Combined use of BDNF, ascorbic acid, low oxygen, and prolonged differentiation time generates tyrosine hydroxylase-expressing neurons after long-term in vitro expansion of human fetal midbrain precursor cells

Experimental Neurology

Volumn 213, Issue 2, 2008, Pages 354-362

  Maciaczyk, Jaroslaw ^a,c   Singec, Ilyas ^b   Maciaczyk, Donata ^a   Nikkhah, Guido ^a  

^a Neurocenter   (Germany)

^b BURNHAM INSTITUTE   (United States)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

BDNF; Cell therapy; Dopamine neuron; Human fetal mesencephalon; Neural precursor cell; Parkinson's disease

Indexed keywords

ASCORBIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; LEUKEMIA INHIBITORY FACTOR; MICROTUBULE ASSOCIATED PROTEIN 2; OXYGEN; TYROSINE 3 MONOOXYGENASE;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MESENCEPHALON; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; STEM CELL TRANSPLANTATION;

ASCORBIC ACID; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; FETUS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MESENCEPHALON; NEURONS; OXYGEN; STEM CELLS; TIME; TIME FACTORS; TYROSINE 3-MONOOXYGENASE;

EID: 51349094603     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.06.014     Document Type: Article

References (55)

1. Ahmed S., Reynolds B.A., and Weiss S. BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J. Neurosci. 15 8 (1995) 5765-5778
2. Anderson L., Burnstein R.M., He X., Luce R., Furlong R., Foltynie T., Sykacek P., Menon D.K., and Caldwell M.A. Gene expression changes in long term expanded human neural progenitor cells passaged by chopping lead to loss of neurogenic potential in vivo. Exp. Neurol. 204 (2007) 512-524
3. Baquet Z.C., Bickford P.C., and Jones K.R. Brain-derived neurotrophic factor is required for the establishment of the proper number of dopaminergic neurons in the substantia nigra pars compacta. J. Neurosci. 25 26 (2005) 6251-6259
4. Barberi T., Klivenyi P., Calingasan N.Y., Lee H., Kawamata H., Loonam K., Perrier A.L., Bruses J., Rubio M.E., Topf N., Tabar V., Harrison N.L., Beal M.F., Moore M.A., and Studer L. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotechnol. 21 10 (2003) 1200-1207
5. Burbach J.P., Smits S., and Smidt M.P. Transcription factors in the development of midbrain dopamine neurons. Ann. N. Y. Acad. Sci. 991 (2003) 61-68
6. Caldwell M.A., He X., Wilkie N., Pollack S., Marshall G., Wafford K.A., and Svendsen C.N. Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat. Biotechnol. 19 5 (2001) 475-479
7. Carpenter M.K., Cui X., Hu Z.Y., Jackson J., Sherman S., Seiger A., and Wahlberg L.U. In vitro expansion of a multipotent population of human neural progenitor cells. Exp. Neurol. 158 2 (1999) 265-278
8. Christophersen N.S., Meijer X., Jørgensen J.R., Englund U., Grønborg M., Seiger A., Brundin P., and Wahlberg L.U. Induction of dopaminergic neurons from growth factor expanded neural stem/progenitor cell cultures derived from human first trimester forebrain. Brain Res. Bull. 70 4-6 (2006) 457-466
9. Chung S., Shin B.S., Hwang M., Lardaro T., Kang U.J., Isacson O., and Kim K.S. Neural precursors derived from embryonic stem cells, but not those from fetal ventral mesencephalon, maintain the potential to differentiate into dopaminergic neurons after expansion in vitro. Stem. Cells 24 6 (2006) 1583-1593
