Paramagnetic inorganic nanoparticles as T1 MRI contrast agents

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 6, Issue 2, 2014, Pages 196-209

  Lee, Soo Hong ^a,b   Kim, Byung Hyo ^a,b   Na, Hyon Bin ^c   Hyeon, Taeghwan ^a,b  

^a Institute for Basic Science   (South Korea)

^b Seoul National University   (South Korea)

^c Myong Ji University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PROCESS; CLINICAL APPLICATION; INORGANIC NANOPARTICLE; MRI CONTRAST AGENTS; MULTIPLE DISCIPLINES; SAFETY AND EFFICIENCIES; SIGNAL ENHANCEMENT; SPHERICAL NANOPARTICLES;

BIOLOGY; MAGNETIC RESONANCE IMAGING; MEDICINE; MOLECULAR IMAGING; PARAMAGNETISM;

NANOPARTICLES;

GADOLINIUM; IRON OXIDE; MANGANESE; MANGANESE OXIDE; NANOPARTICLE; NUCLEAR MAGNETIC RESONANCE IMAGING AGENT;

ARTICLE; BIOMEDICAL ENGINEERING; CONTRAST ENHANCEMENT; HUMAN; IMAGE ENHANCEMENT; IN VITRO STUDY; IN VIVO STUDY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL;

ANIMALS; CONTRAST MEDIA; GADOLINIUM; HUMANS; IRON; MAGNETIC RESONANCE IMAGING; MAGNETITE NANOPARTICLES; MANGANESE; MICE;

EID: 84893753542     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1243     Document Type: Article

References (75)

