Effect of Superoxide Anions on Red Blood Cell Rheologic Properties
Abstract
The human red blood cell (RBC) is known to be susceptible to oxidant damage, with both structural and functional properties altered consequent to oxidant attack. Such oxidant-related alterations may lead to changes of RBC rheologic behavior (i.e., deformability, aggregability). Two different models of oxidant stress were used in this study to generate superoxide anions either internal or external to the RBC. Our results indicate that generation of superoxide within the RBC by phenazine methosulfate decreases RBC deformability without effects on cell aggregation. Conversely, superoxide generated externally by the xanthine oxidase-hypoxanthine system primarily affects RBC aggregability: the shear rate necessary to disaggregate RBC was markedly increased while the extent of aggregation decreased slightly. Increased disaggregation shear rate (i.e., greater aggregate strength) as a result of superoxide radical damage may adversely affect the dynamics of blood flow in low-shear portions of the circulation, and may also play a role in the no-reflow phenomena encountered after ischemia-reperfusion.
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Changes in the redox state of RBCs by alkylating agents, superoxide-generating systems, and peroxides strongly affect RBC deformability.
“Changes in the redox state of RBCs by treatment with alkylating agents, superoxide-generating systems, and peroxides strongly affect RBC deformability (12).”
From Red Blood Cell Function and Dysfunction: Redox Regulation, Nitric Oxide Metabolism, Anemia (2017) · cites this paper as [12]
Cites
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
LAEMMLI, U. K. (1970) · Nature · doi:10.1038/227680a0 · Cited by 249,961 · see citing works
The Autoxidation of Human Red Cell Lipids Induced by Hydrogen Peroxide
Stocks, J., & Dormandy, T. L. (1971) · British Journal of Haematology · doi:10.1111/j.1365-2141.1971.tb00790.x · Cited by 973 · see citing works
Malech, H. L., & Gallin, J. I. (1987) · New England Journal of Medicine · doi:10.1056/nejm198709103171107 · Cited by 840 · see citing works
Murray, R. K. (1998) · Medical Entomology and Zoology · Cited by 811 · see citing works
Role of leukocytes in response to acute myocardial ischemia and reflow in dogs
Engler, R. L., Dahlgren, M. D., Morris, D., Peterson, M. A., & Schmid‐Schönbein, G. W. (1986) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1986.251.2.h314 · Cited by 507 · see citing works
Pathophysiology of ischaemia reperfusion injury: Central role of the neutrophil
Welbourn, C. R. B., Goldman, G., Paterson, I. S., Valeri, C. R., Shepro, D., & Hechtman, H. B. (1991) · Journal of British Surgery · doi:10.1002/bjs.1800780607 · Cited by 501 · see citing works
Davies, K. J. A., & Goldberg, A. L. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47552-7 · Cited by 412 · see citing works
Free Radicals in Medicine. I. Chemical Nature and Biologic Reactions
Southorn, P. A., & Powis, G. (1988) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(12)64861-7 · Cited by 391 · see citing works
Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells.
Davies, K. J. A., & Goldberg, A. L. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47553-9 · Cited by 339 · see citing works
Free Radicals in Medicine. II. Involvement in Human Disease
Southorn, P. A., & Powis, G. (1988) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(12)64862-9 · Cited by 339 · see citing works
Snyder, L. M., Fortier, N. L., Trainor, J., et al. (1985) · Journal of Clinical Investigation · doi:10.1172/jci112196 · Cited by 280 · see citing works
Lipid peroxidation in human red cells.
Chiu, D., Kuypers, F. A., & Lubin, B. H. (1989) · PubMed · Cited by 217 · see citing works
Mechanism of erythrocyte aggregation and sedimentation
Fabry, T. (1987) · Blood · doi:10.1182/blood.v70.5.1572.1572 · Cited by 199 · see citing works
(1990) · Elsevier eBooks · doi:10.1016/b978-0-12-584552-6.x5001-0 · Cited by 195 · see citing works
BESSIS, M. C., Weed, R. I., & Leblond, P. F. (1973) · Springer eBooks · doi:10.1007/978-3-642-88062-9 · Cited by 186 · see citing works
Na+ and K+ transport damage induced by oxygen free radicals in human red cell membranes.
Maridonneau, I., Braquet, P. G., & Garay, R. P. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)32837-0 · Cited by 175 · see citing works
The role of superoxide in the destruction of erythrocyte targets by human neutrophils.
