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. 1993 Nov 15;90(22):10603–10607. doi: 10.1073/pnas.90.22.10603

Isolation of a shark immunoglobulin light chain cDNA clone encoding a protein resembling mammalian kappa light chains: implications for the evolution of light chains.

A S Greenberg 1, L Steiner 1, M Kasahara 1, M F Flajnik 1
PMCID: PMC47825  PMID: 8248152

Abstract

The time of emergence of immunoglobulin kappa and lambda light (L) chains in evolution is unknown. An L chain cDNA clone was isolated from the nurse shark (Ginglymostoma cirratum), a cartilaginous fish, whose predicted variable (V) region amino acid sequence has up to 60% sequence identity to mammalian V kappa domains. Genomic analyses suggest a cluster-type gene organization for this L chain locus, similar to the shark lambda-like immunoglobulin L chain loci rather than mammalian kappa loci. We propose that divergence of the ancestral L chain into isotypes likely occurred before the emergence of elasmobranchs 400-450 million years ago. Similarities in gene organization between the two isotypes in sharks may reflect the gene organization utilized by the ancestral L chain.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berinstein N., Levy S., Levy R. Activation of an excluded immunoglobulin allele in a human B lymphoma cell line. Science. 1989 Apr 21;244(4902):337–339. doi: 10.1126/science.2496466. [DOI] [PubMed] [Google Scholar]
  2. Bernstein F. C., Koetzle T. F., Williams G. J., Meyer E. F., Jr, Brice M. D., Rodgers J. R., Kennard O., Shimanouchi T., Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structures. J Mol Biol. 1977 May 25;112(3):535–542. doi: 10.1016/s0022-2836(77)80200-3. [DOI] [PubMed] [Google Scholar]
  3. Blomberg B., Traunecker A., Eisen H., Tonegawa S. Organization of four mouse lambda light chain immunoglobulin genes. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3765–3769. doi: 10.1073/pnas.78.6.3765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chothia C., Lesk A. M., Tramontano A., Levitt M., Smith-Gill S. J., Air G., Sheriff S., Padlan E. A., Davies D., Tulip W. R. Conformations of immunoglobulin hypervariable regions. Nature. 1989 Dec 21;342(6252):877–883. doi: 10.1038/342877a0. [DOI] [PubMed] [Google Scholar]
  5. Combriato G., Klobeck H. G. V lambda and J lambda-C lambda gene segments of the human immunoglobulin lambda light chain locus are separated by 14 kb and rearrange by a deletion mechanism. Eur J Immunol. 1991 Jun;21(6):1513–1522. doi: 10.1002/eji.1830210627. [DOI] [PubMed] [Google Scholar]
  6. Doolittle R. F., Feng D. F. Nearest neighbor procedure for relating progressively aligned amino acid sequences. Methods Enzymol. 1990;183:659–669. doi: 10.1016/0076-6879(90)83043-9. [DOI] [PubMed] [Google Scholar]
  7. Durdik J., Moore M. W., Selsing E. Novel kappa light-chain gene rearrangements in mouse lambda light chain-producing B lymphocytes. Nature. 1984 Feb 23;307(5953):749–752. doi: 10.1038/307749a0. [DOI] [PubMed] [Google Scholar]
  8. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  9. Feng D. F., Doolittle R. F. Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol. 1987;25(4):351–360. doi: 10.1007/BF02603120. [DOI] [PubMed] [Google Scholar]
  10. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grant J. A., Sanders B., Hood L. Partial amino acid sequences of chicken and turkey immunoglobulin light chains. Homology with mammalian lambda chains. Biochemistry. 1971 Aug 3;10(16):3123–3132. doi: 10.1021/bi00792a022. [DOI] [PubMed] [Google Scholar]
  12. Hieter P. A., Korsmeyer S. J., Waldmann T. A., Leder P. Human immunoglobulin kappa light-chain genes are deleted or rearranged in lambda-producing B cells. Nature. 1981 Apr 2;290(5805):368–372. doi: 10.1038/290368a0. [DOI] [PubMed] [Google Scholar]
