Multifunctional Roles of Hemocyanins

  • Christopher J. CoatesEmail author
  • Elisa M. Costa-Paiva
Part of the Subcellular Biochemistry book series (SCBI, volume 94)


The copper-containing hemocyanins are proteins responsible for the binding, transportation and storage of dioxygen within the blood (hemolymph) of many invertebrates. Several additional functions have been attributed to both arthropod and molluscan hemocyanins, including (but not limited to) enzymatic activity (namely phenoloxidase), hormone transport, homeostasis (ecdysis) and hemostasis (clot formation). An important secondary function of hemocyanin involves aspects of innate immunity—such as acting as a precursor of broad-spectrum antimicrobial peptides and microbial/viral agglutination. In this chapter, we present the reader with an up-to-date synthesis of the known functions of hemocyanins and the structural features that facilitate such activities.


Innate immunity Phenoloxidase Invertebrate Antimicrobial Oxygen transport protein Cryptides 



We should like to thank Prof Andrew Rowley (Swansea University) for providing comments on the text. No direct funding was provided to undertake this review; however, the content was presented and discussed at the SafeAqua workshop on Invertebrate Immunology held in Thailand, July 2019. The SafeAqua project has received funding from the European Union’s Horizon 2020 research and innovation programme under the grant agreement No. 734486 (CJC is the PI for Swansea University).


  1. Adachi K, Hirata T, Nishioka T et al (2003) Hemocyte components in crustaceans convert hemocyanin into a phenoloxidase-like enzyme. Comp Biochem Phys B 134(1):135–141CrossRefGoogle Scholar
  2. Adachi K, Endo H, Watanabe T et al (2005a) Hemocyanin in the exoskeleton of crustaceans: enzymatic properties and immunolocalization. Pigment Cell Res 18(2):136–143CrossRefPubMedPubMedCentralGoogle Scholar
  3. Adachi K, Wakamatsu K, Ito S et al (2005b) An oxygen transporter hemocyanin can act on the late pathway of melanin synthesis. Pigment Cell Res 18(3):214–219CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aguilera F, McDougall C, Degnan BM (2013) Origin, evolution and classification of type-3 copper proteins: lineage-specific gene expansions and losses across the Metazoa. BMC Evol Biol 13(1):96CrossRefPubMedPubMedCentralGoogle Scholar
  5. Alpuche J, Pereyra A, Mendoza-Hernández G et al (2010) Purification and partial cnharacterization of an agglutinin from Octopus maya serum. Comp Biochem Phys B 156(1):1–5CrossRefGoogle Scholar
  6. Baird S, Kelly SM, Price NC et al (2007) Hemocyanin conformational changes associated with SDS-induced phenol oxidase activation. BBA Proteins Proteom 1774(11):1380–1394CrossRefGoogle Scholar
  7. Besser K, Malyon GP, Eborall WS et al (2018) Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans. Nat Commun 9(1):5125CrossRefPubMedPubMedCentralGoogle Scholar
  8. Boonchuen P, Jaree P, Tassanakajon A et al (2018) Hemocyanin of Litopenaeus vannamei agglutinates Vibrio parahaemolyticus AHPND (VPAHPND) and neutralizes its toxin. Dev Comp Immunol 84:371–381CrossRefPubMedPubMedCentralGoogle Scholar
  9. Boone WR, Schoffeniels E (1979) Hemocyanin synthesis during hypo-osmotic stress in the shore crab Carcinus maenas (L.). Comp Biochem Physiol B 63(2):207–214Google Scholar
