Evolution of molluscan hemocyanin structures

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 9, 2013, Pages 1840-1852

  Markl, Jürgen ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Electron microscopy; Evolution; Hemocyanin; Keyhole limpet hemocyanin; KLH; Mollusca; Quaternary structure; Respiratory proteins

Indexed keywords

AMINO ACID; HEMOCYANIN; HETERODIMER; KEYHOLE LIMPET HEMOCYANIN; OLIGOMER; POLYPEPTIDE; ISOPHANE INSULIN; PHORBOL DIBUTYRATE;

ADAPTIVE RADIATION; ARTICLE; BIOMPHALARIA GLABRATA; BIVALVE; CEPHALOPOD; CHITON; CRYSTAL STRUCTURE; DNA SEQUENCE; ELECTRON MICROSCOPY; GASTROPOD; GENE DUPLICATION; GENE STRUCTURE; HEMOLYMPH; MOLECULAR CLOCK; MOLECULAR EVOLUTION; MOLLUSC; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; PROTEIN SUBUNIT; SCAPHOPOD; X RAY CRYSTALLOGRAPHY; 3D-EM; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON MICROSCOPY DATA BANK; EMDB; EVOLUTION; FU; FUNCTIONAL UNIT; HALIOTIS DIVERSICOLOR HEMOCYANIN; HDH; KLH; MELANOIDES TUBERCULATA HEMOCYANIN; METABOLISM; MTH; NAUTILUS POMPILIUS HEMOCYANIN; OCTOPUS (=ENTEROCTOPUS) DOFLEINI HEMOCYANIN; ODH; PROTEIN CONFORMATION; PROTEIN DATA BANK; RESPIRATORY PROTEINS; REVIEW; SEPIA OFFICINALIS HEMOCYANIN; SOH; THREE-DIMENSIONAL ELECTRON MICROSCOPY;

ANIMALIA; ARTHROPODA; MOLLUSCA;

3D-EM; ELECTRON MICROSCOPY; ELECTRON MICROSCOPY DATA BANK; EMDB; EVOLUTION; FU; FUNCTIONAL UNIT; HALIOTIS DIVERSICOLOR HEMOCYANIN; HDH; HEMOCYANIN; KEYHOLE LIMPET HEMOCYANIN; KLH; MELANOIDES TUBERCULATA HEMOCYANIN; MOLLUSCA; MTH; NAUTILUS POMPILIUS HEMOCYANIN; NPH; OCTOPUS (=ENTEROCTOPUS) DOFLEINI HEMOCYANIN; ODH; PDB; PROTEIN DATA BANK; QUATERNARY STRUCTURE; RESPIRATORY PROTEINS; SEPIA OFFICINALIS HEMOCYANIN; SOH; THREE-DIMENSIONAL ELECTRON MICROSCOPY;

ANIMALS; BIOLOGICAL EVOLUTION; CRYSTALLOGRAPHY, X-RAY; HEMOCYANIN; MODELS, MOLECULAR; MOLLUSCA; PROTEIN CONFORMATION;

EID: 84884661197     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.02.020     Document Type: Article

References (109)

