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Intravascular hemolysis and the pathophysiology of sickle cell disease
Open accessAbstract
flow, normoxia to hypoxia, isotonic to hypertonic environment, and acidotic to alkalotic milieu.Multiple components contribute to sickle hemoglobinopathy pathophysiology, including primary components arising from HbS polymerization and secondary components that are downstream effects of the HbS polymer. Understanding how these components' complexity is compounded by genetic and environmental modulation provides insight into the well-known clinical heterogeneity of sickle cell disease (SCD).A cardinal feature of SCD pathogenesis involves inflammation, accompanied by heterocellular leukocyte-platelet-erythrocyte-endothelial adhesive events that trigger vaso-occlusive episodes, acute organ ischemia, and reperfusion injury.Twenty-five years ago, epidemiological studies identified leukocytosis, lower HbF levels, and higher total hemoglobin levels as risk factors associated with increasing incidence of acute painful episodes and acute chest syndrome (ACS) (5).The independent association of high total hemoglobin levels with more pain, ACS events, and osteonecrosis was never mechanistically explained; however, it was implied to be a result of increased blood viscosity (Table 1).Recent epidemiological studies found that lower hemoglobin levels and higher intensity of steady-state hemolytic anemia consistently associate with vasculopathic complications of disease, such as stroke, leg ulcers, PH, priapism, and renal failure.This suggests that certain subphenotypes of SCD relate more to hemolytic anemia severity rather than sickle vaso-occlusion.The reader is referred to recent reviews describing the exceptional strides made in understanding the roles of red cell rigidity (6), inflammation, and cell adhesion in sickle vaso-occlusion (7-9).Here, we review the complementary role of intravascular hemolysis and anemia.Hemolysis is a fundamental feature of sickle cell anemia that contributes to its pathophysiology and phenotypic variability.Decompartmentalized hemoglobin, arginase 1, asymmetric dimethylarginine, and adenine nucleotides are all products of hemolysis that promote vasomotor dysfunction, proliferative vasculopathy, and a multitude of clinical complications of pulmonary and systemic vasculopathy, including pulmonary hypertension, leg ulcers, priapism, chronic kidney disease, and large-artery ischemic stroke.Nitric oxide (NO) is inactivated by cell-free hemoglobin in a dioxygenation reaction that also oxidizes hemoglobin to methemoglobin, a non-oxygen-binding form of hemoglobin that readily loses heme.Circulating hemoglobin and heme represent erythrocytic danger-associated molecular pattern (eDAMP) molecules, which activate the innate immune system and endothelium to an inflammatory, proadhesive state that promotes sickle vaso-occlusion and acute lung injury in murine models of sickle cell disease.Intravascular hemolysis can impair NO bioavailability and cause oxidative stress, altering redox balance and amplifying physiological processes that govern blood flow, hemostasis, inflammation, and angiogenesis.These pathological responses promote regional vasoconstriction and subsequent blood vessel remodeling.Thus, intravascular hemolysis represents an intrinsic mechanism for human vascular disease that manifests clinical complications in sickle cell disease and other chronic hereditary or acquired hemolytic anemias.
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“As HbF falls and fewer F-cells are protected from HbS polymer damage, the propensity for vascular occlusion and intravascular hemolysis increases with the release of heme products into the circulation that scavenge nitric oxide causing endothelial damage and vasculopathy.[57][58][59]”
From Fetal hemoglobin in sickle cell anemia (2020) · cites this paper as [58]
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“Once released, IL-1β binds to IL-1 receptor (IL-1R) on leukocytes and vascular cells, promoting a cascade of downstream events that lead to activation of neutrophils and platelets and upregulation of E-selectin, P-selectin, VCAM-1, ICAM-1, and chemokines such as IL-8 in endothelial cells, all of which promote vaso-occlusion (14, 17) (Figure 1).”
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“Vaso-occlusion contributes to ischemia-reperfusion injury, which, along with release of eDAMPs, promotes the progression of sterile inflammation (Figure 1d) in SCD (14, 17, 18).”
From Pathophysiology of Sickle Cell Disease (2019) · cites this paper as [17]
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“Studies in adults with SCD lend further support to the role of hemolysis by showing a link between the hyperhemolysis phenotype of SCD and stroke risk (17).”
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“Unequal protection by HbF across the gamut of sickle cell disease complications might be partially explained by differences in the pathophysiologic roots of these complications.57,58”
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“Acute painful episodes and acute chest syndrome are a result of sickle vasoocclusion; HbF has the most noticeable beneficial effect on these subphenotypes.”
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“Priapism, nephropathy, and sickle vasculopathy are associated with hemolysis.”
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Metadata
- Authors
- Kato, G. J., Steinberg, M. H., & Gladwin, M. T.
- Affiliations
- University of Pittsburgh (US)
- Boston University (US)
- Corresponding author
- Gladwin, Mark T.
- Venue
- Journal of Clinical Investigation
- Published
- 2017-03-01
- Volume
- 127
- Issue
- 3
- Pages
- 750-760
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC5330745
- OpenAlex
- W2592339311
- Semantic Scholar
- 0c9beb4e3a557982862ac3ec381a89baab12ceae
- Cited by
- 748
- References
- 193
- Citations by year
- 2026: 90 · 2025: 81 · 2024: 76 · 2023: 65 · 2022: 116 · 2021: 81 · 2020: 87 · 2019: 76 · 2018: 53 · 2017: 21
- FWCI
- 9.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Patient-Centered Outcomes Research Institute
- University of Pittsburgh
- Hemophilia Center of Western Pennsylvania
- National Institutes of Health (HL098032)
- National Heart, Lung, and Blood Institute (R01HL087681, R01HL068970, P01HL103455, RC2HL101212, R01HL121386, U01HL107443, T32HL007501, R01HL125886, R01HL098032, T32HL110849)
- National Institute on Minority Health and Health Disparities (R01MD009162)
- Topics
- Health Sciences › Medicine › Genetics (clinical) › Hemoglobinopathies and Related Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Hemoglobin structure and function
- Health Sciences › Medicine › Hematology › Blood properties and coagulation
- Keywords
- intravascular hemolysis, sickle cell disease, free hemoglobin, nitric oxide, methemoglobin, heme, arginase-1, asymmetric dimethylarginine, adenine nucleotides, pulmonary hypertension, inflammation
- MeSH terms
- Anemia, Sickle Cell, Hemolysis, Humans, Methemoglobin, Nitric Oxide, Vascular Diseases, Vasomotor System
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