Superparamagnetic iron oxide nanoparticles as MRI contrast agents for non-invasive stem cell labeling and tracking

Theranostics

Volumn 3, Issue 8, 2013, Pages 595-615

  Li, Li ^a   Jiang, Wen ^a   Luo, Kui ^a   Song, Hongmei ^a   Lan, Fang ^a   Wu, Yao ^a   Gu, Zhongwei ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

Labeling; Magnetic resonance imaging; Stem cells; Superparamagnetic iron oxide nanoparticles; Tracking

Indexed keywords

AMI-227; CHITOSAN; FERUCARBOTRAN; FERUMOXSIL; FERUMOXYTOL; GADODIAMIDE; GADOLINIUM PENTETATE; GADOLINIUM PENTETATE MEGLUMINE; GADOXETIC ACID; HEPARIN; MACROGOL; MAGNETIC NANOPARTICLE; POLY(METHYL METHACRYLATE); POLYETHYLENEIMINE; POLYSACCHARIDE; PULLULAN; SILICON DIOXIDE; SUPERPARAMAGNETIC IRON OXIDE; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE; UNCLASSIFIED DRUG;

APOPTOSIS; BIOCOMPATIBILITY; CELL ADHESION; CELL DIFFERENTIATION; CELL LABELING; CELL PROLIFERATION; CELL SIZE; CELL TRACKING; CONTROLLED STUDY; ENDOCYTOSIS; HIGH TEMPERATURE; HUMAN; HYDROPHOBICITY; IMAGE ANALYSIS; INTERNALIZATION; MATERIAL COATING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARTICLE SIZE; PHAGOCYTOSIS; REVIEW; STEM CELL; SURFACE PROPERTY; SYNTHESIS; ZETA POTENTIAL;

LABELING; MAGNETIC RESONANCE IMAGING.; STEM CELLS; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLES; TRACKING;

ANIMALS; CELL TRACKING; CONTRAST MEDIA; FERRIC COMPOUNDS; HUMANS; MAGNETIC RESONANCE IMAGING; MICE; NANOPARTICLES; STEM CELL TRANSPLANTATION; SWINE;

EID: 84883158369     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.5366     Document Type: Review

References (141)

1. Ramos-Cabrer P and Hoehn M. MRI stem cell tracking for therapy in experimental cerebral ischemia. Transl Stroke Res. 2012; 3: 22-35.
2. Agudelo CA, Tachibana Y, Noboru T, Iida H, and Yamaoka T. Long-term in vivo magnetic resonance imaging tracking of endothelial progenitor cells transplanted in rat ischemic limbs and their angiogenic potential. Tissue Eng Part A. 2011; 17: 2079-89.
3. Green MD and Snoeck HW. Novel approaches for immune reconstitution and adaptive immune modeling with human pluripotent stem cells. BMC Med. 2011; 9: 51.
4. Sandhaus RA. Gene therapy meets stem cells. N Engl J Med. 2012; 366: 567-9.
5. Zhang XL, Wang G, Dong FR and Wang ZM. Application of magnetic resonance imaging for monitoring stem cell transplantation for the treatment of cerebral ischemia. Neural Regen. Res. 2012;7: 1264-71.
6. Gupta PK, Das AK, Chullikana A and Majumdar AS. Mesenchymal stem cells for cartilage repair in osteoarthritis. Stem Cell Res Ther. 2012; 3: 25.
7. Longo UG, Petrillo S, Franceschetti E, Berton A, Maffulli N and Denaro V. Stem cells and gene therapy for cartilage repair. Stem Cells Int. 2012;:168385.
8. Zhao Y, Zhang Z, Wang J, Yin P, Zhou J, Zhen M, Cui W, Xu G, Yang D and Liu Z. Abdominal hernia repair with a decellularized dermal scaffold seeded with autologous bone marrow-derived mesenchymal stem cells. Artif Organs. 2012; 36: 247-55.
9. Ma B, Hankenson KD, Dennis JE, Caplan AI, Goldstein SA and Kilbourn MR. A simple method for stem cell labeling with fluorine 18. Nucl Med Biol. 2005; 32: 701-5.
10. Elhami E, Goertzen A, Xiang B, Deng J, Stillwell C, Mzengeza S, Arora R, Freed D and Tian G. Viability and proliferation potential of adipose-derived stem cells following labeling with a positron-emitting radiotracer. Eur J Nucl Med Mol Imaging. 2011; 38: 1323-34.
11. Patel D, Kell A, Simard B, Xiang B, Lin HY and Tian G. The cell labeling efficacy, cytotoxicity and relaxivity of copper-activated MRI/PET imaging contrast agents. Biomaterials. 2011; 32: 1167-76.
