Targeting inducible Nitric Oxide Synthase (iNOS) in the prevention of vascular damage and cardiac inflammation in CVD
Nafees Uddin Chowdhurya, Abida Tishab, Juthika Sarkerb, Pulak Dev Nathb, Nowshin Ahmedb, Shahanshah Abdullahb, Tasdik Farooqb, Waich Mahmudb, Md. Mohabbulla Mohibb,c, Md. Abu Taher Sagorb
Journal of Angiotherapy 2(1) 067-077 https://doi.org/10.25163/angiotherapy.1200032116160818
Submitted: 01 June 2018 Revised: 15 August 2018 Published: 16 August 2018
Abstract
Vascular damage and subsequent cardiac failure due to immune cytokines is steadily increasing the morbidity of cardiovascular diseases (CVD), making them the leading cause of death globally. Nevertheless, improper diagnosis is an important hurdle in case management. Free radicals are one of major factors in producing vascular abnormalities in CVD. Additionally, some other factors such as high blood pressure, myocardial injuries, vascular damage, ventricular hypertrophy, cardiac fibrosis and myocardial necrosis are also the results of free radical-mediated abnormal cardiac activity/function. Of note, Nitric Oxide Synthase (iNOS) is produced in the body at an elevated rate in the presence of free radicals which has been shown to lead to cardiac issues. Furthermore, iNOS is also increased due to cytoplasmic stress, faulty DNA replication and membrane potential impairment. Moreover, abnormal cardiac rhythm has also been reported to be linked to the presence of iNOS. iNOS can also lead to abnormal cardiac function through inhibition of mitochondrial activity and production of pro-inflammatory cytokines. The molecular mechanism of iNOS that leads to CVD is comprehensively summarized in this review so as to aid in drug discovery strategies for the treatment of CVD.
Key words: iNOS, Immunity, Inflammation, Hypertension, vascular damage
References
Abdelsalam, R. M., & Safar, M. M. (2015). Neuroprotective effects of vildagliptin in rat rotenone Parkinson's disease model: role of RAGE-NFκB and Nrf2-antioxidant signaling pathways. Journal of neurochemistry, 133(5), 700-707.
https://doi.org/10.1111/jnc.13087
PMid:25752913
Abu Taher Sagor, M. Angiotensin-II, a potent peptide, participates in the development of hepatic dysfunctions. Immunology, Endocrine & Metabolic Agents in Medicinal Chemistry, 16, 1-17.
Abu Taher Sagor, M., Mahmud Reza, H., Tabassum, N., Sikder, B., Ulla, A., Subhan, N., . . . Ashraful Alam, M. (2016). Supplementation of rosemary leaves (Rosmarinus officinalis) powder attenuates oxidative stress, inflammation and fibrosis in carbon tetrachloride (CCl4) treated rats. Current Nutrition & Food Science, 12(4), 288-295.
https://doi.org/10.2174/1573401312666160816154610
Aktan, F. (2004). iNOS-mediated nitric oxide production and its regulation. Life sciences, 75(6), 639-653.
https://doi.org/10.1016/j.lfs.2003.10.042
PMid:15172174
Alam, M. A., Chowdhury, M. R. H., Jain, P., Sagor, M. A. T., & Reza, H. M. (2015). DPP-4 inhibitor sitagliptin prevents inflammation and oxidative stress of heart and kidney in two kidney and one clip (2K1C) rats. Diabetology & metabolic syndrome, 7(1), 107.
https://doi.org/10.1186/s13098-015-0095-3
PMid:26609328 PMCid:PMC4658771
Alderton, W. K., Cooper, C. E., & Knowles, R. G. (2001). Nitric oxide synthases: structure, function and inhibition. Biochemical Journal, 357(3), 593-615.
https://doi.org/10.1042/0264-6021:3570593
https://doi.org/10.1042/bj3570593
PMid:11463332 PMCid:PMC1221991
Ali, A., Kaur, G., Hamid, H., Abdullah, T., Ali, M., Niwa, M., & Alam, M. (2003). Terminoside A, a new triterpene glycoside from the bark of Terminalia arjuna inhibits nitric oxide production in murine macrophages. Journal of Asian natural products research, 5(2), 137-142.
https://doi.org/10.1080/1028602031000066834
PMid:12765198
Anavi, S., Eisenberg-Bord, M., Hahn-Obercyger, M., Genin, O., Pines, M., & Tirosh, O. (2015). The role of iNOS in cholesterol-induced liver fibrosis. Laboratory investigation, 95(8), 914.
https://doi.org/10.1038/labinvest.2015.67
PMid:26097999
Asano, K., Chee, C., Gaston, B., Lilly, C. M., Gerard, C., Drazen, J. M., & Stamler, J. S. (1994). Constitutive and inducible nitric oxide synthase gene expression, regulation, and activity in human lung epithelial cells. Proceedings of the National Academy of Sciences, 91(21), 10089-10093.
https://doi.org/10.1073/pnas.91.21.10089
AT Sagor, M., M Mohib, M., S Azam, M., Rahman, A., T Tanmoy, F., K Chowdhury, W., . . . A Alam, M. (2016). Angiotensin-II, a Potent Peptide, Participates in the Development of Hepatic Dysfunctions. Immunology, Endocrine & Metabolic Agents in Medicinal Chemistry (Formerly Current Medicinal Chemistry-Immunology, Endocrine and Metabolic Agents), 16(3), 161-177.