Weiss, S. J. (1980) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)43479-5 · Cited by 154 · see citing works
Contribution of red blood cell aggregation to venous vascular resistance in skeletal muscle
Cabel, M., Meiselman, H. J., Popel, A. S., et al. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.272.2.h1020 · Cited by 154 · see citing works
Self-citationOxidation-induced changes in microrheologic properties of the red blood cell membrane
Hebbel, R., Leung, A., & Mohandas, N. (1990) · Blood · doi:10.1182/blood.v76.5.1015.bloodjournal7651015 · Cited by 153 · see citing works
Chien, S., Dormandy, J. A., Ernst, E. C., et al. (1986) · Developments in cardiovascular medicine · doi:10.1007/978-94-009-4285-1 · Cited by 148 · see citing works
Shiga, T., Maeda, N., & Kon, K. (1990) · Critical Reviews in Oncology/Hematology · doi:10.1016/1040-8428(90)90020-s · Cited by 145 · see citing works
Lowe, G. D. O. (2019) · CRC Press eBooks · doi:10.1201/9780429261183 · Cited by 132 · see citing works
Oxidative stress: a radical view.
Saltman, P. (1989) · PubMed · Cited by 132 · see citing works
Anadere, I., Chmiel, H., Hess, H., & Thurston, G. B. (1979) · Biorheology · doi:10.3233/bir-1979-16305 · Cited by 127 · see citing works
Physicochemical basis and clinical implications of red cell aggregation
Chien, S., & Sung, L. A. (1987) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-1987-7108 · Cited by 122 · see citing works
Machiedo, G. W. (1989) · Archives of Surgery · doi:10.1001/archsurg.1989.01410120032007 · Cited by 116 · see citing works
Alterations of human erythrocyte membrane fluidity by oxygen-derived free radicals and calcium
Watanabe, H. K., Kobayashi, A., Yamamoto, T., et al. (1990) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(90)90150-h · Cited by 115 · see citing works
Effects of superoxide anions on red cell deformability and membrane proteins
Uyesaka, N., Hasegawa, S., Ishioka, N., Ishioka, R., Shio, H., & Schechter, A. N. (1992) · Biorheology · doi:10.3233/bir-1992-292-303 · Cited by 84 · see citing works
Influence of cellular properties on red cell aggregation
Nash, G. B., Wenby, R. B., Sowemimo-Coker, S. O., et al. (1987) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-1987-7109 · Cited by 76 · see citing works
Peroxide-induced membrane damage in human erythrocytes
Jolanda Van der, Z. E. E., Dubbelman, T. M. A. R., & Steveninck, J. V. (1985) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(85)90135-x · Cited by 74 · see citing works
Use of ektacytometry to determine red cell susceptibility to oxidative stress.
Kuypers, F. A., Scott, Ma, S., Lubin, B. H., & Dt, C. (1990) · PubMed · Cited by 74 · see citing works
In Vivo Oxidative Modification of Erythrocyte Membrane Proteins in Copper Deficiency
Sukalski, K. A., LaBerge, T. P., & Johnson, W. T. (1997) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(96)00430-3 · Cited by 68 · see citing works
Determination of specific red blood cell aggregation indices via an automated system
Bauersachs, R. M., Wenby, R. B., & Meiselman, H. J. (1989) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-1989-9101 · Cited by 62 · see citing works
Self-citationErythrocyte aggregation: the roles of cell deformability and geometry
Reinhart, W. H., & Singh, A. P. (1990) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1990.tb01884.x · Cited by 52 · see citing works
Oxidative red blood cell membrane injury in the pathophysiology of severe mouse beta-thalassemia
Advani, R. H., Rubin, E. M., Mohandas, N., et al. (1992) · Blood · doi:10.1182/blood.v79.4.1064.1064 · Cited by 49 · see citing works
Xanthine oxidase-catalyzed crosslinking of cell membrane proteins
Girotti, A. W., Thomas, J. P., & Jordan, J. E. (1986) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(86)90374-7 · Cited by 47 · see citing works
Beppu, M., Inoue, M., Ishikawa, T., et al. (1994) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(94)90298-4 · Cited by 46 · see citing works
Comparison of four indirect methods for fluid superoxide dismutase activities
DiSilvestro, R. A., David, C., & David, E. A. (1990) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(90)90129-7 · Cited by 41 · see citing works
Early in reperfusion, leukocytes alter perfused coronary capillarity and vascular resistance
Reynolds, J. M., & McDonagh, P. F. (1989) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1989.256.4.h982 · Cited by 40 · see citing works
Oxidative red blood cell membrane injury in the pathophysiology of severe mouse beta-thalassemia
Advani, R. H., Rubin, E., Mohandas, N., et al. (1992) · Blood · doi:10.1182/blood.v79.4.1064.bloodjournal7941064 · Cited by 40 · see citing works
Studies on the factors influencing the hydrogen peroxide hemolysis test.
