Oxygenation state of hemoglobin defines dynamics of water molecules in its vicinity

Abstract

This study focuses on assessing the possible impact of changes in hemoglobin (Hb) oxygenation on the state of water in its hydration shell as it contributes to red blood cell deformability. Microwave Dielectric Spectroscopy (MDS) was used to monitor the changes in interactions between water molecules and Hb, the number of water molecules in the protein hydration shell, and the dynamics of pre-protein water in response to the transition of Hb from the tense (T) to the relaxed (R) state, and vice versa. Measurements were performed for Hb solutions of different concentrations (5 g/dl-30 g/dl) in phosphatebuffered saline buffer. Cole-Cole parameters of the main water relaxation peak in terms of interactions of water molecules (dipole-dipole/ionic dipole) during the oxygenation-deoxygenation cycle were used to analyze the obtained data. The water mobility-represented by as a function of ln -differed dramatically between the R (oxygenated) state and the T (deoxygenated) state of Hb at physiologically relevant concentrations (30 g/dl-35 g/dl or 4.5 mM-5.5 mM). At these concentrations, oxygenated hemoglobin was characterized by substantially lower mobility of water in the hydration shell, measured as an increase in relaxation time, compared to deoxyhemoglobin. This change indicated an increase in red blood cell cytosolic viscosity when cells were oxygenated and a decrease in viscosity upon deoxygenation. Information provided by MDS on the intraerythrocytic water state of intact red blood cells reflects its interaction with all of the cytosolic components, making these measurements powerful predictors of the changes in the rheological properties of red blood cells, regardless of the cause.

Electromagnetic tomographic cerebral angiography

“…The availability of scientific reports on dielectric properties of oxyHb and deoxyHb is limited at present. We based our estimations on the publication from Latypova with colleagues 31 . They reported the dielectric properties of different concentrations of oxyHb and deoxyHb in Phosphate Buffered Saline (PBS) , (pH = 7.4 at 25C).…”

Biophysical Reviews’ “Meet the Councilor”—a profile of Anastasia A. Anashkina

“…In studies on hemoglobin, we calculated that hemoglobin molecules are very densely packed in the erythrocyte at physiological concentration; a very thin layer of solvent remains between the hemoglobin molecules (Latypova et al 2020(Latypova et al , 2021. With such a dense arrangement of hemoglobin molecules in the erythrocyte, the formation of a small hydrophobic patch on the surface of hemoglobin will lead to "sticking" of hemoglobin A into hemoglobin S and the appearance of sickle cell disease.…”

Erythrocyte metabolism

“…Haemoglobin, recognized as a prototype of allostery, holds a prominent position in biochemistry and physiology textbooks 18,19 . The erythrocyte has been used as a cell model due to the following characteristics: (i) absence of a nucleus, mitochondria, and other organelles; (ii) shear abundance, ease of collection, and storage; (iii) relatively simple structure and shape; (iv) approximately 97% of its dry mass is comprised of haemoglobin 20 ; and (v) exclusive reliance on glucose and fructose for ATP production. These features may have contributed to the misconception that erythrocytes are simple cells, functioning solely as a passive oxygen carrier.…”