The design and optimization of RNA trans-splicing molecules for skin cancer therapy

Molecular Oncology

Volumn 7, Issue 6, 2013, Pages 1056-1068

  Gruber, Christina ^a   Koller, Ulrich ^a   Murauer, Eva M ^a   Hainzl, Stefan ^a   Hüttner, Clemens ^a   Kocher, Thomas ^a   South, Andrew P ^b   Hintner, Helmut ^a   Bauer, Johann W ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Cancer gene therapy; Epidermolysis bullosa; Herpes simplex virus thymidine kinase (HSV tk); RNA trans splicing; Squamous cell carcinoma

Indexed keywords

CHIMERIC PROTEIN; HERPES SIMPLEX VIRUS THYMIDINE KINASE; MESSENGER RNA PRECURSOR; ORGANIC ANION TRANSPORTER; ORGANIC ANION TRANSPORTER FAMILY MEMBER 1B3; THYMIDINE KINASE; UNCLASSIFIED DRUG; VIRUS ENZYME;

APOPTOSIS; ARTICLE; CANCER GENE THERAPY; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; GENE SEQUENCE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA BINDING; SKIN CANCER; SUICIDE GENE; SUICIDE GENE THERAPY; TRANS SPLICING; WESTERN BLOTTING;

SIMPLEXVIRUS;

3-(4,5-DIMETHYLTHIAZOL-2-YL)2,5-DIPHENYLTETRAZOLIUM BROMIDE; BD; BINDING DOMAIN; BP; BRANCH POINT; CANCER GENE THERAPY; DIPHTHERIA TOXIN SUBUNIT A; DT-A; EB; EB-SCC; EPIDERMOLYSIS BULLOSA; EPIDERMOLYSIS BULLOSA-ASSOCIATED SQUAMOUS CELL CARCINOMA; GANCICLOVIR; GANCICLOVIR TRIPHOSPHATE; GAPDH; GCV; GCVTP; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE; HERPES SIMPLEX VIRUS; HERPES SIMPLEX VIRUS - THYMIDINE KINASE (HSV-TK); HSV; INTERNAL RIBOSOMAL ENTRY SITE; IRES; MATRIX METALLOPROTEINASE 9; MG; MINIGENE; MMP9; MTT; POLY PYRIMIDINE TRACT; PPT; RDEB; RECESSIVE DYSTROPHIC EPIDERMOLYSIS BULLOSA; RNA TRANS-SPLICING; RNA TRANS-SPLICING MOLECULE; RTM; RTM MUTATED 1, RTM MUTATED 2; RTM ORIGINAL; RTMM1, RTMM2; RTMMUT; RTMORG; SCC; SEGMENTAL TRANS-SPLICING; SEMI-QUANTITATIVE REAL TIME PCR; SLCO1B3; SMART; SOLUTE CARRIER ORGANIC ANION TRANSPORTER FAMILY MEMBER 1B3; SPLICE SITE; SPLICEOSOME-MEDIATED RNA TRANS-SPLICING; SPLICING DEFICIENT RTM; SQRT-PCR; SQUAMOUS CELL CARCINOMA; SS; STS; TERMINAL DEOXYNUCLEOTIDYL TRANSFERASE DUTP NICK END LABELING; THYMIDINE KINASE; TK; TUNEL; Β-SUBUNIT OF HUMAN GONADOTROPIN GENE 6; ΒHCG6;

APOPTOSIS; EPIDERMOLYSIS BULLOSA; GENETIC THERAPY; HEK293 CELLS; HUMANS; NEOPLASM PROTEINS; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; RNA, NEOPLASM; SKIN NEOPLASMS; TRANS-SPLICING; TUMOR MARKERS, BIOLOGICAL;

EID: 84887930665     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.08.005     Document Type: Article

References (38)

