Advertisement

Journal of Molecular Evolution

, Volume 42, Issue 6, pp 713–728 | Cite as

Common origin of arthropod tyrosinase, arthropod hemocyanin, insect hexamerin, and dipteran arylphorin receptor

  • Thorsten Burmester
  • Klaus Schellen
Articles

Abstract

Dipteran arylphorin receptors, insect hexamerins, cheliceratan and crustacean hemocyanins, and crustacean and insect tyrosinases display significant sequence similarities. We have undertaken a systematic comparison of primary and secondary structures of these proteins. On the basis of multiple sequence alignments the phylogeny of these proteins was investigated. Hexamerin subunits, hemocyanin subunits, and tyrosinases share extensive similarities throughout the entire amino acid sequence. Our studies suggest the origin of arthropod hemocyanins from ancient tyrosinase-like proteins. Insect hexamerins likely evolved from hemocyanins of ancient crustaceans, supporting the proposed sister-group position of these subphyla. Arylphorin receptors, responsible for incorporation of hexamerins into the larval fat body of diptera, are related to hexamerins, hemocyanins, and tyrosinase. The receptor sequences display extensive similarities to the first and third domains of hemocyanins and hexamerins. In the middle region only limited amino acid conservation was observed. Elements important for hexamer formation are deleted in the receptors. Phylogenetic analysis indicated that dipteran arylphorin receptors diverged from ancient hexamerins, probably early in insect evolution.

Key words

Arthropods Protein evolution Arylphorin receptor Arylphorin Larval serum protein Hexamerin Hemocyanin Tyrosinase 

