Enhancing DPYSL3 gene expression via a promoter-targeted small activating RNA approach suppresses cancer cell motility and metastasis

Oncotarget

Volumn 7, Issue 16, 2016, Pages 22893-22910

  Li, Changlin ^a   Jiang, Wencong ^a,b   Hu, Qingting ^a,c   Li, Long cheng ^d   Dong, Liang ^a   Chen, Ruibao ^a   Zhang, Yinghong ^a   Tang, Yuzhe ^a   Brantley Thrasher, J ^a   Liu, Chang Bai ^c   Li, Benyi ^a,b,c  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b GUANGDONG MEDICAL UNIVERSITY   (China)

^c CHINA THREE GORGES UNIVERSITY   (China)

^d PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

Author keywords

CRMP4; DPYSL3; Metastasis; RNAa; SaRNA

Indexed keywords

ANTIMETASTATIC AGENT; APTAMER; DIHYDROPYRIMIDINASE LIKE 3 PROTEIN VARIANT 1; DIHYDROPYRIMIDINASE LIKE 3 PROTEIN VARIANT 2; MEMBRANE PROTEIN; PROSTATE SPECIFIC MEMBRANE ANTIGEN; RNA; SMALL ACTIVATING RNA; UNCLASSIFIED DRUG; DOUBLE STRANDED RNA; DPYSL3 PROTEIN, HUMAN; ISOPROTEIN; MUSCLE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL MOTILITY; CONTROLLED STUDY; CPG ISLAND; DISTANT METASTASIS; DOWN REGULATION; DPYSL3 GENE; DPYSL3 VARIANT 1 GENE; DPYSL3 VARIANT 2 GENE; DRUG CONJUGATION; DRUG EFFECT; DRUG POTENCY; EMBRYO; FEASIBILITY STUDY; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC TRANSFECTION; GENETIC VARIATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER METASTASIS; LUNG METASTASIS; LYMPH NODE METASTASIS; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; PROMOTER REGION; PROSTATE CANCER; PROSTATE CANCER CELL LINE; RNA ACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL MOTION; DRUG EFFECTS; GENE THERAPY; GENETICS; NUDE MOUSE; PATHOLOGY; PROCEDURES; PROSTATE TUMOR; TUMOR CELL LINE; TUMOR INVASION; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; GENE EXPRESSION; GENETIC THERAPY; HETEROGRAFTS; HUMANS; MALE; MICE; MICE, NUDE; MUSCLE PROTEINS; NEOPLASM INVASIVENESS; PROSTATIC NEOPLASMS; PROTEIN ISOFORMS; RNA, DOUBLE-STRANDED; TRANSCRIPTIONAL ACTIVATION;

EID: 84965034911     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8290     Document Type: Article

References (51)

