Clinically viable magnetic poly(lactide-co-glycolide) particles for MRI-based cell tracking

Magnetic Resonance in Medicine

Volumn 71, Issue 3, 2014, Pages 1238-1250

  Granot, Dorit ^a   Nkansah, Michael K ^a,b   Bennewitz, Margaret F ^a,b   Tang, Kevin S ^a,b   Markakis, Eleni A ^a   Shapiro, Erik M ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

cellular MRI; iron oxide; microparticle; nanoparticle; stem cells

Indexed keywords

BIODEGRADATION; CYTOLOGY; IRON OXIDES; MAGNETIC AFTER EFFECT; MAGNETIC BUBBLES; NANOPARTICLES; STEM CELLS;

BIODEGRADATION STUDIES; CELLULAR MRIS; CELLULAR PERFORMANCE; MAGNETIC CELL LABELING; MICRO PARTICLES; NEURAL PROGENITOR CELLS; POLY-LACTIDE-CO-GLYCOLIDE; STEM CELL DIFFERENTIATION;

MOLECULAR BIOLOGY;

INTERLEUKIN 6; IRON OXIDE; MAGNETITE; POLYGLACTIN; TUMOR NECROSIS FACTOR ALPHA; BIOCOMPATIBLE COATED MATERIAL; CONTRAST MEDIUM; LACTIC ACID; MAGNETITE NANOPARTICLE; NANOCAPSULE; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIODEGRADATION; CELL DIFFERENTIATION; CELL LABELING; CELL MIGRATION; CELL STIMULATION; CELL TRACKING; CELL TRANSPLANTATION; CELL TYPE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; IN VIVO STUDY; MESENCHYMAL STEM CELL; MICROSCOPY; MOUSE; MRI BASED CELL TRACKING; NANOENCAPSULATION; NANOFABRICATION; NEURAL STEM CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARTICLE SIZE; PROCESS DESIGN; RAT; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; IMAGE ENHANCEMENT; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SYNTHESIS; ULTRASTRUCTURE;

ANIMALS; CELL TRACKING; CELLS, CULTURED; COATED MATERIALS, BIOCOMPATIBLE; CONTRAST MEDIA; FEMALE; IMAGE ENHANCEMENT; LACTIC ACID; MAGNETIC RESONANCE IMAGING; MAGNETITE NANOPARTICLES; MICE; NANOCAPSULES; NEURAL STEM CELLS; PARTICLE SIZE; POLYGLYCOLIC ACID; RATS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 84894484566     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.24741     Document Type: Article

References (56)

