Skip to main content
SpringerLink
Log in

Quaternary and subunit structure of Calliphora arylphorin as deduced from electron microscopy, electrophoresis, and sequence similarities with arthropod hemocyanin

  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Summary

Arylphorin was purified from larvae of the blowfly Calliphora vicina and studied in its oligomeric form and after dissociation at pH 9.6 into native subunits. In accordance with earlier literature, it was electrophoretically shown to be a 500 kDa hexamer (1×6) consisting of 78 kDa polypeptides (= subunits). Electron micrographs of negatively stained hexamers show a characteristic curvilinear, equilateral triangle of 12 nm in diameter (top view) and a rectangle measuring 10×12 nm (side view). Alternatively, particles in the top view orientation exhibit a roughly circular shape 12 nm in diameter. Crossed immunoelectrophoresis revealed the presence of a major subunit type; the nature of a very minor and a third immunologically separated component remains unclear. A novel 2×6 arylphorin particle was detected and isolated. It comprises less than 10% of the total arylphorin material and shows a long, narrow interhexamer bridge in the electron microscope. An arylphorin dissociation intermediate identified as a trimer (1/2×6) was isolated; its possible quaternary structure is discussed on the basis of electron micrographs. The epitope of monoclonal antibody Ec-7 directed against tarantula (Eurypelma californicum) hemocyanin subunit d and also reactive to Calliphora arylphorin was traced to a highly conserved peptide of 27 amino acids localized in the center of the protein. The primary structure of Calliphora arylphorin as published in our preceding paper (Naumann and Scheller 1991) is compared in detail to the sequences of spider and spiny lobster hemocyanin. This revealed a basic framework of 103 strictly conserved amino acids. Isofunctional exchanges are proposed for another 76 positions. On the basis of these similarities, and the published three-dimensional model of spiny lobster hemocyanin, a detailed model of the quaternary structure of Calliphora arylphorin is presented. A second larval storage protein previously termed protein II was purified from Calliphora hemolymph. It was demonstrated to be a 500 kDa hexamer of 83 kDa subunits. In the electron microscope it shows a cubic view 9 nm in length with a large central hole and a rectangular view (9×10 nm) with a large central cavity. A morphologically very similar hemolymph protein was detected in Drosophila melanogaster larvae. From its structural appearance it is uncertain whether protein II belongs to the hemocyanin superfamily or not.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

FPLC:

fast performance liquid chromatography

HPLC:

high performance liquid chromatography

LSP:

Larval serum protein

PAGE:

Polyacrylamide gel electrophoresis

SDS:

Sodium dodecyl sulphate

Tris:

Tris-(hydroxymethyl)-aminomethane

References

  • Agrawal OP, Scheller K (1990) Sclerotization of insect cuticle in a cell free system. Z Naturforsch [C] 45: 129–131

    Google Scholar 

  • Bak HJ, Beintema JJ (1987) Panulirus interruptus hemocyanin. The elucidation of the complete amino acid sequence of subunit a. Eur J Biochem 169: 333–348

    Google Scholar 

  • Bruggen EFJ van, Bijlholt MMC, Schutter WG, Wichertjes T, Bonaventura J, Bonaventura C, Lamy J, Lamy J, Leclerc M, Schneider H-J, Markl J, Linzen B (1980) The role of structurally diverse subunits in the assembly of three cheliceratan hemocyanins. FEBS Lett 116: 207–210

    Google Scholar 

  • Bruggen EFJ van, Schutter WG, Breemen JFL van, Bijlholt MMC, Wichertjes T (1981) The hemocyanins. In: Harris JR (ed) Electron microscopy of proteins, 1. Academic Press, London New York, pp 1–38

    Google Scholar 

  • Burmester T, Scheller K (1992) Identification of binding proteins involved in the stage-specific uptake of arylphorin by the fat body cells of Calliphora vicina. Insect Biochem Molec Biol 22: 211–220

    Google Scholar 

  • Chang JY, Brauer D, Wittmann-Liebold B (1978) Micro-sequence analysis of peptides and proteins using 4-NN-dimethylaminoazobenzene 4′-isothiocyanate/phenylisothiocyanate double coupling method. FEBS Lett 93: 205–214

