Tunable thermal bioswitches for in vivo control of microbial therapeutics

Nature Chemical Biology

Volumn 13, Issue 1, 2017, Pages 75-80

  Piraner, Dan I ^a,b   Abedi, Mohamad H ^a,b   Moser, Brittany A ^a   Lee Gosselin, Audrey ^a   Shapiro, Mikhail G ^a  

^a California Institute of Technology   (United States)

^b California Institute of Technology HHMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL THERAPY; ARTICLE; BACTERIAL GENE; CONTAMINATION; ENVIRONMENTAL TEMPERATURE; FEVER; GENE EXPRESSION; HOST; IN VIVO STUDY; MOLECULAR ELECTRONICS; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE; TEMPERATURE SENSITIVE MUTANT; THERMAL BIOSWITCHES; ANIMAL; CHEMISTRY; ESCHERICHIA COLI; FECES; FEMALE; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MOUSE; SKIN DISEASE; TEMPERATURE; ULTRASOUND;

ANTIINFECTIVE AGENT; REPRESSOR PROTEIN;

ANIMALS; ANTI-BACTERIAL AGENTS; ESCHERICHIA COLI; FECES; FEMALE; FEVER; GENE EXPRESSION REGULATION, BACTERIAL; MICE; MICROBIAL VIABILITY; REPRESSOR PROTEINS; SKIN DISEASES; TEMPERATURE; ULTRASONICS;

EID: 84995529465     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2233     Document Type: Article

References (56)