Bae, U.-J., Song, M.-Y., Jang, H.-Y., Lim, J. M., Lee, S. Y., Ryu, J.-H., & Park, B.-H. (2015). Emodin isolated from Rheum palmatum prevents cytokine-induced β-cell damage and the development of type 1 diabetes. Journal of Functional Foods, 16, 9-19.
https://doi.org/10.1016/j.jff.2015.04.016
Ballantyne, C. M., & Nambi, V. (2005). Markers of inflammation and their clinical significance. Atherosclerosis Supplements, 6(2), 21-29.
https://doi.org/10.1016/j.atherosclerosissup.2005.02.005
PMid:15823493
Baynosa, R. C., Naig, A. L., Murphy, P. S., Fang, X. H., Stephenson, L. L., Khiabani, K. T., . . . Zamboni, W. A. (2013). The effect of hyperbaric oxygen on nitric oxide synthase activity and expression in ischemia-reperfusion injury. journal of surgical research, 183(1), 355-361.
https://doi.org/10.1016/j.jss.2013.01.004
PMid:23485074
Cabrera-Fuentes, H. A., Ruiz-Meana, M., Simsekyilmaz, S., Kostin, S., Inserte, J., Saffarzadeh, M., . . . Barreto, G. (2014). RNase1 prevents the damaging interplay between extracellular RNA and tumour necrosis factor-α in cardiac ischaemia/reperfusion injury. Thrombosis & Haemostasis, 112(6), 1110-1119.
https://doi.org/10.1160/th14-08-0703
PMid:25354936
Chan, E. D., Chan, J., & Schluger, N. W. (2001). What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge. American journal of respiratory cell and molecular biology, 25(5), 606-612.
https://doi.org/10.1165/ajrcmb.25.5.4487
PMid:11713103
Charles, I. G., Palmer, R., Hickery, M. S., Bayliss, M. T., Chubb, A. P., Hall, V. S., . . . Moncada, S. (1993). Cloning, characterization, and expression of a cDNA encoding an inducible nitric oxide synthase from the human chondrocyte. Proceedings of the National Academy of Sciences, 90(23), 11419-11423.
https://doi.org/10.1073/pnas.90.23.11419
Chen, B.-Y., Lin, D. P.-C., Wu, C.-Y., Teng, M.-C., Sun, C.-Y., Tsai, Y.-T., . . . Chang, H.-H. (2011). Dietary zerumbone prevents mouse cornea from UVB-induced photokeratitis through inhibition of NF-κB, iNOS, and TNF-α expression and reduction of MDA accumulation.
Cho, H. J., Xie, Q., Calaycay, J., Mumford, R. A., Swiderek, K. M., Lee, T. D., & Nathan, C. (1992). Calmodulin is a subunit of nitric oxide synthase from macrophages. Journal of experimental medicine, 176(2), 599-604.
https://doi.org/10.1084/jem.176.2.599
PMid:1380065
Chow, B. S. M., Chew, E. G. Y., Zhao, C., Bathgate, R. A., Hewitson, T. D., & Samuel, C. S. (2012). Relaxin signals through a RXFP1-pERK-nNOS-NO-cGMP-dependent pathway to up-regulate matrix metalloproteinases: the additional involvement of iNOS. PloS one, 7(8), e42714.
https://doi.org/10.1371/journal.pone.0042714
PMid:22936987 PMCid:PMC3425563
Chowdhury, N. U., Farooq, T., Abdullah, S., Mahadi, A. S., Hasan, M. M., Paran, T. Z., . . . Alam, M. A. (2016). Matrix Metalloproteinases (MMP), a Major Responsible Downstream Signaling Molecule for Cellular Damage-A Review. Molecular Enzymology and Drug Targets.
https://doi.org/10.21767/2572-5475.10019
Costa, M. A., Elesgaray, R., Caniffi, C., Fellet, A., Mac Laughlin, M., & Arranz, C. (2010). Role of nitric oxide as a key mediator on cardiovascular actions of atrial natriuretic peptide in spontaneously hypertensive rats. American Journal of Physiology-Heart and Circulatory Physiology, 298(3), H778-H786.
https://doi.org/10.1152/ajpheart.00488.2009
PMid:19783776
Crump, C., Sundquist, J., Winkleby, M. A., & Sundquist, K. (2017). Interactive effects of obesity and physical fitness on risk of ischemic heart disease. International journal of obesity (2005), 41(2), 255.
https://doi.org/10.1038/ijo.2016.209
PMid:27867205 PMCid:PMC5296285
Csont, T., Viappiani, S., Sawicka, J., Slee, S., Altarejos, J. Y., Batinic-Haberle, I., & Schulz, R. (2005). The involvement of superoxide and iNOS-derived NO in cardiac dysfunction induced by pro-inflammatory cytokines. Journal of molecular and cellular cardiology, 39(5), 833-840.
https://doi.org/10.1016/j.yjmcc.2005.07.010
PMid:16171809
Daff, S., Sagami, I., & Shimizu, T. (1999). The 42-amino acid insert in the FMN domain of neuronal nitric-oxide synthase exerts control over Ca2+/calmodulin-dependent electron transfer. Journal of Biological Chemistry, 274(43), 30589-30595.