    Google Scholar 

  • Chrisanthis G, Marmaras VJ, Christodoulou C (1981) Major haemolymph proteins in Ceratitis capitata: biosynthesis and secretion during development. Wilhelm Roux's Arch 190: 33–39

    Google Scholar 

  • Decker H, Sterner R (1990) Nested allostery of arthropodan hemocyanin (Eurypelma californicum and Homarus americanus): the role of the protons. J Mol Biol 211: 281–293

    Google Scholar 

  • Drexel R, Siegmund S, Schneider H-J, Linzen B, Gielens C, Preaux G, Lontie R, Kellermann J, Lottspeich F (1987) Complete amino-acid sequence of a functional unit from a molluscan hemocyanin (Helix pomatia). Biol Chem Hoppe Seyler 368: 617–635

    Google Scholar 

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

    Google Scholar 

  • Ellerton HD, Ellerton NF, Robinson HA (1983) Hemocyanin-a current perspective. Prog Biophys Mol Biol 41: 143–248

    Google Scholar 

  • Enderle U, Kauser G, Reum K, Scheller K, Koolman J (1983) Ecdysteroids in the hemolymph of blowfly larvae are bound to calliphorin. In: Scheller K (ed) The larval serum proteins of insects. Thieme, Stuttgart New York, pp 40–49

    Google Scholar 

  • Fahrenbach WH (1970) The cyanoblast: hemocyanin formation in Limulus polyphemus. J Cell Biol 44: 445–453

    Google Scholar 

  • Ferguson KA (1964) Starch-gel-electrophoresis-application to the classification of pituitary proteins and polypeptides. Metabolism 13: 985–1002

    Google Scholar 

  • Fujii T, Sakurai H, Izumi S, Tomino S (1989) Structure of the gene for the arylphorin-type storage protein SP2 of Bombyx mori. J Biol Chem 264: 11020–11025

    Google Scholar 

  • Gaykema WPJ, Hol WGJ, Vereijken JM, Soeter NM, Bak HJ, Beintema JJ (1984) 3.2 A structure of the copper-containing, oxygen-carrying protein Panulirus interruptus hemocyanin. Nature 309: 23–29

    Google Scholar 

  • Haas F de, Bijholt MMC, Bruggen EFJ van (1991) An electron microscopic study of two-hexameric hemocyanins from the crab Cancer pagurus and the tarantula Eurypelma californicum: determination of their quaternary structure using image processing and simulation models based on X-ray diffraction data. J Struct Biol 107: 86–94

    Google Scholar 

  • Harris JR, Horne RW (1991) Negative staining. In: Harris JR (ed) Electron microscopy in biology. TRL Press, Oxford, pp 203–228

    Google Scholar 

  • Hedrick JL, Smith AJ (1968) Size and charge isomer separation and estimation of molecular weights of proteins by disk gel electrophoresis. Arch Biochem Biophys 126: 155–164

    Google Scholar 

  • Herskovits TT (1988) Recent aspects of the subunit organization and dissociation of hemocyanins. Comp Biochem Physiol [B] 91: 597–611

    Google Scholar 

  • Holde KE van, Miller KJ (1982) Haemocyanins. Q Rev Biophys 15: 1–129

    Google Scholar 

  • Jeffrey PD (1979) Hemocyanin from the Australian freshwater crayfish Cherax destructor. Electron microscopy of native and reassembled molecules. Biochemistry 18: 2508–2513

    Google Scholar 

  • Jekel PA, Bak HJ, Soeter NM, Vereijken 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

    Google Scholar 

  • Johnes G, Brown N, Manczak M, Shivanand H, Kafatos FC (1990) Molecular cloning, regulation and complete sequence of a hemocyanin-related, juvenile hormone-suppressible protein from insect hemolymph. J Biol Chem 265: 8596–8602

