Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo

Development

Volumn 133, Issue 4, 2006, Pages 581-590

  Wu, Sen ^a   Wu, Yuanyuan ^a   Capecchi, Mario R ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Cell ablation; Diphtheria toxin; Glia; Motoneurons; Oligodendrocytes

Indexed keywords

HELIX LOOP HELIX PROTEIN; OLIG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CELL ISOLATION; CELL KILLING; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOTONEURON; MOUSE; NEURAL STEM CELL; NEUROEPITHELIUM; NONHUMAN; OLIGODENDROGLIA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINEAGE; CLONING, MOLECULAR; DIPHTHERIA TOXIN; EMBRYO; MICE; MICE, KNOCKOUT; MODELS, GENETIC; MOTOR NEURONS; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; SPINAL CORD; STEM CELLS;

ANIMALIA;

EID: 33645088427     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02236     Document Type: Article

References (43)

1. Alvarez-Buylla, A., Garcia-Verdugo, J. M. and Tramontin, A. D. (2001). A unified hypothesis on the lineage of neural stem cells. Nat. Rev Neurosci. 2, 287-293.
2. Anderson, D. J. (2001). Stem cells and pattern formation in the nervous system: the possible versus the actual. Neuron 30, 19-35.
3. Awatramani, R., Soriano, P., Mai, J. J. and Dymecki, S. (2001). An Flp indicator mouse expressing alkaline phosphatase from the ROSA26 locus. Nat. Genet. 29, 257-259.
4. Bignami, A., Eng, L. F., Dahl, D. and Uyeda, C. T. (1972). Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 43, 429-435.
5. Briscoe, J., Pierani, A., Jessell, T. M. and Ericson, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445.
6. Cai, J., Qi, Y., Hu, X., Tan, M., Liu, Z., Zhang, J., Li, Q., Sander, M. and Qiu, M. (2005). Generation of oligodendrocyte precursor cells from mouse dorsal spinal cord independent of nkx6 regulation and shh signaling. Neuron 45, 41-53.
7. Cepko, C. L., Austin, C. P., Yang, X., Alexiades, M. and Ezzeddine, D. (1996). Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. USA 93, 589-595.
8. Fogarty, M., Richardson, W. D. and Kessaris, N. (2005). A subset of oligodendrocytes generated from radial glia in the dorsal spinal cord. Development 132, 1951-1959.
9. Gabay, L., Lowell, S., Rubin, L. L. and Anderson, D. J. (2003). Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40, 485-499.
10. Gregori, N., Proschel, C., Noble, M. and Mayer-Proschel, M. (2002). The tripotential glial-restricted precursor (GRP) cell and glial development in the spinal cord: generation of bipotential oligodendrocyte-type-2 astrocyte progenitor cells and dorsal-ventral differences in GRP cell function. J. Neurosci. 22, 248-256.
11. Harfe, B. D., Scherz, P. J., Nissim, S., Tian, H., McMahon, A. P. and Tabin, C. J. (2004). Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528.
12. Leber, S. M., Breedlove, S. M. and Sanes, J. R. (1990). Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord. J. Neurosci. 10, 2451-2462.
13. Liu, Y. and Rao, M. (2003). Oligodendrocytes, GRPs and MNOPs. Trends Neurosci. 26, 410-412.
14. Liu, Y. and Rao, M. S. (2004). Olig genes are expressed in a heterogeneous population of precursor cells in the developing spinal cord. Glia 45, 67-74.
15. Liu, Y., Wu, Y., Lee, J. C., Xue, H., Pevny, L. H., Kaprielian, Z. and Rao, M. S. (2002). Oligodendrocyte and astrocyte development in rodents: an in situ and immunohistological analysis during embryonic development. Glia 40, 25-43.
16. Lu, Q. R., Yuk, D., Alberta, J. A., Zhu, Z., Pawlitzky, I., Chan, J., McMahon, A. P., Stiles, C. D. and Rowitch, D. H. (2000). Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317-329.
17. Lu, Q. R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C. D. and Rowitch, D. H. (2002). Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75-86.
18. Lyons, D. A., Guy, A. T. and Clarke, J. D. (2003). Monitoring neural progenitor fate through multiple rounds of division in an intact vertebrate brain. Development 130, 3427-3436.
