Native and subunit molecular mass and quarternary structure of the hemoglobin from the primitive branchiopod crustacean Triops cancriformis

FEBS Journal

Volumn 273, Issue 17, 2006, Pages 4055-4071

  Rousselot, Morgane ^a   Jaenicke, Elmar ^b   Lamkemeyer, Tobias ^c   Harris, J Robin ^b   Pirow, Ralph ^d  

^a STATION BIOLOGIQUE   (France)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Crustacea; Hemoglobin; Structure function relationship

Indexed keywords

CYSTEINE; HEMOGLOBIN; HETERODIMER; HOMODIMER; ISOPROTEIN; PROTEIN SUBUNIT; THIOL GROUP;

ANIMAL TISSUE; ARTICLE; CARBAMIDOMETHYLATION; CRUSTACEA; DISSOCIATION; DISULFIDE BOND; ELECTROSPRAY MASS SPECTROMETRY; GEOMETRY; LIGHT SCATTERING; METHYLATION; MOLECULAR SIZE; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; REDUCTION; SHRIMP; STOICHIOMETRY; STRUCTURE ACTIVITY RELATION; TRANSMISSION ELECTRON MICROSCOPY; TRIOPS CANCRIFORMIS; ULTRACENTRIFUGATION;

ANIMALS; CATTLE; CRUSTACEA; HEMOGLOBIN A; HEMOGLOBINS; HEMOLYMPH; MOLECULAR WEIGHT; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; STRUCTURE-ACTIVITY RELATIONSHIP;

BRANCHIOPODA; CRUSTACEA; NOTOSTRACA; TRIOPS CANCRIFORMIS;

EID: 33747384254     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05408.x     Document Type: Article

References (77)

