Efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: Relevance for in vivo cell tracking

Stem Cells

Volumn 26, Issue 2, 2008, Pages 505-516

  Neri, Margherita ^a   Maderna, Claudio ^a   Cavazzin, Chiara ^a   Deidda Vigoriti, Vivien ^a   Politi, Letterio S ^a   Scotti, Giuseppe ^a   Marzola, Pasquina ^b   Sbarbati, Andrea ^b   Vescovi, Angelo L ^a,c   Gritti, Angela ^a,d  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

^d SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

Author keywords

Cell tracking; Human neural precursor cells; Magnetic resonance imaging; Superparamagnetic iron oxide; Transplantation

Indexed keywords

SUPERPARAMAGNETIC IRON OXIDE; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE;

ANALYTIC METHOD; ARTICLE; CELL LABELING; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HISTOLOGY; HUMAN; HUMAN CELL; LONGITUDINAL STUDY; NERVE CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; STEM CELL TRANSPLANTATION; TITRIMETRY; VALIDATION PROCESS;

ANIMALS; BRAIN TISSUE TRANSPLANTATION; CONTRAST MEDIA; HUMANS; IRON; MAGNETIC RESONANCE IMAGING; MAGNETICS; MICE; MICE, SCID; NEURONS; OXIDES; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSPLANTATION, HETEROLOGOUS;

ANIMALIA; MURINAE;

EID: 40949154295     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-0251     Document Type: Article

References (72)