1. Hashemi RH, Bradley WG, Lisanti CJ. MRI: The Basics. 2nd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2004.
2. Prasad PV. Magnetic Resonance Imaging: Methods and Biologic Applications. Totowa, NJ: Humana Press; 2006.
3. Modo MMJ, Bulte JWM. Molecular and Cellular MR Imaging. Boca Raton, FL: CRC Press; 2007.
4. Na HB, Hyeon T. Nanostructured T1 MRI contrast agents. J Mater Chem 2009, 19:6267-6273.
5. Lee N, Hyeon T. Designed synthesis of uniformly sized iron oxide nanoparticles for efficient magnetic resonance imaging contrast agents. Chem Soc Rev 2012, 41:2575-2589.
6. O'Handley RC. Modern Magnetic Materials: Principles and Applications. New York: Wiley-Interscience; 1999.
7. Jun Y, Lee JH, Cheon J. Chemical design of nanoparticle probes for high-performance magnetic resonance imaging. Angew Chem Int Ed 2008, 47:5122-5135.
8. Brown MA, Semelka RC. MRI : Basic Principles and Applications. 3rd ed. Hoboken, NJ: Wiley-Liss; 2003.
9. Caravan P. Strategies for increasing the sensitivity of gadolinium based MRI contrast agents. Chem Soc Rev 2006, 35:512-523.
10. Na HB, Lee JH, An K, Park YI, Park M, Lee IS, Nam D-H, Kim ST, Kim S-H, Kim S-W, et al. Development of a T1 contrast agent for magnetic resonance imaging using MnO nanoparticles. Angew Chem Int Ed Engl 2007, 46:5397-5401.
11. Park J, Joo J, Kwon SG, Jang Y, Hyeon T. Synthesis of monodisperse spherical nanocrystals. Angew Chem Int Ed Engl 2007, 46:4630-4660.
12. Nel A, Xia T, Mädler L, Li N. Toxic potential of materials at the nanolevel. Science 2006, 311:622-627.
13. Ling D, Hyeon T. Chemical design of biocompatible iron oxicde nanoparticles for medical applications. Small 2013, 9:1450-1466.
14. Bourrinet P, Bengele HH, Bonnemain B, Dencausse A, Idee JM, Jacobs PM, Lewis JM. Preclinical safety and pharmacokinetic profile of ferumoxtran 10, an ultrasmall superparamagnetic iron oxide magnetic resonance contrast agent. Invest Radiol 2006, 41:313-324.
15. Xing R, Liu G, Quan Q, Bhirde A, Zhang G, Jin A, Bryant LH, Zhang A, Liang A, Eden HS, et al. Functional MnO nanoclusters for efficient siRNA delivery. Chem Commun 2011, 47:12152-12154.
16. Bae KH, Lee K, Kim C, Park TG. Surface functionalized hollow manganese oxide nanoparticles for cancer targeted siRNA delivery and magnetic resonance imaging. Biomaterials 2011, 32:176-184.
17. Schladt TD, Schneider K, Shukoor MI, Natalio F, Bauer H, Tahir MN, Weber S, Schreiber LM, Schroder HC, Muller WEG, et al. Highly soluble multifunctional MnO nanoparticles for simultaneous optical and MRI imaging and cancer treatment using photodynamic therapy. J Mater Chem 2010, 20:8297-8304.
18. Baek MJ, Park JY, Xu W, Kattel K, Kim HG, Lee EJ, Patel AK, Lee JJ, Chang Y, Kim TJ, et al. Water-soluble MnO nanocolloid for a molecular T1 MR imaging: a facile one-pot synthesis, in vivo T1 MR images, and account for relaxivities. ACS Appl Mater Interfaces 2010, 2:2949-2955.
19. Xing R, Zhang F, Xie J, Aronova M, Zhang G, Guo N, Huang X, Sun X, Liu G, Bryant LH, et al. Polyaspartic acid coated manganese oxide nanoparticles for efficient liver MRI. Nanoscale 2011, 3:4943-4945.
20. Huang J, Xie J, Chen K, Bu L, Lee S, Cheng Z, Li X, Chen X. HSA coated MnO nanoparticles with prominent MRI contrast for tumor imaging. Chem Commun 2010, 46:6684-6686.
21. Yang H, Zhuang Y, Hu H, Du X, Zhang C, Shi X, Wu H, Yang S. Silica-coated manganese oxide nanoparticles as a platform for targeted magnetic resonance and fluorescence imaging of cancer cells. Adv Funct Mater 2010, 20:1733-1741.
22. Peng Y-K, Lai C-W, Liu C-L, Chen H-C, Hsiao Y-H, Liu W-L, Tang K-C, Chi Y, Hsiao J-K, Lim K-E, et al. A new and facile method to prepare uniform hollow MnO/functionalized mSiO2 core/shell nanocomposites. ACS Nano 2011, 5:4177-4187.
