In vitro and in vivo analyses of human embryonic stem cell-derived dopamine neurons

Journal of Neurochemistry

Volumn 92, Issue 5, 2005, Pages 1265-1276

  Park, Chang Hwan ^a   Minn, Yang Ki ^a   Lee, Ji Yeon ^a   Choi, Dong Ho ^b   Chang, Mi Yoon ^a   Shim, Jae Won ^a   Ko, Ji Yun ^a   Koh, Hyun Chul ^a   Kang, Min Jeong ^a   Kang, Jin Sun ^a   Rhie, Duck Joo ^c   Lee, Yong Sung ^a   Son, Hyeon ^a   Moon, Shin Yong ^d   Kim, Kwang Soo ^e   Lee, Sang Hun ^a  

^a Hanyang University   (South Korea)

^b Soonchunhyang University   (South Korea)

^c The Catholic University of Korea   (South Korea)

^d Seoul National University   (South Korea)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Dopamine neurons; Human embryonic stem cells; in vitro differentiation; Parkinson's disease; Transplantation

Indexed keywords

AMPHETAMINE; CELL MARKER; DOPAMINE; NUCLEAR RECEPTOR RELATED FACTOR 1; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN ENGRAILED 1; PROTEIN LMX1B; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX2; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CELL DIFFERENTIATION; CELL NUCLEUS; CELL POPULATION; CELL RENEWAL; CELL SURVIVAL; CORPUS STRIATUM; DEPOLARIZATION; DOPAMINE RELEASE; DOPAMINE UPTAKE; DOPAMINERGIC NERVE CELL; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCEPHALON; NERVE CELL CULTURE; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ROTATION; STEM CELL TRANSPLANTATION; STROMA; TREATMENT FAILURE;

ALPHA-FETOPROTEINS; ANIMALS; BEHAVIOR, ANIMAL; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COCULTURE TECHNIQUES; DNA-BINDING PROTEINS; DOPAMINE; EMBRYONIC INDUCTION; FETUS; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTORS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HEDGEHOG PROTEINS; HN PROTEIN; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INDOLES; INTERMEDIATE FILAMENT PROTEINS; ISOTONIC SOLUTIONS; KI-67 ANTIGEN; MALE; MEMBRANE POTENTIALS; MESENCEPHALON; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NEURONS; ORGANIC CATION TRANSPORT PROTEINS; PATCH-CLAMP TECHNIQUES; PAX2 TRANSCRIPTION FACTOR; POTASSIUM CHLORIDE; PROLIFERATING CELL NUCLEAR ANTIGEN; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; ROTATION; STEM CELL TRANSPLANTATION; STEM CELLS; STROMAL CELLS; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUBULIN; TYROSINE 3-MONOOXYGENASE; VIMENTIN;

PARKINSONIA; RODENTIA;

EID: 20044383922     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.03006.x     Document Type: Article

References (43)