12. Bindslev L, Haack-Sorensen M, Bisgaard K, Kragh L, Mortensen S, Hesse B, Kjaer A and Kastrup J. Labelling of human mesenchymal stem cells with indium-111 for SPECT imaging: effect on cell proliferation and differentiation. Eur J Nucl Med Mol Imaging. 2006; 33: 1171-7.
13. Sheyn D, Kallai I, Tawackoli W, Cohn Yakubovich D, Oh A, Su S, Da X, Lavi A, Kimelman-Bleich N, Zilberman Y, Li N, Bae H, Gazit Z, Pelled G and Gazit D. Gene-modified adult stem cells regenerate vertebral bone defect in a rat model. Mol Pharm. 2011; 8: 1592-601.
14. Wolbank S, Peterbauer A, Wassermann E, Hennerbichler S, Voglauer R, van Griensven M, Duba HC, Gabriel C and Redl H. Labelling of human adipose-derived stem cells for non-invasive in vivo cell tracking. Cell and Tissue Banking. 2007; 8: 163-77.
15. Baba K and Nishida K. Single-molecule tracking in living cells using single quantum dot applications. Theranostics. 2012; 2: 655-67.
16. Higuchi Y, Wu C, Chang KL, Irie K, Kawakami S, Yamashita F and Hashida M. Polyamidoamine dendrimer-conjugated quantum dots for efficient labeling of primary cultured mesenchymal stem cells. Biomaterials. 2011; 32: 6676-6682.
17. Zhang Y. Quantum dot enabled molecular sensing and diagnostics. Theranostics. 2012; 2: 631-54.
18. Hsieh SC, Wang FF, Lin CS, Chen YJ, Hung SC and Wang YJ. The inhibition of osteogenesis with human bone marrow mesenchymal stem cells by CdSe/ZnS quantum dot labels. Biomaterials. 2006; 27: 1656-64.
19. Liu G, Ye X, Zhu Y, Li Y, Sun J, Cui L and Cao Y. Osteogenic differentiation of GFP-labeled human umbilical cord blood derived mesenchymal stem cells after cryopreservation. Cryobiology. 2011; 63: 125-8.
20. Wang L, Neoh KG, Kang ET, Shuter B and Wang SC. Biodegradable magnetic-fluorescent magnetite/poly(DL-lactic acid-co-alpha,beta-malic acid) composite nanoparticles for stem cell labeling. Biomaterials. 2010; 31: 3502-11.
21. Boddington SE, Henning TD, Jha P, Schlieve CR, Mandrussow L, DeNardo D, Bernstein HS, Ritner C, Golovko D, Lu Y, Zhao S and Daldrup-Link HE. Labeling human embryonic stem cell-Derived cardiomyocytes with indocyanine green for noninvasive tracking with optical imaging: an FDA-compatible alternative to firefly luciferase. Cell Transpl. 2010; 19: 55-65.
22. Gildehaus FJ, Haasters F, Drosse I, Wagner E, Zach C, Mutschler W, Cumming P, Bartenstein P and Schieker M. Impact of indium-111 oxine labelling on viability of human mesenchymal stem cells in vitro and 3D cell-tracking using SPECT/CT in vivo. Mol Imaging Biol. 2011; 13: 1204-1214.
23. Rumenapp C, Gleich B and Haase A. Magnetic nanoparticles in magnetic resonance imaging and diagnostics. Pharm Res. 2012; 29: 1165-79.
24. Bulte JWM. In vivo MRI cell tracking: clinical studies. Am J Roentgenol. 2009; 193: 314-25.
25. Hu SL, Lu PG, Zhang LJ, Li F, Chen Z, Wu N, Meng H, Lin JK and Feng H. In vivo magnetic resonance imaging tracking of SPIO-labeled human umbilical cord mesenchymal stem cells. J Cell Biochem. 2012; 113: 1005-1012.
26. Bhirde A, Xie J, Swierczewska M and Chen X. Nanoparticles for cell labeling. Nanoscale. 2011; 3: 142-53.
27. Liu G, Swierczewska M, Niu G, Zhang X and Chen X. Molecular imaging of cell-based cancer immunotherapy. Mol Biosyst. 2011; 7: 993-1003.
28. Akbarzadeh A, Samiei M and Davaran S. Magnetic nanoparticles: preparation, physical properties and applications in biomedicine. Nanoscale Res Lett. 2012; 7: 1-13.
29. Berman SMC, Walczak P and Bulte JWM. Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2011; 3: 343-55.
30. Xie J, Liu G, Eden HS, Ai H and Chen XY. Surface-engineered magnetic nanoparticle platforms for cancer imaging and therapy. Acc Chem Res. 2011; 44: 883-892.
31. Luo K, Tian J, Liu G, Sun J, Xia C, Tang H, Lin L, Miao T, Zhao X, Gao F, Gong Q, Song B, Shuai X, Ai H and Gu Z. Self-assembly of SiO2/Gd-DTPA-polyethylenimine nanocomposites as magnetic resonance imaging probes. J Nanosci Nanotechnol. 2010; 10: 540-8.
