The inhibition of glucose uptake to erythrocytes: microwave dielectric response.
Adenosine triphosphate (ATP)
Cytochalasin B (CCB)
Cytoplasmic water
Forskolin
Inhibitors
Microwave dielectric spectroscopy (MDS)
Red blood cells (RBC)
Water
Journal
European biophysics journal : EBJ
ISSN: 1432-1017
Titre abrégé: Eur Biophys J
Pays: Germany
ID NLM: 8409413
Informations de publication
Date de publication:
Jul 2022
Jul 2022
Historique:
received:
12
01
2022
accepted:
28
04
2022
revised:
24
04
2022
pubmed:
10
5
2022
medline:
29
6
2022
entrez:
9
5
2022
Statut:
ppublish
Résumé
Dielectric spectroscopy has been used in the study and development of non-invasive glucose monitoring (NIGM) sensors, including the range of microwave frequencies. Dielectric relaxation of red blood cell (RBC) cytosolic water in the microwave frequency band has been shown to be sensitive to variations in the glucose concentration of RBC suspensions. It has been hypothesized that this sensitivity stems from the utilization of D-glucose by RBCs. To verify this proposition, RBCs were pretreated with inhibitors of D-glucose uptake (cytochalasin B and forskolin). Then their suspensions were exposed to different D-glucose concentrations as measured by microwave dielectric spectroscopy (MDS) in the 500 MHz-40 GHz frequency band. After incubation of RBCs with either inhibitor, the dielectric response of water in the cytoplasm, and specifically its relaxation time, demonstrated minimal sensitivity to the change of D-glucose concentration in the medium. This result allows us to conclude that the sensitivity of MDS to glucose uptake is associated with variations in the balance of bulk and bound RBC cytosolic water due to intracellular D-glucose metabolism, verifying the correctness of the initial hypothesis. These findings represent a further argument to establish the dielectric response of water as a marker of glucose variation in RBCs.
Identifiants
pubmed: 35532810
doi: 10.1007/s00249-022-01602-3
pii: 10.1007/s00249-022-01602-3
doi:
Substances chimiques
Blood Glucose
0
Suspensions
0
Water
059QF0KO0R
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
353-363Informations de copyright
© 2022. European Biophysical Societies' Association.
Références
AB, m. Smartbuffers-phosphate buffered saline(PBS), pH 7.4 and 7.2. Available from: http://www.medicago.se/sites/default/files/pdf/productsheets/PBS_Buffer_v._01.pdf .
Asami K (2002) Characterization of biological cells by dielectric spectroscopy. J Non-Cryst Solids 305(1):268–277
doi: 10.1016/S0022-3093(02)01110-9
Asami K (2014) Low-frequency dielectric dispersion of bacterial cell suspensions. Colloids Surf B Biointerfaces 119:1–5
pubmed: 24835050
doi: 10.1016/j.colsurfb.2014.04.014
Asami K (2015) Radiofrequency dielectric properties of cell suspensions. Dielectric relaxation in biological systems: physical principles, methods, and applications. Oxford University Press, Oxford, pp 340–362
doi: 10.1093/acprof:oso/9780199686513.003.0013
Axelrod N et al (2004) Dielectric spectroscopy data treatment: I. Frequency domain. Meas Sci Technol 15(4):755–764
doi: 10.1088/0957-0233/15/4/020
Basketter DA, Widdas WF (1978) Asymmetry of the hexose transfer system in human erythrocytes. Comparison of the effects of cytochalasin B, phloretin and maltose as competitive inhibitors. J Physiol 278:389–401
pubmed: 671319
pmcid: 1282356
doi: 10.1113/jphysiol.1978.sp012311
Beving H et al (1994) Dielectric properties of human blood and erythrocytes at radio frequencies (0.2–10 MHz); dependence on cell volume fraction and medium composition. Eur Biophys J 23(3):207–215
pubmed: 7956980
doi: 10.1007/BF01007612
Burrin JM, Price CP (1985) Measurement of blood glucose. Ann Clin Biochem 22(4):327–342
pubmed: 3898972
doi: 10.1177/000456328502200401
Caduff A, Talary M (2015) Glucose detection from skin dielectric measurement. In: F Y, Raicu V (eds) Dielectric relaxation in biological systems. Oxford University Press, Oxford, pp 388–412
doi: 10.1093/acprof:oso/9780199686513.003.0015
Caduff A et al (2003) First human experiments with a novel non-invasive, non-optical continuous glucose monitoring system. Biosens Bioelectron 19(3):209–217
pubmed: 14611756
doi: 10.1016/S0956-5663(03)00196-9
