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Age-Dependent Inhibition of Neural Crest Migration by the Notochord Correlates with Alterations in the S103L Chondroitin Sulfate Proteoglycan

Pettway, Zoé and Domowicz, Miriam and Schwartz, Nancy B. and Bronner-Fraser, Marianne (1996) Age-Dependent Inhibition of Neural Crest Migration by the Notochord Correlates with Alterations in the S103L Chondroitin Sulfate Proteoglycan. Experimental Cell Research, 225 (1). pp. 195-206. ISSN 0014-4827. https://resolver.caltech.edu/CaltechAUTHORS:20160323-081758861

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Abstract

In avian embryos, the notochord inhibits neural crest migration, resulting in the absence of neural crest cells from the perinotochordal space. Here, we test whether temporal changes in the ability of the notochord to inhibit neural crest migration correlate with alterations in the S103L chondroitin sulfate proteoglycan (CSPG). Because CSPGs are abundant in the perinotochordal space and the inhibitory effects of the notochord are chondroitinase sensitive bothin vivoandin vitro,we examined the distribution and biochemical nature of a large CSPG whose core protein is recognized by the S103L antibody. The S103L CSPG is specific to the perinotochordal space during the course of neural crest migration and codistributes with the HNK-1 carbohydrate. Biochemical characterization reveals that the S103L CSPG bears the HNK-1 epitope and is the only HNK-1 immunoreactive proteoglycan present around the notochord at these stages. Following neural crest migration, the S103L CSPG staining is maintained in the perinotochordal region and also is expressed later in cartilage. In 4-day-old embryos, however, the S103L CSPG undergoes a reduction of HNK-1 immunoreactivity. To examine the temporal nature of the notochord's inhibitory ability, we assayed the effects on neural crest migration of grafting notochords from 2- to 5-day-old donor quail embryos into 2-day-old host chick embryos. Donor notochords from 2- to 3-day-old embryos inhibit neural crest cell migration, whereas the degree of inhibition is reduced or absent when notochords are derived from ≥4-day-old donors. This suggests that older notochords lose their inhibitory ability. Interestingly, preincubation of younger notochords with the HNK-1 antibody blocks the inhibitory effect, suggesting that glycosylation of the perinotochordal matrix may be important. The time when the notochord loses its inhibitory ability as assessed by ourin vivografting assay correlates with the biochemical and immunocytochemical changes in the notochordal S103L antigen. These data suggest that a species of S103L CSPG, which is expressed by the early notochord and bears the HNK-1 epitope, may be important for the inhibition of neural crest migration.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1006/excr.1996.0170DOIArticle
http://www.sciencedirect.com/science/article/pii/S0014482796901706PublisherArticle
http://www.ncbi.nlm.nih.gov/pubmed/8635512PubMed CentralArticle
ORCID:
AuthorORCID
Bronner-Fraser, Marianne0000-0003-4274-1862
Additional Information:© 1996 Academic Press, Inc. Received December 18, 1995. Revised version received March 1, 1996. We thank Judith Henry for embryo dissection and Dr. Catherine Krull for helpful comments on the manuscript. This work was supported by AR-19622 and HD-09402 to N.B.S. and HD-15527, DE 10066, and a grant from the Muscular Dystrophy Foundation to M.B.F.
Funders:
Funding AgencyGrant Number
U.S. Public Health Service (USPHS)AR-19622
U.S. Public Health Service (USPHS)HD-09402
U.S. Public Health Service (USPHS)HD-15527
U.S. Public Health Service (USPHS)DE 10066
Muscular Dystrophy FoundationUNSPECIFIED
Issue or Number:1
Record Number:CaltechAUTHORS:20160323-081758861
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160323-081758861
Official Citation:Zoé Pettway, Miriam Domowicz, Nancy B. Schwartz, Marianne Bronner-Fraser, Age-Dependent Inhibition of Neural Crest Migration by the Notochord Correlates with Alterations in the S103L Chondroitin Sulfate Proteoglycan, Experimental Cell Research, Volume 225, Issue 1, 25 May 1996, Pages 195-206, ISSN 0014-4827, http://dx.doi.org/10.1006/excr.1996.0170. (http://www.sciencedirect.com/science/article/pii/S0014482796901706)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:65606
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:30 Mar 2016 23:34
Last Modified:03 Oct 2019 09:48

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