32. Guenoun J, Koning GA, Doeswijk G, Bosman L, Wielopolski PA, Krestin GP and Bernsen MR. Cationic Gd-DTPA liposomes for highly efficient labeling of mesenchymal stem cells and cell tracking with MRI. Cell Transplant. 2012; 21: 191-205.
33. Liu Y, He ZJ, Xu B, Wu QZ, Liu G, Zhu H, Zhong Q, Deng DY, Ai H, Yue Q, Wei Y, Jun S, Zhou G and Gong QY. Evaluation of cell tracking effects for transplanted mesenchymal stem cells with jetPEI/Gd-DTPA complexes in animal models of hemorrhagic spinal cord injury. Brain Res. 2011; 1391: 24-35.
34. G. Liu, H. Yang, X.M. Zhang, Y. Shao and H. Jiang, MR imaging for the longevity of mesenchymal stem cells labeled with poly-L-lysine-Resovist complexes. Contrast Media Mol Imaging. 2010.5: 53-58.
35. Tseng CL, Shih IL, Stobinski L and Lin FH. Gadolinium hexanedione nanoparticles for stem cell labeling and tracking via magnetic resonance imaging. Biomaterials. 2010; 31: 5427-5435.
36. Tran LA, Krishnamurthy R, Muthupillai R, da Graça Cabreira-Hansen M, Willerson JT, Perin EC and Wilson LJ. Gadonanotubes as magnetic nanolabels for stem cell detection. Biomaterials. 2010; 31: 9482-91.
37. Lee HY, Lim NH, Seo JA, Yuk SH, Kwak BK, Khang G, Lee HB and Cho SH. Preparation and magnetic resonance imaging effect of polyvinylpyrrolidone-coated iron oxide nanoparticles. J Biomed Mater Res B Appl Biomater. 2006; 79: 142-150.
38. Luo K, Liu G, He B, Wu Y, Gong Q, Song B, Ai H and Gu Z. Multifunctional gadolinium-based dendritic macromolecules as liver targeting imaging probes. Biomaterials. 2011; 32: 2575-85.
39. Zhang B, Jiang B, Chen Y, Huang H, Xie Q, Kang M, Zhang H, Zhai C and Wu Y. Detection of viability of transplanted beta cells labeled with a novel contrast agent - polyvinylpyrrolidone-coated superparamagnetic iron oxide nanoparticles by magnetic resonance imaging. Contrast Media Mol Imaging. 2012; 7: 35-44.
40. Yang CY, Tai MF, Chen ST, Wang YT, Chen YF, Hsiao JK, Wang JL and Liu HM. Labeling of human mesenchymal stem cell: Comparison between paramagnetic and superparamagnetic agents. J Appl Phy. 2009;: 105.
41. Ke YQ, Hu CC, Jiang XD, Yang ZJ, Zhang HW, Ji HM, Zhou LY, Cai YQ, Qin LS and Xu RX. In vivo magnetic resonance tracking of Feridex-labeled bone marrow-derived neural stem cells after autologous transplantation in rhesus monkey. J Neurosci Meth. 2009; 179: 45-50.
42. Zhu WZ, Li X, Qi JP, Tang ZP, Wang W, Wei L and Lei H. Experimental Study of Cell Migration and functional differentiation of transplanted neural stem cells co-labeled with superparamagnetic iron oxide and Brdu in an ischemic rat model. Biomed Environ Sci. 2008; 21: 420-4.
43. Suzuki Y, Zhang S, Kundu P, Yeung AC, Robbins RC and Yang PC. In vitro comparison of the biological effects of three transfection methods for magnetically labeling mouse embryonic stem cells with ferumoxides. Magnetic Reson Med. 2007; 57: 1173-9.
44. Park BH, Jung JC, Lee GH, Kim TJ, Lee YJ, Kim JY, Kim YW, Jeong JH and Chang Y. Comparison of labeling efficiency of different magnetic nanoparticles into stem cell. Colloids Surf, A Physicochem Eng Asp. 2008; 313: 145-149.
45. Yang L, Xia Y, Zhao H, Zhao J and Zhu X. Magnetic resonance imaging of transplanted neural stem cells in parkinson disease rats. J Huazhong Univ Sci Techn -- Med Sci --. 2006; 26: 489-92.
46. Arbab AS, Yocum GT, Rad AM, Khakoo AY, Fellowes V, Read EJ and Frank JA. Labeling of cells with ferumoxides-protamine sulfate complexes does not inhibit function or differentiation capacity of hematopoietic or mesenchymal stem cells. NMR in Biomedicine. 2005; 18: 553-9.
47. Arbab AS, Yocum GT, Wilson LB, Parwana A, Jordan EK, Kalish H and Frank JA. Comparison of transfection agents in forming complexes with ferumoxides, cell labeling efficiency and cellular viability. Mol Imaging. 2004; 3: 24-32.
