Transduction of NO-bioactivity by the red blood cell in sepsis: novel mechanisms of vasodilation during acute inflammatory disease

Crawford, Jack H.; Chacko, Balu K.; Pruitt, Heather M.; Piknova, Barbora; Hogg, Neil; Patel, Rakesh P.

doi:10.1182/blood-2004-03-0880

Cited by 111Nitric Oxide and Endothelin EffectsSepsis Diagnosis and TreatmentHemoglobin structure and function

Transduction of NO-bioactivity by the red blood cell in sepsis: novel mechanisms of vasodilation during acute inflammatory disease

Crawford, Jack H., Chacko, Balu K., Pruitt, Heather M., Piknova, Barbora, Hogg, Neil, Patel, Rakesh P.·2004·Blood

DOI 10.1182/blood-2004-03-0880

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Abstract

Sepsis is an acute inflammatory disease characterized by dysfunctional blood flow and hypotension. Nitric oxide (NO) is elevated during sepsis and plays an integral role in the associated vascular pathology. However, precise mechanisms and functions of NO in sepsis remain unclear. In this study, we show that red blood cells (RBCs) are foci for nitrosative reactions during acute inflammation, resulting in the formation of cells that can promote systemic vascular relaxation in an uncontrolled manner. Specifically, using experimental models of endotoxemia and surgical sepsis, NO adducts were found in the RBCs, including S-nitrosohemoglobin (SNOHb). These RBCs, referred to as septic RBCs, spontaneously stimulated vasodilation in a manner consistent with elevated SNOHb concentrations. Moreover, relaxation was cyclic guanosine monophosphate (cGMP) dependent and was inhibited by RBC lysis and glutathione but not by the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5 tetramethylimidazoline 1-oxyl 3-oxide (C-PTIO). The potential mechanism of septic RBC-mediated vasorelaxation is discussed and may involve the intermediate, nitroxyl (HNO). Coupled with data showing that NO adducts in septic RBCs were dependent on the inducible nitric oxide synthase and correlated with plasma nitrite, these findings provide a novel framework to understand mechanisms underlying dysfunctional blood flow responses during sepsis. Specifically, the concept that RBCs directly mediate systemic hypotension through NO-dependent mechanisms is discussed.

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Exogenous administration of nitrite correlates with increased levels of S-nitrosothiols in red blood cells and other tissues both in vivo and in vitro.
“exogenous administration of nitrite correlates with increased levels of S-nitrosothiols in red blood cells and other tissues both in vivo and in vitro [25, 43, 46-53].”
From Current perspectives and challenges in understanding the role of nitrite as an integral player in nitric oxide biology and therapy (2011) · cites this paper as [48]
Nitrite supplementation to intact organisms is associated with a widespread increase in the concentration of nitrite and production of NO-derived species such as S-nitrosothiols or nitrosylhemes in several tissues.
“Many reports show that nitrite supplementation to intact organisms is associated with a widespread increase in the concentration of this anion and production of NO-derived species such as S-nitrosothiols or nitrosylhemes in several tissues[25, 43, 46, 48, 49, 96].”
From Current perspectives and challenges in understanding the role of nitrite as an integral player in nitric oxide biology and therapy (2011) · cites this paper as [48]

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Authors: Crawford, J. H., Chacko, B. K., Pruitt, H. M., Piknova, B., Hogg, N., & Patel, R. P.
Affiliations: Medical College of Wisconsin (US)
ORCID: Chacko, Balu K.
Piknova, Barbora
Hogg, Neil
Patel, Rakesh P.
Venue: Blood
Publisher: American Society of Hematology
Published: 2004-09-01
Volume: 104
Issue: 5
Pages: 1375-1382
ISSN: 0006-4971 (ISSN-L)
1528-0020
DOI: 10.1182/blood-2004-03-0880
OpenAlex: W1987088892
Cited by: 111
References: 62
Citations by year: 2026: 1 · 2025: 1 · 2022: 4 · 2021: 4 · 2020: 1 · 2019: 5 · 2017: 9 · 2016: 3 · 2015: 6 · 2014: 5 · 2013: 6 · 2012: 7
FWCI: 5.34
Type: journal article
Language: en
Open access: closed
Locations: Blood (publishedVersion)
PubMed (publishedVersion)
Funders: National Heart, Lung, and Blood Institute (R01HL070146, HL 70146)
National Institute of General Medical Sciences (T32GM008361, T32 GM 08361, GM55792)
National Institute of Biomedical Imaging and Bioengineering (EB001980, P41EB001980)
Topics: Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Health Sciences › Medicine › Epidemiology › Sepsis Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
Keywords: sepsis, nitric oxide, erythrocytes, S-nitrosohemoglobin, nitroxyl, vasodilation, endotoxemia, septic shock, hypotension, inducible nitric oxide synthase, plasma nitrite, glutathione, acute inflammation
MeSH terms: Acute Disease, Animals, Cecum, Disease Models, Animal, Erythrocytes, Hemoglobins, Ligation, Lipopolysaccharides, Male, Nitric Oxide, Nitrites, Oxygen, Vasodilation, Wounds, Stab, Rats, Sprague-Dawley, Sepsis, Nitric Oxide Synthase, Rats, Nitric Oxide Synthase Type II

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Transduction of NO-bioactivity by the red blood cell in sepsis: novel mechanisms of vasodilation during acute inflammatory disease

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