23. Lee Y-C, Chen D-Y, Dodd SJ, Bouraoud N, Koretsky AP, Krishnan KM. The use of silica coated MnO nanoparticles to control MRI relaxivity in response to specific physiological changes. Biomaterials 2012, 33:3560-3567.
24. Schladt TD, Koll K, Prufer S, Bauer H, Natalio F, Dumele O, Raidoo R, Weber S, Wolfrum U, Schreiber LM, et al. Multifunctional superparamagnetic MnO@SiO2 core/shell nanoparticles and their application for optical and magnetic resonance imaging. J Mater Chem 2012, 22:9253-9262.
25. Rodriguez PL, Harada T, Christian DA, Pantano DA, Tsai RK, Discher DE. Minimal "self" peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 2013, 339:971-975.
26. Pan D, Caruthers SD, Senpan A, Schmieder AH, Wickline SA, Lanza GM. Revisiting an old friend: manganese-based MRI contrast agents. WIREs: Nanomed Nanobiotechnol 2011, 3:162-173.
27. Koretsky AP, Silva AC. Manganese-enhanced magnetic resonance imaging (MEMRI). NMR Biomed 2004, 17:527-531.
28. Wolf G, Baum L. Cardiovascular toxicity and tissue proton T1 response to manganese injection in the dog and rabbit. Am J Roentgenol 1983, 141:193-197.
29. Terreno E, Castelli DD, Viale A, Aime S. Challenges for molecular magnetic resonance imaging. Chem Rev 2010, 110:3019-3042.
30. Huang C-C, Khu N-H, Yeh C-S. The characteristics of sub 10nm manganese oxide T1 contrast agents of different nanostructured morphologies. Biomaterials 2010, 31:4073-4078.
31. An K, Park M, Yu JH, Na HB, Lee N, Park J, Choi SH, Song IC, Moon WK, Hyeon T. Synthesis of uniformly sized manganese oxide nanocrystals with various sizes and shapes and characterization of their T1 magnetic resonance relaxivity. Eur J Inorg Chem 2012, 2012:2148-2155.
32. Yu T, Moon J, Park J, Park YI, Na HB, Kim BH, Song IC, Moon WK, Hyeon T. Various-shaped uniform Mn3O4 nanocrystals synthesized at low temperature in air atmosphere. Chem Mater 2009, 21:2272-2279.
33. Park M, Lee N, Choi SH, An K, Yu S-H, Kim JH, Kwon S-H, Kim D, Kim H, Baek S-I, et al. Large-scale synthesis of ultrathin manganese oxide nanoplates and their applications to T1 MRI contrast agents. Chem Mater 2011, 23:3318-3324.
34. Kim T, Cho E-J, Chae Y, Kim M, Oh A, Jin J, Lee E-S, Baik H, Haam S, Suh J-S, et al. Urchin-shaped manganese oxide nanoparticles as pH-responsive activatable T1 contrast agents for magnetic resonance imaging. Angew Chem Int Ed Engl 2011, 50:10589-10593.
35. Kim J-H, Ha TL, Im GH, Yang J, Seo SW, Lee IS, Lee JH. Magnetic resonance imaging of amyloid plaques using hollow manganese oxide nanoparticles conjugated with antibody aβ1-40 in a transgenic mouse model. NeuroReport 2013, 24:16-21. doi: 10.1097/WNR.1090b1013e32835ba32850.
36. Chen Y, Yin Q, Ji X, Zhang S, Chen H, Zheng Y, Sun Y, Qu H, Wang Z, Li Y, et al. Manganese oxide-based multifunctionalized mesoporous silica nanoparticles for pH-responsive MRI, ultrasonography and circumvention of MDR in cancer cells. Biomaterials 2012, 33:7126-7137.
37. Shin J, Anisur RM, Ko MK, Im GH, Lee JH, Lee IS. Hollow manganese oxide nanoparticles as multifunctional agents for magnetic resonance imaging and drug delivery. Angew Chem Int Ed Engl 2009, 48:321-324.
38. Bardhan R, Lal S, Joshi A, Halas NJ. Theranostic nanoshells: from probe design to imaging and treatment of cancer. Acc Chem Res 2011, 44:936-946.
39. Xing H, Bu W, Zhang S, Zheng X, Li M, Chen F, He Q, Zhou L, Peng W, Hua Y, et al. Multifunctional nanoprobes for upconversion fluorescence, MR and CT trimodal imaging. Biomaterials 2012, 33:1079-1089.
40. 1-weighted MRI and simultaneous anti-cancer drug delivery. Biomaterials 2012, 33:2388-2398.
41. Shukoor MI, Natalio F, Tahir MN, Wiens M, Tarantola M, Therese HA, Barz M, Weber S, Terekhov M, Schröder HC, et al. Pathogen-mimicking MnO nanoparticles for selective activation of the TLR9 pathway and imaging of cancer cells. Adv Funct Mater 2009, 19:3717-3725.
