Skip to main content
PMC home page
Protein Science : A Publication of the Protein Society logoLink to Protein Science : A Publication of the Protein Society
. 1992 Feb;1(2):289–302. doi: 10.1002/pro.5560010211

Characterization, primary structure, and evolution of lamprey plasma albumin.

J E Gray 1, R F Doolittle 1
PMCID: PMC2142188  PMID: 1304910

Abstract

The most abundant protein found in blood plasma from the sea lamprey (Petromyzon marinus) has the hallmarks of a plasma albumin: namely, high abundance, solubility in distilled water, a small number of tryptophans, and a high content of cysteines and charged residues. As in other vertebrate albumins, not all the cysteines are disulfide bonded. An unusual feature of this protein is its molecular weight of 175,000, roughly 2.5 times the size of other vertebrate albumins. Its amino acid sequence, deduced from a series of overlapping cDNA clones, can be aligned with other members of the gene family including plasma albumin, alpha-fetoprotein, and vitamin-D binding protein, confirming that it is indeed an oversized albumin. An unusual feature of the sequence is a 28-amino acid stretch consisting of a serine-threonine repeat with the general motif (STTT). Lamprey albumin contains a 23-amino acid putative signal peptide and a 6-residue putative propeptide, which, when cleaved, yield a mature protein of 1,394 amino acids with a calculated molecular weight of 157,000. The sequence also includes nine potential N-linked glycosylation sites (Asn-X-Ser/Thr), consistent with observation that lamprey albumin is a glycoprotein. If all the potential glycosylation sites were occupied by clusters of 2,000 molecular weight each, the total molecular weight would be 175,000. Like other members of the gene family, lamprey albumin is composed of a series of 190-amino acid repeats, there being seven such domains all together. Quantitative amino acid sequence comparisons of lamprey albumin with the other members of the gene family indicate that it diverged from an ancestral albumin prior to the gene duplications leading to this diverse group. This notion is confirmed by the pattern of amino acid insertions and deletions observed in a consideration of all domains that compose this family. Furthermore, it suggests that the invention of albumin antedates the vertebrate radiation.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brown J. R. Structural origins of mammalian albumin. Fed Proc. 1976 Aug;35(10):2141–2144. [PubMed] [Google Scholar]
  3. Brown W. M., Dziegielewska K. M., Foreman R. C., Saunders N. R. Nucleotide and deduced amino acid sequence of sheep serum albumin. Nucleic Acids Res. 1989 Dec 25;17(24):10495–10495. doi: 10.1093/nar/17.24.10495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Byrnes L., Gannon F. Atlantic salmon (Salmo salar) serum albumin: cDNA sequence, evolution, and tissue expression. DNA Cell Biol. 1990 Nov;9(9):647–655. doi: 10.1089/dna.1990.9.647. [DOI] [PubMed] [Google Scholar]
  5. Carter D. C., He X. M., Munson S. H., Twigg P. D., Gernert K. M., Broom M. B., Miller T. Y. Three-dimensional structure of human serum albumin. Science. 1989 Jun 9;244(4909):1195–1198. doi: 10.1126/science.2727704. [DOI] [PubMed] [Google Scholar]
