The molecular heterogeneity of hemocyanin: Its role in the adaptive plasticity of Crustacea

Gene

Volumn 398, Issue 1-2 SPEC. ISS., 2007, Pages 192-201

  Giomi, F ^a   Beltramini, M ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Crustacea; Hemocyanin; Molecular Heterogeneity; Oxygen binding; Phenotypic polymorphism; Quaternary structure; Subunit

Indexed keywords

HEMOCYANIN;

ADAPTATION; ARTICLE; CRUSTACEA; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; NONHUMAN; OXYGEN TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CRUSTACEA; DIMERIZATION; EVOLUTION, MOLECULAR; GENETIC HETEROGENEITY; HEMOCYANIN; OXYGEN; PROTEIN BINDING; SPECIES SPECIFICITY;

CRUSTACEA;

EID: 34447548567     PISSN: 03781119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gene.2007.02.039     Document Type: Article

References (112)

1. Abdennour C. Copper, zinc and haemocyanin concentrations in four caridean decapods (Crustacea): size relationships. Hydrobiologia 346 (1997) 1-9
2. Baden S.P., Pihl L., and Rosenberg R. Effects of oxygen depletion on the ecology, blood physiology and fishery of the Norway lobster Nephrops norvegicus. Mar. Ecol., Prog. Ser. 67 (1990) 141-155
3. Baden S.P., Depledge M.H., and Hagerman L. Glycogen depletion and altered copper and manganese handling in Nephrops norvegicus following starvation and exposure to hypoxia. Mar. Ecol., Prog. Ser. 103 (1994) 65-72
4. Baden S.P., Håkansson C.L.J., and Spicer J.I. Between-individual variation in haemocyanin concentrations in the Norway lobster Nephrops norvegicus following exposure to hypoxia and manganese. Mar. Biol. 143 (2003) 267-273
5. Bellelli A., et al. Sexual and seasonal variability of lobster hemocyanin. Comp. Biochem. Physiol., A 91 (1988) 445-449
6. Beltramini M., et al. Quaternary structure and functional properties of Penaeus monodon hemocyanin. FEBS J 272 8 (2005) 2060-2075
7. Boone W.R., and Schoffeniels E. Hemocyanin synthesis during hypo-osmotic stress in the shore crab Carcinus maenas (L.). Comp. Biochem. Physiol., B 63 (1979) 207-214
8. Bridges C.R. Purines and their interaction with other factors controlling haemocyanin oxygen affinity. In: Préaux G., and Lontie R. (Eds). Invertebrate Dioxygen Carriers (1990), Leuven University Press, Leuven 401-405
9. Bridges C.R. Modulation of haemocyanin oxygen affinity: properties and physiological implications in a changing world. J. Exp. Biol. 204 (2001) 1021-1032
10. Brouwer M., Larkin P., Brown-Peterson N., King C., Manning S., and Denslow N. Effects of hypoxia on gene and protein expression in the blue crab, Callinectes sapidus. Mar. Environ. Res. 58 (2004) 787-792
11. Brown A.C., and Terwilliger N.B. Ontogeny of hemocyanin function in the dungeness crab Cancer magister: hemolymph modulation of hemocyanin oxygen-binding. J. Exp. Biol. 201 (1998) 819-826
12. Brown-Peterson N.J., Larkin P., Denslow N., King C., Manning S., and Brouwer M. Molecular indicators of hypoxia in the blue crab. Mar. Ecol., Prog. Ser. 286 (2005) 203-215