42. Shukoor MI, Natalio F, Tahir MN, Barz M, Weber S, Brochhausen C, Zentel R, Schreiber LM, Brieger J, Tremel W. CpG-DNA loaded multifunctional MnO nanoshuttles for TLR9-specific cellular cargo delivery, selective immune-activation and MRI. J Mater Chem 2012, 22:8826-8834.
43. Gilad AA, Walczak P, McMahon MT, Na HB, Lee JH, An K, Hyeon T, van Zijl PCM, Bulte JWM. MR tracking of transplanted cells with "positive contrast" using manganese oxide nanoparticles. Magn Reson Med 2008, 60:1-7.
44. Létourneau M, Tremblay M, Faucher L, Rojas D, Chevallier P, Gossuin Y, Lagueux J, Fortin M-A. MnO-labeled cells: positive contrast enhancement in MRI. J Phys Chem B 2012, 116:13228-13238.
45. Kim T, Momin E, Choi J, Yuan K, Zaidi H, Kim J, Park M, Lee N, McMahon MT, Quinones-Hinojosa A, et al. Mesoporous silica-coated hollow manganese oxide nanoparticles as positive T1 contrast agents for labeling and MRI tracking of adipose-derived mesenchymal stem cells. J Am Chem Soc 2011, 133:2955-2961.
46. Lee N, Kim H, Choi SH, Park M, Kim D, Kim H-C, Choi Y, Lin S, Kim BH, Jung HS, et al. Magnetosome-like ferrimagnetic iron oxide nanocubes for highly sensitive MRI of single cells and transplanted pancreatic islets. Proc Natl Acad Sci U S A 2011, 108:2662-2667.
47. Huh Y-M, Jun Y-W, Song H-T, Kim S, Choi J-S, Lee J-H, Yoon S, Kim K-S, Shin J-S, Suh J-S, et al. In vivo magnetic resonance detection of cancer by using multifunctional magnetic nanocrystals. J Am Chem Soc 2005, 127:12387-12391.
48. Wang Y-X, Hussain S, Krestin G. Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging. Eur Radiol 2001, 11:2319-2331.
49. Bulte JWM, Kraitchman DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 2004, 17:484-499.
50. Weissleder R, Elizondo G, Wittenberg J, Rabito CA, Bengele HH, Josephson L. Ultrasmall superparamagnetic iron oxide: characterization of a new class of contrast agents for MR imaging. Radiology 1990, 175:489-493.
51. Weissleder R, Moore A, Mahmood U, Bhorade R, Benveniste H, Chiocca EA, Basilion JP. In vivo magnetic resonance imaging of transgene expression. Nat Med 2000, 6:351-354.
52. Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF. Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation 2001, 103:415-422.
53. Strobel K, Hoerr V, Schmid F, Wachsmuth L, Löffler B, Faber C. Early detection of lung inflammation: exploiting T1-effects of iron oxide particles using UTE MRI. Magn Reson Med 2012, 68:1924-1931.
54. Taboada E, Rodríguez E, Roig A, Oró J, Roch A, Muller RN. Relaxometric and magnetic characterization of ultrasmall iron oxide nanoparticles with high magnetization. Evaluation as potential T1 magnetic resonance imaging contrast agents for molecular imaging. Langmuir 2007, 23:4583-4588.
55. Tromsdorf UI, Bruns OT, Salmen SC, Beisiegel U, Weller H. A highly effective, nontoxic T1 MR contrast agent based on ultrasmall pegylated iron oxide nanoparticles. Nano Lett 2009, 9:4434-4440.
56. Kim BH, Lee N, Kim H, An K, Park YI, Choi Y, Shin K, Lee Y, Kwon SG, Na HB, et al. Large-scale synthesis of uniform and extremely small-sized iron oxide nanoparticles for high-resolution T1 magnetic resonance imaging contrast agents. J Am Chem Soc 2011, 133:12624-12631.
57. Coey JMD. Noncollinear spin arrangement in ultrafine ferrimagnetic crystallites. Phys Rev Lett 1971, 27:1140-1142.
58. Linderoth S, Hendriksen PV, Bødker F, Wells S, Davies K, Charles SW, Mørup S. On spin-canting in maghemite particles. J Appl Phys 1994, 75:6583-6585.
59. Li Z, Yi PW, Sun Q, Lei H, Li Zhao H, Zhu ZH, Smith SC, Lan MB, Lu GQ. Ultrasmall water-soluble and biocompatible magnetic iron oxide nanoparticles as positive and negative dual contrast agents. Adv Funct Mater 2012, 22:2387-2393.
