Construction of an inducible cell-communication system that amplifies Salmonella gene expression in tumor tissue

Biotechnology and Bioengineering

Volumn 110, Issue 6, 2013, Pages 1769-1781

  Dai, Yumei ^a   Toley, Bhushan J ^a   Swofford, Charles A ^a   Forbes, Neil S ^a  

^a University of Massachusetts   (United States)

Author keywords

Bacterial anticancer therapy; Cancer; Cell cell communication; Salmonella; Three dimensional in vitro tumor; Triggered gene expression

Indexed keywords

ANTI-CANCER THERAPIES; BACTERIAL COMMUNICATIONS; CANCER; CELL-CELL COMMUNICATIONS; FLUORESCENT REPORTER; IN-VITRO; INCREASING SENSITIVITIES; SYSTEMIC TOXICITIES;

BIOREMEDIATION; CELL SIGNALING; CHEMOTHERAPY; COMMUNICATION SYSTEMS; FLUORESCENCE; MACHINERY; MOLECULES; PROTEINS; SALMONELLA; THREE DIMENSIONAL; TUMORS;

GENE EXPRESSION;

BACTERIAL PROTEIN; PROTEIN BAD;

ARTICLE; BACTERIAL GENE; CELL COMMUNICATION; CONTROLLED STUDY; FLUORESCENCE; GENE EXPRESSION REGULATION; GENE EXPRESSION SYSTEM; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; QUORUM SENSING; REPORTER GENE; SALMONELLA; SIGNAL TRANSDUCTION; VIBRIO FISCHERI;

ANTINEOPLASTIC AGENTS; ARABINOSE; BACTERIAL PROTEINS; CELL COMMUNICATION; CELL LINE, TUMOR; CLONING, MOLECULAR; DRUG RESISTANCE, NEOPLASM; GENES, REPORTER; GENETIC ENGINEERING; HUMANS; LUMINESCENT PROTEINS; MICROFLUIDIC ANALYTICAL TECHNIQUES; NEOPLASMS; PLASMIDS; SALMONELLA;

BACTERIA (MICROORGANISMS); SALMONELLA; VIBRIO FISCHERI;

EID: 84876748264     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.24816     Document Type: Article

References (44)

