Hemoglobin diffusion and the dynamics of oxygen capture by red blood cells

Longeville, Stéphane; Stingaciu, Laura-Roxana

doi:10.1038/s41598-017-09146-9

Title: Hemoglobin diffusion and the dynamics of oxygen capture by red blood cells

Abstract

Translational diffusion of macromolecules in cell is generally assumed to be anomalous due high macromolecular crowding of the milieu. Red blood cells are a special case of cells filled quasi exclusively (95% of the dry weight of the cell) with an almost spherical protein: hemoglobin. Hemoglobin diffusion has since a long time been recognized as facilitating the rate of oxygen diffusion through a solution. We address in this paper the question on how hemoglobin diffusion in the red blood cells can help the oxygen capture at the cell level and hence to improve oxygen transport. We report a measurement by neutron spin echo spectroscopy of the diffusion of hemoglobin in solutions with increasing protein concentration. We show that hemoglobin diffusion in solution can be described as Brownian motion up to physiological concentration and that hemoglobin diffusion in the red blood cells and in solutions at similar concentration are the same. Finally, using a simple model and the concentration dependence of the diffusion of the protein reported here, we show that hemoglobin concentration observed in human red blood cells (≃330 g.L^-1) corresponds to an optimum for oxygen transport for individuals under strong activity.

Authors:

Longeville, Stéphane ^[1];

^[2]

Univ. Paris-Saclay, Gif-sur-Yvette (France). Laboratoire Leon Brillouin, CEA, CNRS
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Juelich Centre for Neutron Science, outstation at SNS

Publication Date:: Tue Sep 05 00:00:00 EDT 2017

Research Org.:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1426557

Grant/Contract Number:: AC05-00OR22725

Resource Type:: Accepted Manuscript

Journal Name:: Scientific Reports

Additional Journal Information:: Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2045-2322

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Biopolymers in vivo; Kinetics

Citation Formats


                    Longeville, Stéphane, and Stingaciu, Laura-Roxana. Hemoglobin diffusion and the dynamics of oxygen capture by red blood cells.  United States: N. p., 2017. 
Web.  doi:10.1038/s41598-017-09146-9.

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                    Longeville, Stéphane, & Stingaciu, Laura-Roxana. Hemoglobin diffusion and the dynamics of oxygen capture by red blood cells.  United States.  https://doi.org/10.1038/s41598-017-09146-9

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                    Longeville, Stéphane, and Stingaciu, Laura-Roxana. Tue .  
"Hemoglobin diffusion and the dynamics of oxygen capture by red blood cells".  United States.  https://doi.org/10.1038/s41598-017-09146-9.  https://www.osti.gov/servlets/purl/1426557.

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@article{osti_1426557,

  title        = {Hemoglobin diffusion and the dynamics of oxygen capture by red blood cells},

  author       = {Longeville, Stéphane and Stingaciu, Laura-Roxana},

  abstractNote = {Translational diffusion of macromolecules in cell is generally assumed to be anomalous due high macromolecular crowding of the milieu. Red blood cells are a special case of cells filled quasi exclusively (95% of the dry weight of the cell) with an almost spherical protein: hemoglobin. Hemoglobin diffusion has since a long time been recognized as facilitating the rate of oxygen diffusion through a solution. We address in this paper the question on how hemoglobin diffusion in the red blood cells can help the oxygen capture at the cell level and hence to improve oxygen transport. We report a measurement by neutron spin echo spectroscopy of the diffusion of hemoglobin in solutions with increasing protein concentration. We show that hemoglobin diffusion in solution can be described as Brownian motion up to physiological concentration and that hemoglobin diffusion in the red blood cells and in solutions at similar concentration are the same. Finally, using a simple model and the concentration dependence of the diffusion of the protein reported here, we show that hemoglobin concentration observed in human red blood cells (≃330 g.L-1) corresponds to an optimum for oxygen transport for individuals under strong activity.},

  doi          = {10.1038/s41598-017-09146-9},

  journal      = {Scientific Reports},

  number       = 1,

  volume       = 7,

  place        = {United States},

  year         = {Tue Sep 05 00:00:00 EDT 2017},

  month        = {Tue Sep 05 00:00:00 EDT 2017}

}

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Works referencing / citing this record:

