Molecular Insights of an Avian Species with Low Oxygen Affinity, the Crystal Structure of Duck T-State Methemoglobin.
Allosteric mechanism
Avian hemoglobin
Crystal structure
Liganded T-state hemoglobin
Low oxygen affinity
Journal
The protein journal
ISSN: 1875-8355
Titre abrégé: Protein J
Pays: Netherlands
ID NLM: 101212092
Informations de publication
Date de publication:
20 May 2024
20 May 2024
Historique:
accepted:
09
05
2024
medline:
20
5
2024
pubmed:
20
5
2024
entrez:
20
5
2024
Statut:
aheadofprint
Résumé
Hemoglobin (Hb) is the key metalloprotein within red blood cells involved in oxygen transportation from lungs to body cells. The heme-iron atom inherent within Hb effectuates the mechanism of oxygen transportation and carbon dioxide removal. Structural investigations on avian Hb are limited when compared with the enormous work has been carried out on mammalian Hb. Here, the crystal structure of T-state methemoglobin (T-metHb) from domestic duck (Anas platyrhynchos), a low oxygen affinity avian species, determined to 2.1Å resolution is presented. Duck T-metHb crystallized in the orthorhombic space group C222
Identifiants
pubmed: 38767790
doi: 10.1007/s10930-024-10206-z
pii: 10.1007/s10930-024-10206-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12:88–118. https://doi.org/10.1016/S0022-2836(65)80285-6
doi: 10.1016/S0022-2836(65)80285-6
pubmed: 14343300
Perutz MF (1970) Stereochemistry of cooperative effects in haemoglobin: haem–haem interaction and the problem of allostery. Nature 228:726–734
pubmed: 5528785
doi: 10.1038/228726a0
Perutz MF (1972) Nature of haem–haem interaction. Nature 237:495–499
pubmed: 12635193
doi: 10.1038/237495a0
Baldwin J, Chothia C (1979) Haemoglobin: the structural changes related to ligand binding and its allosteric mechanism. J Mol Biol 129:175–220
pubmed: 39173
doi: 10.1016/0022-2836(79)90277-8
Perutz MF (1989) Mechanisms of cooperativity and allosteric regulation in proteins. Q Rev Biophys 22:139–237
pubmed: 2675171
doi: 10.1017/S0033583500003826
Perutz MF, Fermi G, Luisi B et al (1987) Stereochemistry of cooperative mechanisms in hemoglobin. Acc Chem Res 20:309–321
doi: 10.1021/ar00141a001
Lenfant C, Kooyman GL, Elsner R, Drabek CM (1969) Respiratory function of blood of the Adélie penguin Pygoscelis adeliae. Am J Physiology-Legacy Content 216:1598–1600
doi: 10.1152/ajplegacy.1969.216.6.1598
Bartlett GR (1970) Patterns of phosphate compounds in red blood cells of man and animals. In: Red cell metabolism and function: Proceedings of the first international conference on red cell metabolism and function, held at the University of Michigan, Ann Arbor, October 1–3, 1969. Springer, pp 245–256
Rollema HS, Bauer C (1979) The interaction of inositol pentaphosphate with the hemoglobins of highland and lowland geese. J Biol Chem 254:12038–12043
pubmed: 40989
doi: 10.1016/S0021-9258(19)86424-4
Weber RE (1995) Hemoglobin adaptations to hypoxia and altitude-the phylogenetic perspective. Hypoxia Brain 31–44
Knapp JE, Oliveira MA, Xie Q et al (1999) The structural and functional analysis of the hemoglobin D component from chicken. J Biol Chem 274:6411–6420
pubmed: 10037733
doi: 10.1074/jbc.274.10.6411
Swan LW (1970) Goose of the Himalayas. Nat Hist 79:691
Liang Y-H, Liu X-Z, Liu S-H, Lu G-Y (2001) The structure of greylag goose oxy haemoglobin: the roles of four mutations compared with bar-headed goose haemoglobin. Acta Crystallogr D Biol Crystallogr 57:1850–1856
pubmed: 11717498
doi: 10.1107/S0907444901016493
Liang Y, Hua Z, Liang X et al (2001) The crystal structure of bar-headed goose hemoglobin in deoxy form: the allosteric mechanism of a hemoglobin species with high oxygen affinity. J Mol Biol 313:123–137
pubmed: 11601851