1. Gritti A, Frolichsthal-Schoeller P, Galli R et al. Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci 1999;19:3287-3297.
2. Gage FH. Mammalian neural stem cells. Science 2000;287:1433-1438.
3. Alvarez-Buylla A, Seri B, Doetsch F. Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 2002;57:751-758.
4. Ourednik V, Ourednik J, Park KI et al. Neural stem cells are uniquely suited for cell replacement and gene therapy in the CNS. Novartis Found Symp 2000;231:242-262; discussion 262-249, 302-306.
5. Park KI, Ourednik J, Ourednik V et al. Global gene and cell replacement strategies via stem cells. Gene Ther 2002;9:613-624.
6. Snyder EY, Yoon C, Flax JD et al. Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex. Proc Natl Acad Sci U S A 1997;94:11663-11668.
7. Yandava BD, Billinghurst LL, Snyder EY. "Global" cell replacement is feasible via neural stem cell transplantation: Evidence from the dysmyelinated shiverer mouse brain. Proc Natl Acad Sci U S A 1999;96:7029-7034.
8. Brustle O, Choudhary K, Karram K et al. Chimeric brains generated by intraventricular transplantation of fetal human brain cells into embryonic rats. Nat Biotechnol 1998;16:1040-1044.
9. Aboody KS, Brown A, Rainov NG et al. Neural stem cells display extensive tropism for pathology in adult brain: Evidence from intracranial gliomas. Proc Natl Acad Sci U S A 2000;97:12846-12851; erratum in Proc Natl Acad Sci U S A 2001;98:777.
10. Einstein O, Karussis D, Grigoriadis N et al. Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis. Mol Cell Neurosci 2003;24:1074-1082.
11. Pluchino S, Quattrini A, Brambilla E et al. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 2003;422:688-694.
12. Pluchino S, Zanotti L, Rossi B et al. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005;436:266-271.
13. Vescovi AL, Gritti A, Galli R et al. Isolation and intracerebral grafting of nontransformed multipotential embryonic human CNS stem cells. J Neurotrauma 1999;16:689-693.
14. Galli R, Pagano SF, Gritti A et al. Regulation of neuronal differentiation in human CNS stem cell progeny by leukemia inhibitory factor. Dev Neurosci 2000;22:86-95
15. Svendsen CN, Caldwell MA, Ostenfeld T. Human neural stem cells: Isolation, expansion and transplantation. Brain Pathol 1999;9:499-513.
16. Flax JD, Aurora S, Yang C et al. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol 1998;16:1033-1039.
17. Carpenter MK, Cui X, Hu ZY et al. In vitro expansion of a multipotent population of human neural progenitor cells. Exp Neurol 1999;158:265-278.
18. Consiglio A, Gritti A, Dolcetta D et al. Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc Natl Acad Sci U S A 2004;101:14835-14840.
19. Nakatomi H, Kuriu T, Okabe S et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 2002;110:429-441.
20. Curtis MA, Penney EB, Pearson AG et al. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci U S A 2003;100:9023-9027.
21. Mitchell BD, Emsley JG, Magavi SS et al. Constitutive and induced neurogenesis in the adult mammalian brain: Manipulation of endogenous precursors toward CNS repair. Dev Neurosci 2004;26:101-117.
22. Cooper O, Isacson O. Intrastriatal transforming growth factor alpha delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J Neurosci 2004;24:8924-8931.
23. Hoehn M, Kustermann E, Blunk J et al. Monitoring of implanted stem cell migration in vivo: A highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci U S A 2002;99:16267-16272.
24. Bulte JW, Ben-Hur T, Miller BR et al. MR microscopy of magnetically labeled neurospheres transplanted into the Lewis EAE rat brain. Magn Reson Med 2003;50:201-205.
25. Stroh A, Faber C, Neuberger T et al. In vivo detection limits of magnetically labeled embryonic stem cells in the rat brain using high-field (17.6 T) magnetic resonance imaging. Neuroimage 2005;24:635-645.
26. Zhang Z, Jiang Q, Jiang F et al. In vivo magnetic resonance imaging tracks adult neural progenitor cell targeting of brain tumor. Neuroimage 2004;23:281-287.
27. Jiang Q, Zhang ZG, Ding GL et al. Investigation of neural progenitor cell induced angiogenesis after embolic stroke in rat using MRI. Neuroimage 2005;28:698-707.
28. Jiang Q, Zhang ZG, Ding GL et al. MRI detects white matter reorganization after neural progenitor cell treatment of stroke. Neuroimage 2006;32:1080-1089.
29. Frank JA, Zywicke H, Jordan EK et al. Magnetic intracellular labeling of mammalian cells by combining (FDA-approved) superparamagnetic iron oxide MR contrast agents and commonly used transfection agents. Acad Radiol 2002;9(suppl 2):S484-S487.
30. Bulte JW, Laughlin PG, Jordan EK et al. Tagging of T cells with superparamagnetic iron oxide: Uptake kinetics and relaxometry. Acad Radiol 1996;3(suppl 2):S301-S303.
31. Josephson L, Tung CH, Moore A et al. High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. Bioconjug Chem 1999;10:186-191.
32. Lewin M, Carlesso N, Tung CH et al. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat Biotechnol 2000;18:410-414.
33. Moore A, Josephson L, Bhorade RM et al. Human transferrin receptor gene as a marker gene for MR imaging. Radiology 2001;221:244-250.
34. Ahrens ET, Feili-Hariri M, Xu H et al. Receptor-mediated endocytosis of iron-oxide particles provides efficient labeling of dendritic cells for in vivo MR imaging. Magn Reson Med 2003;49:1006-1013.
35. 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.
36. Bulte JW, Douglas T, Witwer B et al. Monitoring stem cell therapy in vivo using magnetodendrimers as a new class of cellular MR contrast agents. Acad Radiol 2002;9(suppl 2):S332-S335.
37. Dunning MD, Lakatos A, Loizou L et al. Superparamagnetic iron oxide-labeled Schwann cells and olfactory ensheathing cells can be traced in vivo by magnetic resonance imaging and retain functional properties after transplantation into the CNS. J Neurosci 2004;24:9799-9810.