1. Anderson JC, Clarke EJ, Arkin AP, Voigt CA. 2006. Environmentally controlled invasion of cancer cells by engineered bacteria. J Mol Biol 355(4): 619-627.
2. Arrach N, Zhao M, Porwollik S, Hoffman RM, McClelland M. 2008. Salmonella promoters preferentially activated inside tumors. Cancer Res 68(12): 4827-4832.
3. Casciari JJ, Sotirchos SV, Sutherland RM. 1992. Mathematical modelling of microenvironment and growth in EMT6/Ro multicellular tumour spheroids. Cell Prolif 25(1): 1-22.
4. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci 97(12): 6640-6645.
5. Deans TL, Cantor CR, Collins JJ. 2007. A tunable genetic switch based on RNAi and repressor proteins for regulating gene expression in mammalian cells. Cell 130(2): 363-372.
6. Foley JE, Cushman SW, Salans LB. 1978. Glucose transport in isolated rat adipocytes with measurements of L-arabinose uptake. Am J Physiol 234(2): E112-E119.
7. Forbes NS. 2010. Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer 10(11): 785-794.
8. Forbes NS, Munn LL, Fukumura D, Jain RK. 2003. Sparse initial entrapment of systemically injected Salmonella typhimurium leads to heterogeneous accumulation within tumors. Cancer Res 63(17): 5188-5193.
9. Galan JE, Nakayama K, Curtiss R III. 1990. Cloning and characterization of the asd gene of Salmonella typhimurium: Use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene 94(1): 29-35.
10. Ganai S, Arenas RB, Forbes NS. 2009. Tumour-targeted delivery of TRAIL using Salmonella typhimurium enhances breast cancer survival in mice. Br J Cancer 101(10): 1683-1691.
11. Ganai S, Arenas RB, Sauer JP, Bentley B, Forbes NS. 2011. In tumors Salmonella migrate away from vasculature toward the transition zone and induce apoptosis. Cancer Gene Ther 18(7): 457-466.
12. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177(14): 4121-4130.
13. Jiang SN, Phan TX, Nam TK, Nguyen VH, Kim HS, Bom HS, Choy HE, Hong Y, Min JJ. 2010. Inhibition of tumor growth and metastasis by a combination of Escherichia coli-mediated cytolytic therapy and radiotherapy. Mol Ther 18(3): 635-642.
14. Kambam PKR, Sayut DJ, Niu Y, Eriksen DT, Sun LH. 2008. Directed evolution of LuxI for enhanced OHHL production. Biotechnol Bioeng 101(2): 263-272.
15. Kasinskas RW, Forbes NS. 2006. Salmonella typhimurium specifically chemotax and proliferate in heterogeneous tumor tissue in vitro. Biotechnol Bioeng 94(4): 710-721.
16. Kasinskas RW, Forbes NS. 2007. Salmonella typhimurium lacking ribose chemoreceptors localize in tumor quiescence and induce apoptosis. Cancer Res 67(7): 3201-3209.
17. Khlebnikov A, Risa O, Skaug T, Carrier TA, Keasling JD. 2000. Regulatable arabinose-inducible gene expression system with consistent control in all cells of a culture. J Bacteriol 182(24): 7029-7034.
18. Khlebnikov A, Datsenko KA, Skaug T, Wanner BL, Keasling JD. 2001. Homogeneous expression of the P(BAD) promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter. Microbiology 147(Pt 12): 3241-3247.
19. Lankelma J, Dekker H, Luque FR, Luykx S, Hoekman K, van der Valk P, van Diest PJ, Pinedo HM. 1999. Doxorubicin gradients in human breast cancer. Clin Cancer Res 5(7): 1703-1707.
20. Le UN, Kim H-S, Kwon J-S, Kim MY, Nguyen VH, Jiang SN, Lee B-I, Hong Y, Shin MG, Rhee JH, Bom H-S, Ahn Y, Gambhir SS, Choy HE, Min J-J. 2011. Engineering and visualization of bacteria for targeting infarcted myocardium. Mol Ther 19(5): 951-959.
21. Li L, Hooi D, Chhabra SR, Pritchard D, Shaw PE. 2004. Bacterial N-acylhomoserine lactone-induced apoptosis in breast carcinoma cells correlated with down-modulation of STAT3. Oncogene 23(28): 4894-4902.
22. Loeffler M, Le'Negrate G, Krajewska M, Reed JC. 2008. Inhibition of tumor growth using Salmonella expressing Fas ligand. J Natl Cancer Inst 100(15): 1113-1116.
23. Loessner H, Endmann A, Leschner S, Westphal K, Rohde M, Miloud T, Hammerling G, Neuhaus K, Weiss S. 2007. Remote control of tumour-targeted Salmonella enterica serovar Typhimurium by the use of L-arabinose as inducer of bacterial gene expression in vivo. Cell Microbiol 9(6): 1529-1537.
