On the dynamics of nitrite, nitrate and other biomarkers of nitric oxide production in inflammatory bowel disease
Abstract
Nitrite and nitrate are frequently used surrogate markers of nitric oxide (NO) production. Using rat models of acute and chronic DSS-induced colitis we examined the applicability of these and other NO-related metabolites, in tissues and blood, for the characterization of inflammatory bowel disease. Global NO dynamics were assessed by simultaneous quantification of nitrite, nitrate, nitroso and nitrosyl species over time in multiple compartments. NO metabolite levels were compared to a composite disease activity index (DAI) and contrasted with measurements of platelet aggregability, ascorbate redox status and the effects of 5-aminosalicylic acid (5-ASA). Nitroso products in the colon and in other organs responded in a manner consistent with the DAI. In contrast, nitrite and nitrate, in both intra- and extravascular compartments, exhibited variations that were not always in step with the DAI. Extravascular nitrite, in particular, demonstrated significant temporal instabilities, ranging from systemic drops to marked increases. The latter was particularly evident after cessation of the inflammatory stimulus and accompanied by profound ascorbate oxidation. Treatment with 5-ASA effectively reversed these fluctuations and the associated oxidative and nitrosative stress. Platelet activation was enhanced in both the acute and chronic model. Our results offer a first glimpse into the systemic nature of DSS-induced inflammation and reveal a greater complexity of NO metabolism than previously envisioned, with a clear dissociation of nitrite from other markers of NO production. The remarkable effectiveness of 5-ASA to abrogate the observed pattern of nitrite instability suggests a hitherto unrecognized role of this molecule in either development or resolution of inflammation. Its possible link to tissue oxygen consumption and the hypoxia that tends to accompany the inflammatory process warrants further investigation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Tissue nitrite levels are repleted within four days after DSS withdrawal.
“tissue nitrite levels were repleted within four days after DSS withdrawal that may or may not be associated with chronic inflammation.”
From Inorganic nitrite therapy: historical perspective and future directions (2011) · cites this paper as [234]
5-aminosalicylic acid attenuates depletion of colon tissue nitrite levels, increases systemic nitrite levels, and reduces oxidative stress during DSS colitis.
“the effects of 5-aminosalicylic acid (5-ASA- an anti-inflammatory agent for the treatment of inflammatory bowel disease) attenuated depletion of colon tissue nitrite levels, increased systemic nitrite levels, and oxidative stress during DSS colitis.”
From Inorganic nitrite therapy: historical perspective and future directions (2011) · cites this paper as [234]
The development of DSS colitis involves an early loss of colon tissue nitrite levels with a concomitant increase in systemic nitrite.
“This study found that the development of DSS colitis involves an early loss of colon tissue nitrite levels with a concomitant increase in systemic nitrite.”
From Inorganic nitrite therapy: historical perspective and future directions (2011) · cites this paper as [234]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics
Lundberg, J. O., Weitzberg, E., & Gladwin, M. T. (2008) · Nature Reviews Drug Discovery · doi:10.1038/nrd2466 · Cited by 2,739 · cited 1× · see citing works
“that it is a biochemically and pharmacologically active molecule [7–12] and that its levels are maintained within a tight concentration range (200–500 nM) across many mammalian species [13], suggesting”
BackgroundOkayasu, I., Hatakeyama, S., Yamada, M., Ohkusa, T., Inagaki, Y., & NAKAYA, R. (1990) · Gastroenterology · doi:10.1016/0016-5085(90)90290-h · Cited by 2,405 · see citing works
Clinicopathologic study of dextran sulfate sodium experimental acute colitis
Shichijo, K., Matuu, M., Ikeda, Y., Naito, S., Ito, M., & Sekine, I. (1998) · The Japanese Journal of Pharmacology · doi:10.1016/s0021-5198(19)41298-5 · Cited by 1,943 · see citing works
Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity
Krawisz, J. E., Sharon, P., & Stenson, W. F. (1984) · Gastroenterology · doi:10.1016/0016-5085(84)90202-6 · Cited by 1,770 · see citing works
NF-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α
Rius, J., Guma, M., Schachtrup, C., Akassoglou, K., Zinkernagel, A. S., Nizet, V., Johnson, R. S., Haddad, G. G., & Karin, M. (2008) · Nature · doi:10.1038/nature06905 · Cited by 1,614 · see citing works
Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils
Eiserich, J. P., Hristova, M., Cross, C. E., Jones, A. D., Freeman, B. A., Halliwell, B., & van der Vliet, A. (1998) · Nature · doi:10.1038/34923 · Cited by 1,496 · see citing works
Guzy, R. D., & Schumacker, P. T. (2006) · Experimental Physiology · doi:10.1113/expphysiol.2006.033506 · Cited by 881 · see citing works
Intragastric nitric oxide production in humans: measurements in expelled air.