38. Raynal I, Prigent P, Peyramaure S et al. Macrophage endocytosis of superparamagnetic iron oxide nanoparticles: Mechanisms and comparison of ferumoxides and ferumoxtran-10. Invest Radiol 2004;39:56-63.
39. Kalish H, Arbab AS, Miller BR et al. 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.
40. Magnitsky S, Watson DJ, Walton RM et al. In vivo and ex vivo MRI detection of localized and disseminated neural stem cell grafts in the mouse brain. Neuroimage 2005;26:744-754.
41. Watson DJ, Walton RM, Magnitsky SG et al. Structure-specific patterns of neural stem cell engraftment after transplantation in the adult mouse brain. Hum Gene Ther 2006;17:693-704.
42. Bulte JW, Zhang S, van Gelderen P et al. Neurotransplantation of magnetically labeled oligodendrocyte progenitors: Magnetic resonance tracking of cell migration and myelination. Proc Natl Acad Sci U S A 1999;96:15256-15261.
43. Franklin RJ, Blaschuk KL, Bearchell MC et al. Magnetic resonance imaging of transplanted oligodendrocyte precursors in the rat brain. Neuroreport 1999;10:3961-3965.
44. Ben-Hur T, van Heeswijk RB, Einstein O et al. Serial in vivo MR tracking of magnetically labeled neural spheres transplanted in chronic EAE mice. Magn Reson Med 2007;57:164-171.
45. Politi LS, Bacigaluppi M, Brambilla E et al. Magnetic resonance-based tracking and quantification of intravenously-injected neural stem cell accumulation in the brain of mice with experimental multiple sclerosis. STEM CELLS 2007;25:2583-2592.
46. Arbab AS, Bashaw LA, Miller BR et al. 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.
47. Arbab AS, Yocum GT, Wilson LB et al. Comparison of transfection agents in forming complexes with ferumoxides, cell labeling efficiency, and cellular viability. Mol Imaging 2004;3:24-32.
48. Frank JA, Miller BR, Arbab AS et al. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 2003;228:480-487.
49. Frank JA, Anderson SA, Kalsih H et al. Methods for magnetically labeling stem and other cells for detection by in vivo magnetic resonance imaging. Cytotherapy 2004;6:621-625.
50. Arbab AS, Pandit SD, Anderson SA et al. Magnetic resonance imaging and confocal microscopy studies of magnetically labeled endothelial progenitor cells trafficking to sites of tumor angiogenesis. STEM CELLS 2006;24:671-678.
51. Guzman R, Uchida N, Bliss TM et al. Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc Natl Acad Sci U S A 2007;104:10211-10216.
52. Sigal R, Vogl T, Casselman J et al. Lymph node metastases from head and neck squamous cell carcinoma: MR imaging with ultrasmall superparamagnetic iron oxide particles (Sinerem MR) - Results of a phase-III multicenter clinical trial. Eur Radiol 2002;12:1104-1113.
53. Gritti A, Bonfanti L, Doetsch F et al. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci 2002;22:437-445.
54. Galli R, Fiocco R, De Filippis L et al. Emx2 regulates the proliferation of stem cells of the adult mammalian central nervous system. Development 2002;129:1633-1644.
55. Sun R, Dittrich J, Le-Huu M et al. Physical and biological characterization of superparamagnetic iron oxide- and ultrasmall superparamagnetic iron oxide-labeled cells: A comparison. Invest Radiol 2005;40:504-513.
56. Corot C, Robert P, Idee JM et al. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Deliv Rev 2006;58:1471-1504.
57. Memarsadeghi M, Riedl CC, Kaneider A et al. Axillary lymph node metastases in patients with breast carcinomas: Assessment with non-enhanced versus uspio-enhanced MR imaging. Radiology 2006;241:367-377.
58. Matuszewski L, Persigehl T, Wall A et al. Cell tagging with clinically approved iron oxides: Feasibility and effect of lipofection, particle size, and surface coating on labeling efficiency. Radiology 2005;235:155-161.
59. Vescovi AL, Parati EA, Gritti A et al. Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Exp Neurol 1999;156:71-83.
60. Reynolds BA, Rietze RL. Neural stem cells and neurospheres - Reevaluating the relationship. Nat Methods 2005;2:333-336.
61. Singec I, Knoth R, Meyer RP et al. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat Methods 2006;3:801-806.
62. Brown KE, Mathahs MM, Broadhurst KA et al. Chronic iron overload stimulates hepatocyte proliferation and cyclin D1 expression in rodent liver. Transl Res 2006;148:55-62.
63. Nurtjahja-Tjendraputra E, Fu D, Phang JM et al. Iron chelation regulates cyclin D1 expression via the proteasome: A link to iron deficiency-mediated growth suppression. Blood 2007;109:4045-4054.
64. Whitnall M, Howard J, Ponka P et al. A class of iron chelators with a wide spectrum of potent antitumor activity that overcomes resistance to chemotherapeutics. Proc Natl Acad Sci U S A 2006;103:14901-14906.
65. Defrere S, Van Langendonckt A, Vaesen S et al. Iron overload enhances epithelial cell proliferation in endometriotic lesions induced in a murine model. Hum Reprod 2006;21:2810-2816.
66. Knobel Y, Glei M, Osswald K et al. Ferric iron increases ROS formation, modulates cell growth and enhances genotoxic damage by 4-hydroxynonenal in human colon tumor cells. Toxicol In Vitro 2006;20:793-800.
67. Kostura L, Kraitchman DL, Mackay AM et al. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed 2004;17:513-517.
68. Arbab AS, Bashaw LA, Miller BR et al. Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 2003;229:838-846.
69. Bulte JW, Kraitchman DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 2004;17:484-499.
70. Park KI, Liu S, Flax JD et al. Transplantation of neural progenitor and stem cells: Developmental insights may suggest new therapies for spinal cord and other CNS dysfunction. J Neurotrauma 1999;16:675-687.
71. Walczak P, Kedziorek DA, Gilad AA et al. 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.
72. Gilad AA, Winnard PT, Jr., van Zijl PC, Bulte JW. Developing MR reporter genes: Promises and pitfalls. NMR Biomed 2007;20:275-290.