  6. Cooke N. E., David E. V. Serum vitamin D-binding protein is a third member of the albumin and alpha fetoprotein gene family. J Clin Invest. 1985 Dec;76(6):2420–2424. doi: 10.1172/JCI112256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cottrell B. A., Doolittle R. F. Amino acid sequences of lamprey fibrinopeptides A and B and characterizations of the junctions split by lamprey and mammalian thrombins. Biochim Biophys Acta. 1976 Dec 22;453(2):426–438. doi: 10.1016/0005-2795(76)90138-0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Dugaiczyk A., Law S. W., Dennison O. E. Nucleotide sequence and the encoded amino acids of human serum albumin mRNA. Proc Natl Acad Sci U S A. 1982 Jan;79(1):71–75. doi: 10.1073/pnas.79.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eiferman F. A., Young P. R., Scott R. W., Tilghman S. M. Intragenic amplification and divergence in the mouse alpha-fetoprotein gene. Nature. 1981 Dec 24;294(5843):713–718. doi: 10.1038/294713a0. [DOI] [PubMed] [Google Scholar]
  11. Fellows F. C., Hird F. J. A comparative study of the binding of L-tryptophan and bilirubin by plasma proteins. Arch Biochem Biophys. 1982 Jun;216(1):93–100. doi: 10.1016/0003-9861(82)90192-8. [DOI] [PubMed] [Google Scholar]
  12. Filosa M. F., Sargent P. A., Fisher M. M., Youson J. H. An electrophoretic and immunoelectrophoretic characterization of the serum proteins of the adult lamprey, Petromyzon marinus L. Comp Biochem Physiol B. 1982;72(4):521–530. doi: 10.1016/0305-0491(82)90500-4. [DOI] [PubMed] [Google Scholar]
  13. Gibbs P. E., Dugaiczyk A. Origin of structural domains of the serum-albumin gene family and a predicted structure of the gene for vitamin D-binding protein. Mol Biol Evol. 1987 Jul;4(4):364–379. doi: 10.1093/oxfordjournals.molbev.a040447. [DOI] [PubMed] [Google Scholar]
  14. Gibbs P. E., Zielinski R., Boyd C., Dugaiczyk A. Structure, polymorphism, and novel repeated DNA elements revealed by a complete sequence of the human alpha-fetoprotein gene. Biochemistry. 1987 Mar 10;26(5):1332–1343. doi: 10.1021/bi00379a020. [DOI] [PubMed] [Google Scholar]
  15. Gitlin D., Perricelli A., Gitlin J. D. The presence of serum alpha-fetoprotein in sharks and its synthesis by fetal gastrointestinal tract and liver. Comp Biochem Physiol B. 1973 Oct 15;46(2):207–215. doi: 10.1016/0305-0491(73)90311-8. [DOI] [PubMed] [Google Scholar]
  16. Gorin M. B., Cooper D. L., Eiferman F., van de Rijn P., Tilghman S. M. The evolution of alpha-fetoprotein and albumin. I. A comparison of the primary amino acid sequences of mammalian alpha-fetoprotein and albumin. J Biol Chem. 1981 Feb 25;256(4):1954–1959. [PubMed] [Google Scholar]
  17. Gorin M. B., Tilghman S. M. Structure of the alpha-fetoprotein gene in the mouse. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1351–1355. doi: 10.1073/pnas.77.3.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  19. Haefliger D. N., Moskaitis J. E., Schoenberg D. R., Wahli W. Amphibian albumins as members of the albumin, alpha-fetoprotein, vitamin D-binding protein multigene family. J Mol Evol. 1989 Oct;29(4):344–354. doi: 10.1007/BF02103621. [DOI] [PubMed] [Google Scholar]
  20. Hay A. W., Watson G. The plasma transport proteins of 25-hydroxycholecalciferol in fish, amphibians, reptiles and birds. Comp Biochem Physiol B. 1976;53(2):167–172. doi: 10.1016/0305-0491(76)90029-8. [DOI] [PubMed] [Google Scholar]
  21. Kragh-Hansen U. Structure and ligand binding properties of human serum albumin. Dan Med Bull. 1990 Feb;37(1):57–84. [PubMed] [Google Scholar]
  22. Law S. W., Dugaiczyk A. Homology between the primary structure of alpha-fetoprotein, deduced from a complete cDNA sequence, and serum albumin. Nature. 1981 May 21;291(5812):201–205. doi: 10.1038/291201a0. [DOI] [PubMed] [Google Scholar]
