Nucleofection is the most efficient nonviral transfection method for neuronal stem cells derived from ventral mesencephali with no changes in cell composition or dopaminergic fate

Stem Cells

Volumn 24, Issue 12, 2006, Pages 2776-2791

  Cesnulevicius, Konstantin ^a   Timmer, Marco ^a   Wesemann, Maike ^a   Thomas, Tobias ^a   Barkhausen, Tanja ^a   Grothe, Claudia ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Dopaminergic neurons; Neural stem cells; Nucleofection; Transfection; Transplantation

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEIN; NEUROTROPHIC FACTOR; RED FLUORESCENT PROTEIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; DOPAMINERGIC NERVE CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; MESENCEPHALON; NEURAL STEM CELL; NONHUMAN; RAT; STEM CELL;

ANIMALS; CELL COUNT; CELL DIFFERENTIATION; CELL LINEAGE; CELL NUCLEUS; CELL SURVIVAL; DOPAMINE; ELECTROPORATION; FIBROBLAST GROWTH FACTOR 2; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; MESENCEPHALON; NEURONS; OXIDOPAMINE; RATS; RATS, SPRAGUE-DAWLEY; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSFECTION; VIRUSES;

EID: 33751427733     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2006-0176     Document Type: Article

References (73)

1. Kordower JH, Freeman TB, Snow BJ et al. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. N Engl J Med 1995;332:1118-1124.
2. Piccini P, Brooks DJ, Bjorklund A et al. Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nat Neurosci 1999;2:1137-1140.
3. Piccini P, Lindvall O, Bjorklund A et al. Delayed recovery of movement-related cortical function in Parkinson's disease after striatal dopaminergic grafts. Ann Neurol 2000;48:689-695.
4. Chung S, Sonntag KC, Andersson T et al. Genetic engineering of mouse embryonic stem cells by Nurr1 enhances differentiation and maturation into dopaminergic neurons. Eur J Neurosci 2002;16:1829-1838.
5. Kim JH, Auerbach JM, Rodriguez-Gomez JA et al. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 2002;418:50-56.
6. Lee S-H, Lumelsky N, Studer L et al. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol 2000;18:675-679.
7. Lindvall O, Kokaia Z, Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Med 2004;10(Suppl):42-50.
8. Nishimura F, Yoshikawa M, Kanda S et al. Potential use of embryonic stem cells for the treatment of mouse parkinsonian models: Improved behavior by transplantation of in vitro differentiated dopaminergic neurons from embryonic stem cells. STEM CELLS 2003;21:171-180.
9. Roybon L, Christophersen NS, Brundin P, Li JY. Stem cell therapy for Parkinson's disease: Where do we stand? Cell Tissue Res 2004;318:261-273.
10. Snyder BJ, Olanow CW. Stem cell treatment for Parkinson's disease: An update for 2005. Curr Opin Neurol 2005;18:376-385.
11. Brundin P, Bjorklund A. Survival, growth and function of dopaminergic neurons grafted to the brain. Prog Brain Res 1987;71:293-308.
12. Nikkhah G, Bentlage C, Cunningham MG et al. Intranigral fetal dopamine grafts induce behavioral compensation in the rat Parkinson model. J Neurosci 1994;14:3449-3461.
13. Lindvall O, Hagell P. Clinical observations after neural transplantation in Parkinson's disease. Prog Brain Res 2000;127:299-320.
14. Lindvall O, Sawle G, Widner H et al. Evidence for long-term survival and function of dopaminergic grafts in progressive Parkinson's disease. Ann Neurol 1994;35:172-180.
15. Polgar S, Morris ME, Reilly S et al. Reconstructive neurosurgery for Parkinson's disease: A systematic review and preliminary meta-analysis. Brain Res Bull 2003;60:1-24.
16. Freed CR, Greene PE, Breeze RE et al. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 2001;344:710-719.
17. Hagell P, Piccini P, Bjorklund A et al. Dyskinesias following neural transplantation in Parkinson's disease. Nat Neurosci 2002;5:627-628.
18. Olanow CW, Goetz CG, Kordower JH et al. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann Neurol 2003;54:403-414.
19. Brundin P, Karlsson J, Emgard M et al. Improving the survival of grafted dopaminergic neurons: A review over current approaches. Cell Transplant 2000;9:179-195.
20. Sorensen AT, Thompson L, Kirik D et al. Functional properties and synaptic integration of genetically labelled dopaminergic neurons in intrastriatal grafts. Eur J Neurosci 2005;21:2793-2799.
21. Zhao S, Maxwell S, Jimenez-Beristain A et al. Generation of embryonic stem cells and transgenic mice expressing green fluorescence protein in midbrain dopaminergic neurons. Eur J Neurosci 2004;19:1133-1140.
22. Brundin P, Bjorklund A. Survival of expanded dopaminergic precursors is critical for clinical trials. Nat Neurosci 1998;1:537.
