P0 and PMP22 mark a multipotent neural crest-derived cell type that displays community effects in response to TGF-β family factors

Development

Volumn 126, Issue 17, 1999, Pages 3781-3794

  Hagedorn, Lilian ^a   Suter, Ueli ^a   Sommer, Lukas ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Community effect; Dorsal root ganglia; Multipotency; Neural crest; Peripheral myelin protein 22; Protein zero; TGF factors

Indexed keywords

CELL MARKER; MYELIN PROTEIN; NERVE PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL TYPE; CONTROLLED STUDY; GLIA CELL; MYELINATION; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; SPINAL GANGLION; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; GANGLIA, SPINAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MODELS, NEUROLOGICAL; MUTATION; MYELIN PROTEINS; NERVE TISSUE PROTEINS; NEURAL CREST; PERIPHERAL NERVOUS SYSTEM; RATS; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 0032871477     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (86)

1. Anderson, D. J. (1997). Cellular and molecular biology of neural crest cell lineage determination. Trends Genet. 13, 276-280.
2. Anderson, D. J., Groves, A., Lo, L., Ma, Q., Rao, M., Shah, N. M. and Sommer, L. (1997). Cell lineage determination and the control of neuronal identity in the neural crest. Cold Spring Harb. Symp. Quant. Biol. 62, 493-504.
3. Artinger, K. B. and Bronner-Fraser, M. (1992). Partial restriction in the developmental potential of late emigrating avian neural crest cells. Dev. Biol. 149, 149-157.
4. Attisano, L. and Wrana, J. L. (1998). Mads and Smads in TGF beta signalling. Curr. Opin. Cell Biol. 10, 188-194.
5. Baechner, D., Liehr, T., Hameister, H., Altenberger, H., Grehl, H., Suter, U. and Rautenstrauss, B. (1995). Widespread expression of the peripheral myelin protein-22 gene (PMP22) in neural and non-neural tissues during murine development. J. Neurosci. Res. 42, 733-741.
6. Baroffio, A., Dupin, E. and LeDouarin, N. M. (1988). Clone-forming ability and differentiation potential of migratory neural crest cells. Proc. Natl. Acad. Sci. USA 85, 5325-5329.
7. Bhattacharyya, A., Frank, E., Ratner, N. and Brackenbury, R. (1991). Po is an early marker of the Schwann cell lineage in chickens. Neuron 7, 831-844.
8. Birren, S. J., Lo, L. C. and Anderson, D. J. (1993). Sympathetic neurons undergo a developmental switch in trophic dependence. Development 119, 597-610.
9. Bitgood, M. J. and McMahon, A. P. (1995). Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172, 126-138.
10. Bosse, F., Zoidl, G., Wilms, S., Gillen, C. P., Kuhn, H. G. and Muller, H. W. (1994). Differential expression of two mRNA species indicates a dual function of the peripheral myelin protein PMP22 in cell growth and myelination. J. Neurosci. Res. 37, 529-537.
11. Bronner-Fraser, M. and Fraser, S. (1988). Cell lineage analysis shows multipotentiality of some avian neural crest cells. Nature 335, 161-164.
12. Burden, S. and Yarden, Y. (1997). Neuregulins and their receptors: a versatile signalling module in organogenesis and oncogenesis. Neuron 18, 847-855.
13. de Caestecker, M. P., Parks, W. T., Frank, C. J., Castagnino, P., Bottaro, D. P., Roberts, A. B. and Lechleider, R. J. (1998). Smad2 transduces common signals from receptor serine-threonine and tyrosine kinases. Genes Dev. 12, 1587-1592.
14. de Ferra, F., Engh, H., Hudson, L., Kamholz, J., Puckett, C., Molineaux, S. and Lazzarini, R. A. (1985). Alternative splicing accounts for the four forms of myelin basic protein. Cell 43, 721-727.
15. Dong, Z., Brennan, A., Liu, N., Yarden, Y., Lefkowitz, G., Mirsky, R. and Jessen, K. R. (1995). Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15, 585-596.
16. Duff, R. S., Langtimm, C. J., Richardson, M. K. and Sieber-Blum, M. (1991). In Vitro Clonal Analysis of Progenitor Cell Patterns in Dorsal Root and Sympathetic Ganglia of the Quail Embryo. Dev. Biol. 147, 451-459.
17. Edlund, T. and Jessell, T. M. (1999). Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 96, 211-224.
18. Fabbretti, E., Edomi, P., Brancolini, C. and Schneider, C. (1995). Apoptotic phenotype induced by overexpression of wild-type gas3/PMP22: its relation to the demyelinating peripheral neuropathy CMT1A. Genes Dev. 9, 1846-1856.
