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

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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.

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Abbreviations

aa:

amino acid

MYA:

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

References

  • 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 18:11–19

    CAS  Google Scholar 

  • 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 92:939–943

    CAS  PubMed  Google Scholar 

  • Aspan A, Söderhäll K (1991) Purification of prophenoloxidase from crayfish blood cells, and its activation by an endogenous serine proteinase. Insect Biochem 21:363–373

    CAS  Google Scholar 

  • Bak HJ, Beintema JJ (1987)Panulirus interruptus hemocyanin. The elucidation of the complete amino acid sequence of subunit a. FEBS Lett 204:141–144

    Google Scholar 

  • Beintema JJ, Stam WT, Hazes B, Smidt MP (1994) Evolution of arthropod hemocyanins and insect storage proteins (hexamerins). Mol Biol Evol 11:493–503

    CAS  PubMed  Google Scholar 

  • 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 33–56

    Google Scholar 

  • 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 22:211–220

    CAS  Google Scholar 

  • 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 25:799–806

    CAS  Google Scholar 

  • 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 25:981–989

    CAS  PubMed  Google Scholar 

  • Chung SO, Kubo T, Natori S (1995) Molecular cloning and sequencing of arylphorin-binding protein in protein granules ofSarcophaga fat body. J Biol Chem 270:4624–4631

    CAS  PubMed  Google Scholar 

  • Dayhoff MO (1979) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Washington, DC

    Google Scholar 

  • de Haas F, van Bruggen EFJ (1994) The interhexameric contacts in the four-hexameric hemocyanin from the tarantulaEurypelma californicum. J Mol Biol 237:464–478

    PubMed  Google Scholar 

  • 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 40:527–535

    Google Scholar 

  • Doolittle RF (1981) Similar amino acid sequences: chance or common ancestry? Science 214:149–159

    CAS  PubMed  Google Scholar 

  • 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 368:617–635

    CAS  PubMed  Google Scholar 

  • Duhamel RC, Kunkel JG (1983) Cockroach larval-specific protein, a tyrosine-rich serum protein. J Biol Chem 258:14461–14465

    CAS  PubMed  Google Scholar 

  • Duhamel RC, Kunkel JG (1987) Moulting-cycle regulation of haemolymph protein clearance in cockroaches possible size-dependent mechanism. J Insect Physiol 33:155–158

    Article  CAS  Google Scholar 

  • 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 40–49

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1993) PHYLIP: (phylogeny inference package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle

    Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specified tree topology. System Zool 20:406–416

    Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284

    CAS  PubMed  Google Scholar 

  • 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 264:11020–11025

    CAS  PubMed  Google Scholar 

  • 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: 23–29

    Article  CAS  Google Scholar 

  • 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. L42556

  • Hennig W (1969) Stammesgeschichte der Insekten. W Kramer, Frankfurt

    Google Scholar 

  • 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: 403–412

    Article  CAS  PubMed  Google Scholar 

  • 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 25:8596–8602

    Google Scholar 

  • 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 268:1284–1291

    CAS  PubMed  Google Scholar 

  • 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 41:509–518

    Article  CAS  Google Scholar 

  • Levenbook L, Bauer A (1984) The fate of the larval storage protein calliphorin during adult development ofCalliphora vicina. Insect Biochem 14:77–86

    CAS  Google Scholar 

  • 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 229:519–524

    CAS  PubMed  Google Scholar 

  • 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 12:431–440

    CAS  Google Scholar 

  • Marinotti O, de Bianchi AG (1986) Uptake of storage protein byMusca fat body. J Insect Physiol 32:819–825

    Article  CAS  Google Scholar 

  • Markl J (1986) Evolution and function of structurally diverse subunits in the respiratory protein hemocyanin from arthropods. Biol Bull 171: 90–115

    CAS  Google Scholar 

  • 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] 162:665–680

    CAS  Google Scholar 

  • Markl J, Markl A, Schartau W, Linzen B (1979a) Subunit heterogeneity in arthropod hemocyanins: I. Chelicerata. J Comp Physiol 130: 283–292

    CAS  Google Scholar 

  • 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 133:67–175

    Google Scholar 

  • Markl J, Winter S (1989)Subunit-specific monoclonal antibodies of tarantula hemocyanin, and a common epitope shared with calliphorin. J Comp Physiol [B] 159:139–151

    CAS  Google Scholar 

  • 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 24:291–299

    CAS  PubMed  Google Scholar 

  • Maschat F, Dubertret ML, Therond P, Claverie JM, Lepesant JA (1990) Structure of the ecdysone-inducible P1 gene ofDrosophila melanogaster. J Mol Biol 214:359–372

    Article  CAS  PubMed  Google Scholar 

  • 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 24:133–144

    CAS  PubMed  Google Scholar 

  • Memmel NA, Trewitt PM, Silhacek DL, Kumaran AK (1992) Nucleotide sequence and structure of the arylphorin gene fromGalleria mellonella. Insect Biochem Mol Biol 22:333–342