  10. Bourchookarn A, Havanapan PO, Thongboonkerd V et al (2008) Proteomic analysis of altered proteins in lymphoid organ of yellow head virus infected Penaeus monodon. BBA Proteins Proteom 1784(3):504–511CrossRefGoogle Scholar
  11. Brown-Peterson NJ, Larkin P, Denslow N et al (2005) Molecular indicators of hypoxia in the blue crab Callinectes sapidus. Mar Ecol Prog Ser 286:203–215CrossRefGoogle Scholar
  12. Burmester T (1999) Evolution and function of the insect hexamerins. Eur J Entomol 96:213–226Google Scholar
  13. Burmester T (2002) Origin and evolution of arthropod hemocyanins and related proteins. J Comp Physiol B 172(2):95–107CrossRefPubMedPubMedCentralGoogle Scholar
  14. Burmester T (2015) Evolution of respiratory proteins across the Pancrustacea. Integr Comp Biol 55(5):792–801CrossRefGoogle Scholar
  15. Cerenius L, Söderhäll K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198(1):116–126CrossRefGoogle Scholar
  16. Cerenius L, Lee BL, Söderhäll K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29(6):263–271CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cerenius L, Babu R, Söderhäll K et al (2010a) In vitro effects on bacterial growth of phenoloxidase reaction products. J Invert Pathol 103(1):21–23CrossRefGoogle Scholar
  18. Cerenius L, Kawabata SI, Lee BL et al (2010b) Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci 35(10):575–583CrossRefGoogle Scholar
  19. Choi H, Lee DG (2014) Antifungal activity and pore-forming mechanism of astacidin 1 against Candida albicans. Biochimie 105:58–63CrossRefPubMedPubMedCentralGoogle Scholar
  20. Chongsatja PO, Bourchookarn A, Lo CF et al (2007) Proteomic analysis of differentially expressed proteins in Penaeus vannamei hemocytes upon Taura syndrome virus infection. Proteomics 7(19):3592–3601CrossRefPubMedPubMedCentralGoogle Scholar
  21. Chou KC, Zhang CT, Maggiora GM (1997) Disposition of amphiphilic helices in heteropolar environments. Proteins: Struct Funct Bioinform 28(1):99–108Google Scholar
  22. Coates CJ (2012) Hemocyanin-derived phenoloxidase; biochemical and cellular investigations of innate immunity. Ph.D. thesis.
  23. Coates CJ, Albalat (2014) Engaging with strategies to impede post-mortem hyperpigmentation in commercial crustaceans. In: Hay RM (ed) Shellfish: human consumption, health implications and conservation concerns. Nova Science Publishers, pp 169–194. ISBN: 978-163321196-4, 978-163321195-7Google Scholar
  24. Coates CJ, Decker H (2017) Immunological properties of oxygen-transport proteins: hemoglobin, hemocyanin and hemerythrin. Cell Mol Life Sci 74(2):293–317CrossRefGoogle Scholar
  25. Coates CJ, Nairn J (2013) Hemocyanin-derived phenoloxidase activity: a contributing factor to hyperpigmentation in Nephrops norvegicus. Food Chem 140(1–2):361–369CrossRefPubMedPubMedCentralGoogle Scholar
  26. Coates CJ, Nairn J (2014) Diverse immune functions of hemocyanins. Dev Comp Immunol 45(1):43–55CrossRefPubMedPubMedCentralGoogle Scholar
  27. Coates CJ, Talbot J (2018) Hemocyanin-derived phenoloxidase reaction products display anti-infective properties. Dev Comp Immunol 86:47–51CrossRefPubMedPubMedCentralGoogle Scholar
  28. Coates CJ, Kelly SM, Nairn J (2011) Possible role of phosphatidylserine–hemocyanin interaction in the innate immune response of Limulus polyphemus. Dev Comp Immunol 35(2):155–163CrossRefPubMedPubMedCentralGoogle Scholar