  13. Hill R. L., Delaney R., Fellows R. E., Lebovitz H. E. The evolutionary origins of the immunoglobulins. Proc Natl Acad Sci U S A. 1966 Dec;56(6):1762–1769. doi: 10.1073/pnas.56.6.1762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hinds K. R., Litman G. W. Major reorganization of immunoglobulin VH segmental elements during vertebrate evolution. Nature. 1986 Apr 10;320(6062):546–549. doi: 10.1038/320546a0. [DOI] [PubMed] [Google Scholar]
  15. Hohman V. S., Schluter S. F., Marchalonis J. J. Complete sequence of a cDNA clone specifying sandbar shark immunoglobulin light chain: gene organization and implications for the evolution of light chains. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):276–280. doi: 10.1073/pnas.89.1.276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ishiguro H., Kobayashi K., Suzuki M., Titani K., Tomonaga S., Kurosawa Y. Isolation of a hagfish gene that encodes a complement component. EMBO J. 1992 Mar;11(3):829–837. doi: 10.1002/j.1460-2075.1992.tb05120.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kabat E. A. Comparison of invariant residues in the variable and constant regions of human K, human L, and mouse K Bence-Jones proteins. Proc Natl Acad Sci U S A. 1967 Jul;58(1):229–233. doi: 10.1073/pnas.58.1.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 1983 Dec;22(12):2577–2637. doi: 10.1002/bip.360221211. [DOI] [PubMed] [Google Scholar]
  19. Kasahara M., Vazquez M., Sato K., McKinney E. C., Flajnik M. F. Evolution of the major histocompatibility complex: isolation of class II A cDNA clones from the cartilaginous fish. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6688–6692. doi: 10.1073/pnas.89.15.6688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kokubu F., Litman R., Shamblott M. J., Hinds K., Litman G. W. Diverse organization of immunoglobulin VH gene loci in a primitive vertebrate. EMBO J. 1988 Nov;7(11):3413–3422. doi: 10.1002/j.1460-2075.1988.tb03215.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kozak M. An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol. 1991 Nov;115(4):887–903. doi: 10.1083/jcb.115.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Marchalonis J. J., Schluter S. F. Immunoproteins in evolution. Dev Comp Immunol. 1989 Fall;13(4):285–301. doi: 10.1016/0145-305x(89)90039-6. [DOI] [PubMed] [Google Scholar]
  23. Marchalonis J. J., Schluter S. F., Rosenshein I. L., Wang A. C. Partial characterization of immunoglobulin light chains of carcharhine sharks: evidence for phylogenetic conservation of variable region and divergence of constant region structure. Dev Comp Immunol. 1988 Winter;12(1):65–74. doi: 10.1016/0145-305x(88)90025-0. [DOI] [PubMed] [Google Scholar]
  24. McCormack W. T., Tjoelker L. W., Thompson C. B. Avian B-cell development: generation of an immunoglobulin repertoire by gene conversion. Annu Rev Immunol. 1991;9:219–241. doi: 10.1146/annurev.iy.09.040191.001251. [DOI] [PubMed] [Google Scholar]
  25. Mikoryak C. A., Steiner L. A. Amino acid sequence of the constant region of immunoglobulin light chains from Rana catesbeiana. Mol Immunol. 1988 Aug;25(8):695–703. doi: 10.1016/0161-5890(88)90105-8. [DOI] [PubMed] [Google Scholar]
  26. Mäkelä O., Litman G. W. Lack of heterogeneity in antihapten antibodies of a phylogenetically primitive shark. Nature. 1980 Oct 16;287(5783):639–640. doi: 10.1038/287639a0. [DOI] [PubMed] [Google Scholar]
  27. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  28. Reidl L. S., Kinoshita C. M., Steiner L. A. Wild mice express an Ig V lambda gene that differs from any V lambda in BALB/c but resembles a human V lambda subgroup. J Immunol. 1992 Jul 15;149(2):471–480. [PubMed] [Google Scholar]
