The embryonic midbrain directs neuronal specification of embryonic stem cells at early stages of differentiation

Developmental Biology

Volumn 325, Issue 1, 2009, Pages 49-59

  Baizabal, José Manuel ^a   Covarrubias, Luis ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Differentiation; Dopaminergic neurons; Embryonic stem cells; Midbrain; Neural precursor cells; Parkinson's disease

Indexed keywords

PROTEIN DERIVATIVE; PROTEIN LMX1A; PROTEIN NKX6.1; TRANSCRIPTION FACTOR PAX7; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; MESENCEPHALON; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; STEM CELL TRANSPLANTATION;

EID: 57949110808     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.09.024     Document Type: Article

References (41)

1. Andersson E., Tryggvason U., Deng Q., Friling S., Alekseenko Z., Robert B., Perlmann T., and Ericson J. Identification of intrinsic determinants of midbrain dopamine neurons. Cell 124 (2006) 393-405
2. Bayer S.A., Wills K.V., Triarhou L.C., and Ghetti B. Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp. Brain Res. 105 (1995) 191-199
3. Benninger F., Beck H., Wernig M., Tucker K.L., Brustle O., and Scheffler B. Functional integration of embryonic stem cell-derived neurons in hippocampal slice cultures. J. Neurosci. 23 (2003) 7075-7083
4. 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. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci. U S A. 99 (2002) 2344-2349
5. Brustle O., Spiro A.C., Karram K., Choudhary K., Okabe S., and McKay R.D. In vitro-generated neural precursors participate in mammalian brain development. Proc. Natl. Acad. Sci. U S A. 94 (1997) 14809-14814
6. 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. Genetic engineering of mouse embryonic stem cells by Nurr1 enhances differentiation and maturation into dopaminergic neurons. Eur. J. Neurosci. 16 (2002) 1829-1838
7. Elkabetz Y., Panagiotakos G., Al Shamy G., Socci N.D., Tabar V., and Studer L. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 22 (2008) 152-165
8. Fedtsova N., and Turner E.E. Signals from the ventral midline and isthmus regulate the development of Brn3.0-expressing neurons in the midbrain. Mech. Dev. 105 (2001) 129-144
9. Gregg C., and Weiss S. CNTF/LIF/gp130 receptor complex signaling maintains a VZ precursor differentiation gradient in the developing ventral forebrain. Development 132 (2005) 565-578
10. Hynes M., Porter J.A., Chiang C., Chang D., Tessier-Lavigne M., Beachy P.A., and Rosenthal A. Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron 15 (1995) 35-44
11. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Nishikawa S.I., and Sasai Y. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28 (2000) 31-40
12. Kittappa R., Chang W.W., Awatramani R.B., and McKay R.D. The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age. PLoS Biol. 5 (2007) e325
13. Lee S.H., Lumelsky N., Studer L., Auerbach J.M., and McKay R.D. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 18 (2000) 675-679
14. Lee S., Lee B., Joshi K., Pfaff S.L., Lee J.W., and Lee S.K. A regulatory network to segregate the identity of neuronal subtypes. Dev. Cell 14 (2008) 877-889
15. Lin L., Rao Y., and Isacson O. Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol. Cell. Neurosci. 28 (2005) 547-555
16. Liu A., and Niswander L.A. Bone morphogenetic protein signalling and vertebrate nervous system development. Nat. Rev., Neurosci. 6 (2005) 945-954
17. Lupo G., Harris W.A., and Lewis K.E. Mechanisms of ventral patterning in the vertebrate nervous system. Nat. Rev., Neurosci. 7 (2006) 103-114
18. Martinat C., Bacci J.J., Leete T., Kim J., Vanti W.B., Newman A.H., Cha J.H., Gether U., Wang H., and Abeliovich A. Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phenotype. Proc. Natl. Acad. Sci. U S A. 103 (2006) 2874-2879
19. Murry C.E., and Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132 (2008) 661-680