https://doi.org/10.1074/jbc.274.43.30589
PMid:10521442
Das, A., Xi, L., & Kukreja, R. C. (2005). Phosphodiesterase-5 inhibitor sildenafil preconditions adult cardiac myocytes against necrosis and apoptosis Essential role of nitric oxide signaling. Journal of Biological Chemistry, 280(13), 12944-12955.
https://doi.org/10.1074/jbc.M404706200
PMid:15668244
Das, S., Alagappan, V. K., Bagchi, D., Sharma, H. S., Maulik, N., & Das, D. K. (2005). Coordinated induction of iNOS–VEGF–KDR–eNOS after resveratrol consumption: A potential mechanism for resveratrol preconditioning of the heart. Vascular pharmacology, 42(5), 281-289.
https://doi.org/10.1016/j.vph.2005.02.013
PMid:15905131
Depre, C., Havaux, X., Renkin, J., Vanoverschelde, J. L. J., & Wijns, W. (1999). Expression of inducible nitric oxide synthase in human coronary atherosclerotic plaque. Cardiovascular research, 41(2), 465-472.
https://doi.org/10.1016/S0008-6363(98)00304-6
Depré, C., Wijns, W., Robert, A. M., Renkin, J. P., & Havaux, X. (1997). Pathology of unstable plaque: correlation with the clinical severity of acute coronary syndromes. Journal of the American College of Cardiology, 30(3), 694-702.
https://doi.org/10.1016/S0735-1097(97)00213-1
Dhillon, S. S., Mastropaolo, L. A., Murchie, R., Griffiths, C., Thöni, C., Elkadri, A., . . . Guo, C. (2014). Higher activity of the inducible nitric oxide synthase contributes to very early onset inflammatory bowel disease. Clinical and translational gastroenterology, 5(1), e46.
https://doi.org/10.1038/ctg.2013.17
PMid:24430113 PMCid:PMC3912315
Dias, A. S., Porawski, M., Alonso, M., Marroni, N., Collado, P. S., & González-Gallego, J. (2005). Quercetin decreases oxidative stress, NF-κB activation, and iNOS overexpression in liver of streptozotocin-induced diabetic rats. The Journal of nutrition, 135(10), 2299-2304.
https://doi.org/10.1093/jn/135.10.2299
PMid:16177186
Dwivedi, S. (2007). Terminalia arjuna Wight & Arn.—a useful drug for cardiovascular disorders. Journal of Ethnopharmacology, 114(2), 114-129.
https://doi.org/10.1016/j.jep.2007.08.003
PMid:17875376
Eckel, R. H. (1997). Obesity and heart disease. Circulation, 96(9), 3248-3250.
https://doi.org/10.1161/01.CIR.96.9.3248
PMid:9386201
Eggers, K. M., Oldgren, J., Nordenskjöld, A., & Lindahl, B. (2004). Diagnostic value of serial measurement of cardiac markers in patients with chest pain: limited value of adding myoglobin to troponin I for exclusion of myocardial infarction. American heart journal, 148(4), 574-581.
https://doi.org/10.1016/j.ahj.2004.04.030
PMid:15459585
Escames, G., Khaldy, H., León, J., González, L., & Acu-a-Castroviejo, D. (2004). Changes in iNOS activity, oxidative stress and melatonin levels in hypertensive patients treated with lacidipine. Journal of hypertension, 22(3), 629-635.
https://doi.org/10.1097/00004872-200403000-00027
PMid:15076170
Ferrari, P. F., Palmieri, D., Casazza, A. A., Aliakbarian, B., Perego, P., & Palombo, D. (2015). TNFα-induced endothelial activation is counteracted by polyphenol extract from UV-stressed cyanobacterium Arthrospira platensis. Medicinal Chemistry Research, 24(1), 275-282.
https://doi.org/10.1007/s00044-014-1126-6
Ferreiro, C. R., Chagas, A. C. P., Carvalho, M. H. C., Dantas, A. P., Jatene, M. B., de Souza, L. C. B., & da Luz, P. L. (2001). Influence of hypoxia on nitric oxide synthase activity and gene expression in children with congenital heart disease: a novel pathophysiological adaptive mechanism. Circulation, 103(18), 2272-2276.
https://doi.org/10.1161/01.CIR.103.18.2272
PMid:11342476
Fukumura, D., Gohongi, T., Kadambi, A., Izumi, Y., Ang, J., Yun, C.-O., . . . Jain, R. K. (2001). Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proceedings of the National Academy of Sciences, 98(5), 2604-2609.
https://doi.org/10.1073/pnas.041359198
PMid:11226286 PMCid:PMC30185
Funakoshi, H., Kubota, T., Kawamura, N., Machida, Y., Feldman, A. M., Tsutsui, H., . . . Takeshita, A. (2002). Disruption of inducible nitric oxide synthase improves β-adrenergic inotropic responsiveness but not the survival of mice with cytokine-induced cardiomyopathy. Circulation research, 90(9), 959-965.
https://doi.org/10.1161/01.RES.0000017632.83720.68
PMid:12016261
Funakoshi, H., Kubota, T., Machida, Y., Kawamura, N., Feldman, A. M., Tsutsui, H., . . . Takeshita, A. (2002). Involvement of inducible nitric oxide synthase in cardiac dysfunction with tumor necrosis factor-α. American Journal of Physiology-Heart and Circulatory Physiology, 282(6), H2159-H2166.
