Lack of conventional oxygen-linked proton and anion binding sites does not impair allosteric regulation of oxygen binding in dwarf caiman hemoglobin

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 3, 2013, Pages

  Weber, Roy E ^a   Fago, Angela ^a   Malte, Hans ^a   Storz, Jay F ^b   Gorr, Thomas A ^c,d  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF NEBRASKA   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Allosteric interaction; Bohr effect; Carbon dioxide; Crocodilians; Oxygen binding

Indexed keywords

ANION; BICARBONATE; CARBON DIOXIDE; HEMOGLOBIN; HEMOGLOBIN ALPHA CHAIN; HEMOGLOBIN BETA CHAIN; ORGANOPHOSPHATE; OXYGEN; PROTON;

ALLOSTERISM; ARTICLE; BICARBONATE BLOOD LEVEL; BINDING SITE; BOHR EFFECT; CAIMAN; CROCODILIAN; DEOXYGENATION; DIVING; NONHUMAN; OXYGEN AFFINITY; PALEOSUCHUS PALPEBROSUS; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

ALLOSTERIC INTERACTION; BOHR EFFECT; CARBON DIOXIDE; CROCODILIANS; OXYGEN-BINDING;

ALLIGATORS AND CROCODILES; ALLOSTERIC REGULATION; ALPHA-GLOBINS; ANIMALS; ANIONS; BETA-GLOBINS; BINDING SITES; CARBON DIOXIDE; CHLORIDES; CHROMATOGRAPHY, GEL; HEMOGLOBINS; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; MOLECULAR WEIGHT; OXYGEN CONSUMPTION; PEPTIDES; PHOSPHATES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN HYDROLYSATES; PROTONS; TEMPERATURE; TRYPSIN;

EID: 84880971703     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00014.2013     Document Type: Article

References (100)

1. Ackers GK. Molecular exclusion and restricted diffusion processes in molecular-sieve chromatography. Biochemistry 3: 723-730, 1964.
2. Amiconi G, Bertollini A, Bellelli A, Coletta M, Condò SG, Brunori M. Evidence for two oxygen-linked binding sites for polyanions in dromedary hemoglobin. Eur J Biochem 150: 387-393, 1985.
3. Antonini E, Wyman J, Brunori M, Fronticelli C, Bucci E, Rossi-Fanelli A. Studies on the relations between molecular and functional properties of hemoglobin. V. The influence of temperature on the Bohr effect in human and in horse hemoglobin. J Biol Chem 240: 1096-1103, 1965.
4. Atha DH, Ackers GK. Calorimetric determination of the heat of oxygenation of human hemoglobin as a function of pH and the extent of reaction. Biochemistry 13: 2376-2382, 1974.
5. Bårdgard A, Fago A, Malte H, Weber RE. Oxygen binding and aggregation of hemoglobin from the common European frog, Rana temporaria. Comp Biochem Physiol B Biochem Mol Biol 117: 225-231, 1997.
6. Baudin-Creuza V, Fablet C, Zal F, Green BN, Prome D, Marden MC, Pagnier J, Wajcman H. Hemoglobin Porto Alegre forms a tetramer of tetramers superstructure. Protein Sci 11: 129-136, 2002.
7. 2 and 2,3 diphosphoglycerate on the Bohr effect of human haemoglobin. Life Sci 8: 1041-1046, 1969.
8. Bauer C, Forster M, Gros G, Mosca A, Perrella M, Rollema HS, Vogel D. Analysis of bicarbonate binding to crocodilian hemoglobin. J Biol Chem 256: 8429-8435, 1981.
9. Bauer C, Jelkmann W. Carbon dioxide governs the oxygen affinity of crocodile blood. Nature 269: 825-827, 1977.
10. 2 binding to isolated β subunits of human hemoglobin. J Biol Chem 252: 2952-2955, 1977.
11. Berenbrink M. Evolution of vertebrate haemoglobins: histidine side chains, specific buffer value and Bohr effect. Respir Physiol Neurobiol 154: 165-184, 2006.