1. K.E. van Holde, K.I. Miller, Hemocyanins, Adv. Protein Chem. 47 (1995) 1-81.
2. T. Burmester, K. Scheller, Common origin of arthropod tyrosinase, arthropod hemocyanin, insect hexamerin, and dipteran arylphorin receptor, J. Mol. Evol. 42 (1996) 713-728. (Pubitemid 26244153)
3. H. Decker, T. Schweikardt, F. Tuczek, The first crystal structure of tyrosinase: all questions answered? Angew. Chem. Int. Ed Engl. 45 (2006) 4546-4550. (Pubitemid 44106069)
4. H. Decker, N. Hellmann, E. Jaenicke, B. Lieb, U. Meissner, J. Markl, Minireview: Recent progress in hemocyanin research, Integr. Comp. Biol. 47 (2007) 631-644. (Pubitemid 351176849)
5. H. Decker, N. Terwilliger, COPs and robbers: evolution of copper oxygen proteins, J. Exp. Biol. 203 (2000) 1777-1782. (Pubitemid 30441782)
6. Y. Matoba, T. Kumagai, A. Yamamoto, H. Yoshitsu, M. Sugiyama, Crystallographic evidence that the dinuclear copper center of tyrosinase is flexible during catalysis, J. Biol. Chem. 281 (2006) 8981-8990. (Pubitemid 43848005)
7. B. Lieb, B. Altenhein, J. Markl, The sequence of a gastropod hemocyanin (HtH1 from Haliotis tuberculata), J. Biol. Chem. 275 (2000) 5675-5681. (Pubitemid 30115207)
8. B. Lieb, J. Markl, Evolution of molluscan hemocyanins as deduced from DNA sequencing, Micron 35 (2004) 117-119. (Pubitemid 38214839)
9. T. Burmester, Origin and evolution of arthropod hemocyanins and related proteins, J. Comp. Physiol. B 172 (2002) 95-117.
10. T. Burmester, Molecular evolution of the arthropod hemocyanin superfamily, Mol. Biol. Evol. 18 (2001) 184-195. (Pubitemid 32118863)
11. K. Kusche, H. Ruhberg, T. Burmester, A hemocyanin from the Onychophora and the emergence of respiratory proteins, Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 10545-10548.
12. A.G. Martin, F. Depoix, M. Stohr, U. Meissner, S. Hagner-Holler, K. Hammouti, T. Burmester, J. Heyd, W. Wriggers, J. Markl, Limulus polyphemus hemocyanin: 10 Å cryo-EM structure, sequence analysis, molecular modelling and rigid-body fitting reveal the interfaces between the eight hexamers, J. Mol. Biol. 366 (2007) 1332-1350. (Pubitemid 46186383)
13. C. Pick, M. Schneuer, T. Burmester, The occurrence of hemocyanin in Hexapoda, FEBS J. 276 (2009) 1930-1941.
14. Y. Cong, Q. Zhang, D. Woolford, T. Schweikardt, H. Khant, M. Dougherty, S.J. Ludtke, W. Chiu, H. Decker, Structural mechanism of SDS-induced enzyme activity of scorpion hemocyanin revealed by electron cryomicroscopy, Structure 17 (2009) 749-758.
15. M. Paoli, F. Giomi, N. Hellmann, E. Jaenicke, H. Decker, P. Di Muro, M. Beltramini, The molecular heterogeneity of hemocyanin: Structural and functional properties of the 4×6-meric protein of Upogebia pusilla (Crustacea), Gene 398 (2007) 177-182. (Pubitemid 47068884)
16. P. Rehm, C. Pick, J. Borner, J. Markl, T. Burmester, The diversity and evolution of chelicerate hemocyanins, BMC Evol. Biol. 12 (2012) 19.
17. I. Mičetić, C. Losasso, P.D. Muro, G. Tognon, P. Benedetti, M. Beltramini, Solution structures of 2×6-meric and 4×6-meric hemocyanins of crustaceans Carcinus aestuarii, Squilla mantis and Upogebia pusilla, J. Struct. Biol. 171 (2010) 1-10.
18. J. Markl, A. Moeller, A.G. Martin, J. Rheinbay, W. Gebauer, F. Depoix, 10-Å cryoEM structure and molecular model of the Myriapod (Scutigera) 6×6mer hemocyanin: understanding a giant oxygen transport protein, J. Mol. Biol. 392 (2009) 362-380.
19. U. Albrecht, H. Keller, W. Gebauer, J. Markl, Rhogocytes (pore cells)as the site ofhemocyanin biosynthesis inthe marine gastropod Haliotis tuberculata, Cell Tissue Res. 304 (2001) 455-462. (Pubitemid 32480575)
20. K. Beuerlein, P. Ruth, F.R. Scholz, J. Springer, B. Lieb, W. Gebauer, B. Westermann, H. Schmidtberg, S. von Boletzky, J. Markl, R. Schipp, Blood cells and the biosynthesis of hemocyanin in Sepia embryos, Micron 35 (2004) 115-116. (Pubitemid 38214838)
21. A.M. Martin, G.G. Martin, R. Butler, S.K. Goffredi, Synthesis of keyhole limpet hemocyanin by the rhogocytes of Megathura crenulata, Invertebr. Biol. 130 (2011) 302-312.
