Enhancement of Gemcitabine sensitivity in pancreatic adenocarcinoma by novel exosome-mediated delivery of the Survivin-T34A mutant

Journal of Extracellular Vesicles

Volumn 3, Issue 1, 2014, Pages 1-9

  Aspe, Jonathan R ^a   Osterman, Carlos J Diaz ^a   Jutzy, Jessica M S ^a   Deshields, Simone ^a   Whang, Sonia ^a   Wall, Nathan R ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GEMCITABINE; SURVIVIN; SURVIVIN T34A; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG POTENTIATION; DRUG SENSITIVITY; EXOSOME; HUMAN; HUMAN CELL; MUTANT; PANCREAS ADENOCARCINOMA; PROTEIN EXPRESSION;

EID: 85014653850     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.3402/jev.v3.23244     Document Type: Article

References (51)

1. Kleeff J, Michalski C, Friess H, Buchler MW. Pancreatic cancer: from bench to 5-year survival. Pancreas. 2006;33: 111-8.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69-90.
3. Muller MW, Friess H, Koninger J, Martin D, Wente MN, Hinz U, et al. Factors influencing survival after bypass procedures in patients with advanced pancreatic adenocarcinomas. Am J Surg. 2008;195:221-8.
4. Ueno H, Kiyosawa K, Kaniwa N. Pharmacogenomics of gemcitabine: can genetic studies lead to tailor-made therapy? Br J Cancer. 2007;97:145-51.
5. Reni M, Cereda S, Galli L. PEFG (cisplatin, epirubicin, 5-fluorouracil, gemcitabine) for patients with advanced pancreatic cancer: the ghost regimen. Cancer Lett. 2007;256:25-8.
6. Oettle H, Neuhaus P. Adjuvant therapy in pancreatic cancer: a critical appraisal. Drugs. 2007;67:2293-310.
7. Galloway NR, Aspe JR, Sellers C, Wall NR. Enhanced antitumor effect of combined gemcitabine and proton radiation in the treatment of pancreatic cancer. Pancreas. 2009;38: 782-90.
8. Vishnu P, Colon-Otero G, Kennedy GT, Marlow LA, Kennedy WP, Wu KJ, et al. RhoB mediates antitumor synergy of combined ixabepilone and sunitinib in human ovarian serous cancer. Gynecol Oncol. 2012;124:589-97.
9. Karapanagiotou EM, Roulstone V, Twigger K, Ball M, Tanay M, Nutting C, et al. Phase I/II trial of carboplatin and paclitaxel chemotherapy in combination with intravenous oncolytic reovirus in patients with advanced malignancies. Clin Cancer Res. 2012;18:2080-9.
10. Li F. Survivin study: what is the next wave? J Cell Physiol. 2003;197:8-29.
11. Asanuma K, Kobayashi D, Furuya D, Tsuji N, Yagihashi A, Watanabe N. A role for Survivin in radioresistance of pancreatic cancer cells. Jpn J Cancer Res. 2002;93:1057-62.
12. Kami K, Doi R, Koizumi M, Toyoda E, Mori T, Ito D, et al. Downregulation of Survivin by siRNA diminishes radioresistance of pancreatic cancer cells. Surgery. 2005;138:299-305.
13. Sarela AI, Verbeke CS, Ramsdale J, Davies CL, Markham AF, Guillou PJ. Expression of Survivin, a novel inhibitor of apoptosis and cell cycle regulatory protein, in pancreatic adenocarcinoma. Br J Cancer. 2002;86:886-92.
14. Kami K, Doi R, Koizumi M, Toyoda E, Mori T, Ito D, et al. Survivin expression is a prognostic marker in pancreatic cancer patients. Surgery. 2004;136:443-8.
15. Satoh K, Kaneko K, Hirota M, Masamune A, Satoh A, Shimosegawa T. Expression of Survivin is correlated with cancer cell apoptosis and is involved in the development of human pancreatic duct cell tumors. Cancer. 2001;92:271-8.
16. Adida C, Crotty PL, McGrath J, Berrebi D, Diebold J, Altieri DC. Developmentally regulated expression of the novel cancer anti-apoptosis gene Survivin in human and mouse differentiation. Am J Pathol. 1998;152:43-9.
17. Fukuda S, Pelus LM. Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther. 2006;5:1087-98.
18. Zhu H, Wang Q, Hu C, Zhang W, Quan L, Liu M, et al. High expression of Survivin predicts poor prognosis in esophageal squamous cell carcinoma following radiotherapy. Tumour Biol. 2011;32:1147-53.
19. Shen X, Zheng JY, Shi H, Zhang Z, Wang WZ. Survivin Knockdown enhances gastric cancer cell sensitivity to radiation and chemotherapy in vitro and in nude mice. Am J Med Sci. 2012;344:52-8.
20. Mita AC, Mita MM, Nawrocki ST, Giles FJ. Survivin: key regulator of mitosis and apoptosis and novel target for cancer therapeutics. Clin Cancer Res. 2008;14(16):5000-5.
21. Andersen MH, Pedersen LO, Capeller B, Brocker EB, Becker JC, Thor Straten P. Spontaneous cytotoxic T-cell responses against Survivin-derived MHC class I-restricted T-cell epitopes in situ as well as ex vivo in cancer patients. Cancer Res. 2001;61:5964-8.
22. Grossman D, Kim PJ, Schechner JS, Altieri DC. Inhibition of melanoma tumor growth in vivo by Survivin targeting. Proc Natl Acad Sci U S A. 2001;98:635-40.