Lundberg, J. O., Weitzberg, E., Lundberg, J. M., & Alving, K. (1994) · Gut · doi:10.1136/gut.35.11.1543 · Cited by 661 · see citing works
Determination of nitrite/nitrate in human biological material by the simple Griess reaction
Guevara, I., Iwanejko, J., Dembinska-Kiec, A., Pankiewicz, J. E., Wanat, A., Anna, P., Leszczynska-Golabek, I., Bartuś, S., Malczewska-Malec, M., & Szczudlik, A. (1998) · Clinica Chimica Acta · doi:10.1016/s0009-8981(98)00060-6 · Cited by 647 · see citing works
Vascular Complications of Inflammatory Bowel Disease
Talbot, R. W., Heppell, J. P., Dozois, R. R., & Beart, R. W. (1986) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(12)65200-8 · Cited by 623 · see citing works
Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals
Kleinbongard, P., Dejam, A., Lauer, T., Rassaf, T., Schindler, A., Picker, O., Scheeren, T., Gödecke, A., Schrader, J., Schulz, R., et al. (2003) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(03)00406-4 · Cited by 586 · see citing works
Self-citationSinger, I., Kawka, D. W., Scott, S., Weidner, J., Mumford, R., Riehl, T. E., & Stenson, W. F. (1996) · Gastroenterology · doi:10.1016/s0016-5085(96)70055-0 · Cited by 584 · see citing works
Velayos, F. S., Terdiman, J. P., & Walsh, J. M. E. (2005) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2005.41442.x · Cited by 546 · see citing works
Nitric oxide in inflammatory bowel disease: a universal messenger in an unsolved puzzle
Kolios, G. C., Valatas, V., & Ward, S. G. (2004) · Immunology · doi:10.1111/j.1365-2567.2004.01984.x · Cited by 541 · see citing works
Rousseaux, C., Lefebvre, B., Dubuquoy, L., Lefèbvre, P., Romano, O., Auwerx, J. H., METZGER, D., Wahli, W., Desvergne, B., Naccari, G. C., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20041948 · Cited by 528 · see citing works
Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues
Bryan, N. S., Fernandez, B. O., Bauer, S. M., Garcia-Saura, M. F., Milsom, A. B., Rassaf, T., Maloney, R. E., Bharti, A., Rodriguez, J., & Feelisch, M. (2005) · Nature Chemical Biology · doi:10.1038/nchembio734 · Cited by 518 · see citing works
Self-citationMammalian Nitric Oxide Synthases
Stuehr, D. J., & Griffith, O. W. (1992) · Advances in enzymology and related areas of molecular biology/Advances in enzymology and related subjects · doi:10.1002/9780470123119.ch8 · Cited by 507 · see citing works
Is inflammatory bowel disease an independent and disease specific risk factor for thromboembolism?
Miehsler, W., Reinisch, W., Valic, E., Osterode, W., Tillinger, W., Feichtenschlager, T., Grisar, J., Machold, K. P., Scholz, S., Vogelsang, H., et al. (2004) · Gut · doi:10.1136/gut.2003.025411 · Cited by 470 · see citing works
T cell transfer model of chronic colitis: concepts, considerations, and tricks of the trade
Ostanin, D. V., Bao, J. R., Koboziev, I., Gray, L. T., Robinson-Jackson, S. A., Kosloski-Davidson, M., Price, V. H., & Grisham, M. B. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90462.2008 · Cited by 444 · see citing works
Nitrite as Regulator of Hypoxic Signaling in Mammalian Physiology
van Faassen, E. E., Bahrami, S., Feelisch, M., Hogg, N., Kelm, M., Kim‐Shapiro, D. B., Kozlov, A. V., Li, H., Lundberg, J. O., Mason, R., et al. (2009) · Medicinal Research Reviews · doi:10.1002/med.20151 · Cited by 435 · see citing works
Self-citationFeelisch, M., Rassaf, T., Mnaimneh, S., Singh, N., Bryan, N. S., Jourd'Heuil, D., & Kelm, M. (2002) · The FASEB Journal · doi:10.1096/fj.02-0363com · Cited by 401 · see citing works
Self-citationBryan, N. S., Rassaf, T., Maloney, R. E., Rodriguez, C. M., Saijo, F., Rodriguez, J. R., & Feelisch, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306706101 · Cited by 400 · see citing works
Self-citationExtraintestinal manifestations in inflammatory bowel disease
Danese, S. (2005) · World Journal of Gastroenterology · doi:10.3748/wjg.v11.i46.7227 · Cited by 373 · see citing works
NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response?