22. M.E. Cuff, K.I. Miller, K.E. van Holde, W.A. Hendrickson, Crystal structure of a functional unit from Octopus hemocyanin, J. Mol. Biol. 278 (1998) 855-870. (Pubitemid 28224901)
23. M. Perbandt, E.W. Guthohrlein, W. Rypniewski, K. Idakieva, S. Stoeva, W. Voelter, N. Genov, C. Betzel, The structure of a functional unit from the wall of a gastropod hemocyanin offers a possible mechanism for cooperativity, Biochemistry 42 (2003) 6341-6346. (Pubitemid 36665807)
24. E. Jaenicke, K. Büchler, J. Markl, H. Decker, T.R. Barends, Cupredoxin-like domains in haemocyanins, Biochem. J. 426 (2010) 373-378.
25. E. Jaenicke, K. Büchler, H. Decker, J. Markl, G.F. Schröder, The refined structure of functional unit h of keyhole limpet hemocyanin (KLH1-h) reveals disulfide bridges, IUBMB Life 63 (2011) 183-187.
26. K.I. Miller, M.E. Cuff, W.F. Lang, P. Varga-Weisz, K.G. Field, K.E. van Holde, Sequence of the Octopus dofleini hemocyanin subunit: structural and evolutionary implications, J. Mol. Biol. 278 (1998) 827-842. (Pubitemid 28224899)
27. B. Altenhein, J. Markl, B. Lieb, Gene structure and hemocyanin isoform HtH2 from the mollusc Haliotis tuberculata indicate early and late intron hot spots, Gene 301 (2002) 53-60. (Pubitemid 35469123)
28. S. Bergmann, B. Lieb, P. Ruth, J. Markl, The hemocyanin from a living fossil, the cephalopod Nautilus pompilius: protein structure, gene organization, and evolution, J. Mol. Evol. 62 (2006) 362-374.
29. S. Bergmann, J. Markl, B. Lieb, Thefirst complete cDNA sequence of the hemocyanin from a bivalve, the protobranch Nucula nucleus, J. Mol. Evol. 64 (2007) 500-510. (Pubitemid 46717936)
30. B. Lieb, V. Boisguerin, W. Gebauer, J. Markl, cDNA sequence, protein structure, and evolution of the single hemocyanin from Aplysia californica, an opisthobranch gastropod, J. Mol. Evol. 59 (2004) 536-545. (Pubitemid 39305145)
31. L. De Smet, I. Dimitrov, G. Debyser, P. Dolashka-Angelova, A. Dolashki, J. Van Beeumen, B. Devreese, The cDNA sequence of three hemocyanin subunits from the garden snail Helix lucorum, Gene 487 (2011) 118-128.
32. B. Lieb, K. Dimitrova, H.S. Kang, S. Braun, W. Gebauer, A. Martin, B. Hanelt, S.A. Saenz, C.M. Adema, J. Markl, Red blood with blue-blood ancestry: intriguing structure of a snail hemoglobin, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 12011-12016. (Pubitemid 44215802)
33. B. Lieb, W. Gebauer, C. Gatsogiannis, F. Depoix, N. Hellmann, M.G. Harasewych, E.E. Strong, J. Markl, Molluscan mega-hemocyanin: an ancient oxygen carrier tuned by a 550 kDa polypeptide, BMC Front. Zool. 7 (2010) 14.
34. J.E. Mellema, A. Klug, Quaternary structure of gastropod haemocyanin, Nature 239 (1972) 146-150.
35. R.J. Siezen, E.F. van Bruggen, Structure and properties of hemocyanins. XII. Electron microscopy of dissociation products of Helix pomatia alpha-hemocyanin: quaternary structure, J. Mol. Biol. 90 (1974) 77-89.
36. R.van Driel, E.F. van Bruggen, Oxygen-linked association-dissociation of Helix pomatia hemocyanin, Biochemistry 13 (1974) 4079-4083.