doi: 10.1006/jmbi.2001.5028
Liu X-Z, Li S-L, Jing H et al (2001) Avian haemoglobins and structural basis of high affinity for oxygen: structure of bar-headed goose aquomet haemoglobin. Acta Crystallogr D Biol Crystallogr 57:775–783
pubmed: 11375496
doi: 10.1107/S0907444901004243
Zhang J, Hua Z, Tame JRH et al (1996) The crystal structure of a high oxygen affinity species of haemoglobin (bar-headed goose haemoglobin in the oxy form). J Mol Biol 255:484–493
pubmed: 8568892
doi: 10.1006/jmbi.1996.0040
Black CP, Tenney SM (1980) Oxygen transport during progressive hypoxia in high-altitude and sea-level waterfowl. Respir Physiol 39:217–239
pubmed: 7375742
doi: 10.1016/0034-5687(80)90046-8
Perutz MF (1983) Species adaptation in a protein molecule. Mol Biol Evol 1:1–28
pubmed: 6400645
Shaanan B (1983) Structure of human oxyhaemoglobin at 2· 1resolution. J Mol Biol 171:31–59
pubmed: 6644819
doi: 10.1016/S0022-2836(83)80313-1
Holle JP, Meyer M, Scheid P (1977) Oxygen affinity of duck blood determined by in vivo and in vitro technique. Respir Physiol 29:355–361
pubmed: 18767
doi: 10.1016/0034-5687(77)90009-3
Petschow D, Wurdinger I, Baumann R et al (1977) Causes of high blood O2 affinity of animals living at high altitude. J Appl Physiol 42:139–143
pubmed: 14096
doi: 10.1152/jappl.1977.42.2.139
Neelagandan K, Moorthy PS, Balasubramanian M, Ponnuswamy MN (2007) Crystallization of sheep (Ovis aries) and goat (Capra hircus) haemoglobins under unbuffered low-salt conditions. Acta Crystallogr Sect F Struct Biol Cryst Commun 63:887–889
pubmed: 17909297
pmcid: 2339733
doi: 10.1107/S1744309107044296
Kamariah N, Ponnuraj SM, Moovarkumudalvan B, Ponnuswamy MNG (2014) Structural studies on a low oxygen affinity hemoglobin from mammalian species: Sheep (Ovis aries). Biochem Biophys Res Commun 450:36–41
pubmed: 24858681
doi: 10.1016/j.bbrc.2014.05.062
Moorthy PS, Neelagandan K, Balasubramanian M, Ponnuswamy MNG (2009) Purification, crystallization and preliminary X-Ray Diffraction studies on Goat (Capra hircus) Hemoglobin-A low Oxygen Affinity species. Protein Pept Lett 16:454–456
pubmed: 19356147
doi: 10.2174/092986609787847992
Sathya Moorthy P, Neelagandan K, Balasubramanian M, Ponnuswamy MN (2009) Purification, crystallization and preliminary X-ray diffraction studies on avian haemoglobin from pigeon (Columba livia). Acta Crystallogr Sect F Struct Biol Cryst Commun 65:120–122
pubmed: 19194000
pmcid: 2635874
doi: 10.1107/S1744309108038505
Balasubramanian M, Sathya Moorthy P, Neelagandan K, Ponnuswamy MN (2009) Purification, crystallization and preliminary crystallographic study of haemoglobin from camel (Camelus dromedarius): a high oxygen-affinity lowland species. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:773–775
pubmed: 19652336
pmcid: 2720330
doi: 10.1107/S1744309109024154
Balasubramanian M, Moorthy PS, Neelagandan K, Gounder Ponnuswamy MN (2009) Preliminary crystallographic study of Hemoglobin from Buffalo (Bubalus bubalis): a low Oxygen Affinity species. Protein Pept Lett 16:213–215
pubmed: 19200047
doi: 10.2174/092986609787316216
Balasubramanian M, Sathya Moorthy P, Neelagandan K et al (2014) Structure of liganded T-state haemoglobin from cat (Felis silvestris Catus), a low oxygen-affinity species, in two different crystal forms. Acta Crystallogr D Biol Crystallogr 70:1898–1906
pubmed: 25004966
doi: 10.1107/S139900471400916X
Balasubramanian M, Moorthy PS, Neelagandan K, Ponnuswamy MN (2009) Purification, crystallization and preliminary crystallographic study of low oxygen-affinity haemoglobin from cat (Felis silvestris Catus) in two different crystal forms. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:313–316
pubmed: 19255493
pmcid: 2650469
doi: 10.1107/S1744309109004503