1. Ford, T.J., Silver, P.A. Synthetic biology expands chemical control of microorganisms. Curr. Opin. Chem. Biol. 28, 20-28 (2015).
2. Fischbach, M.A., Bluestone, J.A., Lim, W.A. Cell-based therapeutics: the next pillar of medicine. Sci. Transl. Med. 5, 179ps177 (2013).
3. Steidler, L., et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289, 1352-1355 (2000).
4. Daniel, C., Roussel, Y., Kleerebezem, M., Pot, B. Recombinant lactic acid bacteria as mucosal biotherapeutic agents. Trends Biotechnol. 29, 499-508 (2011).
5. Claesen, J., Fischbach, M.A. Synthetic microbes as drug delivery systems. ACS Synth. Biol. 4, 358-364 (2015).
6. Wells, J.M., Mercenier, A. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat. Rev. Microbiol. 6, 349-362 (2008).
7. Courbet, A., Endy, D., Renard, E., Molina, F., Bonnet, J. Detection of pathological biomarkers in human clinical samples via amplifying genetic switches and logic gates. Sci. Transl. Med. 7, 289ra283 (2015).
8. Danino, T., et al. Programmable probiotics for detection of cancer in urine. Sci. Transl. Med. 7, 289ra28 (2015).
9. Kotula, J.W., et al. Programmable bacteria detect and record an environmental signal in the mammalian gut. Proc. Natl. Acad. Sci. USA 111, 4838-4843 (2014).
10. Archer, E.J., Robinson, A.B., Suël, G.M. Engineered E. coli that detect and respond to gut inflammation through nitric oxide sensing. ACS Synth. Biol. 1, 451-457 (2012).
11. Ntziachristos, V. Going deeper than microscopy: the optical imaging frontier in biology. Nat. Methods 7, 603-614 (2010).
12. Haar, G.T., Coussios, C. High intensity focused ultrasound: physical principles and devices. Int. J. Hyperthermia 23, 89-104 (2007).
13. Huang, X., El-Sayed, I.H., Qian, W., El-Sayed, M.A. Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J. Am. Chem. Soc. 128, 2115-2120 (2006).
14. Thiesen, B., Jordan, A. Clinical applications of magnetic nanoparticles for hyperthermia. Int. J. Hyperthermia 24, 467-474 (2008).
15. Zhao, K., Liu, M., Burgess, R.R. The global transcriptional response of Escherichia coli to induced sigma 32 protein involves sigma 32 regulon activation followed by inactivation and degradation of sigma 32 in vivo. J. Biol. Chem. 280, 17758-17768 (2005).
16. de Marco, A., Vigh, L., Diamant, S., Goloubinoff, P. Native folding of aggregation-prone recombinant proteins in Escherichia coli by osmolytes, plasmid-or benzyl alcohol-overexpressed molecular chaperones. Cell Stress Chaperones 10, 329-339 (2005).
17. Inda, M.E., et al. A lipid-mediated conformational switch modulates the thermosensing activity of DesK. Proc. Natl. Acad. Sci. USA 111, 3579-3584 (2014).
18. Kortmann, J., Sczodrok, S., Rinnenthal, J., Schwalbe, H., Narberhaus, F. Translation on demand by a simple RNA-based thermosensor. Nucleic Acids Res. 39, 2855-2868 (2011).
19. Neupert, J., Karcher, D., Bock, R. Design of simple synthetic RNA thermometers for temperature-controlled gene expression in Escherichia coli. Nucleic Acids Res. 36, e124 (2008).
20. Waldminghaus, T., Kortmann, J., Gesing, S., Narberhaus, F. Generation of synthetic RNA-based thermosensors. Biol. Chem. 389, 1319-1326 (2008).
21. Hoynes-O'Connor, A., Hinman, K., Kirchner, L., Moon, T.S. De novo design of heat-repressible RNA thermosensors in E. coli. Nucleic Acids Res. 43, 6166-6179 (2015).
22. Satija, R., Sen, S., Siegal-Gaskins, D., Murray, R.M. Design of a toolbox of RNA thermometers. Preprint at bioRxiv http://dx.doi.org/10.1101/017269 (2015).
23. Wieland, M., Hartig, J.S. RNA quadruplex-based modulation of gene expression. Chem. Biol. 14, 757-763 (2007).
24. Hurme, R., Berndt, K.D., Namork, E., Rhen, M. DNA binding exerted by a bacterial gene regulator with an extensive coiled-coil domain. J. Biol. Chem. 271, 12626-12631 (1996).
25. Valdez-Cruz, N.A., Caspeta, L., Pérez, N.O., Ramírez, O.T., Trujillo-Roldán, M.A. Production of recombinant proteins in E. coli by the heat inducible expression system based on the phage lambda pL and/or pR promoters. Microb. Cell Fact. 9, 18 (2010).
26. Sussman, R., Jacob, F. Sur un systeme de repression thermosensible chez le bacteriophage lambda d'Escherichia coli. C. R. Hebd. Seances Acad. Sci. 24, 1517-1519 (1962).
27. Wissmann, A., et al. Selection for Tn10 tet repressor binding to tet operator in Escherichia coli: isolation of temperature-sensitive mutants and combinatorial mutagenesis in the DNA binding motif. Genetics 128, 225-232 (1991).
28. Chao, Y.P., Chern, J.T., Wen, C.S., Fu, H. Construction and characterization of thermo-inducible vectors derived from heat-sensitive lacI genes in combination with the T7 A1 promoter. Biotechnol. Bioeng. 79, 1-8 (2002).