1. Svedberg T & Eriksson-Quensel IB (1934) The molecular weight of erythrocruorin - II. J Am Chem Soc 56, 1700-1706.
2. Ilan E & Daniel E (1979) Structural diversity of arthropod extracellular hemoglobins. Comp Biochem Physiol B Biochem Mol Biol 63, 303-308.
3. Terwilliger RC (1980) Structures of invertebrate hemoglobins. Am Zool 20, 53-67.
4. Dangott LJ & Terwilliger RC (1981) Arthropod extracellular hemoglobins: structural and functional properties. Comp Biochem Physiol B Biochem Mol Biol 70, 549-557.
5. Ghidalia W (1985) Structural and biological aspects of pigments. In The Biology of Crustacea, Vol. 9 Integument, Pigments, and Hormonal Processes (Bliss DE & Mantel LH, eds), pp. 347-363. Academic Press, New York.
6. Vinogradov SN (1985) The structure of invertebrate extracellular hemoglobins (erythrocruorins and chlorocruorins). Comp Biochem Physiol B Biochem Mol Biol 82, 1-15.
7. Terwilliger NB (1992) Molecular structure of the extracellular heme proteins. In Advances in Comparative and Environmental Physiology, Vol. 13 Blood and Tissue Oxygen Carriers (Mangum CP, ed.), pp. 193-229. Springer-Verlag, Berlin.
8. Weber RE & Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81, 569-628.
9. Gruner H-E (1993) Lehrbuch der Speziellen Zoologie (begr. durch Kaestner A), Band 1, 4. Teil, Wirbellose Tiere: Arthropoda (Ohne Insecta). Gustav Fischer Verlag, Jena.
10. Fox HM (1948) The hemoglobin of Daphnia. Proc R Soc Lond B Biol Sci 135, 195-212.
11. Fox HM, Gilchrist BM & Phear EA (1951) Functions of hemoglobin in Daphnia. Proc R Soc Lond B Biol Sci 138, 514-527.
12. Kobayashi M & Hoshi T (1982) Relationship between the hemoglobin concentration of Daphnia magna and the ambient oxygen concentration. Comp Biochem Physiol A Physiol 72, 247-249.
13. Zeis B, Becher B, Goldmann T, Clark R, Vollmer E, Bolke B, Bredebusch I, Lamkemeyer T, Pinkhaus O, Pirow R et al. (2003) Differential hemoglobin gene expression in the crustacean Daphnia magna exposed to different oxygen partial pressures. Biol Chem 384, 1133-1145.
14. Paul RJ, Zeis B, Lamkemeyer T, Seidl M & Pirow R (2004) Control of oxygen transport in the microcrustacean Daphnia: regulation of hemoglobin expression as central mechanism of adaptation to different oxygen and temperature conditions. Acta Physiol Scand 182, 259-275.
15. Kobayashi M, Fujiki M & Suzuki T (1988) Variation in and oxygen-binding properties of Daphnia magna hemoglobin. Physiol Zool 61, 415-419.
16. Kobayashi M, Ishigaki K-I, Kobayashi M, Igarashi Y & Imai K (1994) Oxygen transport efficiency of multiple-component hemoglobin in Daphnia magna. Can J Zool 72, 2169-2171.
17. Tokishita S, Shiga Y, Kimura S, Ohta T, Kobayashi M, Hanazato T & Yamagata H (1997) Cloning and analysis of a cDNA encoding a two-domain hemoglobin chain from the water flea Daphnia magna. Gene 189, 73-78.
18. Dewilde S, Van Hauwaert ML, Peeters K, Vanfleteren J & Moens L (1999) Daphnia pulex didomain hemoglobin: structure and evolution of polymeric hemoglobins and their coding genes. Mol Biol Evol 16, 1208-1218.
19. Hebert PDN, Um YM, Prokopowich CD & Taylor DJ (1999) Gene conversion and evolution of daphniid hemoglobins (Crustacea, Cladocera). J Mol Evol 49, 769-779.
20. Kimura S, Tokishita S, Ohta T, Kobayashi M & Yamagata H (1999) Heterogeneity and differential expression under hypoxia of two-domain hemoglobin chains in the water flea, Daphnia magna. J Biol Chem 274, 10649-10653.
21. Nunes F, Spiering S, Wolf M, Wendler A, Pirow R & Paul RJ (2005) Sequencing of hemoglobin gene 4 (dmhb4) and southern blot analysis provide evidence of more than four members of the Daphnia magna globin family. Biosci Biotechnol Biochem 69, 1193-1197.
22. Gorr TA, Cahn JD, Yamagata H & Bunn HF (2004) Hypoxia-induced synthesis of hemoglobin in the crustacean Daphnia magna is hypoxia-inducible factor-dependent. J Biol Chem 279, 36038-36047.
23. Kobayashi M & Hoshi T (1984) Analysis of respiratory role of hemoglobin in Daphnia magna. Zool Sci 1, 523-532.
24. Pirow R, Bäumer C & Paul RJ (2001) Benefits of hemoglobin in the cladoceran crustacean Daphnia magna. J Exp Biol 204, 3425-3441.
25. Pirow R, Baumer C & Paul RJ (2004) Crater landscape: two-dimensional oxygen gradients in the circulatory system of the microcrustacean Daphnia magna. J Exp Biol 207, 4393-4405.
