A comparison of functional and structural consequences of the tyrosine B10 and glutamine E7 motifs in two invertebrate hemoglobins (Ascaris suum and Lucina pectinata)

Eric S. Peterson, Shuocai Huang, Jiaqian Wang, Lisa M. Miller, Gediminas Vidugiris, Andrew P. Kloek, Daniel E. Goldberg, Mark R. Chance, Jonathan B. Wittenberg, Joel M. Friedman

Research output: Contribution to journalArticle

58 Citations (Scopus)

Abstract

The architecture of the distal heine pocket in hemoglobins and myoglobins can play an important role in controlling ligand binding dynamics. The size and polarity of the residues occupying the distal pocket may contribute steric and dielectric effects. In vertebrate systems, the distal pocket typically contains a 'distal' histidine at position E7 and a leucine at position B10. Then are several invertebrate organisms that have hemoglobins or myoglobins that display a pattern in which residues E7 and B10 are a glutamine and tyrosine, respectively. These proteins often have very high oxygen affinities stemming from very slow ligand off rates. In this study, two such hemoglobins, one from the nematode Ascaris suum and the other from the sulfide-fixing clam Lucina pectinata, are compared with respect to conformational and functional properties. Ultraviolet resonance Raman spectroscopy and visible resonance Raman spectroscopy are used to probe, respectively, the ligand-dependent hydrogen bonding pattern of the tyrosine residues and the proximal heine pocket interactions. Fourier transform infrared absorption spectroscopy is used to probe the dielectric properties of the distal heine pocket through the stretching frequency of carbon monoxide bound to the heme. Functionality is probed through the geminate rebinding of both CO and O2. The findings reveal two very different patterns indicative of two different mechanisms for achieving low oxygen off rates. In Hb Ascaris, a hydrogen bonding network that includes the E7 Gln. B10 Tyr, and oxygen bound to the heine results in a tight cage for the oxygen. Dissociation of the O2 requires a large amplitude conformational fluctuation that results both in a spontaneous dissociation of the oxygen through the loss of hydrogen bond stabilization and in an enhanced probability for ligand escape though the transient disruption and opening of the tight distal cage. In the case of the Hb from Lucina, there is no evidence for a tight cage. Instead the data support a model in which the hydrogen bonding network is far more tenuous and the equilibrium state of distal pocket is far more open and accessible than is the case in Ascaris. The results explain why Hb Ascaris has one of the highest oxygen affinities known (P50 ~ 10-3 Torr) while Hb Lucina II has an oxygen affinity comparable to that of Mb (P50 = 0.13 Torr) even though both of these Hbs contain the B10 Tyr and E7 Gln motif and display very low oxygen off rates. The roles of water and proximal strain are discussed.

Original languageEnglish (US)
Pages (from-to)13110-13121
Number of pages12
JournalBiochemistry
Volume36
Issue number42
DOIs
StatePublished - Oct 21 1997

Fingerprint

Ascaris suum
Invertebrates
Glutamine
Tyrosine
Hemoglobins
Oxygen
Ascaris
Hydrogen bonds
Hydrogen Bonding
Ligands
Raman Spectrum Analysis
Myoglobin
Carbon Monoxide
Raman spectroscopy
Ascaris haemoglobin
Bivalvia
Infrared absorption
Sulfides
Fourier Transform Infrared Spectroscopy
Heme

ASJC Scopus subject areas

  • Biochemistry

Cite this

A comparison of functional and structural consequences of the tyrosine B10 and glutamine E7 motifs in two invertebrate hemoglobins (Ascaris suum and Lucina pectinata). / Peterson, Eric S.; Huang, Shuocai; Wang, Jiaqian; Miller, Lisa M.; Vidugiris, Gediminas; Kloek, Andrew P.; Goldberg, Daniel E.; Chance, Mark R.; Wittenberg, Jonathan B.; Friedman, Joel M.

In: Biochemistry, Vol. 36, No. 42, 21.10.1997, p. 13110-13121.