Schopfer, F. J. (2003) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2003.10.006 · Cited by 369 · see citing works
Rachmilewitz, D., Stamler, J. S., Bachwich, D. R., Karmeli, F., Ackerman, Z., & Podolsky, D. K. (1995) · Gut · doi:10.1136/gut.36.5.718 · Cited by 365 · see citing works
Mean platelet volume: a useful marker of inflammatory bowel disease activity
Kapsoritakis, A. N., Koukourakis, M. I., Sfiridaki, A., Potamianos, S. P., Kosmadaki, M. G., Κoutroubakis, I. E., & Kouroumalis, E. (2001) · The American Journal of Gastroenterology · doi:10.1016/s0002-9270(00)02414-x · Cited by 358 · see citing works
Venous Thromboembolism in Inflammatory Bowel Disease
Solem, C. A., Loftus, E. V., Tremaine, W. J., & Sandborn, W. J. (2004) · The American Journal of Gastroenterology · doi:10.1046/j.1572-0241.2003.04026.x · Cited by 316 · see citing works
Hypoxia and gastrointestinal disease
Taylor, C. T., & Colgan, S. P. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-007-0277-z · Cited by 313 · see citing works
Kihara, N., de la Fuente, S. G., Fujino, K., Takahashi, T., Pappas, T. N., & Mantyh, C. R. (2003) · Gut · doi:10.1136/gut.52.5.713 · Cited by 301 · see citing works
Whiteman, M., & Moore, P. K. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00645.x · Cited by 261 · see citing works
Signal transduction by reactive oxygen species in non-phagocytic cells
Finkel, T. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.65.3.337 · Cited by 256 · see citing works
Platelets in Inflammatory Bowel Disease: Clinical, Pathogenic, and Therapeutic Implications
Danese, S., de la Motte, C., & Fiocchi, C. (2004) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2004.04129.x · Cited by 253 · see citing works
Kimura, H., Hokari, R., Miura, S., Shigematsu, T., Hirokawa, M., Akiba, Y., Kurose, I., Higuchi, H., Fujimori, H., Tsuzuki, Y., et al. (1998) · Gut · doi:10.1136/gut.42.2.180 · Cited by 250 · see citing works
An <i>S</i> -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
Platelets circulate in an activated state in inflammatory bowel disease
Collins, C. E., Cahill, M. R., Newland, A. C., & Rampton, D. S. (1994) · Gastroenterology · doi:10.1016/0016-5085(94)90741-2 · Cited by 226 · see citing works
Dijkstra, G. D. H., Moshage, H. J., van Dullemen, H. M., de Jager-Krikken, A., Tiebosch, A. T. M. G., Kleibeuker, J. H., Jansen, P. L. M., & van Goor, H. (1998) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(199812)186:4 · Cited by 223 · see citing works
Nitric Oxide, Cytochrome C Oxidase, and the Cellular Response to Hypoxia
Taylor, C. T., & Moncada, S. (2010) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.108.181628 · Cited by 220 · see citing works
Oxidation and Nitrosation of Thiols at Low Micromolar Exposure to Nitric Oxide
Jourd’heuil, D., Jourd’heuil, F. L., & Feelisch, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300203200 · Cited by 194 · see citing works
Self-citationTherapeutic Uses of Inorganic Nitrite and Nitrate: From the Past to the Future
Butler, A. R., & Feelisch, M. (2008) · Circulation · doi:10.1161/circulationaha.107.753814 · Cited by 184 · see citing works
Self-citationStucchi, A. F., Shofer, S. L., Leeman, S. E., Materne, O. L. J., Beer, E. R., McClung, J. P., Shebani, K. O., Moore, F., O’Brien, M. J., & Becker, J. M. (2000) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2000.279.6.g1298 · Cited by 174 · see citing works
Terada, M., Watanabe, Y., Kunitomo, M., & Hayashi, E. (1978) · Analytical Biochemistry · doi:10.1016/0003-2697(78)90083-0 · Cited by 165 · see citing works