37. M. Brouwer, M. Wolters, E.F. van Bruggen, Proteolytic fragmentation of Helix pomatia alpha-hemocyanin: structural domains in the polypeptide chain, Biochemistry 15 (1976) 2618-2623.
38. R. Torensma, J.M. van der Laan, E.F. van Bruggen, Structural and functional aspects of collar domains of Helix pomatia beta c-hemocyanin, Biochim. Biophys. Acta 668 (1981) 268-276.
39. J.F. van Breemen, J.H. Ploegman, E.F. van Bruggen, Structure of Helix pomatia oxy-beta-hemocyanin and deoxy-beta-hemocyanin tubular polymers, Eur. J. Biochem. 100 (1979) 61-65.
40. R. Torensma, J.M. van der Laan, E.F. van Bruggen, C. Gielens, L. van Paemel, L.J. Verschueren, R. Lontie, Functional properties of the isolated domains of Helix pomatia beta c-hemocyanin, FEBS Lett. 115 (1980) 213-215.
41. T. Vannoppen-ver Eecke, R. D'Hulster, R. Lontie, Influence of the saturation with carbon monoxide and of deoxygenation on the alkaline dissociation of Helix pomatia haemocyanin, Comp. Biochem. Physiol. B 46 (1973) 499-507.
42. J. Berger, I. Pilz, R. Witters, R. Lontie, Studies by small-angle X-ray scattering of the quaternary structure of the beta-haemocyanin of Helix pomatia, Eur. J. Biochem. 80 (1977) 79-82. (Pubitemid 8209985)
43. C. Gielens, L.J. Verschueren, G. Preaux, R. Lontie, Fragmentation of crystalline beta-haemocyanin of Helix pomatia with plasmin and trypsin. Location of the fragments in the polypeptide chain, Eur. J. Biochem. 103 (1980) 463-470.
44. C. Gielens, F. Smets, G. Preaux, R. Lontie, Proceedings: sodium dodecyl sulphate electrophoresis on polyacrylamide gel of functional tryptic fragments of crystalline beta-haemocyanin of Helix pomatia, Arch. Int. Physiol. Biochim. 82 (1974) 787.
45. C. Gielens, N. De Geest, X.Q. Xin, B. Devreese, J. Van Beeumen, G. Preaux, Evidence for a cysteine-histidine thioether bridge in functional units of molluscan haemocyanins and location of the disulfide bridges in functional units d and g of the betaC-haemocyanin of Helix pomatia, Eur. J. Biochem. 248 (1997) 879-888. (Pubitemid 27400045)
46. T.T. Herskovits, S.E. Carberry, G.B. Villanueva, Subunit dissociation of Busycon canaliculatum hemocyanin, Biochim. Biophys. Acta 828 (1985) 278-289.
47. T.T. Herskovits, M.D. Edwards, M.G. Hamilton, The hemocyanin of the Californian black sea hare, Aplysia vaccaria Winkler, Comp. Biochem. Physiol. B 110 (1995) 515-521.
48. T.T. Herskovits, M.G. Hamilton, L.J. Mazzella, Hemocyanin of the chiton Acanthopleura granulata, Biochemistry 25 (1986) 3612-3619.
49. T.T. Herskovits, M.G. Hamilton, Hemocyanin of the chiton, Stenoplax conspicua (Dall), Comp. Biochem. Physiol. B 88 (1987) 127-132.
50. T.T. Herskovits, R.M. Otero, M.G. Hamilton, The hemocyanin of the ramshorn snail, Marisa cornuarietis (Linne), Comp. Biochem. Physiol. B 97 (1990) 623-629.
51. T.T. Herskovits, M.G. Hamilton, C.J. Cousins, J.S. Wall, Light-scattering and scanning transmission electron microscopic investigation of the hemocyanin of the bivalve, Yoldia limatula (Say), Comp. Biochem. Physiol. B 96 (1990) 497-503. (Pubitemid 20216210)
52. T.T. Herskovits, M.W. Russell, Light-scattering investigation of the subunit structure and dissociation of Helix pomatia hemocyanin. Effects of salts and ureas, Biochemistry 23 (1984) 2812-2819.