Caduff A et al (2007) Non-invasive glucose monitoring in patients with diabetes: a novel system based on impedance spectroscopy. Biosens Bioelectron 22:598–604
doi: 10.1016/j.bios.2006.01.031
Caduff A et al (2015) The effect of a global, subject, and device-specific model on a noninvasive glucose monitoring multisensor system. J Diabetes Sci Technol 9(4):865–872
pubmed: 25910542
pmcid: 4525657
doi: 10.1177/1932296815579459
Cherkasova O, Nazarov M, Shkurinov A (2016) Noninvasive blood glucose monitoring in the terahertz frequency range. Opt Quant Electron 48(3):217
doi: 10.1007/s11082-016-0490-5
Cho NH et al (2018) IDF Diabetes Atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281
pubmed: 29496507
doi: 10.1016/j.diabres.2018.02.023
Choi H et al (2015) Design and in vitro interference test of microwave noninvasive blood glucose monitoring sensor. IEEE Trans Microw Theory Tech 63(10):3016–3025
pubmed: 26568639
pmcid: 4641327
doi: 10.1109/TMTT.2015.2472019
Cole KS, Cole RH (1941) Dispersion and absorption in dielectrics I. Alternating current characteristics. J ChemPhys 9(4):341–351
Cooper GM (2000) The cell: a molecular approach, 2nd edn. Sinauer Associates, Sunderland, MA
Deves R, Krupka R (1978) Cytochalasin B and the kinetics of inhibition of biological transport. A case of asymmetric binding to the glucose carrier. Biochim Biophys Acta (BBA)-Biomembr 510(2):339–348
doi: 10.1016/0005-2736(78)90034-2
Estimates of Diabetes and its Burden in the United States. National Statistics Reports. 2020; Available from: https://www.cdc.gov/diabetes/pdfs/data/statistics/national-diabetes-statistics-report.pdf .
Fayzullin D et al (2013) Hydration of AMP and ATP molecules in aqueous solution and solid films. Int J Mol Sci 14:22876–22890
doi: 10.3390/ijms141122876
Feldman Y, Ermolina I, Hayashi Y (2003) Time domain dielectric spectroscopy study of biological systems. IEEE Trans Dielect Electr Insul 10:728–753
doi: 10.1109/TDEI.2003.1237324
Feldman Y et al (2014) The dielectric response of interfacial water—from the ordered structures to the single hydrated shell. Colloid Polym Sci 292(8):1923–1932
doi: 10.1007/s00396-014-3296-7
Fuchs K, Kaatze U (2001) Molecular dynamics of carbohydrate aqueous solutions. Dielectric relaxation as a function of glucose and fructose concentration. J Phys Chem B-J Phys Chem B 105:2036
doi: 10.1021/jp0030084
Gabriel S, Lau RW, Gabriel C (1996) The dielectric properties of biological tissue II: measurements in the frequency range 10 Hz to 20 GHz. Phys Med Biol 41:2251–2269
pubmed: 8938025
doi: 10.1088/0031-9155/41/11/002
Grant EH, Sheppard RJ, South GP (1978) Dielectric behaviour of biological molecules in solution. Clarendon Press, Oxford
Guizouarn H, Allegrini B (2020) Erythroid glucose transport in health and disease. Pflugers Arch 472(9):1371–1383
pubmed: 32474749
doi: 10.1007/s00424-020-02406-0
Guyton AC (1991) Textbook of medical physiology. Saunders, Philadelphia
Hayashi Y, Shinyashiki N, Yagihara S (2002) Dynamical structure of water around biopolymers investigated by microwave dielectric measurements using time domain reflectometry method. J Non-Cryst Solids 305:328–332
doi: 10.1016/S0022-3093(02)01113-4
Hayashi Y et al (2003) Dielectric spectroscopy study of specific glucose reaction on erythrocyte membranes. J Phys D Appl Phys 36:369
doi: 10.1088/0022-3727/36/4/307
Heard KS, Fidyk N, Carruthers A (2000) ATP-dependent substrate occlusion by the human erythrocyte sugar transporter. Biochemistry 39(11):3005–3014
pubmed: 10715121
doi: 10.1021/bi991931u
Helgerson AL, Carruthers A (1987) Equilibrium ligand binding to the human erythrocyte sugar transporter. Evidence for two sugar-binding sites per carrier. J Biol Chem 262(12):5464–5475
pubmed: 3571218
doi: 10.1016/S0021-9258(18)45595-0
Kaatze U (1990) On the existence of bound water in biological systems as probed by dielectric spectroscopy. Phys Med Biol 35(12):1663–1681
pubmed: 2284336
doi: 10.1088/0031-9155/35/12/006
Keller AS et al (2017) Possible roles for ATP release from RBCs exclude the cAMP-mediated Panx1 pathway. Am J Physiol Cell Physiol 313(6):C593-c603
pubmed: 28855161
pmcid: 5814586
doi: 10.1152/ajpcell.00178.2017