  29. Reynaud C. A., Anquez V., Dahan A., Weill J. C. A single rearrangement event generates most of the chicken immunoglobulin light chain diversity. Cell. 1985 Feb;40(2):283–291. doi: 10.1016/0092-8674(85)90142-4. [DOI] [PubMed] [Google Scholar]
  30. Reynaud C. A., Anquez V., Grimal H., Weill J. C. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell. 1987 Feb 13;48(3):379–388. doi: 10.1016/0092-8674(87)90189-9. [DOI] [PubMed] [Google Scholar]
  31. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  32. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schluter S. F., Hohman V. S., Edmundson A. B., Marchalonis J. J. Evolution of immunoglobulin light chains: cDNA clones specifying sandbar shark constant regions. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9961–9965. doi: 10.1073/pnas.86.24.9961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schwager J., Bürckert N., Schwager M., Wilson M. Evolution of immunoglobulin light chain genes: analysis of Xenopus IgL isotypes and their contribution to antibody diversity. EMBO J. 1991 Mar;10(3):505–511. doi: 10.1002/j.1460-2075.1991.tb07976.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shamblott M. J., Litman G. W. Complete nucleotide sequence of primitive vertebrate immunoglobulin light chain genes. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4684–4688. doi: 10.1073/pnas.86.12.4684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Shamblott M. J., Litman G. W. Genomic organization and sequences of immunoglobulin light chain genes in a primitive vertebrate suggest coevolution of immunoglobulin gene organization. EMBO J. 1989 Dec 1;8(12):3733–3739. doi: 10.1002/j.1460-2075.1989.tb08549.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Siminovitch K. A., Bakhshi A., Goldman P., Korsmeyer S. J. A uniform deleting element mediates the loss of kappa genes in human B cells. Nature. 1985 Jul 18;316(6025):260–262. doi: 10.1038/316260a0. [DOI] [PubMed] [Google Scholar]
  38. Sledge C., Clem L. W., Hood L. Antibody structure: amino terminal sequences of nurse shark light and heavy chains. J Immunol. 1974 Mar;112(3):941–948. [PubMed] [Google Scholar]
  39. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  40. Storb U., Haasch D., Arp B., Sanchez P., Cazenave P. A., Miller J. Physical linkage of mouse lambda genes by pulsed-field gel electrophoresis suggests that the rearrangement process favors proximate target sequences. Mol Cell Biol. 1989 Feb;9(2):711–718. doi: 10.1128/mcb.9.2.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Strohal R., Helmberg A., Kroemer G., Kofler R. Mouse Vk gene classification by nucleic acid sequence similarity. Immunogenetics. 1989;30(6):475–493. doi: 10.1007/BF02421180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Udey J. A., Blomberg B. Human lambda light chain locus: organization and DNA sequences of three genomic J regions. Immunogenetics. 1987;25(1):63–70. doi: 10.1007/BF00768834. [DOI] [PubMed] [Google Scholar]
  43. Williams A. F., Barclay A. N. The immunoglobulin superfamily--domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405. doi: 10.1146/annurev.iy.06.040188.002121. [DOI] [PubMed] [Google Scholar]
  44. Zezza D. J., Mikoryak C. A., Schwager J., Steiner L. A. Sequence of C region of L chains from Xenopus laevis Ig. J Immunol. 1991 Jun 1;146(11):4041–4047. [PubMed] [Google Scholar]
  45. Zezza D. J., Stewart S. E., Steiner L. A. Genes encoding Xenopus laevis Ig L chains. Implications for the evolution of kappa and lambda chains. J Immunol. 1992 Dec 15;149(12):3968–3977. [PubMed] [Google Scholar]

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