1. Altaner C. Prodrug cancer gene therapy. Cancer Lett. 2008, 270:191-201.
2. Avale M.E., Rodríguez-Martín T., Gallo J.M. Trans-splicing correction of tau isoform imbalance in a mouse model of tau mis-splicing. Hum. Mol. Genet. 2013, 22:2603-2611.
3. Bauer J.W., Murauer E.M., Wally V., Koller U. RNA trans-splicing for genodermatoses. Methods Mol. Biol. 2013, 961:441-455.
4. Chao H., Mansfield S.G., Bartel R.C., Hiriyanna S., Mitchell L.G., Garcia-Blanco M.A., Walsh C.E. Phenotype correction of hemophilia A mice by spliceosome-mediated RNA trans-splicing. Nat. Med. 2003, 9:1015-1019.
5. Coady T.H., Lorson C.L. Trans-splicing-mediated improvement in a severe mouse model of spinal muscular atrophy. J.Neurosci. 2010, 30:126-130.
6. Cole C.L., Pourreyron C., Foerster J., Purdie K., Salas-Alanis J.C., Murrell D.F., Bruckner-Tuderman L., McGrath J.A., Leigh I.M., South A.P. SLCO1B3 expression in recessive dystrophic epidermolysis bullosa associated squamous cell carcinoma is reduced by recombinant type VII collagen. J.Invest Dermatol. 2009, 129:S55.
7. Dallinger G., Puttaraju M., Mitchell L.G., Yancey K.B., Yee C., Klausegger A., Hintner H., Bauer J.W. Development of spliceosome-mediated RNA trans-splicing (SMaRT) for the correction of inherited skin diseases. Exp. Dermatol. 2003, 12:37-46.
8. Elion G.B., Furman P.A., Fyfe J.A., de Miranda P., Beauchamp L., Schaeffer H.J. Selectivity of action of an antiherpetic agent, 9-(2-hydroxyethoxymethyl) guanine. Proc. Natl. Acad. Sci. U S A 1977, 74:5716-5720.
9. Fillat C., Carrio M., Cascante A., Sangro B. Suicide gene therapy mediated by the Herpes Simplex virus thymidine kinase gene/Ganciclovir system: fifteen years of application. Curr. Gene Ther. 2003, 3:13-26.
10. Freeman S.M., Abboud C.N., Whartenby K.A., Packman C.H., Koeplin D.S., Moolten F.L., Abraham G.N. The "bystander effect": tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res. 1993, 53:5274-5283.
11. Gruber C., Gratz I.K., Murauer E.M., Mayr E., Koller U., Bruckner-Tuderman L., Meneguzzi G., Hintner H., Bauer J.W. Spliceosome-mediated RNA trans-splicing facilitates targeted delivery of suicide genes to cancer cells. Mol. Cancer Ther. 2011, 10:233-241.
12. Hamel W., Magnelli L., Chiarugi V.P., Israel M.A. Herpes simplex virus thymidine kinase/ganciclovir-mediated apoptotic death of bystander cells. Cancer Res. 1996, 56:2697-2702.
13. Hosseini S.J., Zomorodipour A., Jalal R., Sabouni F., Ataei F. A study of the expression of functional human coagulation factor IX in keratinocytes using a nonviral vector regulated by K14 promoter. Appl. Biochem. Biotechnol. 2010, 162:1599-1611.
14. Immonen A., Vapalahti M., Tyynela K., Hurskainen H., Sandmair A., Vanninen R., Langford G., Murray N., Yla-Herttuala S. AdvHSV-tk gene therapy with intravenous ganciclovir improves survival in human malignant glioma: a randomised, controlled study. Mol. Ther. 2004, 10:967-972.
15. Kalliokoski A., Niemi M. Impact of OATP transporters on pharmacokinetics. Br. J. Pharmacol. 2009, 158:693-705.
16. Kikumori T., Cote G.J., Gagel R.F. Promiscuity of pre-mRNA spliceosome-mediated trans splicing: a problem for gene therapy?. Hum. Gene Ther. 2001, 12:1429-1441.
17. Koller U., Wally V., Mitchell L.G., Klausegger A., Murauer E.M., Mayr E., Gruber C., Hainzl S., Hintner H., Bauer J.W. A novel screening system improves genetic correction by internal exon replacement. Nucleic Acids Res. 2011, 39:e108.
18. Lee W., Belkhiri A., Lockhart A.C., Merchant N., Glaeser H., Harris E.I., Washington M.K., Brunt E.M., Zaika A., Kim R.B., El Rifai W. Overexpression of OATP1B3 confers apoptotic resistance in colon cancer. Cancer Res. 2008, 68:10315-10323.
19. Liu X., Luo M., Zhang L.N., Yan Z., Zak R., Ding W., Mansfield S.G., Mitchell L.G., Engelhardt J.F. Spliceosome-mediated RNA trans-splicing with recombinant adeno-associated virus partially restores cystic fibrosis transmembrane conductance regulator function to polarized human cystic fibrosis airway epithelial cells. Hum. Gene Ther. 2005, 16:1116-1123.
20. Murauer E.M., Gache Y., Gratz I.K., Klausegger A., Muss W., Gruber C., Meneguzzi G., Hintner H., Bauer J.W. Functional correction of type VII collagen expression in dystrophic epidermolysis bullosa. J.Invest Dermatol. 2011, 131:74-83.