10. Freeman T.B., Vawter D.E., Leaverton P.E., Godbold J.H., Hauser R.A., Goetz C.G., and Olanow C.W. Use of placebo surgery in controlled trials of a cellular-based therapy for Parkinson's disease. N. Engl. J. Med. 341 13 (1999) 988-992
11. Hagell P., Schrag A., Piccini P., Jahanshahi M., Brown R., Rehncrona S., Widner H., Brundin P., Rothwell J.C., Odin P., Wenning G.K., Morrish P., Gustavii B., Björklund A., Brooks D.J., Marsden C.D., Quinn N.P., and Lindvall O. Sequential bilateral transplantation in Parkinson's disease: effects of the second graft. Brain 122 Pt 6 (1999) 1121-1132
12. Horiguchi S., Takahashi J., Kishi Y., Morizane A., Okamoto Y., Koyanagi M., Tsuji M., Tashiro K., Honjo T., Fujii S., and Hashimoto N. Neural precursor cells derived from human embryonic brain retain regional specificity. J. Neurosci. Res. 75 (2004) 817-824
13. Hyman C., Hofer M., Barde Y.A., Juhasz M., Yancopoulos G.D., Squinto S.P., and Lindsay R.M. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350 6315 (1991) 230-232
14. Iacovitti L., Stull N.D., and Jin H. Differentiation of human dopamine neurons from an embryonic carcinomal stem cell line. Brain Res. 912 1 (2001) 99-104
15. Jin G., Tan X., Tian M., Qin J., Zu H., Huang Z., and Xu H. The controlled differentiation of human neural stem cells into TH-immunoreactive (ir) neurons in vitro. Neurosci. Lett. 386 (2005) 105-110
16. Kim H.J., Sugimori M., Nakafuku M., and Svendsen C.N. Control of neurogenesis and tyrosine hydroxylase expression in neural progenitor cells through bHLH proteins and Nurr1. Exp. Neurol. 203 2 (2007) 394-405
17. Knusel B., Winslow J.W., Rosenthal A., Burton L.E., Seid D.P., Nikolics K., and Hefti F. Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin 3. Proc. Natl. Acad. Sci. U. S. A. 88 3 (1991) 961-965
18. Kordower J.H., Freeman T.B., Chen E.Y., Mufson E.J., Sanberg P.R., Hauser R.A., Snow B., and Olanow C.W. Fetal nigral grafts survive and mediate clinical benefit in a patient with Parkinson's disease. Mov. Disord. 13 3 (1998) 383-393
19. Liste I., Garcia-Garcia E., and Martinez-Serrano A. The generation of dopaminergic neurons by human neural stem cells is enhanced by Bcl-XL, both in vitro and in vivo. J. Neurosci. 24 (2004) 10786-10795
20. Lotharius J., Falsig J., van Beek J., Payne S., Dringen R., Brundin P., and Leist M. Progressive degeneration of human mesencephalic neuron-derived cells triggered by dopamine-dependent oxidative stress is dependent on the mixed-lineage kinase pathway. J. Neurosci. 25 27 (2005) 6329-6342
21. Mendez I., Sanchez-Pernaute R., Cooper O., Viñuela A., Ferrari D., Björklund L., Dagher A., and Isacson O. Cell type analysis of functional fetal dopamine cell suspension transplants in the striatum and substantia nigra of patients with Parkinson's disease. Brain 128 Pt 7 (2005) 1498-1510 2005 Jul
22. Mendez I., Dagher A., Hong M., Gaudet P., Weerasinghe S., McAlister V., King D., Desrosiers J., Darvesh S., Acorn T., and Robertson H. Simultaneous intrastriatal and intranigral fetal dopaminergic grafts in patients with Parkinson disease: a pilot study. Report of three cases. J. Neurosurg. 96 3 (2002) 589-596
23. Milosevic J., Schwarz S.C., Krohn K., Poppe M., Storch A., and Schwarz J. Low atmospheric oxygen avoids maturation, senescence and cell death of murine mesencephalic neural precursors. J. Neurochem. 92 4 (2005) 718-729