High-resolution neutron spectroscopy using backscattering and neutron spin-echo spectrometers in soft and hard condensed matter
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Extracellular Heme Proteins Influence Bovine Myosatellite Cell Proliferation and the Color of Cell-Based Meat
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Simsa, Robin; Yuen, John; Stout, Andrew
Foods, Vol. 8, Issue 10
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Title: Hemoglobin diffusion and the dynamics of oxygen capture by red blood cells

Abstract

Citation Formats

Identifying anomalous diffusion and melting in dusty plasmas journal, September 2010

The intrinsic viscosity of biological macromolecules. Progress in measurement, interpretation and application to structure in dilute solution journal, September 1997

A new approach to the dynamics of oxygen capture by the human lung journal, January 2015

Microscopic protein diffusion at high concentration by neutron spin-echo spectroscopy journal, April 2008

Diffusion of Dissolved Gases in Liquids journal, October 1964

Diffusion coefficients of oxygen and hemoglobin as obtained simultaneously from photometric determination of the oxygenation of layers of hemoglobin solutions journal, April 1980

Experimental evidence that mutual and tracer diffusion coefficients for hemoglobin are not equal journal, April 1980

Dynamical Heterogeneity Close to the Jamming Transition in a Sheared Granular Material journal, December 2005

Facilitated Diffusion of Oxygen through Hæmerythrin Solutions journal, August 1963

Coupling and Decoupling of Rotational and Translational Diffusion of Proteins under Crowding Conditions journal, August 2016

Neutron spin echo: A new concept in polarized thermal neutron techniques journal, April 1972

The diffusion coefficient of human hemoglobin at high concentrations journal, May 1967

The viscosity of a concentrated suspension of spherical particles journal, April 1951

Oxygen Transport through Hemoglobin Solutions journal, February 1960

Rotational and Translational Self-Diffusion in Colloidal Sphere Suspensions and the Applicability of Generalized Stokes−Einstein Relations journal, June 2000

Crowding and hydrodynamic interactions likely dominate in vivo macromolecular motion journal, October 2010

Tracer and mutual diffusion coefficients of proteins journal, February 1971

The spin-echo spectrometer at the Spallation Neutron Source (SNS) journal, December 2012

The application of neutron spin echo on pulsed neutron sources journal, August 1979

Diffusion coefficients of oxygen and hemoglobin measured by facilitated oxygen diffusion through hemoglobin solutions journal, March 1997

A study of the dynamic properties of the human red blood cell membrane using quasi-elastic light-scattering spectroscopy journal, December 1993

Photon correlation spectroscopy of hemoglobin: Diffusion of Oxy-HbA and Oxy-HbS journal, June 1978

The diffusion coefficient of haemoglobin journal, January 1966

Microscopic Diffusion and Hydrodynamic Interactions of Hemoglobin in Red Blood Cells journal, August 2007

Tracer diffusion coefficients of oxyhemoglobin a and oxyhemoglobin s in blood cells as determined by pulsed field gradient NMR journal, November 1982

Concentration Dependence of the Self-Diffusion of Human and Lumbricus terrestris Hemoglobin journal, June 1978

Pulsed field gradient nmr determination of the temperature dependence of the tracer diffusion coefficient of hemoglobin journal, October 1982

Hard quasispherical model for the viscosity of hemoglobin solutions journal, June 1977

Dynamics and scaling in hard-sphere colloidal suspensions journal, January 1997

Excluded volume as a determinant of macromolecular structure and reactivity journal, October 1981

Probing short-range protein Brownian motion in the cytoplasm of living cells journal, December 2014

Anomalous transport in the crowded world of biological cells journal, March 2013

Die Carrier-Funktion des H�moglobins beim Sauerstoff-Transport im Erythrocyten journal, January 1962

Quasielastic Neutron Scattering in Biology, Part II: Applications book, January 2006

High-resolution neutron spectroscopy using backscattering and neutron spin-echo spectrometers in soft and hard condensed matter journal, January 2020