Kimura, H., Miura, S., Shigematsu, T., Ohkubo, N., Tsuzuki, Y., Kurose, I., Higuchi, H., Akiba, Y., Hokari, R., Hirokawa, M., et al. (1997) · Digestive Diseases and Sciences · doi:10.1023/a:1018849405922 · Cited by 164 · see citing works
Togawa, J.-I., Nagase, H., Tanaka, K., Inamori, M., Nakajima, A., Ueno, N., Saito, T., & Sekihara, H. (2002) · Journal of Gastroenterology and Hepatology · doi:10.1046/j.1440-1746.2002.02868.x · Cited by 133 · see citing works
Impact of Dextran Sulfate Sodium Load on the Severity of Inflammation in Experimental Colitis
Vowinkel, T., Kalogeris, T. J., Mori, M., Krieglstein, C. F., & Granger, D. N. (2004) · Digestive Diseases and Sciences · doi:10.1023/b:ddas.0000026298.72088.f7 · Cited by 129 · see citing works
Self-citationNitric oxide and superoxide: Interference with hypoxic signaling
Brüne, B., & ZHOU, J. (2007) · Cardiovascular Research · doi:10.1016/j.cardiores.2007.03.005 · Cited by 126 · see citing works
Altered Ascorbic Acid Status in the Mucosa from Inflammatory Bowel Disease Patients
Buffinton, G. D., & Doe, W. F. (1995) · Free Radical Research · doi:10.3109/10715769509147535 · Cited by 122 · see citing works
EFFECTS OF DIET ON MEASUREMENT OF NITRIC OXIDE METABOLITES
Wang, J., Brown, M. A., Tarn, S. H., Chan, M. C., & Whitworth, J. A. (1997) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.1997.tb01212.x · Cited by 113 · see citing works
Osman, N., Adawi, D., Ahrné, S., Jeppsson, B. W., & Molin, G. (2004) · Digestive Diseases and Sciences · doi:10.1023/b:ddas.0000017459.59088.43 · Cited by 106 · see citing works
Bacteriological studies of experimental ulcerative colitis
Onderdonk, A. B., & Bartlett, J. (1979) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/32.1.258 · Cited by 96 · see citing works
Myocardial protection by nitrite
Calvert, J. W., & Lefer, D. J. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp079 · Cited by 82 · see citing works
Nitrite uptake and metabolism and oxidant stress in human erythrocytes
May, J. M., Qu, Z., Li, X., & Cobb, C. E. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.279.6.c1946 · Cited by 82 · see citing works
Herulf, M. (1998) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365529850166897 · Cited by 78 · see citing works
Expression of nitric oxide synthase in ulcerative colitis
Godkin, A. J., de Belder, A., VILLA, L., WONG, A., Beesley, J. E., Kane, S. P., & Martin, J. (1996) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1996.tb02131.x · Cited by 76 · see citing works
Distribution of inducible nitric oxide synthase in ulcerative colitis.
Ikeda, I., Kasajima, T., Ishiyama, S., Shimojo, T., Takeo, Y., Nishikawa, T., Kameoka, S., Hiroe, M., & Mitsunaga, A. (1997) · PubMed · Cited by 76 · see citing works
Murthy, Cooper, Yoshitake, Meyer, Meyer, & Murthy (1999) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.1999.00457.x · Cited by 75 · see citing works
Tsikas, D., Gutzki, F., & Stichtenoth, D. O. (2005) · European Journal of Clinical Pharmacology · doi:10.1007/s00228-005-0020-z · Cited by 72 · see citing works
Inflammatory bowel disease stimulates formation of carcinogenic N -nitroso compounds: Table 1
de Kok, T. M. C. M., Engels, L. G. J. B., Moonen, E. J. C., & Kleinjans, J. C. S. (2005) · Gut · doi:10.1136/gut.2004.057471 · Cited by 67 · see citing works
Cheng, Y. (2005) · World Journal of Gastroenterology · doi:10.3748/wjg.v11.i3.309 · Cited by 63 · see citing works
Nitrite from inflammatory cells—A cancer risk factor in ulcerative colitis?
