Export by red blood cells of nitric oxide bioactivity

Pawloski, John R.; Hess, Douglas T.; Stamler, Jonathan S.

doi:10.1038/35054560

Cited by 579Hemoglobin structure and functionNitric Oxide and Endothelin EffectsHeme Oxygenase-1 and Carbon Monoxide

Export by red blood cells of nitric oxide bioactivity

Pawloski, John R., Hess, Douglas T., Stamler, Jonathan S.·2001·Nature

DOI 10.1038/35054560

Open this paper in CoChat — free account

Abstract

Previous studies support a model in which the physiological O2 gradient is transduced by haemoglobin into the coordinate release from red blood cells of O2 and nitric oxide (NO)-derived vasoactivity to optimize oxygen delivery in the arterial periphery. But whereas both O2 and NO diffuse into red blood cells, only O2 can diffuse out. Thus, for the dilation of blood vessels by red blood cells, there must be a mechanism to export NO-related vasoactivity, and current models of NO-mediated intercellular communication should be revised. Here we show that in human erythrocytes haemoglobin-derived S-nitrosothiol (SNO), generated from imported NO, is associated predominantly with the red blood cell membrane, and principally with cysteine residues in the haemoglobin-binding cytoplasmic domain of the anion exchanger AE1. Interaction with AE1 promotes the deoxygenated structure in SNO-haemoglobin, which subserves NO group transfer to the membrane. Furthermore, we show that vasodilatory activity is released from this membrane precinct by deoxygenation. Thus, the oxygen-regulated cellular mechanism that couples the synthesis and export of haemoglobin-derived NO bioactivity operates, at least in part, through formation of AE1-SNO at the membrane-cytosol interface.

Integrity signals

Registry

Crossref · 10.1038/35054560

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Under conditions of decreased oxygen saturation, RBCs induce vasodilation of vessel strips by exporting NO bioactivity.
“This view changed radically after the discovery of RBC-mediated hypoxic vasodilation: under conditions of decreased oxygen saturation, RBCs were shown to induce vasodilation of vessel strips by exporting NO bioactivity (146).”
From Red Blood Cell Function and Dysfunction: Redox Regulation, Nitric Oxide Metabolism, Anemia (2017) · cites this paper as [146]