1. Aus G, Robinson D, Rosell J, Sandblom G, Varenhorst E, South-East Region Prostate Cancer G. Survival in prostate carcinoma-outcomes from a prospective, population-based cohort of 8887 men with up to 15 years of follow-up: results from three countries in the population-based National Prostate Cancer Registry of Sweden. Cancer. 2005; 103:943-951.
2. Aaronson NK, Mattioli V, Minton O, Weis J, Johansen C, Dalton SO, Verdonck-de Leeuw IM, Stein KD, Alfano CM, Mehnert A, de Boer A, van de Poll-Franse LV. Beyond treatment-Psychosocial and behavioural issues in cancer survivorship research and practice. EJC Suppl. 2014; 12:54-64.
3. Datta K, Muders M, Zhang H, Tindall DJ. Mechanism of lymph node metastasis in prostate cancer. Future oncology. 2010; 6:823-836.
4. Rosenthal SA, Sandler HM. Treatment strategies for highrisk locally advanced prostate cancer. Nature reviews Urology. 2010; 7:31-38.
5. Schmidt EF, Strittmatter SM. The CRMP family of proteins and their role in Sema3A signaling. Adv Exp Med Biol. 2007; 600:1-11.
6. Goshima Y, Nakamura F, Strittmatter P, Strittmatter SM. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature. 1995; 376:509-514.
7. Gaetano C, Matsuo T, Thiele CJ. Identification and characterization of a retinoic acid-regulated human homologue of the unc-33-like phosphoprotein gene (hUlip) from neuroblastoma cells. The Journal of biological chemistry. 1997; 272:12195-12201.
8. Quach TT, Mosinger B, Jr., Ricard D, Copeland NG, Gilbert DJ, Jenkins NA, StankoffB, Honnorat J, Belin MF, Kolattukudy P. Collapsin response mediator protein-3/unc-33-like protein-4 gene: organization, chromosomal mapping and expression in the developing mouse brain. Gene. 2000; 242:175-182.
9. Fukada M, Watakabe I, Yuasa-Kawada J, Kawachi H, Kuroiwa A, Matsuda Y, Noda M. Molecular characterization of CRMP5, a novel member of the collapsin response mediator protein family. The Journal of biological chemistry. 2000; 275:37957-37965.
10. Shih JY, Yang SC, Hong TM, Yuan A, Chen JJ, Yu CJ, Chang YL, Lee YC, Peck K, Wu CW, Yang PC. Collapsin response mediator protein-1 and the invasion and metastasis of cancer cells. Journal of the National Cancer Institute. 2001; 93:1392-1400.
11. Shih JY, Lee YC, Yang SC, Hong TM, Huang CY, Yang PC. Collapsin response mediator protein-1: a novel invasion-suppressor gene. Clinical & experimental metastasis. 2003; 20:69-76.
12. Mukherjee J, DeSouza LV, Micallef J, Karim Z, Croul S, Siu KW, Guha A. Loss of collapsin response mediator Protein1, as detected by iTRAQ analysis, promotes invasion of human gliomas expressing mutant EGFRvIII. Cancer research. 2009; 69:8545-8554.
13. Wu CC, Chen HC, Chen SJ, Liu HP, Hsieh YY, Yu CJ, Tang R, Hsieh LL, Yu JS, Chang YS. Identification of collapsin response mediator protein-2 as a potential marker of colorectal carcinoma by comparative analysis of cancer cell secretomes. Proteomics. 2008; 8:316-332.
14. Gao X, Pang J, Li LY, Liu WP, Di JM, Sun QP, Fang YQ, Liu XP, Pu XY, He D, Li MT, Su ZL, Li BY. Expression profiling identifies new function of collapsin response mediator protein 4 as a metastasis-suppressor in prostate cancer. Oncogene. 2010; 29:4555-4566.
15. Li K, Pang J, Cheng H, Liu WP, Di JM, Xiao HJ, Luo Y, Zhang H, Huang WT, Chen MK, Li LY, Shao CK, Feng YH, Gao X. Manipulation of prostate cancer metastasis by locus-specific modification of the CRMP4 promoter region using chimeric TALE DNA methyltransferase and demethylase. Oncotarget. 2015; 6:10030-10044. doi:10.18632/oncotarget.3192.
16. Zhou W, Xie P, Pang M, Yang B, Fang Y, Shu T, Liu C, Wang X, Zhang L, Li S, Rong L. Upregulation of CRMP4, a new prostate cancer metastasis suppressor gene, inhibits tumor growth in a nude mouse intratibial injection model. International journal of oncology. 2015; 46:290-298.