  29. Coates CJ, Bradford EL, Krome CA et al (2012) Effect of temperature on biochemical and cellular properties of captive Limulus polyphemus. Aquaculture 334:30–38CrossRefGoogle Scholar
  30. Coates CJ, Whalley T, Wyman M et al (2013) A putative link between phagocytosis-induced apoptosis and hemocyanin-derived phenoloxidase activation. Apoptosis 18(11):1319–1331CrossRefPubMedPubMedCentralGoogle Scholar
  31. Cong Y, Zhang Q, Woolford D et al (2009) Structural mechanism of SDS-induced enzyme activity of scorpion hemocyanin revealed by electron cryomicroscopy. Structure 17(5):749–758CrossRefPubMedPubMedCentralGoogle Scholar
  32. Costa-Paiva EM, Schrago CG, Coates CJ et al (2018) Discovery of novel hemocyanin-like genes in metazoans. Biol Bull 235(3):134–151CrossRefPubMedPubMedCentralGoogle Scholar
  33. Decker H, Föll R (2000) Temperature adaptation influences the aggregation state of hemocyanin from Astacus leptodactylus. Comp Biochem Physiol A 127(2):147–154CrossRefGoogle Scholar
  34. Decker H, Rimke T (1998) Tarantula hemocyanin shows phenoloxidase activity. J Biol Chem 273(40):25889–25892CrossRefPubMedPubMedCentralGoogle Scholar
  35. Decker H, Tuczek F (2000) Tyrosinase/catecholoxidase activity of hemocyanins: structural basis and molecular mechanism. Trends Biochem Sci 25(8):392–397CrossRefPubMedPubMedCentralGoogle Scholar
  36. Decker H, Ryan M, Jaenicke E et al (2001) SDS-induced phenoloxidase activity of hemocyanins from limulus polyphemus, eurypelma californicum, and cancer magister. J Biol Chem 276(21):17796–17799CrossRefPubMedPubMedCentralGoogle Scholar
  37. Decker H, Hellmann N, Jaenicke E et al (2007) Minireview: recent progress in hemocyanin research. Integr Comp Biol 47(4):631–644CrossRefPubMedPubMedCentralGoogle Scholar
  38. Decker H, Solem E, Tuczek F (2018) Are glutamate and asparagine necessary for tyrosinase activity of type-3 copper proteins? Inorg Chim Acta 481:32–37CrossRefGoogle Scholar
  39. Destoumieux-Garzón D, Saulnier D, Garnier J et al (2001) Crustacean immunity antifungal peptides are generated from the c terminus of shrimp hemocyanin in response to microbial challenge. J Biol Chem 276(50):47070–47077CrossRefPubMedPubMedCentralGoogle Scholar
  40. Dolashka P, Velkova L, Shishkov S et al (2010) Glycan structures and antiviral effect of the structural subunit RvH2 of Rapana hemocyanin. Carbohydr Res 345(16):2361–2367CrossRefPubMedPubMedCentralGoogle Scholar
  41. Dolashka P, Moshtanska V, Borisova V et al (2011) Antimicrobial proline-rich peptides from the hemolymph of marine snail Rapana venosa. Peptides 32(7):1477–1483CrossRefPubMedPubMedCentralGoogle Scholar
  42. Dolashka-Angelova P, Lieb B, Velkova L et al (2009) Identification of glycosylated sites in Rapana hemocyanin by mass spectrometry and gene sequence, and their antiviral effect. Bioconjug Chem 20(7):1315–1322CrossRefPubMedPubMedCentralGoogle Scholar
  43. García-Carreño FL, Cota K, Navarrete del Toro MA (2008) Phenoloxidase activity of hemocyanin in whiteleg shrimp Penaeus vannamei: conversion, characterization of catalytic properties, and role in postmortem melanosis. J Agricul Food Chem 56(15):6454–6459CrossRefGoogle Scholar
  44. Gatsogiannis C, Hofnagel O, Markl J et al (2015) Structure of mega-hemocyanin reveals protein origami in snails. Structure 23(1):93–103CrossRefPubMedPubMedCentralGoogle Scholar
