A pH-activatable nanoparticle with signal-amplification capabilities for non-invasive imaging of tumour malignancy

Nature Nanotechnology

Volumn 11, Issue 8, 2016, Pages 724-730

  Mi, Peng ^a,b,c   Kokuryo, Daisuke ^d   Cabral, Horacio ^b   Wu, Hailiang ^b   Terada, Yasuko ^e   Saga, Tsuneo ^d   Aoki, Ichio ^d   Nishiyama, Nobuhiro ^a,c   Kataoka, Kazunori ^b,c,f  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c KAWASAKI INSTITUTE OF INDUSTRIAL PROMOTION   (Japan)

^d NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^e JAPAN SYNCHROTRON RADIATION RESEARCH INSTITUTE   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM PHOSPHATE; DIAGNOSIS; MAGNETIC RESONANCE IMAGING; MANGANESE; NANOMAGNETICS; NANOPARTICLES; POLYETHYLENE GLYCOLS; REDOX REACTIONS; RESONANCE; TUMORS;

BIOLOGICAL PROCESS; CANCER DIAGNOSIS; ENGINEERED NANOPARTICLES; MRI CONTRAST AGENTS; NON-INVASIVE IMAGING; PATHOPHYSIOLOGICAL; REDOX POTENTIALS; SIGNAL AMPLIFICATIONS;

PHOSPHORUS COMPOUNDS;

CALCIUM PHOSPHATE; GADOLINIUM PENTETATE MEGLUMINE; GADOXETIC ACID; MACROGOL; MANGANESE DERIVATIVE; MANGANESE DOPED CALCIUM PHOSPHATE NANOPARTICLE; NANOPARTICLE; NUCLEAR MAGNETIC RESONANCE IMAGING AGENT; UNCLASSIFIED DRUG; URANYL ACETATE; CONTRAST MEDIUM; MANGANESE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER DIAGNOSIS; CANCER SURVIVAL; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DRUG CLEARANCE; DRUG SYNTHESIS; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; LD50; LIVER METASTASIS; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATION REDUCTION POTENTIAL; PH; PRIORITY JOURNAL; PROTEIN BINDING; SYNCHROTRON RADIATION; TUMOR MICROENVIRONMENT; ANIMAL; CHEMISTRY; DIAGNOSTIC IMAGING; EXPERIMENTAL NEOPLASM; LIVER TUMOR; METABOLISM; MOLECULAR IMAGING; NANOMEDICINE; NEOPLASM; PROCEDURES;

ANIMALS; CALCIUM PHOSPHATES; CONTRAST MEDIA; HYDROGEN-ION CONCENTRATION; LIVER NEOPLASMS; MAGNETIC RESONANCE IMAGING; MANGANESE; MICE; MOLECULAR IMAGING; NANOMEDICINE; NANOPARTICLES; NEOPLASMS; NEOPLASMS, EXPERIMENTAL; POLYETHYLENE GLYCOLS;

EID: 84968542763     PISSN: 17483387     EISSN: 17483395     Source Type: Journal    
DOI: 10.1038/nnano.2016.72     Document Type: Article

References (46)