S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control
Jia, L., Bonaventura, C., Bonaventura, J., & Stamler, J. S. (1996) · Nature · doi:10.1038/380221a0 · Cited by 1,586 · see citing works
Self-citation
Blood Flow Regulation by S -Nitrosohemoglobin in the Physiological Oxygen Gradient
Stamler, J. S., Jia, L., Eu, J. P., McMahon, T. J., Demchenko, I. T., Bonaventura, J., Gernert, K., & Piantadosi, C. A. (1997) · Science · doi:10.1126/science.276.5321.2034 · Cited by 1,050 · see citing works
Self-citation
(S)NO Signals: Translocation, Regulation, and a Consensus Motif
Stamler, J. S., Toone, E. J., Lipton, S. A., & Sucher, N. J. (1997) · Neuron · doi:10.1016/s0896-6273(00)80310-4 · Cited by 674 · see citing works
Self-citation
Reactions between nitric oxide and haemoglobin under physiological conditions
Gow, A. J., & Stamler, J. S. (1998) · Nature · doi:10.1038/34402 · Cited by 562 · see citing works
Self-citation
Diffusion-limited reaction of free nitric oxide with erythrocytes
Liu, X., Miller, M. J. S., Joshi, M. S., Sadowska-Krowicka, H., Clark, D. A., & Lancaster, J. R. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.30.18709 · Cited by 512 · see citing works
The oxyhemoglobin reaction of nitric oxide
Gow, A. J., Luchsinger, B. P., Pawloski, J. R., Singel, D. J., & Stamler, J. S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.16.9027 · Cited by 414 · see citing works
Self-citation
Structure and function of the cytoplasmic domain of band 3: center of erythrocyte membrane—peripheral protein interactions
Low, P. S. (1986) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(86)90009-2 · Cited by 407 · see citing works
The interaction of hemoglobin with the cytoplasmic domain of band 3 of the human erythrocyte membrane.
Walder, J. A., Chatterjee, R., Steck, T. L., Low, P. S., Musso, G. F., Kaiser, E. T., Rogers, P. H., & Arnone, A. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)90956-7 · Cited by 302 · see citing works
Erythrocytes Possess an Intrinsic Barrier to Nitric Oxide Consumption
Vaughn, M. W., Huang, K., Kuo, L., & Liao, J. C. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.4.2342 · Cited by 220 · see citing works
Light-scattering measurements of hemoglobin binding to the erythrocyte membrane. Evidence for transmembrane effects related to a disulfonic stilbene binding to band 3
Salhany, J. M., Cordes, K. A., & Gaines, E. D. (1980) · Biochemistry · doi:10.1021/bi00548a028 · Cited by 144 · see citing works
Red blood cell band 3. Lysine 539 and lysine 851 react with the same H2DIDS (4,4‘-diisothiocyanodihydrostilbene-2,2‘-disulfonic acid) molecule.
Okubo, K., Kang, D., Hamasaki, N., & Jennings, M. L. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42114-4 · Cited by 140 · see citing works
Functional Coupling of Oxygen Binding and Vasoactivity inS-Nitrosohemoglobin
McMahon, T., Stone, A. E., Bonaventura, J., Singel, D. J., & Stamler, J. S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000532200 · Cited by 140 · see citing works
Self-citation
Cell-Free and Erythrocytic S -Nitrosohemoglobin Inhibits Human Platelet Aggregation
Pawloski, J. R., Swaminathan, R. V., & Stamler, J. S. (1998) · Circulation · doi:10.1161/01.cir.97.3.263 · Cited by 105 · see citing works
Self-citation
Affinity of hemoglobin for the cytoplasmic fragment of human erythrocyte membrane band 3
Chetrite, G. S., & Cassoly, R. (1985) · Journal of Molecular Biology · doi:10.1016/0022-2836(85)90076-2 · Cited by 103 · see citing works
Molecular mechanisms of band 3 inhibitors. 1. Transport site inhibitors
Falke, J. J., & Chan, S. I. (1986) · Biochemistry · doi:10.1021/bi00372a015 · Cited by 81 · see citing works
[11] Concerted nitric oxide/oxygen delivery by hemoglobin
McMahon, T., & Stamler, J. S. (1999) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(99)01073-3 · Cited by 76 · see citing works
Self-citation
Evidence that inhibitors of anion exchange induce a transmembrane conformational change in band 3.
Macara, I. G., Kuo, S., & Cantley, L. C. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)33056-4 · Cited by 58 · see citing works
Human Erythrocyte Antigens
Telen, M. J., Scearce, R. M., & Haynes, B. F. (1987) · Vox Sanguinis · doi:10.1111/j.1423-0410.1987.tb03035.x · Cited by 58 · see citing works
Identification of the hemoglobin binding sites on the inner surface of the erythrocyte membrane
Rauenbuehler, P. B., Cordes, K. A., & Salhany, J. M. (1982) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(82)90385-6 · Cited by 51 · see citing works
Degradation of the human erythrocyte membrane band 3 studied with the monoclonal antibody directed against an epitope on the cytoplasmic fragment of band 3
Czerwiński, M., Waśniowska, K., Steuden, I., Duk, M., WIȨDŁHA, A., & Lisowska, E. (1988) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1988.tb14147.x · Cited by 44 · see citing works
Direct Measurement of Nitrite Transport Across Erythrocyte Membrane Vesicles Using the Fluorescent Probe, 6-Methoxy-N-(3-sulfopropyl) quinolinium
Shingles, R., Roh, M. H., & McCarty, R. E. (1997) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1022491220299 · Cited by 43 · see citing works
Cross-linking of hemoglobin to the cytoplasmic surface of human erythrocyte membranes. Identification of band 3 as a site for hemoglobin binding in Cu2+-o-phenanthroline catalyzed cross-linking.
Sayare, M., & Fikiet, M. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)43020-7 · Cited by 41 · see citing works
Molecular mechanisms of band 3 inhibitors. 3. Translocation inhibitors
Falke, J. J., & Chan, S. I. (1986) · Biochemistry · doi:10.1021/bi00372a017 · Cited by 39 · see citing works
The interaction of human erythrocyte band 3 with cytoskeletal components
Hsu, L., & Morrison, M. (1983) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(83)90345-4 · Cited by 36 · see citing works
Lys-430, site of irreversible inhibition of band 3 Cl- flux by eosin-5-maleimide, is not at the transport site
Liu, S. Q., & Knauf, P. A. (1993) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1993.264.5.c1155 · Cited by 27 · see citing works
The binding of nitrate to the human anion exchange protein (AE1) studied with 14N nuclear magnetic resonance
Galanter, W., & Labotka, R. (1991) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(91)90119-k · Cited by 21 · see citing works
Penetration of erythrocyte membrane by peroxynitrite: participation of the anion exchange protein
Soszyński, M., & Bartosz, G. (1997) · IUBMB Life · doi:10.1080/15216549700204101 · Cited by 17 · see citing works
[10] Preparation of microcapsules from human erythrocytes: Use in transport experiments of glutathione and its S-conjugate
Kondo, T. (1989) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(89)71013-2 · Cited by 10 · see citing works

