Nanoparticulate delivery of diphtheria toxin DNA effectively kills Mesothelin expressing pancreatic cancer cells

Cancer Biology and Therapy

Volumn 7, Issue 10, 2008, Pages 1584-1590

  Showalter, Shayna L ^a   Huang, Yu Hung ^b   Witkiewicz, Agneszka ^a   Costantino, Christina L ^a   Yeo, Charles J ^a   Green, Jordan J ^d   Langer, Robert ^d   Anderson, Daniel G ^d   Sawicki, Janet A ^b,c   Brody, Jonathan R ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c LANKENAU INSTITUTE FOR MEDICAL RESEARCH   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Mesothelin; Nanoparticles; Pancreatic cancer; Targeted DNA delivery

Indexed keywords

DIPHTHERIA TOXIN; DIPHTHERIA TOXIN A; DNA; LUCIFERASE; MESOTHELIN; MESSENGER RNA; NANOPARTICLE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER MODEL; CELL DEATH; CLONING; CONTROLLED STUDY; DNA SEQUENCE; DRUG EFFECT; DRUG EFFICACY; ENZYME INHIBITION; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; NONVIRAL GENE DELIVERY SYSTEM; PANCREAS CANCER; PANCREAS DUCT ADENOCARCINOMA; PROMOTER REGION; PROTEIN EXPRESSION; SUICIDE GENE;

EID: 54349091298     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.7.10.6562     Document Type: Article

References (44)