48. Thu MS, Bryant LH, Coppola T, Jordan EK, Budde MD, Lewis BK, Chaudhry A, Ren J, Varma NRS, Arbab AS and Frank JA. Self-assembling nanocomplexes by combining ferumoxytol, heparin and protamine for cell tracking by magnetic resonance imaging. Nature Med. 2012; 18: 463-U165.
49. Arnold LJ, Dagan A, Gutheil J and Kaplan NO. Antineoplastic activity of poly(L-lysine) with some ascites tumor cells. Proc Natl Acad Sci U S A. 1979; 76: 3246-50.
50. Bulte JWM, Kraitchman DL, Mackay AM and Pittenger MF. Chondrogenic differentiation of mesenchymal stem cells is inhibited after magnetic labeling with ferumoxides. Blood. 2004; 104: 3410-3412.
51. Liu YJ and Zhang N. Gadolinium loaded nanoparticles in theranostic magnetic resonance imaging. Biomaterials. 2012; 33: 5363-75.
52. Laurent S, Forge D, Port M, Roch A, Robic C, Vander Elst L and Muller RN. Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations and biological applications. Chem Rev. 2008; 108: 2064-110.
53. Song M, Moon WK, Kim Y, Lim D, Song IC and Yoon BW. Labeling efficacy of superparamagnetic iron oxide nanoparticles to human neural stem cells: Comparison of ferumoxides, monocrystalline iron oxide, cross-linked iron oxide (CLIO)-NH2 and tat-CLIO. Korean J Rad. 2007; 8: 365-71.
54. Pawelczyk E, Arbab AS, Chaudhry A, Balakumaran A, Robey PG and Frank JA. In vitro model of bromodeoxyuridine or iron oxide nanoparticle uptake by activated macrophages from labeled stem cells: implications for cellular therapy. Stem Cells. 2008; 26: 1366-75.
55. Terrovitis J, Stuber M, Youssef A, Preece S, Leppo M, Kizana E, Schaer M, Gerstenblith G, Weiss RG, Marban E and Abraham MR. Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation. 2008; 117: 1555-62.
56. Berry I, Benderbous S, Ranjeva JP, Gracia-Meavilla D and Claude Manelfe DLB. Contribution of sinerem@ used as blood-Pool contrast agent: detection of cerebral blood volume hanges during apnea in the rabbit. Magn Reson Med. 1996; 36: 415-9.
57. Li W, Tutton S, Vu AT, Pierchala L, Li BS, Lewis JM, Prasad PV and Edelman RR. First-pass contrast-enhanced magnetic resonance angiography in humans using ferumoxytol, a novel ultrasmall superparamagnetic iron oxide (USPIO)-based blood pool agent. J Magn Reson Imaging. 2005; 21: 46-52.
58. Jung CW. Surface properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magn Reson Imaging. 1995; 13: 675-91.
59. Reimer P, Marx C, Rummeny EJ, Muller M, Lentschig M, Balzer T, Dietl KH, Sulkowski U, Berns T, Shamsi K and Peters PE. SPIO-enhanced 2D-TOF MR angiography of the portal venous system: results of an intraindividual comparison. J Magn Reson Imaging. 1997; 7: 945-49.
60. Kellar KE, Fujii DK, Gunther WH, Briley-Saebo K, Bjornerud A, Spiller M and Koenig SH. NC100150 Injection, a preparation of optimized iron oxide nanoparticles for positive-contrast MR angiography. J Magn Reson Imaging. 2000; 11: 488-94.
61. Shapiro EM, Skrtic S, Sharer K, Hill JM, Dunbar CE and Koretsky AP. MRI detection of single particles for cellular imaging. Proc Natl Acad Sci U S A. 2004; 101: 10901-6.
62. Ju S, Teng G, Zhang Y, Ma M, Chen F and Ni Y. In vitro labeling and MRI of mesenchymal stem cells from human umbilical cord blood. Magnetic Resonance Imaging. 2006; 24: 611-7.
63. Babic M, Horák D, Trchová M, et al. Poly(l-lysine)-modified iron oxide nanoparticles for stem cell labeling. Bioconj Chem. 2008; 19: 740-50.
64. Horak D, Babic M, Jendelova P, Herynek V, Trchova M, Likavcanova K, Kapcalova M, Hajek M and Sykova E. Effect of different magnetic nanoparticle coatings on the efficiency of stem cell labeling. J Magn Magn Mater. 2009; 321: 1539-47.
65. Liu G, Wang Z, Lu J, Xia C, Gao F, Gong Q, Song B, Zhao X, Shuai X, Chen X, Ai H and Gu Z. Low molecular weight alkyl-polycation wrapped magnetite nanoparticle clusters as MRI probes for stem cell labeling and in vivo imaging. Biomaterials. 2011; 32: 528-537.