13. Burmester T. Molecular evolution of the arthropod hemocyanin superfamily. Mol. Biol. Evol. 18 (2001) 184-195
14. Burmester T. Evolutionary history and diversity of arthropod hemocyanins. Micron 35 (2004) 121-122
15. Burnett L.E. Integrated function of the respiratory pigment hemocyanin in crabs. Am. Zool. 32 (1992) 438-446
16. Bursey C.R., and Lane C.E. Ionic and protein concentration changes during the molt cycle of Penaeus duorarum. Comp. Biochem. Physiol. 40A (1971) 155-162
17. Callicott K.A., and Mangum C.P. Phenotypic variation and lability of the subunit composition of the hemocyanin of Uca pugilator. J. Exp. Mar. Biol. Ecol. 165 (1993) 143-159
18. Chen J.C., and Cheng S.Y. Studies on haemocyanin and haemolymph protein levels of Penaeus japonicus based on sex, size and moulting cycle. Comp. Biochem. Physiol. 106B (1993) 293-296
19. Dainese E., Di Muro P., Beltramini M., Salvato B., and Decker H. Subunits composition and allosteric control in Carcinus aestuarii hemocyanin. Eur. J. Biochem. 256 (1998) 350-358
20. Decker H., and Föll R. Temperature adaptation influences the aggregation state of hemocyanin from Astacus leptodactylus. Comp. Biochem. Physiol., A 127 (2000) 147-154
21. Decker H., and Jaenicke E. Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins. Dev. Comp. Immunol. 28 (2004) 673-687
22. Decker H., and Sterner R. Nested allostery of arthropodan hemocyanin (Eurypelma californicum and Homarus americanus). The role of protons. J. Mol. Biol. 211 (1990) 281-293
23. Decker H., and Terwilliger N.B. Cops and robbers: putative evolution of copper oxygen-binding proteins. J. Exp. Biol. 203 (2000) 1777-1782
24. DeFur P.L., Mangum C.P., and Reese J.E. Respiratory responses of the blue crab Callinectes sapidus to long-term hypoxia. Biol. Bull. Mar. Biol. Lab. 178 (1990) 46-54
25. Djangmah J.S. The effects of feeding and starvation on copper in the blood and hepatopancreas, and on blood proteins of Crangon vulgaris (Fabricius). Comp. Biochem. Physiol. 32 (1970) 709-731
26. Durstewitz G., and Terwilliger N.B. Developmental changes in hemocyanin expression in the Dungeness crab, Cancer magister. J. Biol. Chem. 272 (1997) 4347-4350
27. Engel D.W. Metal regulation and molting in the blue crab, Callinectes sapidus: copper, zinc and metallothionein. Biol. Bull. Mar. Biol. Lab. 172 (1987) 69-82
28. Engel D.W., Brower M., and McKenna S. Hemocyanin concentrations in marine crustaceans as a function of environmental conditions. Mar. Ecol., Prog. Ser. 93 (1993) 235-244
29. Gilles R. Effect of osmotic stresses on the protein concentration and pattern of Eriocheir sinensis blood. Comp. Biochem. Physiol., A 56 (1977) 109-114
30. Giomi, F., Raicevich, S., Ferrarese, A., Pranovi, F., Di Muro, P., Beltramini, M., in press. Structural and functional heterogeneity of hemocyanin: intra- and inter-specific comparison in four species of portunid crabs (Crustacea: Portunidae). Mar. Biol.