1. Bilimoria KY, Bentrem DJ, Ko CY, Stewart AK, Winchester DP, Talamonti MS. National failure to operate on early stage pancreatic cancer. Ann Surg 2007; 246:173-80.
2. Kleeff J, Michalski CW, Friess H, Buchler MW. Surgical treatment of pancreatic cancer: the role of adjuvant and multimodal therapies. Eur J Surg Oncol 2007; 33:817-23.
3. Sener SF, Fremgen A, Menck HR, Winchester DP. Pancreatic cancer: a report of treatment and survival trends for 100,313 patients diagnosed from 1985-1995, using the National Cancer Database. J Am Coll Surg 1999; 189:1-7.
4. Hruban RH, Iacobuzio-Donahue C, Wilentz RE, Goggins M, Kern SE. Molecular pathology of pancreatic cancer. Cancer J 2001; 7:251-8.
5. Showalter SL, Showalter TN, Witkiewicz A, Havens R, Kennedy EP, Hucl T, Kern SE, Yeo CJ, Brody JR. Evaluating the drug-target relationship between thymidylate synthase expression and tumor response to 5-fluorouracil: Is it time to move forward? Cancer Biol Ther 2008; 7.
6. Argani P, Iacobuzio-Donahue C, Ryu B, Rosty C, Goggins M, Wilentz RE, Murugesan SR, Leach SD, Jaffee E, Yeo CJ, Cameron JL, Kern SE, Hruban RH. Mesothelin is overexpressed in the vast majority of ductal adenocarcinomas of the pancreas: identification of a new pancreatic cancer marker by serial analysis of gene expression (SAGE). Clin Cancer Res 2001; 7:3862-8.
7. Watanabe H, Okada G, Ohtsubo K, Yamaguchi Y, Mouri H, Motoo Y, Wakabayashi T, Sawabu N. Expression of mesothelin mRNA in pure pancreatic juice from patients with pancreatic carcinoma, intraductal papillary mucinous neoplasm of the pancreas, and chronic pancreatitis. Pancreas 2005; 30:349-54.
8. Maitra A, Adsay NV, Argani P, Iacobuzio-Donahue C, De Marzo A, Cameron JL, Yeo CJ, Hruban RH. Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray. Mod Pathol 2003; 16:902-12.
9. Iacobuzio-Donahue CA, Ashfaq R, Maitra A, Adsay NV, Shen-Ong GL, Berg K, Hollingsworth MA, Cameron JL, Yeo CJ, Kern SE, Goggins M, Hruban RH. Highly expressed genes in pancreatic ductal adenocarcinomas: a comprehensive characterization and comparison of the transcription profiles obtained from three major technologies. Cancer Res 2003; 63:8614-22.
10. Ryu B, Jones J, Blades NJ, Parmigiani G, Hollingsworth MA, Hruban RH, Kern SE. Relationships and differentially expressed genes among pancreatic cancers examined by large-scale serial analysis of gene expression. Cancer Res 2002; 62:819-26.
11. Sato N, Fukushima N, Maitra A, Iacobuzio-Donahue CA, van Heek NT, Cameron JL, Yeo CJ, Hruban RH, Goggins M. Gene expression profiling identifies genes associated with invasive intraductal papillary mucinous neoplasms of the pancreas. Am J Pathol 2004; 164:903-14.
12. Sato N, Maitra A, Fukushima N, van Heek NT, Matsubayashi H, Iacobuzio-Donahue CA, Rosty C, Goggins M. Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Cancer Res 2003; 63:4158-66.
13. Hassan R, Laszik ZG, Lerner M, Raffeld M, Postier R, Brackett D. Mesothelin is overexpressed in pancreaticobiliary adenocarcinomas but not in normal pancreas and chronic pancreatitis. Am J Clin Pathol 2005; 124:838-45.
14. Hucl T, Brody JR, Gallmeier E, Iacobuzio-Donahue CA, Farrance IK, Kern SE. High cancer-specific expression of mesothelin (MSLN) is attributable to an upstream enhancer containing a transcription enhancer factor dependent MCAT motif. Cancer Res 2007; 67:9055-65.
15. Li M, Bharadwaj U, Zhang R, Zhang S, Mu H, Fisher WE, Brunicardi FC, Chen C, Yao Q. Mesothelin is a malignant factor and therapeutic vaccine target for pancreatic cancer. Mol Cancer Ther 2008; 7:286-96.
16. Hassan R, Viner JL, Wang QC, Margulies I, Kreitman RJ, Pastan I. Anti-tumor activity of K1-LysPE38QQR, an immunotoxin targeting mesothelin, a cell-surface antigen overexpressed in ovarian cancer and malignant mesothelioma. J Immunother 2000; 23:473-9.
17. Chang K, Pastan I. Molecular cloning and expression of a cDNA encoding a protein detected by the K1 antibody from an ovarian carcinoma (OVCAR-3) cell line. Int J Cancer 1994; 57:90-7.
18. Scholler N, Fu N, Yang Y, Ye Z, Goodman GE, Hellstrom KE, Hellstrom I. Soluble member(s) of the mesothelin/megakaryocyte potentiating factor family are detectable in sera from patients with ovarian carcinoma. Proc Natl Acad Sci USA 1999; 96:11531-6.
19. Thomas AM, Santarsiero LM, Lutz ER, Armstrong TD, Chen YC, Huang LQ, Laheru DA, Goggins M, Hruban RH, Jaffee EM. Mesothelin-specific CD8(+) T cell responses provide evidence of in vivo cross-priming by antigen-presenting cells in vaccinated pancreatic cancer patients. J Exp Med 2004; 200:297-306.
20. Maxwell IH, Maxwell F, Glode LM. Regulated expression of a diphtheria toxin A-chain gene transfected into human cells: possible strategy for inducing cancer cell suicide. Cancer Res 1986; 46:4660-4.
21. Anderson DG, Peng W, Akinc A, Hossain N, Kohn A, Padera R, Langer R, Sawicki JA. A polymer library approach to suicide gene therapy for cancer. Proc Natl Acad Sci USA 2004; 101:16028-33.
