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Complex expression patterns of lymphocyte-specific genes during the development of cartilaginous fish implicate unique lymphoid tissues in generating an immune repertoire

Miracle, Ann L. and Anderson, Michele K. and Litman, Ronda T. and Walsh, Cathy J. and Luer, Carl A. and Rothenberg, Ellen V. and Litman, Gary W. (2001) Complex expression patterns of lymphocyte-specific genes during the development of cartilaginous fish implicate unique lymphoid tissues in generating an immune repertoire. International Immunology, 13 (4). pp. 567-580. ISSN 0953-8178. https://resolver.caltech.edu/CaltechAUTHORS:20111116-111340077

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Abstract

Cartilaginous fish express canonical B and T cell recognition genes, but their lymphoid organs and lymphocyte development have been poorly defined. Here, the expression of Ig, TCR, recombination-activating gene (Rag)-1 and terminal deoxynucleosidase (TdT) genes has been used to identify roles of various lymphoid tissues throughout development in the cartilaginous fish, Raja eglanteria (clearnose skate). In embryogenesis, Ig and TCR genes are sharply up-regulated at 8 weeks of development. At this stage TCR and TdT expression is limited to the thymus; later, TCR gene expression appears in peripheral sites in hatchlings and adults, suggesting that the thymus is a source of T cells as in mammals. B cell gene expression indicates more complex roles for the spleen and two special organs of cartilaginous fish—the Leydig and epigonal (gonad-associated) organs. In the adult, the Leydig organ is the site of the highest IgM and IgX expression. However, the spleen is the first site of IgM expression, while IgX is expressed first in gonad, liver, Leydig and even thymus. Distinctive spatiotemporal patterns of Ig light chain gene expression also are seen. A subset of Ig genes is pre-rearranged in the germline of the cartilaginous fish, making expression possible without rearrangement. To assess whether this allows differential developmental regulation, IgM and IgX heavy chain cDNA sequences from specific tissues and developmental stages have been compared with known germline-joined genomic sequences. Both non-productively rearranged genes and germline-joined genes are transcribed in the embryo and hatchling, but not in the adult.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1093/intimm/13.4.567DOIArticle
http://intimm.oxfordjournals.org/content/13/4/567PublisherArticle
ORCID:
AuthorORCID
Rothenberg, Ellen V.0000-0002-3901-347X
Additional Information:© 2001 Japanese Society for Immunology. Received December 15, 2000; Accepted January 10, 2001. We would like to thank Barbara Pryor for editorial assistance. This work was supported by grants R37 AI23338 to G. W. L. from the National Institutes of Health, and NAG2-1370 to M. K. A. and E. V. R. from NASA. A. L. M has been supported in part by the Institute for Biomolecular Science, University of South Florida and M. K. A. is a fellow of the Stowers Institute. C. A. L. received partial support from the Henry L. and Grace Doherty Charitable Foundation, the Vernal W. and Florence Bates Foundation, and the Disney Wildlife Conservation Fund.
Funders:
Funding AgencyGrant Number
NIHR37 AI23338
NASANAG2-1370
University of South Florida Institute for Biomolecular ScienceUNSPECIFIED
Henry L. and Grace Doherty Charitable FoundationUNSPECIFIED
Vernal W. and Florence Bates FoundationUNSPECIFIED
Disney Wildlife Conservation FundUNSPECIFIED
Subject Keywords:epigonal organ; Ig; Leydig organ; Rag; real-time PCR; TCR; TdT; CDR complementarity-determining region; FR framework region; LCI light chain type I; LCII light chain type II; LDS lithium dodecylsulfate; PBL peripheral blood lymphocytes; Rag recombination-activating gene; TdT terminal deoxynucleoside transferase
Issue or Number:4
Record Number:CaltechAUTHORS:20111116-111340077
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20111116-111340077
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:27809
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:16 Nov 2011 22:23
Last Modified:03 Oct 2019 03:26

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