    Google Scholar 

  • Kefaliakou-Bourdopoulou M, Christodoulou C, Marmaras VJ (1981) Storage proteins on the olive fruit fly, Dacus oleae: Characterization and immunological studies. Insect Biochem 11: 707–711

    Google Scholar 

  • Kejzlarova-Lepesant J, Mousseron S, Benes H, Jowett T, Chihara C, Claverie J-M, Lepesant J-A (1987) Structure and expression of the LSP-2 gene of Drosophila melanogaster. Biol Chem Hoppe Seyler 368: 575–576

    Google Scholar 

  • Kempter B, Markl J, Brenowitz M, Bonaventura C, Bonaventura J (1985) Immunological correspondence between arthropod hemocyanin subunits II. Xiphosuran (Limulus) and spider (Eurypelma, Cupiennius) hemocyanin. Biol Chem Hoppe Seyler 366: 77–86

    Google Scholar 

  • Kinnear JF, Thomson JA (1975) Nature, origin and fate of major hemolymph proteins in Calliphora. Insect Biochem 5: 531–552

    Google Scholar 

  • König M, Agrawal OP, Schenkel H, Scheller K (1986) Incorporation of calliphorin into the cuticle of the developing blowfly, Calliphora vicina. Roux's Arch Dev Biol 195: 296–301

    Google Scholar 

  • Kramer SJ, Mundall EC, Law JH (1980) Purification and properties of manducin, an aminoacid storage protein of the haemolymph of larval and pupal Manduca sexta. Insect Biochem 10: 279–288

    Google Scholar 

  • Kroll J (1973) Crossed-line immunoelectrophoresis. Scand J Immunol 2 [Suppl 1]: 79–81

    Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685

    Google Scholar 

  • Lamy J, Lamy J, Weill J, Markl J, Schneider H-J, Linzen B (1979) Hemocyanins in spiders, VII. Immunological comparison of the subunits of Eurypelma californicum hemocyanin. Hoppe-Seyler's Z Physiol Chem 360: 889–895

    Google Scholar 

  • Lamy J, Billiald P, Taveau JC, Boisset N, Motta G, Lamy J (1990) Topological mapping of 13 epitopes on a subunit of Androctonus australis hemocyanin. J Struct Biol 103: 64–74

    Google Scholar 

  • Lang WH, Holde KE van (1991) Cloning and sequencing of Octopus dofleini hemocyanin cDNA: derived sequences of functional units Ode and Odf. Proc Natl Acad Sci USA 88: 244–248

    Google Scholar 

  • Levenbook L (1983) The structure and function of calliphorin. In: Scheller K (ed) The larval serum proteins of insects. Thieme, Stuttgart New York, pp 1–17

    Google Scholar 

  • Levenbook L (1985) Insect storage proteins. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 307–346

    Google Scholar 

  • Levenbook L, Bauer AC (1980) Caliphorin and soluble protein of haemolymph and tissues during larval growth, and adult development of Calliphora vicina. Insect Biochem 10: 693–701

    Google Scholar 

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

    Google Scholar 

  • Linzen B, Soeter MN, Riggs AF, Schneider H-J, Schartau W, Moore MD, Yokota E, 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

    Google Scholar 

  • Magnus K, Lattman EE, Volbeda A, Hol WGJ (1991) Hexamers of subunit II from Limulus hemocyanin (a 48-mer) have the same quaternary structure as whole Panulirus hemocyanin molecules. Proteins 9: 240–247

    Google Scholar 

  • Mangum CP, Johansen K (1975) The colloid osmotic pressures of invertebrate body fluids. J Exp Zool 63: 661–671

    Google Scholar 

  • Mangum CP, Scott JL, Black REL, Miller KI, Holde KE van (1985) Centipedal hemocyanin: its structure and its implications for arthropod phylogeny. Proc Natl Acad Sci USA 82: 3721–3725

    Google Scholar 

  • Markl J (1980) Hemocyanins in spiders. XI. The quaternary structure of Cupiennius hemocyanin. J Comp Physiol [B] 140: 199–207

    Google Scholar 

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

    Google Scholar 

  • Markl J, Decker H (1992) Molecular structure of the arthropod hemocyanins. Adv Comp Environ Physiol 13: 325–376