53. T.T. Herskovits, M.G. Hamilton, Physical investigations of the hemocyanin of the chiton, Cryptochiton stelleri (Middendorff), Comp. Biochem. Physiol. B 86 (1987) 641-649.
54. T.T. Herskovits, J. Zou, M.G. Hamilton, Physical studies of the hemocyanin of the marine gastropod, Kelletia kelleti (Forbes), Comp. Biochem. Physiol. B 103 (1992) 447-453.
55. + on the di-decameric structure of Yoldia limatula hemocyanin, Biochim. Biophys. Acta 1076 (1991) 71-78.
56. T.T. Herskovits, P.A. Blake, M.G. Hamilton, Subunit dissociation and denaturation of Fasciolaria tulipa hemocyanin, Comp. Biochem. Physiol. B 90 (1988) 869-874.
57. F. Mouche, N. Boisset, J. Lamy, F. Zal, J.N. Lamy, Structural comparison of cephalopod hemocyanins: phylogenetic significance, J. Struct. Biol. 127 (1999) 199-212.
58. J. Lamy, C. Gielens, O. Lambert, J.C. Taveau, G. Motta, P. Loncke, N. De Geest, G. Preaux, Further approaches to the quaternary structure of octopus hemocyanin: a model based on immunoelectron microscopy and image processing, Arch. Biochem. Biophys. 305 (1993) 17-29. (Pubitemid 23241989)
59. J. Lamy, V. You, J.C. Taveau, N. Boisset, J.N. Lamy, Intramolecular localization of the functional units of Sepia officinalis hemocyanin by immunoelectron microscopy, J. Mol. Biol. 284 (1998) 1051-1074. (Pubitemid 28558556)
60. O. Lambert, N. Boisset, P. Penczek, J. Lamy, J.C. Taveau, J. Frank, J.N. Lamy, Quaternary structure of Octopus vulgaris hemocyanin. Three-dimensional reconstruction from frozen-hydrated specimens and intramolecular location of functional units Ove and Ovb, J. Mol. Biol. 238 (1994) 75-87.
61. K.I. Miller, K.E. van Holde, A. Toumadje, W.C. Johnson Jr., J. Lamy, Structure and function of the carboxyl-terminal oxygen-binding domain from the subunit of Octopus dofleini hemocyanin, Biochemistry 27 (1988) 7282-7288.
62. O. Lambert, N. Boisset, J.C. Taveau, J.N. Lamy, Three-dimensional reconstruction of Sepia officinalis hemocyanin from frozen-hydrated specimens, Arch. Biochem. Biophys. 316 (1995) 950-959.
63. O. Lambert, J.C. Taveau, N. Boisset, J.N. Lamy, Three-dimensional reconstruction of the hemocyanin of the protobranch bivalve mollusc Nucula hanleyi from frozen-hydrated specimens, Arch. Biochem. Biophys. 319 (1995) 231-243.
64. K.E. van Holde, K.I. Miller, Association-dissociation equilibria of Octopus hemocyanin, Biochemistry 24 (1985) 4577-4582.
65. K.I. Miller, E. Schabtach, K.E. van Holde, Arrangement of subunits and domains within the Octopus dofleini hemocyanin molecule, Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 1496-1500.
