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Identification of Igσ and Igλ in channel catfish, Ictalurus punctatus, and Igλ in Atlantic cod, Gadus morhua

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Abstract

Immunoglobulin light (IGL) chain genes encoding σ and λ from channel catfish, Ictalurus punctatus, and λ from Atlantic cod, Gadus morhua, were identified by mining of expressed sequence tag databases, 5′-RACE and RT-PCR protocols. cDNAs for each of these IGL chains encode typical variable (V), joining (J), and constant (C) regions and Southern blot analyses and genomic sequencing show that genes encoding these isotypes, like other teleost IGL genes, are found in a cluster organization of one or two V gene segments, followed by single J and C gene segments, all in the same transcriptional orientation. However, unlike the teleost κ genes, genes encoding catfish σ and λ are few in number and the two isotypes are each encoded by only two clusters. Similarly, Atlantic cod λ genes are predicted to be encoded by two or three clusters. As expected, sequence and phylogenetic analyses comparisons demonstrate that catfish Vσ and Cσ genes are most similar to Vσ and Cσ genes of other ectothermic vertebrates. Although catfish and Atlantic cod Vλ genes cluster with other vertebrate Vλ genes, their Cλ sequences cluster in a distinct group separate from other vertebrate IGL C sequences. However, support for classifying these sequences as λ, is their V and J recombination signal sequence (RSS) organization. The catfish and Atlantic cod genes have typical λ-like RSS with the Vλ RSS consisting of heptamer-23 bp spacer-nonamer and the Jλ RSS consisting of heptamer-12 bp spacer-nonamer. This is the first report demonstrating the presence of Igλ in teleosts.

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Acknowledgments

This work was supported by grants from the National Institutes of Health (RO1AI-19530), US Department of Agriculture (2002-35204-12211, 2003-35205-12829, and 2006-35204-16880), UMMC IRSP (59908) awarded to M.W., and UMMC IRSP (55901) awarded to N.W.M. We also thank the Drs Ellen Hsu and Mike Criscitiello for sharing their IGL sequence information pre-publication.

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  1. Department of Microbiology, University of Mississippi Medical Center, 2500 North State Street, Jackson, MS, 39216-4505, USA

    Eva-Stina Edholm, Melanie Wilson, Manoranjan Sahoo, Norman W. Miller, Niklas E. Wermenstam & Eva Bengtén

  2. Department of Cell and Molecular Biology, Immunology Programme, University of Uppsala, Biomedical Center, Box 596, SE-751 24, Uppsala, Sweden

    Lars Pilström

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  1. Eva-Stina Edholm
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sTable 1

Channel catfish primers used for PCR, probes and sequencing (PDF 18 kb)

sTable 2

Molecular markers distinguishing κ, λ and σ isotypes (PDF 12 kb)

sFig. 1

Catfish Igσ and Igλ and Atlantic cod Igλ chains. Nucleotide and predicted amino acid sequences of a catfish Igσ, b catfish Igλ and c Atlantic cod Igλ. The predicted leader sequence, VL, JL and C regions are labeled above the sequence. The stop (TGA) codons are marked with (*) and nucleotide and amino acid numbers are at left. GenBank accession numbers are: Catfish Igσ (IpIgσ, EU872021), catfish Igλ (IpIgLλ, EU872022), Atlantic cod Ig λ (GmIgLλ, CAC03754). (PDF 25 kb)

sFig. 2

Amino acid alignment of catfish Vσ sequences. IGSV1-1*01, IGSV1-2*01, and IGSV1-3P are genomic sequences obtained from IgLσ gene clusters 3C and 5A, respectively. IGSV1-2*02 was obtained by RT-PCR and IGSV1-1*02 and IGSV1-1*03 by 5'-RACE. The conserved cysteine residues that form the intrachain disulfide bonds are labeled (*). Residues identical to the catfish sequence are shown as (.) and (–) represents gaps in the alignment, an arrow denotes the primer used for 5′ RACE. GenBank accession numbers are: IGSV1-1*01 (EU872024), IGSV1-2*01 and IGSV1-3P (EU872023), IGSV-2*02 (EU925377), IGSV1-1*02 (EU925378), IGSV1-1*03 (EU925379). (PDF 48 kb)