https://doi.org/10.1152/ajpheart.00872.2001
PMid:12003824
Gupta, A., Rhodes, G. J., Berg, D. T., Gerlitz, B., Molitoris, B. A., & Grinnell, B. W. (2007). Activated protein C ameliorates LPS-induced acute kidney injury and downregulates renal INOS and angiotensin 2. American Journal of Physiology-Renal Physiology, 293(1), F245-F254.
https://doi.org/10.1152/ajprenal.00477.2006
PMid:17409278
Ham, Y.-M., Ko, Y.-J., Song, S.-M., Kim, J., Kim, K.-N., Yun, J.-H., . . . Yoon, W.-J. (2015). Anti-inflammatory effect of litsenolide B2 isolated from Litsea japonica fruit via suppressing NF-κB and MAPK pathways in LPS-induced RAW264. 7 cells. Journal of functional foods, 13, 80-88.
https://doi.org/10.1016/j.jff.2014.12.031
Haywood, G. A., Tsao, P. S., Heiko, E., Mann, M. J., Keeling, P. J., Trindade, P. T., . . . Bishopric, N. H. (1996). Expression of inducible nitric oxide synthase in human heart failure. Circulation, 93(6), 1087-1094.
https://doi.org/10.1161/01.CIR.93.6.1087
PMid:8653828
Heger, J., Gödecke, A., Flögel, U., Merx, M. W., Molojavyi, A., Kühn-Velten, W. N., & Schrader, J. (2002). Cardiac-specific overexpression of inducible nitric oxide synthase does not result in severe cardiac dysfunction. Circulation research, 90(1), 93-99.
https://doi.org/10.1161/hh0102.102757
PMid:11786524
Heron, M., & Anderson, R. N. (2016). Changes in the leading cause of death: recent patterns in heart disease and cancer mortality. Cancer, 400(500,000), 600,000.
Heymes, C., Bendall, J. K., Ratajczak, P., Cave, A. C., Samuel, J.-L., Hasenfuss, G., & Shah, A. M. (2003). Increased myocardial NADPH oxidase activity in human heart failure. Journal of the American College of Cardiology, 41(12), 2164-2171.
https://doi.org/10.1016/S0735-1097(03)00471-6
Ishibashi, M., Hiasa, K.-i., Zhao, Q., Inoue, S., Ohtani, K., Kitamoto, S., . . . Kura, S. (2004). Critical role of monocyte chemoattractant protein-1 receptor CCR2 on monocytes in hypertension-induced vascular inflammation and remodeling. Circulation research, 94(9), 1203-1210.
https://doi.org/10.1161/01.RES.0000126924.23467.A3
PMid:15059935
Islam, M. N., Choi, R. J., Jin, S. E., Kim, Y. S., Ahn, B. R., Zhao, D., . . . Choi, J. S. (2012). Mechanism of anti-inflammatory activity of umbelliferone 6-carboxylic acid isolated from Angelica decursiva. Journal of ethnopharmacology, 144(1), 175-181.
https://doi.org/10.1016/j.jep.2012.08.048
PMid:22981803
Islam, M. N., Ishita, I. J., Jin, S. E., Choi, R. J., Lee, C. M., Kim, Y. S., . . . Choi, J. S. (2013). Anti-inflammatory activity of edible brown alga Saccharina japonica and its constituents pheophorbide a and pheophytin a in LPS-stimulated RAW 264.7 macrophage cells. Food and Chemical Toxicology, 55, 541-548.
https://doi.org/10.1016/j.fct.2013.01.054
PMid:23402855
Janakiram, N. B., & Rao, C. V. (2012). iNOS-selective inhibitors for cancer prevention: promise and progress. Future medicinal chemistry, 4(17), 2193-2204.
https://doi.org/10.4155/fmc.12.168
PMid:23190107 PMCid:PMC3588580
Janssen-Heininger, Y. M., Macara, I., & Mossman, B. T. (1999). Cooperativity between Oxidants and Tumor Necrosis Factor in the Activation of Nuclear Factor (NF)-κ B: Requirement of Ras/Mitogen-Activated Protein Kinases in the Activation of NF-κ B by Oxidants. American journal of respiratory cell and molecular biology, 20(5), 942-952.
https://doi.org/10.1165/ajrcmb.20.5.3452
PMid:10226064
Jiang, Q., Elson-Schwab, I., Courtemanche, C., & Ames, B. N. (2000). γ-Tocopherol and its major metabolite, in contrast to α-tocopherol, inhibit cyclooxygenase activity in macrophages and epithelial cells. Proceedings of the National Academy of Sciences, 97(21), 11494-11499.
https://doi.org/10.1073/pnas.200357097
PMid:11005841 PMCid:PMC17228
Jin, M., Suh, S.-J., Yang, J. H., Lu, Y., Kim, S. J., Kwon, S., . . . Ahn, G. W. (2010). Anti-inflammatory activity of bark of Dioscorea batatas DECNE through the inhibition of iNOS and COX-2 expressions in RAW264. 7 cells via NF-κB and ERK1/2 inactivation. Food and chemical toxicology, 48(11), 3073-3079.