31. Giomi F., Raicevich S., Ferrarese A., Pranovi F., Di Muro P., and Beltramini M. Structural and functional heterogeneity of hemocyanin: intra- and inter-specific comparison in four species of portunid crabs (Crustacea: Portunidae). Mar. Biol. 151 (2007) 1237-1247
32. Hagerman L. Haemocyanin concentration in juvenile lobsters (Homarus gammarus) in relation to moulting cycle and feeding condition. Mar. Biol. 77 (1983) 11-17
33. Hagerman L. Haemocyanin concentration in the shrimp Crangon crangon (L.) after exposure to moderate hypoxia. Comp. Biochem. Physiol. 85A (1986) 721-724
34. Hagerman L., and Baden S.P. Nephrops norvegicus: field study on the effects of oxygen deficiency on haemocyanin concentration. J. Exp. Mar. Biol. Ecol. 116 (1988) 135-142
35. Hagerman L., and Oksama M. Haemocyanin concentration, carrying capacity and haemolymph pH under hypoxia in Mesidothea entomon (L.). (Isopoda, Crustacea). Ophelia 24 (1985) 47-52
36. Hagerman L., and Uglow R.F. Effects of hypoxia on the respiratory and circulatory regulation of Nephrops norvegicus. Mar. Biol. 87 (1985) 273-278
37. Hagerman L., Søndergaard T., Weile K., Hosie D., and Uglow R.F. Aspects of blood physiology and ammonia excretion in under hypoxia. Comp. Biochem. Physiol. 97A (1990) 51-55
38. Hellmann N., Jaenicke E., and Decker H. Two types of urate binding sites on hemocyanin from the crayfish Astacus leptodactylus: an ITC study. Biophys. Chemist. 90 (2001) 279-299
39. Hodgson E., and Spicer J.I. Subunit compositions of crustacean haemocyanins are species-specific: evidence from non-decapod species. Comp. Biochem. Physiol. 128A (2001) 873-888
40. Hughes A.L. Evolution of the arthropod prophenoloxidase/hexamerin protein family. Immunogenetics 49 (1999) 106-114
41. Jaenicke E., and Decker H. Functional changes in the family of type 3 copper proteins during evolution. Chem. Biochem. 5 (2004) 163-169
42. Jeffrey P.D., Shaw D.C., and Treacy G.B. Hemocyanin from the Australian crayfish Cherax destructor: studies of two different monomers and their participation in the formation of multiple hexamers. Biochemistry 15 (1976) 5527-5533
43. Johnson B.A., Bonaventura C., and Bonaventura J. Allosteric regulation of Callinectes sapidus hemocyanin by binding of L-lactate. Biochemistry 23 (1984) 872-878
44. Johnson B.A., Bonaventura J., and Bonaventura C. Determination of L-lactate binding stoichiometry and differences in allosteric interactions of structurally distinct homohexamers from Panulirus interruptus hemocyanin. Biochim. Biophys. Acta 916 (1987) 376-380
45. Larson B.A., Terwilliger N.B., and Terwilliger R.C. Subunit heterogeneity of Cancer magister hemocyanin. Biochim. Biophys. Acta 667 (1981) 294-302
46. Linzen B., et al. The structure of arthropod hemocyanins. Science 229 5 (1985) 19-524
47. Magnus K.A., Ton-That H., and Carpenter J.E. Recent structural work on the oxygen transport protein hemocyanin. Chem. Rev. 94 (1994) 727-735
48. Mangum C., and McKenney A.L. Subunit composition of the crustacean hemocyanins: divergence in incipient speciation. Biol. Bull. Mar. Biol. Lab. 191 (1996) 33-41
49. Mangum C.P. Hemocyanin subunit composition and oxygen binding in two species of the lobster genus Homarus and their hybrids. Biol. Bull. Mar. Biol. Lab. 184 (1993) 105-113
50. Mangum C.P. Structural and functional polymorphism of the haemocyanin O2 transport system of the sand fiddler crab Uca pugilator. J. Exp. Mar. Biol. Ecol. 165 (1993) 133-141
51. Mangum C.P. Subunit composition of hemocyanins of Callinectes sapidus: phenotypes from naturally hypoxic waters and isolated oligomers. Comp. Biochem. Physiol. 108B (1994) 537-541