29. McCabe, K.M., Lacherndo, E.J., Albino-Flores, I., Sheehan, E., Hernandez, M. LacI(Ts)-regulated expression as an in situ intracellular biomolecular thermometer. Appl. Environ. Microbiol. 77, 2863-2868 (2011).
30. Hurme, R., Berndt, K.D., Normark, S.J., Rhen, M. A proteinaceous gene regulatory thermometer in Salmonella. Cell 90, 55-64 (1997).
31. Wilson, C.J., Zhan, H., Swint-Kruse, L., Matthews, K.S. The lactose repressor system: paradigms for regulation, allosteric behavior and protein folding. Cell. Mol. Life Sci. 64, 3-16 (2007).
32. Bertram, R., Hillen, W. The application of Tet repressor in prokaryotic gene regulation and expression. Microb. Biotechnol. 1, 2-16 (2008).
33. Jensen, P.R., Westerhoff, H.V., Michelsen, O. The use of lac-type promoters in control analysis. Eur. J. Biochem. 211, 181-191 (1993).
34. Altschul, S.F., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997).
35. Al-Bataineh, O., Jenne, J., Huber, P. Clinical and future applications of high intensity focused ultrasound in cancer. Cancer Treat. Rev. 38, 346-353 (2012).
36. Elias, W.J., et al. A pilot study of focused ultrasound thalamotomy for essential tremor. N. Engl. J. Med. 369, 640-648 (2013).
37. Deckers, R., et al. Image-guided, noninvasive, spatiotemporal control of gene expression. Proc. Natl. Acad. Sci. USA 106, 1175-1180 (2009).
38. Fite, B.Z., et al. Magnetic resonance thermometry at 7T for real-time monitoring and correction of ultrasound induced mild hyperthermia. PLoS One 7, e35509 (2012).
39. McDannold, N.J., King, R.L., Jolesz, F.A., Hynynen, K.H. Usefulness of MR imaging-derived thermometry and dosimetry in determining the threshold for tissue damage induced by thermal surgery in rabbits. Radiology 216, 517-523 (2000).
40. McDannold, N., Vykhodtseva, N., Jolesz, F.A., Hynynen, K. MRI investigation of the threshold for thermally induced blood-brain barrier disruption and brain tissue damage in the rabbit brain. Magn. Reson. Med. 51, 913-923 (2004).
41. Rudaya, A.Y., Steiner, A.A., Robbins, J.R., Dragic, A.S., Romanovsky, A.A. Thermoregulatory responses to lipopolysaccharide in the mouse: dependence on the dose and ambient temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1244-R1252 (2005).
42. Pritchard, M.T., et al. Protocols for simulating the thermal component of fever: preclinical and clinical experience. Methods 32, 54-62 (2004).
43. Illing, A.C., Shawki, A., Cunningham, C.L., Mackenzie, B. Substrate profile and metal-ion selectivity of human divalent metal-ion transporter-1. J. Biol. Chem. 287, 30485-30496 (2012).
44. Nistala, G.J., Wu, K., Rao, C.V., Bhalerao, K.D. A modular positive feedback-based gene amplifier. J. Biol. Eng. 4, 4 (2010).
45. Andersen, J.B., et al. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl. Environ. Microbiol. 64, 2240-2246 (1998).
46. Natori, Y., Kano, Y., Imamoto, F. Characterization and promoter selectivity of Lactobacillus acidophilus RNA polymerase. Biochimie 70, 1765-1774 (1988).
47. Mimee, M., Tucker, A.C., Voigt, C.A., Lu, T.K. Programming a human commensal bacterium, Bacteroides thetaiotaomicron, to sense and respond to stimuli in the murine gut microbiota. Cell Syst. 1, 62-71 (2015).
48. Tey, S.-K. Adoptive T-cell therapy: adverse events and safety switches. Clin. Transl. Immunology 3, e17 (2014).
49. Chan, C.T., Lee, J.W., Cameron, D.E., Bashor, C.J., Collins, J.J. 'Deadman' and 'Passcode' microbial kill switches for bacterial containment. Nat. Chem. Biol. 12, 82-86 (2016).
50. Gallagher, R.R., Patel, J.R., Interiano, A.L., Rovner, A.J., Isaacs, F.J. Multilayered genetic safeguards limit growth of microorganisms to defined environments. Nucleic Acids Res. 43, 1945-1954 (2015).
51. Lang, K., Chin, J.W. Cellular incorporation of unnatural amino acids and bioorthogonal labeling of proteins. Chem. Rev. 114, 4764-4806 (2014).
52. Handley, A., Schauer, T., Ladurner, A.G., Margulies, C.E. Designing cell-type-specific genome-wide experiments. Mol. Cell 58, 621-631 (2015).
53. Grammel, M., Hang, H.C. Chemical reporters for biological discovery. Nat. Chem. Biol. 9, 475-484 (2013).
54. Ai, H.W., Olenych, S.G., Wong, P., Davidson, M.W., Campbell, R.E. Hue-shifted monomeric variants of Clavularia cyan fluorescent protein: identification of the molecular determinants of color and applications in fluorescence imaging. BMC Biol. 6, 13 (2008).
55. Shaner, N.C., et al. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572 (2004).
56. Kutrowska, B.W., Narczyk, M., Buszko, A., Bzowska, A., Clark, P.L. Folding and unfolding of a non-fluorescent mutant of green fluorescent protein. J. Phys. Condens. Matter 19, 285223 (2007).