    Google Scholar 

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

    Google Scholar 

  • Markl J, Decker H, Stöcker W, Linzen B, Schutter WG, Bruggen EFJ van (1981a) On the role of dimeric subunits in the quaternary structure of arthropod hemocyanins. Hoppe-Seyler's Z Physiol Chem 362: 185–188

    Google Scholar 

  • Markl J, Kempter B, Linzen B, Bijlholt MMC, Bruggen EFJ van (1981b) Hemocyanins in spiders, XVI. Subunit topography and a model of the quaternary structure of Eurypelma hemocyanin. Hoppe-Seyler's Z Physiol Chem 362: 1631–1641

    Google Scholar 

  • Markl J, Savel A, Linzen B (1981c) Hemocyanins in spiders, XIV. Subunit composition of dissociation intermediates, and its bearing on the quanternary structure of Eurypelma hemocyanin. Hoppe-Seyler's Z Physiol Chem 362: 1255–1262

    Google Scholar 

  • Markl J, Stumpp S, Bosch FX, Voit R (1990) Hemocyanin biosynthesis in the tarantula Eurypelma californicum, studied by in situ hybridization and immuno-electron microscopy. In: Preaux G (ed) Invertebrate dioxygen carriers. University Press, Leuven, pp 497–502

    Google Scholar 

  • Martin MD, Kinnear JF, Thomson JA (1971) Developmental stages in the late larva of Calliphora stygia. IV. Uptake of plasma protein by the fat body. Aust J Biol Sci 24: 291–299

    Google Scholar 

  • Marx R (1983) Ultrastructural aspects of protein synthesis and protein transport in larvae of Calliphora vicina. In: Scheller K (ed) The larval serum proteins of insects. Thieme, Stuttgart New York, pp 50–60

    Google Scholar 

  • Maurer HR (1968) Disk-Electrophorese. Walter de Gruyter, Berlin

    Google Scholar 

  • Mian IS, Bradwell AR, Olson AJ (1991) Structure, function and properties of antibody binding sites. J Mol Biol 217: 133–151

    Google Scholar 

  • Mousseron S (1986) Contribution a l'etude structurale du gene LSP-2 de Drosophila melanogaster: determination de sa sequence nucleotidique complete. Thesis; l'Ecole Pratique des Hautes Etudes, Paris

  • Munn EA, Greville GD (1969) The soluble proteins of developing Calliphora erythrocephala, particularly calliphorin, and similar proteins in other insects. J Insect Physiol 15: 1935–1950

    Google Scholar 

  • Munn EA, Feinstein A, Greville GD (1967) A major protein constituent of pupae of the blowfly, Calliphora erythrocephala (Diptera). Biochem J 102: 5–6P

    Google Scholar 

  • Munn EA, Feinstein A, Greville GD (1971) The isolation and properties of the protein calliphorin. Biochem J 124: 367–374

    Google Scholar 

  • Naumann U, Scheller K (1991) Complete cDNA and gene sequence of the developmentally regulated arylphorin of Calliphora vicina and its homology to insect hemolymph proteins and arthropod hemocyanins. Biochem Biophys Res Commun 177: 963–972

    Google Scholar 

  • Palli SR, Locke M (1987) Purification and localization of the three major haemolymph proteins of an insect, Calpodes ethlius (Lepidoptera, Hesperiidae). Arch Insect Biochem Biophys 5: 233–245

    Google Scholar 

  • Rehn KG, Rolim ALR (1990) Purification and properties of a storage protein from the hemolymph of Rhodnius prolixus. Insect Biochem 20: 195–201

    Google Scholar 

  • Roberts DB (1983) The evolution of the larval serum protein genes in Drosophila. In: Scheller K (ed) The larval serum proteins in insects. Thieme, Stuttgart New York, pp 86–100

    Google Scholar 

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

    Google Scholar 

  • Roberts D, Wolfe J, Akam M (1977) The developmental profiles of two major haemolymph proteins from Drosophila melanogaster. J Insect Physiol 23: 871–878

