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Evolution of the vertebrate claudin gene family: insights from a basal vertebrate, the sea lamprey

Mukendi, Christian and Dean, Nicholas and Lala, Rushil and Smith, Jeramiah J. and Bronner, Marianne E. and Nikitina, Natalya V. (2016) Evolution of the vertebrate claudin gene family: insights from a basal vertebrate, the sea lamprey. International Journal of Developmental Biology, 60 (1-3). pp. 39-51. ISSN 0214-6282. http://resolver.caltech.edu/CaltechAUTHORS:20160601-081405569

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Abstract

Claudins are major constituents of tight junctions, contributing both to their intercellular sealing and selective permeability properties. While claudins and claudin-like molecules are present in some invertebrates, the association of claudins with tight junctions has been conclusively documented only in vertebrates. Here we report the sequencing, phylogenetic analysis and comprehensive spatiotemporal expression analysis of the entire claudin gene family in the basal extant vertebrate, the sea lamprey. Our results demonstrate that clear orthologues to about half of all mammalian claudins are present in the lamprey, suggesting that at least one round of whole genome duplication contributed to the diversification of this gene family. Expression analysis revealed that claudins are expressed in discrete and specific domains, many of which represent vertebrate-specific innovations, such as in cranial ectodermal placodes and the neural crest; whereas others represent structures characteristic of chordates, e.g. pronephros, notochord, somites, endostyle and pharyngeal arches. By comparing the embryonic expression of claudins in the lamprey to that of other vertebrates, we found that ancestral expression patterns were often preserved in higher vertebrates. Morpholino mediated loss of Cldn3b demonstrated a functional role for this protein in placode and pharyngeal arch morphogenesis. Taken together, our data provide novel insights into the origins and evolution of the claudin gene family and the significance of claudin proteins in the evolution of vertebrates.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1387/ijdb.150364nnDOIArticle
http://www.ijdb.ehu.es/web/paper.php?doi=150364nnPublisherArticle
ORCID:
AuthorORCID
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© 2016 UPV/EHU Press. Accepted: 18 February 2016. We thank Tatjana Sauka-Spengler for providing PmCldn3b, PmCldn8b and Pm Cldn19b clones, Thembekile Zwane for assistance with lamprey embryo collection and morpholino injection. This work is based on the research supported wholly by the National Research Foundation of South Africa (Grant reference number 80717 to NN and grantholder-linked student funding to CK and RL). The grantholder acknowledges that opinions, findings, conclusions and recommendations expressed in any publication generated by the NRF supported research are those of the authors, and that the NRF accepts no liability whatsoever in this regard.
Funders:
Funding AgencyGrant Number
National Research Foundation of South Africa80717
Subject Keywords:claudin, lamprey, vertebrate primordia, embryo
Record Number:CaltechAUTHORS:20160601-081405569
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160601-081405569
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:67514
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:01 Jun 2016 20:36
Last Modified:01 Jun 2016 20:36

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