24. Mengesha A, Dubois L, Lambin P, Landuyt W, Chiu RK, Wouters BG, Theys J. 2006. Development of a flexible and potent hypoxia-inducible promoter for tumor-targeted gene expression in attenuated Salmonella . Cancer Biol Ther 5(9): 1120-1128.
25. Miller MB, Bassler BL. 2001. Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199.
26. Neddermann P, Gargioli C, Muraglia E, Sambucini S, Bonelli F, De Francesco R, Cortese R. 2003. A novel, inducible, eukaryotic gene expression system based on the quorum-sensing transcription factor TraR. EMBO Rep 4(4): 439.
27. Nguyen VH, Kim HS, Ha JM, Hong Y, Choy HE, Min JJ. 2010. Genetically engineered Salmonella typhimurium as an imageable therapeutic probe for cancer. Cancer Res 70(1): 18-23.
28. Nuyts S, Theys J, Landuyt W, van Mellaert L, Lambin P, Anne J. 2001a. Increasing specificity of anti-tumor therapy: Cytotoxic protein delivery by non-pathogenic clostridia under regulation of radio-induced promoters. Anticancer Res 21(2A): 857-861.
29. Nuyts S, Van Mellaert L, Theys J, Landuyt W, Bosmans E, Anne J, Lambin P. 2001b. Radio-responsive recA promoter significantly increases TNFalpha production in recombinant clostridia after 2Gy irradiation. Gene Ther 8(15): 1197-1201.
30. Nuyts S, Van Mellaert L, Theys J, Landuyt W, Lambin P, Anne J. 2001c. The use of radiation-induced bacterial promoters in anaerobic conditions: A means to control gene expression in clostridium-mediated therapy for cancer. Radiat Res 155(5): 716-723.
31. Royo JL, Becker PD, Camacho EM, Cebolla A, Link C, Santero E, Guzman CA. 2007. In vivo gene regulation in Salmonella spp. by a salicylate-dependent control circuit. Nat Methods 4(11): 937-942.
32. Ryan RM, Green J, Williams PJ, Tazzyman S, Hunt S, Harmey JH, Kehoe SC, Lewis CE. 2009. Bacterial delivery of a novel cytolysin to hypoxic areas of solid tumors. Gene Ther 16(3): 329-339.
33. Sayut DJ, Niu Y, Sun L. 2006. Construction and engineering of positive feedback loops. ACS Chem Biol 1(11): 692-696.
34. Seri K, Sanai K, Matsuo N, Kawakubo K, Xue C, Inoue S. 1996. Arabinose selectively inhibits intestinal sucrase in an uncompetitive manner and suppresses glycemic response after sucrose ingestion in animals. Metabolism 45(11): 1368-1374.
35. Siegele DA, Hu JC. 1997. Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations. Proc Natl Acad Sci 94(15): 8168-8172.
36. Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB. 2003. Bacteria-host communication: The language of hormones. Proc Natl Acad Sci USA 100(15): 8951-8956.
37. Stritzker J, Weibel S, Hill PJ, Oelschlaeger TA, Goebel W, Szalay AA. 2007. Tumor-specific colonization, tissue distribution, and gene induction by probiotic Escherichia coli Nissle 1917 in live mice. Int J Med Microbiol 297(3): 151-162.
38. Thomas MD, van Tilburg A. 2000. Overexpression of foreign proteins using the Vibrio fischeri lux control system. Methods Enzymol 305: 315-329.
39. Toley BJ, Forbes NS. 2012. Motility is critical for effective distribution and accumulation of bacteria in tumor tissue. Integr Biol 4(2): 165-176.
40. Toley BJ, Ganz DE, Walsh CL, Forbes NS. 2011. Microfluidic device for recreating a tumor microenvironment. J Vis Exp 57: e2425, DOI: 10.3791/2425
41. Tsao CY, Hooshangi S, Wu HC, Valdes JJ, Bentley WE. 2010. Autonomous induction of recombinant proteins by minimally rewiring native quorum sensing regulon of E. coli . Metab Eng 12(3): 291-297.
42. Walsh CL, Babin BM, Kasinskas RW, Foster JA, McGarry MJ, Forbes NS. 2009. A multipurpose microfluidic device designed to mimic microenvironment gradients and develop targeted cancer therapeutics. Lab Chip 9(4): 545-554.
43. Weber W, Malphettes L, de Jesus M, Schoenmakers R, El-Baba MD, Spielmann M, Keller B, Weber CC, van de Wetering P, Aubel D, Wurm FM, Fussenegger M. 2005. Engineered Streptomyces quorum-sensing components enable inducible siRNA-mediated translation control in mammalian cells and adjustable transcription control in mice. J Gene Med 7(4): 518-525.
44. You YS, Marella H, Zentella R, Zhou YY, Ulmasov T, Ho THD, Quatrano RS. 2006. Use of bacterial quorum-sensing components to regulate gene expression in plants. Plant Physiol 140(4): 1205-1212.