Telencephalic neural precursor cells show transient competence to interpret the dopaminergic niche of the embryonic midbrain

Developmental Biology

Volumn 349, Issue 2, 2011, Pages 192-203

  Baizabal, José Manuel ^a   Valencia, Concepción ^a   Guerrero Flores, Gilda ^a   Covarrubias, Luis ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Dopaminergic Neuron; Embryonic Stem Cells; Mesencephalon; Neural Precursor Cells; Neurogenesis; Niche; Telencephalon

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXG1; TRANSCRIPTION FACTOR LMX1A; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR TH; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL LINEAGE; CELL SPECIFICITY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO; EMBRYO DEVELOPMENT; GABAERGIC SYSTEM; MESENCEPHALON; MOUSE; MOUSE EMBRYO; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL NICHE; TELENCEPHALON;

EID: 78650825617     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.11.003     Document Type: Article

References (56)

1. Akamatsu W., DeVeale B., Okano H., Cooney A.J., van der Kooy D. Suppression of Oct4 by germ cell nuclear factor restricts pluripotency and promotes neural stem cell development in the early neural lineage. J. Neurosci. 2009, 29:2113-2124.
2. Anderson D.J. Stem cells and pattern formation in the nervous system: the possible versus the actual. Neuron 2001, 30:19-35.
3. Andersson E., Tryggvason U., Deng Q., Friling S., Alekseenko Z., Robert B., Perlmann T., Ericson J. Identification of intrinsic determinants of midbrain dopamine neurons. Cell 2006, 124:393-405.
4. Ang S.L. Transcriptional control of midbrain dopaminergic neuron development. Development 2006, 133:3499-3506.
5. Ashe H.L., Briscoe J. The interpretation of morphogen gradients. Development 2006, 133:385-394.
6. Baizabal J.M., Covarrubias L. The embryonic midbrain directs neuronal specification of embryonic stem cells at early stages of differentiation. Dev. Biol. 2009, 325:49-59.
7. Baizabal J.M., Furlan-Magaril M., Santa-Olalla J., Covarrubias L. Neural stem cells in development and regenerative medicine. Arch. Med. Res. 2003, 34:572-588.
8. Batista-Brito R., Close J., Machold R., Fishell G. The distinct temporal origins of olfactory bulb interneuron subtypes. J. Neurosci. 2008, 28:3966-3975.
9. Bayer S.A., Wills K.V., Triarhou L.C., Ghetti B. Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp. Brain Res. 1995, 105:191-199.
10. Cai J., Donaldson A., Yang M., German M.S., Enikolopov G., Iacovitti L. The role of Lmx1a in the differentiation of human embryonic stem cells into midbrain dopamine neurons in culture and after transplantation into Parkinson's disease model. Stem Cells 2009, 27:220-229.
11. Carletti B., Grimaldi P., Magrassi L., Rossi F. Specification of cerebellar progenitors after heterotopic-heterochronic transplantation to the embryonic CNS in vivo and in vitro. J. Neurosci. 2002, 22:7132-7146.
12. Carletti B., Grimaldi P., Magrassi L., Rossi F. Engraftment and differentiation of neocortical progenitor cells transplanted to the embryonic brain in utero. J. Neurocytol. 2004, 33:309-319.
13. Daadi M.M., Weiss S. Generation of tyrosine hydroxylase-producing neurons from precursors of the embryonic and adult forebrain. J. Neurosci. 1999, 19:4484-4497.
14. Dou C.L., Li S., Lai E. Dual role of brain factor-1 in regulating growth and patterning of the cerebral hemispheres. Cereb. Cortex 1999, 9:543-550.
15. Edlund T., Jessell T.M. Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 1999, 96:211-224.
16. Elkabetz Y., Panagiotakos G., Al Shamy G., Socci N.D., Tabar V., Studer L. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 2008, 22:152-165.
17. Ericson J., Morton S., Kawakami A., Roelink H., Jessell T.M. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 1996, 87:661-673.
18. Ferri A.L., Lin W., Mavromatakis Y.E., Wang J.C., Sasaki H., Whitsett J.A., Ang S.L. Foxa1 and Foxa2 regulate multiple phases of midbrain dopaminergic neuron development in a dosage-dependent manner. Development (Cambridge, England) 2007, 134:2761-2769.
19. Frielingsdorf H., Schwarz K., Brundin P., Mohapel P. No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc. Natl Acad. Sci. USA 2004, 101:10177-10182.
20. Grove E.A., Tole S., Limon J., Yip L., Ragsdale C.W. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 1998, 125:2315-2325.
21. Guillemot F. Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr. Opin. Cell Biol. 2005, 17:639-647.
22. Hebert J.M., Fishell G. The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci. 2008, 9:678-685.
23. Hitoshi S., Seaberg R.M., Koscik C., Alexson T., Kusunoki S., Kanazawa I., Tsuji S., van der Kooy D. Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling. Genes Dev. 2004, 18:1806-1811.
24. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 2000, 1:20-29.
25. Joksimovic M., Yun B.A., Kittappa R., Anderegg A.M., Chang W.W., Taketo M.M., McKay R.D., Awatramani R.B. Wnt antagonism of Shh facilitates midbrain floor plate neurogenesis. Nat. Neurosci. 2009, 12:125-131.