12. Bonaventura J, Bonaventura C, Brunori M, Giardina B, Antonini E, Bossa F, Wyman J. Functional properties of carboxypeptidase-digested hemoglobins. J Mol Biol 82: 499-511, 1974.
13. Borgese TA, Harrington JP, Ganjian I, Duran C. Haemoglobin properties and polymerization in the marine teleost Lophius americanus (Goosefish). Comp Biochem Physiol 91: 663-670, 1988.
14. Briehl RW. The relation between the oxygen equilibrium and aggregation of subunits in lamprey hemoglobin. J Biol Chem 238: 2361-2366, 1963.
15. Brochu CA. Phylogenetic relationships of Necrosuchus ionensis Simpson, 1937 and the early history of caimanines. Zool J Linnean Soc 163: S228-S256, 2011.
16. Brunori M, Cutruzzolà F, Vallone B. Haemoglobin engineering: for fun and money. Curr Biol 5: 462-465, 1995.
17. Chiancone E. Dissociation of hemoglobin into subunits. II. Human oxyhemoglobin: gel filtration studies. J Biol Chem 243: 1212-1219, 1968.
18. Choi H. Paleosuchus palpebrosus (online). Animal Diversity Web. Accessed February 22, 2013 at http://animaldiversity.ummz.umich.edu/accounts/Paleosuchus_palpebrosus/.
19. Coulson RA, Hernandez T. Increase in metabolic rate of the alligator fed proteins or amino acids. J Nutr 109: 538-550, 1979.
20. Coulson RA, Hernandez T. Alligator metabolism: studies on chemical reactions in vivo. Comp Biochem Physiol B 74: 1-175, 1983.
21. D'Avino R, Fago A, Kunzmann A, Prisco G. The primary structure and oxygen-binding properties of the single haemoglobin of the high-Antarctic fish Aethotaxis mitopteryx DeWitt. Polar Biol 12: 135-140, 1992.
22. Elder GE, Lappin TR, Horne AB, Fairbanks VF, Jones RT, Winter PC, Green BN, Hoyer JD, Reynolds TM, Shih DT, Mccormick DJ, Kubik KS, Madden BJ, Head CG, Harvey D, Roberts NB. Hemoglobin Old Dominion/Burton-upon-Trent, beta 143 (H21) His→Tyr, codon 143 CAC→TAC-a variant with altered oxygen affinity that compromises measurement of glycated hemoglobin in diabetes mellitus: structure, function, and DNA sequence. Mayo Clin Proc 73: 321-328, 1998.
23. Elli R, Giuliani A, Tentori L, Chiancone E, Antonini E. The hemoglobin of amphibia. X. Sedimentation behaviour of frog, Triton and Axolotl hemoglobins. Comp Biochem Physiol 36: 163-171, 1970.
24. Fablet C, Marden MC, Green BN, Ho C, Pagnier J, Baudin-Creuza V. Stable octameric structure of recombinant hemoglobin alpha(2)beta(2)83 Gly→Cys. Protein Sci 12: 690-695, 2003.
25. Fago A, Romano M, Tamburrini M, Coletta M, D'Avino R, Di Prisco G. A polymerising Root-effect fish hemoglobin with high subunit heterogeneity. Correlation with primary structure. Eur J Biochem 218: 829-835, 1993.
26. Fago A, Weber RE. Hagfish hemoglobins. In: The Biology of Hagfishes, edited by Jørgensen JM, Lomholt JP, Malte H, and Weber RE. London: Chapman & Hall, 1996.
27. Fang TY, Zou M, Simplaceanu V, Ho NT, Ho C. Assessment of roles of surface histidyl residues in the molecular basis of the Bohr effect and of β143 histidine in the binding of 2,3-bisphosphoglycerate in human normal adult hemoglobin. Biochemistry 38: 13423-13432, 1999.