Flagged first, then by citations

Sorted by citations

Protein S-nitrosylation: Purview and parameters
Hess, D. T., Matsumoto, A., Kim, S.-O., Marshall, H. E., & Stamler, J. S. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1569 · Cited by 2,153 · see citing works
Self-citation
Cysteine-Mediated Redox Signaling: Chemistry, Biology, and Tools for Discovery
Paulsen, C. E., & Carroll, K. S. (2013) · Chemical Reviews · doi:10.1021/cr300163e · Cited by 1,283 · see citing works
Untitled work
Stamler (2001) · doi:10.1016/s0092-8674(01)00495-0 · Cited by 1,261 · see citing works
Self-citation
Nitric oxide in health and disease of the respiratory system
Ricciardolo, F. L. M., Sterk, P. J., Gaston, B., & Folkerts, G. (2004) · Physiological Reviews · doi:10.1152/physrev.00034.2003 · Cited by 903 · see citing works
Nitric Oxide: The Versatility of an Extensive Signal Molecule
Lamattina, L., García‐Mata, C., Graziano, M., & Pagnussat, G. C. (2003) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.54.031902.134752 · Cited by 877 · see citing works
Nitric oxide signalling in cardiovascular health and disease
Farah, C., Michel, L. Y. M., & Balligand, J.-L. (2018) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.224 · Cited by 779 · see citing works
Protein S-nitrosylation in health and disease: a current perspective
Foster, M. W., Hess, D. T., & Stamler, J. S. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2009.06.007 · Cited by 752 · see citing works
Self-citation
Evolution of adverse changes in stored RBCs
Bennett‐Guerrero, E., Veldman, T. H., Doctor, A., Telen, M. J., Ortel, T. L., Reid, T. S., Mulherin, M. A., Zhu, H., Buck, R. D., Califf, R. M., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708160104 · Cited by 614 · see citing works
S-nitrosylation in health and disease
Foster, M. W., McMahon, T., & Stamler, J. S. (2003) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(03)00028-5 · Cited by 552 · see citing works
Self-citation
Essential Roles of S-Nitrosothiols in Vascular Homeostasis and Endotoxic Shock
Liu, L., Yan, Y., Zeng, M., Zhang, J., Hanes, M. A., Ahearn, G. S., McMahon, T., Dickfeld, T. L., Marshall, H. E., Que, L. G., et al. (2004) · Cell · doi:10.1016/s0092-8674(04)00131-x · Cited by 546 · see citing works
Self-citation
Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation
Tejero, J., Shiva, S., & Gladwin, M. T. (2019) · Physiological Reviews · doi:10.1152/physrev.00036.2017 · Cited by 541 · see citing works
Protein denitrosylation: enzymatic mechanisms and cellular functions
Benhar, M., Forrester, M. T., & Stamler, J. S. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2764 · Cited by 519 · see citing works
Self-citation
S -Nitrosylation in Cardiovascular Signaling
Lima, B., Forrester, M. T., Hess, D. T., & Stamler, J. S. (2010) · Circulation Research · doi:10.1161/circresaha.109.207381 · Cited by 490 · see citing works
Self-citation
CHEMICAL PHYSIOLOGY OF BLOOD FLOW REGULATION BY RED BLOOD CELLS: The Role of Nitric Oxide and S-Nitrosohemoglobin
Singel, D. J., & Stamler, J. S. (2005) · Annual Review of Physiology · doi:10.1146/annurev.physiol.67.060603.090918 · Cited by 481 · see citing works
Self-citation
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
Nitric oxide in the human respiratory cycle
McMahon, T., Moon, R. E., Luschinger, B. P., Carraway, M. S., Stone, A. E., Stolp, B. W., Gow, A. J., Pawloski, J. R., Watke, P., Singel, D. J., et al. (2002) · Nature Medicine · doi:10.1038/nm718 · Cited by 462 · see citing works
Self-citation
How biology handles nitrite
Maia, L. B., & Moura, J. J. G. (2014) · Chemical Reviews · doi:10.1021/cr400518y · Cited by 401 · see citing works
Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69
Haendeler, J., Hoffmann, J., Tischler, V., Berk, B. C., Zeiher, A. M., & Dimmeler, S. (2002) · Nature Cell Biology · doi:10.1038/ncb851 · Cited by 399 · see citing works
GAPDH mediates nitrosylation of nuclear proteins
Kornberg, M. D., Sen, N., Hara, M. R., Juluri, K. R., Nguyen, J. V., Snowman, A. M., Law, L., Hester, L. D., & Snyder, S. H. (2010) · Nature Cell Biology · doi:10.1038/ncb2114 · Cited by 394 · see citing works
Biological significance of nitric oxide-mediated protein modifications
Gow, A. J., Farkouh‐Karoleski, C., Munson, D. A., Posencheg, M. A., & Ischiropoulos, H. (2004) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00295.2003 · Cited by 384 · see citing works
The Biochemistry and Physiology of S-Nitrosothiols
Hogg, N. (2002) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.42.092501.104328 · Cited by 412 · see citing works
Red blood cell pH, the Bohr effect, and other oxygenation‐linked phenomena in blood O 2 and CO 2 transport
Jensen, F. B. (2004) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2004.01361.x · Cited by 346 · see citing works
Active Nitric Oxide Produced in the Red Cell under Hypoxic Conditions by Deoxyhemoglobin-mediated Nitrite Reduction
Nagababu, E., Ramasamy, S., Abernethy, D. R., & Rifkind, J. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307572200 · Cited by 349 · see citing works
Early Inhaled Nitric Oxide Therapy in Premature Newborns with Respiratory Failure
Kinsella, J. P., Cutter, G., Walsh, W. F., Gerstmann, D. R., Bose, C. L., Hart, C., Sekar, K. C., Auten, R. L., Bhutani, V. K., Gerdes, J. S., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa060442 · Cited by 340 · see citing works
NO Generation From Nitrite and Its Role in Vascular Control
Lundberg, J. O., & Weitzberg, E. (2005) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000161048.72004.c2 · Cited by 341 · see citing works
S-Nitrosothiols signal the ventilatory response to hypoxia
Lipton, A. S., Johnson, M. A., Macdonald, T. L., Lieberman, M. W., Gozal, D., & Gaston, B. M. (2001) · Nature · doi:10.1038/35093117 · Cited by 321 · see citing works
Unraveling the Reactions of Nitric Oxide, Nitrite, and Hemoglobin in Physiology and Therapeutics