Research output: Contribution to journalArticle

Peterson, ES, Huang, S, Wang, J, Miller, LM, Vidugiris, G, Kloek, AP, Goldberg, DE, Chance, MR, Wittenberg, JB & Friedman, JM 1997, 'A comparison of functional and structural consequences of the tyrosine B10 and glutamine E7 motifs in two invertebrate hemoglobins (Ascaris suum and Lucina pectinata)', Biochemistry, vol. 36, no. 42, pp. 13110-13121. https://doi.org/10.1021/bi971156n
Peterson, Eric S. ; Huang, Shuocai ; Wang, Jiaqian ; Miller, Lisa M. ; Vidugiris, Gediminas ; Kloek, Andrew P. ; Goldberg, Daniel E. ; Chance, Mark R. ; Wittenberg, Jonathan B. ; Friedman, Joel M. / A comparison of functional and structural consequences of the tyrosine B10 and glutamine E7 motifs in two invertebrate hemoglobins (Ascaris suum and Lucina pectinata). In: Biochemistry. 1997 ; Vol. 36, No. 42. pp. 13110-13121.
@article{dd453ff3915d4ed3858d0cdf92ab57e6,
title = "A comparison of functional and structural consequences of the tyrosine B10 and glutamine E7 motifs in two invertebrate hemoglobins (Ascaris suum and Lucina pectinata)",
abstract = "The architecture of the distal heine pocket in hemoglobins and myoglobins can play an important role in controlling ligand binding dynamics. The size and polarity of the residues occupying the distal pocket may contribute steric and dielectric effects. In vertebrate systems, the distal pocket typically contains a 'distal' histidine at position E7 and a leucine at position B10. Then are several invertebrate organisms that have hemoglobins or myoglobins that display a pattern in which residues E7 and B10 are a glutamine and tyrosine, respectively. These proteins often have very high oxygen affinities stemming from very slow ligand off rates. In this study, two such hemoglobins, one from the nematode Ascaris suum and the other from the sulfide-fixing clam Lucina pectinata, are compared with respect to conformational and functional properties. Ultraviolet resonance Raman spectroscopy and visible resonance Raman spectroscopy are used to probe, respectively, the ligand-dependent hydrogen bonding pattern of the tyrosine residues and the proximal heine pocket interactions. Fourier transform infrared absorption spectroscopy is used to probe the dielectric properties of the distal heine pocket through the stretching frequency of carbon monoxide bound to the heme. Functionality is probed through the geminate rebinding of both CO and O2. The findings reveal two very different patterns indicative of two different mechanisms for achieving low oxygen off rates. In Hb Ascaris, a hydrogen bonding network that includes the E7 Gln. B10 Tyr, and oxygen bound to the heine results in a tight cage for the oxygen. Dissociation of the O2 requires a large amplitude conformational fluctuation that results both in a spontaneous dissociation of the oxygen through the loss of hydrogen bond stabilization and in an enhanced probability for ligand escape though the transient disruption and opening of the tight distal cage. In the case of the Hb from Lucina, there is no evidence for a tight cage. Instead the data support a model in which the hydrogen bonding network is far more tenuous and the equilibrium state of distal pocket is far more open and accessible than is the case in Ascaris. The results explain why Hb Ascaris has one of the highest oxygen affinities known (P50 ~ 10-3 Torr) while Hb Lucina II has an oxygen affinity comparable to that of Mb (P50 = 0.13 Torr) even though both of these Hbs contain the B10 Tyr and E7 Gln motif and display very low oxygen off rates. The roles of water and proximal strain are discussed.",
author = "Peterson, {Eric S.} and Shuocai Huang and Jiaqian Wang and Miller, {Lisa M.} and Gediminas Vidugiris and Kloek, {Andrew P.} and Goldberg, {Daniel E.} and Chance, {Mark R.} and Wittenberg, {Jonathan B.} and Friedman, {Joel M.}",
year = "1997",
month = "10",
day = "21",
doi = "10.1021/bi971156n",
language = "English (US)",
volume = "36",
pages = "13110--13121",
journal = "Biochemistry",
issn = "0006-2960",
publisher = "American Chemical Society",
number = "42",

}

TY - JOUR

T1 - A comparison of functional and structural consequences of the tyrosine B10 and glutamine E7 motifs in two invertebrate hemoglobins (Ascaris suum and Lucina pectinata)

AU - Peterson, Eric S.

AU - Huang, Shuocai

AU - Wang, Jiaqian

AU - Miller, Lisa M.

AU - Vidugiris, Gediminas

AU - Kloek, Andrew P.

AU - Goldberg, Daniel E.

AU - Chance, Mark R.

AU - Wittenberg, Jonathan B.

AU - Friedman, Joel M.