66. Guo R, Cao N, Zhang F, Wang Y, Wen X, Shen J and Shuai X. Controllable labelling of stem cells with a novel superparamagnetic iron oxide-loaded cationic nanovesicle for MR imaging. Eur Radiol. 2012;22: 2328-37.
67. Shi Z, Neoh KG, Kang ET, Shuter B, Wang SC, Poh C and Wang W. (Carboxymethyl)chitosan-modified superparamagnetic iron oxide nanoparticles for magnetic resonance imaging of stem cells. ACS Applied Materials & Interfaces. 2008; 1: 328-35.
68. Jo JI, Aoki I and Tabata Y. Design of iron oxide nanoparticles with different sizes and surface charges for simple and efficient labeling of mesenchymal stem cells. Journal of Controlled Release. 2010; 142: 465-73.
69. Lee JH, Jung MJ, Hwang YH, Lee YJ, Lee S, Lee DY and Shin H. Heparin-coated superparamagnetic iron oxide for in vivo MR imaging of human MSCs. Biomaterials. 2012; 33: 4861-71.
70. Chung HJ, Lee H, Bae KH, Lee Y, Park J, Cho SW, Hwang JY, Park H, Langer R Anderson D and Park TG. Facile Synthetic route for surface-functionalized magnetic nanoparticles: cell labeling and magnetic resonance imaging studies. ACS Nano. 2011; 5: 4329-36.
71. Kim H, Dae HM, Park C, Kim EO, Kim D, Kim IH, Kim YH and Choi Y. A highly sensitive magnetite nanoparticle as a simple and rapid stem cell labelling agent for MRI tracking. J Mater Chem. 2011; 21: 7742-7.
72. Babic M, Horak D, Jendelova P, Glogarova KI, Herynek VT, Trchova M, Likavcanova KN, Lesny P, Pollert E, Hajek M and Sykova E. Poly(N,N-dimethylacrylamide)-coated maghemite nanoparticles for stem cell labeling. Bioconj Chem. 2009; 20: 283-94.
73. Xu C, Miranda-Nieves D, Ankrum JA, Matthiesen ME, Phillips JA, Roes I, Wojtkiewicz GR, Juneja V, Kultima JR, Zhao W, Vemula PK, Lin CP, Nahrendorf M and Karp JM. Tracking mesenchymal stem cells with iron oxide nanoparticle loaded poly(lactide-co-glycolide) microparticles. Nano Lett. 2012; 12: 4131-9.
74. Andreas K, Georgieva R, Ladwig M, Mueller S, Notter M, Sittinger M and Ringe J. Highly efficient magnetic stem cell labeling with citrate-coated superparamagnetic iron oxide nanoparticles for MRI tracking. Biomaterials. 2012; 33: 4515-25.
75. Horak D, Babic M, Jendelova P, Herynek V, Trchova M, Pientka Z, Pollert E, Hajek M and Sykova E. D-Mannose-modified iron oxide nanoparticles for stem cell labeling. Bioconjugate Chemistry. 2007; 18: 635-44.
76. Wang HH, Wang YXJ, Leung KCF, Au DWT, Xuan S, Chak CP, Lee SKM, Sheng H, Zhang G, Qin L, Griffith JF and Ahuja AT. Durable mesenchymal stem cell labelling by using polyhedral superparamagnetic iron oxide nanoparticles. Chem - A Eur J. 2009; 15: 12417-25.
77. Yoon TJ, Kim JS, Kim BG, Yu KN, Cho MH and Lee JK. Multifunctional nanoparticles possessing a "magnetic motor effect" for drug or gene delivery. Angew Chem Int Ed. 2005; 44: 1068-71.
78. Lu CW, Hung Y, Hsiao JK, Yao M, Chung TH, Lin YS, Wu SH, Hsu SC, Liu HM, Mou CY, Yang CS, Huang DM and Chen YC. Bifunctional magnetic silica nanoparticles for highly efficient human stem cell labeling. Nano Lett. 2007; 7: 149-54.
79. Kim TH, Kim JK, Shim W, Kim SY, Park TJ and Jung JY. Tracking of transplanted mesenchymal stem cells labeled with fluorescent magnetic nanoparticle in liver cirrhosis rat model with 3-T MRI. Magnc Reson Imaging. 2010; 28: 1004-13.
80. Huang DM, Hung Y, Ko BS, Hsu SC, Chen WH, Chien CL, Tsai CP, Kuo CT, Kang JC, Yang CS, Mou CY and Chen YC. Highly efficient cellular labeling of mesoporous nanoparticles in human mesenchymal stem cells: implication for stem cell tracking. FASEB J. 2005; 19: 2014-6.