Kim-Shapiro, D. B., Schechter, A. N., & Gladwin, M. T. (2006) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000204350.44226.9a · Cited by 308 · see citing works
Protein S-Nitrosylation: Determinants of Specificity and Enzymatic Regulation of S-Nitrosothiol-Based Signaling
Stomberski, C. T., Hess, D. T., & Stamler, J. S. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7403 · Cited by 292 · see citing works
Self-citation
S -nitrosohemoglobin deficiency: A mechanism for loss of physiological activity in banked blood
Reynolds, J. D. H., Ahearn, G. S., Angelo, M., Zhang, J., Cobb, F. R., & Stamler, J. S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707958104 · Cited by 282 · see citing works
Self-citation
Structure and function of haemoglobins
Gell, D. A. (2017) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2017.10.006 · Cited by 277 · see citing works
Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease
Anand, P., & Stamler, J. S. (2012) · Journal of Molecular Medicine · doi:10.1007/s00109-012-0878-z · Cited by 270 · see citing works
Self-citation
Nitric Oxide as a Unique Bioactive Signaling Messenger in Physiology and Pathophysiology
Tuteja, N., Chandra, M., Tuteja, R., & Misra, M. K. (2004) · BioMed Research International · doi:10.1155/s1110724304402034 · Cited by 269 · see citing works
Interactions of Organic Nitroso Compounds with Metals
Lee, J., Chen, L., West, A. H., & Richter-Addo, G. B. (2002) · Chemical Reviews · doi:10.1021/cr0000731 · Cited by 267 · see citing works
Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking
Iwakiri, Y., Satoh, A., Chatterjee, S., Toomre, D. K., Chalouni, C. M., Fulton, D. J., Groszmann, R. J., Shah, V. H., & Sessa, W. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605907103 · Cited by 260 · see citing works
Nitric Oxide Improves Internal Iron Availability in Plants
Graziano, M., Beligni, M. V., & Lamattina, L. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.009076 · Cited by 260 · see citing works
The Noncanonical Pathway for In Vivo Nitric Oxide Generation: The Nitrate-Nitrite-Nitric Oxide Pathway
Kapil, V., Khambata, R. S., Jones, D. A., Rathod, K., Primus, C., Massimo, G., Fukuto, J. M., & Ahluwalia, A. (2020) · Pharmacological Reviews · doi:10.1124/pr.120.019240 · Cited by 248 · see citing works
Ozone as Janus: this controversial gas can be either toxic or medically useful
Bocci, V. A. (2004) · Mediators of Inflammation · doi:10.1080/0962935062000197083 · Cited by 245 · see citing works
Modeling pulmonary nitric oxide exchange
George, S. C., Högman, M., Permutt, S., & Silkoff, P. E. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00950.2003 · Cited by 244 · see citing works
The SNO-proteome: causation and classifications
Seth, D., & Stamler, J. S. (2010) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2010.10.012 · Cited by 240 · see citing works
Self-citation
The dual roles of red blood cells in tissue oxygen delivery: oxygen carriers and regulators of local blood flow
Jensen, F. B. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.023697 · Cited by 237 · see citing works
An S -nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate
Angelo, M., Singel, D. J., & Stamler, J. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600942103 · Cited by 233 · see citing works
Self-citation
Chronic hypoxia increases blood pressure and noradrenaline spillover in healthy humans
Calbet, J. A. L. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.045112 · Cited by 231 · see citing works
Stimulation of Suicidal Erythrocyte Death by Methylglyoxal
Nicolay, J. P., Schneider, J., Niemoeller, O. M., Artunç, F., Portero‐Otín, M., HAIK, G. M., Thornalley, P. J., Schleicher, E. D., Wieder, T., & Lang, F. J. W. (2006) · Cellular Physiology and Biochemistry · doi:10.1159/000097669 · Cited by 226 · see citing works
Vascular nitric oxide: formation and function
Loscalzo, J., & Jin (2010) · Journal of Blood Medicine · doi:10.2147/jbm.s7000 · Cited by 228 · see citing works
Nitric oxide is consumed, rather than conserved, by reaction with oxyhemoglobin under physiological conditions
Joshi, M. S., Ferguson, T. B., Han, T. H., Hyduke, D. R., Liao, J. C., Rassaf, T., Bryan, N., Feelisch, M., & Lancaster, J. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152149699 · Cited by 216 · see citing works
S-Nitrosothiol Signaling in Respiratory Biology
Gaston, B. M., Singel, D. J., Doctor, A., & Stamler, J. S. (2006) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200510-1584pp · Cited by 214 · see citing works
Self-citation
Red Blood Cell and Endothelial eNOS Independently Regulate Circulating Nitric Oxide Metabolites and Blood Pressure
Leo, F., Suvorava, T., Heuser, S. K., Li, J., LoBue, A., Barbarino, F., Piragine, E., Schneckmann, R., Hutzler, B., Good, M. E., et al. (2021) · Circulation · doi:10.1161/circulationaha.120.049606 · Cited by 209 · see citing works
Hemoglobin conformation couples erythrocyte S -nitrosothiol content to O 2 gradients
Doctor, A., Platt, R., Sheram, M. L., Eischeid, A. C., McMahon, T., Maxey, T., Doherty, J., Axelrod, M. J., Kline, J. M., Gurka, M. J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407490102 · Cited by 205 · see citing works
The redox switch: dynamic regulation of protein function by cysteine modifications
Spadaro, D., Yun, B., Spoel, S. H., Chu, C., Wang, Y., & Loake, G. J. (2009) · Physiologia Plantarum · doi:10.1111/j.1399-3054.2009.01307.x · Cited by 205 · see citing works
Routes to S -nitroso-hemoglobin formation with heme redox and preferential reactivity in the β subunits
Luchsinger, B. P., Rich, E. N., Gow, A. J., Williams, E. M., Stamler, J. S., & Singel, D. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0233287100 · Cited by 202 · see citing works
Self-citation
Regulation of the Catalytic Activity and Structure of Human Thioredoxin 1 via Oxidation and S-Nitrosylation of Cysteine Residues
Hashemy, S. I., & Holmgren, A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m801047200 · Cited by 192 · see citing works
