Engineering intracellular biomineralization and biosensing by a magnetic protein

Nature Communications

Volumn 6, Issue , 2015, Pages

  Matsumoto, Yuri ^a   Chen, Ritchie ^a,b   Anikeeva, Polina ^a,b   Jasanoff, Alan ^a,b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACCUMULATION; BIOENGINEERING; BIOMINERALIZATION; CELLS AND CELL COMPONENTS; GENE EXPRESSION; IRON OXIDE; MAGNETIC PROPERTY; MOLECULAR ANALYSIS; PHYSIOLOGY; PROTEIN;

MAMMALIA;

CARRIER PROTEIN; FTR1 PROTEIN, S CEREVISIAE; IRON; SACCHAROMYCES CEREVISIAE PROTEIN;

CHEMISTRY; GENETIC PROCEDURES; GENETICS; MAGNETISM; METABOLISM; PROTEIN ENGINEERING; SACCHAROMYCES CEREVISIAE;

BIOSENSING TECHNIQUES; IRON; MAGNETICS; MEMBRANE TRANSPORT PROTEINS; PROTEIN ENGINEERING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84946197909     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9721     Document Type: Article

References (47)

1. van der Graaf, M. In vivo magnetic resonance spectroscopy: basic methodology and clinical applications. Eur. Biophys. J. 39, 527-540 (2010).
2. Atanasijevic, T., Shusteff, M., Fam, P. & Jasanoff, A. Calcium-sensitive MRI contrast agents based on superparamagnetic iron oxide nanoparticles and calmodulin. Proc. Natl Acad. Sci. USA 103, 14707-14712 (2006).
3. Li, W. H., Fraser, S. E. & Meade, T. J. A calcium-sensitive magnetic resonance imaging contrast agent. J. Am. Chem. Soc. 121, 1413-1414 (1999).
4. Louie, A. Y., et al. In vivo visualization of gene expression using magnetic resonance imaging. Nat. Biotechnol. 18, 321-325 (2000).
5. Weissleder, R., et al. In vivo magnetic resonance imaging of transgene expression. Nat. Med. 6, 351-355 (2000).
6. Cho, M. H., et al. A magnetic switch for the control of cell death signalling in in vitro and in vivo systems. Nat. Mater. 11, 1038-1043 (2012).
7. Huang, H., Delikanli, S., Zeng, H., Ferkey, D. M. & Pralle, A. Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. Nat. Nanotechnol. 5, 602-606 (2010).
8. Etoc, F., et al. Subcellular control Rac-GTPase signalling by magnetogenetic manipulation inside living cells. Nat. Nanotechnol. 8, 193-198 (2013).
9. Nishida, K. & Silver, P. A. Induction of biogenic magnetization and redox control by a component of the target of rapamycin complex 1 signaling pathway. PLoS Biol. 10, e1001269 (2012).
10. Kim, T., Moore, D. & Fussenegger, M. Genetically programmed superparamagnetic behavior of mammalian cells. J. Biotechnol. 162, 237-245 (2012).
11. Bartelle, B. B., Szulc, K. U., Suero-Abreu, G. A., Rodriguez, J. J. & Turnbull, D. H. Divalent metal transporter, DMT1: A novel MRI reporter protein. Magn. Reson. Med. 70, 842-850 (2013).
12. Genove, G., DeMarco, U., Xu, H. Y., Goins, W. F. & Ahrens, E. T. A new transgene reporter for in vivo magnetic resonance imaging. Nat. Med. 11, 450-454 (2005).
13. Cohen, B., Dafni, H., Meir, G., Harmelin, A. & Neeman, M. Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6 glioma tumors. Neoplasia 7, 109-117 (2005).
14. Zurkiya, O., Chan, A. W. S. & Hu, X. P. MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Magn. Reson. Med. 59, 1225-1231 (2008).
15. Theil, E. C. Ferritin-structure, gene-regulation, and cellular function in animals, plants, and microorganisms. Annu. Rev. Biochem. 56, 289-315 (1987).
16. Liu, J., et al. Noninvasive monitoring of embryonic stem cells in vivo with MRI transgene reporter. Tissue. Eng. Part C Methods 15, 739-747 (2009).
17. Naumova, A. V., et al. Ferritin overexpression for noninvasive magnetic resonance imaging-based tracking of stem cells transplanted into the heart. Mol. Imaging 9, 201-210 (2010).
18. Wang, Q., Mercogliano, C. P. & Lowe, J. A ferritin-based label for cellular electron cryotomography. Structure 19, 147-154 (2011).
19. Stanley, S. A., et al. Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice. Science 336, 604-608 (2012).
20. Shi, H. F., Bencze, K. Z., Stemmler, T. L. & Philpott, C. C. A cytosolic iron chaperone that delivers iron to ferritin. Science 320, 1207-1210 (2008).
21. Meldrum, F. C., Heywood, B. R. & Mann, S. Magnetoferritin - in vitro synthesis of a novel magnetic protein. Science 257, 522-523 (1992).
