Cited by 775Nitric Oxide and Endothelin EffectsAtherosclerosis and Cardiovascular DiseasesAngiogenesis and VEGF in Cancer

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Tumor necrosis factor downregulates an endothelial nitric oxide synthase mRNA by shortening its half-life

Yoshizumi, M, Perrella, M A, Burnett, J C, Lee, M E·1993·Circulation Research

DOI 10.1161/01.res.73.1.205

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Abstract

Nitric oxide (NO), which accounts for the biological properties of endothelium-derived relaxing factor, is generated by NO synthase (NOS). The vascular endothelium contains two types of NOS: one is constitutively expressed (cNOS), and the other is inducible. Endothelium-mediated vasorelaxation is impaired in atherosclerotic vessels. To determine whether tumor necrosis factor (TNF)-alpha, which is commonly found in atherosclerotic lesions, has an effect on NOS message, we measured cNOS mRNA levels in TNF-treated human umbilical vein endothelial cells (HUVECs) by RNA blot analysis with a cNOS cDNA probe. TNF-alpha markedly reduced cNOS mRNA levels in HUVECs in a dose- and time-dependent manner. In response to 3 ng/mL TNF-alpha, cNOS mRNA levels began to decrease at 4 hours and diminished to only 5% of control levels at 24 hours. As little as 0.1 ng/mL TNF-alpha reduced cNOS mRNA levels by 50%. This reduction in cNOS message in response to TNF-alpha depended on protein synthesis as it was blocked by cycloheximide. In nuclear runoff experiments, TNF-alpha did not change the rate of cNOS gene transcription. cNOS mRNA is very stable under basal conditions, with a half-life of 48 hours; however, treatment with TNF-alpha shortened this half-life to 3 hours. TNF-alpha thus appears to decrease cNOS mRNA levels by increasing the rate of mRNA degradation. TNF-induced reductions in cNOS mRNA levels may have an important effect on impaired endothelium-mediated vasorelaxation in atherosclerosis.