https://doi.org/10.1016/j.fct.2010.07.048
PMid:20691245
Jung, H. A., Jin, S. E., Ahn, B. R., Lee, C. M., & Choi, J. S. (2013). Anti-inflammatory activity of edible brown alga Eisenia bicyclis and its constituents fucosterol and phlorotannins in LPS-stimulated RAW264. 7 macrophages. Food and Chemical Toxicology, 59, 199-206.
https://doi.org/10.1016/j.fct.2013.05.061
PMid:23774261
Kapoor, D., Vijayvergiya, R., & Dhawan, V. (2014). Terminalia arjuna in coronary artery disease: ethnopharmacology, pre-clinical, clinical & safety evaluation. Journal of ethnopharmacology, 155(2), 1029-1045.
https://doi.org/10.1016/j.jep.2014.06.056
PMid:25014508
Kapur, S., Marcotte, B., & Marette, A. (1999). Mechanism of adipose tissue iNOS induction in endotoxemia. American Journal of Physiology-Endocrinology and Metabolism, 276(4), E635-E641.
https://doi.org/10.1152/ajpendo.1999.276.4.E635
Kengatharan, K. M., De Kimpe, S., Robson, C., Foster, S. J., & Thiemermann, C. (1998). Mechanism of gram-positive shock: identification of peptidoglycan and lipoteichoic acid moieties essential in the induction of nitric oxide synthase, shock, and multiple organ failure. Journal of Experimental Medicine, 188(2), 305-315.
https://doi.org/10.1084/jem.188.2.305
PMid:9670043
Keyes, K. T., Ye, Y., Lin, Y., Zhang, C., Perez-Polo, J. R., Gjorstrup, P., & Birnbaum, Y. (2010). Resolvin E1 protects the rat heart against reperfusion injury. American Journal of Physiology-Heart and Circulatory Physiology, 299(1), H153-H164.
https://doi.org/10.1152/ajpheart.01057.2009
PMid:20435846
Khan, M. I., Ostadhadi, S., Mumtaz, F., Momeny, M., Moghaddaskho, F., Hassanipour, M., . . . Dehpour, A. R. (2017). Thalidomide attenuates the development and expression of antinociceptive tolerance to μ-opioid agonist morphine through l-arginine-iNOS and nitric oxide pathway. Biomedicine & Pharmacotherapy, 85, 493-502.
https://doi.org/10.1016/j.biopha.2016.11.056
PMid:27899254
Khan, S., & Jena, G. (2014). Sodium butyrate, a HDAC inhibitor ameliorates eNOS, iNOS and TGF-β1-induced fibrogenesis, apoptosis and DNA damage in the kidney of juvenile diabetic rats. Food and chemical toxicology, 73, 127-139.
https://doi.org/10.1016/j.fct.2014.08.010
PMid:25158305
Khanduja, K. L., Sohi, K. K., Pathak, C. M., & Kaushik, G. (2006). Nimesulide inhibits lipopolysaccharide-induced production of superoxide anions and nitric oxide and iNOS expression in alveolar macrophages. Life sciences, 78(15), 1662-1669.
https://doi.org/10.1016/j.lfs.2005.07.033
PMid:16243362
Kibbe, M. R., Li, J., Nie, S., Watkins, S. C., Lizonova, A., Kovesdi, I., . . . Tzeng, E. (2000). Inducible nitric oxide synthase (iNOS) expression upregulates p21 and inhibits vascular smooth muscle cell proliferation through p42/44 mitogen-activated protein kinase activation and independent of p53 and cyclic guanosine monophosphate. Journal of vascular surgery, 31(6), 1214-1228.
https://doi.org/10.1067/mva.2000.105006
PMid:10842159
Korkmaz, B., Buharalioglu, K., Sahan-Firat, S., Cuez, T., Demiryurek, A. T., & Tunctan, B. (2011). Activation of MEK1/ERK1/2/iNOS/sGC/PKG pathway associated with peroxynitrite formation contributes to hypotension and vascular hyporeactivity in endotoxemic rats. Nitric Oxide, 24(3), 160-172.
https://doi.org/10.1016/j.niox.2011.02.004
PMid:21354320
Lechner, M., Lirk, P., & Rieder, J. (2005). Inducible nitric oxide synthase (iNOS) in tumor biology: the two sides of the same coin. Paper presented at the Seminars in cancer biology.
https://doi.org/10.1016/j.semcancer.2005.04.004
PMid:15914026
Lee, D.-H., Cho, H. J., Kim, J.-T., Choi, J. S., & Joo, C.-K. (2001). Expression of vascular endothelial growth factor and inducible nitric oxide synthase in pterygia. Cornea, 20(7), 738-742.
https://doi.org/10.1097/00003226-200110000-00013
PMid:11588427
Lee, H.-H., Paudel, K. R., & Kim, D.-W. (2015). Terminalia chebula fructus inhibits migration and proliferation of vascular smooth muscle cells and production of inflammatory mediators in RAW 264.7. Evidence-Based Complementary and Alternative Medicine, 2015.