Roediger, W. E. W., Lawson, M. J., & Radcliffe, B. C. (1990) · Diseases of the Colon & Rectum · doi:10.1007/bf02139219 · Cited by 61 · see citing works
Guihot, G., Guimbaud, R., Bertrand, V., Narcy-Lambare, B., Couturier, D., Duée, P., Chaussade, S., & Blachier, F. (2000) · Amino Acids · doi:10.1007/s007260050020 · Cited by 60 · see citing works
Role of Blood- and Tissue-Associated Inducible Nitric-Oxide Synthase in Colonic Inflammation
Krieglstein, C. F., Anthoni, C., Cerwinka, W. H., Stokes, K. Y., Russell, J., Grisham, M. B., & Granger, D. N. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.060594 · Cited by 57 · see citing works
Self-citationThromboembolism-an Important Manifestation of Inflammatory Bowel Disease
Quera, R., & Shanahan, F. (2004) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2004.40923.x · Cited by 57 · see citing works
Nikolaus, S., Fölscn, U., & Schreiber, S. (2000) · PubMed · Cited by 53 · see citing works
Comparison of methods for determination of ascorbic acid in animal tissues
Carr, R. S., Bally, M. B., Thomas, P., & Neff, J. M. (1983) · Analytical Chemistry · doi:10.1021/ac00259a012 · Cited by 51 · see citing works
Increased aggregation response of platelets in patients with inflammatory bowel disease
Andoh, A., Yoshida, T., Yagi, Y., Bamba, S., Hata, K., Tsujikawa, T., Kitoh, K., Sasaki, M., & Fujiyama, Y. (2006) · Journal of Gastroenterology · doi:10.1007/s00535-005-1721-x · Cited by 50 · see citing works
Ahn, B., Ko, K., Oh, T., Cho, H., Kim, W. B., Lee, K., Cho, S. W., & Hahm, K. (2001) · International Journal of Colorectal Disease · doi:10.1007/s003840000282 · Cited by 48 · see citing works
The anti-oxidant properties of 5-aminosalicylic acid
Pearson, D. C., Jourd’heuil, D., & Meddings, J. B. (1996) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(96)00031-7 · Cited by 41 · see citing works
Aoi, Y., Terashima, S., Ogura, M., Nishio, H., Kato, S., & Takeuchi, K. (2008) · PubMed · Cited by 38 · see citing works
Taniguchi, E., Matsunami, M., Kimura, T., Yonezawa, D., Ishiki, T., Sekiguchi, F., Nishikawa, H., Maeda, Y., Ishikura, H., & Kawabata, A. (2009) · Toxicology · doi:10.1016/j.tox.2009.07.018 · Cited by 32 · see citing works
Grisham, M. B., & Miles, A. M. (1994) · Biochemical Pharmacology · doi:10.1016/0006-2952(94)90320-4 · Cited by 27 · see citing works
Rumi, G., Tsubouchi, R., Nishio, H., Kato, S., Mózsik, G., & Takeuchi, K. (2004) · PubMed · Cited by 26 · see citing works
Resolving the nitric oxide paradox in acute tissue damage
Billiar, T., & Harbrecht, B. G. (1997) · Gastroenterology · doi:10.1053/gast.1997.v113.agast971131405 · Cited by 25 · see citing works
Reynolds, P. D., Middleton, S. J., Hansford, G. M., & Hunter, J. O. (1997) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-199705000-00010 · Cited by 24 · see citing works
Garcia-Saura, M. F., Fernandez, B. O., McAllister, B. P., Whitlock, D. R., Cruikshank, W. W., & Feelisch, M. (2010) · Journal of Investigative Dermatology · doi:10.1038/jid.2009.303 · Cited by 8 · see citing works
Self-citation
Flagged first, then by citations
1 of the 75 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Graves, D. B. (2012) · Journal of Physics D Applied Physics · doi:10.1088/0022-3727/45/26/263001 · Cited by 1,512 · see citing works
Oxidative Stress and Redox-Modulating Therapeutics in Inflammatory Bowel Disease
Bourgonje, A. R., Feelisch, M., Faber, K. N., Pasch, A., Dijkstra, G. D. H., & van Goor, H. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.06.006 · Cited by 399 · see citing works
Self-citationBurger, D. E., & Touyz, R. M. (2012) · Journal of the American Society of Hypertension · doi:10.1016/j.jash.2011.11.003 · Cited by 212 · see citing works