1. Na, H. B. & Hyeon, T. Nanostructured T1 MRI contrast agents. J. Mater. Chem. 19, 6267-6273 (2009).
2. Sun, C., Lee, J. S. H. & Zhang, M. Q. Magnetic nanoparticles in MR imaging and drug delivery. Adv. Drug Deliver. Rev. 60, 1252-1265 (2008).
3. Ghosh, D. et al. M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer. Nature Nanotech. 7, 677-682 (2012).
4. Lee, J. H. et al. Artificially engineered magnetic nanoparticles for ultra-sensitive molecular imaging. Nature Med. 13, 95-99 (2007).
5. Burrell, R. A., McGranahan, N., Bartek, J. & Swanton, C. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501, 338-345 (2013).
6. Kim, T. et al. Urchin-shaped manganese oxide nanoparticles as pH-responsive activatable T1 contrast agents for magnetic resonance imaging. Angew. Chem. Int. Ed. 50, 10589-10593 (2011).
7. Gao, G. H. et al. Magnetite-nanoparticle-encapsulated pH-responsive polymeric micelle as an MRI probe for detecting acidic pathologic areas. Small 6, 1201-1204 (2010).
8. Chen, Y. et al. Manganese oxide-based multifunctionalized mesoporous silica nanoparticles for pH-responsive MRI, ultrasonography and circumvention of MDR in cancer cells. Biomaterials 33, 7126-7137 (2012).
9. Sowers, M. A. et al. Redox-responsive branched-bottlebrush polymers for in vivo MRI and fluorescence imaging. Nature Commun. 5, 5460 (2014).
10. Huang, X. N. et al. Multi-chromatic pH-activatable 19F-MRI nanoprobes with binary ON/OFF pH transitions and chemical-shift barcodes. Angew. Chem. Int. Ed. 52, 8074-8078 (2013).
11. Oishi, M., Sumitani, S. & Nagasaki, Y. On-Off regulation of 19F magnetic resonance signals based on pH-sensitive PEGylated nanogels for potential tumor-specific smart 19F MRI probes. Bioconjug. Chem. 18, 1379-1382 (2007).
12. Bennewitz, M. F. et al. Biocompatible and pH-sensitive PLGA encapsulated MnO nanocrystals for molecular and cellular MRI. ACS Nano 5, 3438-3446 (2011).
13. Koylu, M. Z., Asubay, S. & Yilmaz, A. Determination of proton relaxivities of Mn(II), Cu(II) and Cr(III) added to solutions of serum proteins. Molecules 14, 1537-1545 (2009).
14. Aime, S., Canton, S., Crich, S. G. & Terreno, E. 1H and 17O relaxometric investigations of the binding of Mn(II) ion to human serum albumin. Magn. Reson. Chem. 40, 41-48 (2002).
15. Na, H. B. et al. Development of a T1 contrast agent for magnetic resonance imaging using MnO nanoparticles. Angew. Chem. Int. Ed. 46, 5397-5401 (2007).
16. Zhang, M. Z. & Kataoka, K. Nano-structured composites based on calcium phosphate for cellular delivery of therapeutic and diagnostic agents. Nano Today 4, 508-517 (2009).
17. LeGeros, R. Z. Calcium phosphate-based osteoinductive materials. Chem. Rev. 108, 4742-4753 (2008).
18. Kakizawa, Y. & Kataoka, K. Block copolymer self-assembly into monodispersive nanoparticles with hybrid core of antisense DNA and calcium phosphate. Langmuir 18, 4539-4543 (2002).
19. Yushmanov, V. E., Tominaga, T. T., Borissevitch, I. E., Imasato, H. & Tabak, M. Binding of manganese and iron tetraphenylporphine sulfonates to albumin is relevant to their contrast properties. Magn. Reson. Imaging 14, 255-261 (1996).
20. Marchal, G. et al. Comparison between Gd-DTPA, Gd-EOB-DTPA, and Mn-DPDP in induced HCC in rats: a correlation study of MR imaging, microangiography, and histology. Magn Reson Imaging 11, 665-674 (1993).
21. Wheaton, A. J. & Miyazaki, M. Non-contrast enhanced MR angiography: physical principles. J. Magn. Reson. Imaging 36, 286-304 (2012).
22. Terreno, E., Castelli, D. D., Viale, A. & Aime, S. Challenges for molecular magnetic resonance imaging. Chem. Rev. 110, 3019-3042 (2010).