  45. Glazer L, Tom M, Weil S et al (2013) Hemocyanin with phenoloxidase activity in the chitin matrix of the crayfish gastrolith. J Exp Biol 216(10):1898–1904CrossRefPubMedPubMedCentralGoogle Scholar
  46. Guo L, Zhao X, Zhang Y, Wang Z, Zhong M, Li S, Lun J, (2013) Evidences of SNPs in the variable region of hemocyanin Ig-like domain in shrimp litopenaeus vannamei. Fish Shellfish Immunol 35(5):1532–1538Google Scholar
  47. Hartmann H, Decker H (2004) Small-angle scattering techniques for analyzing conformational transitions in hemocyanins. In: Methods in enzymology, vol 379. Academic Press, pp 81–106Google Scholar
  48. Havanapan PO, Kanlaya R, Bourchookarn A et al (2009) C-terminal hemocyanin from hemocytes of Penaeus vannamei interacts with ERK1/2 and undergoes serine phosphorylation. J Proteome Res 8(5):2476–2483CrossRefPubMedPubMedCentralGoogle Scholar
  49. Jaenicke E, Decker H (2008) Kinetic properties of catecholoxidase activity of tarantula hemocyanin. FEBS J 275(7):1518–1528CrossRefPubMedPubMedCentralGoogle Scholar
  50. Jaenicke E, Föll R, Decker H (1999) Spider hemocyanin binds ecdysone and 20-OH-ecdysone. J Biol Chem 274(48):34267–34271CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jaenicke E, Fraune S, May S et al (2009) Is activated hemocyanin instead of phenoloxidase involved in immune response in woodlice? Dev Comp Immunol 33(10):1055–1063CrossRefPubMedPubMedCentralGoogle Scholar
  52. Jiang N, Tan NS, Ho B et al (2007) Respiratory protein–generated reactive oxygen species as an antimicrobial strategy. Nat Immunol 8(10):1114CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kato S, Matsui T, Gatsogiannis C et al (2018) Molluscan hemocyanin: structure, evolution, and physiology. Biophys Rev 10(2):191–202CrossRefPubMedPubMedCentralGoogle Scholar
  54. Klotz IM, Schlesinger AH, Tietze F (1948) Comparison of the binding ability of hemocyanin and serum albumin for organic ions. Biol Bull 94(1):40–44CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kuballa AV, Elizur A (2008) Differential expression profiling of components associated with exoskeletal hardening in crustaceans. BMC Genom 9(1):575CrossRefGoogle Scholar
  56. Kuballa AV, Holton TA, Paterson B et al (2011) Moult cycle specific differential gene expression profiling of the crab Portunus pelagicus. BMC Genom 12(1):147CrossRefGoogle Scholar
  57. Le Bris C, Cudennec B, Dhulster P et al (2016) Melanosis in Penaeus monodon: involvement of the laccase-like activity of hemocyanin. J Agricul Food Chem 64(3):663–670CrossRefGoogle Scholar
  58. Lee SY, Lee BL, Söderhäll K (2003) Processing of an antibacterial peptide from hemocyanin of the freshwater crayfish Pacifastacus leniusculus. J Biol Chem 278(10):7927–7933CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lee SY, Lee BL, Söderhäll K (2004) Processing of crayfish hemocyanin subunits into phenoloxidase. Biochem Biophys Res Commun 322(2):490–496Google Scholar
  60. Lei K, Li F, Zhang M et al (2008) Difference between hemocyanin subunits from shrimp Penaeus japonicus in anti-WSSV defense. Dev Comp Immunol 32(7):808–813CrossRefPubMedPubMedCentralGoogle Scholar
  61. Li C, Wang F, Aweya JJ et al (2018) Trypsin of Litopenaeus vannamei is required for the generation of hemocyanin-derived peptides. Dev Comp Immunol 79:95–104CrossRefPubMedPubMedCentralGoogle Scholar