Abbreviations used

aa

amino acid

MYA

million years ago; the other abbreviations are listed in Table 1

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ashida M, Yoshida H (1988) Limited proteolysis of prophenoloxidase during activation by microbial products in insect plasma and effect of phenoloxidase on electrophoresic mobility of plasma proteins. Insect Biochem 18:11–19Google Scholar
  2. Aspan A, Huang TS, Cerenius L, Söderhäll K (1995) cDNA cloning of a prophenoloxidase from the freshwater crayfishPacifastacus leniusculus and its activation. Proc Natl Acad Sci USA 92:939–943PubMedGoogle Scholar
  3. Aspan A, Söderhäll K (1991) Purification of prophenoloxidase from crayfish blood cells, and its activation by an endogenous serine proteinase. Insect Biochem 21:363–373Google Scholar
  4. Bak HJ, Beintema JJ (1987)Panulirus interruptus hemocyanin. The elucidation of the complete amino acid sequence of subunit a. FEBS Lett 204:141–144Google Scholar
  5. Beintema JJ, Stam WT, Hazes B, Smidt MP (1994) Evolution of arthropod hemocyanins and insect storage proteins (hexamerins). Mol Biol Evol 11:493–503PubMedGoogle Scholar
  6. Bergström J (1979) Morphology of fossil arthropods as a guide to polyphyetic relationship. In: Gupta AP (ed) Arthropod phylogeny. Van Nordstrand Reinhold, New York, pp 33–56Google Scholar
  7. Burmester T, Scheller K (1992) Identification of binding proteins involved in the stage-specific uptake of arylphorin by the fat body cells ofCalliphora vicina. Insect Biochem Mol Biol 22:211–220Google Scholar
  8. Burmester T, Scheller K (1995a) Ecdysterone-mediated uptake of arylphorin by larval fat bodies ofCalliphora vicina: involvement and developmental regulation of arylphorin binding proteins. Insect Biochem Mol Biol 25:799–806Google Scholar
  9. Burmester T, Scheller K (1995b) Complete cDNA-sequence of the receptor responsible for arylphorin uptake by the larval fat body of the blowfly,Calliphora vicina. Insect Biochem Mol Biol 25:981–989PubMedGoogle Scholar
  10. Chung SO, Kubo T, Natori S (1995) Molecular cloning and sequencing of arylphorin-binding protein in protein granules ofSarcophaga fat body. J Biol Chem 270:4624–4631PubMedGoogle Scholar
  11. Dayhoff MO (1979) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Washington, DCGoogle Scholar
  12. de Haas F, van Bruggen EFJ (1994) The interhexameric contacts in the four-hexameric hemocyanin from the tarantulaEurypelma californicum. J Mol Biol 237:464–478PubMedGoogle Scholar
  13. de Kort CAD, Koopmanschap AB (1994) Nucleotide and deduced amino acid sequence of a cDNA clone encoding diapause protein 1, an arylphorin-type storage hexamer of the Colorado potato beetle. J Insect Physiol 40:527–535Google Scholar
  14. Doolittle RF (1981) Similar amino acid sequences: chance or common ancestry? Science 214:149–159PubMedGoogle Scholar
  15. Drexel R, Siegmund S, Schneider HJ, Linzen B, Gielens C, Lontie R, Kellermann J, Lottspeich F (1987) Complete sequence of a functional unit from a molluscan hemocyanin (Helix pomatia). Biol Chem Hoppe Seyler 368:617–635PubMedGoogle Scholar
  16. Duhamel RC, Kunkel JG (1983) Cockroach larval-specific protein, a tyrosine-rich serum protein. J Biol Chem 258:14461–14465PubMedGoogle Scholar
  17. Duhamel RC, Kunkel JG (1987) Moulting-cycle regulation of haemolymph protein clearance in cockroaches possible size-dependent mechanism. J Insect Physiol 33:155–158CrossRefGoogle Scholar
  18. Enderle U, Kduser G, Renn L, Scheller K, Koolman J (1983) Ecdysteroids in the hemolymph of blowfly are bound to calliphorin. In: Scheller K (ed) The larval serum proteins of insects: function, biosynthesis, genetic. Thieme, Stuttgart, pp 40–49Google Scholar
  19. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  20. Felsenstein J (1993) PHYLIP: (phylogeny inference package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, SeattleGoogle Scholar
  21. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specified tree topology. System Zool 20:406–416Google Scholar
  22. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284PubMedGoogle Scholar
  23. Fujii T, Sakurai H, Izumi S, Tomino S (1989) Structure of the gene for the arylphorin-type storage protein SP2 ofBombyx mori. J Biol Chem 264:11020–11025PubMedGoogle Scholar
  24. Gaykema WPJ, Hol WGJ, Vereijken JM, Soeter NM, Bak HL, Beintema JJ (1984) 3.2 Å structure of the copper-containing, oxygencarrying proteinPanulirus interruptus hemocyanin. Nature 309: 23–29CrossRefGoogle Scholar