22. Peng W, Anderson DG, Bao Y, Padera RF Jr, Langer R, Sawicki JA. Nanoparticulate delivery of suicide DNA to murine prostate and prostate tumors. Prostate 2007; 67:855-62.
23. Zugates GT, Peng W, Zumbuehl A, Jhunjhunwala S, Huang YH, Langer R, Sawicki JA, Anderson DG. Rapid optimization of gene delivery by parallel end-modification of poly(beta-amino ester)s. Mol Ther 2007; 15:1306-12.
24. Brody JR, Calhoun ES, Gallmeier E, Creavalle TD, Kern SE. Ultra-fast high-resolution agarose electrophoresis of DNA and RNA using low-molarity conductive media. Biotechniques 2004; 37:598-602.
25. Breidenbach M, Rein DT, Everts M, Glasgow JN, Wang M, Passineau MJ, Alvarez RD, Korokhov N, Curiel DT. Mesothelin-mediated targeting of adenoviral vectors for ovarian cancer gene therapy. Gene Ther 2005; 12:187-93.
26. Ikawa M, Kominami K, Yoshimura Y, Tanaka K, Nishimune Y, Okabe M. Green fluorescent protein as a marker in transgenic mice. Development Growth & Differentiation 1995; 37:455-9.
27. Peng W, Chen J, Huang YH, Sawicki JA. Tightly-regulated suicide gene expression kills PSA-expressing prostate tumor cells. Gene Ther 2005; 12:1573-80.
28. Brody JR, Witkiewicz A, Williams TK, Kadkol SS, Cozzitorto J, Durkan B, Pasternack GR, Yeo CJ. Reduction of pp32 expression in poorly differentiated pancreatic ductal adenocarcinomas and intraductal papillary mucinous neoplasms with moderate dysplasia. Mod Pathol 2007; 20:1238-44.
29. Brody JR, Hucl T, Gallmeier E, Winter JM, Kern SE, Murphy KM. Genomic copy number changes affecting the thymidylate synthase (TYMS) gene in cancer: a model for patient classification to aid fluoropyrimidine therapy. Cancer Res 2006; 66:9369-73.
30. Gallmeier E, Calhoun ES, Rago C, Brody JR, Cunningham SC, Hucl T, Gorospe M, Kohli M, Lengauer C, Kern SE. Targeted disruption of FANCC and FANCG in human cancer provides a preclinical model for specific therapeutic options. Gastroenterology 2006; 130:2145-54.
31. van der Heijden MS, Brody JR, Gallmeier E, Cunningham SC, Dezentje DA, Shen D, Hruban RH, Kern SE. Functional defects in the fanconi anemia pathway in pancreatic cancer cells. Am J Pathol 2004; 165:651-7.
32. Hassan R, Bullock S, Premkumar A, Kreitman RJ, Kindler H, Willingham MC, Pastan I. Phase I study of SS1P, a recombinant anti-mesothelin immunotoxin given as a bolus IV infusion to patients with mesothelin-expressing mesothelioma, ovarian, and pancreatic cancers. Clin Cancer Res 2007; 13:5144-9.
33. Collier RJ. Diphtheria toxin: mode of action and structure. Bacteriol Rev 1975; 39:54-85.
34. White RJ, Trouche D, Martin K, Jackson SP, Kouzarides T. Repression of RNA polymerase III transcription by the retinoblastoma protein. Nature 1996; 382:88-90.
35. White RJ. Regulation of RNA polymerases I and III by the retinoblastoma protein: a mechanism for growth control? Trends Biochem Sci 1997; 22:77-80.
36. Stein T, Crighton D, Boyle JM, Varley JM, White RJ. RNA polymerase III transcription can be derepressed by oncogenes or mutations that compromise p53 function in tumours and Li-Fraumeni syndrome. Oncogene 2002; 21:2961-70.
37. Felton-Edkins ZA, Kenneth NS, Brown TR, Daly NL, Gomez-Roman N, Grandori C, Eisenman RN, White RJ. Direct regulation of RNA polymerase III transcription by RB, p53 and c-Myc. Cell Cycle 2003; 2:181-4.
38. Felton-Edkins ZA, Fairley JA, Graham EL, Johnston IM, White RJ, Scott PH. The mitogen-activated protein (MAP) kinase ERK induces tRNA synthesis by phosphorylating TFIIIB. Embo J 2003; 22:2422-32.
39. Pham NA, Schwock J, Iakovlev V, Pond G, Hedley DW, Tsao MS. Immunohistochemical analysis of changes in signaling pathway activation downstream of growth factor receptors in pancreatic duct cell carcinogenesis. BMC Cancer 2008; 8:43.
40. Browne GJ, Proud CG. A novel mTOR-regulated phosphorylation site in elongation factor 2 kinase modulates the activity of the kinase and its binding to calmodulin. Mol Cell Biol 2004; 24:2986-97.
41. Onda M, Willingham M, Nagata S, Bera TK, Beers R, Ho M, Hassan R, Kreitman RJ, Pastan I. New monoclonal antibodies to mesothelin useful for immunohistochemistry, fluorescence-activated cell sorting, Western blotting, and ELISA. Clin Cancer Res 2005; 11:5840-6.
42. Peng W, Verbitsky A, Bao Y, Sawicki J. Regulated expression of diphtheria toxin in prostate cancer cells. Mol Ther 2002; 6:537-45.
43. Argani P, Rosty C, Reiter RE, Wilentz RE, Murugesan SR, Leach SD, Ryu B, Skinner HG, Goggins M, Jaffee EM, Yeo CJ, Cameron JL, Kern SE, Hruban RH. Discovery of new markers of cancer through serial analysis of gene expression: prostate stem cell antigen is overexpressed in pancreatic adenocarcinoma. Cancer Res 2001; 61:4320-4.
44. Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH, Rustgi AK, Chang S, Tuveson DA. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005; 7:469-83.