19. Flanders, K. C., Ludecke, G., Engels, S., Cissel, D. S., Roberts, A. B., Kondaiah, P., Lafyatis, R., Sporn, M. B. and Unsicker, K. (1991). Localization and actions of transforming growth factor-βs in the embryonic nervous system. Development 113, 183-191.
20. Frank, E. and Sanes, J. R. (1991). Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus. Development 111, 895-908.
21. Fraser, S. E. and Bronner-Fraser, M. E. (1991). Migrating neural crest cells in the trunk of the avian embryo are multipotent. Development 112, 913-920.
22. Gavrilovic, J., Brennan, A., Mirsky, R. and Jessen, K. R. (1995). Fibroblast growth factors and insulin growth factors combine to promote survival of rat Schwann cell precursors without induction of DNA synthesis. Eur. J. Neurosci. 7, 77-85.
23. Green, J. B., New, H. V. and Smith, J. C. (1992). Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm. Cell 71, 731-739.
24. Green, J. B. and Smith, J. C. (1990). Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347, 391-394.
25. Green, J. B., Smith, J. C. and Gerhart, J. C. (1994). Slow emergence of a multithreshold response to activin requires cell-contact-dependent sharpening but not prepattern. Development 120, 2271-2278.
26. Gurdon, J. B., Lemaire, P. and Kato, K. (1993). Community effects and related phenomena in development. Cell 75, 831-834.
27. Hall, A. K. and Landis, S. C. (1991). Early commitment of precursor cells from the rat superior cervical ganglion to neuronal or nonneuronal fates. Neuron 6, 741-752.
28. Harland, R. and Gerhart, J. (1997). Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 13, 611-667.
29. Heldin, C. H., Miyazono, K. and ten Dijke, P. (1997). TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
30. Henion, P. D. and Weston, J. A. (1997). Timing and pattern of cell fate restrictions in the neural crest lineage. Development 124, 4351-4359.
31. Heuckeroth, R. O., Lampe, P. A., Johnson, E. M. and Milbrandt, J. (1998). Neurturin and GDNF promote proliferation and survival of enteric neuron and glial progenitors in vitro. Dev. Biol. 200, 116-129.
32. Hogan, B. L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
33. Ito, K., Morita, T. and Sieber-Blum, M. (1993). In vitro clonal analysis of mouse neural crest development. Dev. Biol. 157, 517-525.
34. Kretzschmar, M., Doody, J. and Massague, J. (1997). Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389, 618-622.
35. Krishna, S., Maduzia, L. L. and Padgett, R. W. (1999). Specificity of TGFbeta signaling is conferred by distinct type I receptors and their associated SMAD proteins in Caenorhabditis elegans. Development 126, 251-260.
36. Landry, C. F., Ellison, J., Skinner, E. and Campagnoni, A. T. (1997). Golli-MBP proteins mark the earliest stages of fiber extension and terminal arboration in the mouse peripheral nervous system. J. Neurosci. Res. 50, 265-271.
37. Lahav, R., Dupin, E., Lecoin, L., Glavieux, C., Champeval, D., Ziller, C. and Le Douarin, N. M. (1998). Endothelin 3 selectively promotes survival and proliferation of neural crest-derived glial and melanocytic precursors in vitro. Proc. Natl. Acad. Sci. USA 95, 14214-14219.
38. Le Douarin, N. M. (1982). The Neural Crest. Cambridge, UK: Cambridge University Press.
39. Le Douarin, N. M. (1986). Cell line segregation during peripheral nervous system ontogeny. Science 231, 1515-1522.
40. Le Douarin, N. M. and Ziller, C. (1993). Plasticity in neural crest cell differentiation. Curr. Opin. Cell Biol. 5, 1036-1043.
41. Lechleider, R. J., de Caestecker, M. P., Dehejia, A., Polymeropoulos, M. H. and Roberts, A. B. (1996). Serine phosphorylation, chromosomal localization, and transforming growth factor-beta signal transduction by human bsp-1. J. Biol. Chem. 271, 17617-17620.
42. Lee, M., Brennan, A., Blanchard, A., Zoidl, G., Dong, Z., Tabernero, A., Zoidl, C., Dent, M. A., Jessen, K. R. and Mirsky, R. (1997). P0 is constitutively expressed in the rat neural crest and embryonic nerves and is negatively and positively regulated by axons to generate non-myelin-forming and myelin-forming Schwann cells, respectively. Mol. Cell. Neurosci. 8, 336-350.