17. Wang J, Place RF, Portnoy V, Huang V, Kang MR, Kosaka M, Ho MK, Li LC. Inducing gene expression by targeting promoter sequences using small activating RNAs. J Biol Methods. 2015; 2.
18. Li LC, Okino ST, Zhao H, Pookot D, Place RF, Urakami S, Enokida H, Dahiya R. Small dsRNAs induce transcriptional activation in human cells. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103:17337-17342.
19. Rockey WM, Hernandez FJ, Huang SY, Cao S, Howell CA, Thomas GS, Liu XY, Lapteva N, Spencer DM, McNamara JO, Zou X, Chen SJ, Giangrande PH. Rational truncation of an RNA aptamer to prostate-specific membrane antigen using computational structural modeling. Nucleic Acid Ther. 2011; 21:299-314.
20. Huang V, Qin Y, Wang J, Wang X, Place RF, Lin G, Lue TF, Li LC. RNAa is conserved in mammalian cells. PloS one. 2010; 5:e8848.
21. Mao Q, Li Y, Zheng X, Yang K, Shen H, Qin J, Bai Y, Kong D, Jia X, Xie L. Up-regulation of E-cadherin by small activating RNA inhibits cell invasion and migration in 5637 human bladder cancer cells. Biochemical and biophysical research communications. 2008; 375:566-570.
22. Chen Z, Place RF, Jia ZJ, Pookot D, Dahiya R, Li LC. Antitumor effect of dsRNA-induced p21(WAF1/CIP1) gene activation in human bladder cancer cells. Molecular cancer therapeutics. 2008; 7:698-703.
23. Kang MR, Yang G, Place RF, Charisse K, Epstein-Barash H, Manoharan M, Li LC. Intravesical delivery of small activating RNA formulated into lipid nanoparticles inhibits orthotopic bladder tumor growth. Cancer research. 2012; 72:5069-5079.
24. Wang J, Place RF, Huang V, Wang X, Noonan EJ, Magyar CE, Huang J, Li LC. Prognostic value and function of KLF4 in prostate cancer: RNAa and vectormediated overexpression identify KLF4 as an inhibitor of tumor cell growth and migration. Cancer research. 2010; 70:10182-10191.
25. Quinn CC, Chen E, Kinjo TG, Kelly G, Bell AW, Elliott RC, McPherson PS, Hockfield S. TUC-4b, a novel TUC family variant, regulates neurite outgrowth and associates with vesicles in the growth cone. The Journal of neuroscience. 2003; 23:2815-2823.
26. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, Antipin Y, Mitsiades N, Landers T, Dolgalev I, Major JE, Wilson M, et al. Integrative genomic profiling of human prostate cancer. Cancer cell. 2010; 18:11-22.
27. Holzbeierlein J, Lal P, LaTulippe E, Smith A, Satagopan J, Zhang L, Ryan C, Smith S, Scher H, Scardino P, Reuter V, Gerald WL. Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgenresponsive genes and mechanisms of therapy resistance. Am J Pathol. 2004; 164:217-227.
28. Zhu Q, Youn H, Tang J, Tawfik O, Dennis K, Terranova PF, Du J, Raynal P, Thrasher JB, Li B. Phosphoinositide 3-OH kinase p85alpha and p110beta are essential for androgen receptor transactivation and tumor progression in prostate cancers. Oncogene. 2008; 27:4569-4579.
29. Cole AR, Causeret F, Yadirgi G, Hastie CJ, McLauchlan H, McManus EJ, Hernandez F, Eickholt BJ, Nikolic M, Sutherland C. Distinct priming kinases contribute to differential regulation of collapsin response mediator proteins by glycogen synthase kinase-3 in vivo. The Journal of biological chemistry. 2006; 281:16591-16598.
30. Vichai V, Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc. 2006; 1:1112-1116.
31. Lupold SE, Hicke BJ, Lin Y, Coffey DS. Identification and characterization of nuclease-stabilized RNA molecules that bind human prostate cancer cells via the prostate-specific membrane antigen. Cancer research. 2002; 62:4029-4033.
32. Dassie JP, Liu XY, Thomas GS, Whitaker RM, Thiel KW, Stockdale KR, Meyerholz DK, McCaffrey AP, McNamara JO, 2nd, Giangrande PH. Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors. Nat Biotechnol. 2009; 27:839-849.