    Google Scholar 

  • Roberts DB, Jowett T, Hughes J, Smith DF, Glover DM (1991) The major serum proteins of Drosophila larvae, larval serum protein 1, is dispensable. Eur J Biochem 195: 195–201

    Google Scholar 

  • Sakurai H, Fujii T, Izumi S, Tomino S (1988) Structure and expression of gene coding for sex-specific storage protein of Bombyx mori. J Biol Chem 263: 7876–7880

    Google Scholar 

  • Salvato B, Beltramini M (1990) Hemocyanin molecular architecture: structure and reactivity of the binuclear copper-active site. Life Chem Rep 8: 1–47

    Google Scholar 

  • Sato JD, Roberts DB (1983) Synthesis of larval serum proteins 1 and 2 of Drosophila melanogaster by third instar fat body. Insect Biochem 13: 1–5

    Google Scholar 

  • Savel-Niemann A, Markl J, Linzen B (1988) Hemocyanins in spiders, XXII. Range of allosteric interaction in a four-hexamer hemocyanin. Co-operativity and Bohr effect in dissociation intermediates. J Mol Biol 204: 385–395

    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 from Eurypelma californicum hemocyanin, and comparison to chain e. Hoppe-Seyler's Z Physiol Chem 364: 1383–1409

    Google Scholar 

  • Scheller K (1983) The larval serum proteins of insects. Thieme, Stuttgart New York, pp 1–190

    Google Scholar 

  • Scheller K (1987) 3rd Workshop in Larval Serum Proteins on Insects. Biol Chem Hoppe Seyler 368: 571–578

    Google Scholar 

  • Scheller K, Zimmermann H-P, Sekeris CE (1980) Calliphorin, a protein involved in the cuticle formation of the blowfly, Calliphora vicina. Z Naturforsch [C] 35: 387–389

    Google Scholar 

  • Scheller K, Fischer B, Schenkel H (1990) Molecular properties, functions and developmentally regulated biosynthesis of arylphorin in Calliphora vicina. In: Hagedorn HH, Hildebrand JG, Kidwell MG, Law JH (eds) Molecular insect science. Plenum Press, New York, pp 155–162

    Google Scholar 

  • Schenkel H, Kejzlarova-Lepesant J, Berreur P, Moreau J, Scheller K, Bregegere F, Lepesant J-A (1985) Identification and molecular analysis of a multigene family encoding calliphorin, the major larval serum protein of Calliphora vicina. EMBO J 4: 2983–2990

    Google Scholar 

  • Schneider HJ, Drexel R, Feldmaier G, Linzen B, Lottspeich F, Henschen A (1983) Hemocyanins in spiders, XVIII. Complete amino-acid sequence of subunit e from Eurypelma californicum hemocyanin. Hoppe-Seyler's Z Physiol Chem 364: 1357–1381

    Google Scholar 

  • Schneider H-J, Voll W, Lehmann L, Grißhammer R, Goettgens A, Linzen B (1986) Partial amino acid sequence of crayfish (Astacus leptodactylus) hemocyanin. In: Linzen B (ed) Invertebrate oxygen carriers. Springer, Berlin Heidelberg New York, pp 172–176

    Google Scholar 

  • Schram FR (1982) The fossil record and evolution of Crustacea. In: Abele LG (ed) The biology of the Crustacea. Academic Press New York, pp 93–147

    Google Scholar 

  • Sekeris CE, Scheller K (1977) Calliphorin, a major protein of the blowfly: correlation between the amount of protein, its biosynthesis, and the titre of translatable calliphorin-mRNA during development. Dev Biol 59: 12–23

    Google Scholar 

  • Siezen RJ, Bruggen EFJ van (1974) Structure and properties of hemocyanins. XII. Electron microscopy of dissociation products of Helix pomatia alpha hemocyanin: quaternary structure. J Mol Biol 96: 77–80

    Google Scholar 

  • Stöcker W, Raeder U, Bijlholt MMC, Wichertjes T, Bruggen EFJ van, Markl J (1988) The quaternary structure of four crustacean 2×6 hemocyanins: immunocorrelation, stoichiometry, reassembly and topology of individual subunits. J Comp Physiol [B] 158: 271–289