24. Milosevic J., Brandt A., Roemuss U., Arnold A., Wegner F., Schwarz S.C., Storch A., Zimmermann H., and Schwarz J. Uracil nucleotides stimulate human neural precursor cell proliferation and dopaminergic differentiation: involvement of MEK/ERK signalling. J. Neurochem. 99 3 (2006) 913-923
25. Nikkhah G., Falkenstein G., and Rosenthal C. Restorative plasticity of dopamine neuronal transplants depends on the degree of hemispheric dominance. J. Neurosci. 21 16 (2001) 6252-6263
26. Nishino H., Hida H., Takei N., Kumazaki M., Nakajima K., and Baba H. Mesencephalic neural stem (progenitor) cells develop to dopaminergic neurons more strongly in dopamine-depleted striatum than in intact striatum. Exp. Neurol. 164 1 (2000) 209-214
27. Ostenfeld T., Joly E., Tai Y.T., Peters A., Caldwell M., Jauniaux E., and Svendsen C.N. Regional specification of rodent and human neurospheres. Brain Res. Dev. Brain Res. 134 1-2 (2002) 43-55
28. Perrier A.L., Tabar V., Barberi T., Rubio M.E., Bruses J., Topf N., Harrison N.L., and Studer L. Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 101 34 (2004) 12543-12548
29. Riaz S.S., Jauniaux E., Stern G.M., and Bradford H.F. The controlled conversion of human neural progenitor cells derived from foetal ventral mesencephalon into dopaminergic neurons in vitro. Brain Res. Dev. Brain Res. 136 1 (2002) 27-34
30. Riaz S.S., Theofilopoulos S., Jauniaux E., Stern G.M., and Bradford H.F. The differentiation potential of human foetal neuronal progenitor cells in vitro. Brain Res. Dev. Brain Res. 153 1 (2004) 39-51
31. Sanchez-Pernaute R., Studer L., Bankiewicz K.S., Major E.O., and McKay R.D. In vitro generation and transplantation of precursor-derived human dopamine neurons. J. Neurosci. Res. 65 4 (2001) 284-288
32. Sauer H., Fischer W., Nikkhah G., Wiegand S.J., Brundin P., Lindsay R.M., and Bjorklund A. Brain-derived neurotrophic factor enhances function rather than survival of intrastriatal dopamine cell-rich grafts. Brain Res. 626 1-2 (1993) 37-44
33. Sawamoto K., Nakao N., Kakishita K., Ogawa Y., Toyama Y., Yamamoto A., Yamaguchi M., Mori K., Goldman S.A., Itakura T., and Okano H. Generation of dopaminergic neurons in the adult brain from mesencephalic precursor cells labeled with a nestin-GFP transgene. J. Neurosci. 21 11 (2001) 3895-3903
34. Silver I., and Erecinska M. Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv. Exp. Med. Biol. 454 (1998) 7-16
35. Singec I., Knoth R., Meyer R.P., Maciaczyk J., Volk B., Nikkhah G., Frotscher M., and Snyder E.Y. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat. Methods 3 10 (2006) 801-806
36. Spenger C., Hyman C., Studer L., Egli M., Evtouchenko L., Jackson C., Dahl-Jorgensen A., Lindsay R.M., and Seiler R.W. Effects of BDNF on dopaminergic, serotonergic, and GABAergic neurons in cultures of human fetal ventral mesencephalon. Exp. Neurol. 133 1 (1995) 50-63
37. Stokes A.H., Hastings T.G., and Vrana K.E. Cytotoxic and genotoxic potential of dopamine. J. Neurosci. Res. 55 (1999) 659-665
38. Storch A., Paul G., Csete M., Boehm B.O., Carvey P.M., Kupsch A., and Schwarz J. Long-term proliferation and dopaminergic differentiation of human mesencephalic neural precursor cells. Exp. Neurol. 170 2 (2001) 317-325
39. Studer L., Spenger C., Seiler R.W., Othberg A., Lindvall O., and Odin P. Effects of brain-derived neurotrophic factor on neuronal structure of dopaminergic neurons in dissociated cultures of human fetal mesencephalon. Exp. Brain Res. 108 2 (1996) 328-336
40. Studer L., Tabar V., and McKay R.D. Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats. Nat. Neurosci. 1 4 (1998) 290-295