33. Rahim S, Minas T, Hong SH, Justvig S, Celik H, Kont YS, Han J, Kallarakal AT, Kong Y, Rudek MA, Brown ML, Kallakury B, Toretsky JA, Uren A. A small molecule inhibitor of ETV1, YK-4-279, prevents prostate cancer growth and metastasis in a mouse xenograft model. PloS one. 2014; 9:e114260.
34. Guan X. Cancer metastases: challenges and opportunities. Acta Pharm Sin B. 2015; 5:402-418.
35. Zhu G, Niu G, Chen X. Aptamer-Drug Conjugates. Bioconjug Chem. 2015; 26:2186-2197.
36. Ghosh A, Heston WD. Tumor target prostate specific membrane antigen (PSMA) and its regulation in prostate cancer. Journal of cellular biochemistry. 2004; 91:528-539.
37. Ristau BT, O'Keefe DS, Bacich DJ. The prostate-specific membrane antigen: lessons and current clinical implications from 20 years of research. Urologic oncology. 2014; 32:272-279.
38. Pan W, Clawson GA. The shorter the better: reducing fixed primer regions of oligonucleotide libraries for aptamer selection. Molecules. 2009; 14:1353-1369.
39. Chen R, Zhao Y, Huang Y, Yang Q, Zeng X, Jiang W, Liu J, Thrasher JB, Forrest ML, Li B. Nanomicellar TGX221 blocks xenograft tumor growth of prostate cancer in nude mice. The Prostate. 2015; 75:593-602.
40. Yang J, Xie SX, Huang Y, Ling M, Liu J, Ran Y, Wang Y, Thrasher JB, Berkland C, Li B. Prostate-targeted biodegradable nanoparticles loaded with androgen receptor silencing constructs eradicate xenograft tumors in mice. Nanomedicine (Lond). 2012; 7:1297-1309.
41. Zhao Y, Duan S, Zeng X, Liu C, Davies NM, Li B, Forrest ML. Prodrug strategy for PSMA-targeted delivery of TGX-221 to prostate cancer cells. Molecular pharmaceutics. 2012; 9:1705-1716.
42. Sun A, Li C, Chen R, Huang Y, Chen Q, Cui X, Liu H, Thrasher JB, Li B. GSK-3beta controls autophagy by modulating LKB1-AMPK pathway in prostate cancer cells. The Prostate. 2016;76:172-83.
43. Campeau E, Ruhl VE, Rodier F, Smith CL, Rahmberg BL, Fuss JO, Campisi J, Yaswen P, Cooper PK, Kaufman PD. A versatile viral system for expression and depletion of proteins in mammalian cells. PloS one. 2009; 4:e6529.
44. Padilla R, Sousa R. Efficient synthesis of nucleic acids heavily modified with non-canonical ribose 2'-groups using a mutantT7 RNA polymerase (RNAP). Nucleic acids research. 1999; 27:1561-1563.
45. Alabed YZ, Pool M, Ong Tone S, Fournier AE. Identification of CRMP4 as a convergent regulator of axon outgrowth inhibition. The Journal of neuroscience. 2007; 27:1702-1711.
46. Chen R, Zeng X, Zhang R, Huang J, Kuang X, Yang J, Liu J, Tawfik O, Thrasher JB, Li B. Cav1.3 channel alpha1D protein is overexpressed and modulates androgen receptor transactivation in prostate cancers. Urologic oncology. 2014; 32:524-536.
47. Liao X, Tang S, Thrasher JB, Griebling TL, Li B. Smallinterfering RNA-induced androgen receptor silencing leads to apoptotic cell death in prostate cancer. Molecular cancer therapeutics. 2005; 4:505-515.
48. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR. New colorimetric cytotoxicity assay for anticancer-drug screening. Journal of the National Cancer Institute. 1990; 82:1107-1112.
49. Schleef RR, Birdwell CR. The effect of fibrin on endothelial cell migration in vitro. Tissue Cell. 1982; 14:629-636.
50. Zigmond SH and Hirsch JG. Leukocyte locomotion, chemotaxis. New methods for evaluation, and demonstration of a cell-derived chemotactic factor. The Journal of experimental medicine. 1973; 137:387-410.
51. Li B, Sun A, Youn H, Hong Y, Terranova PF, Thrasher JB, Xu P, Spencer D. Conditional Akt activation promotes androgen-independent progression of prostate cancer. Carcinogenesis. 2007; 28:572-583.