66. K.E. van Holde, K. Miller, E. Schabtach, L. Libertini, Assembly of Octopus dofleini hemocyanin. A study of the kinetics by sedimentation, light scattering and electron microscopy, J. Mol. Biol. 217 (1991) 307-321. (Pubitemid 121003943)
67. R.D. Swerdlow, R.F. Ebert, P. Lee, C. Bonaventura, K.I. Miller, Keyhole limpet hemocyanin: structural and functional characterization of two different subunits and multimers, Comp. Biochem. Physiol. B 113 (1996) 537-548. (Pubitemid 26135422)
68. B. Lieb, B. Altenhein, J. Markl, A. Vincent, E. van Olden, K.E. van Holde, K.I. Miller, Structures of two molluscan hemocyanin genes: significance for gene evolution, Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 4546-4551. (Pubitemid 32295013)
69. U. Meissner, A.G. Martin, B.O. Schwarz, M. Stohr, W. Gebauer, J.R. Harris, J. Markl, 3-D reconstruction of hemocyanins and other invertebrate hemolymph proteins by cryo-TEM: an overview, Micron 35 (2004) 7-9. (Pubitemid 38214805)
70. J.R. Harris, U. Meissner, W. Gebauer, J. Markl, 3D reconstruction of the hemocyanin subunit dimer from the chiton Acanthochiton fascicularis, Micron 35 (2004) 23-26. (Pubitemid 38214810)
71. H. Keller, B. Lieb, B. Altenhein, D. Gebauer, S. Richter, S. Stricker, J. Markl, Abalone (Haliotis tuberculata) hemocyanin type 1 (HtH1). Organization of the approximately 400 kDa subunit, and amino acid sequence of its functional units f, g and h, Eur. J. Biochem. 264 (1999) 27-38. (Pubitemid 29385864)
72. U. Meissner, C. Gatsogiannis, A. Moeller, F. Depoix, J.R. Harris, J. Markl, Comparative 11 Å structure of two molluscan hemocyanins from 3D cryo-electron microscopy, Micron 38 (2007) 754-765. (Pubitemid 47212740)
73. J.R. Harris, D. Scheffler, W. Gebauer, R. Lehnert, J. Markl, Haliotis tuberculata hemocyanin (HtH): analysis of oligomeric stability of HtH1 and HtH2, and comparison with keyhole limpet hemocyanin KLH1 and KLH2, Micron 31 (2000) 613-622. (Pubitemid 30390820)
74. T. Kurokawa, M. Wuhrer, G. Lochnit, H. Geyer, J. Markl, R. Geyer, Hemocyanin from the keyhole limpet Megathura crenulata (KLH) carries a novel type of N-glycans with Gal(beta1-6)Man-motifs, Eur. J. Biochem. 269 (2002) 5459-5473. (Pubitemid 35365534)
75. W. Gebauer, S. Stoeva, W. Voelter, E. Dainese, B. Salvato, M. Beltramini, J. Markl, Hemocyanin subunit organization of the gastropod Rapana thomasiana, Arch. Biochem. Biophys. 372 (1999) 128-134.
76. J.R. Harris, W. Gebauer, F.U. Guderian, J. Markl, Keyhole limpet hemocyanin (KLH), I: reassociation from Immucothel followed by separation of KLH1 and KLH2, Micron 28 (1997) 31-41. (Pubitemid 27275221)
77. J.R. Harris, W. Gebauer, S.M. Söhngen, M.V. Nermut, J. Markl, Keyhole limpet hemocyanin (KLH), II: characteristic reassociation properties of purified KLH1 and KLH2, Micron 28 (1997) 43-56. (Pubitemid 27275222)
78. S.M. Söhngen, A. Stahlmann, J.R. Harris, S.A. Müller, A. Engel, J. Markl, Mass determination, subunit organization and control of oligomerization states of keyhole limpet hemocyanin (KLH), Eur. J. Biochem. 248 (1997) 602-614. (Pubitemid 27387510)
79. U. Meissner, P. Dube, J.R. Harris, H. Stark, J. Markl, Structure of a molluscan hemocyanin didecamer (HtH1 from Haliotis tuberculata) at 12 Å resolution by cryoelectron microscopy, J. Mol. Biol. 298 (2000) 21-34.