41. Studer L., Csete M., Lee S.H., Kabbani N., Walikonis J., Wold B., and McKay R. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J. Neurosci. 20 19 (2000) 7377-7383
42. Svendsen C.N., ter Borg M.G., Armstrong R.J., Rosser A.E., Chandran S., Ostenfeld T., and Caldwell M.A. A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods 85 2 (1998) 141-152
43. Svendsen C.N. Stem cells and Parkinson's disease: toward a treatment, not a cure. Cell Stem. Cell 2 5 (2008) 412-413 2008 May 8
44. Theofilopoulos S., Goggi J., Riaz S.S., Jauniaux E., Stern G.M., and Bradford H.F. Parallel induction of the formation of dopamine and its metabolites with induction of tyrosine hydroxylase expression in foetal rat and human cerebral cortical cells by brain-derived neurotrophic factor and glial-cell derived neurotrophic factor. Brain. Res. Dev. Brain Res. 127 2 (2001) 111-122
45. Timmer M., Grosskreutz J., Schlesinger F., Krampfl K., Wesemann M., Just L., Bufler J., and Grothe C. Dopaminergic properties and function after grafting of attached neural precursor cultures. Neurobiol. Dis. 21 3 (2006) 587-606
46. Volpicelli F., Consales C., Caiazzo M., Colucci-D'Amato L., Perrone-Capano C., and di Porzio U. Enhancement of dopaminergic differentiation in proliferating midbrain neuroblasts by sonic hedgehog and ascorbic acid. Neural. Plast. 11 1-2 (2004) 45-57
47. Wang X., Li X., Wang K., Zhou H., Xue B., Li L., and Wand X. Forskolin cooperating with growth factor on generation of dopaminergic neurons from human fetal mesencephalic neural progenitor cells. Neurosci. Lett. 362 (2004) 117-121
48. Wenning G.K., Odin P., Morrish P., Rehncrona S., Widner H., Brundin P., Rothwell J.C., Brown R., Gustavii B., Hagell P., Jahanshahi M., Sawle G., Björklund A., Brooks D.J., Marsden C.D., Quinn N.P., and Lindvall O. Short- and long-term survival and function of unilateral intrastriatal dopaminergic grafts in Parkinson's disease. Ann. Neurol. 42 1 (1997) 95-107
49. Wright L.S., Li J., Caldwell M.A., Wallace K., Johnson J.A., and Svendsen C.N. Gene expression in human neural stem cells: effects of leukemia inhibitory factor. J. Neurochem. 86 1 (2003) 179-195
50. Yan J., Studer L., and McKay R.D. Ascorbic acid increases the yield of dopaminergic neurons derived from basic fibroblast growth factor expanded mesencephalic precursors. J. Neurochem. 76 1 (2001) 307-311
51. Yang M., Donaldson A.E., Marshall C.E., Shen J., and Iacovitti L. Studies on the differentiation of dopaminergic traits in human neural progenitor cells in vitro and in vivo. Cell Transplant 13 5 (2004) 535-547
52. Zecca L., Youdim M.B., Riederer P., Connor J.R., and Crichton R.R. Iron, brain ageing and neurodegenerative disorders. Nat. Rev., Neurosci. 5 (2004) 863-873
53. Zhou J., Bradford H.F., and Stern G.M. The response of human and rat fetal ventral mesencephalon in culture to the brain-derived neurotrophic factor treatment. Brain Res. 656 1 (1994) 147-156
54. Zhou J., Bradford H.F., and Stern G.M. The stimulatory effect of brain-derived neurotrophic factor on dopaminergic phenotype expression of embryonic rat cortical neurons in vitro. Brain Res. Dev. Brain Res. 81 2 (1994) 318-324
55. Zhou J., Pliego-Rivero B., Bradford H.F., Stern G.M., and Jauniaux E.R. Induction of tyrosine hydroxylase gene expression in human foetal cerebral cortex. Neurosci. Lett. 252 3 (1998) 215-217