81. Wunderbaldinger P, Josephson L and Weissleder R. Tat peptide directs enhanced clearance and hepatic permeability of magnetic nanoparticles. Bioconj Chem. 2002; 13: 264-8
82. Suh JS, Lee JY, Choi YS, Yu F, Yang V, Lee SJ, Chung CP and Park YJ. Efficient labeling of mesenchymal stem cells using cell permeable magnetic nanoparticles. Biochem Biophy Res Co. 2009; 379: 669-75.
83. Doherty GJ and McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem. 2009; 78: 857-902.
84. Bae H, Ahmad T, Rhee I, Chang Y, Jin SU and Hong S. Carbon-coated iron oxide nanoparticles as contrast agents in magnetic resonance imaging. Nanoscale Res Lett. 2012; 7: 44.
85. Conner SD and Schmid SL. Regulated portals of entry into the cell. Nature. 2003; 422: 37-44.
86. Thorek DL and Tsourkas A. Size, charge and concentration dependent uptake of iron oxide particles by non-phagocytic cells. Biomaterials. 2008; 29: 3583-90.
87. Rejman J, Oberle V, Zuhorn IS and Hoekstra D. Size-dependent internalization of particles via the pathways of clathrinand caveolae-mediated endocytosis. Biochem J. 2004; 377: 159-69.
88. Hu JG, Fu SL, Wang YX, Li Y, Jiang XY, Wang XF, Qiu MS, Lu PH and Xu XM. Platelet-derived growth factor-AA mediates oligodendrocyte lineage differentiation through activation of extracellular signal-regulated kinase signaling pathway. Neuroscience. 2008; 151: 138-47.
89. Li L, Nie Y, Zhu R, Shi S, Luo K, He B, Yang Y, Yang J and Gu Z. Preparation and gene delivery of alkaline amino acids-based cationic liposomes. Arch Pharm Res. 2008; 31: 924-31.
90. Li L, Song H, Luo K, He B, Nie Y, Yang Y, Wu Y and Gu Z. Gene transfer efficacies of serum-resistant amino acids-based cationic lipids: Dependence on headgroup, lipoplex stability and cellular uptake. Int J Pharm. 2011; 408: 183-90.
91. Luo K, Li C, Wang G, Nie Y, He B, Wu Y and Gu Z. Peptide dendrimers as efficient and biocompatible gene delivery vectors: Synthesis and in vitro characterization. J Contr Rel. 2011; 155: 77-87.
92. Luo K, Li C, Li L, She W, Wang G and Gu Z. Arginine functionalized peptide dendrimers as potential gene delivery vehicles. Biomaterials. 2012; 33: 4917-27.
93. Yu C, Zhao J, Guo Y, Lu C, Ma X and Gu Z. A novel method to prepare water-dispersible magnetic nanoparticles and their biomedical applications: Magnetic capture probe and specific cellular uptake. J Biomed Mater Res A. 2008; 87A: 364-72.
94. Dousset V, Tourdias T, Brochet B, Boiziau C and Petry KG. How to trace stem cells for MRI evaluation? J Neurol Sci. 2008; 265: 122-6.
95. Bulte JW, Douglas T, Witwer B, Zhang SC, Strable E, Lewis BK, Zywicke H, Miller B, van Gelderen P, Moskowitz BM, Duncan ID and Frank JA. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol. 2001; 19: 1141-7.
96. Ai H. Layer-by-layer capsules for magnetic resonance imaging and drug delivery. Adv Drug Deliver Rev. Reviews. 2011; 63: 772-88.
97. Xu C, Mu L, Roes I, Miranda-Nieves D, Nahrendorf M, Ankrum JA, Zhao W and Karp JM. Nanoparticle-based monitoring of cell therapy. Nanotechnology. 2011; 22: 494001.
98. Perez JM, Josephson L, O'Loughlin T, Hogemann D and Weissleder R. Magnetic relaxation switches capable of sensing molecular interactions. Nat Biotechnol. 2002; 20: 816-20.
99. Lan F, Liu KX, Jiang W, Zeng XB, Wu Y and Gu ZW. Facile synthesis of monodisperse superparamagnetic Fe3O4/PMMA composite nanospheres with high magnetization. Nanotechnology. 2011; 22: 225604.
100. Lan F, Hu H, Jiang W, Liu K, Zeng X, Wu Y and Gu Z. Synthesis of superparamagnetic Fe3O4/PMMA/SiO2 nanorattles with periodic mesoporous shell for lysozyme adsorption. Nanoscale. 2012; 4: 2264.
101. Bowen CV, Zhang X, Saab G, Gareau PJ and Rutt BK. Application of the static dephasing regime theory to superparamagnetic iron-oxide loaded cells. Magn Reson Med. 2002; 48: 52-61.
102. Lee JH, Huh YM, Jun YW, Seo JW, Jang JT, Song HT, Kim S, Cho EJ, Yoon HG, Suh JS and Cheon J. Artificially engineered magnetic nanoparticles for ultra-sensitive molecular imaging. Nat Med. 2007; 13: 95-9.