20. Nakatani T., Minaki Y., Kumai M., and Ono Y. Helt determines GABAergic over glutamatergic neuronal fate by repressing Ngn genes in the developing mesencephalon. Development 134 (2007) 2783-2793
21. Olsson M., Campbell K., and Turnbull D.H. Specification of mouse telencephalic and mid-hindbrain progenitors following heterotopic ultrasound-guided embryonic transplantation. Neuron 19 (1997) 761-772
22. Ono Y., Nakatani T., Sakamoto Y., Mizuhara E., Minaki Y., Kumai M., Hamaguchi A., Nishimura M., Inoue Y., Hayashi H., Takahashi J., and Imai T. Differences in neurogenic potential in floor plate cells along an anteroposterior location: midbrain dopaminergic neurons originate from mesencephalic floor plate cells. Development 134 (2007) 3213-3225
23. Pankratz M.T., Li X.J., Lavaute T.M., Lyons E.A., Chen X., and Zhang S.C. Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 25 (2007) 1511-1520
24. Parmar M., and Li M. Early specification of dopaminergic phenotype during ES cell differentiation. BMC Dev. Biol. 7 (2007) 86
25. Plachta N., Bibel M., Tucker K.L., and Barde Y.A. Developmental potential of defined neural progenitors derived from mouse embryonic stem cells. Development 131 (2004) 5449-5456
26. Pruszak J., Sonntag K.C., Aung M.H., Sanchez-Pernaute R., and Isacson O. Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 25 (2007) 2257-2268
27. Rathjen J., and Rathjen P.D. Mouse ES cells: experimental exploitation of pluripotent differentiation potential. Curr. Opin. Genet. Dev. 11 (2001) 587-594
28. Rodriguez-Gomez J.A., Lu J.Q., Velasco I., Rivera S., Zoghbi S.S., Liow J.S., Musachio J.L., Chin F.T., Toyama H., Seidel J., Green M.V., Thanos P.K., Ichise M., Pike V.W., Innis R.B., and McKay R.D. Persistent dopamine functions of neurons derived from embryonic stem cells in a rodent model of Parkinson disease. Stem Cells 25 (2007) 918-928
29. Roy N.S., Cleren C., Singh S.K., Yang L., Beal M.F., and Goldman S.A. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 12 (2006) 1259-1268
30. Saucedo-Cardenas O., Quintana-Hau J.D., Le W.D., Smidt M.P., Cox J.J., De Mayo F., Burbach J.P., and Conneely O.M. Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl. Acad. Sci. U S A. 95 (1998) 4013-4018
31. Simon H.H., Saueressig H., Wurst W., Goulding M.D., O, and Leary D.D. Fate of midbrain dopaminergic neurons controlled by the engrailed genes. J. Neurosci. 21 (2001) 3126-3134
32. Smidt M.P., Smits S.M., Bouwmeester H., Hamers F.P., van der Linden A.J., Hellemons A.J., Graw J., and Burbach J.P. Early developmental failure of substantia nigra dopamine neurons in mice lacking the homeodomain gene Pitx3. Development 131 (2004) 1145-1155
33. Smukler S.R., Runciman S.B., Xu S., and van der Kooy D. Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J. Cell Biol. 172 (2006) 79-90
34. Thomas M., Beazley L., and Ziman M. A multiphasic role for Pax7 in tectal development. Exp. Brain Res. 169 (2006) 266-271
35. Thompson J., Lovicu F., and Ziman M. The role of Pax7 in determining the cytoarchitecture of the superior colliculus. Dev. Growth Differ. 46 (2004) 213-218
36. Watanabe K., Kamiya D., Nishiyama A., Katayama T., Nozaki S., Kawasaki H., Watanabe Y., Mizuseki K., and Sasai Y. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat. Neurosci. 8 (2005) 288-296
37. Wernig M., Benninger F., Schmandt T., Rade M., Tucker K.L., Bussow H., Beck H., and Brustle O. Functional integration of embryonic stem cell-derived neurons in vivo. J. Neurosci. 24 (2004) 5258-5268
38. Yan Y., Yang D., Zarnowska E.D., Du Z., Werbel B., Valliere C., Pearce R.A., Thomson J.A., and Zhang S.C. Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells 23 (2005) 781-790
39. Ye W., Shimamura K., Rubenstein J.L., Hynes M.A., and Rosenthal A. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93 (1998) 755-766
40. Ying Q.L., Stavridis M., Griffiths D., Li M., and Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21 (2003) 183-186
41. Zhang S.C., Wernig M., Duncan I.D., Brustle O., and Thomson J.A. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19 (2001) 1129-1133