  62. Markl J (2013) Evolution of molluscan hemocyanin structures. BBA Proteins Proteom 1834(9):1840–1852CrossRefGoogle Scholar
  63. Markl J, Decker H (1992) Molecular structure of the arthropod hemocyanins. In: Blood and tissue oxygen carriers. Springer, Berlin, pp 325–376Google Scholar
  64. Martín-Durán JM, de Mendoza A, Sebé-Pedrós A et al (2013) A broad genomic survey reveals multiple origins and frequent losses in the evolution of respiratory hemerythrins and hemocyanins. Genome Biol Evol 5(7):1435–1442CrossRefPubMedPubMedCentralGoogle Scholar
  65. Martínez-Alvarez O, Gómez-Guillén C, Montero P (2008) Presence of hemocyanin with diphenoloxidase activity in deepwater pink shrimp (Parapenaeus longirostris) post mortem. Food Chem 107(4):1450–1460CrossRefGoogle Scholar
  66. Nagai T, Kawabata SI (2000) A link between blood coagulation and prophenol oxidase activation in arthropod host defense. J Biol Chem 275(38):29264–29267CrossRefPubMedPubMedCentralGoogle Scholar
  67. Nagai T, Osaki T, Kawabata SI (2001) Functional conversion of hemocyanin to phenoloxidase by horseshoe crab antimicrobial peptides. J Biol Chem 276(29):27166–27170CrossRefPubMedPubMedCentralGoogle Scholar
  68. Naresh KN, Sreekumar A, Rajan SS (2015) Structural insights into the interaction between molluscan hemocyanins and phenolic substrates: an in silico study using docking and molecular dynamics. J Mol Graph Model 61:272–280CrossRefPubMedPubMedCentralGoogle Scholar
  69. Pan D, He N, Yang Z et al (2005) Differential gene expression profile in hepatopancreas of WSSV-resistant shrimp (Penaeus japonicus) by suppression subtractive hybridization. Dev Comp Immunol 29(2):103–112CrossRefPubMedPubMedCentralGoogle Scholar
  70. Pan JY, Zhang YL, Wang SY et al (2008) Dodecamer is required for agglutination of Litopenaeus vannamei hemocyanin with bacterial cells and red blood cells. Mar Biotechnol 10(6):645–652CrossRefPubMedPubMedCentralGoogle Scholar
  71. Paul RJ, Pirow R (1998) The physiological significance of respiratory proteins in invertebrates. Zoology 100(4):298–306Google Scholar
  72. Paul R, Bergner B, Pfeffer-Seidl A et al (1994) Gas transport in the haemolymph of arachnids-oxygen transport and the physiological role of haemocyanin. J Exp Biol 188(1):25–46PubMedPubMedCentralGoogle Scholar
  73. Petit VW, Rolland JL, Blond A et al (2016) A hemocyanin-derived antimicrobial peptide from the penaeid shrimp adopts an alpha-helical structure that specifically permeabilizes fungal membranes. BBA Gen Subj 1860(3):557–568Google Scholar
  74. Pettersen EF, Goddard TD, Huang CC et al (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rattanarojpong T, Wang HC, Lo CF et al (2007) Analysis of differently expressed proteins and transcripts in gills of Penaeus vannamei after yellow head virus infection. Proteomics 7(20):3809–3814CrossRefPubMedPubMedCentralGoogle Scholar
  76. Ravi M, Basha AN, Taju G et al (2010) Clearance of Macrobrachium rosenbergii nodavirus (MrNV) and extra small virus (XSV) and immunological changes in experimentally injected Macrobrachium rosenbergii. Fish Shellfish Immunol 28(3):428–433CrossRefPubMedPubMedCentralGoogle Scholar
  77. Rehm P, Pick C, Borner J et al (2012) The diversity and evolution of chelicerate hemocyanins. BMC Evol Biol 12(1):19CrossRefPubMedPubMedCentralGoogle Scholar