103. Basti H, Ben Tahar L, Smiri LS, Herbst F, Vaulay MJ, Chau F, Ammar S and Benderbous S. Catechol derivatives-coated Fe3O4 and gamma-Fe2O3 nanoparticles as potential MRI contrast agents. J Colloid Interface Sci. 2010; 341: 248-54.
104. Cromer Berman SM, Kshitiz, Wang CJ, Orukari I, Levchenko A, Bulte JW and Walczak P. Cell motility of neural stem cells is reduced after SPIO-labeling, which is mitigated after exocytosis. Magn Reson Med. 2013; 69: 255-62.
105. Lewinski N, Colvin V and Drezek R. Cytotoxicity of nanoparticles. Small. 2008; 4: 26-49.
106. Bulte JW and Kraitchman DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 2004; 17: 484-99.
107. Chen YC, Hsiao JK, Liu HM, Lai IY, Yao M, Hsu SC, Ko BS, Chen YC, Yang CS and Huang DM. The inhibitory effect of superparamagnetic iron oxide nanoparticle (Ferucarbotran) on osteogenic differentiation and its signaling mechanism in human mesenchymal stem cells. Toxicol Appl Pharmacol. 2010; 245: 272-9.
108. Kedziorek DA, Muja N, Walczak P, Ruiz-Cabello J, Gilad AA, Jie CC and Bulte JW. Gene expression profiling reveals early cellular responses to intracellular magnetic labeling with superparamagnetic iron oxide nanoparticles. Magn Reson Med. 2010; 63: 1031-1043.
109. Lu AH, Salabas EL and Schüth F. Magnetic nanoparticles: synthesis, protection, functionalization and application. Angew Chem Int Ed. 2007; 46: 1222-44.
110. Jiang W, Wu Y, He B, Zeng X, Lai K and Gu Z. Effect of sodium oleate as a buffer on the synthesis of superparamagnetic magnetite colloids. J Colloid Interf Sci. 2010; 347: 1-7.
111. Jiang W, Lai KL, Hu H, Zeng XB, Lan F, Liu KX, Wu Y and Gu ZW. The effect of [Fe3+]/[Fe2+] molar ratio and iron salts concentration on the properties of superparamagnetic iron oxide nanoparticles in the water/ethanol/toluene system. J Nanopart Res. 2011; 13: 5135-45.
112. Neoh KG and Kang ET. Surface modification of magnetic nanoparticles for stem cell labeling. Soft Matter. 2012; 8: 2057-69.
113. Zhu R, Jiang W, Pu Y, Luo K, Wu Y, He B and Gu Z. Functionalization of magnetic nanoparticles with peptide dendrimers. J Mater Chem. 2011; 21: 5464-74.
114. Hyeon T, Lee SS, Park J, Chung Y and Na HB. Synthesis of highly crystalline and monodisperse maghemite nanocrystallites without a size-selection process. J Am Chem Soc. 2001; 123: 12798-801.
115. Ge S, Shi X, Sun K, Li C, Baker JR, Banaszak Holl MM andOrr BG. A facile hydrothermal synthesis of iron oxide nanoparticles with tunable magnetic properties. J Phys Chem C Nanomater Interfaces. 2009; 13: 13593-9.
116. Dai Z, Meiser F and Mohwald H. Nanoengineering of iron oxide and iron oxide/silica hollow spheres by sequential layering combined with a sol-gel process. J Colloid Interface Sci. 2005; 288: 298-300.
117. Stephen ZR, Kievit FM and Zhang M. Magnetite nanoparticles for medical MR imaging. Mater Today (Kidlington). 2011; 14: 330-8.
118. Sun S, Zeng H, Robinson DB, Raoux S, Rice PM, Wang SX and Li G. Monodisperse MFe2O4 (M = Fe, Co, Mn) nanoparticles. J Am Chem Soc. 2004; 126: 273-9.
119. Liu K, Lan F, Jiang W, Zeng X, Hu H, Wu Y and Gu Z. Controllable preparation of ternary superparamagnetic nanoparticles dual-Doped with Mn and Zn elements. J Nanosci Nanotechno. 2012; 12: 8437-42
120. Wen X, Yang J, He B and Gu Z. Preparation of monodisperse magnetite nanoparticles under mild conditions. Curr Appl Phys. 2008; 8: 535-41.
121. Wen X and Zhongwei G. Preparation of monodispersed superpara-magnetic magnetite nanoparticles. China: C.p bureau. 2007.
122. Yocum GT, Wilson LB, Ashari P, Jordan EK, Frank JA and Arbab AS. Effect of human stem cells labeled with ferumoxides-poly-L-lysine on hematologic and biochemical measurements in rats. Radiology. 2005; 235: 547-52.
123. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B and Behr JP. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci U S A. 1995; 92: 7297-301.