52. Mangum C.P. Subunit composition of polymorphic hemocyanins in the decapod crustaceans: differences between sibling species. Physiol. Zool. 69 (1996) 568-585
53. Mangum C.P. Adaptation of the oxygen transport system to hypoxia in the blue crab, Callinectes sapidus. Am. Zool. 37 (1997) 604-611
54. Mangum C.P., and Greaves J. Hemocyanins of the genus Uca: structural polymorphisms and native oligomers. J. Exp. Mar. Biol. Ecol. 199 (1996) 1-15
55. 2 binding of blue crab hemocyanin. Biol. Bull. Mar. Biol. Lab. 174 (1988) 77-82
56. Mangum C.P., McMahon B.R., DeFur P.L., and Wheatly M.G. Gas exchange, acid-base balance, and the oxygen supply to the tissues during a molt of the blue crab Callinectes sapidus. J. Crustac. Biol. 5 (1985) 188-206
57. Mangum C.P., Greaves J., and Rainer J.S. Oligomer composition and oxygen binding of the hemocyanin of the blue crab Callinectes sapidus. Biol. Bull. Mar. Biol. Lab. 181 (1991) 453-458
58. Markl J. Evolution and function of structurally diverse subunits in the respiratory protein hemocyanin from arthropods. Biol. Bull. Mar. Biol. Lab. 171 (1986) 90-115
59. Markl J., and Decker H. Molecular structure of the arthropod hemocyanins. In: Mangum C.P. (Ed). Advances in Comparative and Environmental Physiology. Blood and tissue oxygen carriers vol. 13 (1992), Springer-Verlag, Berlin 325-376
60. Markl J., Markl A., Schartau W., and Linzen B. Subunit heterogeneity in arthropod hemocyanins. I. Chelicerata. J. Comp. Physiol. 130 (1979) 283-292
61. Markl J., Hofer A., Bauer G., Markl A., Kempter B., Brenzinger M., and Linzen B. Subunit heterogeneity in arthropod hemocyanins: II. Crustacea. J. Comp. Physiol. 133 (1979) 167-175
62. Markl J., Stöcker W., Runzler R., and Precht E. Immunological correspondences between the hemocyanin subunits of 86 arthropods: evolution of a multigene protein family. In: Linzen B. (Ed). Invertebrate Oxygen Carriers (1986), Springer, Heidelberg 281-292
63. Mason R.P., Mangum C.P., and Godette G. The influence of inorganic ions and acclimation salinity on hemocyanin oxygen binding in the blue crab Callinectes sapidus. Biol. Bull. Mar. Biol. Lab. 164 (1983) 104-123
64. McMahon B.R. Respiratory and circulatory compensation to hypoxia in crustaceans. Res. Physiol. 128 (2001) 349-364
65. Molon A., et al. Molecular heterogeneity of the hemocyanin isolated from the king crab Paralithodes camtschaticae. Eur. J. Biochem. 267 (2000) 7046-7057
66. Morris S. Organic ions as modulators of respiratory function during stress. Physiol. Zool. 63 (1990) 253-287
67. Morris S., Bridges C.R., and Grieshaber M.K. A new role for uric acid: modulator of haemocyanin oxygen affinity in crustaceans. J. Exp. Zool. 235 (1985) 135-139
68. Murray A.C., and Jeffrey P.D. Hemocyanin from the Australian freshwater crayfish Cherax destructor. Subunit heterogeneity. Biochemistry 13 (1974) 3667-3671
69. Neuteboom B., Jekel P.A., and Beintema J.J. Primary structure of hemocyanin subunit c from Panulirus interruptus. Eur. J. Biochem. 206 (1992) 243-249
70. Nies A., Zeis B., Bridges C.R., and Grieshaber M.K. Allosteric modulation of haemocyanin oxygen-affinity by L-lactate and urate in the lobster Homarus vulgaris. II. Characterization of specific effector binding sites. J. Exp. Biol. 168 (1992) 111-124
71. Olson K.S., and Mcdowell Capuzzo J. Structure and function of hemocyanin in larval American lobsters. Am. Zool. 29 (1989) 20A
72. Olson K., Terwilliger N., and Mcdowell Capuzzo J. Structure of hemocyanin in larval and adult American lobsters. Am. Zool. 28 (1988) 47A