S-Nitrosylation Signaling in Cell Biology
Gaston, B. M. (2003) · Molecular Interventions · doi:10.1124/mi.3.5.253 · Cited by 192 · see citing works
Pharmacology and potential therapeutic applications of nitric oxide‐releasing non‐steroidal anti‐inflammatory and related nitric oxide‐donating drugs
Keeble, J. E., & Moore, P. K. (2002) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0704876 · Cited by 187 · see citing works
Redox-based protein modifications: the missing link in plant immune signalling
Spoel, S. H., & Loake, G. J. (2011) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2011.03.007 · Cited by 187 · see citing works
Nitric oxide and iron in plants: an emerging and converging story
Graziano, M., & Lamattina, L. (2004) · Trends in Plant Science · doi:10.1016/j.tplants.2004.12.004 · Cited by 184 · see citing works
Nitric Oxide and Cell Signaling Pathways in Mitochondrial-Dependent Apoptosis
Boyd, C. S., & Cadenas, E. (2002) · Biological Chemistry · doi:10.1515/bc.2002.045 · Cited by 182 · see citing works
Redox Regulation in Photosynthetic Organisms: Focus on Glutathionylation
Zaffagnini, M., Bedhomme, M., Marchand, C. H., Morisse, S., Trost, P., & Lemaire, S. D. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4255 · Cited by 181 · see citing works
Mechanism of transfer of NO from extracellular S -nitrosothiols into the cytosol by cell-surface protein disulfide isomerase
Ramachandran, N., Root, P. D., Jiang, X., Hogg, P. J., & Mutus, B. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171180998 · Cited by 179 · see citing works
Plasma Nitrosothiols Contribute to the Systemic Vasodilator Effects of Intravenously Applied NO: Experimental and Clinical Study on the Fate of NO in Human Blood
Rassaf, T., Kleinbongard, P., Preik, M., Dejam, A., Gharini, P., Lauer, T., Erckenbrecht, J., Duschin, A., Schulz, R., Heusch, G., et al. (2002) · Circulation Research · doi:10.1161/01.res.0000035038.41739.cb · Cited by 178 · see citing works
New Insights into Protein S-Nitrosylation
Foster, M. W., & Stamler, J. S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313853200 · Cited by 177 · see citing works
Self-citation
S -Nitrosylation Is Emerging as a Specific and Fundamental Posttranslational Protein Modification: Head-to-Head Comparison with O -Phosphorylation
Lane, P. B., Hao, G., & Gross, S. S. (2001) · Science s STKE · doi:10.1126/stke.2001.86.re1 · Cited by 177 · see citing works
Nitrosothiol Reactivity Profiling Identifies S-Nitrosylated Proteins with Unexpected Stability
Paige, J. S., Xu, G., Stancevic, B., & Jaffrey, S. R. (2008) · Chemistry & Biology · doi:10.1016/j.chembiol.2008.10.013 · Cited by 173 · see citing works
Blood transfusion and increased risk for vasospasm and poor outcome after subarachnoid hemorrhage
Smith, M. J., Roux, P. D. L., Elliott, J. P., & Winn, H. R. (2004) · Journal of neurosurgery · doi:10.3171/jns.2004.101.1.0001 · Cited by 170 · see citing works
The mechanism of transmembrane S -nitrosothiol transport
Zhang, Y., & Hogg, N. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401167101 · Cited by 172 · see citing works
Modulation of nitric oxide bioavailability by erythrocytes
Huang, K., Han, T. H., Hyduke, D. R., Vaughn, M. W., Herle, H. M.-L. V., Hein, T. W., Zhang, C., Kuo, L., & Liao, J. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.201276698 · Cited by 171 · see citing works
S -Nitrosothiols in the Blood: Roles, Amounts, and Methods of Analysis
Stamler, J. S. (2004) · Circulation Research · doi:10.1161/01.res.0000122071.55721.bc · Cited by 170 · see citing works
Self-citation
Paracrine Factors in Tubuloglomerular Feedback: Adenosine, ATP, and Nitric Oxide
Schnermann, J. B., & Levine, D. Z. (2003) · Annual Review of Physiology · doi:10.1146/annurev.physiol.65.050102.085738 · Cited by 167 · see citing works
Hemoglobin, nitric oxide and molecular mechanisms of hypoxic vasodilation
Allen, B. W., Stamler, J. S., & Piantadosi, C. A. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2009.08.002 · Cited by 165 · see citing works
Self-citation
Nitric oxide NO - biogeneration regulation and relevence to human diseases
Bian, K. (2003) · Frontiers in bioscience · doi:10.2741/997 · Cited by 164 · see citing works
Erythrocytes and Vascular Function: Oxygen and Nitric Oxide
Helms, C. C., Gladwin, M. T., & Kim‐Shapiro, D. B. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00125 · Cited by 166 · see citing works
S-Nitrosothiols signal hypoxia-mimetic vascular pathology
Palmer, L. A., Doctor, A., Chhabra, P., Sheram, M. L., Laubach, V. E., Karlinsey, M. Z., Forbes, M. S., Macdonald, T. L., & Gaston, B. M. (2007) · Journal of Clinical Investigation · doi:10.1172/jci29444 · Cited by 161 · see citing works
S-Nitrosohemoglobin Is Unstable in the Reductive Erythrocyte Environment and Lacks O2/NO-linked Allosteric Function
Gladwin, M. T., Wang, X., Reiter, C. D., Yang, B. K., Vivas, E. X., Bonaventura, C., & Schechter, A. N. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203236200 · Cited by 160 · see citing works
A Multiplex Enzymatic Machinery for Cellular Protein S-nitrosylation
Seth, D., Hess, D. T., Hausladen, A., Wang, L., Wang, Y., & Stamler, J. S. (2018) · Molecular Cell · doi:10.1016/j.molcel.2017.12.025 · Cited by 160 · see citing works
Self-citation
Red blood cells
Klinken, S. P. (2002) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(02)00087-0 · Cited by 160 · see citing works
Red blood cell dysfunction: a new player in cardiovascular disease
Pernow, J., Mahdi, A., Yang, J., & Zhou, Z. (2019) · Cardiovascular Research · doi:10.1093/cvr/cvz156 · Cited by 163 · see citing works
SNO-hemoglobin is not essential for red blood cell–dependent hypoxic vasodilation
Isbell, T. S., Sun, C.-W., Wu, L.-C., Teng, X., Vitturi, D. A., Branch, B. G., Kevil, C. G., Peng, N., Wyss, J. M., Ambalavanan, N., et al. (2008) · Nature Medicine · doi:10.1038/nm1771 · Cited by 157 · see citing works
Circulating no pool: assessment of nitrite and nitroso species in blood and tissues