43. Lemke, G. and Axel, R. (1985). Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin. Cell 40, 501-508.
44. Lo, L. and Anderson, D. J. (1995). Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. Neuron 15, 527-539.
45. Lo, L., Sommer, L. and Anderson, D. J. (1997). MASH1 maintains competence for BMP2-induced neuronal differentiation in post-migratory neural crest cells. Curr. Biol. 7, 440-450.
46. Manfioletti, G., Ruaro, M. E., Del Sal, G., Philipson, L. and Schneider, C. (1990). A growth arrest-specific (gas) gene codes for a membrane protein. Mol. Cell. Biol. 10, 2924-2930.
47. Marchionni, M. A., Goodearl, A. D. J., Chen, M. S., Bermingham-McDonogh, O., Kirk, C., Hendricks, M., Danehy, F., Misumi, D., Sudhalter, J. and Kobayashi, K. (1993). Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362, 312-318.
48. Massague, J. (1996). TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 85, 947-950.
49. Meyer, D. and Birchmeier, C. (1995). Multiple essential functions of neuregulin in development. Nature 378, 386-390.
50. Millan, F. A., Denhez, F., Kondaiah, P. and Akhurst, R. J. (1991). Embryonic gene expression patterns of TGF β1, β2 and β3 suggest different developmental functions in vivo. Development 111, 131-144.
51. Mirsky, R. and Jessen, K. R. (1996). Schwann cell development, differentiation and myelination. Curr. Opin. Neurobiol. 6, 89-96.
52. Morrison, S. J., White, P. M., Zock, C. and Anderson, D. J. (1999). Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96, 737-749.
53. Naef, R. and Suter, U. (1998). Many facets of the peripheral myelin protein PMP22 in myelination and disease. Microsc. Res. Tech. 41, 359-371.
54. Ockel, M., Lewin, G. R. and Barde, Y. A. (1996). In vivo effects of neurotrophin-3 during sensory neurogenesis. Development 122, 301-307.
55. Paratore, C., Suter, U. and Sommer, L. (1999). Embryonic gene expression resolved at the cellular level by fluorescence in situ hybridization. Histochem. Cell Biol. 111, 435-443.
56. Parmantier, E., Braun, C., Thomas, J. L., Peyron, F., Martinez, S. and Zalc, B. (1997). PMP-22 expression in the central nervous system of the embryonic mouse defines potential transverse segments and longitudinal columns. J. Comp. Neurol. 378, 159-172.
57. Parmantier, E., Cabon, F., Braun, C., D'Urso, D., Muller, H. W. and Zalc, B. (1995). Peripheral myelin protein-22 is expressed in rat and mouse brain and spinal cord motoneurons. Eur. J. Neurosci. 7, 1080-1088.
58. Raff, M. C. (1992). Social controls on cell survival and cell death. Nature 356, 397-400.
59. Reid, K., Turnley, A. M., Maxwell, G. D., Kurihara, Y., Kurihara, H., Bartlett, P. F. and Murphy, M. (1996). Multiple roles for endothelin in melanocyte development: regulation of progenitor number and stimulation of differentiation. Development 122, 3911-3919.
60. Richardson, M. K. and Sieber-Blum, M. (1993). Pluripotent neural crest cells in the developing skin of the quail embryo. Dev. Biol. 157, 348-358.
61. Sextier-Sainte-Claire Deville, F., Ziller, C. and Le Douarin, N. (1992). Developmental potentialities of cells derived from the truncal neural crest in clonal cultures. Brain Res. Dev. Brain Res. 66, 1-10.
62. Shah, N., Groves, A. and Anderson, D. J. (1996). Alternative neural crest cell fates are instructively promoted by TGFß superfamily members. Cell 85, 331-343.
63. Shah, N. M. and Anderson, D. J. (1997). Integration of multiple instructive cues by neural crest stem cells reveals cell-intrinsic biases in relative growth factor responsiveness. Proc. Natl. Acad. Sci. USA 94, 11369-11374.
64. Shah, N. M., Marchionni, M. A., Isaacs, I., Stroobant, P. and Anderson, D. J. (1994). Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77, 349-360.
65. Sieber-Blum. M. and Cohen, A. (1980). Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in vitro in the absence of non-neural crest cells. Dev. Biol. 80, 96-106.
66. Snipes, G. J., Suter, U., Welcher, A. A. and Shooter, E. M. (1992). Characterization of a novel peripheral nervous system myelin protein (PMP-22/SR13). J. Cell Biol. 117, 225-238.