sFig. 3

Amino acid alignment of catfish Cσ sequences. IGSC1*01 is a genomic sequence obtained from the IgLσ gene cluster 3C. IGSC1*02, IGSC1*03 and IGSC1*04 are representative sequences obtained by 5'-RACE. In total, 23 RACE products were amplified from PBL cDNA made from a single catfish: three IGSC1*03, five IGSC1*02, and 15 IGSC1*04 products were sequenced. The conserved cysteine residues that form the intrachain disulfide bonds are labeled (*) and the cysteine that form the interchain disulfide bond is marked by (↓). The number of amino acids is on the right. Residues identical to the catfish sequence are shown as (.). GenBank accession numbers are: IGSC1*01 (EU872024), IGSC1*02 (EU925380), IGSC1*03 (EU925381), IGSC1*04 (EU925382). (PDF 16 kb)

sFig. 4

Comparison of nucleotide sequence identities of teleost Vσ and Vλ sequences. Pairwise alignments were performed using CLUSTAL W and yellow highlights indicate >75% identity. VS and Vl subgroup membership is indicated above the sequence names and Genbank accession numbers are listed in the figure. Accession numbers referring to genomic sequences containing more than 1 V are labeled −1, −2, or −3, depending on the order of the V in the gene fragment. Species abbreviations are: Cc carp, Dr zebrafish, Om rainbow trout, Ip channel catfish, If blue catfish, Gm Atlantic cod. (PDF 7 kb)

sFig. 5

Amino acid alignment of catfish Vλ sequences. IGLV1-1*01 is a genomic sequence obtained from the IgLλ gene cluster 2A. IGLV1-1*02 and IGLV1-1*03 were obtained by RT-PCR and IGLV1-2*01 by 5′-RACE. The conserved cysteine residues that form the intrachain disulfide bonds are labeled (*) and the two cysteines found at the 3' end are labeled (^). Residues identical to the catfish sequence are shown as (.) and (–) represents gaps in the alignment, arrows denotes the primers used for 5′ RACE and genomic PCR. GenBank accession numbers are: IGLV1-1*01 (EU872025), IGLV1-1*02 (EU925383), IGLV1-1*03 (EU925384), IGLV1-2*01 (EU925385), IGLV1-2*02 (FJ716623). (PDF 49 kb)

sFig. 6

Amino acid alignment of representative IGL sequences. Sequences are aligned as recommended by Das et al. 2008 and molecular markers that distinguish κ, λ, and σ isotypes are boxed in blue (or red when not valid for teleosts). The amino acids conforming to the criteria proposed by Das et al. 2008 are highlighted in yellow and additional markers not defined by Das are highlighted in green. CDR regions are removed to optimize the alignment and their respective locations are marked by triangles. Amino acid numbers are according to the standardized rules of the IMGT unique numbering and are shown above the sequence (Lefranc et al. 2005). Accession numbers are catfish G-type (IpG, L25533); Carp L1 (CcL1, V and J (AB073328), C (AB015904)); zebrafish L1 (DrL1, AF246185); rainbow trout L1 (OmL1, X65260); Atlantic cod L1 (GmL1, V and J (AF104898.3), C (X68514)); catfish F-type (IpF, U25705); carp L3 (CcL3, V and J (BAB91006), C (BAB90987)); zebrafish L3 (DrL3, AB246193); X. laevis κ (Xlκ, V (L15570), J and C (M94392)); green anole κ (Acκ, FG748778); human κ (Hsκ, AAH73764); channel catfish λ (Ipλ, EU872022); blue catfish λ (Ifλ, CK403484); rainbow trout λ (Omλ, BX861350); Atlantic cod λ (Gmλ, AJ293807); X. laevis III (XlIII, L76579); green anole λ (Acλ, FG746006); chicken λ (Ggλ, K00678); human λ (Ηsλ, ABU90549); catfish σ (Ιpσ, EU872023); carp L2 (CcL2, V and J (AB091113), C (BAC81202)); zebrafish L2 (DrL2, AAG31698); rainbow trout L2 (OmL2, AAB41310); Atlantic cod σ (Gmσ, V (EX732557), J and C (EC907978)); and X. laevis σ (Xlσ, AAH82413). (PDF 69 kb)

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Edholm, ES., Wilson, M., Sahoo, M. et al. Identification of Igσ and Igλ in channel catfish, Ictalurus punctatus, and Igλ in Atlantic cod, Gadus morhua . Immunogenetics 61, 353–370 (2009). https://doi.org/10.1007/s00251-009-0365-z

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