23. Mesri M, Wall NR, Li J, Kim RW, Altieri DC. Cancer gene therapy using a Survivin mutant adenovirus. J Clin Invest. 2001;108:981-90.
24. Wall NR, O'Connor DS, Plescia J, Pommier Y, Altieri DC. Suppression of Survivin phosphorylation on Thr34 by flavopiridol enhances tumor cell apoptosis. Cancer Res. 2003;63: 230-5.
25. Plescia J, Salz W, Xia F, Pennati M, Zaffaroni N, Daidone MG, et al. Rational design of shepherdin, a novel anticancer agent. Cancer Cell. 2005;7:457-68.
26. Olie RA, Simoes-Wust AP, Baumann B, Leech SH, Fabbro D, Stahel RA, et al. A novel antisense oligonucleotide targeting Survivin expression induces apoptosis and sensitizes lung cancer cells to chemotherapy. Cancer Res. 2000;60:2805-9.
27. Kanwar JR, Shen WP, Kanwar RK, Berg RW, Krissansen GW. Effects of Survivin antagonists on growth of established tumors and B7-1 immunogene therapy. J Natl Cancer Inst. 2001;93:1541-52.
28. Andersen MH, Svane IM, Becker JC, Straten PT. The universal character of the tumor-associated antigen survivin. Clin Cancer Res. 2007;13:5991-4.
29. Aspe JR, Wall NR. Survivin-T34A: molecular mechanism and therapeutic potential. Onco Targets Ther. 2010;3:247-54.
30. Li HX, Zhao XY, Wang L, Wang YS, Kan B, Xu JR, et al. Antitumor effect of mSurvivinThr340Ala in murine colon carcinoma when administered intravenously. Med Oncol. 2010;27:1156-63.
31. Peng XC, Yang L, Yang LP, Mao YQ, Yang HS, Liu JY, et al. Efficient inhibition of murine breast cancer growth and metastasis by gene transferred mouse survivin Thr340Ala mutant. J Exp Clin Cancer Res. 2008;27:46.
32. Shen C, Liu W, Buck AK, Reske SN. Pro-apoptosis and antiproliferation effects of a recombinant dominant-negative survivin-T34A in human cancer cells. Anticancer Res. 2009; 29:1423-8.
33. Khan S, Aspe JR, Asumen MG, Almaguel F, Odumosu O, Acevedo-Martinez S, et al. Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential. Br J Cancer. 2009;100:1073-86.
34. Khan S, Jutzy JM, Aspe JR, McGregor DW, Neidigh JW, Wall NR. Survivin is released from cancer cells via exosomes. Apoptosis. 2011;16:1-12.
35. Bobrie A, Thery C. Exosomes and communication between tumours and the immune system: are all exosomes equal? Biochem Soc Trans. 2013;41:263-7.
36. EL Andaloussi S, Mager I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 2013;12:347-57.
37. Tan A, De La Pena H, Seifalian AM. The application of exosomes as a nanoscale cancer vaccine. Int J Nanomedicine. 2010;5:889-900.
38. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol.;Chapter:Unit 3. 2006;3:22.
39. Lancaster GI, Febbraio MA. Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem. 2005;280:23349-55.
40. Li F, Ackermann EJ, Bennett CF, Rothermel AL, Plescia J, Tognin S, et al. Pleiotropic cell-division defects and apoptosisinduced by interference with survivin function. Nat Cell Biol. 1999;1:461-6.
41. Khan S, Jutzy JM, Valenzuela MM, Turay D, Aspe JR, Ashok A, et al. Plasma-derived exosomal survivin, a plausible biomarker for early detection of prostate cancer. PloS One. 2012;7:e46737.
42. Bokarewa M, Lindblad S, Bokarew D, Tarkowski A. Balance between survivin, a key member of the apoptosis inhibitor family, and its specific antibodies determines erosivity in rheumatoid arthritis. Arthritis Res Ther. 2005;7:R349-58.
43. Mera S, Magnusson M, Tarkowski A, Bokarewa M. Extracellular survivin up-regulates adhesion molecules on the surface of leukocytes changing their reactivity pattern. J Leukoc Biol. 2008;83:149-55.
44. Khan S, Jutzy JM, Aspe JR, Asuncion-Valenzuela MM, Park JS, Turay D, et al. The application of membrane vesicles for cancer therapy. In: Gali-Muhtasib H, editor. Advances in cancer therapy: intech; 2011. p. 21-52.
45. Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998;4:594-600.
46. Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001;7:297-303.
47. Couzin J. Cell biology: the ins and outs of exosomes. Science. 2005;308:1862-3.
48. Chaput N, Flament C, Viaud S, Taieb J, Roux S, Spatz A, et al. Dendritic cell derived-exosomes: biology and clinical implementations. J Leukoc Biol. 2006;80:471-8.
49. Blanc-Brude OP, Mesri M, Wall NR, Plescia J, Dohi T, Altieri DC. Therapeutic targeting of the survivin pathway in cancer: initiation of mitochondrial apoptosis and suppression of tumor-associated angiogenesis. Clin Cancer Res. 2003;9: 2683-92.
50. Liu T, Brouha B, Grossman D. Rapid induction of mitochondrial events and caspase-independent apoptosis in Survivintargeted melanoma cells. Oncogene. 2004;23:39-48.
51. Nicholson DW. From bench to clinic with apoptosis-based therapeutic agents. Nature. 2000;407:810-6.