23. Studer L, Tabar V, McKay RD. Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats. Nat Neurosci 1998;1:290-295.
24. Timmer M, Grosskreutz J, Schlesinger F et al. Dopaminergic properties and function after grafting of attached neural precursor cultures. Neurobiol Dis 2006;21:587-606.
25. Beck KD, Knusel B, Hefti F. The nature of the trophic action of brain-derived neurotrophic factor, des(1-3)-insulin-like growth factor-1, and basic fibroblast growth factor on mesencephalic dopaminergic neurons developing in culture. Neuroscience 1993;52:855-866.
26. Bouvier MM, Mytilineou C. Basic fibroblast growth factor increases division and delays differentiation of dopamine precursors in vitro. J Neurosci 1995;15:7141-7149.
27. Engele J, Bohn MC. The neurotrophic effects of fibroblast growth factors on dopaminergic neurons in vitro are mediated by mesencephalic glia. J Neurosci 1991;11:3070-3078.
28. Ferrari G, Minozzi MC, Toffano G et al. Basic fibroblast growth factor promotes the survival and development of mesencephalic neurons in culture. Dev Biol 1989;133:140-147.
29. Grothe C, Schulze A, Semkova I et al. The high molecular weight fibroblast growth factor-2 isoforms (21,000 mol. wt and 23,000 mol. wt) mediate neurotrophic activity on rat embryonic mesencephalic dopaminergic neurons in vitro. Neuroscience 2000;100:73-86.
30. Knusel B, Michel PP, Schwaber JS et al. Selective and nonselective stimulation of central cholinergic and dopaminergic development in vitro by nerve growth factor, basic fibroblast growth factor, epidermal growth factor, insulin and the insulin-like growth factors I and II. J Neurosci 1990;10:558-570.
31. Mayer E, Dunnett SB, Pellitteri R et al. Basic fibroblast growth factor promotes the survival of embryonic ventral mesencephalic dopaminergic neurons-I. Effects in vitro. Neuroscience 1993;56:379-388.
32. Date I, Yoshimoto Y, Imaoka T et al. Enhanced recovery of the nigrostriatal dopaminergic system in MPTP-treated mice following intrastriatal injection of basic fibroblast growth factor in relation to aging. Brain Res 1993;621:150-154.
33. Mayer E, Fawcett JW, Dunnett SB. Basic fibroblast growth factor promotes the survival of embryonic ventral mesencephalic dopaminergic neurons-II. Effects on nigral transplants in vivo. Neuroscience 1993;56:389-398.
34. Takayama H, Ray J, Raymon HK et al. Basic fibroblast growth factor increases dopaminergic graft survival and function in a rat model of Parkinson's disease. Nat Med 1995;1:53-58.
35. Timmer M, Muller-Ostermeyer F, Kloth V et al. Enhanced survival, reinnervation, and functional recovery of intrastriatal dopamine grafts co-transplanted with Schwann cells overexpressing high molecular weight FGF-2 isoforms. Exp Neurol 2004;187:118-136.
36. Georgievska B, Kirik D, Bjorklund A. Overexpression of glial cell line-derived neurotrophic factor using a lentiviral vector induces time-and dose-dependent downregulation of tyrosine hydroxylase in the intact nigrostriatal dopamine system. J Neurosci 2004;24:6437-6445.
37. Kirik D, Rosenblad C, Bjorklund A et al. Long-term rAAV-mediated gene transfer of GDNF in the rat Parkinson's model: Intrastriatal but not intranigral transduction promotes functional regeneration in the lesioned nigrostriatal system. J Neurosci 2000;20:4686-4700.
38. Pfeifer A, Ikawa M, Dayn Y et al. Transgenesis by lentiviral vectors: Lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc Natl Acad Sci USA 2002;99:2140-2145.
39. Smith-Arica JR, Thomson AJ, Ansell R et al. Infection efficiency of human and mouse embryonic stem cells using adenoviral and adeno-associated viral vectors. Cloning Stem Cells 2003;5:51-62.
40. Dityateva G, Hammond M, Thiel C et al. Rapid and efficient electroporation-based gene transfer into primary dissociated neurons. J Neurosci Methods 2003;130:65-73.
41. Gresch O, Engel FB, Nesic D et al. New non-viral method for gene transfer into primary cells. Methods 2004;33:151-163.
42. Mertz KD, Weisheit G, Schilling K et al. Electroporation of primary neural cultures: A simple method for directed gene transfer in vitro. Histochem Cell Biol 2002;118:501-506.
43. Lai W, Chang CH, Farber DL. Gene transfection and expression in resting and activated murine CD4 T cell subsets. J Immunol Methods 2003;282:93-102.
44. Martinet W, Schrijvers DM, Kockx MM. Nucleofection as an efficient nonviral transfection method for human monocytic cells. Biotechnol Lett 2003;25:1025-1029.
45. Trompeter HI, Weinhold S, Thiel C et al. Rapid and highly efficient gene transfer into natural killer cells by nucleofection. J Immunol Methods 2003;274:245-256.