80. E.V. Orlova, P. Dube, J.R. Harris, E. Beckman, F. Zemlin, J. Markl, M. van Heel, Structure of keyhole limpet hemocyanin type 1 (KLH1) at 15 Å resolution by electron cryomicroscopy and angular reconstitution, J. Mol. Biol. 271 (1997) 417-437. (Pubitemid 27348508)
81. B. Lieb, B. Altenhein, R. Lehnert, W. Gebauer, J. Markl, Subunit organization of the abalone Haliotis tuberculata hemocyanin type 2 (HtH2), and the cDNA sequence encoding its functional units d, e, f, g and h, Eur. J. Biochem. 265 (1999) 134-144. (Pubitemid 29466021)
82. W. Gebauer, J. Robin Harris, J. Markl, Topology of the 10 subunits within the decamer of KLH, the hemocyanin of the marine gastropod Megathura crenulata, J. Struct. Biol. 139 (2002) 153-159. (Pubitemid 35425642)
83. W. Gebauer, J.R. Harris, H. Heid, M. Süling, R. Hillenbrand, S. Söhngen, A. Wegener-Strake, J. Markl, Quaternary structure, subunits and domain patterns of two discrete forms of keyhole limpet hemocyanin: KLH1 and KLH2, Zoology 98 (1994) 51-68. (Pubitemid 2086323)
84. J. Markl, A. Savel-Niemann, A. Wegener-Strake, M. Süling, A. Schneider, W. Gebauer, J.R. Harris, The role of two distinct subunit types in the architecture of keyhole limpet hemocyanin (KLH), Naturwissenschaften 78 (1991) 30-31.
85. B. Lieb, C. Todt, Hemocyanin in mollusks-a molecular survey and new data on hemocyanin genes in Solenogastres and Caudofoveata, Mol. Phylogenet. Evol. 49 (2008) 382-385.
86. W. Gebauer, J.R. Harris, G. Geisthardt, J. Markl, Keyhole limpet hemocyanin type 2 (KLH2): detection and immunolocalization of a labile functional unit h, J. Struct. Biol. 128 (1999) 280-286. (Pubitemid 30078396)
87. R. Favilla, F. Del Signore, E. Dainese, M. Beltramini, B. Salvato, Dissociation kinetics of hemocyanin from Octopus vulgaris, Biochim. Biophys. Acta 1385 (1998) 115-125. (Pubitemid 28277050)
88. B. Salvato, A. Ghiretti-Magaldi, F. Ghiretti, Hemocyanin of Octopus vulgaris. The molecular weight of the minimal functional subunit in 3 M urea, Biochemistry 18 (1979) 2731-2736.
89. P. De Ioannes, B. Moltedo, H. Oliva, R. Pacheco, F. Faunes, A.E. De Ioannes, M.I. Becker, Hemocyanin of the molluscan Concholepas concholepas exhibits an unusual heterodecameric array of subunits, J. Biol. Chem. 279 (2004) 26134-26142. (Pubitemid 38798758)
90. P. Dolashka-Angelova, A. Beck, A. Dolashki, S. Stevanovic, M. Beltramini, B. Salvato, R. Hristova, L. Velkova, W. Voelter, Carbohydrate moieties of molluscan Rapana venosa hemocyanin, Micron 35 (2004) 101-104. (Pubitemid 38214833)
91. L. Velkova, P. Dolashka, A. Dolashki, W. Voelter, B. Atanasov, Structural analysis and molecular modeling of the RvH2-e functional unit of Rapana venosa hemocyanin, Biochim. Biophys. Acta 1804 (2010) 2177-2182.
92. K. Idakieva, S. Severov, I. Svendsen, N. Genov, S. Stoeva, M. Beltramini, G. Tognon, P. Di Muro, B. Salvato, Structural properties of Rapana thomasiana Grosse hemocyanin: isolation, characterization and N-terminal amino acid sequence of two different dissociation products, Comp. Biochem. Physiol. B 106 (1993) 53-59. (Pubitemid 23225868)
93. F. Spinozzi, P. Mariani, I. Micetic, C. Ferrero, D. Pontoni, M. Beltramini, Heterogeneity of oligomeric proteins: a SAXS and SANS study of the dissociation products of Octopus vulgaris hemocyanin, PLoS One 7 (2012) e49644.
94. H. Hartmann, A. Bongers, H. Decker, Monte Carlo based reconstruction of keyhole limpet hemocyanin type 1 (KLH1): Small angle X-ray scattering reveals oxygen dependent conformational change of the surface, J. Biol. Chem. 279 (2004) 2841-2845.