Rassaf, T., Feelisch, M., & Kelm, M. (2003) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2003.11.011 · Cited by 155 · see citing works
Calcium-dependent membrane association sensitizes soluble guanylyl cyclase to nitric oxide
Zabel, U., Kleinschnitz, C., Oh, P., Nedvetsky, P. I., Smolenski, A., Müller, H., Kronich, P., Kügler, P., Walter, U., Schnitzer, J. E., et al. (2002) · Nature Cell Biology · doi:10.1038/ncb775 · Cited by 151 · see citing works
NO adducts in mammalian red blood cells: too much or too little?
Rassaf, T., Bryan, N. S., Maloney, R. E., Specian, V., Kelm, M., Kalyanaraman, B., Rodriguez, J., & Feelisch, M. (2003) · Nature Medicine · doi:10.1038/nm0503-481 · Cited by 151 · see citing works
Erythrocyte Signal Transduction Pathways, their Oxygenation Dependence and Functional Significance
Barvitenko, N. N., Adragna, N. C., & Weber, R. E. (2005) · Cellular Physiology and Biochemistry · doi:10.1159/000083634 · Cited by 150 · see citing works
Emerging Role of Protein-Protein Transnitrosylation in Cell Signaling Pathways
Nakamura, T., & Lipton, S. A. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4703 · Cited by 150 · see citing works
Hemoglobin-mediated nitric oxide signaling
Helms, C., & Kim-Shapiro, D. B. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.04.028 · Cited by 146 · see citing works
Hypoxic Vasodilation by Red Blood Cells
Diesen, D. L., Hess, D. T., & Stamler, J. S. (2008) · Circulation Research · doi:10.1161/circresaha.108.176867 · Cited by 145 · see citing works
Self-citation
S-Nitrosylation of Ascorbate Peroxidase Is Part of Programmed Cell Death Signaling in Tobacco Bright Yellow-2 Cells
de Pinto, M. C., Locato, V., Sgobba, A., Romero‐Puertas, M. C., Gadaleta, C., Delledonne, M., & Gara, L. D. (2013) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.222703 · Cited by 147 · see citing works
Recent advances in the understanding of the role of nitric oxide in cardiovascular homeostasis
Schulz, R., Rassaf, T., Massion, P. B., Kelm, M., & Balligand, J. (2005) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2005.04.005 · Cited by 146 · see citing works
GSNOR-mediated de-nitrosylation in the plant defence response
Malik, S. I., Hussain, A., Yun, B., Spoel, S. H., & Loake, G. J. (2011) · Plant Science · doi:10.1016/j.plantsci.2011.04.004 · Cited by 146 · see citing works
Role of Nitric Oxide Carried by Hemoglobin in Cardiovascular Physiology
Premont, R. T., Reynolds, J. D. H., Zhang, R., & Stamler, J. S. (2019) · Circulation Research · doi:10.1161/circresaha.119.315626 · Cited by 142 · see citing works
Self-citation
Nitric oxide and S-nitrosothiols in human blood
Giustarini, D., Milzani, A., Colombo, R., Dalle-Donne, I., & Rossi, R. (2003) · Clinica Chimica Acta · doi:10.1016/s0009-8981(03)00046-9 · Cited by 136 · see citing works
Impaired vasodilation by red blood cells in sickle cell disease
Pawloski, J. R., Hess, D. T., & Stamler, J. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409876102 · Cited by 137 · see citing works
Self-citation
Catalysis of S -nitrosothiols formation by serum albumin: The mechanism and implication in vascular control
Rafikova, O., Rafikov, R., & Nudler, E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092048999 · Cited by 135 · see citing works
Acute Effects of Aerosolized S -Nitrosoglutathione in Cystic Fibrosis
Snyder, A. H., McPherson, M. E., Hunt, J. F., Johnson, M. A., Stamler, J. S., & Gaston, B. M. (2002) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.165.7.2105032 · Cited by 133 · see citing works
Self-citation
S-Nitrosylation: an emerging redox-based post-translational modification in plants
Wang, Y. (2006) · Journal of Experimental Botany · doi:10.1093/jxb/erj211 · Cited by 131 · see citing works
The Key Role of Nitric Oxide in Hypoxia: Hypoxic Vasodilation and Energy Supply–Demand Matching
Umbrello, M., Dyson, A., Feelisch, M., & Singer, M. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4979 · Cited by 131 · see citing works
A nitric oxide processing defect of red blood cells created by hypoxia: Deficiency of S-nitrosohemoglobin in pulmonary hypertension
McMahon, T., Ahearn, G. S., Moya, M. M., Gow, A. J., Huang, Y.-C. T., Luchsinger, B. P., Nudelman, R., Yan, Y., Krichman, A. D., Bashore, T. M., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506957102 · Cited by 130 · see citing works
Self-citation
Vasorelaxation by Red Blood Cells and Impairment in Diabetes
James, P. E., Lang, D., Tufnell-Barret, T., Milsom, A. B., & Frenneaux, M. P. (2004) · Circulation Research · doi:10.1161/01.res.0000122044.21787.01 · Cited by 125 · see citing works
Nitrite is an alternative source of NO in vivo
Tsuchiya, K., Kanematsu, Y., Yoshizumi, M., Ohnishi, H., Kirima, K., Izawa, Y., Shikishima, M., Ishida, T., Kondo, S., Kagami, S., et al. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00525.2004 · Cited by 127 · see citing works
Thioredoxin 1-Mediated Post-Translational Modifications: Reduction, Transnitrosylation, Denitrosylation, and Related Proteomics Methodologies
Wu, C.-G., Parrott, A. M., Fu, C.-X., Liu, T., Marino, S., Gladyshev, V., Jain, M., Baykal, A., Li, Q., Oka, S.-I., et al. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3831 · Cited by 129 · see citing works
Oxidative Stress and Thrombosis during Aging: The Roles of Oxidative Stress in RBCs in Venous Thrombosis
Wang, Q., & Zennadi, R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124259 · Cited by 124 · see citing works
Horseradish Peroxidase Catalyzed Nitric Oxide Formation from Hydroxyurea
Huang, J., Sommers, E. M., Kim‐Shapiro, D. B., & King, S. B. (2002) · Journal of the American Chemical Society · doi:10.1021/ja012271v · Cited by 124 · see citing works
Specificity in S-Nitrosylation: A Short-Range Mechanism for NO Signaling?
Martı́nez-Ruiz, A., Araújo, I. M., Izquierdo-Álvarez, A., Hernansanz‐Agustín, P., Lamas, S., & Serrador, J. M. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.5066 · Cited by 121 · see citing works