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
pubmed: 5432063
doi: 10.1038/227680a0
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
pubmed: 942051
doi: 10.1016/0003-2697(76)90527-3
Bartels KS, Klein C (2003) The automar Manual, v. 1.4. MAR Research GmbH, Norderstedt, Germany
McCoy AJ, Grosse-Kunstleve RW, Adams PD et al (2007) Phaser crystallographic software. J Appl Crystallogr 40:658–674
pubmed: 19461840
pmcid: 2483472
doi: 10.1107/S0021889807021206
CCP C (1994) Collaborative computational project number 4. Acta Crystallogr D Biol Crystallogr 50:760–763
Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53:240–255
pubmed: 15299926
doi: 10.1107/S0907444996012255
Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126–2132
pubmed: 15572765
doi: 10.1107/S0907444904019158
Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291
doi: 10.1107/S0021889892009944
Matthews BW (1968) Solvent content of protein crystals. J Mol Biol 33:491–497
pubmed: 5700707
doi: 10.1016/0022-2836(68)90205-2
Dall’Acqua W, Simon AL, Mulkerrin MG, Carter P (1998) Contribution of domain interface residues to the stability of antibody CH3 domain homodimers. Biochemistry 37:9266–9273
pubmed: 9649307
doi: 10.1021/bi980270i
Fermi G, Perutz MF, Shaanan B, Fourme R (1984) The crystal structure of human deoxyhaemoglobin at 1.74 Å resolution. J Mol Biol 175:159–174
pubmed: 6726807
doi: 10.1016/0022-2836(84)90472-8
Borgese TA, Nagel RL (1977) Differential effects of 2, 3-DPG, ATP and inositol pentaphosphate (IP5) on the oxygen equilibria of duck embryonic, fetal and adult hemoglobins. Comp Biochem Physiol Physiol 56:539–543
doi: 10.1016/0300-9629(77)90282-1
Isaacks RE, Harkness DR (1980) Erythrocyte organic phosphates and hemoglobin function in birds, reptiles, and fishes. Am Zool 20:115–129
doi: 10.1093/icb/20.1.115
Arnone A (1972) X-ray diffraction study of binding of 2, 3-diphosphoglycerate to human deoxyhaemoglobin. Nature 237:146–149
pubmed: 4555506
doi: 10.1038/237146a0
Natarajan C, Jendroszek A, Kumar A et al (2018) Molecular basis of hemoglobin adaptation in the high-flying bar-headed goose. PLoS Genet 14:e1007331
pubmed: 29608560
pmcid: 5903655
doi: 10.1371/journal.pgen.1007331
Jaimohan SM, Naresh MD, Mandal AB (2021) Parakeet hemoglobin-its Crystal structure and Oxygen Affinity in Relation to some avian hemoglobins. Protein Pept Lett 28:18–30
pubmed: 32196438
doi: 10.2174/0929866527666200320100109
Ramesh P, Sundaresan SS, Shobana N et al (2021) Structural studies of hemoglobin from two flightless birds, ostrich and Turkey: insights into their differing oxygen-binding properties. Acta Crystallogr D Struct Biol 77:690–702
pubmed: 33950023
doi: 10.1107/S2059798321003417
Jessen T-H, Weber RE, Fermi G et al (1991) Adaptation of bird hemoglobins to high altitudes: demonstration of molecular mechanism by protein engineering. Proceedings of the National Academy of Sciences 88:6519–6522
Weber RE, Jessen T-H, Malte H, Tame J (1993) Mutant hemoglobins (alpha 119-Ala and beta 55-Ser): functions related to high-altitude respiration in geese. J Appl Physiol 75:2646–2655
pubmed: 8125885
doi: 10.1152/jappl.1993.75.6.2646
Ganapathy J, Palayam M, Pennathur G et al (2018) Crystal Structure Analysis of Great Cormorant (Phalacrocorax carbo) Hemoglobin to understand its high Oxygen Affinity characteristics by Special Structural features. Protein Pept Lett 25:748–756
pubmed: 29929459
doi: 10.2174/0929866525666180620163632
Liddington R, Derewenda Z, Dodson E et al (1992) High resolution crystal structures and comparisons of T-state deoxyhaemoglobin and two liganded T-state haemoglobins: T (α-oxy) haemoglobin and T (met) haemoglobin. J Mol Biol 228:551–579
pubmed: 1453464
doi: 10.1016/0022-2836(92)90842-8