23. Gatenby, R. A. & Gillies, R. J. Why do cancers have high aerobic glycolysis? Nature Rev. Cancer 4, 891-899 (2004).
24. Helmlinger, G., Yuan, F., Dellian, M. & Jain, R. K. Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nature Med. 3, 177-182 (1997).
25. Gujar, S. K., Maheshwari, S., Bjorkman-Burtscher, I. & Sundgren, P. C. Magnetic resonance spectroscopy. J. Neuroophthalmol. 25, 217-226 (2005).
26. Fingar, V. H., Wieman, T. J., Park, Y. J. & Henderson, B. W. Implications of a pre-existing tumor hypoxic fraction on photodynamic therapy. J. Surg. Res. 53, 524-528 (1992).
27. Vogl, T. J. et al. Liver tumors: comparison of MR imaging with Gd-EOB-DTPA and Gd-DTPA. Radiology 200, 59-67 (1996).
28. Cory, D. A., Schwartzentruber, D. J. & Mock, B. H. Ingested manganese chloride as a contrast agent for magnetic resonance imaging. Magn. Reson. Imaging 5, 65-70 (1987).
29. Wu, H. L. et al. Polymeric micelles loaded with platinum anticancer drugs target preangiogenic micrometastatic niches associated with inflammation. J. Control. Release 189, 1-10 (2014).
30. Lu, H. T., Ouyang, W. M. & Huang, C. S. Inflammation, a key event in cancer development. Mol. Cancer Res. 4, 221-233 (2006).
31. Gallagher, F. A. et al. Magnetic resonance imaging of pH in vivo using hyperpolarized 13C-labelled bicarbonate. Nature 453, 940-943 (2008).
32. Webb, B. A., Chimenti, M., Jacobson, M. P. & Barber, D. L. Dysregulated pH: a perfect storm for cancer progression. Nature Rev. Cancer 11, 671-677 (2011).
33. Wilson, W. R. & Hay, M. P. Targeting hypoxia in cancer therapy. Nature Rev. Cancer 11, 393-410 (2011).
34. Hashim, A. I., Zhang, X. M., Wojtkowiak, J. W., Martinez, G. V. & Gillies, R. J. Imaging pH and metastasis. NMR Biomed. 24, 582-591 (2011).
35. Zhang, G., Palmer, G. M., Dewhirst, M. W. & Fraser, C. L. A dual-emissivematerials design concept enables tumour hypoxia imaging. Nature Mater. 8, 747-751 (2009).
36. Kircher, M. F. et al. A brain tumor molecular imaging strategy using a new triplemodality MRI-photoacoustic-Raman nanoparticle. Nature Med. 18, 829-834 (2012).
37. Komar, G. et al. 18F-EF5: a new PET tracer for imaging hypoxia in head and neck cancer. J. Nucl. Med. 49, 1944-1951 (2008).
38. Schroeder, A. et al. Treating metastatic cancer with nanotechnology. Nature Rev. Cancer 12, 39-50 (2012).
39. Chaffer, C. L. & Weinberg, R. A. A perspective on cancer cell metastasis. Science 331, 1559-1564 (2011).
40. Ichikawa, T. et al. Detection and characterization of focal liver lesions: a Japanese phase III, multicenter comparison between gadoxetic acid disodium-enhanced magnetic resonance imaging and contrast-enhanced computed tomography predominantly in patients with hepatocellular carcinoma and chronic liver disease. Invest. Radiol. 45, 133-141 (2010).
41. Chan, K. W. Y. et al. MRI-detectable pH nanosensors incorporated into hydrogels for in vivo sensing of transplanted-cell viability. Nature Mater. 12, 268-275 (2013).
42. Willmann, J. K., van Bruggen, N., Dinkelborg, L. M. & Gambhir, S. S. Molecular imaging in drug development. Nature Rev. Drug Discov. 7, 591-607 (2008).
43. Weissleder, R. & Pittet, M. J. Imaging in the era of molecular oncology. Nature 452, 580-589 (2008).
44. Nishiyama, N. et al. Novel cisplatin-incorporated polymeric micelles can eradicate solid tumors in mice. Cancer Res. 63, 8977-8983 (2003).
45. Cabral, H. et al. Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nature Nanotechnol. 6, 815-823 (2011).
46. Terada, Y. et al. Construction and commissioning of BL37XU at SPring8. AIP Conf. Proc. 705, 376-379 (2004).