Transport and Peripheral Bioactivities of Nitrogen Oxides Carried by Red Blood Cell Hemoglobin: Role in Oxygen Delivery
Sonveaux, P., Lobysheva, I. I., Féron, O., & McMahon, T. J. (2007) · Physiology · doi:10.1152/physiol.00042.2006 · Cited by 70 · see citing works
Hypoxic Vasodilation by Red Blood Cells and Impairment in Vascular Disorders.
Pawloski, J. R., McMahon, T., Ahearne, G., Piantadosi, C. A., Singel, D. J., & Stamler, J. S. (2004) · Blood · doi:10.1182/blood.v104.11.1585.1585 · Cited by 2 · see citing works
Self-citation
Hemoglobin β93 Cysteine Is Not Required for Export of Nitric Oxide Bioactivity From the Red Blood Cell
Sun, C., Yang, J., Kleschyov, A. L., Zhuge, Z., Carlström, M., Pernow, J., Wajih, N., Isbell, T. S., Oh, J., Cabrales, P., et al. (2019) · Circulation · doi:10.1161/circulationaha.118.039284 · Cited by 47 · see citing works
S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control
Jia, L., Bonaventura, C., Bonaventura, J., & Stamler, J. S. (1996) · Nature · doi:10.1038/380221a0 · Cited by 1,586 · see citing works
Self-citation
Hemoglobin as a chariot for NO bioactivity
Lane, P. B., & Gross, S. S. (2002) · Nature Medicine · doi:10.1038/nm0702-657 · Cited by 39 · see citing works