28. Fermi G, Perutz MF. Atlas of Molecular Structures in Biology. 2. Haemoglobin and Myoglobin. Oxford, UK: Clarendon Press, 1981.
29. Focesi A, Ogo SH, Matsuura MS, Say JC. Further evidence of dimertetramer transition in hemoglobin from Liophis miliaris. Braz J Med Biol Res 20: 861-864, 1987.
30. Gienger CM, Tracy CR, Brien ML, Manolis SC, Webb GJ, Seymour RS, Christian KA. Energetic costs of digestion in Australian crocodiles. Aust J Zool 59: 416-421, 2012.
31. Gorr TA, Mable BK, Kleinschmidt T. Phylogenetic analysis of reptilian hemoglobins: trees, rates, and divergences. J Mol Evol 47: 471-485, 1998.
32. Grispo MT, Natarajan C, Projecto-Garcia J, Moriyama H, Weber RE, Storz JF. Gene duplication and the evolution of hemoglobin isoform differentiation in birds. J Biol Chem 287: 37647-37658, 2012.
33. Harano T, Harano K, Kushida Y, Imai K, Nishinakamura R, Matsunaga T. Hb Kodaira [beta 146(HC3)His--Gln]: a new beta chain variant with an amino acid substitution at the C-terminus. Hemoglobin 16: 85-91, 1992.
34. Hasegawa T, Shishikura F, Kuwada T. Side-necked turtle (Pleurodira, Chelonia, reptilia) hemoglobin: cDNA-derived primary structures and X-ray crystal structures of Hb A. IUBMB Life 63: 188-196, 2011.
35. Hastings AK, Bloch JI, Jaramillo CA, Rincon AF, MacFadden BJ. Systematics and biogeography of crocodylians from the Miocene of Panama. J Vert Paleontol 33: 239-263, 2013.
36. Hoffmann FG, Storz JF, Gorr TA, Opazo JC. Lineage-specific patterns of functional diversification in the alpha- and beta-globin gene families of tetrapod vertebrates. Mol Biol Evol 27: 1126-1138, 2010.
37. Hofmann O, Carrucan G, Robson N, Brittain T. The chloride effect in the human embryonic haemoglobins. Biochem J 309: 959-962, 1995.
38. Imai K. Oxygen-equilibrium characteristics of abnormal hemoglobin Hiroshima (alpha-2 beta-2 143 Asp). Arch Biochem Biophys 127: 543-547, 1968.
39. Jelkmann W, Bauer C. Oxygen binding properties of caiman blood in the absence and presence of carbon dioxide. Comp Biochem Physiol A 65: 331-336, 1980.
40. Jensen FB. Hydrogen ion equilibria in fish haemoglobins. J Exp Biol 143: 225-234, 1989.
41. Jensen FB, Wang T, Jones DR, Brahm J. Carbon dioxide transport in alligator blood and its erythrocyte permeability to anions and water. Am J Physiol Regul Integr Comp Physiol 274: R661-R671, 1998.
42. 2 and 2,3- diphosphoglycerate. Br Med Bull 32: 209-213, 1976.
43. Kilmartin JV, Wootton JF. Inhibition of Bohr effect after removal of C-terminal histidines from haemoglobin β-chains. Nature 228: 766-767, 1970.
44. Knipp M, Taing JJ, He C. Reduction of the lipocalin type heme containing protein nitrophorin-sensitivity of the fold-stabilizing cysteine disulfides toward routine heme-iron reduction. J Inorg Biochem 105: 1405-1412, 2011.
45. Koldkjaer P, Berenbrink M. In vivo red blood cell sickling and mechanism of recovery in whiting, Merlangius merlangus. J Exp Biol 210: 3451-3460, 2007.
46. Komiyama N, Tame J, Nagai K. A hemoglobin-based blood substitute: transplanting a novel allosteric effect of crocodile Hb. Biol Chem 377: 543-548, 1996.
47. Komiyama NH, Miyazaki G, Tame J, Nagai K. Transplanting a unique allosteric effect from crocodile into human haemoglobin. Nature 373: 244-246, 1995.
