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Spatial and temporal changes in the distribution of proteoglycans during avian neural crest development

Perris, Roberto and Krotoski, Danuta and Lallier, Thomas and Domingo, Carmen and Sorrell, Michael and Bronner-Fraser, Marianne (1991) Spatial and temporal changes in the distribution of proteoglycans during avian neural crest development. Development, 111 (2). pp. 583-599. ISSN 0950-1991.

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In this study, we describe the distribution of various classes of proteoglycans and their potential matrix ligand, hyaluronan, during neural crest development in the trunk region of the chicken embryo. Different types of chondroitin and keratan sulfate proteoglycans were recognized using a panel of monoclonal antibodies produced against specific epitopes on their glycosaminoglycan chains. A heparan sulfate proteoglycan was identified by an antibody against its core protein. The distribution of hyaluronan was mapped using a biotinylated fragment that corresponds to the hyaluronan-binding region of cartilage proteoglycans. Four major patterns of proteoglycan immunoreactivity were observed. (1) Chondroitin-6-sulfate-rich proteoglycans and certain keratin sulfate proteoglycans were absent from regions containing migrating neural crest cells, but were present in interstitial matrices and basement membranes along prospective migratory pathways such as the ventral portion of the sclerotome. Although initially distributed uniformly along the rostrocaudal extent of the sclerotome, these proteoglycans became rearranged to the caudal portion of the sclerotome with progressive migration of neural crest cells through the rostral sclerotome and their aggregation into peripheral ganglia. (2) A subset of chondroitin/keratan sulfate proteoglycans bearing primarily unsulfated chondroitin chains was observed exclusively in regions where neural crest cells were absent or delayed from entering, such as the perinotochordal and subepidermal spaces. (3) A subset of chondroitin/keratan sulfate proteoglycans was restricted to the perinotochordal region and, following gangliogenesis, was arranged in a metameric pattern corresponding to the sites where presumptive vertebral arches form. (4) Certain keratan sulfate proteoglycans and a heparan sulfate proteoglycan were observed in basement membranes and in an interstitial matrix uniformly distributed along the rostrocaudal extent of the sclerotome. After gangliogenesis, the neural crest-derived dorsal root and sympathetic ganglia contained both these proteoglycan types, but were essentially free of other chondroitin/keratan-proteoglycan subsets. Hyaluronan generally colocalized with the first set of proteoglycans, but also was concentrated around migrating neural crest cells and was reduced in neural crest-derived ganglia. These observations demonstrate that proteoglycans have diverse and dynamic distributions during times of neural crest development and chondrogenesis of the presumptive vertebrae. In general, chondroitin/keratan sulfate proteoglycans are abundant in regions where neural crest cells are absent, and their segmental distribution inversely correlates with that of neural crest-derived ganglia.

Item Type:Article
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URLURL TypeDescription
Lallier, Thomas0000-0001-6577-6676
Bronner-Fraser, Marianne0000-0003-4274-1862
Additional Information:© 1991 Company of Biologists Limited. Accepted 23 November 1990. We thank Drs Bruce Caterson and Douglas Fambrough for providing various antibodies, and Dr Toward Laurent for donation of the purified proteoglycan fragment. Kristie Bruk, Mary Flowers, and Michael Artinger are thanked for their excellent technical assistance. This study was supported by NIH grant USPHS HD-15527 and the Muscular Dystrophy Association. MB-F is a Sloan Research Fellow.
Funding AgencyGrant Number
Muscular Dystrophy AssociationUNSPECIFIED
Alfred P. Sloan FoundationUNSPECIFIED
Subject Keywords:proteoglycans, hyaluronan, neural crest, avian embryo, cell migration, extracellular matrix
Issue or Number:2
Record Number:CaltechAUTHORS:20120419-110230403
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Official Citation:R. Perris, D. Krotoski, T. Lallier, C. Domingo, J.M. Sorrell, and M. Bronner-Fraser Spatial and temporal changes in the distribution of proteoglycans during avian neural crest development Development 1991 111:583-599
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:30198
Deposited By: Ruth Sustaita
Deposited On:19 Apr 2012 18:22
Last Modified:23 Dec 2022 17:06

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