21. Murauer E.M., Koller U., Hainzl S., Wally V., Bauer J.W. A reporter-based screen to identify potent 3' trans-splicing molecules for endogenous RNA repair. Hum. Gene Ther. Methods 2013, 24:19-27.
22. Muto M., Onogawa T., Suzuki T., Ishida T., Rikiyama T., Katayose Y., Ohuchi N., Sasano H., Abe T., Unno M. Human liver-specific organic anion transporter-2 is a potent prognostic factor for human breast carcinoma. Cancer Sci. 2007, 98:1570-1576.
23. Nagai M., Furihata T., Matsumoto S., Ishii S., Motohashi S., Yoshino I., Ugajin M., Miyajima A., Matsumoto S., Chiba K. Identification of a new organic anion transporting polypeptide 1B3 mRNA isoform primarily expressed in human cancerous tissues and cells. Biochem. Biophys. Res. Commun. 2012, 418:818-823.
24. Nakayama K., Pergolizzi R.G., Crystal R.G. Gene transfer-mediated pre-mRNA segmental trans-splicing as a strategy to deliver intracellular toxins for cancer therapy. Cancer Res. 2005, 65:254-263.
25. Nasu Y., Saika T., Ebara S., Kusaka N., Kaku H., Abarzua F., Manabe D., Thompson T.C., Kumon H. Suicide gene therapy with adenoviral delivery of HSV-tK gene for patients with local recurrence of prostate cancer after hormonal therapy. Mol. Ther. 2007, 15:834-840.
26. Niemi M. Role of OATP transporters in the disposition of drugs. Pharmacogenomics 2007, 8:787-802.
27. Peckl-Schmid D., Wolkerstorfer S., Konigsberger S., Achatz-Straussberger G., Feichtner S., Schwaiger E., Zaborsky N., Huemer M., Gratz I.K., Schibli R., Lamers M., Crameri R., Moser K., Luger E.O., Achatz G. HAX1 deficiency: impact on lymphopoiesis and B-cell development. Eur. J. Immunol. 2010, 40:3161-3172.
28. Puttaraju M., Jamison S.F., Mansfield S.G., Garcia-Blanco M.A., Mitchell L.G. Spliceosome-mediated RNA trans-splicing as a tool for gene therapy. Nat. Biotechnol. 1999, 17:246-252.
29. Rheinwald J.G., Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 1975, 6:331-343.
30. Schwarzenberger P., Byrne P., Gaumer R., Norton J., Harrison L., Marrogi A., Kolls J.K. Treatment of mesothelioma with gene-modified PA1STK cells and ganciclovir: a phase I study. Cancer Gene Ther. 2011, 18:906-912.
31. Song Y., Lou H.H., Boyer J.L., Limberis M.P., Vandenberghe L.H., Hackett N.R., Leopold P.L., Wilson J.M., Crystal R.G. Functional cystic fibrosis transmembrane conductance regulator expression in cystic fibrosis airway epithelial cells by AAV6.2-mediated segmental trans-splicing. Hum. Gene Ther. 2009, 20:267-281.
32. Staggers W.R., Paterson A.J., Kudlow J.E. Sequence of the functional human keratin K14 promoter. Gene 1995, 153:297-298.
33. Wally V., Brunner M., Lettner T., Wagner M., Koller U., Trost A., Murauer E.M., Hainzl S., Hintner H., Bauer J.W. K14 mRNA reprogramming for dominant epidermolysis bullosa simplex. Hum. Mol. Genet. 2010, 19:4715-4725.
34. Wally V., Murauer E.M., Bauer J.W. Spliceosome-mediated trans-splicing: the therapeutic cut and paste. J.Invest Dermatol. 2012, 132:1959-1966.
35. Wang J., Mansfield S.G., Cote C.A., Jiang P.D., Weng K., Amar M.J., Brewer B.H., Remaley A.T., McGarrity G.J., Garcia-Blanco M.A., Puttaraju M. Trans-splicing into highly abundant albumin transcripts for production of therapeutic proteins invivo. Mol. Ther. 2009, 17:343-351.
36. Watt S.A., Pourreyron C., Purdie K., Hogan C., Cole C.L., Foster N., Pratt N., Bourdon J.C., Appleyard V., Murray K., Thompson A.M., Mao X., Mein C., Bruckner-Tuderman L., Evans A., McGrath J.A., Proby C.M., Foerster J., Leigh I.M., South A.P. Integrative mRNA profiling comparing cultured primary cells with clinical samples reveals PLK1 and C20orf20 as therapeutic targets in cutaneous squamous cell carcinoma. Oncogene 2011, 30:4666-4677.
37. Xu F., Li S., Li X.L., Guo Y., Zou B.Y., Xu R., Liao H., Zhao H.Y., Zhang Y., Guan Z.Z., Zhang L. Phase I and biodistribution study of recombinant adenovirus vector-mediated herpes simplex virus thymidine kinase gene and ganciclovir administration in patients with head and neck cancer and other malignant tumors. Cancer Gene Ther. 2009, 16:723-730.
38. Zolk O., Schnepf R., Muschler M., Fromm M.F., Wendler O., Traxdorf M., Iro M., Zenk H. Transporter gene expression in human head and neck squamous cell carcinoma and associated epigenetic regulatory mechanisms. Am. J. Pathol. 2013, 182:234-243.