48. Kosugi H, Weinstein AS, Kikugawa K, Asakura T, Schroeder WA. Characterization and properties of Hb York (beta 146 His leads to Pro). Hemoglobin 7: 205-226, 1983.
49. Kwiatkowski LD, Noble RW. The contribution of histidine (HC3) (146 beta) to the R state Bohr effect of human hemoglobin. J Biol Chem 257: 8891-8895, 1982.
50. Laurent TC, Killander J. A theory of gel filtration and its experimental verification. J Chromatogr 14: 317-330, 1964.
51. Leach M, Greaves M, Porter N, Williamson D, Brown K. Haemoglobin Hallamshire (b146 HIS→TYR): a new high oxygen affinity haemoglobin responsible for familial erythrocytosis. Clin Lab Haematol 18: 237-239, 1996.
52. Leclercq F, Schnek AG, Braunitzer G, Stangl A, Schrank B. Direct reciprocal allosteric interaction of oxygen and hydrogen carbonate. Sequence of the haemoglobins of the caiman (Caiman crocodilus), the Nile crocodile (Crocodylus niloticus) and the Mississippi crocodile (Alligator mississippiensis). Hoppe-Seylers Z Physiol Chem 362: 1151-1158, 1981.
53. Lee YW, Ki CS, Kim HJ, Lee ST, Kim CK, Shin HB, Hong DS, Lee YK. High oxygen-affinity hemoglobin variant associated with high-level venous oxygen saturation. Clin Chem Lab Med 46: 417-418, 2008.
54. Lukin JA, Ho C. The structure-function relationship of hemoglobin in solution at atomic resolution. Chem Rev 104: 1219-1230, 2004.
55. Matsuura MS, Ogo SH, Focesi A Jr. Dimer-tetramer transition in hemoglobins from Liophis miliaris-I. Effect of organic polyphosphates. Comp Biochem Physiol A Comp Physiol 86: 683-687, 1987.
56. Misgeld E, Gattermann N, Wehmeier A, Weiland C, Peters U, Kohne E. Hemoglobinopathy York [beta146 (HC3) His→Pro]: first report of a family history. Ann Hematol 80: 365-367, 2001.
57. Moffat K, Olson JS, Gibson QH, Kilmartin JV. The ligand-binding properties of desHis (146beta) hemoglobin. J Biol Chem 248: 6387-6393, 1973.
58. Monod J, Wyman J, Changeux JP. On the nature of allosteric transitions: a plausible model. J Mol Biol 12: 88-118, 1965.
59. Nielsen MS, Weber RE. Antagonistic interaction between oxygenationlinked lactate and CO2 binding to human hemoglobin. Comp Biochem Physiol A Mol Integr Physiol 146: 429-434, 2007.
60. Olianas A, Messana I, Sanna MT, Castagnola M, Manconi B, Masia D, Coluccia E, Giardina B, Pellegrini M. Two sites for GTP binding in cathodic haemoglobins from Anguilliformes. Comp Biochem Physiol B Biochem Mol Biol 141: 400-407, 2005.
61. Parkhurst LJ, Goss DJ, Perutz MF. Kinetic and equilibrium studies on the role of the β-147 histidine in the Root effect and cooperativity in carp hemoglobin. Biochemistry 22: 5401-5409, 1983.
62. Perutz MF. Stereochemistry of cooperative effects in haemoglobin. Haem-haem interaction and the problem of allostery. Nature 228: 726-734, 1970.
63. Perutz MF. Species adaptation in a protein molecule. Mol Biol Evol 1: 1-28, 1983.
64. Perutz MF, Bauer C, Gros G, Leclercq F, Vandecasserie C, Schnek AG, Braunitzer G, Friday AE, Joysey KA. Allosteric regulation of crocodilian haemoglobin. Nature 291: 682-684, 1981.