PY - 1997/10/21

Y1 - 1997/10/21

N2 - The architecture of the distal heine pocket in hemoglobins and myoglobins can play an important role in controlling ligand binding dynamics. The size and polarity of the residues occupying the distal pocket may contribute steric and dielectric effects. In vertebrate systems, the distal pocket typically contains a 'distal' histidine at position E7 and a leucine at position B10. Then are several invertebrate organisms that have hemoglobins or myoglobins that display a pattern in which residues E7 and B10 are a glutamine and tyrosine, respectively. These proteins often have very high oxygen affinities stemming from very slow ligand off rates. In this study, two such hemoglobins, one from the nematode Ascaris suum and the other from the sulfide-fixing clam Lucina pectinata, are compared with respect to conformational and functional properties. Ultraviolet resonance Raman spectroscopy and visible resonance Raman spectroscopy are used to probe, respectively, the ligand-dependent hydrogen bonding pattern of the tyrosine residues and the proximal heine pocket interactions. Fourier transform infrared absorption spectroscopy is used to probe the dielectric properties of the distal heine pocket through the stretching frequency of carbon monoxide bound to the heme. Functionality is probed through the geminate rebinding of both CO and O2. The findings reveal two very different patterns indicative of two different mechanisms for achieving low oxygen off rates. In Hb Ascaris, a hydrogen bonding network that includes the E7 Gln. B10 Tyr, and oxygen bound to the heine results in a tight cage for the oxygen. Dissociation of the O2 requires a large amplitude conformational fluctuation that results both in a spontaneous dissociation of the oxygen through the loss of hydrogen bond stabilization and in an enhanced probability for ligand escape though the transient disruption and opening of the tight distal cage. In the case of the Hb from Lucina, there is no evidence for a tight cage. Instead the data support a model in which the hydrogen bonding network is far more tenuous and the equilibrium state of distal pocket is far more open and accessible than is the case in Ascaris. The results explain why Hb Ascaris has one of the highest oxygen affinities known (P50 ~ 10-3 Torr) while Hb Lucina II has an oxygen affinity comparable to that of Mb (P50 = 0.13 Torr) even though both of these Hbs contain the B10 Tyr and E7 Gln motif and display very low oxygen off rates. The roles of water and proximal strain are discussed.

AB - The architecture of the distal heine pocket in hemoglobins and myoglobins can play an important role in controlling ligand binding dynamics. The size and polarity of the residues occupying the distal pocket may contribute steric and dielectric effects. In vertebrate systems, the distal pocket typically contains a 'distal' histidine at position E7 and a leucine at position B10. Then are several invertebrate organisms that have hemoglobins or myoglobins that display a pattern in which residues E7 and B10 are a glutamine and tyrosine, respectively. These proteins often have very high oxygen affinities stemming from very slow ligand off rates. In this study, two such hemoglobins, one from the nematode Ascaris suum and the other from the sulfide-fixing clam Lucina pectinata, are compared with respect to conformational and functional properties. Ultraviolet resonance Raman spectroscopy and visible resonance Raman spectroscopy are used to probe, respectively, the ligand-dependent hydrogen bonding pattern of the tyrosine residues and the proximal heine pocket interactions. Fourier transform infrared absorption spectroscopy is used to probe the dielectric properties of the distal heine pocket through the stretching frequency of carbon monoxide bound to the heme. Functionality is probed through the geminate rebinding of both CO and O2. The findings reveal two very different patterns indicative of two different mechanisms for achieving low oxygen off rates. In Hb Ascaris, a hydrogen bonding network that includes the E7 Gln. B10 Tyr, and oxygen bound to the heine results in a tight cage for the oxygen. Dissociation of the O2 requires a large amplitude conformational fluctuation that results both in a spontaneous dissociation of the oxygen through the loss of hydrogen bond stabilization and in an enhanced probability for ligand escape though the transient disruption and opening of the tight distal cage. In the case of the Hb from Lucina, there is no evidence for a tight cage. Instead the data support a model in which the hydrogen bonding network is far more tenuous and the equilibrium state of distal pocket is far more open and accessible than is the case in Ascaris. The results explain why Hb Ascaris has one of the highest oxygen affinities known (P50 ~ 10-3 Torr) while Hb Lucina II has an oxygen affinity comparable to that of Mb (P50 = 0.13 Torr) even though both of these Hbs contain the B10 Tyr and E7 Gln motif and display very low oxygen off rates. The roles of water and proximal strain are discussed.

UR - http://www.scopus.com/inward/record.url?scp=0030681291&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0030681291&partnerID=8YFLogxK

U2 - 10.1021/bi971156n

DO - 10.1021/bi971156n

M3 - Article

C2 - 9335574

AN - SCOPUS:0030681291

VL - 36

SP - 13110

EP - 13121

JO - Biochemistry

JF - Biochemistry

SN - 0006-2960

IS - 42

ER -