  23. Lawn R. M., Adelman J., Bock S. C., Franke A. E., Houck C. M., Najarian R. C., Seeburg P. H., Wion K. L. The sequence of human serum albumin cDNA and its expression in E. coli. Nucleic Acids Res. 1981 Nov 25;9(22):6103–6114. doi: 10.1093/nar/9.22.6103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McLachlan A. D., Walker J. E. Evolution of serum albumin. J Mol Biol. 1977 Jun 5;112(4):543–558. doi: 10.1016/s0022-2836(77)80163-0. [DOI] [PubMed] [Google Scholar]
  25. Meloun B., Morávek L., Kostka V. Complete amino acid sequence of human serum albumin. FEBS Lett. 1975 Oct 15;58(1):134–137. doi: 10.1016/0014-5793(75)80242-0. [DOI] [PubMed] [Google Scholar]
  26. Minghetti P. P., Law S. W., Dugaiczyk A. The rate of molecular evolution of alpha-fetoprotein approaches that of pseudogenes. Mol Biol Evol. 1985 Jul;2(4):347–358. doi: 10.1093/oxfordjournals.molbev.a040350. [DOI] [PubMed] [Google Scholar]
  27. Minghetti P. P., Ruffner D. E., Kuang W. J., Dennison O. E., Hawkins J. W., Beattie W. G., Dugaiczyk A. Molecular structure of the human albumin gene is revealed by nucleotide sequence within q11-22 of chromosome 4. J Biol Chem. 1986 May 25;261(15):6747–6757. [PubMed] [Google Scholar]
  28. Morinaga T., Sakai M., Wegmann T. G., Tamaoki T. Primary structures of human alpha-fetoprotein and its mRNA. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4604–4608. doi: 10.1073/pnas.80.15.4604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Peters T., Jr Serum albumin. Adv Protein Chem. 1985;37:161–245. doi: 10.1016/s0065-3233(08)60065-0. [DOI] [PubMed] [Google Scholar]
  30. Roux K. H., Dhanarajan P. A strategy for single site PCR amplification of dsDNA: priming digested cloned or genomic DNA from an anchor-modified restriction site and a short internal sequence. Biotechniques. 1990 Jan;8(1):48–57. [PubMed] [Google Scholar]
  31. 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]
  32. Sargent T. D., Jagodzinski L. L., Yang M., Bonner J. Fine structure and evolution of the rat serum albumin gene. Mol Cell Biol. 1981 Oct;1(10):871–883. doi: 10.1128/mcb.1.10.871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schoentgen F., Metz-Boutigue M. H., Jollès J., Constans J., Jollès P. Complete amino acid sequence of human vitamin D-binding protein (group-specific component): evidence of a three-fold internal homology as in serum albumin and alpha-fetoprotein. Biochim Biophys Acta. 1986 Jun 5;871(2):189–198. doi: 10.1016/0167-4838(86)90173-1. [DOI] [PubMed] [Google Scholar]
  34. Strong D. D., Moore M., Cottrell B. A., Bohonus V. L., Pontes M., Evans B., Riley M., Doolittle R. F. Lamprey fibrinogen gamma chain: cloning, cDNA sequencing, and general characterization. Biochemistry. 1985 Jan 1;24(1):92–101. doi: 10.1021/bi00322a014. [DOI] [PubMed] [Google Scholar]
  35. Weinstock J., Baldwin G. S. Nucleotide sequence of porcine liver albumin. Nucleic Acids Res. 1988 Sep 26;16(18):9045–9045. doi: 10.1093/nar/16.18.9045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yang F., Bergeron J. M., Linehan L. A., Lalley P. A., Sakaguchi A. Y., Bowman B. H. Mapping and conservation of the group-specific component gene in mouse. Genomics. 1990 Aug;7(4):509–516. doi: 10.1016/0888-7543(90)90193-x. [DOI] [PubMed] [Google Scholar]
  37. Yokoyama R., Yokoyama S. Convergent evolution of the red- and green-like visual pigment genes in fish, Astyanax fasciatus, and human. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9315–9318. doi: 10.1073/pnas.87.23.9315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Protein Science : A Publication of the Protein Society are provided here courtesy of The Protein Society

RESOURCES