1. Abeyta M. J., Clark A. T., Rodriguez R. T., Bodnar M. S., Pera R. A. and Firpo M. T. (2004) Unique gene expression signatures of independently-derived human embryonic stem cell lines. Hum. Mol. Genet. 13, 601-608.
2. Bayer S. A. and Altman J. (1991) Neurocortical Development. Raven Press, New York.
3. Bjorklund L. M., Sanchez-Pernaute R., Chung S., Andersson T., Chen I. Y., McNaught K. S., Brownell A. L., Jenkins B. G., Wahlestedt C., Kim K. S. and Isacson O. (2002) Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci. USA 99, 2344-2349.
4. Chang M. Y., Son H., Lee Y. S. and Lee S. H. (2003) Neurons and astrocytes secrete factors that cause stem cells to differentiate into neurons and astrocytes, respectively. Mol. Cell. Neurosci. 2, 414-426.
5. Chung S., Sonntag K.-C., Andersson T., Bjorklund L. M., Park J. J., Kim D. W., Kang U. J., Isacson O. and Kim K. S. (2002) Genetic engineering of mouse embryonic stem cells by Nurr1 enhances differentiation and maturation into dopaminergic neurons. Eur. J. Neurosci. 16, 1829-1838.
6. Damier P., Hirsch E. C., Agid Y. and Graybiel A. M. (1999) The substantia nigra of the human brain. I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D (28K) immunohistochemistry. Brain 122, 1421-1436.
7. Freed C. R., Greene P. E., Breeze R. E., Tsai W. Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J. Q. et al. (2001) Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344, 710-719.
8. Gaspar P., Ben Jelloun N. and Febvret A. (1994) Sparing of the dopaminergic neurons containing calbindin-D28k and of the dopaminergic mesocortical projections in weaver mutant mice. J. Neurosci. 61, 293-305.
9. Hitoshi S., Seaberg R. M., Koscik C., Alexson T., Kusunoki S., Kanazawa I., Tsuji S. and Kooy D. (2004) Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling. Genes Dev. 18, 1806-1811.
10. Hwang W. S., Ryu Y. J., Park J. H., Park E. S., Lee E. G., Koo J. M., Jeon H. Y., Lee B. C., Kang S. K., Kim S. J. et al. (2004) Evidence of a pluripotent human embryonic stem cell line derived from a cloned blastocyst. Science 303, 1669-1674.
11. Jacobson M. (1991) Developmental Neurobiology. Plenum Press, New York.
12. Johe K. K., Hazel T. G., Muller T., Dugich-Djordjevic M. M. and McKay R. D. (1996) Single factors direct the differentiation of stem cells from the fetal and adult nervous system. Genes Dev. 10, 3129-3140.
13. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Nishikawa S.-I. and Sasai Y. (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28, 31-40.
14. Kawasaki H., Suemori H., Mizuseki K., Watanabe K., Urano F., Ichinose H., Haruta M., Takahashi M., Yoshikawa K., Nishikawa S et al. (2002) Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. Proc. Natl Acad. Sci. USA 99, 1580-1585.
15. Kenney A. M. and Rowitch D. H. (2000) Sonic hedgehog promotes G (1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol. Cell. Biol. 20, 9055-9067.
16. Kim J. H., Auerbach J. M., Rodreguez-Gomez J. A., Velasco I., Gavin D., Lumelsky N., Lee S. H., Nguyen J., Sanchez-Pernaute R., Bankiewicz K. and McKay R. D. (2002) Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418, 50-56.
17. Kim J. Y., Koh H. C., Lee J. Y., Chang M. Y., Kim Y. C., Chung H. Y., Son H., Lee Y. S., Studer L., McKay R. and Lee S. H. (2003) Dopaminergic neuronal differentiation from rat embryonic neural precursors by Nurr1 overexpression. J. Neurochem. 85, 1443-1454.
18. Lai K., Kaspar B. K., Gage F. H. and Schaffer D. V. (2003) Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nature Neurosci. 6, 21-27.
19. Larsson L. C., Czech K. A., Brundin P. and Widner H. (2000) Intrastriatal ventral mesencephalic xenografts of porcine tissue in rats: immune responses and functional effects. Cell Transplant. 9, 261-272.
20. Le W., Conneely O. M., He Y., Jankovic J. and Appel S. H. (1999) Reduced Nurr1 expression increases the vulnerability of mesencephalic dopamine neurons to MPTP-induced injury. J. Neurochem. 73, 2218-2221.
21. Lee S. H., Lumelsky N., Studer L., Auerbach J. and McKay R. D. (2000a) Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nature Biotech. 18, 675-679.