95. C. Bonaventura, J. Bonaventura, K.I. Miller, K.E. Van Holde, Hemocyanin of the chambered nautilus: structure-function relationships, Arch. Biochem. Biophys. 211 (1981) 589-598.
96. N.B. Terwilliger, R.C. Terwilliger, E. Meyhöfer, P. Morse, Bivalve hemocyanins - a comparison with other molluscan hemocyanins, Comp. Biochem. Physiol. B 89 (1988) 189-195.
97. M.P. Morse, E. Meyhöfer, J.J. Otto, A.M. Kuzirian, Hemocyanin respiratory pigment in bivalve mollusks, Science 231 (1986) 1302-1304. (Pubitemid 16036738)
98. N. Boisset, F. Mouche, Sepia officinalis hemocyanin: a refined 3D structure from field emission gun cryoelectron microscopy, J. Mol. Biol. 296 (2000) 459-472.
99. K. Cheng, P.J. Koeck, H. Elmlund, K. Idakieva, K. Parvanova, H. Schwarz, T. Ternstrom, H. Hebert, Rapana thomasiana hemocyanin (RtH): comparison of the two isoforms, RtH1 and RtH2, at 19 Å and 16 Å resolution, Micron 37 (2006) 566-576. (Pubitemid 44056019)
100. C. Gatsogiannis, A. Moeller, F. Depoix, U. Meissner, J. Markl, Nautilus pompilius hemocyanin: 9 Å cryo-EM structure and molecular model reveal the subunit pathway and the interfaces between the 70 functional units, J. Mol. Biol. 374 (2007) 465-486. (Pubitemid 350007652)
101. C. Gatsogiannis, J. Markl, Keyhole limpet hemocyanin: 9-Å CryoEM structure and molecular model of the KLH1 didecamer reveal the interfaces and intricate topology of the 160 functional units, J. Mol. Biol. 385 (2009) 963-983.
102. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, T.E. Ferrin, UCSF Chimera-a visualization system for exploratory research and analysis, J. Comput. Chem. 25 (2004) 1605-1612.
103. R. Drexel, S. Siegmund, H.J. Schneider, B. Linzen, C. Gielens, G. Preaux, R. Lontie, J. Kellermann, F. Lottspeich, Complete amino-acid sequence of a functional unit from a molluscan hemocyanin (Helix pomatia), Biol. Chem. Hoppe Seyler 368 (1987) 617-635.
104. J. Markl, B. Lieb, W. Gebauer, B. Altenhein, U. Meissner, J.R. Harris, Marine tumor vaccine carriers: structure of the molluscan hemocyanins KLH and HtH, J. Cancer Res. Clin. Oncol. 127 (Suppl. 2) (2001) R3-R9. (Pubitemid 33739044)
105. J.R. Harris, J. Markl, Keyhole limpet hemocyanin (KLH): a biomedical review, Micron 30 (1999) 597-623. (Pubitemid 29492383)
106. L. Velkova, I. Dimitrov, H. Schwarz, S. Stevanovic, W. Voelter, B. Salvato, P. Dolashka-Angelova, Structure of hemocyanin from garden snail Helix lucorum, Comp. Biochem. Physiol. B 157 (2010) 16-25.
107. S. Zielinski, F.J. Sartoris, H.O. Pörtner, Temperature effects on hemocyanin oxygen binding in an antarctic cephalopod, Biol. Bull. 200 (2001) 67-76. (Pubitemid 32177051)
108. O. Lambert, N. Boisset, J.C. Taveau, J.N. Lamy, Three-dimensional reconstruction from a frozen-hydrated specimen of the chiton Lepidochiton sp. hemocyanin, J. Mol. Biol. 244 (1994) 640-647. (Pubitemid 24381814)
109. Q. Zhang, X. Dai, Y. Cong, J. Zhang, D.H. Chen, M.T. Dougherty, J. Wang, S.J. Ludtke, M.F. Schmid, W. Chiu, Cryo-EM structure of a molluscan hemocyanin suggests its allosteric mechanism, Structure (2013), http://dx.doi.org/10.1016/ j.str.2013.02.018.