  78. Riciluca KCT, Sayegh RSR, Melo RL et al (2012) Rondonin an antifungal peptide from spider (Acanthoscurria rondoniae) haemolymph. Results Immunol 2:66–71CrossRefPubMedPubMedCentralGoogle Scholar
  79. Rowley AF, Powell A (2007) Invertebrate immune systems–specific, quasi-specific, or nonspecific? J Immunol 179(11):7209–7214CrossRefPubMedPubMedCentralGoogle Scholar
  80. Salvato B, Santamaria M, Beltramini M et al (1998) The enzymatic properties of Octopus vulgaris hemocyanin: o-diphenol oxidase activity. Biochem 37(40):14065–14077CrossRefGoogle Scholar
  81. Sanggaard KW, Dyrlund TF, Bechsgaard JS et al (2016) The spider hemolymph clot proteome reveals high concentrations of hemocyanin and von Willebrand factor-like proteins. BBA Proteins Proteom 1864(2):233–241Google Scholar
  82. Schenk S, Schmidt J, Hoeger U, Decker H (2015) Lipoprotein-induced phenoloxidase-activity in tarantula hemocyanin. BBA Proteins Proteom 1854(8):939–949CrossRefGoogle Scholar
  83. Shi XZ, Li XC, Wang S et al (2010) Transcriptome analysis of hemocytes and hepatopancreas in red swamp crayfish, Procambarus clarkii, challenged with white spot syndrome virus. Invertebrate Surviv J 7(1):119–131Google Scholar
  84. Siddiqui NI, Akosung RF, Gielens C (2006) Location of intrinsic and inducible phenoloxidase activity in molluscan hemocyanin. Biochem Biophys Res Commun 348(3):1138–1144CrossRefPubMedPubMedCentralGoogle Scholar
  85. Šobotník J, Bourguignon T, Hanus R et al (2012) Explosive backpacks in old termite workers. Science 337(6093):436CrossRefPubMedPubMedCentralGoogle Scholar
  86. Spicer JI, Hodgson E (2003) Structural basis for salinity-induced alteration in oxygen binding by haemocyanin from the estuarine amphipod Chaetogammarus marinus (L.). Physiol Biochem Zool 76(6):843–849Google Scholar
  87. Tanner CA, Burnett LE, Burnett KG (2006) The effects of hypoxia and pH on phenoloxidase activity in the Atlantic blue crab, Callinectes sapidus. Comp Biochem Physiol A 144(2):218–223CrossRefGoogle Scholar
  88. Terwilliger NB (2007) Hemocyanins and the immune response: defense against the dark arts. Integr Comp Biol 47(4):662–665CrossRefPubMedPubMedCentralGoogle Scholar
  89. Terwilliger NB (2015) Oxygen transport proteins in crustacean: hemocyanin and hemoglobin. In: Chang ES, Thiel M (eds) The natural history of the crustacea: physiology. Oxford University Press. ISBN: 9780199832415Google Scholar
  90. Terwilliger NB, Ryan MC (2006) Functional and phylogenetic analyses of phenoloxidases from brachyuran (Cancer magister) and branchiopod (Artemia franciscana, Triops longicaudatus) crustaceans. Biol Bull 210(1):38–50CrossRefPubMedPubMedCentralGoogle Scholar
  91. Theopold U, Schmidt O, Söderhäll K et al (2004) Coagulation in arthropods: defence, wound closure and healing. Trends Immunol 25(6):289–294CrossRefPubMedPubMedCentralGoogle Scholar
  92. Vance JE, Steenbergen R (2005) Metabolism and functions of phosphatidylserine. Prog Lipid Res 44(4):207–234CrossRefPubMedPubMedCentralGoogle Scholar
  93. Wang DL, Sun T, Zuo D et al (2013) Cloning and tissue expression of hemocyanin gene in Cherax quadricarinatus during white spot syndrome virus infection. Aquaculture 410:216–224CrossRefGoogle Scholar
  94. Whitten MM, Coates CJ (2017) Re-evaluation of insect melanogenesis research: views from the dark side. Pigment Cell Melanoma Res 30(4):386–401CrossRefPubMedPubMedCentralGoogle Scholar