60. Caravan P, Ellison JJ, McMurry TJ, Lauffer RB. Gadolinium(III) chelates as MRI contrast agents: structure, dynamics, and applications. Chem Rev 1999, 99:2293-2352.
61. Kattel K, Park JY, Xu W, Kim HG, Lee EJ, Bony BA, Heo WC, Lee JJ, Jin S, Baeck JS, et al. A facile synthesis, in vitro and in vivo MR studies of d-glucuronic acid-coated ultrasmall Ln2O3 (Ln=Eu, Gd, Dy, Ho, and Er) nanoparticles as a new potential MRI contrast agent. ACS Appl Mater Interfaces 2011, 3:3325-3334.
62. Soo Choi H, Liu W, Misra P, Tanaka E, Zimmer JP, Itty Ipe B, Bawendi MG, Frangioni JV. Renal clearance of quantum dots. Nat Biotech 2007, 25:1165-1170.
63. Bridot J-L, Faure A-C, Laurent S, Rivière C, Billotey C, Hiba B, Janier M, Josserand V, Coll J-L, Vander Elst L, et al. Hybrid gadolinium oxide nanoparticles: multimodal contrast agents for in vivo imaging. J Am Chem Soc 2007, 129:5076-5084.
64. Park JY, Baek MJ, Choi ES, Woo S, Kim JH, Kim TJ, Jung JC, Chae KS, Chang Y, Lee GH. Paramagnetic ultrasmall gadolinium oxide nanoparticles as advanced T1 MRI contrast agent: account for large longitudinal relaxivity, optimal particle diameter, and in vivo T1 MR images. ACS Nano 2009, 3:3663-3669.
65. Evanics F, Diamente PR, van Veggel FCJM, Stanisz GJ, Prosser RS. Water-soluble GdF3 and GdF3/LaF3 nanoparticles physical characterization and NMR relaxation properties. Chem Mater 2006, 18:2499-2505.
66. Cheung ENM, Alvares RDA, Oakden W, Chaudhary R, Hill ML, Pichaandi J, Mo GCH, Yip C, Macdonald PM, Stanisz GJ, et al. Polymer-stabilized lanthanide fluoride nanoparticle aggregates as contrast agents for magnetic resonance imaging and computed tomography. Chem Mater 2010, 22:4728-4739.
67. Hifumi H, Yamaoka S, Tanimoto A, Citterio D, Suzuki K. Gadolinium-based hybrid nanoparticles as a positive MR contrast agent. J Am Chem Soc 2006, 128:15090-15091.
68. Kumar R, Nyk M, Ohulchanskyy TY, Flask CA, Prasad PN. Combined optical and MR bioimaging using rare earth ion doped NaYF4 nanocrystals. Adv Funct Mater 2009, 19:853-859.
69. Park YI, Kim JH, Lee KT, Jeon K-S, Na HB, Yu JH, Kim HM, Lee N, Choi SH, Baik S-I, et al. Nonblinking and nonbleaching upconverting nanoparticles as an optical imaging nanoprobe and T1 magnetic resonance imaging contrast agent. Adv Mater 2009, 21:4467-4471.
70. Park YI, Kim HM, Kim JH, Moon KC, Yoo B, Lee KT, Lee N, Choi Y, Park W, Ling D, et al. Theranostic probe based on lanthanide-doped nanoparticles for simultaneous in vivo dual-modal imaging and photodynamic therapy. Adv Mater 2012, 24:5755-5761.
71. Chen F, Bu W, Zhang S, Liu X, Liu J, Xing H, Xiao Q, Zhou L, Peng W, Wang L, et al. Positive and negative lattice shielding effects co-existing in Gd (III) ion doped bifunctional upconversion nanoprobes. Adv Funct Mater 2011, 21:4285-4294.
72. Johnson NJJ, Oakden W, Stanisz GJ, Scott Prosser R, van Veggel FCJM. Size-tunable, ultrasmall NaGdF4 nanoparticles: insights into their T1 MRI contrast enhancement. Chem Mater 2011, 23:3714-3722.
73. Tian G, Gu Z, Zhou L, Yin W, Liu X, Yan L, Jin S, Ren W, Xing G, Li S, et al. Mn2+ dopant-controlled synthesis of NaYF4:Yb/Er upconversion nanoparticles for in vivo imaging and drug delivery. Adv Mater 2012, 24:1226-1231.
74. Zhang Y, Lin JD, Vijayaragavan V, Bhakoo KK, Tan TTY. Tuning sub-10nm single-phase NaMnF3 nanocrystals as ultrasensitive hosts for pure intense fluorescence and excellent T1 magnetic resonance imaging. Chem Commun 2012, 48:10322-10324.
75. Ju Q, Tu D, Liu Y, Li R, Zhu H, Chen J, Chen Z, Huang M, Chen X. Amine-functionalized lanthanide-doped KGdF4 nanocrystals as potential optical/magnetic multimodal bioprobes. J Am Chem Soc 2011, 134:1323-1330.