26. Seidl MD, Paul RJ & Pirow R (2005) Effects of hypoxia acclimation on morpho-physiological traits over three generations of Daphnia magna. J Exp Biol 208, 2165-2175.
27. Kobayashi M & Yamagata H (2000) Structure and function of hemoglobin in Daphnia magna. Trends Comp Biochem Physiol 6, 163-174.
28. Lamkemeyer T, Paul RJ, Stocker W, Yiallouros I & Zeis B (2005) Macromolecular isoforms of Daphnia magna hemoglobin. Biol Chem 386, 1087-1096.
29. Feder ME & Mitchell-Olds T (2003) Evolutionary and ecological functional genomics. Nat Rev Genet 4, 651-657.
30. Fryer G (1988) Studies on the functional morphology and biology of the notostraca (Crustacea, Branchiopoda). Phil Trans R Soc Lond B 321, 27-127.
31. Horne FR & Beyenbach KW (1974) Physicochemical features of hemoglobin of the crustacean, Triops longicaudatus. Arch Biochem Biophys 161, 369-374.
32. Guadagnoli JA, Braun AA, Roberts SP & Reiber CL (2005) Environmental hypoxia influences hemoglobin subunit composition in the branchiopod crustacean Triops longicaudatus. J Exp Biol 208, 3543-3551.
33. Robert CH, Decker H, Richey B, Gill SJ & Wyman J (1987) Nesting: hierarchies of allosteric interactions. Proc Natl Acad Sci USA 84, 1891-1895.
34. Hellmann N, Weber RE & Decker H (2003) Nested allosteric interactions in extracellular hemoglobin of the leech Macrobdella decora. J Biol Chem 278, 44355-44360.
35. Fish WW, Reynolds JA & Tanford C (1970) Gel chromatography of proteins in denaturating solvents. J Biol Chem 245, 5166-5168.
36. Vinogradov SA, Shlom JM & Doyle M (1980) Dissociation of the extracellular hemoglobin of Arenicola cristata. Comp Biochem Physiol B Biochem Mol Biol 65, 145-150.
37. Eike JH & Palmer AF (2004) Effects of glutaraldehyde concentration on the physical properties of polymerized hemoglobin-based oxygen carriers. Biotechnol Prog 20, 1225-1232.
38. Rousselot M, Le Guen D, Chabasse C & Zal F (2006) Novel dissociation mechanism of a polychaetous annelid extracellular hemoglobin. FEBS J 273, 1582-1596.
39. Ferguson KA (1964) Starch-gel electrophoresis - application to the classification of pituitary proteins and polypeptides. Metabolism 13, 985-1002.
40. Rodbard D & Chrambach A (1970) Unified theory for gel electrophoresis and gel filtration. Proc Natl Acad Sci USA 65, 970-977.
41. Chrambach A & Rodbard D (1971) Polyacrylamide gel electrophoresis. Science 172, 440-451.
42. Ilan E, Weisselberg E & Daniel E (1982) Erythrocruorin from the water-flea Daphnia magna. Quarternary structure and arrangement of subunits. Biochem J 207, 297-303.
43. Harris JR & Scheffler D (2002) Routine preparation of air-dried negatively stained and unstained specimens on holey carbon support films: a review of applications. Micron 33, 461-480.
44. Sanglier S, Leize E, Van Dorsselaer A & Zal F (2003) Comparative ESI-MS study of ∼ 2.2 MDa native hemocyanins from deep-sea and shore crabs: from protein oligomeric state to biotope. J Am Soc Mass Spectrom 14, 419-429.
45. Pirow R (2003) The contribution of hemoglobin to oxygen transport in the microcrustacean Daphnia magna - a conceptual approach. Adv Exp Med Biol 510, 101-107.
46. Pirow R & Buchen I (2004) The dichotomous oxyregulatory behaviour of the planktonic crustacean Daphnia magna. J Exp Biol 207, 683-696.
47. Hoshi T & Kobayashi M (1971) Studies on physiology and ecology of plankton. XXV. Iron-content and millimolar extinction coefficient of the Daphnia-hemoglobin. Sci Rep Niigata University Ser D (Biol) 8, 65-68.
48. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
49. Westermeier R (2006) Elektrophorese-Praktikum. VCH, New York.
50. Ferrige AG, Seddon MJ, Green BN, Jarvis SA & Skilling J (1992) Disentangling electrospray spectra with maximum-entropy. Rapid Commun Mass Spectrom 6, 707-711.
51. Vistica J, Dam J, Balbo A, Yikilmaz E, Mariuzza RA, Rouault TA & Schuck P (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal Biochem 326, 234-256.
52. Schuck P & Demeler B (1999) Direct sedimentation analysis of interference optical data in analytical ultracentrifugation. Biophys J 76, 2288-2296.
53. Schuck P (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78, 1606-1619.