65. Perutz MF, Pulsinelli P, Eyck LT, Kilmartin JV, Shibata S, Iuchi I, Miyaji T, Hamilton HB. Haemoglobin Hiroshima and the mechanism of the alkaline Bohr effect. Nat New Biol 232: 147-149, 1971.
66. Rana MS, Knapp JE, Holland RA, Riggs AF. Component D of chicken hemoglobin and the hemoglobin of the embryonic Tammar wallaby (Macropus eugenii) self-associate upon deoxygenation: effect on oxygen binding. Proteins 70: 553-561, 2008.
67. Reischl E. High sulfhydryl content in turtle erythrocytes: is there a relation with resistance to hypoxia? Comp Biochem Physiol B 85: 723-726, 1986.
68. Reischl E, da Diefenbach CO. Heterogeneity and polymerization of hemoglobins of Caiman latirostris (Crocodylia: Reptilia). Comp Biochem Physiol B 54: 543-545, 1976.
69. Riccio A, Tamburrini M, Giardina B, Di Prisco G. Molecular dynamics analysis of a second phosphate site in the hemoglobins of the seabird, south polar skua. Is there a site-site migratory mechanism along the central cavity? Biophys J 81: 1938-1946, 2001.
70. Riggs A, Sullivan B, Agee JR. Polymerization of frog and turtle hemoglobins. Proc Natl Acad Sci USA 51: 1127-1134, 1964.
71. Riggs AF. The Bohr effect. Annu Rev Physiol 50: 181-204, 1988.
72. Riggs AF. Self-association, cooperativity and supercooperativity of oxygen binding by hemoglobins. J Exp Biol 201: 1073-1084, 1998.
73. Riggs A, Rona M. The oxygen equilibria and aggregation behavior of polymerizing mouse hemoglobins. Biochim Biophys Acta 175: 248-259, 1969.
74. Rollema HS, De Bruin SH, Janssen LH, Van Os GA. The effect of potassium chloride on the Bohr effect of human hemoglobin. J Biol Chem 250: 1333-1339, 1975.
75. Roos J, Aggarwal RK, Janke A. Extended mitogenomic phylogenetic analyses yield new insight into crocodylian evolution and their survival of the Cretaceous-Tertiary boundary. Mol Phylogenet Evol 45: 663-673, 2007.
76. Schäfer W, Braunitzer G, Stangl A. Direct allosteric interaction of oxygen and bicarbonate: N-acetyl-alanyl-seryl-phenylalanine, N-terminal sequence of the b-chains of the haemoglobins of Nile crocodile (Crocodylus niloticus) and Mississippi crocodile (Alligator mississippiensis). Z Naturforsch 36: 902-903, 1981.
77. Schneider RG, Bremner JE, Brimhall B, Jones RT, Shih TB. Hemoglobin Cowtown (beta 146 HC3 His-Leu): a mutant with high oxygen affinity and erythrocytosis. Am J Clin Pathol 72: 1028-1032, 1979.
78. Seymour RS, Bennett AF, Bradford DF. Blood gas tensions and acidbase balance in the salt-water crocodile, Crocodylus porosus, at rest and after exhaustive exercise. J Exp Biol 118: 143-159, 1985.
79. Shih T, Jones RT, Bonaventura J, Bonaventura C, Schneider RG. Involvement of His HC3 (146) beta in the Bohr effect of human hemoglobin. Studies of native and N-ethylmaleimide-treated hemoglobin A and hemoglobin Cowtown (beta 146 His replaced by Leu). J Biol Chem 259: 967-974, 1984.
80. Stacy NI, Alleman AR, Sayler KA. Diagnostic hematology of reptiles. Clin Lab Med 31: 87-108, 2011.
81. Sullivan B. Reptilian hemoglobins. In: Chemical Zoology, Vol. IX. Amphibia and Reptilia, edited by Florkin M and Scheer BT. New York: Academic Press, 1974, p. 377-398.
82. Sullivan B, Riggs A. Hæmoglobin: reversal of oxidation and polymerization in turtle red cells. Nature 204: 1098-1099, 1964.