Lee, J. K., Sayers, B. C., Chun, K.-S., Lao, H.-C., Shipley-Phillips, J. K., Bonner, J. C., & Langenbach, R. (2012). Multi-walled carbon nanotubes induce COX-2 and iNOS expression via MAP kinase-dependent and-independent mechanisms in mouse RAW264. 7 macrophages. Particle and fibre toxicology, 9(1), 14.
https://doi.org/10.1186/1743-8977-9-14
PMid:22571318 PMCid:PMC3485091
Li, X., Ye, X., Li, X., Sun, X., Liang, Q., Tao, L., . . . Chen, J. (2011). Salidroside protects against MPP+-induced apoptosis in PC12 cells by inhibiting the NO pathway. Brain research, 1382, 9-18.
https://doi.org/10.1016/j.brainres.2011.01.015
PMid:21241673
Li, Y., Shen, L., & Luo, H. (2016). Luteolin ameliorates dextran sulfate sodium-induced colitis in mice possibly through activation of the Nrf2 signaling pathway. Int Immunopharmacol, 40, 24-31.
https://doi.org/10.1016/j.intimp.2016.08.020
https://doi.org/10.1016/j.intimp.2016.01.027
Lim, H.-W., Kumar, H., Kim, B.-W., More, S. V., Kim, I.-W., Park, J.-I., . . . Choi, D.-K. b-Asarone (cis-2, 4, 5-trimethoxy-1-allyl phenyl), attenuates pro-inflammatory mediators by inhibiting NF-jB signaling and the JNK pathway in LPS activated BV-2 microglia cells.
Liu, F.-q., Zhang, X.-l., Gong, L., Wang, X.-p., Wang, J., Hou, X.-g., . . . Zhang, Y. (2011). Glucagon-like peptide 1 protects microvascular endothelial cells by inactivating the PARP-1/iNOS/NO pathway. Molecular and cellular endocrinology, 339(1-2), 25-33.
https://doi.org/10.1016/j.mce.2011.03.007
PMid:21458523
Liu, X.-m., Peyton, K. J., Wang, X., & Durante, W. (2012). Sildenafil stimulates the expression of gaseous monoxide-generating enzymes in vascular smooth muscle cells via distinct signaling pathways. Biochemical pharmacology, 84(8), 1045-1054.
https://doi.org/10.1016/j.bcp.2012.07.023
PMid:22864061 PMCid:PMC3487387
Loh, S. Y., Giribabu, N., & Salleh, N. (2017). Changes in plasma aldosterone and electrolytes levels, kidney epithelial sodium channel (ENaC) and blood pressure in normotensive WKY and hypertensive SHR rats following gonadectomy and chronic testosterone treatment. Steroids.
https://doi.org/10.1016/j.steroids.2017.09.008
PMid:28954214
Lowenstein, C. J., & Padalko, E. (2004). iNOS (NOS2) at a glance. Journal of cell science, 117(14), 2865-2867.
https://doi.org/10.1242/jcs.01166
PMid:15197240
Luoma, J. S., Strålin, P., Marklund, S. L., Hiltunen, T. P., Särkioja, T., & Ylä-Herttuala, S. (1998). Expression of extracellular SOD and iNOS in macrophages and smooth muscle cells in human and rabbit atherosclerotic lesions: colocalization with epitopes characteristic of oxidized LDL and peroxynitrite-modified proteins. Arteriosclerosis, thrombosis, and vascular biology, 18(2), 157-167.
https://doi.org/10.1161/01.ATV.18.2.157
MacMicking, J., Xie, Q.-w., & Nathan, C. (1997). Nitric oxide and macrophage function. Annual review of immunology, 15(1), 323-350.
https://doi.org/10.1146/annurev.immunol.15.1.323
PMid:9143691
MacMicking, J. D., North, R. J., LaCourse, R., Mudgett, J. S., Shah, S. K., & Nathan, C. F. (1997). Identification of nitric oxide synthase as a protective locus against tuberculosis. Proceedings of the National Academy of Sciences, 94(10), 5243-5248.
https://doi.org/10.1073/pnas.94.10.5243
Marumo, T., Nakaki, T., Hishikawa, K., Hirahashi, J., Suzuki, H., Kato, R., & Saruta, T. (1995). Natriuretic peptide-augmented induction of nitric oxide synthase through cyclic guanosine 3', 5'-monophosphate elevation in vascular smooth muscle cells. Endocrinology, 136(5), 2135-2142.
https://doi.org/10.1210/endo.136.5.7536663
PMid:7536663
Mayer, B., & Hemmens, B. (1997). Biosynthesis and action of nitric oxide in mammalian cells. Trends in biochemical sciences, 22(12), 477-481.
https://doi.org/10.1016/S0968-0004(97)01147-X
Metwaly, H., Ebrahem, M. A.-M., & Saku, T. (2014). Vascular endothelial growth factor (VEGF) and inducible nitric oxide synthase (iNOS) in oral lichen planus: An immunohistochemical study for the correlation between vascular and inflammatory reactions. Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology, 26(3), 390-396.
https://doi.org/10.1016/j.ajoms.2013.09.009
Mogensen, J., Murphy, R. T., Shaw, T., Bahl, A., Redwood, C., Watkins, H., . . . McKenna, W. J. (2004). Severe disease expression of cardiac troponin C and T mutations in patients with idiopathic dilated cardiomyopathy. Journal of the American College of Cardiology, 44(10), 2033-2040.
https://doi.org/10.1016/j.jacc.2004.08.027
PMid:15542288
Mohib, M. M., Afnan, K., Paran, T. Z., Khan, S., Sarker, J., Hasan, N., . . . Sagor, M. A. T. (2017). Beneficial Role of Citrus Fruit Polyphenols Against Hepatic Dysfunctions: A Review. Journal of dietary supplements, 1-29.