    CAS  Google Scholar 

  • 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 12:293–300

    CAS  Google Scholar 

  • Müller G, Ruppert S, Schmid E, Schütz G (1988) Functional analysis of alternatively spliced tyrosinase gene transcripts. EMBO J 7: 2723–2730

    PubMed  Google Scholar 

  • Nakashima H, Behrens PQ, Moore MD, Yokota E, Riggs AF (1986) Structure of hemocyanin 11 from the horseshoe crab,Limulus polyphemus. J Biol Chem 261:10526–10533

    CAS  PubMed  Google Scholar 

  • 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 177:963–972

    Article  CAS  PubMed  Google Scholar 

  • Neuteboom B, Jekel PA, Beintema JJ (1992) Primary structure of hemocyanin subunit c fromPanulirus interruptus. Eur J Biochem 206:243–249

    Article  CAS  PubMed  Google Scholar 

  • Pan MI, Telfer WH (1992) Selectivity in storage hexamerin clearing demonstrated with hemolymph transfusions betweenHyalophora cecropia andActias luna. Arch Insect Biochem Physiol 19:203–219

    Article  CAS  PubMed  Google Scholar 

  • 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 115–124

    Google Scholar 

  • Roberts DB, Brock HW (1981) The major serum proteins of diptera larvae. Experientia 37:103–110

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sakurai H, Tomoko F, Izumi S, Tomino S (1988) Complete nucleotide sequence of gene for sex-specific storage protein ofBombyx mori. Nucleic Acids Res 16:7717–7718

    CAS  PubMed  Google Scholar 

  • 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 364:1383–1409

    CAS  PubMed  Google Scholar 

  • 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 155–162

    Google Scholar 

  • Sellos DY (1995) EMBL accession No. X82502

  • Telfer WH, Keim PS, Law JH (1983) Arylphorin, a new protein fromHyalophora ceuropia: comparison with calliphorin and manducin. Insect Biochem 13:601–613

    CAS  Google Scholar 

  • Telfer WH, Kunkel JG (1991) The function and evolution of insect storage hexamers. Annu Rev Entomol 36:205–228

    Article  CAS  PubMed  Google Scholar 

  • Turbeville JM, Pfeifer DM, Field KG, Raff RA (1991) The phylogenetic status of arthropods, as inferred from 18S rRNA sequences. Mol Biol Evol 8:669–686

    CAS  PubMed  Google Scholar 

  • Ueno K, Natori S (1982) Activation of fat body by 20-hydroxyecdysone for the selective incorporation of storage protein inSarcophaga peregrina larvae. Insect Biochem 12:185–191

    CAS  Google Scholar 

  • Ueno K, Natori S (1984) Identification of storage protein receptor in the fat body membranes ofSarcophaga peregrina. J Biol Chem 259:12107–12111

    CAS  PubMed  Google Scholar 

  • 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 265:19447–19452

    CAS  PubMed  Google Scholar 

  • Volbeda A, Hol WGJ (1989) Crystal structure of hexameric hemocyanin fromPanulirus interruptus refined at 3.2 Å resolution. J Mol Biol 209:249–279

    Article  CAS  PubMed  Google Scholar 

  • Wang XY, Frohlich DR, Wells MA (1993) Polymorphic cDNAs encode for the methionine-rich storage protein fromManduca sexta. EMBL accession No. L07609

  • Wang Z, Haunerland N (1994a) Receptor-mediated endocytosis of storage proteins by the fat body ofHelicoverpa zea. Cell Tissue Res 278:107–115

    CAS  Google Scholar 

  • Wang Z, Haunerland N (1994b)Storage protein uptake inHelicoverpa zea: arylphorin and VHDL share a single receptor. Arch Insect Biochem Physiol 26:15–26

    Article  CAS  Google Scholar 

  • 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 264:19052–19059

    Google Scholar 

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  1. Thorsten Burmester

    Present address: Institut Jacques-Monod, CNRS et Universite Paris 7, 2, place Jussieu, F-75251, Paris, Cedex 05, France

Authors and Affiliations

  1. Department of Cell and Developmental Biology, Biocenter, University of Würzburg, Am Hubland, D-97074, Würzburg, Germany

    Thorsten Burmester & Klaus Schellen

  2. Institut Jacques-Monod, CNRS et Universite Paris 7, 2, place Jussieu, F-75251, Paris, Cedex 05, France

    Thorsten Burmester

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  1. Thorsten Burmester
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  2. Klaus Schellen
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Correspondence to: T. Burmester

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Burmester, T., Schellen, K. Common origin of arthropod tyrosinase, arthropod hemocyanin, insect hexamerin, and dipteran arylphorin receptor. J Mol Evol 42, 713–728 (1996). https://doi.org/10.1007/BF02338804

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