Makoto, M. I. N. D., Nishida, Y., Murata, K., TAKEGAWA, M., Katsui, G., & Yuguchi, Y. (1978) · Journal of Nutritional Science and Vitaminology · doi:10.3177/jnsv.24.383 · Cited by 30 · see citing works
Activated granulocyte induced alterations in red blood cells and protection by antioxidant enzymes
Baskurt, O. K. (1996) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-1996-16110 · Cited by 29 · see citing works
Self-citationBrooks, D. E., & Evans, E. A. (1987) · Developments in cardiovascular medicine · doi:10.1007/978-94-009-4285-1_3 · Cited by 27 · see citing works
Effect of alpha-tocopherol on red cell deformability and survival in sepsis.
Rj, P., Gw, M., Bf, R., et al. (1989) · PubMed · Cited by 27 · see citing works
Surface Properties of Cells Reflected by Partitioning: Red Blood Cells as a Model
Walter, H. (1985) · Elsevier eBooks · doi:10.1016/b978-0-12-733860-6.50017-7 · Cited by 22 · see citing works
Effect of oxygen free radicals on rabbit and human erythrocytes:Studies on Cellular Deformability
Hirayama, T., Folmerz, P., Hansson, R., et al. (1986) · Scandinavian Journal of Thoracic and Cardiovascular Surgery · doi:10.3109/14017438609105933 · Cited by 21 · see citing works
Do plasma proteins adsorb to red cells?
Janzen, J., & Brooks, D. E. (1989) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-1989-9502 · Cited by 20 · see citing works
Manning, W. J. (1995) · Environmental Pollution · doi:10.1016/0269-7491(95)90024-1 · Cited by 16 · see citing works
Effects of neuraminidase and trypsin on surface charge and aggregation of red blood cells
Böhler, T., & Linderkamp, O. (1993) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-1993-13609 · Cited by 14 · see citing works
Schmid-Schönbein, H. (2019) · CRC Press eBooks · doi:10.1201/9780429261176-7 · Cited by 14 · see citing works
Enzymatic degradation of the red cell surface and its effect on Rouleaux formation
RAMPLING, M. W., & Pearson, M. J. (1994) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-1994-14408 · Cited by 10 · see citing works
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Red Blood Cell Function and Dysfunction: Redox Regulation, Nitric Oxide Metabolism, Anemia
Kuhn, V., Diederich, L., Keller, T. C. S., Kramer, C. M., Lückstädt, W., Panknin, C., Suvorava, T., Isakson, B. E., Kelm, M., & Cortese-Krott, M. M. (2017) · Antioxidants & Redox Signaling · doi:10.1089/ars.2016.6954 · Cited by 469 · see citing works
Park, S.-K., Hur, M., Kim, E., Kim, W. H., Park, J. B., Kim, Y., Yang, J.-H., Jun, T.-G., & Kim, C. S. (2016) · PLOS ONE · doi:10.1371/journal.pone.0166328 · Cited by 133 · see citing works
- Authors
- Baskurt, O. K., Temiz, A., & Meiselman, H. J.
- Affiliations
- University of Southern California (US)
- Corresponding author
- Meiselman, Herbert J.
- Venue
- Free Radical Biology and Medicine
- Publisher
- Elsevier BV
- Published
- 1998-01
- Volume
- 24
- Issue
- 1
- Pages
- 102-110
- ISSN
- 0891-5849 (ISSN-L)
- OpenAlex
- W2052023508
- Cited by
- 192
- References
- 51
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 3 · 2023: 6 · 2022: 10 · 2021: 4 · 2020: 5 · 2019: 5 · 2018: 16 · 2017: 9 · 2016: 6 · 2015: 9 · 2014: 13 · 2013: 8 · 2012: 12
- FWCI
- 5.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Free Radical Biology and Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5p60hl048484-10)
- National Heart, Lung, and Blood Institute (HL48484, HL 15722)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Blood properties and coagulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Health Sciences › Medicine › Physiology › Erythrocyte Function and Pathophysiology
- Keywords
- superoxide, red blood cell rheology, erythrocyte deformability, erythrocyte aggregation, oxidative damage, phenazine methosulfate, no-reflow phenomenon, ischemia-reperfusion
- MeSH terms
- Erythrocyte Aggregation, Erythrocyte Deformability, Free Radicals, Humans, Methylphenazonium Methosulfate, Reference Values, Stress, Mechanical, Superoxides, Xanthine Oxidase, Reactive Oxygen Species, Oxidative Stress
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