A designed whole-cell biosensor for live diagnosis of gut inflammation through nitrate sensing
Woo, S., Moon, S., Kim, S. K., Kim, T. H., Lim, H. S., Yeon, G.-H., Sung, B. H., Lee, C., Lee, S., Hwang, J. H., et al. (2020) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2020.112523 · Cited by 117 · see citing works
Inorganic nitrite therapy: historical perspective and future directions
Kevil, C. G., Kolluru, G. K., Pattillo, C. B., & Giordano, T. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.04.042 · Cited by 113 · see citing works
Ferrante, C., Recinella, L., Ronci, M., Menghini, L., Brunetti, L., Chiavaroli, A., Leone, S., Di Iorio, L., Carradori, S., Tirillini, B., et al. (2019) · Food and Chemical Toxicology · doi:10.1016/j.fct.2019.01.035 · Cited by 99 · see citing works
Schicho, R., Nazyrova, A., Shaykhutdinov, R. A., Duggan, G. E., Vogel, H. J., & Storr, M. (2010) · Journal of Proteome Research · doi:10.1021/pr100547y · Cited by 96 · see citing works
Bourgonje, A. R., Klóska, D., Grochot‐Przeczek, A., Feelisch, M., Cuadrado, A., & van Goor, H. (2023) · Redox Biology · doi:10.1016/j.redox.2023.102603 · Cited by 95 · see citing works
Self-citationShi, L., Lin, Q., Li, X., Nie, Y., Sun, S., Deng, X., Wang, L., Lu, J., Tang, Y., & Luo, F. (2017) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201601013 · Cited by 93 · see citing works
Tenuta, M. C., Deguin, B., Loizzo, M. R., Dugay, A., Acquaviva, R., Malfa, G. A., Bonesi, M., Bouzidi, C., & Tundis, R. (2020) · Antioxidants · doi:10.3390/antiox9020184 · Cited by 84 · see citing works
Amrouche-Mekkioui, I., & Djerdjouri, B. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.06.014 · Cited by 81 · see citing works
Suriyaprom, S., Srisai, P., Intachaisri, V., Kaewkod, T., Pekkoh, J., Desvaux, M., & Tragoolpua, Y. (2023) · Molecules · doi:10.3390/molecules28114395 · Cited by 79 · see citing works
Zengin, G., Ferrante, C., Orlando, G., Zheleva‐Dimitrova, D., Gevrenova, R., Recinella, L., Chiavaroli, A., Leone, S., Brunetti, L., Aumeeruddy, M. Z., et al. (2019) · Journal of Food Biochemistry · doi:10.1111/jfbc.13003 · Cited by 78 · see citing works
Nitric oxide deficiency is a primary driver of hypertension
Bryan, N. S. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.115325 · Cited by 77 · see citing works
Self-citationShi, L., Lin, Q., Yang, T., Nie, Y., Li, X., Liu, B., Shen, J., Liang, Y., Tang, Y., & Luo, F. (2016) · Food & Function · doi:10.1039/c6fo01043a · Cited by 73 · see citing works
The impact of gut microbiota metabolites on cellular bioenergetics and cardiometabolic health
Tomášová, L., Grman, M., Ondriaš, K., & Ufnal, M. (2021) · Nutrition & Metabolism · doi:10.1186/s12986-021-00598-5 · Cited by 58 · see citing works
Shinu, P., Sharma, M., Gupta, G. L., Mujwar, S., Kandeel, M. K., Kumar, M., Nair, A. B., Goyal, M., Addanki, P. S., Attimarad, M., et al. (2022) · Molecules · doi:10.3390/molecules27206905 · Cited by 52 · see citing works
Chemistry meets biology in colitis-associated carcinogenesis
Mangerich, A., Dedon, P. C., Fox, J. G., Tannenbaum, S. R., & Wogan, G. N. (2013) · Free Radical Research · doi:10.3109/10715762.2013.832239 · Cited by 51 · see citing works
Chichiriccò, G., Ferrante, C., Menghini, L., Recinella, L., Leone, S., Chiavaroli, A., Brunetti, L., Simone, S. C. D., Ronci, M., Piccone, P., et al. (2019) · Food and Chemical Toxicology · doi:10.1016/j.fct.2019.01.040 · Cited by 48 · see citing works
Endothelial Dysfunction and Coronary Artery Disease
Veerasamy, M., Bagnall, A. J., Neely, D., Allen, J., Sinclair, H., & Kunadian, V. (2014) · Cardiology in Review · doi:10.1097/crd.0000000000000047 · Cited by 45 · see citing works