    Google Scholar 

  • Swanson RM (1984) A unifying concept for the amino acid code. Bull Math Biol 42: 187–203

    Google Scholar 

  • Telfer WH, Massey HC (1987) A storage hexamer from Hyalophora that binds riboflavin and resembles the apoprotein of hemocyanin. In: Law J (ed) Molecular entomology. Liss, New York, pp 305–314

    Google Scholar 

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

    Google Scholar 

  • Telfer WH, Keim PS, Law JH (1983) Arylphorin, a new protein from Hyalophora cecropia: comparisons with calliphorin and manducin. Insect Biochem 13: 601–613

    Google Scholar 

  • Terwilliger N (1982) Effect of subunit composition on the quaternary structure of isopod (Ligia pallasii) hemocyanin. Biochemistry 21: 2579–2586

    Google Scholar 

  • Traut TW (1988) Do exons code for structural or functional units in proteins? Proc Natl Acad Sci USA 85: 2944–2948

    Google Scholar 

  • Ueno K, Ohsawa F, Natori S (1983) Identification and activation of storage protein receptor of Sarcophaga peregrina fat body by 20-hydroxyecdysone. J Biol Chem 258: 12210–12214

    Google Scholar 

  • Voit R, Feldmaier-Fuchs G (1990) Arthropod hemocyanins: molecular cloning and sequencing of cDNAs encoding the tarantula hemocyanin subunits a and e. J Biol Chem 265: 19447–19452

    Google Scholar 

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

    Google Scholar 

  • Volbeda A, Hol WGJ (1989b) Pseudo 2-fold symmetry in the copper-binding domain of arthropodan haemocanins. Possible implications for the evolution of oxygen transport proteins. J Mol Biol 206: 531–546

    Google Scholar 

  • Voll W, Voit R (1990) Characterization of the gene encoding the hemocyanin subunit e from the tarantula Eurypelma californicum. Proc Natl Acad Sci USA 87: 5312–5316

    Google Scholar 

  • Webb BA, Riddiford LM (1988) Synthesis of two storage proteins during larval development of the tabacco hornworm, Manduca sexta. Develop Biol 130: 671–681

    Google Scholar 

  • Weeke B (1973) Crossed immunoelectrophoresis. Scand J Immunol 2 [Suppl 1]: 47–56

    Google Scholar 

  • Wichertjes T, Keegstra W, Neuteboom B, Hazes B, Beintema JJ, Bruggen EFJ van (1989) Crystallization properties and structure of Panulirus interruptus haemocyanin. Eur J Biochem 184: 287–296

    Google Scholar 

  • Willot E, Wang X-Y, Wells MA (1989) cDNA and gene sequence of Manduca sexta arylphorin, an aromatic amino acid-rich larval serum protein. Homology to arthropod hemocyanin. J Biol Chem 264: 19052–19059

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Zoologie, Universität Mainz, Saarstraße 21, W-6500, Mainz, Federal Republic of Germany

    Jürgen Markl, J. Robin Harris & Michaela Süling

  2. Theodor Boveri Institut (Biozentrum), Universität Würzburg, W-8700, Würzburg, Federal Republic of Germany

    Thorsten Burmester, Ulrike Naumann & Klaus Scheller

  3. Zoologisches Institut, Universität München, W-8000, München 2, Federal Republic of Germany

    Heinz Decker & Anette Savel-Niemann

Authors
  1. Jürgen Markl
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thorsten Burmester
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heinz Decker
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anette Savel-Niemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Robin Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michaela Süling
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ulrike Naumann
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Klaus Scheller
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Markl, J., Burmester, T., Decker, H. et al. Quaternary and subunit structure of Calliphora arylphorin as deduced from electron microscopy, electrophoresis, and sequence similarities with arthropod hemocyanin. J Comp Physiol B 162, 665–680 (1992). https://doi.org/10.1007/BF00301616

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00301616

Key words

Search

Navigation