Mohib, M. M., Hasan, I., Chowdhury, W. K., Chowdhury, N. U., Mohiuddin, S., Sagor, M. A. T., . . . Alam, M. A. (2016). Role of angiotensin ii in hepatic inflammation through MAPK pathway: A review. Hepatitis.
Mohib, M. M., Rabby, S. F., Paran, T. Z., Hasan, M. M., Ahmed, I., Hasan, N., . . . Mohiuddin, S. (2016). Protective role of green tea on diabetic nephropathy—A review. Cogent Biology, 2(1), 1248166.
Mohib, M. M., Rabby, S. M. F., Paran, T. Z., Hasan, M. M., Ahmed, I., Hasan, N., . . . Hsu, T.-C. (2016). Protective role of green tea on diabetic nephropathy -A review. Cogent Biology, 1248166. doi:10.1080/23312025.2016.1248166
https://doi.org/10.1080/23312025.2016.1248166
Müller-Werdan, U., Schumann, H., Fuchs, R., Reithmann, C., Loppnow, H., Koch, S., . . . Jungblut, P. (1997). Tumor Necrosis Factorα (TNFα) is Cardiodepressant in Pathophysiologically Relevant Concentrations Without Inducing Inducible Nitric Oxide-(NO)-Synthase (iNOS) or Triggering Serious Cytotoxicity. Journal of molecular and cellular cardiology, 29(11), 2915-2923.
https://doi.org/10.1006/jmcc.1997.0526
PMid:9405166
Mungrue, I. N., Gros, R., You, X., Pirani, A., Azad, A., Csont, T., . . . Husain, M. (2002a). Cardiomyocyte overexpression of iNOS in mice results in peroxynitrite generation, heart block, and sudden death. The Journal of clinical investigation, 109(6), 735-743.
https://doi.org/10.1172/JCI0213265
PMid:11901182 PMCid:PMC150906
Mungrue, I. N., Gros, R., You, X., Pirani, A., Azad, A., Csont, T., . . . Husain, M. (2002b). Cardiomyocyte overexpression of iNOS in mice results in peroxynitrite generation, heart block, and sudden death. The Journal of clinical investigation, 109(6), 735.
https://doi.org/10.1172/JCI0213265
PMid:11901182 PMCid:PMC150906
Nathan, C. (1992). Nitric oxide as a secretory product of mammalian cells. The FASEB journal, 6(12), 3051-3064.
https://doi.org/10.1096/fasebj.6.12.1381691
PMid:1381691
Padureanu, V., Enescu, A. S., Silosi, I., Fortofoiu, M., Enescu, A., Bogdan, M., . . . Mita, A. (2017). The association between chronic pancreatitis and the iNOS-2087A> G polymorphism. Romanian Journal of Internal Medicine, 55(2), 89-95.
https://doi.org/10.1515/rjim-2017-0009
PMid:28125406
Palmer, J., Guillard, F., Laurijssens, B., Wentz, A., Dixon, R., & Williams, P. (2009). A randomised, single-blind, placebo-controlled, adaptive clinical trial of GW274150, a selective iNOS inhibitor, in the treatment of acute migraine. Cephalalgia, 29(1), 124.
Papapetropoulos, A., García-Carde-a, G., Madri, J. A., & Sessa, W. C. (1997). Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. The Journal of clinical investigation, 100(12), 3131-3139.
https://doi.org/10.1172/JCI119868
PMid:9399960 PMCid:PMC508526
Piplani, H., Vaish, V., & Sanyal, S. N. (2012). Dolastatin 15, a mollusk linear peptide, and Celecoxib, a selective cyclooxygenase-2 inhibitor, prevent preneoplastic colonic lesions and induce apoptosis through inhibition of the regulatory transcription factor NF-κB and an inflammatory protein, iNOS. European Journal of Cancer Prevention, 21(6), 511-522.
https://doi.org/10.1097/CEJ.0b013e328351c69d
PMid:22441428
Ramlagan, P., Rondeau, P., Planesse, C., Neergheen-Bhujun, V. S., Fawdar, S., Bourdon, E., & Bahorun, T. (2017). Punica granatum L. mesocarp suppresses advanced glycation end products (AGEs)-and H 2 O 2-induced oxidative stress and pro-inflammatory biomarkers. Journal of Functional Foods, 29, 115-126.
https://doi.org/10.1016/j.jff.2016.12.007
Rasoanaivo, P., Wright, C. W., Willcox, M. L., & Gilbert, B. (2011). Whole plant extracts versus single compounds for the treatment of malaria: synergy and positive interactions. Malaria Journal, 10(1), S4.
https://doi.org/10.1186/1475-2875-10-S1-S4
PMid:21411015 PMCid:PMC3059462
Rodrigues, J. P. F., Caldas, I. S., Gonçalves, R. V., Almeida, L. A., Souza, R. L. M., & Novaes, R. D. (2017). S. mansoni-T. cruzi co-infection modulates arginase-1/iNOS expression, liver and heart disease in mice. Nitric Oxide, 66, 43-52.
https://doi.org/10.1016/j.niox.2017.02.013
PMid:28268114
Romano, B., Pagano, E., Orlando, P., Capasso, R., Cascio, M. G., Pertwee, R., . . . Borrelli, F. (2016). Pure Δ 9-tetrahydrocannabivarin and a Cannabis sativa extract with high content in Δ 9-tetrahydrocannabivarin inhibit nitrite production in murine peritoneal macrophages. Pharmacological Research, 113, 199-208.