26. Keller G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev. 2005, 19:1129-1155.
27. Kittappa R., Chang W.W., Awatramani R.B., McKay R.D. The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age. PLoS Biol. 2007, 5:e325.
28. 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.
29. Lei Q., Jeong Y., Misra K., Li S., Zelman A.K., Epstein D.J., Matise M.P. Wnt signaling inhibitors regulate the transcriptional response to morphogenetic Shh-Gli signaling in the neural tube. Dev. Cell 2006, 11:325-337.
30. Li X.J., Du Z.W., Zarnowska E.D., Pankratz M., Hansen L.O., Pearce R.A., Zhang S.C. Specification of motoneurons from human embryonic stem cells. Nat. Biotechnol. 2005, 23:215-221.
31. Lie D.C., Dziewczapolski G., Willhoite A.R., Kaspar B.K., Shults C.W., Gage F.H. The adult substantia nigra contains progenitor cells with neurogenic potential. J. Neurosci. 2002, 22:6639-6649.
32. Lin W., Metzakopian E., Mavromatakis Y.E., Gao N., Balaskas N., Sasaki H., Briscoe J., Whitsett J.A., Goulding M., Kaestner K.H., Ang S.L. Foxa1 and Foxa2 function both upstream of and cooperatively with Lmx1a and Lmx1b in a feedforward loop promoting mesodiencephalic dopaminergic neuron development. Dev. Biol. 2009, 333:386-396.
33. Lupo G., Harris W.A., Lewis K.E. Mechanisms of ventral patterning in the vertebrate nervous system. Nat. Rev. Neurosci. 2006, 7:103-114.
34. Martynoga B., Morrison H., Price D.J., Mason J.O. Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev. Biol. 2005, 283:113-127.
35. Matsunaga E., Araki I., Nakamura H. Pax6 defines the di-mesencephalic boundary by repressing En1 and Pax2. Development 2000, 127:2357-2365.
36. Na E., McCarthy M., Neyt C., Lai E., Fishell G. Telencephalic progenitors maintain anteroposterior identities cell autonomously. Curr. Biol. 1998, 8:987-990.
37. Nakatani T., Kumai M., Mizuhara E., Minaki Y., Ono Y. Lmx1a and Lmx1b cooperate with Foxa2 to coordinate the specification of dopaminergic neurons and control of floor plate cell differentiation in the developing mesencephalon. Dev. Biol. 2010, 339:101-113.
38. Nakatani T., Minaki Y., Kumai M., Ono Y. Helt determines GABAergic over glutamatergic neuronal fate by repressing Ngn genes in the developing mesencephalon. Development 2007, 134:2783-2793.
39. Nery S., Fishell G., Corbin J.G. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 2002, 5:1279-1287.
40. Nikoletopoulou V., Plachta N., Allen N.D., Pinto L., Gotz M., Barde Y.A. Neurotrophin receptor-mediated death of misspecified neurons generated from embryonic stem cells lacking Pax6. Cell Stem Cell 2007, 1:529-540.
41. Olsson M., Campbell K., Turnbull D.H. Specification of mouse telencephalic and mid-hindbrain progenitors following heterotopic ultrasound-guided embryonic transplantation. Neuron 1997, 19:761-772.
42. Ono Y., Nakatani T., Sakamoto Y., Mizuhara E., Minaki Y., Kumai M., Hamaguchi A., Nishimura M., Inoue Y., Hayashi H., Takahashi J., Imai T. Differences in neurogenic potential in floor plate cells along an anteroposterior location: midbrain dopaminergic neurons originate from mesencephalic floor plate cells. Development 2007, 134:3213-3225.
43. 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.
44. Parrish-Aungst S., Shipley M.T., Erdelyi F., Szabo G., Puche A.C. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J. Comp. Neurol. 2007, 501:825-836.
45. Placzek M., Briscoe J. The floor plate: multiple cells, multiple signals. Nat. Rev. Neurosci. 2005, 6:230-240.
46. Qiu M., Shimamura K., Sussel L., Chen S., Rubenstein J.L. Control of anteroposterior and dorsoventral domains of Nkx-6.1 gene expression relative to other Nkx genes during vertebrate CNS development. Mech. Dev. 1998, 72:77-88.
47. Rathjen J., Rathjen P.D. Mouse ES cells: experimental exploitation of pluripotent differentiation potential. Curr. Opin. Genet. Dev. 2001, 11:587-594.
48. Shimamura K., Rubenstein J.L. Inductive interactions direct early regionalization of the mouse forebrain. Development 1997, 124:2709-2718.
49. Tao W., Lai E. Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 1992, 8:957-966.
50. Tao W., Lai E. Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 1992, 8:957-966.
51. Watanabe K., Kamiya D., Nishiyama A., Katayama T., Nozaki S., Kawasaki H., Watanabe Y., Mizuseki K., Sasai Y. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat. Neurosci. 2005, 8:288-296.
52. Wichterle H., Lieberam I., Porter J.A., Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002, 110:385-397.
53. Wichterle H., Turnbull D.H., Nery S., Fishell G., Alvarez-Buylla A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 2001, 128:3759-3771.
54. Wood H.B., Episkopou V. Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech. Dev. 1999, 86:197-201.
55. Ye W., Shimamura K., Rubenstein J.L., Hynes M.A., Rosenthal A. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 1998, 93:755-766.
56. Young K.M., Fogarty M., Kessaris N., Richardson W.D. Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J. Neurosci. 2007, 27:8286-8296.