Differences in neuronal differentiation between the transient cranial (Frorieps') and normal dorsal root ganglia

Camila Avivi; Sheng Cui; Shlomo Goren; Ronald S. Goldstein

doi:10.1016/s0165-3806(02)00272-9

Differences in neuronal differentiation between the transient cranial (Frorieps') and normal dorsal root ganglia

Camila Avivi, Sheng Cui, Shlomo Goren, Ronald S. Goldstein

The Mina and Everard Goodman Faculty of Life Sciences

Research output: Contribution to journal › Article › peer-review

10 Scopus citations

Abstract

The Frorieps' ganglia are dorsal root ganglia (DRG) that form, grow slowly compared to normal DRG, and then degenerate during normal embryonic development of amniotes. Their fate has been shown to be regulated by the Hox family and other genes involved in pattern formation, and by the mesodermal microenvironment of the cranial somites in which they develop. Neurons are known to differentiate within the Frorieps' DRG in the course of their short life span. In this study, we compared several aspects of neural differentiation between the longest-lived Frorieps' ganglia, DRG2, and normal trunk DRG in chick embryos. The expression of transcription factor Islet-1 and the RNA-binding protein Hu differ between normal and Frorieps' DRG at St. 23 (embryonic day 4). Islet-1 is expressed in a higher proportion of cells in DRG2 than DRG5, suggesting that cells in DRG2 differentiate more rapidly into neurons than in normal DRG. This molecular difference appears at the same developmental stage as overt morphological differences between DRG2 and normal DRG. Other LIM-homeobox proteins (Lim-1, -2 and -3 and Islet-2) are not expressed either in normal or Frorieps' DRG at early stages of development. Somite-grafting experiments reveal that the increased proportion of Isl-1⁺ in DRG2 is due to the special microenvironment of the cranial somites. In contrast to Islet-1, the Hu antigen is expressed in a slightly lower proportion of cells in DRG2 at St. 23. At St. 28, there is a significant population of neurons in DRG2 that are Isl-1⁺/Hu^-. Since Islet-1 is normally expressed before Hu in DRG cells, it is possible that the reduced growth rate of the DRG2 ganglion may partially result from the inability of precociously differentiating Islet-1⁺ neurons to further mature, as reflected by Hu antigen expression. In contrast to the neuronal markers examined, the satellite cell marker 7B3 is expressed at similar levels in DRG2 and DRG5.

Original language	English
Pages (from-to)	19-28
Number of pages	10
Journal	Developmental Brain Research
Volume	135
Issue number	1-2
DOIs	https://doi.org/10.1016/s0165-3806(02)00272-9
State	Published - 30 Apr 2002

Bibliographical note

Funding Information:
This work was supported by grants from the Dysautonomia Foundation Inc., The Aviv Fund for Neuroscience Research and the Health Science Center at Bar-Ilan University. S.C. was supported, in part, by a Kort Israel–China friendship fellowship. We thank Jim Weston for his very generous gift of monoclonal antibody 7B3. Monoclonal antibodies 40.2D6 4F2, 67, 4E12, 51, 4H9 and QCPN were developed by Thomas Jessel and B&J Carlson, respectively, and obtained from the Developmental Studies Hybridoma Bank established under the auspices of the NICHD and maintained by the Department of Biological Sciences, University of Iowa, Iowa City, IA 52242, USA. Monoclonal antibody anti-Hu Mab 16A11 was purchased from the University of Oregon monoclonal antibody facility. We are grateful for critical reading of the manuscript by Drs. Chaya Kalcheim and Shelley Schwarzbaum.

Funding

This work was supported by grants from the Dysautonomia Foundation Inc., The Aviv Fund for Neuroscience Research and the Health Science Center at Bar-Ilan University. S.C. was supported, in part, by a Kort Israel–China friendship fellowship. We thank Jim Weston for his very generous gift of monoclonal antibody 7B3. Monoclonal antibodies 40.2D6 4F2, 67, 4E12, 51, 4H9 and QCPN were developed by Thomas Jessel and B&J Carlson, respectively, and obtained from the Developmental Studies Hybridoma Bank established under the auspices of the NICHD and maintained by the Department of Biological Sciences, University of Iowa, Iowa City, IA 52242, USA. Monoclonal antibody anti-Hu Mab 16A11 was purchased from the University of Oregon monoclonal antibody facility. We are grateful for critical reading of the manuscript by Drs. Chaya Kalcheim and Shelley Schwarzbaum.