22. Lee S. H., Chang M. Y., Lee K. H., Park B. S., Lee Y. S., Chin H. R. and Lee Y. S. (2000b) Importance of valine at position I52 for the substrate transport and 2 beta-carbomethoxy-3beta-(4-fluorophenyl) tropane binding of dopamine transporter. Mol. Pharmacol. 57, 883-889.
23. Machold R., Hayashi S., Rutlin M., Muzumdar M. D., Nery S., Corbin J. G., Gritli-Linde A., Dellovade T., Porter J. A., Rubin L. L. et al (2003) Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39, 937-950.
24. Okabe S., Forsberg-Nilsson K., Spiro A. C., Segal M. and McKay R. D. (1996) Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 59, 89-102.
25. Olsson M., Nikkhah G., Bentlage C. and Borklund A. (1995) Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 15, 3863-3875.
26. Park J. H., Kim S. J., Oh E. J., Moon S. Y., Roh S. I., Kim C. G. and Yoon H. S. (2003) Establishment and maintenance of human embryonic stem cells on STO, a permanently growing cell line. Biol. Reprod. 69, 2007-2014.
27. Paxinos G. and Watson C. (1982) The rat brain in stereotaxic co-ordinates. Academic Press, San Diego.
28. Perlmann T. and Wallen-Mackenzie A. (2004) Nurr1, an orphan nuclear receptor with essential functions in developing dopamine cells. Cell Tissue Res. 318, 45-52.
29. Perrier A. L., Tabar V., Barberi T., Rubio M. E., Bruses J., Topf N., Harrison N. L. and Studer L. (2004) Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 101, 12 543-12 548.
30. Piccini P., Brooks D. J., Bjorklund A., Gunn R. N., Grasby P. M., Rimoldi O., Brundin P., Hagell P., Rehncrona S., Widner H. and Lindvall O. (1999) Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nature Neurosci. 2, 1137-1140.
31. Qian X., Shen Q., Goderie S. K., He W., Capela A., Davis A. A. and Temple A. (2000) Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28, 69-80.
32. Reubinoff B. E., Pera M. F., Fong C.-Y., Trounson A. and Bongso A. (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nature Biotechn 18, 399-404.
33. Rosenblad C., Martinez-Serrano A. and Bjorklund A. (1996) Glial cell line-derived neurotrophic factor increases survival, growth and function of intrastriatal fetal nigral dopaminergic grafts. Neuroscience 75, 979-985.
34. Shim J. W., Koh H. C., Chang M. Y., Roh E., Choi C. Y., Oh Y. J., Son H., Lee Y. S., Studer L. and Lee S. H. (2004) Enhanced in vitro midbrain dopamine neuron differentiation, dopaminergic function, neurite outgrowth, and 1-methyl-4-phenylpyridium resistance in mouse embryonic stem cells overexpressing Bcl-XL. J. Neurosci. 24, 843-852.
35. Simon H. H., Saueressig H., Wurst W., Goulding M. D. and O'Leary D. D. M. (2001) Fate of Midbrain Dopaminergic Neurons Controlled by the Engrailed Genes. J. Neurosci. 21, 3126-3134.
36. Smidt M. P., Asbreuk C. H., Cox J. J., Chen H., Johnson R. L. and Burbach J. P. (2000) A second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b. Nature Neurosci. 3, 337-341.
37. Studer L., Tabar V. and McKay R. D. (1998) Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats. Nature Neurosci. 1, 290-295.
38. Temple S. and Davis A. A. (1994) Isolated rat cortical progenitor cells are maintained in division in vitro by membrane-associated factors. Development 120, 999-1008.
39. Thibert C., Teiltet M. A., Lapointe F., Mazelin L., Le Douarin N. M. and Mehlen P. (2003) Inhibition of neuroepithelial patched-induced apoptosis by sonic hedgehog. Science 301, 843-846.
40. Yamada T., McGeer P. L., Baimbridge K. G. and McGeer E. G. (1990) Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K. Brain Res. 526, 303-307.
41. Ye W., Shimamura K., Rubenstein J. L., Hymes M. A. and Rosenthal A. (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93, 755-766.
42. Zawada W. M., Zastrow D. J., Clarkson E. D., Adams F. S., Bell K. P. and Feed C. R. (1998) Growth factors improve immediate survival of embryonic dopamine neurons after transplantation into rats. Brain Res. 786, 96-103.
43. Zeng X., Cai J., Chen J., Luo Y., You Z.-B., Fotter E., Wang Y., Harvey B., Miura T., Backman C et al. (2004) Dopaminergic differentiation of human embryonic stem cells. Stem Cells 22, 925-940.