46. Aluigi M, Fogli M, Curti A et al. Nucleofection is an efficient non-viral transfection technique for human bone marrow-derived mesenchymal stem cells. STEM CELLS 2006;24:454-461.
47. Kobayashi N, Rivas-Carrillo JD, Soto-Gutierrez A et al. Gene delivery to embryonic stem cells. Birth Defects Res C Embryo Today 2005;75:10-18.
48. Lakshmipathy U, Pelacho B, Sudo K et al. Efficient transfection of embryonic and adult stem cells. STEM CELLS 2004;22:531-543.
49. Lorenz P, Harnack U, Morgenstern R. Efficient gene transfer into murine embryonic stem cells by nucleofection. Biotechnol Lett 2004;26:1589-1592.
50. Leclere PG, Panjwani A, Docherty R et al. Effective gene delivery to adult neurons by a modified form of electroporation. J Neurosci Methods 2005;142:137-143.
51. Gartner A, Collin L, Lalli G. Nucleofection of primary neurons. Methods Enzymol 2006;406:374-388.
52. Richard I, Ader M, Sytnyk V et al. Electroporation-based gene transfer for efficient transfection of neural precursor cells. Brain Res Mol Brain Res 2005;138:182-190.
53. Nikkhah G, Cunningham MG, Jodicke A et al. Improved graft survival and striatal reinnervation by microtransplantation of fetal nigral cell suspensions in the rat Parkinson model. Brain Res 1994;633:133-143.
54. Nikkhah G, Olsson M, Eberhard J et al. A microtransplantation approach for cell suspension grafting in the rat Parkinson model: A detailed account of the methodology. Neuroscience 1994;63:57-72.
55. Bjorklund H, Dahl D, Haglid K et al. Astrocytic development in fetal parietal cortex grafted to cerebral and cerebellar cortex of immature rats. Brain Res 1983;285:171-180.
56. Muller-Ostermeyer F, Claus P, Grothe C. Distinctive effects of rat fibroblast growth factor-2 isoforms on PC12 and Schwann cells. Growth Factors 2001;19:175-191.
57. Claus P, Bruns AF, Grothe C. Fibroblast growth factor-2(23) binds directly to the survival of motoneuron protein and is associated with small nuclear RNAs. Biochem J 2004;384:559-565.
58. Claus P, Doring F, Gringel S et al. Differential intranuclear localization of fibroblast growth factor-2 isoforms and specific interaction with the survival of motoneuron protein. J Biol Chem 2003;278:479-485.
59. Grothe C, Zachmann K, Unsicker K et al. High molecular weight forms of basic fibroblast growth factor recognized by a new anti-bFGF antibody. FEBS Lett 1990;260:35-38.
60. Fuhrmann S, Kirsch M, Wewetzer K, Hofmann HD. Use of cell ELISA for the screening of neurotrophic activities on minor cell populations in retinal monolayer cultures. J Neurosci Methods 1997;75:199-205.
61. Francoeur A-M, Assalian A. MICROCAT: A novel cell proliferation and cytotoxicity assay based on WST-1. http://www.roche-applied-science.com/ PROD_INF/BIOCHEMI/No.3_96/no3_toc.htm
62. Meisinger C, Zeschnigk C, Grothe C. In vivo and in vitro effect of glucocorticoids on fibroblast growth factor (FGF)-2 and FGF receptor 1 expression. J Biol Chem 1996;271:16520-16525.
63. Dono R. Fibroblast growth factors as regulators of central nervous system development and function. Am J Physiol Regul Integr Comp Physiol 2003;284:R867-R881.
64. Bauer M, Meyer M, Sautter J et al. Liposome-mediated gene transfer to fetal human ventral mesencephalic explant cultures. Neurosci Lett 2001;308:169-172.
65. Siemen H, Nix M, Endl E et al. Nucleofection of human embryonic stem cells. Stem Cells Dev 2005;14:378-383.
66. Lindvall O, Bjorklund A. Cell therapy in Parkinson's disease. NeuroRx 2004;1:382-393.
67. Gehl J. Electroporation: Theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol Scand 2003;177:437-447.
68. Kawabata I, Umeda T, Yamamoto K et al. Electroporation-mediated gene transfer system applied to cultured CNS neurons. Neuroreport 2004;15:971-975.
69. Yang ZJ, Appleby VJ, Coyle B et al. Novel strategy to study gene expression and function in developing cerebellar granule cells. J Neurosci Methods 2004;132:149-160.
70. Piotrowicz RS, Martin JL, Dillman WH et al. The 27-kDa heat shock protein facilitates basic fibroblast growth factor release from endothelial cells. J Biol Chem 1997;272:7042-7047.
71. Eves EM, Skoczylas C, Yoshida K et al. FGF induces a switch in death receptor pathways in neuronal cells. J Neurosci 2001;21:4996-5006.
72. Jungnickel J, Klutzny A, Guhr S et al. Regulation of neuronal death and calcitonin gene-related peptide by fibroblast growth factor-2 and FGFR3 after peripheral nerve injury: Evidence from mouse mutants. Neuroscience 2005;134:1343-1350.
73. Grothe C, Haastert K, Jungnickel J. Physiological function and putative therapeutic impact of the FGF-2 system in peripheral nerve regeneration - Lessons from in vivo studies in mice and rats. Brain Res Brain Res Rev 2006;51:293-299.