  95. Wright J, Clark WM, Cain JA et al (2012) Effects of known phenoloxidase inhibitors on hemocyanin-derived phenoloxidase from Limulus polyphemus. Comp Biochem Physiol B 163(3–4):303–308CrossRefPubMedPubMedCentralGoogle Scholar
  96. Yan F, Qiao J, Zhang Y et al (2011a) Hemolytic properties of hemocyanin from mud crab Scylla serrata. J Shellfish Res 30(3):957–963CrossRefGoogle Scholar
  97. Yan F, Zhang Y, Jiang R et al (2011b) Identification and agglutination properties of hemocyanin from the mud crab (Scylla serrata). Fish Shellfish Immunol 30(1):354–360CrossRefPubMedPubMedCentralGoogle Scholar
  98. Yao D, Wang Z, Wei M et al (2019) Analysis of Litopenaeus vannamei hemocyanin interacting proteins reveals its role in hemolymph clotting. J Proteomics 201:57–64CrossRefPubMedPubMedCentralGoogle Scholar
  99. Zhan S, Aweya JJ, Wang F et al (2019) Litopenaeus vannamei attenuates white spot syndrome virus replication by specific antiviral peptides generated from hemocyanin. Dev Comp Immunol 91:50–61CrossRefPubMedPubMedCentralGoogle Scholar
  100. Zhang X, Huang C, Qin Q (2004a) Antiviral properties of hemocyanin isolated from shrimp Penaeus monodon. Antiviral Res 61(2):93–99CrossRefPubMedPubMedCentralGoogle Scholar
  101. Zhang Y, Wang S, Peng X (2004b) Identification of a type of human IgG-like protein in shrimp Penaeus vannamei by mass spectrometry. J Exp Mar Biol Ecol 301(1):39–54CrossRefGoogle Scholar
  102. Zhang Y, Wang S, Xu A et al (2006) Affinity proteomic Approach for identification of an IgA-like protein in Litopenaeus vannamei and study on its Agglutination characterization. J Proteome Res 5(4):815–821CrossRefPubMedPubMedCentralGoogle Scholar
  103. Zhang Y, Yan F, Hu Z et al (2009) Hemocyanin from shrimp Litopenaeus vannamei shows hemolytic activity. Fish Shellfish Immunol 27(2):330–335CrossRefPubMedPubMedCentralGoogle Scholar
  104. Zhang YL, Peng B, Li H et al (2017a) C-terminal domain of hemocyanin, a major antimicrobial protein from Litopenaeus vannamei: structural homology with immunoglobulins and molecular diversity. Front Immunol 8:611CrossRefPubMedPubMedCentralGoogle Scholar
  105. Zhang Z, Wang F, Chen C et al (2017b) Glycosylation of hemocyanin in Litopenaeus vannamei is an antibacterial response feature. Immunol Lett 192:42–47CrossRefPubMedPubMedCentralGoogle Scholar
  106. Zhao X, Guo L, Zhang Y et al (2012) SNPs of hemocyanin C-terminal fragment in shrimp Litopenaeus vannamei. FEBS Lett 586(4):403–410CrossRefPubMedPubMedCentralGoogle Scholar
  107. Zhu H, Zhuang J, Feng H et al (2014) Cryo-EM structure of isomeric molluscan hemocyanin triggered by viral infection. PLoS ONE 9(6):e98766CrossRefPubMedPubMedCentralGoogle Scholar
  108. Zhuang J, Coates CJ, Zhu H et al (2015) Identification of candidate antimicrobial peptides derived from abalone hemocyanin. Dev Comp Immunol 49(1):96–102CrossRefPubMedPubMedCentralGoogle Scholar
  109. Zlateva T, Di Muro P, Salvato B et al (1996) The o-diphenol oxidase activity of arthropod hemocyanin. FEBS Lett 384(3):251–254CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Biosciences, College of ScienceSwansea UniversitySwanseaUK
  2. 2.Departamento de Zoologia, Instituto Biociências, Universidade de São PauloSão PauloBrazil

Personalised recommendations