  25. Hall M, Scott T, Sugumaran M, Söderhäll K, Law JH (1995) Prophenoloxidase of the hawkmothManduca sexta. Purification, activation, substrate specificity of the enzyme, and molecular cloning. EMBL accession No. L42556Google Scholar
  26. Hennig W (1969) Stammesgeschichte der Insekten. W Kramer, FrankfurtGoogle Scholar
  27. Jekel PA, Bak HL Soeter NM, Verejken JM, Beintema JJ (1988)Panulirus interruptus hemocyanin. The amino acid sequence of subunit b and anomalous behaviour of subunits a and b on polyacrylamide gel electrophoresis in the presence of SDS. Eur J Biochem 178: 403–412CrossRefPubMedGoogle Scholar
  28. Jones G, Brown N, Manczak M, Hiremath S, Kafatos FC (1990) Molecular cloning, regulation, and complete sequence of a hemocyanin-related, juvenile hormone-suppressible protein from insect hemolymph. J Biol Chem 25:8596–8602Google Scholar
  29. Jones G, Manczak M, Horn M (1993) Hormonal regulation and properties of a new group of basic hemolymph proteins expressed during insect metamorphosis. J Biol Chem 268:1284–1291PubMedGoogle Scholar
  30. Koopmanschap AB, Lammers JHM, de Kort CAD (1995) The structure of the gene encoding diapause protein 1 of the Colorado potato beetle (Leptinotarsa decemlineata). J Insect Physiol 41:509–518CrossRefGoogle Scholar
  31. Levenbook L, Bauer A (1984) The fate of the larval storage protein calliphorin during adult development ofCalliphora vicina. Insect Biochem 14:77–86Google Scholar
  32. Linzen B, Soeter NM, Riggs AF, Schneider HJ, Schartau W, Moore MD, Behrens PQ, Nakashima H, Takagi T, Nemoto T, Vereijken JM, Bak HJ, Beintema JJ, Volbeda A, Gaykema WPJ, Hol WGJ (1985) The structure of arthropod hemocyanins. Science 229:519–524PubMedGoogle Scholar
  33. Locke M, McDermind H, Brac T, Atkinson B (1982) Developmental changes in the synthesis of haemolymph polypeptides and their sequestration by the prepupal fat body ofCalpodes ethlius Stoll (Lepidoptera, Hesperiidae). Insect Biochem 12:431–440Google Scholar
  34. Marinotti O, de Bianchi AG (1986) Uptake of storage protein byMusca fat body. J Insect Physiol 32:819–825CrossRefGoogle Scholar
  35. Markl J (1986) Evolution and function of structurally diverse subunits in the respiratory protein hemocyanin from arthropods. Biol Bull 171: 90–115Google Scholar
  36. Markl J, Burmester T, Decker H, Sievel-Niemann A, Harris JR, Süling M, Naumann U, Scheller K (1992) Quaternary and subunit structure ofCalliphora arylphorin as deduced from electron microscopy, electrophoresis, and sequence similarities with arthropod hemocyanins. J Comp Physiol [B] 162:665–680Google Scholar
  37. Markl J, Markl A, Schartau W, Linzen B (1979a) Subunit heterogeneity in arthropod hemocyanins: I. Chelicerata. J Comp Physiol 130: 283–292Google Scholar
  38. Markl J, Hofer A, Bauer G, Markl A, Kemptner B, Brenzinger M, Linzen B (1979b) Subunit heterogeneity in arthropod hemocyanins: II. Crustacea. J Comp Physiol 133:67–175Google Scholar
  39. Markl J, Winter S (1989)Subunit-specific monoclonal antibodies of tarantula hemocyanin, and a common epitope shared with calliphorin. J Comp Physiol [B] 159:139–151Google Scholar
  40. Martin MD, Kinnear JF, Thomson JA (1971) Developmental changes in the late larvae ofCalliphora stygia: IV. Uptake of plasma protein by the fat body. Aust J Biol Sci 24:291–299PubMedGoogle Scholar
  41. Maschat F, Dubertret ML, Therond P, Claverie JM, Lepesant JA (1990) Structure of the ecdysone-inducible P1 gene ofDrosophila melanogaster. J Mol Biol 214:359–372CrossRefPubMedGoogle Scholar
  42. Memmel NA, Trewitt PM, Grzelak K, Rajaratnam VS, Kumaran AK (1994) Nucleotide sequence, structure and developmental regulation of LHP82, a juvenile hormone-suppressible hexamerin gene from the waxmoth,Galleria mellonella. Insect Biochem Mol Biol 24:133–144PubMedGoogle Scholar
  43. Memmel NA, Trewitt PM, Silhacek DL, Kumaran AK (1992) Nucleotide sequence and structure of the arylphorin gene fromGalleria mellonella. Insect Biochem Mol Biol 22:333–342Google Scholar
  44. Miller S, Silhacek DL (1982) The synthesis and uptake of haemolymph storage proteins by the fat body of the greater wax moth,Galleria mellonella (L.). Insect Biochem 12:293–300Google Scholar
  45. Müller G, Ruppert S, Schmid E, Schütz G (1988) Functional analysis of alternatively spliced tyrosinase gene transcripts. EMBO J 7: 2723–2730PubMedGoogle Scholar