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Claudio Napoli, A., Lerman, L. O., de Nigris, F., Loscalzo, J., & Ignarro, L. J. (2002) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(02)02306-9 · Cited by 42
“During the last 3 min, bradykinin (Sigma) at a final concentration of 3 nM was added, followed by extraction with trichloroacetic acid solution (30).”
Method
Monocyte-Induced Downregulation of Nitric Oxide Synthase in Cultured Aortic Endothelial Cells
Marczin, N., Antonov, A., Papapetropoulos, A., Munn, D. H., Virmani, R., Kolodgie, F. D., Gerrity, R. G., & Catravas, J. D. (1996) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.16.9.1095 · Cited by 44
Rho kinase mediates Porphyromonas gingivalis outer membrane vesicle-induced suppression of endothelial nitric oxide synthase through ERK1/2 and p38 MAPK
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Cardio‐renal cachexia syndromes (CRCS): pathophysiological foundations of a vicious pathological circle
Cicoira, M., Anker, S. D., & Ronco, C. (2011) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1007/s13539-011-0038-2 · Cited by 40
“Cytokines also reduce constitutive nitric oxide synthase mRNA in endothelial cells [63] and therefore impair endothelial function.”
Background
Functional Role of Connexins and Pannexins in the Interaction Between Vascular and Nervous System
Gaete, P. S., Lillo, M. A., & Figueroa, X. F. (2014) · Journal of Cellular Physiology · doi:10.1002/jcp.24563 · Cited by 42
“…responses (Wang et al., 1996; Sorkin et al., 1997; Brain and Grant, 2004) may explain the endothelial dysfunction related to a reduction of eNOS levels typically described in pathological conditions associated with inflammation (Yoshizumi et al., 1993; Huang and Vita, 2006; Ding et al., 2009).”
Background
Structure and function of nitric of oxide synthases
Hattori, R., Sase, K., Eizawa, H., Kosuga, K., Aoyama, T., Inoue, R., Sasayama, S., Kawai, C., & Yui, Y. (1994) · International Journal of Cardiology · doi:10.1016/0167-5273(94)90329-8 · Cited by 40
Megakaryocytes From Patients With Coronary Atherosclerosis Express the Inducible Nitric Oxide Synthase
de Belder, A., Radomski, M. W., Hancock, V., et al. (1995) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.15.5.637 · Cited by 39
The Role of Endogenous Nitric Oxide in Modulating Ischemia-Reperfusion Injury in the Isolated, Blood-perfused Rat Lung
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Inhibitory effects of Kaempferia parviflora extract on monocyte adhesion and cellular reactive oxygen species production in human umbilical vein endothelial cells
Horigome, S., Yoshida, I., Ito, S., Inohana, S., Fushimi, K., Nagai, T., Yamaguchi, A., Fujita, K., Satoyama, T., Katsuda, S.-I., et al. (2015) · European Journal of Nutrition · doi:10.1007/s00394-015-1141-5 · Cited by 38
“KP extract was previously reported to induce production of eNOS in vascular endothelial cells [27], and the mRNA expression of NOS3 was downregulated by stimulation with low concentrations of TNF-α [28].”
Background
The role of NO synthases in arginine-dependent small intestinal and colonic carcinogenesis
Yerushalmi, H. F., Besselsen, D. G., Ignatenko, N. A., Blohm-Mangone, K. A., Padilla‐Torres, J., Stringer, D. E., Cui, H., Holubec, H., Payne, C. M., & Gerner, E. W. (2005) · Molecular Carcinogenesis · doi:10.1002/mc.20168 · Cited by 38
Importance of Endothelial Function in Chronic Heart Failure
Drexler, H., & Hornig, B. (1996) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199600002-00003 · Cited by 38
Nitric Oxide Gas Decreases Endothelin-1 mRNA in Cultured Pulmonary Artery Endothelial Cells
Smith, A., Demoncheaux, E. A. G., & Higenbottam, T. (2002) · Nitric Oxide · doi:10.1006/niox.2001.0400 · Cited by 38
Correlation of tumor necrosis factor alpha and interleukin 6 with hypertensive renal damage
Yu, X., Yang, Z., & Yu, M. (2010) · Renal Failure · doi:10.3109/08860221003664280 · Cited by 37
Arterial Stiffening, Wave Reflection, and Inflammation in Habitually Exercising Systemic Lupus Erythematosus Patients
Barnes, J. N., Nualnim, N., Sugawara, J., Sommerlad, S. M., Renzi, C., & Tanaka, H. (2011) · American Journal of Hypertension · doi:10.1038/ajh.2011.143 · Cited by 37
Nitric Oxide (NO) Upregulates NO Synthase Expression in Fetal Intrapulmonary Artery Endothelial Cells
Yuhanna, I. S., MacRitchie, A. N., Lantin-Hermoso, R. L., Wells, L. B., & Shaul, P. W. (1999) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.21.5.3749 · Cited by 37
Hypoxia-specific upregulation of calpain activity and gene expression in pulmonary artery endothelial cells
Zhang, J., Patel, J. M., & Block, E. R. (1998) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1998.275.3.l461 · Cited by 38
“The 18S complementary oligonucleotide (-ACG GTA TCT GAT CGT CTT CGA ACC-) (47) was labeled at its 38-end with terminal transferase by synthesis of a DNA tail of 40–50 nucleotide lengths with several incorporated DIG-dUTPs, as described previously (33).”
Method
Role of ecNOS-derived NO in mediating TNF-induced endothelial barrier dysfunction
Bove, K., Neumann, P. H., Gertzberg, N., & Johnson, A. (2001) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2001.280.5.l914 · Cited by 37
“Moreover, previous studies indicate that the decrease in expression is caused in part by the degradation of ecNOS mRNA (43, 44).”
BackgroundResultInfluential
Expressional Down-Regulation of Neuronal-Type Nitric Oxide Synthase I by Glucocorticoids in N1E-115 Neuroblastoma Cells
Schwarz, P. M., Gierten, B., Boissel, J., & Förstermann, U. (1998) · Molecular Pharmacology · doi:10.1124/mol.54.2.258 · Cited by 37
“Studies with relative selective NOS inhibitors or with knockout mice lacking specific NOS isoforms imply that both NOS I (Hara et al., 1996; Huang et al., 1994) and NOS II (Iadecola et al., 1997) contribute to the ischemic brain damage, whereas NOS III is likely to have protective effects (Huang et al., 1994).”
BackgroundInfluential
Regulation of the Expression of Nitric Oxide Synthase Isoforms
Kleinert, H., Boissel, J., Schwarz, P. M., & Förstermann, U. (2000) · Elsevier eBooks · doi:10.1016/b978-012370420-7/50008-3 · Cited by 38
Evidence That Expression of Inducible Nitric Oxide Synthase in Response to Endotoxin Is Augmented in Atherosclerotic Rabbits
Sobey, C. G., Brooks, R. M., & Heistad, D. D. (1995) · Circulation Research · doi:10.1161/01.res.77.3.536 · Cited by 37
Protein kinase C activation inhibits cytokine-induced nitric oxide synthesis in vascular smooth muscle cells
Geng, Y., Wu, Q. Y., & Hansson, G. K. (1994) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(94)90081-7 · Cited by 37
Endothelıal dysfunctıon ın patıents wıth prımary Sjögren’s syndrome
Pırıldar, T., Tıkız, C., Özkaya, S., et al. (2005) · Rheumatology International · doi:10.1007/s00296-005-0599-5 · Cited by 36

Authors: Yoshizumi, M., Perrella, M. A., Burnett, J. C., & Lee, M. E.
Affiliations: Harvard University (US)
ORCID: Yoshizumi, M
Perrella, M A
Venue: Circulation Research
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 1993-07
Volume: 73
Issue: 1
Pages: 205-209
ISSN: 0009-7330 (ISSN-L)
1524-4571
DOI: 10.1161/01.res.73.1.205
OpenAlex: W2145570729
Cited by: 771
References: 0
Citations by year: 2026: 4 · 2025: 5 · 2024: 9 · 2023: 10 · 2022: 13 · 2021: 15 · 2020: 16 · 2019: 12 · 2018: 16 · 2017: 14 · 2016: 11 · 2015: 17 · 2014: 35 · 2013: 19 · 2012: 18
FWCI: 21.77
Type: journal article
Language: en
Open access: closed
Locations: Circulation Research (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords: TNF-α, endothelial nitric oxide synthase, constitutive nitric oxide synthase, mRNA stability, mRNA degradation, human umbilical vein endothelial cells, atherosclerosis, cycloheximide, gene transcription
MeSH terms: Amino Acid Oxidoreductases, Base Sequence, Endothelium, Vascular, Half-Life, Humans, Molecular Sequence Data, RNA, Messenger, Transcription, Genetic, Tumor Necrosis Factor-alpha, Umbilical Veins, Down-Regulation, Polymerase Chain Reaction, Nitric Oxide Synthase

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Tumor necrosis factor downregulates an endothelial nitric oxide synthase mRNA by shortening its half-life

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