67. Sommer, L., Ma, Q. and Anderson, D. J. (1996). Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell. Neurosci. 8, 221-241.
68. Sommer, L., Shah, N., Rao, M. and Anderson, D. J. (1995). The cellular function of MASH1 in autonomic neurogenesis. Neuron 15, 1245-1258.
69. Sommer, L. and Suter, U. (1998). The glycoprotein P0 in peripheral gliogenesis. Cell Tissue Res. 292, 11-16.
70. Spreyer, P., Kuhn, G., Hanemann, C. O., Gillen, C., Schaal, H., Kuhn, R., Lemke, G. and Muller, H. W. (1991). Axon-regulated expression of a Schwann cell transcript that is homologous to a 'growth arrest-specific' gene. EMBO J. 10, 3661-3668.
71. Stemple, D. L. and Anderson, D. J. (1992). Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71, 973-985.
72. Suter, U. (1997). Myelin: keeping nerves well wrapped up. Current Biology 7, R21-R23.
73. Suter, U. and Snipes, G. J. (1995). Biology and genetics of hereditary motor and sensory neuropathies. Annu. Rev. Neurosci. 18, 45-75.
74. Thoenen, H. (1991). The changing scene of neurotrophic factors. Trends in Neurosci. 14, 165-170.
75. Topper, J. N., Cai, J., Qiu, Y., Anderson, K. R., Xu, Y. Y., Deeds, J. D., Feeley, R., Gimeno, C. J., Woolf, E. A., Tayber, O., Mays, G. G., Sampson, B. A., Schoen, F. J., Gimbrone, M. A., Jr. and Falb, D. (1997). Vascular MADs: two novel MAD-related genes selectively inducible by flow in human vascular endothelium. Proc. Natl. Acad. Sci. USA 94, 9314-9319.
76. Weinstein, D. C. and Hemmati-Brivanlou, A. (1997). Neural induction in Xenopus laevis: evidence for the default model. Curr. Opin. Neurobiol. 7, 7-12.
77. Welcher, A. A., Suter, U., De Leon, M., Snipes, G. J. and Shooter, E. M. (1991). A myelin protein is encoded by the homologue of a growth arrest-specific gene. Proc. Natl. Acad. Sci. USA 88, 7195-7199.
78. Whitman, M. (1998). Smads and early developmental signaling by the TGFbeta superfamily. Genes Dev. 12, 2445-2462.
79. Wilson, P. A. and Melton, D. A. (1994). Mesodermal patterning by an inducer gradient depends on secondary cell-cell communication. Curr. Biol. 4, 676-686.
80. Yamaguchi, K., Nagai, S., Ninomiya-Tsuji, J., Nishita, M., Tamai, K., Irie, K., Ueno, N., Nishida, E., Shibuya, H. and Matsumoto, K. (1999). XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1-TAK1 in the BMP signaling pathway. EMBO J. 18, 179-187.
81. Yamaguchi, K., Shirakabe, K., Shibuya, H., Irie, K., Oishi, I., Ueno, N., Taniguchi, T., Nishida, E. and Matsumoto, K. (1995). Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 270, 2008-2011.
82. Yingling, J. M., Das, P., Savage, C., Zhang, M., Padgett, R. W. and Wang, X. F. (1996). Mammalian dwarfins are phosphorylated in response to transforming growth factor beta and are implicated in control of cell growth. Proc. Natl. Acad. Sci. USA 93, 8940-8944.
83. Zhang, S.-M., Marsh, R., Ratner, N. and Brackenbury, R. (1995). Myelin glycoprotein P0 is expressed at early stages of chicken and rat embryogenesis. J. Neurosci. Res. 40, 241-250.
84. Zoidl, G., Blass-Kampmann, S., D'Urso, D., Schmalenbach, C. and Muller, H. W. (1995). Retroviral-mediated gene transfer of the peripheral myelin protein PMP22 in Schwann cells: modulation of cell growth. EMBO J. 14, 1122-1128.
85. Zoidl, G., D'Urso, D., Blass-Kampmann, S., Schmalenbach, C., Kuhn, R. and Muller, H. W. (1997). Influence of elevated expression of rat wild-type PMP22 and its mutant PMP22Trembler on cell growth of NIH3T3 fibroblasts. Cell Tissue Res. 287, 459-470.
86. Zou, H., Wieser, R., Massague, J. and Niswander, L. (1997). Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev 11, 2191-2203.