  46. Nakashima H, Behrens PQ, Moore MD, Yokota E, Riggs AF (1986) Structure of hemocyanin 11 from the horseshoe crab,Limulus polyphemus. J Biol Chem 261:10526–10533PubMedGoogle Scholar
  47. Naumann U, Scheller K (1991) Complete cDNA and gene sequence of the developmentally regulated arylphorin ofCalliphora vicina and its relationship to insect haemolymph proteins and arthropod hemocyanins. Biochem Biophys Res Commun 177:963–972CrossRefPubMedGoogle Scholar
  48. Neuteboom B, Jekel PA, Beintema JJ (1992) Primary structure of hemocyanin subunit c fromPanulirus interruptus. Eur J Biochem 206:243–249CrossRefPubMedGoogle Scholar
  49. Pan MI, Telfer WH (1992) Selectivity in storage hexamerin clearing demonstrated with hemolymph transfusions betweenHyalophora cecropia andActias luna. Arch Insect Biochem Physiol 19:203–219CrossRefPubMedGoogle Scholar
  50. Peter MG, Scheller K (1991) Arylphorins and the integument. In: Retnakaran A, Binnington K (eds) The physiology of insect epidermis. CSIRO, East Melbourne, Australia, pp 115–124Google Scholar
  51. Roberts DB, Brock HW (1981) The major serum proteins of diptera larvae. Experientia 37:103–110CrossRefGoogle Scholar
  52. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  53. Sakurai H, Tomoko F, Izumi S, Tomino S (1988) Complete nucleotide sequence of gene for sex-specific storage protein ofBombyx mori. Nucleic Acids Res 16:7717–7718PubMedGoogle Scholar
  54. Schartau W, Eyerle F, Reisinger P, Geisert H, Storz H, Linzen B (1983) Hemocyanins in spiders, XIX. Complete amino-acid sequence of subunit d fromEurypelma californicum hemocyanin, and comparison with chain e. Hoppe-Seyler's Z Physiol Chem 364:1383–1409PubMedGoogle Scholar
  55. Scheller K, Fischer B, Schenkel H (1990) Molecular properties, functions and developmentally regulated biosynthesis of arylphorin inCalliphora vicina. In: Hagedom HH, Hildebrand JG, Kidwell MG, Law JH (eds) Molecular insect science. Plenum Press, New York, pp 155–162Google Scholar
  56. Sellos DY (1995) EMBL accession No. X82502Google Scholar
  57. Telfer WH, Keim PS, Law JH (1983) Arylphorin, a new protein fromHyalophora ceuropia: comparison with calliphorin and manducin. Insect Biochem 13:601–613Google Scholar
  58. Telfer WH, Kunkel JG (1991) The function and evolution of insect storage hexamers. Annu Rev Entomol 36:205–228CrossRefPubMedGoogle Scholar
  59. Turbeville JM, Pfeifer DM, Field KG, Raff RA (1991) The phylogenetic status of arthropods, as inferred from 18S rRNA sequences. Mol Biol Evol 8:669–686PubMedGoogle Scholar
  60. Ueno K, Natori S (1982) Activation of fat body by 20-hydroxyecdysone for the selective incorporation of storage protein inSarcophaga peregrina larvae. Insect Biochem 12:185–191Google Scholar
  61. Ueno K, Natori S (1984) Identification of storage protein receptor in the fat body membranes ofSarcophaga peregrina. J Biol Chem 259:12107–12111PubMedGoogle Scholar
  62. Voit R, Feldmaier-Fuchs G (1990) Arthropod hemocyanins. Molecular cloning and sequencing of cDNAs encoding for tarantula hemocyanins subunits a and e. J Biol Chem 265:19447–19452PubMedGoogle Scholar
  63. Volbeda A, Hol WGJ (1989) Crystal structure of hexameric hemocyanin fromPanulirus interruptus refined at 3.2 Å resolution. J Mol Biol 209:249–279CrossRefPubMedGoogle Scholar
  64. Wang XY, Frohlich DR, Wells MA (1993) Polymorphic cDNAs encode for the methionine-rich storage protein fromManduca sexta. EMBL accession No. L07609Google Scholar
  65. Wang Z, Haunerland N (1994a) Receptor-mediated endocytosis of storage proteins by the fat body ofHelicoverpa zea. Cell Tissue Res 278:107–115Google Scholar
  66. Wang Z, Haunerland N (1994b)Storage protein uptake inHelicoverpa zea: arylphorin and VHDL share a single receptor. Arch Insect Biochem Physiol 26:15–26CrossRefGoogle Scholar
  67. Willot E, Wang X-Y, Wells MA (1989) cDNA and gene sequence ofManduca sexta arylphorin, an aromatic amino acid-rich larval serum protein: homology to arthropod hemocyanins. J Biol Chem 264:19052–19059Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1996

Authors and Affiliations

  • Thorsten Burmester
    • 1
    • 2
  • Klaus Schellen
    • 1
  1. 1.Department of Cell and Developmental Biology, BiocenterUniversity of WürzburgWürzburgGermany
  2. 2.Institut Jacques-MonodCNRS et Universite Paris 7ParisFrance

Personalised recommendations