1. Bulte JW,. In vivo MRI cell tracking: clinical studies. AJR Am J Roentgenol 2009; 193: 314-325.
2. Shapiro EM, Skrtic S, Koretsky AP,. Sizing it up: cellular MRI using micron-sized iron oxide particles. Magn Reson Med 2005; 53: 329-338.
3. Shapiro EM, Skrtic S, Sharer K, Hill JM, Dunbar CE, Koretsky AP,. MRI detection of single particles for cellular imaging. Proc Natl Acad Sci USA 2004; 101: 10901-10906.
4. Bulte JW, Douglas T, Witwer B, et al. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol 2001; 19: 1141-1147.
5. Hill JM, Dick AJ, Raman VK, et al. Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 2003; 108: 1009-1014.
6. Kircher MF, Allport JR, Graves EE, Love V, Josephson L, Lichtman AH, Weissleder R,. In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors. Cancer Res 2003; 63: 6838-6846.
7. Artemov D, Bhujwalla ZM, Bulte JW,. Magnetic resonance imaging of cell surface receptors using targeted contrast agents. Curr Pharm Biotechnol 2004; 5: 485-494.
8. Benderbous S, Corot C, Jacobs P, Bonnemain B,. Superparamagnetic agents: physicochemical characteristics and preclinical imaging evaluation. Acad Radiol 1996; 3 (Suppl 2): S292-S294.
9. Raynal I, Prigent P, Peyramaure S, Najid A, Rebuzzi C, Corot C,. Macrophage endocytosis of superparamagnetic iron oxide nanoparticles: mechanisms and comparison of ferumoxides and ferumoxtran-10. Invest Radiol 2004; 39: 56-63.
10. Saleh A, Schroeter M, Ringelstein A, Hartung HP, Siebler M, Modder U, Jander S,. Iron oxide particle-enhanced MRI suggests variability of brain inflammation at early stages after ischemic stroke. Stroke 2007; 38: 2733-2737.
11. Levy M, Luciani N, Alloyeau D, et al. Long term in vivo biotransformation of iron oxide nanoparticles. Biomaterials 2011; 32: 3988-3999.
12. Arbab AS, Bashaw LA, Miller BR, Jordan EK, Bulte JW, Frank JA,. Intracytoplasmic tagging of cells with ferumoxides and transfection agent for cellular magnetic resonance imaging after cell transplantation: methods and techniques. Transplantation 2003; 76: 1123-1130.
13. Kalish H, Arbab AS, Miller BR, Lewis BK, Zywicke HA, Bulte JW, Bryant LH, Jr, Frank JA,. Combination of transfection agents and magnetic resonance contrast agents for cellular imaging: relationship between relaxivities, electrostatic forces, and chemical composition. Magn Reson Med 2003; 50: 275-282.
14. Frank JA, Miller BR, Arbab AS, Zywicke HA, Jordan EK, Lewis BK, Bryant LH, Jr, Bulte JW,. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 2003; 228: 480-487.
15. Arbab AS, Yocum GT, Kalish H, Jordan EK, Anderson SA, Khakoo AY, Read EJ, Frank JA,. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood 2004; 104: 1217-1223.
16. Janic B, Rad AM, Jordan EK, Iskander AS, Ali MM, Varma NR, Frank JA, Arbab AS,. Optimization and validation of FePro cell labeling method. PLoS One 2009; 4: e5873.
17. Thu MS, Bryant LH, Coppola T, et al. Self-assembling nanocomplexes by combining ferumoxytol, heparin and protamine for cell tracking by magnetic resonance imaging. Nat Med 2012; 18: 463-467.
18. Hinds KA, Hill JM, Shapiro EM, Laukkanen MO, Silva AC, Combs CA, Varney TR, Balaban RS, Koretsky AP, Dunbar CE,. Highly efficient endosomal labeling of progenitor and stem cells with large magnetic particles allows magnetic resonance imaging of single cells. Blood 2003; 102: 867-872.
19. Shapiro EM, Sharer K, Skrtic S, Koretsky AP,. In vivo detection of single cells by MRI. Magn Reson Med 2006; 55: 242-249.
20. Heyn C, Ronald JA, Mackenzie LT, MacDonald IC, Chambers AF, Rutt BK, Foster PJ,. In vivo magnetic resonance imaging of single cells in mouse brain with optical validation. Magn Reson Med 2006; 55: 23-29.
21. Wu YL, Ye Q, Foley LM, Hitchens TK, Sato K, Williams JB, Ho C,. In situ labeling of immune cells with iron oxide particles: an approach to detect organ rejection by cellular MRI. Proc Natl Acad Sci USA 2006; 103: 1852-1857.
22. Wischke C, Schwendeman SP,. Principles of encapsulating hydrophobic drugs in PLA/PLGA microparticles. Int J Pharm 2008; 364: 298-327.
23. Lo CT, Van Tassel PR, Saltzman WM,. Poly(lactide-co-glycolide) nanoparticle assembly for highly efficient delivery of potent therapeutic agents from medical devices. Biomaterials 2010; 31: 3631-3642.
24. Kumari A, Yadav SK, Yadav SC,. Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surf B Biointerfaces 2010; 75: 1-18.
25. Shive MS, Anderson JM,. Biodegradation and biocompatibility of PLA and PLGA microspheres. Adv Drug Deliv Rev 1997; 28: 5-24.
26. Nkansah MK, Thakral D, Shapiro EM,. Magnetic poly(lactide-co-glycolide) and cellulose particles for MRI-based cell tracking. Magn Reson Med 2011; 65: 1776-1785.
27. Bennewitz MF, Tang KS, Markakis EA, Shapiro EM,. Specific chemotaxis of magnetically labeled mesenchymal stem cells: implications for MRI of glioma. Mol Imaging Biol 2012; 14: 676-687.
28. Weischenfeldt J, Porse B,. Bone marrow-derived macrophages (BMM): isolation and applications. CSH Protoc 2008. doi: 10.1101/pdb.prot5080.
29. Briley-Saebo K, Hustvedt SO, Haldorsen A, Bjornerud A,. Long-term imaging effects in rat liver after a single injection of an iron oxide nanoparticle based MR contrast agent. J Magn Reson Imaging 2004; 20: 622-631.