124. Liu G, Xie J, Zhang F, Wang Z, Luo K, Zhu L, Quan Q, Niu G, Lee S, Ai H and Chen X. N-Alkyl-PEI-Functionalized iron oxide nanoclusters for efficient siRNA delivery. Small. 2011; 7: 2742-9.
125. Mizrahy S and Peer D. Polysaccharides as building blocks for nanotherapeutics. Chem Soc Rev. 2012; 41: 2623-40.
126. Tao T, Peng XF and Lee DJ. Fragmentation of wastewater sludge floc by planar ice front. J Colloid Interface Sci. 2005; 290: 298-301.
127. Reddy AM, Kwak BK, Shim HJ, Ahn C, Lee HS, Suh YJ and Park ES. In vivo In vivo Tracking of mesenchymal stem cells labeled with a novel chitosan-coated superparamagnetic iron oxide nanoparticles using 3.0T MRI. J Korean Med Sci. 2010; 25: 211-9.
128. Cheng LN, Duan XH, Zhong XM, Guo RM, Zhang F, Zhou CP and Shen J. Transplanted neural stem cells promote nerve regeneration in acute peripheral nerve traction injury: assessment using MRI. AJR Am J Roentgenol. 2011; 196: 1381-7.
129. Bhaskar U, Sterner E, Hickey AM, Onishi A, Zhang F, Dordick JS and Linhardt RJ. Engineering of routes to heparin and related polysaccharides. Appl Microbiol Biotechnol. 2012; 93: 1-16.
130. Wang YXJ, Quercy-Jouvet T, Wang HH, Li AW, Chak CP, Xuan S, Shi L, Wang DF, Lee SF, Leung PC, Lau CBS, Fung KP and Leung KCF. Efficacy and durability in direct labeling of mesenchymal stem cells using ultrasmall superparamagnetic iron oxide nanoparticles with organosilica, dextran and PEG coatings. Materials. 2011; 4: 703-15.
131. Liao MH and Chen DH. Preparation and characterization of a novel magnetic nano-adsorbent. J Mater Chem. 2002; 12: 3654-9.
132. Nkansah MK, Thakral D and Shapiro EM. Magnetic poly(lactide-co-glycolide) and cellulose particles for MRI-based cell tracking. Magn Reson Med. 2011; 65: 1776-85.
133. Wilhelm C and Gazeau F. Universal cell labelling with anionic magnetic nanoparticles. Biomaterials. 2008; 29: 3161-74.
134. Zhang J, Zhu J, Bu X, Cushion M, Kinane TB, Avraham H and Koziel H. Cdc42 and RhoB activation are required for mannose receptor-mediated phagocytosis by human alveolar macrophages. Mol Biol Cell. 2005; 16: 824-34.
135. Zhang C, Wangler B, Morgenstern B, Zentgraf H, Eisenhut M, Untenecker H, Kruger R, Huss R, Seliger C, Semmler W and Kiessling F. Silica- and alkoxysilane-coated ultrasmall superparamagnetic iron oxide particles: a promising tool to label cells for magnetic resonance imaging. Langmuir. 2007; 23: 1427-34.
136. Park KS, Tae J, Choi B, Kim YS, Moon C, Kim SH, Lee HS, Kim J, Kim J, Park J, Lee JH, Lee JE, Joh JW and Kim S. Characterization, in vitro cytotoxicity assessment and in vivo visualization of multimodal, RITC-labeled, silica-coated magnetic nanoparticles for labeling human cord blood-derived mesenchymal stem cells. Nanomed-Nanotechno Biol and Med. 2010; 6: 263-76.
137. Liu HM, Wu SH, Lu CW, Yao M, Hsiao JK, Hung Y, Lin YS, Mou CY, Yang CS, Huang DM and Chen YC. Mesoporous silica nanoparticles improve magnetic labeling efficiency in human stem cells. Small. 2008; 4: 619-26.
138. Bernard AL, Guedeau-Boudeville MA, Marchi-Artzner V, Gulik-Krzywicki T, di Meglio JM and Jullien L. Shear-induced permeation and fusion of lipid vesicles. J Colloid Interface Sci. 2005; 287: 298-306.
139. Gilad AA, McMahon MT, Walczak P, Jr Winnard PT, Raman V, van Laarhoven HW, Skoglund CM, Bulte JW andvan Zijl PC. Artificial reporter gene providing MRI contrast based on proton exchange. Nat Biotechnol. 2007; 25: 217-9.
140. Ly HQ, Frangioni JV and Hajjar RJ. Imaging in cardiac cell-based therapy: in vivo tracking of the biological fate of therapeutic cells. Nat Clin Pract Cardiovasc Med. 2008; 5 Suppl 2: S96-102.
141. Budde MD and Frank JA. Magnetic tagging of therapeutic cells for MRI. J Nucl Med. 2009; 50: 171-4