Tun, X., Yasukawa, K., & Yamada, K. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.06.020 · Cited by 39 · see citing works
An integrated approach to assessing nitroso-redox balance in systemic inflammation
Dyson, A., Bryan, N. S., Fernandez, B. O., Garcia-Saura, M. F., Saijo, F., Mongardon, N., Rodríguez, J., Singer, M., & Feelisch, M. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.06.012 · Cited by 38 · see citing works
Self-citationGenetically engineered bacteria as inflammatory bowel disease therapeutics
Zou, Z., Zhang, X.-P., Zhang, Q., Yin, B., Zhou, Y. Q., & Ye, B. (2024) · Engineering Microbiology · doi:10.1016/j.engmic.2024.100167 · Cited by 32 · see citing works
Ferrante, C., Recinella, L., Ronci, M., Orlando, G., Simone, S. C. D., Brunetti, L., Chiavaroli, A., Leone, S., Politi, M., Tirillini, B. B., et al. (2019) · Phytotherapy Research · doi:10.1002/ptr.6429 · Cited by 31 · see citing works
Nitric Oxide and its Metabolites in the Critical Phase of Illness: Rapid Biomarkers in the Making
Mian, A. I., Aranke, M., & Bryan, N. S. (2013) · The Open Biochemistry Journal · doi:10.2174/1874091x01307010024 · Cited by 26 · see citing works
Self-citationTenuta, M. C., Loizzo, M. R., Tundis, R., Dugay, A., Bouzidi, C., Marie, A., Acquaviva, R., Cappello, A. R., & Deguin, B. (2023) · Food & Function · doi:10.1039/d3fo02987e · Cited by 22 · see citing works
Zengin, G., Ferrante, C., Şenkardeş, İ., Gevrenova, R., Zheleva‐Dimitrova, D., Menghini, L., Orlando, G., Recinella, L., Chiavaroli, A., Leone, S., et al. (2019) · Food and Chemical Toxicology · doi:10.1016/j.fct.2019.03.041 · Cited by 22 · see citing works
Björnsson, B., Winbladh, A., Bojmar, L., Sundqvist, T., Gullstrand, P., & Sandström, P. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i28.9506 · Cited by 20 · see citing works
Yang, Z., Du, C., Chang, Z., Yang, Y., & Hu, L. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1612223 · Cited by 19 · see citing works
Pinheiro, L. C., Ferreira, G. C., de Angelis, C. D., Toledo, J. C., & Tanus-Santos, J. E. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.03.006 · Cited by 19 · see citing works
Dextran sulfate sodium-induced acute colitis impairs dermal lymphatic function in mice
Agollah, G. D. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i45.12767 · Cited by 14 · see citing works
Wang, W., Liu, Z., Yue, W., Zhu, L., Zhong, H., Yang, C., He, T., Wan, P., & Geng, J. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.875238 · Cited by 12 · see citing works
Pulmonary functions in children with inflammatory bowel disease
Gut, G., Ben‐Tov, A., Lahad, A., Soferman, R., Cohen, S., Tauman, R., & Sivan, Y. (2016) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000000606 · Cited by 9 · see citing works
Zengin, G., Ferrante, C., Menghini, L., Orlando, G., Brunetti, L., Recinella, L., Chiavaroli, A., Leone, S., Ronci, M., Aumeeruddy, M. Z., et al. (2019) · Journal of Food Biochemistry · doi:10.1111/jfbc.12766 · Cited by 8 · see citing works
Touyz, R. M., & Burger, D. E. (2012) · Springer eBooks · doi:10.1007/978-88-470-2601-8_19 · Cited by 8 · see citing works
Dissanayake, W. M. N., Ch, M. R., Lee, S., Heo, J. M., & Yi, Y. (2023) · Animal Bioscience · doi:10.5713/ab.23.0052 · Cited by 6 · see citing works
SILVA, J. K., Verás, A. C. C., Sousa, S. G. D. C., Albuquerque, J. S. S., Ribeiro, F. P. B., Lima, N. K. S., NASCIMENTO, L. B. S., Alves, R. R. D. V., Aires, R. S., Coelho, L. C. B. B., et al. (2024) · Anais da Academia Brasileira de Ciências · doi:10.1590/0001-3765202420231266 · Cited by 6 · see citing works
Molecular topology: a strategy to identify novel compounds against ulcerative colitis