30. Briley-Saebo K, Bjornerud A, Grant D, Ahlstrom H, Berg T, Kindberg GM,. Hepatic cellular distribution and degradation of iron oxide nanoparticles following single intravenous injection in rats: implications for magnetic resonance imaging. Cell Tissue Res 2004; 316: 315-323.
31. Briley-Saebo KC, Johansson LO, Hustvedt SO, Haldorsen AG, Bjornerud A, Fayad ZA, Ahlstrom HK,. Clearance of iron oxide particles in rat liver: effect of hydrated particle size and coating material on liver metabolism. Invest Radiol 2006; 41: 560-571.
32. Shapiro EM, Gonzalez-Perez O, Garcia-Verdugo JM, Alvarez-Buylla A, Koretsky AP,. Magnetic resonance imaging of the migration of neuronal precursors generated in the adult rodent brain. Neuroimage 2006; 32: 1150-1157.
33. Granot D, Scheinost D, Markakis EA, Papademetris X, Shapiro EM,. Serial monitoring of endogenous neuroblast migration by cellular MRI. Neuroimage 2011; 57: 817-824.
34. Sun S, Zeng H, Robinson DB, Raoux S, Rice PM, Wang SX, Li G,. Monodisperse MFe2O4 (M = Fe, Co, Mn) nanoparticles. J Am Chem Soc 2004; 126: 273-279.
35. Reich G,. Ultrasound-induced degradation of PLA and PLGA during microsphere processing: influence of formulation variables. Eur J Pharm Biopharm 1998; 45: 165-171.
36. Bennewitz MF, Lobo TL, Nkansah MK, Ulas G, Brudvig GW, Shapiro EM,. Biocompatible and pH-sensitive PLGA encapsulated MnO nanocrystals for molecular and cellular MRI. ACS Nano 2011; 5: 3438-3446.
37. Bowen CV, Zhang XW, Saab G, Gareau PJ, Rutt BK,. Application of the static dephasing regime theory to superparamagnetic iron-oxide loaded cells. Magn Reson Med 2002; 48: 52-61.
38. Hirsjarvi S, Peltonen L, Hirvonen J,. Effect of sugars, surfactant, and tangential flow filtration on the freeze-drying of poly(lactic acid) nanoparticles. AAPS PharmSciTech 2009; 10: 488-494.
39. Hirsjarvi S, Peltonen L, Kainu L, Hirvonen J,. Freeze-drying of low molecular weight poly(l-lactic acid) nanoparticles: effect of cryo- and lyoprotectants. J Nanosci Nanotechnol 2006; 6: 3110-3117.
40. Schachner M, Kim SK, Zehnle R,. Developmental expression in central and peripheral nervous system of oligodendrocyte cell surface antigens (O antigens) recognized by monoclonal antibodies. Dev Biol 1981; 83: 328-338.
41. Palfreyman JW, Thomas DG, Ratcliffe JG, Graham DI,. Glial fibrillary acidic protein (GFAP): purification from human fibrillary astrocytoma, development and validation of a radioimmunoassay for GFAP-like immunoactivity. J Neurol Sci 1979; 41: 101-113.
42. Moody SA, Quigg MS, Frankfurter A,. Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-beta-tubulin monoclonal antibody. J Comp Neurol 1989; 279: 567-580.
43. Shapiro EM, Medford-Davis LN, Fahmy TM, Dunbar CE, Koretsky AP,. Antibody-mediated cell labeling of peripheral T cells with micron-sized iron oxide particles (MPIOs) allows single cell detection by MRI. Contrast Media Mol Imaging 2007; 2: 147-153.
44. Dobrovolskaia MA, McNeil SE,. Immunological properties of engineered nanomaterials. Nat Nanotechnol 2007; 2: 469-478.
45. Duyn JH,. Study of brain anatomy with high-field MRI: recent progress. Magn Reson Imaging 2010; 28: 1210-1215.
46. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A,. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999; 97: 703-716.
47. Heyn C, Bowen CV, Rutt BK, Foster PJ,. Detection threshold of single SPIO-labeled cells with FIESTA. Magn Reson Med 2005; 53: 312-320.
48. Nohroudi K, Arnhold S, Berhorn T, Addicks K, Hoehn M, Himmelreich U,. In vivo MRI stem cell tracking requires balancing of detection limit and cell viability. Cell Transplant 2009; 19: 431-441.
49. Crabbe A, Vandeputte C, Dresselaers T, Sacido AA, Verdugo JM, Eyckmans J, Luyten FP, Van LK, Verfaillie, CM, Himmelreich, U,. Effects of MRI Contrast Agents on the Stem cell Phenotype. Cell Transplant 2010; 19: 919-936.
50. Montet-Abou K, Montet X, Weissleder R, Josephson L,. Cell internalization of magnetic nanoparticles using transfection agents. Mol Imaging 2007; 6: 1-9.
51. Walczak P, Ruiz-Cabello J, Kedziorek DA, Gilad AA, Lin S, Barnett B, Qin L, Levitsky H, Bulte JW,. Magnetoelectroporation: improved labeling of neural stem cells and leukocytes for cellular magnetic resonance imaging using a single FDA-approved agent. Nanomedicine 2006; 2: 89-94.
52. Qiu B, Xie D, Walczak P, Li X, Ruiz-Cabello J, Minoshima S, Bulte JW, Yang X,. Magnetosonoporation: instant magnetic labeling of stem cells. Magn Reson Med 2010; 63: 1437-1441.
53. Bulte JW, Kraitchman DL,. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 2004; 17: 484-499.
54. Slotkin JR, Cahill KS, Tharin SA, Shapiro EM,. Cellular magnetic resonance imaging: nanometer and micrometer size particles for noninvasive cell localization. Neurotherapeutics 2007; 4: 428-433.
55. Walczak P, Kedziorek DA, Gilad AA, Barnett BP, Bulte JW,. Applicability and limitations of MR tracking of neural stem cells with asymmetric cell division and rapid turnover: the case of the shiverer dysmyelinated mouse brain. Magn Reson Med 2007; 58: 261-269.
56. Tanimoto A, Oshio K, Suematsu M, Pouliquen D, Stark DD,. Relaxation effects of clustered particles. J Magn Reson Imaging 2001; 14: 72-77