Funders	Funder number
Health Science Center at Bar-Ilan University
Kort Israel–China
Dysautonomia Foundation

Keywords

DRG
Differentation
Hu
Islet-1
Neurodegeneration

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10.1016/s0165-3806(02)00272-9

Cite this

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title = "Differences in neuronal differentiation between the transient cranial (Frorieps') and normal dorsal root ganglia",

abstract = "The Frorieps' ganglia are dorsal root ganglia (DRG) that form, grow slowly compared to normal DRG, and then degenerate during normal embryonic development of amniotes. Their fate has been shown to be regulated by the Hox family and other genes involved in pattern formation, and by the mesodermal microenvironment of the cranial somites in which they develop. Neurons are known to differentiate within the Frorieps' DRG in the course of their short life span. In this study, we compared several aspects of neural differentiation between the longest-lived Frorieps' ganglia, DRG2, and normal trunk DRG in chick embryos. The expression of transcription factor Islet-1 and the RNA-binding protein Hu differ between normal and Frorieps' DRG at St. 23 (embryonic day 4). Islet-1 is expressed in a higher proportion of cells in DRG2 than DRG5, suggesting that cells in DRG2 differentiate more rapidly into neurons than in normal DRG. This molecular difference appears at the same developmental stage as overt morphological differences between DRG2 and normal DRG. Other LIM-homeobox proteins (Lim-1, -2 and -3 and Islet-2) are not expressed either in normal or Frorieps' DRG at early stages of development. Somite-grafting experiments reveal that the increased proportion of Isl-1+ in DRG2 is due to the special microenvironment of the cranial somites. In contrast to Islet-1, the Hu antigen is expressed in a slightly lower proportion of cells in DRG2 at St. 23. At St. 28, there is a significant population of neurons in DRG2 that are Isl-1+/Hu-. Since Islet-1 is normally expressed before Hu in DRG cells, it is possible that the reduced growth rate of the DRG2 ganglion may partially result from the inability of precociously differentiating Islet-1+ neurons to further mature, as reflected by Hu antigen expression. In contrast to the neuronal markers examined, the satellite cell marker 7B3 is expressed at similar levels in DRG2 and DRG5.",

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note = "Funding Information: This work was supported by grants from the Dysautonomia Foundation Inc., The Aviv Fund for Neuroscience Research and the Health Science Center at Bar-Ilan University. S.C. was supported, in part, by a Kort Israel–China friendship fellowship. We thank Jim Weston for his very generous gift of monoclonal antibody 7B3. Monoclonal antibodies 40.2D6 4F2, 67, 4E12, 51, 4H9 and QCPN were developed by Thomas Jessel and B&J Carlson, respectively, and obtained from the Developmental Studies Hybridoma Bank established under the auspices of the NICHD and maintained by the Department of Biological Sciences, University of Iowa, Iowa City, IA 52242, USA. Monoclonal antibody anti-Hu Mab 16A11 was purchased from the University of Oregon monoclonal antibody facility. We are grateful for critical reading of the manuscript by Drs. Chaya Kalcheim and Shelley Schwarzbaum.",

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N1 - Funding Information: This work was supported by grants from the Dysautonomia Foundation Inc., The Aviv Fund for Neuroscience Research and the Health Science Center at Bar-Ilan University. S.C. was supported, in part, by a Kort Israel–China friendship fellowship. We thank Jim Weston for his very generous gift of monoclonal antibody 7B3. Monoclonal antibodies 40.2D6 4F2, 67, 4E12, 51, 4H9 and QCPN were developed by Thomas Jessel and B&J Carlson, respectively, and obtained from the Developmental Studies Hybridoma Bank established under the auspices of the NICHD and maintained by the Department of Biological Sciences, University of Iowa, Iowa City, IA 52242, USA. Monoclonal antibody anti-Hu Mab 16A11 was purchased from the University of Oregon monoclonal antibody facility. We are grateful for critical reading of the manuscript by Drs. Chaya Kalcheim and Shelley Schwarzbaum.