73. Rainbow P.S., and Abdennour C. Copper and haemocyanin in the mesopelagic decapod crustacean Systellaspis debilis. Oceanol. Acta 12 (1989) 91-94
74. 2 binding of the crustacean hemocyanins: interspecific relationships. Biol. Bull. Mar. Biol. Lab. 187 (1994) 385-397
75. Rickey B., Decker H., and Gill S.J. Binding of oxygen and carbon monoxide to arthropod hemocyanin: an allosteric analysis. Biochemistry 24 (1985) 109-117
76. Salvato B., and Beltramini M. Hemocyanins: molecular architecture, structure and reactivity of the binuclear copper active site. Life Chem. Rep. 8 (1990) 1-47
77. Schluter D. Ecology and the origin of species. Trends Ecol. Evol. 16 (2001) 372-380
78. Senkbeil E.G., and Wriston Jr. J.C. Hemocyanin synthesis in the American lobster, Homarus americanus. Comp. Biochem. Physiol. 68B (1980) 163-171
79. Skinner D. Molting and regeneration. In: Bliss D.E., and Mantel L.H. (Eds). The Biology of Crustacea vol. 9 (1985), Academic Press, Orlando 44-128
80. Soeter N.M., Beintema J.J., Jekel P.A., Bak H.J., Vereijken J.M., and Neuteboom B. Subunits a, b and c of Panulirus interruptus hemocyanin and evolution of arthropod hemocyanin. In: Linzen B. (Ed). Invertebrate Oxygen Carriers (1986), Springer, Heidelberg 153-163
81. Spicer J.I., and Baden S.P. Natural variation in the concentrations of haemocyanin from three decapod crustaceans, Nephrops norvegicus, Liocarcinus depurator and Hyas aranaeus. Mar. Biol. 136 (2000) 55-61
82. Spicer J.I., and Baden S.P. Environmental hypoxia and haemocyanin variability in Norway lobsters Nephrops norvegicus (L.). Mar. Biol. 139 (2001) 727-734
83. Spicer J.I., and Eriksson S.P. Does the development of respiratory regulation always accompany the transition from pelagic larvae to benthic fossorial postlarvae in the Norway lobster Nephrops norvegicus (L)?. J. Exp. Mar. Biol. Ecol. 295 (2003) 219-243
84. Spicer J.I., and Hodgson E. Between-population variation in haemocyanin subunit composition of the beachflea Orchestia gammarellus (Crustacea: Amphipoda). J. Mar. Biol. Assoc. UK 83 (2003) 945-947
85. Spicer J.I., and Hodgson E. Structural basis for salinity-induced alteration in oxygen binding by haemocyanin from the estuarine amphipod Chaetogammarus marinus (L.). Physiol. Biochem. Zool. 76 (2003) 26-32
86. Spicer J.I., and Strömberg J.O. Diel vertical migration and the haemocyanin of krill Meganyctiphanes norvegica. Mar. Ecol., Prog. Ser. 238 (2002) 153-162
87. Spicer J.I., and Weber R.E. Respiratory impairment in crustaceans and molluscs due to exposure to heavy metals. Comp. Biochem. Physiol. 100C (1991) 339-342
88. Spicer J.I., Thomasson M.A., and Strömberg J.O. Possessing a poor anaerobic capacity does not prevent the diel vertical migration of Nordic krill Meganyctiphanes norvegica into hypoxic waters. Mar. Ecol., Prog. Ser. 185 (1999) 181-187
89. Spindler K.D., Hennecke R., and Gellisson G. Protein production and the molting cycle in the crayfish Astacus leptodactylus (Nordmann, 1842). II. Hemocyanin and protein synthesis in the midgut gland. Gen. Comp. Endocr. 85 (1992) 248-253
90. Stöcker W., Raeder U., Bijolt M.M., Wichertjes T., van Bruggen E.F.J., and Markl J. The quaternary structure of four crustacean two-hexameric hemocyanins: immunocorrelation, stoichiometry, reassembly and topology of individual subunits. J. Comp. Physiol., B 158 (1988) 271-289
91. Strömberg J.O., and Spicer J.I. Cold comfort for krill? Respiratory consequences of diel vertical migration of Meganyctiphanes norvegica into deep hypoxic waters. Ophelia 53 (2001) 213-217