19. Malatesta, P., Hack, M. A., Hartfuss, E., Kettenmann, H., Klinkert, W., Kirchhoff, F. and Gotz, M. (2003). Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37, 751-764.
20. Maxwell, F., Maxwell, I. H. and Glode, L. M. (1987). Cloning, sequence determination, and expression in transfected cells of the coding sequence for the tox 176 attenuated diphtheria toxin A chain. Mol. Cell. Biol. 7, 1576-1579.
21. Mayer-Proschel, M., Kalyani, A. J., Mujtaba, T. and Rao, M. S. (1997). Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 19, 773-785.
22. Mitamura, T., Higashiyama, S., Taniguchi, N., Klagsbrun, M. and Mekada, E. (1995). Diphtheria toxin binds to the epidermal growth factor (EGF)-like domain of human heparin-binding EGF-like growth factor/diphtheria toxin receptor and inhibits specifically its mitogenic activity. J. Biol. Chem. 270, 1015-1019.
23. Morimoto, H. and Bonavida, B. (1992). Diphtheria toxin- and Pseudomonas A toxin-mediated apoptosis. ADP ribosylation of elongation factor-2 is required for DNA fragmentation and cell lysis and synergy with tumor necrosis factor-alpha. J. Immunol. 149, 2089-2094.
24. Noble, M., Proschel, C. and Mayer-Proschel, M. (2004). Getting a GR(i)P on oligodendrocyte development. Dev. Biol. 265, 33-52.
25. Novitch, B. G., Chen, A. I. and Jessell, T. M. (2001). Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31, 773-789.
26. Pearson, B. J. and Doe, C. Q. (2004). Specification of temporal identity in the developing nervous system. Annu. Rev. Cell Dev. Biol. 20, 619-647.
27. Pringle, N. P. and Richardson, W. D. (1993). A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 117, 525-533.
28. Pringle, N. P., Yu, W. P., Howell, M., Colvin, J. S., Ornitz, D. M. and Richardson, W. D. (2003). Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 130, 93-102.
29. Qian, X., Shen, Q., Goderie, S. K., He, W., Capela, A., Davis, A. A. and Temple, S. (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.
30. Rao, M. S. and Mayer-Proschel, M. (1997). Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev. Biol. 188, 48-63.
31. Rao, M. S., Noble, M. and Mayer-Proschel, M. (1998). A tripotential glial precursor cell is present in the developing spinal cord. Proc. Natl. Acad. Sci. USA 95, 3996-4001.
32. Richardson, W. D., Smith, H. K., Sun, T., Pringle, N. P., Hall, A. and Woodruff, R. (2000). Oligodendrocyte lineage and the motor neuron connection. Glia 29, 136-142.
33. Rowitch, D. H., Lu, Q. R., Kessaris, N. and Richardson, W. D. (2002). An 'oligarchy' rules neural development. Trends Neurosci. 25, 417-422.
34. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
35. Srinivas, S., Watanabe, T., Lin, C. S., William, C. M., Tanabe, Y., Jessell, T. M. and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
36. Stiles, C. D. (2003). Lost in space: misregulated positional cues create tripotent neural progenitors in cell culture. Neuron 40, 447-449.
37. Takebayashi, H., Nabeshima, Y., Yoshida, S., Chisaka, O., Ikenaka, K. and Nabeshima, Y. (2002). The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr. Biol. 12, 1157-1163.
38. Vallstedt, A., Klos, J. M. and Ericson, J. (2005). Multiple dorsoventral origins of oligodendrocyte generation in the spinal cord and hindbrain. Neuron 45, 55-67.
39. Yamaizumi, M., Mekada, E., Uchida, T. and Okada, Y. (1978). One molecule of diphtheria toxin fragment A introduced into a cell can kill the cell. Cell 15, 245-250.
40. Yang, X., Arber, S., William, C., Li, L., Tanabe, Y., Jessell, T. M., Birchmeier, C. and Burden, S. J. (2001). Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30, 399-410.
41. Zhou, Q. and Anderson, D. J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73.
42. Zhou, Q., Wang, S. and Anderson, D. J. (2000). Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25, 331-343.
43. Zhou, Q., Choi, G. and Anderson, D. J. (2001). The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31, 791-807.