Authors: Pawloski, J. R., Hess, D. T., & Stamler, J. S.
Affiliations: Howard Hughes Medical Institute (US)
Corresponding author: Stamler, Jonathan S.
ORCID: Stamler, Jonathan S.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2001-02
Volume: 409
Issue: 6820
Pages: 622-626
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/35054560
OpenAlex: W2118023300
Cited by: 579
References: 28
Citations by year: 2026: 2 · 2025: 8 · 2024: 13 · 2023: 13 · 2022: 22 · 2021: 20 · 2020: 17 · 2019: 17 · 2018: 10 · 2017: 19 · 2016: 12 · 2015: 18 · 2014: 16 · 2013: 27 · 2012: 22
FWCI: 16.77
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: American Heart Association
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
Keywords: nitric oxide, erythrocytes, S-nitrosothiols, hemoglobin, band 3, oxygen gradients, vasodilation, oxygen delivery, intercellular communication, cysteine residues
MeSH terms: Animals, Aorta, Biological Transport, Erythrocyte Membrane, Erythrocytes, Hemoglobins, Humans, Mercaptoethanol, Nitric Oxide, Nitroso Compounds, Rabbits, Vasoconstriction, 4,4'-Diisothiocyanostilbene-2,2'-Disulfonic Acid, Antiporters, S-Nitrosothiols, Chloride-Bicarbonate Antiporters, In Vitro Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Export by red blood cells of nitric oxide bioactivity

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks