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Monodelphis Domestica in the Opossum Λ Conservation Of Marsupial Light Chains: Complexity and Conservation of λ in the Opossum Monodelphis domestica This information is current as Julie E. Lucero, George H. Rosenberg and Robert D. Miller of September 29, 2021. J Immunol 1998; 161:6724-6732; ; http://www.jimmunol.org/content/161/12/6724 Downloaded from References This article cites 35 articles, 10 of which you can access for free at: http://www.jimmunol.org/content/161/12/6724.full#ref-list-1 Why The JI? Submit online. http://www.jimmunol.org/ • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average by guest on September 29, 2021 Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 1998 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Marsupial Light Chains: Complexity and Conservation of l in the Opossum Monodelphis domestica1,2 Julie E. Lucero, George H. Rosenberg, and Robert D. Miller3 The Igl chains in the South American opossum, Monodelphis domestica, were analyzed at the expressed cDNA and genomic organization level, the first described for a nonplacental mammal. The Vl segment repertoire in the opossum was found to be comprised of at least three diverse Vl families. Each of these families appears to be related to distinct Vl families present in placental mammals, suggesting the divergence of these genes before the separation of metatherians and eutherians more than 100 million years ago. Based on framework and constant region sequences from full-length cDNAs and intron sequences from genomic clones, it appears that there are multiple functional Jl-Cl pairs in the opossum locus. The opossum Jl-Cl sequences are phylogenetically clustered, suggesting that these gene duplications are more recent and species specific. Sequence analysis of a large set of functional, expressed Vl-Jl recombinations is consistent with an unbiased, highly diverse l light chain repertoire in Downloaded from the adult opossum. Overall, the complexity of the Igl locus appears to be greater than that found in the Ig heavy chain locus in the opossum, and light chains are therefore likely to contribute significantly to Ig diversity in this species. The Journal of Immunology, 1998, 161: 6724–6732. wo identical heavy chains paired with two identical light Our knowledge of the structure, diversity, and evolution of the chains is the generic structure of vertebrate Ig molecules. mammalian IgL genes is based on studies of only one of the three http://www.jimmunol.org/ T In mammals, the Ig heavy chains (IgH)4 are encoded at a major orders of mammals, the eutherians or “placental” mammals. single site in the genome, but the two types of Ig light chains (IgL), To date there has been no reported IgL gene structure from either k and l, are encoded at separate, unlinked loci. The use of the two of the other two mammalian orders, the prototherians (egg laying IgL types can vary between species, some having a bias or pref- monotremes, e.g., the platypus) or the metatherians (marsupials). erential use of one over the other (reviewed in Ref. 1). Mice and The relationship of these three mammalian lineages has been a rabbits, for example, use predominantly Igk, whereas horses, subject of continued debate over much of this century with most sheep, and cattle use primarily Igl (1–6). The use of one IgL type investigators placing the metatherians and the eutherians together over another correlates, in general, with the overall complexity of as sister taxa, with the prototherians diverging earliest (12). How- the loci in most species. Humans, for example, have a significant ever, more recent analysis of mitochondrial DNA supports the idea by guest on September 29, 2021 amount of Vl and Vk diversity and use both extensively, 60% that prototherians and metatherians are sister taxa, with the euth- Igk:40% Igl (2, 7–9). Mice, on the other hand, have only three erians splitting off first (12, 13). Possible times for the divergence functional Vl segments but a large number of available Vk and of these groups range from less than 120 million years ago, during have a 95% Igk:5% Igl ratio (7, 9). The contributions that IgL the Cretaceous Period, to possibly greater than 170 million years make to Ab diversity can also vary greatly between species. Hu- ago, during the Jurassic Period (14, 15). A more extensive analysis mans appear to have a significant amount of light chain diversity of metatherian and prototherian immunobiology provides a com- (7, 10). In contrast, the l repertoire of cattle is restricted to a parison between very distantly related mammalian species and recurrent Vl-Jl rearrangement, even though they appear to have should yield important knowledge into the evolution of mamma- multiple functional Vl and Jl segments in their germline (5). Per- lian immune systems. haps the most extreme case of limited contribution by light chains In addition to their importance to mammalian evolution, mar- occurs in the camelids (camels and llamas), which produce a form supials also provide an opportunity to study mammals that are born of IgG lacking light chains entirely (11). comparatively less developed than mice or humans. Developmen- tal immaturity combined with the lack of a placenta, which sup- ports the transfer of maternal Ig, in most marsupial species creates unique immunological problems for metatherians (16). The opos- Department of Biology, University of New Mexico, Albuquerque, NM 87131 sum, Monodelphis domestica, has been established over the last Received for publication July 6, 1998. Accepted for publication August 26, 1998. decade as an important laboratory-bred marsupial for studies of The costs of publication of this article were defrayed in part by the payment of page many areas of comparative and biomedical research (17, 18). M. charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. domestica are native to South America and are a member of the family Didelphidae, which contains the largest number of species 1 This work was supported by a National Science Foundation CAREER Award (MCB-9600875) to R.D.M., and a Research Experience for Undergraduates (National within the marsupials, and Monodelphis is the most species-rich Science Foundation) supplement. J.E.L. was supported by a fellowship from the genus of the family (19). The Didelphidae are also thought to have Howard Hughes Medical Institute Undergraduate Research Program. diverged earliest from the rest of the metatheria and may contain 2 All sequences reported have been deposited in the GenBank/EMBL database and some of the oldest extant mammalian species (20, 21). assigned accession numbers AF049746–AF049790. We have begun characterizing the Ig genes of M. domestica, and 3 Address correspondence and reprint requests to Dr. R. D. Miller, Department of Biology, University of New Mexico, Albuquerque, NM 87131-0001. we previously reported that the IgH repertoire was derived from 4 Abbreviations used in this paper: IgH, Ig heavy chain; IgL, Ig light chain; FR, two related group III type VH families (22). To extend this analysis framework region; CDR, complementarity determining region. to opossum IgL, we have cloned and characterized Igl-containing Copyright © 1998 by The American Association of Immunologists 0022-1767/98/$02.00 The Journal of Immunology 6725 cDNAs and have found the presence of at least three highly di- Results vergent Vl families, the absence of bias in the Vl-Jl combina- Isolation of M. domestica Igl cDNAs tions, and evidence that the duplicated Jl-Cl pair arrangements To isolate clones containing opossum Igl sequences, fragments of found in placental mammals is conserved in the opossum. It ap- Vl segments were first amplified from a spleen cDNA by an- pears that the genetic complexity of the M. domestica Igl locus is chored PCR using a FR2-specific degenerate primer and then, greater than that for the IgH locus, suggesting that l light chains cloned and sequenced. Four unique clones were found to be ho- contribute significantly to the diversity of the Ig repertoire in this mologous to the leader, FR1, and complementarity determining species. region 1 (CDR1) of known mammalian Vl segments (not shown). The clones varied from 175 to 184 nucleotides in length and shared from 52% to 74% nucleotide similarity to mammalian Vl, but less Materials and Methods than 40% similarity to any mammalian Vk sequences (not shown). l PCR amplification of Ig sequences Two of the PCR-generated clones were from different Vl families, A degenerate oligonucleotide (59-CCNGGYTTYTGYTGRTACCA) com- based on less than 50% similarity, and were used independently to plementary to the coding strand for the amino acid sequence WYQQKPG screen a cDNA phage library constructed from M. domestica conserved in framework region 2 (FR2) of light chain V segments (also see spleen RNA. Three clones were identified using each probe, and Ref. 23) was used to amplify opossum V fragments by anchored PCR. L l The target for PCR was a commercially available M. domestica spleen all six clones were found to contain full length light chain cDNA library constructed using the lZAPII cloning vector (Stratagene, La cDNAs containing variable and constant regions (Fig. 1). Jolla, CA). The degenerate FR2 oligonucleotide was used in PCR as a Downloaded from reverse primer in combination with the T3 universal sequencing primer Identification of three Vl families in M.
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