Efficient expansion and dopaminergic differentiation of human fetal ventral midbrain neural stem cells by midbrain morphogens

Neurobiology of Disease

Volumn 49, Issue 1, 2013, Pages 118-127

  Ribeiro, Diogo ^a   Laguna Goya, Rocio ^b   Ravindran, Geeta ^a   Vuono, Romina ^b   Parish, Clare L ^a,f   Foldi, Claire ^a   Piroth, Tobias ^c   Yang, Shanzheng ^a   Parmar, Malin ^d   Nikkhah, Guido ^c   Hjerling Leffler, Jens ^a   Lindvall, Olle ^e   Barker, Roger A ^b   Arenas, Ernest ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF FREIBURG   (Germany)

^d LUND UNIVERSITY   (Sweden)

^e LUND UNIVERSITY HOSPITAL   (Sweden)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Dopaminergic; Human fetal ventral midbrain

Indexed keywords

DOPAMINE; WNT5A PROTEIN; ONCOPROTEIN; WNT PROTEIN; WNT5A PROTEIN, HUMAN;

ARTICLE; CELL COUNT; CELL EXPANSION; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC SYSTEM; FETUS; HUMAN; HUMAN TISSUE; MESENCEPHALON; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEURAL STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; CULTURE TECHNIQUE; CYTOLOGY; DOPAMINERGIC NERVE CELL; EMBRYOLOGY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

CELL COUNT; CELL CULTURE TECHNIQUES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOPAMINE; DOPAMINERGIC NEURONS; HUMANS; IMMUNOHISTOCHEMISTRY; MESENCEPHALON; NEURAL STEM CELLS; NEUROGENESIS; PATCH-CLAMP TECHNIQUES; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS; WNT PROTEINS;

EID: 84866511789     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.08.006     Document Type: Article

References (36)

