P, Princen F, Lopez M, Fillet G, Gielen J, Merville MP, Bours V (2000) Combined suicide and cytokine gene therapy for peritoneal carcinomatosis. Gut 47(3):343-348. doi:10.1136/gut.47.3.343
22. Lerman MI, Minna JD (2000) The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: identification and evaluation of the resident candidate tumor suppressor genes. Cancer Res 60(21):6116-6133
23. Mahoney CL, Choudhury B, Davies H, Edkins S, Greenman C, Haaften Gv, Mironenko T, Santarius T, Stevens C, Stratton MR, Futreal PA (2009) LKB1/KRAS mutant lung cancers constitute a genetic subset of NSCLC with increased sensitivity to MAPK and mTOR signalling inhibition. Br J Cancer 100(2):370-375. doi:10.1038/sj.bjc.6604886
24. Moriuchi S, Glorioso JC, Maruno M, Izumoto S, Wolfe D, Huang S, Cohen JB, Yoshimine T (2005) Combination gene therapy for glioblastoma involving herpes simplex virus vector-mediated codelivery of mutant IκBα and HSV thymidine kinase. Cancer Gene Ther 12(5):487-496. doi:10.1038/sj.cgt.7700816 (Pubitemid 40629339)
25. Nguyen DX, Massagué J (2007) Genetic determinants of cancer metastasis. Nat Rev Genet 8(5):341-352. doi:10.1038/nrg2101 (Pubitemid 46625811)
26. Nishizaki M, Sasaki J, Fang B, Atkinson EN, Minna JD, Roth JA, Ji L (2004) Synergistic tumor suppression by coexpression of FHIT and p53 coincides with FHIT-mediated MDM2 inactivation and p53 stabilization in human non-small cell lung cancer cells. Cancer Res 64(16):5745-5752. doi:10.1158/0008-5472.CAN- 04-0195 (Pubitemid 39095573)
27. Ou W, Ye S, Yang W, Wan Y, Ma Q, Yu C, Shi H, Yuan Z, Zhong G, Ren J (2012) Enhanced antitumor effect of cisplatin in human NSCLC cells by tumor suppressor LKB1. Cancer Gene Ther 19(7):489-498. doi:10.1038/cgt.2012.18
28. Pan L, Peng XC, Leng F, Yuan QZ, Shan Y, Yu DD, Li ZY, Chen X, Xiao WJ, Wen Y, Ma TT, Yang L, Mao YQ, Yang HS, Wei YQ, Wang CT (2011) Therapeutic effects of survivin dominant negative mutant in a mouse model of prostate cancer. J Cancer Res Clin Oncol 137(1):19-28. doi:10.1007/s00432-010-0855-2
29. Prudkin L, Behrens C, Liu DD, Zhou X, Ozburn NC, Bekele BN, Minna JD, Moran C, Roth JA, Ji L, Wistuba II (2008) Loss and reduction of FUS1 protein expression is a frequent phenomenon in the pathogenesis of lung cancer. Clin Cancer Res 14(1):41-47. doi:10.1158/1078-0432 (Pubitemid 351377976)
30. Ramalingam SS, Owonikoko TK, Khuri FR (2011) Lung cancer: new biological insights and recent therapeutic advances. CA Cancer J Clin 61(2):91-112. doi:10.3322/caac.20102
31. Robinson J, Lai C, Martin A, Nye E, Tomlinson I, Silver A (2009) Oral rapamycin reduces tumour burden and vascularization in Lkb1(+/-) mice. J Pathol 219(1):35-40. doi:10.1002/path.2562
32. Rojiani MV, Alidina J, Esposito N, Rojiani AM (2010) Expression of MMP-2 correlates with increased angiogenesis in CNS metastasis of lung carcinoma. Int J Clin Exp Pathol 3(8):775-781
33. Sakamaki K (2004) Regulation of endothelial cell death and its role in angiogenesis and vascular regression. Curr Neurovasc Res 1(4):305-315. doi:10.2174/1567202043362072
34. Tessema M, Klinge DM, Yingling CM, Do K, Van Neste L, Belinsky SA (2010) Re-expression of CXCL14, a common target for epigenetic silencing in lung cancer, induces tumor necrosis. Oncogene 29(37):5159-5170. doi:10.1038/onc.2010. 255
35. van der Velden YU, Wang L, Zevenhoven J, van Rooijen E, van Lohuizen M, Giles RH, Clevers H, Haramis AP (2011) The serinethreonine kinase LKB1 is essential for survival under energetic stress in zebrafish. Proc Natl Acad Sci U S A 108(11):4358-4363. doi:10.1073/pnas.1010210108
36. Wu C, Wangpaichitr M, Feun L, Kuo MT, Robles C, Lampidis T, Savaraj N (2005) Overcoming cisplatin resistance by mTOR inhibitor in lung cancer. Mol Cancer 4(1):25. doi:10.1186/1476-4598-4-25
37. Xiang YZ, Feng ZH, Zhang J, Liao YL, Yu CJ, Yi WJ, Zhu W, Yu XQ (2010) Linear cyclen-based polyamine as a novel and efficient reagent in gene delivery. Org Biomol Chem 8(3):640-647. doi:10.1039/b914877a
38. Yu CJ, Ye SJ, Feng ZH, Ou WJ, Zhou XK, Li LD, Mao YQ, Zhu W, Wei YQ (2010) Effect of fraxiparine, a type of low molecular weight heparin, on the invasion and metastasis of lung adenocarcinoma A549 cells. Oncol Lett 1(4):755-760. doi:10.3892/ol-00000132
39. Zeng PY, Berger SL (2006) LKB1 is recruited to the p21/WAF1 promoter by p53 to mediate transcriptional activation. Cancer Res 66(22):10701-10708. doi:10.1158/0008-5472.CAN-06-0999
40. Zhang P, Ying L, Xu R, Ge S, Mei W, Li F, Dai B, Lu J, Qian G (2009) Tumor-specific, hypoxia-regulated, WW domain-containing oxidoreductase- expressing adenovirus inhibits human non-small cell lung cancer growth in vivo. Hum Gene Ther 21(1):27-39. doi:10.1089/hum.2009.021
41. Zhuang ZG, Di GH, Shen ZZ, Ding J, Shao ZM (2006) Enhanced expression of LKB1 in breast cancer cells attenuates angiogenesis, invasion, and metastatic potential. Mol Cancer Res 4(11):843-849. doi:10.1158/1541-7786.MCR-06-0118 (Pubitemid 44877014)