83. Sullivan B, Riggs A. Structure, function and evolution of turtle hemoglobins. I. Distribution of heavy hemoglobins. Comp Biochem Physiol 23: 437-447, 1967.
84. Tam LT, Riggs AF. Oxygen binding and aggregation of bullfrog hemoglobin. J Biol Chem 259: 2610-2616, 1984.
85. Tamburrini M, Riccio A, Romano M, Giardina B, Di Prisco G. Structural and functional analysis of the two haemoglobins of the Antarctic seabird Catharacta maccormicki characterization of an additional phosphate binding site by molecular modelling. Eur J Biochem 267: 6089-6098, 2000.
86. Torsoni MA, Souza-Torsoni A, Ogo SH, Souza Torsoni A. Involvement of available SH groups in the heterogeneity of hemoglobin from the tortoise Geochelone carbonaria. Biochem Mol Biol Int 44: 851-860, 1998.
87. Villar JL, Puigbo P, Riera-Codina M. Analysis of highly phosphorylated inositols in avian and crocodilian erythrocytes. Comp Biochem Physiol B Biochem Mol Biol 135: 169-175, 2003.
88. Wajcman H, Kilmartin JV, Najman A, Labie D. Hemoglobin Cochin-Port-Royal: consequences of the replacement of the β-chain C-terminal by an arginine. Biochim Biophys Acta 400: 354-364, 1975.
89. 2 affinity in lugworm erythrocruorin. Nature 292: 386-387, 1981.
90. Weber RE. Use of ionic and zwitterionic (Tris/BisTris and HEPES) buffers in studies on hemoglobin function. J Appl Physiol 72: 1611-1615, 1992.
91. Weber RE, Campbell KL. Temperature dependence of haemoglobinoxygen affinity in heterothermic vertebrates: mechanisms and biological significance. Acta Physiol (Oxf) 202: 549-562, 2011.
92. Weber RE, Fago A. Functional adaptation and its molecular basis in vertebrate hemoglobins, neuroglobins and cytoglobins. Respir Physiol Neurobiol 144: 141-159, 2004.
93. Weber RE, Fago A, Val AL, Bang A, Van Hauwaert ML, Dewilde S, Zal F, Moens L. Isohemoglobin differentiation in the bimodal-breathing Amazon catfish Hoplosternum littorale. J Biol Chem 275: 17297-17305, 2000.
94. Weber RE, Jensen FB, Cox RP. Analysis of teleost hemoglobin by Adair and Monod-Wyman-Changeux models. Effects of nucleoside triphosphates and pH on oxygenation of tench hemoglobin. J Comp Physiol B 157: 145-152, 1987.
95. Weber RE, Malte H, Braswell EH, Oliver RW, Green BN, Sharma PK, Kuchumov A, Vinogradov SN. Mass spectrometric composition, molecular mass and oxygen binding of Macrobdella decora hemoglobin and its tetramer and monomer subunits. J Mol Biol 251: 703-720, 1995.
96. Weber RE, White FN. Oxygen binding in alligator blood related to temperature, diving and "alkaline tide". Am J Physiol 20: R901-R908, 1986.
97. Weber RE, White FN. Chloride-dependent organic phosphate sensitivity of the oxygenation reaction in crocodilian hemoglobins. J Exp Biol 192: 1-11, 1994.
98. 2 affinity in heterothermic billfish. J Exp Biol 213: 1579-1585, 2010.
99. Zhang N, Palmer AF. Polymerization of human hemoglobin using the crosslinker 1,11-bis(maleimido)triethylene glycol for use as an oxygen carrier. Biotechnol Prog 26: 1481-1485, 2010.
100. Zuiderweg ER, Hamers LF, Rollema HS, De Bruin SH, Hilbers CW. 31P NMR study of the kinetics of binding of myo-inositol hexakisphosphate to human hemoglobin. Observation of fast-exchange kinetics in high-affinity systems. Eur J Biochem 118: 95-104, 1981.