1. 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.S., Studer L. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotechnol. 2003, 21:1200-1207.
2. Bjorklund A., Dunnett S.B., Brundin P., Stoessl A.J., Freed C.R., Breeze R.E., Levivier M., Peschanski M., Studer L., Barker R. Neural transplantation for the treatment of Parkinson's disease. Lancet Neurol. 2003, 2:437-445.
3. Blakely B.D., Bye C.R., Fernando C.V., Horne M.K., Macheda M.L., Stacker S.A., Arenas E., Parish C.L. Wnt5a regulates midbrain dopaminergic axon growth and guidance. PLoS One 2011, 6(3):e18373. 10.1371/journal.pone.0018373.
4. Bryja V., Schulte G., Rawal N., Grahn A., Arenas E. Wnt-5a induces Dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism. J. Cell Sci. 2007, 120:586-595.
5. Courtois E.T., Castillo C.G., Seiz E.G., Ramos M., Bueno C., Liste I., Martinez-Serrano A. In vitro and in vivo enhanced generation of human A9 dopamine neurons from neural stem cells by Bcl-X-L. J. Biol. Chem. 2010, 285:9881-9897.
6. Damier P., Hirsch E.C., Agid Y., Graybiel A.M. The substantia nigra of the human brain. I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D(28K) immunohistochemistry. Brain 1999, 122(8):1421-1436.
7. Donato R., Miljan E.A., Hines S.J., Aouabdi S., Pollock K., Patel S., Edwards F.A., Sinden J.D. Differential development of neuronal physiological responsiveness in two human neural stem cell lines. BMC Neurosci. 2007, 8.
8. 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., Eidelberg D., Fahn S. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 2001, 344:710-719.
9. Hargus G., Cooper O., Deleidi M., Levy A., Lee K., Marlow E., Yow A., Soldner F., Hockemeyer D., Hallett P.J., Osborn T., Jaenisch R., Isacson O. Differentiated Parkinson patient-derived induced pluripotent stem cells grow in the adult rodent brain and reduce motor asymmetry in Parkinsonian rats. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15921-15926.
10. Hovakimyan M., Haas S.J.P., Schmitt O., Gerber B., Wree A., Andressen C. Mesencephalic human neural progenitor cells transplanted into the neonatal hemiparkinsonian rat striatum differentiate into neurons and improve motor behaviour. J. Anat. 2006, 209:721-732.
11. Inestrosa N.C., Arenas E. Emerging roles of Wnts in the adult nervous system. Nat. Rev. Neurosci. 2010, 11:77-86.
12. Jin G.H., Tan X.F., Tian M.L., Qin J.B., Zhu H.X., Huang Z., Xu H.J. The controlled differentiation of human neural stem cells into TH-immunoreactive (ir) neurons in vitro. Neurosci. Lett. 2005, 386:105-110.
13. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Sasai Y. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 2000, 28:31-40.
14. Kim J.H., Auerbach J.M., Rodriguez-Gomez J.A., Velasco I., Gavin D., Lumelsky N., Lee S.H., Nguyen J., Sanchez-Pernaute R., Bankiewicz K., McKay R. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 2002, 418:50-56.
15. Kordower J.H., Freeman T.B., Snow B.J., Vingerhoets F.J.G., Mufson E.J., Sanberg P.R., Hauser R.A., Smith D.A., Nauert G.M., Perl D.P., Olanow C.W. 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.
16. Kriks S., Shim J.W., Piao J.H., Ganat Y.M., Wakeman D.R., Xie Z., Carrillo-Reid L., Auyeung G., Antonacci C., Buch A., Yang L.C., Beal M.F., Surmeier D.J., Kordower J.H., Tabar V., Studer L. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 2011, 480:547-U177.
17. Lee S.H., Lumelsky N., Studer L., Auerbach J.M., McKay R.D. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 2000, 18:675-679.
18. Lotharius J., Barg S., Wiekop P., Lundberg C., Raymon H.K., Brundin P. Effect of mutant alpha-synuclein on dopamine homeostasis in a new human mesencephalic cell line. J. Biol. Chem. 2002, 277:38884-38894.
19. Maciaczyk J., Singec Y., Maciaczyk D., Nikkhah G. 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. Exp. Neurol. 2008, 213:354-362.
20. Mendez I., Sanchez-Pernaute R., Cooper O., Vinuela A., Ferrari D., Bjorklund L., Dagher A., 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 2005, 128:1498-1510.
21. Milosevic J., Brandt A., Roemuss U., Arnold A., Wegner F., Schwarz S.C., Storch A., Zimmermann H., Schwarz J. Uracil nucleotides stimulate human neural precursor cell proliferation and dopaminergic differentiation: involvement of MEK/ERK signalling. J. Neurochem. 2006, 99:913-923.
22. Olanow C.W., Goetz C.G., Kordower J.H., Stoessl A.J., Sossi V., Brin M.F., Shannon K.M., Nauert G.M., Perl D.P., Godbold J., Freeman T.B. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann. Neurol. 2003, 54:403-414.
23. Parish C.L., Castelo-Branco G., Rawal N., Tonnesen J., Sorensen A.T., Salto C., Kokaia M., Lindvall O., Arenas E. Wnt5a-treated midbrain neural stem cells improve dopamine cell replacement therapy in parkinsonian mice. J. Clin. Invest. 2008, 118:149-160.
24. Piccini P., Brooks D.J., Bjorklund A., Gunn R.N., Grasby P.M., Rimoldi O., Brundin P., Hagell P., Rehncrona S., Widner H., Lindvall O. Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nat. Neurosci. 1999, 2:1137-1140.
25. Politis M., Wu K., Loane C., Quinn N.P., Brooks D.J., Rehncrona S., Bjorklund A., Lindvall O., Piccini P. Serotonergic neurons mediate dyskinesia side effects in Parkinson's patients with neural transplants. Sci. Transl. Med. 2010, 2.
26. Rawal N., Castelo-Branco G., Sousa K.M., Kele J., Kobayashi K., Okano H., Arenas E. Dynamic temporal and cell type-specific expression of Wnt signaling components in the developing midbrain. Exp. Cell. Res. 2006, 312:1626-1636.
27. Roy N.S., Cleren C., Singh S.K., Yang L., Beal M.F., Goldman S.A. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 2006, 12:1259-1268.
28. Sanchez-Pernaute R., Studer L., Bankiewicz K.S., Major E.O., McKay R.D.G. In vitro generation and transplantation of precursor-derived human dopamine neurons. J. Neurosci. Res. 2001, 65:284-288.
29. Sanchez-Pernaute R., Lee H., Patterson M., Reske-Nielsen C., Yoshizaki T., Sonntag K.C., Studer L., Isacson O. Parthenogenetic dopamine neurons from primate embryonic stem cells restore function in experimental Parkinsons disease. Brain 2008, 131:2127-2139.
30. Schulte G., Bryja V., Rawal N., Castelo-Branco G., Sousa K.M., Arenas E. Purified Wnt-5a increases differentiation of midbrain dopaminergic cells and dishevelled phosphorylation. J. Neurochem. 2005, 92(6):1550-1553.
31. Sonntag K.C., Pruszak J., Yoshizaki T., van Arensbergen J., Sanchez-Pernaute R., Isacson O. Enhanced yield of neuroepithelial precursors and midbrain-like dopaminergic neurons from human embryonic stem cells using the bone morphogenic protein antagonist Noggin. Stem Cells 2007, 25:411-418.
32. Storch A., Paul G., Csete M., Boehm B.O., Carvey P.M., Kupsch A., Schwarz J. Long-term proliferation and dopaminergic differentiation of human mesencephalic neural precursor cells. Exp. Neurol. 2001, 170:317-325.
33. Villa A., Liste I., Courtois E.T., Seiz E.G., Ramos M., Meyer M., Juliusson B., Kusk P., Martinez-Serrano A. Generation and properties of a new human ventral mesencephalic neural stem cell line. Exp. Cell. Res. 2009, 315:1860-1874.
34. Wang X., Li X.X., Wang K., Zhou H.F., Xue B., Li L.S., Wang X.M. Forskolin cooperating with growth factor on generation of dopaminergic neurons from human fetal mesencephalic neural progenitor cells. Neurosci. Lett. 2004, 362:117-121.
35. Wernig M., Zhao J.P., Pruszak J., Hedlund E., Fu D.D., Soldner F., Broccoli V., Constantine-Paton M., Isacson O., Jaenisch R. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:5856-5861.
36. Winkler C., Kirik D., Bjorklund A. Cell transplantation in Parkinson's disease: how can we make it work?. Trends Neurosci. 2005, 28:86-92.