The Spectrum of α-Thalassemia Mutations in the Lak Population of Iran journal, March 2019

Extracellular Heme Proteins Influence Bovine Myosatellite Cell Proliferation and the Color of Cell-Based Meat journal, October 2019

Identifying anomalous diffusion and melting in dusty plasmas
journal, September 2010

The intrinsic viscosity of biological macromolecules. Progress in measurement, interpretation and application to structure in dilute solution
journal, September 1997

A new approach to the dynamics of oxygen capture by the human lung
journal, January 2015

Microscopic protein diffusion at high concentration by neutron spin-echo spectroscopy
journal, April 2008

Diffusion of Dissolved Gases in Liquids
journal, October 1964

Diffusion coefficients of oxygen and hemoglobin as obtained simultaneously from photometric determination of the oxygenation of layers of hemoglobin solutions
journal, April 1980

Experimental evidence that mutual and tracer diffusion coefficients for hemoglobin are not equal
journal, April 1980

Dynamical Heterogeneity Close to the Jamming Transition in a Sheared Granular Material
journal, December 2005

Facilitated Diffusion of Oxygen through Hæmerythrin Solutions
journal, August 1963

Coupling and Decoupling of Rotational and Translational Diffusion of Proteins under Crowding Conditions
journal, August 2016

Neutron spin echo: A new concept in polarized thermal neutron techniques
journal, April 1972

The diffusion coefficient of human hemoglobin at high concentrations
journal, May 1967

The viscosity of a concentrated suspension of spherical particles
journal, April 1951

Oxygen Transport through Hemoglobin Solutions
journal, February 1960

Rotational and Translational Self-Diffusion in Colloidal Sphere Suspensions and the Applicability of Generalized Stokes−Einstein Relations
journal, June 2000

Crowding and hydrodynamic interactions likely dominate in vivo macromolecular motion
journal, October 2010

Tracer and mutual diffusion coefficients of proteins
journal, February 1971

The spin-echo spectrometer at the Spallation Neutron Source (SNS)
journal, December 2012

The application of neutron spin echo on pulsed neutron sources
journal, August 1979

Diffusion coefficients of oxygen and hemoglobin measured by facilitated oxygen diffusion through hemoglobin solutions
journal, March 1997

A study of the dynamic properties of the human red blood cell membrane using quasi-elastic light-scattering spectroscopy
journal, December 1993

Photon correlation spectroscopy of hemoglobin: Diffusion of Oxy-HbA and Oxy-HbS
journal, June 1978

The diffusion coefficient of haemoglobin
journal, January 1966

Microscopic Diffusion and Hydrodynamic Interactions of Hemoglobin in Red Blood Cells
journal, August 2007

Tracer diffusion coefficients of oxyhemoglobin a and oxyhemoglobin s in blood cells as determined by pulsed field gradient NMR
journal, November 1982

Concentration Dependence of the Self-Diffusion of Human and Lumbricus terrestris Hemoglobin
journal, June 1978

Pulsed field gradient nmr determination of the temperature dependence of the tracer diffusion coefficient of hemoglobin
journal, October 1982

Hard quasispherical model for the viscosity of hemoglobin solutions
journal, June 1977

Dynamics and scaling in hard-sphere colloidal suspensions
journal, January 1997

Excluded volume as a determinant of macromolecular structure and reactivity
journal, October 1981

Probing short-range protein Brownian motion in the cytoplasm of living cells
journal, December 2014

Anomalous transport in the crowded world of biological cells
journal, March 2013

Die Carrier-Funktion des H�moglobins beim Sauerstoff-Transport im Erythrocyten
journal, January 1962

Quasielastic Neutron Scattering in Biology, Part II: Applications
book, January 2006

High-resolution neutron spectroscopy using backscattering and neutron spin-echo spectrometers in soft and hard condensed matter
journal, January 2020

The Spectrum of α-Thalassemia Mutations in the Lak Population of Iran
journal, March 2019

Extracellular Heme Proteins Influence Bovine Myosatellite Cell Proliferation and the Color of Cell-Based Meat
journal, October 2019