Kraszewski A, Kulinski S, Matuszewski M (1976) Dielectric properties and a model of biphase water suspension at 9.4 GHz. J Appl Phys 47(4):1275–1277
doi: 10.1063/1.322825
Levy E et al (2012a) Dielectric spectra broadening as the signature of dipole-matrix interaction. I. Water in nonionic solutions. J Chem Phys 136(11):114502
pubmed: 22443772
doi: 10.1063/1.3687914
Levy E et al (2012b) Dielectric spectra broadening as the signature of dipole-matrix interaction. II. Water in ionic solutions. J Chem Phys 136(11):114503
pubmed: 22443773
doi: 10.1063/1.3691183
Levy E et al (2016) Dielectric response of cytoplasmic water and its connection to the vitality of human red blood cells: I. Glucose concentration influence. J Phys Chem B 120(39):10214–10220
pubmed: 27618444
doi: 10.1021/acs.jpcb.6b06996
Lotspeich-Steininger K (1998) Clinical hematology: principles, procedures and correlations. Lippincott, Philadelphia
MacLean-Fletcher S, Pollard TD (1980) Mechanism of action of cytochalasin B on actin. Cell 20(2):329–341
pubmed: 6893016
doi: 10.1016/0092-8674(80)90619-4
Navale AM, Paranjape AN (2016) Glucose transporters: physiological and pathological roles. Biophys Rev 8(1):5–9
pubmed: 28510148
pmcid: 5425736
doi: 10.1007/s12551-015-0186-2
Nikawa Y, Someya D (2001) Non-invasive measurement of blood sugar level by millimeter waves. In: 2001 IEEE MTT-S International Microwave Sympsoium Digest (Cat. No.01CH37157).
Noertemann K, Hilland J, Kaatze U (1997) Dielectric properties of aqueous NaCl solutions at microwave frequencies. Phys Chem A 101:6864
doi: 10.1021/jp971623a
Pethig R, Kell DB (1987) The passive electrical properties of biological systems: their significance in physiology, biophysics and biotechnology. Phys Med Biol 32(8):933–970
pubmed: 3306721
doi: 10.1088/0031-9155/32/8/001
Raicu V, Fldman Y (2015) Dielectric relaxation in biological systems: physical principles, methods, and applications. Oxford University Press, Oxford, p 464
doi: 10.1093/acprof:oso/9780199686513.001.0001
Rodríguez-Arteche I et al (2012) Dielectric spectroscopy in the GHz region on fully hydrated zwitterionic amino acids. Phys Chem Chem Phys 14(32):11352–11362
pubmed: 22796741
doi: 10.1039/c2cp41496a
Rr P (1977) Dielectric and related molecular processes, Chap 5. Mansel D (ed). The Chemical Society, London
Ryabov YE et al (2002) The symmetric broadening of the water relaxation peak in polymer-water mixtures and its relationship to the hydrophilic and hydrophobic properties of polymers. J Chem Phys 116(19):8610–8615
doi: 10.1063/1.1471551
Schwabbauer (1998) Normal erythrocyte production, physiology and destruction. In: EA S-M (ed) Clinical Hematology principles, procedures, correlations. Lippincott-Raven, Philadelphia
Schwan HP (1957) Electrical properties of tissue and cell suspensions* *This work was supported in part by grants from the United States Public Health Service, H-1253(c2–4) and in part by the Office of Naval Research, 119–289. In: Lawrence JH, Tobias CA (eds) Advances in biological and medical physics. Elsevier, Amsterdamn, pp 147–209
Shinyashiki N et al (1998) Dynamics of water in a polymer matrix studied by a microwave dielectric measurement. J Phys Chem B 102:3249–3251
doi: 10.1021/jp9729627
Siegel PH et al (2015) Compact non-invasive millimeter-wave glucose sensor. In: 2015 40th International Conference on Infrared, Millimeter, and Terahertz waves (IRMMW-THz).
Sprague RS et al (2001) Participation of cAMP in a signal-transduction pathway relating erythrocyte deformation to ATP release. Am J Physiol Cell Physiol 281(4):C1158–C1164
pubmed: 11546651
doi: 10.1152/ajpcell.2001.281.4.C1158
Tadi TKMP (2020) Blood glucose monitoring. StatPearls Publishing, Treasure Island, pp 1–7
Takashima S (1989) Electrical properties of biopolymers and membranes. Adam Hilger, Bristol
Vrba J et al (2019) Metamaterial sensor for microwave non-invasive blood glucose monitoring. Springer, Singapore
doi: 10.1007/978-981-10-9023-3_143
Wessells NK et al (1971) Microfilaments in cellular and developmental processes. Science 171(3967):135–143
pubmed: 5538822
doi: 10.1126/science.171.3967.135
Wolf M et al (2015) Dynamics of protein hydration water. Phys Rev E Stat Nonlin Soft Matter Phys 92(3):032727
pubmed: 26465518
doi: 10.1103/PhysRevE.92.032727