22. Vymazal, J., Zak, O., Bulte, J. W. M., Aisen, P. & Brooks, R. A. T1 and T2 of ferritin solutions: effect of loading factor. Magn. Reson. Med. 36, 61-65 (1996).
23. Yamaguchi-Iwai, Y., Ueta, R., Fukunaka, A. & Sasaki, R. Subcellular localization of Aft1 transcription factor responds to iron status in Saccharomyces cerevisiae. J. Biol. Chem. 277, 18914-18918 (2002).
24. Yamaguchi-Iwai, Y., Stearman, R., Dancis, A. & Klausner, R. D. Iron-regulated DNA binding by the AFT1 protein controls the iron regulon in yeast. EMBO J. 15, 3377-3384 (1996).
25. Strochlic, T. I., Setty, T. G., Sitaram, A. & Burd, C. G. Grd19/Snx3p functions as a cargo-specific adapter for retromer-dependent endocytic recycling. J. Cell Biol. 177, 115-125 (2007).
26. Tatur, J., Hagedoorn, P. L., Overeijnder, M. L. & Hagen, W. R. A highly thermostable ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus. Extremophiles 10, 139-148 (2006).
27. Stefanini, S., et al. Thermal stability of horse spleen apoferritin and human recombinant H apoferritin. Arch. Biochem. Biophys. 325, 58-64 (1996).
28. Friedman, J. R., Voskoboynik, U. & Sarachik, M. P. Anomalous magnetic relaxation in ferritin. Phys. Rev. B 56, 10793-10796 (1997).
29. Tejada, J., Zhang, X. X., del Barco, E., Hernandez, J. M. & Chudnovsky, E. M. Macroscopic resonant tunneling of magnetization in ferritin. Phys. Rev. Lett. 79, 1754-1757 (1997).
30. Tatur, J., Hagen, W. R. & Matias, P. M. Crystal structure of the ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus. J. Biol. Inorg. Chem. 12, 615-630 (2007).
31. Kasyutich, O., et al. Silver ion incorporation and nanoparticle formation inside the cavity of Pyrococcus furiosus ferritin: structural and size-distribution analyses. J. Am. Chem. Soc. 132, 3621-3627 (2010).
32. Iordanova, B., Robison, C. S. & Ahrens, E. T. Design and characterization of a chimeric ferritin with enhanced iron loading and transverse NMR relaxation rate. J. Biol. Inorg. Chem. 15, 957-965 (2010).
33. Bennett, K. M., Shapiro, E. M., Sotak, C. H. & Koretsky, A. P. Controlled aggregation of ferritin to modulate MRI relaxivity. Biophys. J. 95, 342-351 (2008).
34. Shapiro, M. G., Szablowski, J. O., Langer, R. & Jasanoff, A. Protein nanoparticles engineered to sense kinase activity in MRI. J. Am. Chem. Soc 131, 2484-2486 (2009).
35. Shapiro, M. G., Atanasijevic, T., Faas, H., Westmeyer, G. G. & Jasanoff, A. Dynamic imaging with MRI contrast agents: quantitative considerations. Magn. Reson. Imaging 24, 449-462 (2006).
36. Lawson, D. M., et al. Identification of the ferroxidase center in ferritin. FEBS Lett. 254, 207-210 (1989).
37. Levi, S., et al. Mutational analysis of the channel and loop sequences of human ferritin H-chain. Biochem. J. 264, 381-388 (1989).
38. Wade, V. J., et al. Influence of site-directed modifications on the formation of iron cores in ferritin. J. Mol. Biol. 221, 1443-1452 (1991).
39. Shapiro, M. G., et al. Directed evolution of a magnetic resonance imaging contrast agent for noninvasive imaging of dopamine. Nat. Biotechnol. 28, 264-270 (2010).
40. Uchida, M., Kang, S., Reichhardt, C., Harlen, K. & Douglas, T. The ferritin superfamily: Supramolecular templates for materials synthesis. Biochim. Biophys. Acta 1800, 834-845 (2010).
41. Wach, A., Brachat, A., Pohlmann, R. & Philippsen, P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808 (1994).
42. Volschenk, H., et al. Malolactic fermentation in grape musts by a genetically engineered strain of Saccharomyces cerevisiae. Am. J. Enol. Vitic. 48, 193-197 (1997).
43. Chao, G., et al. Isolating and engineering human antibodies using yeast surface display. Nat. Protoc. 1, 755-768 (2006).
44. Tamarit, J., Irazusta, V., Moreno-Cermeno, A. & Ros, J. Colorimetric assay for the quantitation of iron in yeast. Anal. Biochem. 351, 149-151 (2006).
45. Ebrahimi, K. H., Hagedoorn, P. L., Jongejan, J. A. & Hagen, W. R. Catalysis of iron core formation in Pyrococcus furiosus ferritin. J. Biol. Inorg. Chem. 14, 1265-1274 (2009).
46. Athavankar, S. & Peterson, B. R. Control of gene expression with small molecules: Biotin-mediated acylation of targeted lysine residues in recombinant yeast. Chem. Biol. 10, 1245-1253 (2003).
47. von der Haar, T. Optimized protein extraction for quantitative proteomics of yeasts. PLoS ONE 2, e1078 (2007).