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N2 - The Frorieps' ganglia are dorsal root ganglia (DRG) that form, grow slowly compared to normal DRG, and then degenerate during normal embryonic development of amniotes. Their fate has been shown to be regulated by the Hox family and other genes involved in pattern formation, and by the mesodermal microenvironment of the cranial somites in which they develop. Neurons are known to differentiate within the Frorieps' DRG in the course of their short life span. In this study, we compared several aspects of neural differentiation between the longest-lived Frorieps' ganglia, DRG2, and normal trunk DRG in chick embryos. The expression of transcription factor Islet-1 and the RNA-binding protein Hu differ between normal and Frorieps' DRG at St. 23 (embryonic day 4). Islet-1 is expressed in a higher proportion of cells in DRG2 than DRG5, suggesting that cells in DRG2 differentiate more rapidly into neurons than in normal DRG. This molecular difference appears at the same developmental stage as overt morphological differences between DRG2 and normal DRG. Other LIM-homeobox proteins (Lim-1, -2 and -3 and Islet-2) are not expressed either in normal or Frorieps' DRG at early stages of development. Somite-grafting experiments reveal that the increased proportion of Isl-1+ in DRG2 is due to the special microenvironment of the cranial somites. In contrast to Islet-1, the Hu antigen is expressed in a slightly lower proportion of cells in DRG2 at St. 23. At St. 28, there is a significant population of neurons in DRG2 that are Isl-1+/Hu-. Since Islet-1 is normally expressed before Hu in DRG cells, it is possible that the reduced growth rate of the DRG2 ganglion may partially result from the inability of precociously differentiating Islet-1+ neurons to further mature, as reflected by Hu antigen expression. In contrast to the neuronal markers examined, the satellite cell marker 7B3 is expressed at similar levels in DRG2 and DRG5.

AB - The Frorieps' ganglia are dorsal root ganglia (DRG) that form, grow slowly compared to normal DRG, and then degenerate during normal embryonic development of amniotes. Their fate has been shown to be regulated by the Hox family and other genes involved in pattern formation, and by the mesodermal microenvironment of the cranial somites in which they develop. Neurons are known to differentiate within the Frorieps' DRG in the course of their short life span. In this study, we compared several aspects of neural differentiation between the longest-lived Frorieps' ganglia, DRG2, and normal trunk DRG in chick embryos. The expression of transcription factor Islet-1 and the RNA-binding protein Hu differ between normal and Frorieps' DRG at St. 23 (embryonic day 4). Islet-1 is expressed in a higher proportion of cells in DRG2 than DRG5, suggesting that cells in DRG2 differentiate more rapidly into neurons than in normal DRG. This molecular difference appears at the same developmental stage as overt morphological differences between DRG2 and normal DRG. Other LIM-homeobox proteins (Lim-1, -2 and -3 and Islet-2) are not expressed either in normal or Frorieps' DRG at early stages of development. Somite-grafting experiments reveal that the increased proportion of Isl-1+ in DRG2 is due to the special microenvironment of the cranial somites. In contrast to Islet-1, the Hu antigen is expressed in a slightly lower proportion of cells in DRG2 at St. 23. At St. 28, there is a significant population of neurons in DRG2 that are Isl-1+/Hu-. Since Islet-1 is normally expressed before Hu in DRG cells, it is possible that the reduced growth rate of the DRG2 ganglion may partially result from the inability of precociously differentiating Islet-1+ neurons to further mature, as reflected by Hu antigen expression. In contrast to the neuronal markers examined, the satellite cell marker 7B3 is expressed at similar levels in DRG2 and DRG5.

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Differences in neuronal differentiation between the transient cranial (Frorieps') and normal dorsal root ganglia

Abstract

Bibliographical note

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Keywords

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