Gálvez-Llompart, M., Recio, M. C., García‐Domenech, R., & Gálvez, J. (2016) · Molecular Diversity · doi:10.1007/s11030-016-9706-7 · Cited by 5 · see citing works
Lima-Silva, A. K., Rebelo, M. A., Barros, A. C., Conde-Tella, S. O., & Tanus-Santos, J. E. (2024) · Antioxidants · doi:10.3390/antiox13030255 · Cited by 4 · see citing works
Sharma, V., Gupta, G. L., & Sharma, M. (2023) · Current Drug Delivery · doi:10.2174/1567201820666230308100040 · Cited by 2 · see citing works
Stevens, J. L., McKenna, H., Minnion, M., Murray, A. J., Feelisch, M., & Martín, D. (2025) · Experimental Biology and Medicine · doi:10.3389/ebm.2025.10254 · Cited by 1 · see citing works
Self-citationAlamri, M. A., Soliman, G. A., Alamri, M. A., Abdel-Rahman, R. F., Alhalabi, A. W., Almahmoud, R. S., Alsagheir, I. M., Alharbi, A. G., & Abdel-Kader, M. S. (2025) · Scientific Reports · doi:10.1038/s41598-025-26010-3 · Cited by 1 · see citing works
Terriac, L., Alsabi, K., Patingre, E., Tertrin, E., Maugars, Y., Garnier, C., Hélesbeux, J., & Delplace, V. (2026) · Biomaterials Science · doi:10.1039/d5bm01473e · Cited by 1 · see citing works
Nitric oxide and inducible nitric oxide synthase levels in EE and NERD patients.
Pish‐Kenari, F. N., Qujeq, D., Bonahi, S. S. M., Kashifard, M., & Hajian‐Tilaki, K. (2022) · Gastroenterology and hepatology from bed to bench. · Cited by 1 · see citing works
Lee, W.-H., Do, S., Shin, J., & Kim, S. (2025) · Food Science and Biotechnology · doi:10.1007/s10068-025-01850-x · Cited by 1 · see citing works
Mohammadi, E., Qujeq, D., Taheri, H., & Hajian‐Tilaki, K. (2018) · Annals of Colorectal Research · doi:10.5812/acr.64029
Experimental Biology and Medicine Volume 250 Issue 3
(2025) · Frontiers Media SA eBooks · doi:10.3389/978-2-8325-6281-9
Mango Fruit Contribution to Human Nutrition and Health
Celis, M. E. M., & Yahia, E. M. (2026) · Botany, production and uses. · doi:10.1079/9781800622647.0024
Enwere, M., Bryan, N. S., Onu, A., Neufeld, M., Hussein, M. T. E., Yakub, I., Omale, C., Onyedike, O., Atim, T., Agbeyomi, O. A., et al. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1904698
Self-citation
- Authors
- Saijo, F., Milsom, A. B., Bryan, N. S., Bauer, S. M., Vowinkel, T., Ivanovic, M., Andry, C., Granger, D. N., Rodriguez, J., & Feelisch, M.
- Affiliations
- Boston University (US)
- Louisiana State University (US)
- Corresponding author
- Feelisch, Martin
- Venue
- Nitric Oxide
- Publisher
- Elsevier BV
- Published
- 2010-02
- Volume
- 22
- Issue
- 2
- Pages
- 155-167
- ISSN
- 1089-8603 (ISSN-L)
- OpenAlex
- W2004445259
- Cited by
- 51
- References
- 75
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 3 · 2023: 5 · 2022: 4 · 2021: 1 · 2020: 5 · 2019: 6 · 2018: 2 · 2017: 1 · 2016: 3 · 2015: 1 · 2014: 3 · 2013: 2 · 2012: 4
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nitric Oxide (publishedVersion)
- PubMed (publishedVersion)
- Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
- ePrints Soton (University of Southampton) (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL-69029, R01HL069029)
- National Center for Research Resources (P20RR16456, P20RR016456)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- nitrite, nitrate, nitric oxide metabolites, inflammatory bowel disease, DSS-induced colitis, nitroso compounds, disease activity index, platelet aggregation, 5-aminosalicylic acid, oxidative stress, nitrosative stress, inflammation resolution, tissue oxygen consumption, hypoxia
- MeSH terms
- Animals, Disease Models, Animal, Male, Nitrates, Nitric Oxide, Nitrites, Inflammatory Bowel Diseases, Biomarkers, Rats, Wistar, Mesalamine, Rats
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