54. Lebowitz J, Lewis MS & Schuck P (2002) Modern analytical ultracentrifugation in protein science: a tutorial review. Protein Sci 11, 2067-2079.
55. Ar A & Schejter A (1970) Isolation and properties of the hemoglobin of the clam shrimp Cyzicus cf. hierosolymitanus (S. Fischer). Comp Biochem Physiol 33, 481-490.
56. Zimm BH (1948) The scattering of light and the radial distribution function of high polymer solutions. J Chem Phys 16, 1093-1099.
57. Perkins SJ (1986) Protein volumes and hydration effects. The calculations of partial specific volumes, neutron scattering matchpoints and 280-nm absorption coefficients for proteins and glycoproteins from amino acid sequences. Eur J Biochem 157, 169-180.
58. Cohn EJ & Edsall JT (1943) Proteins, Amino Acids and Peptides as Ions and Dipolar Ions. Reinhold Publishing Corporation, New York.
59. De Haen C (1987) Molecular weight standards for calibration of gel filtration and sodium dodecyl sulfate-polyacrylamide gel electrophoresis: ferritin and apoferritin. Anal Biochem 166, 235-245.
60. Harpaz Y, Gerstein M & Chothia C (1994) Volume changes on protein folding. Structure 2, 641-649.
61. Harris JR (1997) Negative Staining and Cryoelectron Microscopy: the Thin Film Techniques. Bios Scientific Publishers, Oxford.
62. Harris JR, Schröder E, Isupov MN, Scheffler D, Kristensen P, Littlechild JA, Vagin AA & Meissner U (2001) Comparison of the decameric structure of peroxiredoxin-II by transmission electron microscopy and X-ray crystallography. Biochim Biophys Acta 1547, 221-234.
63. Moens L & Kondo M (1978) Evidence for a dimeric form of Artemia salina extracellular hemoglobins with high-molecular-weight subunits. Eur J Biochem 82, 65-72.
64. Matthews CM, Vandenberg CJ & Trotman CNA (1998) Variable substitution rates of the 18 domain sequences in Artemia hemoglobin. J Mol Evol 46, 729-733.
65. Ilan E, David MM & Daniel E (1981) Erythrocruorin from the crustacean Caenestheria inopinata. Quarternary structure and arrangement of subunits. Biochemistry 20, 6190-6194.
66. Ilan E & Daniel E (1979) Haemoglobin from the tadpole shrimp, Lepidurus apus lubbocki. Characterization of the molecule and determination of the number of polypeptide chains. Biochem J 183, 325-330.
67. Dangott LJ & Terwilliger RC (1979) Structural studies of a branchiopod crustacean (Lepidurus bilobatus) extracellular hemoglobin. Evidence for oxygen-binding domains. Biochim Biophys Acta 579, 452-461.
68. Zeis B, Becher B, Lamkemeyer T, Rolf S, Pirow R & Paul RJ (2003) The process of hypoxic induction of Daphnia magna hemoglobin: subunit composition and functional properties. Comp Biochem Physiol B Biochem Mol Biol 134, 243-252.
69. Dangott LJ & Terwilliger RC (1980) The subunit structure of Daphnia pulex hemoglobin. Comp Biochem Physiol B Biochem Mol Biol 67, 301-306.
70. Peeters K, Mertens J, Hebert P & Moens L (1990) The globin composition of Daphnia pulex hemoglobin and the comparison of the amino acid composition of invertebrate hemoglobins. Comp Biochem Physiol B Biochem Mol Biol 97, 369-381.
71. Sugano H & Hoshi T (1971) Purification and properties of blood hemoglobin from fresh-water cladocera, Moina macrocopa and Daphnia magna. Biochim Biophys Acta 229, 349-358.
72. Kato K, Tokishita S, Mandokoro Y, Kimura S, Ohta T, Kobayashi M & Yamagata H (2001) Two-domain hemoglobin gene of the water flea Moina macrocopa: duplication in the ancestral Cladocera, diversification, and loss of a bridge intron. Gene 273, 41-50.
73. Moens L (1982) The extracellular hemoglobins of Artemia sp.: a biochemical and ontogenetical study. Meded K Acad Wet Lett Schone Kunsten Belg Kl Wet 44, 1-21.
74. Tsfadia Y, Shaked I & Daniel E (1990) Molecular symmetry and arrangement of subunits in extracellular hemoglobin from Caenestheria inopinata. Eur J Biochem 193, 25-29.
75. David MM, Schejter A, Daniel E, Ar A & Ben Shaul Y (1977) Subunit structure of hemoglobin from the clam shrimp Cyzicus. J Mol Biol 111, 211-214.
76. Yamauchi K & Ochiai T (1984) Dissociation of the extracellular hemoglobin of Daphnia magna. Comp Biochem Physiol B Biochem Mol Biol 79, 465-471.
77. Svedberg T (1933) Sedimentation constants, molecular weights, and isoelectric points of respiratory proteins. J Biol Chem 103, 311-325.