92. Taylor H.H., and Anstiss J.M. Copper and haemocyanin dynamics in aquatic invertebrates. Mar. Freshw. Res. 50 (1999) 907-931
93. Taylor J.R.A., and Kier W.M. Switching skeletons: hydrostatic support in molting crabs. Science 301 (2003) 209-210
94. Terwilliger N.B. Functional adaptations of oxygen-transport proteins. J. Exp. Biol. 201 (1998) 1085-1098
95. Terwilliger N.B., and Brown A.C. Ontogeny of hemocyanin function in the Dungeness crab Cancer magister: the interactive effects of developmental stage and divalent cations on hemocyanin oxygenation properties. J. Exp. Biol. 183 (1993) 1-13
96. Terwilliger N.B., and Otoshi C. Cryptocyanin and hemocyanin: fluctuations of crab hemolymph proteins during molting. Physiologist 37 (1994) A-67
97. Terwilliger N.B., and Dumler K. Ontogeny of decapod crustacean hemocyanin: effects of temperature and nutrition. J. Exp. Biol. 204 (2001) 1013-1020
98. Terwilliger N.B., and Ryan M. Ontogeny of crustacean respiratory proteins. Am. Zool. 41 (2001) 1057-1067
99. Terwilliger N.B., and Ryan M.C. Functional and phylogenetic analyses of phenoloxidases from Brachyuran (Cancer magister) and Branchiopod (Artemia franciscana, Triops longicaudatus) Crustaceans. Biol. Bull. Mar. Biol. Lab. 210 (2006) 38-50
100. Terwilliger N.B., and Terwilliger R.C. Changes in the subunit structure of Cancer magister hemocyanin during larval development. J. Exp. Zool. 221 (1982) 181-191
101. Terwilliger N.B., Ryan M.C., and Towle D. Evolution of novel functions: cryptocyanin helps build new exoskeleton in Cancer magister. J. Exp. Biol. 208 (2005) 2467-2474
102. Terwilliger N.B., Ryan M., and Phillips M.R. Crustacean hemocyanin gene family and microarrays of expression change during eco-physiological stress. Integr. Comp. Biol. 46 (2006) 991-999
103. Terwilliger N.B., Terwilliger R.C., and Graham R. Crab hemocyanin function changes during development. In: Linzen B. (Ed). Invertebrate oxygen carriers (1986), Springer, Heidelberg 333-335
104. Truchot J.P. Variations de la concentration sanguine d'hémocyanine fonctionnelle au cours du cycle d'intermue chez le crabe Carcinus maenas (L.). Arch. Zool. Exp. Gén. 119 (1978) 265-282
105. Truchot J.P. Respiratory function of arthropod hemocyanins. In: Mangum C.P. (Ed). Advances in Comparative and Environmental Physiology. Blood and tissue oxygen carriers vol. 13 (1992), Springer-Verlag, Berlin 377-410
106. Uglow R.F. Haemolymph protein concentrations in portunid crabs-I. Studies on adult Carcinus maenas. Comp. Biochem. Physiol. 30 (1969) 1083-1090
107. Uglow R.F. Haemolymph protein concentrations in portunid crabs. II. The effects of imposed fasting on Carcinus maenas. Comp. Biochem. Physiol. 31 (1969) 959-967
108. van Holde K.E., Miller K.I., and Decker H. Hemocyanins and invertebrate evolution. J. Biol. Chem. 276 (2001) 15563-15566
109. Voit R., Feldmaier-Fuchs G., Schweikardt T., Decker H., and Burmester T. Complete sequence of the 24mer hemocyanin of the tarantula Eurypelma californicum: structure and intramolecular evolution of the subunits. J. Biol. Chem. 275 (2000) 39339-39344
110. Volbeda A., and Hol W.G.J. Crystal structure of hexameric hemocyanin from Panulirus interruptus refined at 3.2 Å resolution. J. Mol. Biol. 209 (1989) 249-279
111. Yoo B.S., Kim S.B., Lee J.H., and Yang K.H. The subunit composition of Portunus trituberculatus hemocyanin polymers. Biochem. Biophys. Res. Commun. 153 (1988) 748-752
112. Zuckerkandl E. Hémocyanine et cuivre chez un Crustacé Décapode dans leurs rapports avec le cycle d'intermue. Ann. Inst. Océanogr., Paris 38 (1960) 1-122