https://doi.org/10.1016/j.phrs.2016.07.045
PMid:27498155
Ryu, S., Shin, J.-S., Cho, Y.-W., Kim, H. K., Paik, S. H., Lee, J. H., . . . Lee, K.-T. (2013). Fimasartan, anti-hypertension drug, suppressed inducible nitric oxide synthase expressions via nuclear factor-kappa B and activator protein-1 inactivation. Biological and Pharmaceutical Bulletin, 36(3), 467-474.
https://doi.org/10.1248/bpb.b12-00859
PMid:23449332
Sagor, M. A. T., Mohib, M., Tabassum, N., Ahmed, I., & Reza, H. (2016). Fresh seed supplementation of Syzygium cumini attenuated oxidative stress, inflammation, fibrosis, iron overload, hepatic dysfunction and renal injury in acetaminophen induced rats. Journal of Drug Metabolism & Toxicology, 7(2).
Sagor, M. A. T., Tabassum, N., Potol, M. A., & Alam, M. A. (2015). Xanthine oxidase inhibitor, allopurinol, prevented oxidative stress, fibrosis, and myocardial damage in isoproterenol induced aged rats. Oxidative medicine and cellular longevity, 2015.
https://doi.org/10.1155/2015/478039
PMid:26137187 PMCid:PMC4475550
Sagor, M. A. T., Tabassum, N., Potol, M. A., & Alam, M. A. (2015). Xanthine Oxidase Inhibitor, Allopurinol, Prevented Oxidative Stress, Fibrosis, and Myocardial Damage in Isoproterenol Induced Aged Rats. Oxidative Medicine and Cellular Longevity, 2015, 9. doi:10.1155/2015/478039
https://doi.org/10.1155/2015/478039
Salerno, J. C., Harris, D. E., Irizarry, K., Patel, B., Morales, A. J., Smith, S. M., . . . Jones, C. L. (1997). An autoinhibitory control element defines calcium-regulated isoforms of nitric oxide synthase. Journal of Biological Chemistry, 272(47), 29769-29777.
https://doi.org/10.1074/jbc.272.47.29769
PMid:9368047
Salvemini, D., Nucci, G., Sneddon, J. M., & Vane, J. R. (1989). Superoxide anions enhance platelet adhesion and aggregation. British journal of pharmacology, 97(4), 1145-1150.
https://doi.org/10.1111/j.1476-5381.1989.tb12572.x
PMid:2551440 PMCid:PMC1854596
Sangartit, W., Pakdeechote, P., Kukongviriyapan, V., Donpunha, W., Shibahara, S., & Kukongviriyapan, U. (2016). Tetrahydrocurcumin in combination with deferiprone attenuates hypertension, vascular dysfunction, baroreflex dysfunction, and oxidative stress in iron-overloaded mice. Vascular Pharmacology, 87, 199-208.
https://doi.org/10.1016/j.vph.2016.10.001
PMid:27713040
Sarady, J. K., Zuckerbraun, B. S., Bilban, M., Wagner, O., Usheva, A., Liu, F., . . . Otterbein, L. E. (2004). Carbon monoxide protection against endotoxic shock involves reciprocal effects on iNOS in the lung and liver. The FASEB journal, 18(7), 854-856.
https://doi.org/10.1096/fj.03-0643fje
PMid:15001560
Satoh, M., Nakamura, M., Tamura, G., Makita, S., Segawa, I., Tashiro, A., . . . Hiramori, K. (1997). Inducible nitric oxide synthase and tumor necrosis factor-alpha in myocardium in human dilated cardiomyopathy. Journal of the American College of Cardiology, 29(4), 716-724.
https://doi.org/10.1016/S0735-1097(96)00567-0
Seccombe, J. F., Pearson, P. J., & Schaff, H. V. (1994). Oxygen radical—mediated vascular injury selectively inhibits receptor-dependent release of nitric oxide from canine coronary arteries. The Journal of thoracic and cardiovascular surgery, 107(2), 505-509.
PMid:8302070
Seo, S., Shin, J.-S., Lee, W.-S., Rhee, Y. K., Cho, C.-W., Hong, H.-D., & Lee, K.-T. (2017). Anti-colitis effect of Lactobacillus sakei K040706 via suppression of inflammatory responses in the dextran sulfate sodium-induced colitis mice model. Journal of Functional Foods, 29, 256-268.
https://doi.org/10.1016/j.jff.2016.12.045
Shabeeh, H., Khan, S., Jiang, B., Brett, S., Melikian, N., Casadei, B., . . . Shah, A. M. (2017). Blood Pressure in Healthy Humans Is Regulated by Neuronal NO SynthaseNovelty and Significance. Hypertension, 69(5), 970-976.
https://doi.org/10.1161/HYPERTENSIONAHA.116.08792
PMid:28264923 PMCid:PMC5389591
Shimabukuro, M., Ohneda, M., Lee, Y., & Unger, R. H. (1997). Role of nitric oxide in obesity-induced beta cell disease. Journal of Clinical Investigation, 100(2), 290.
https://doi.org/10.1172/JCI119534
PMid:9218505 PMCid:PMC508191
Simsekyilmaz, S., Cabrera-Fuentes, H. A., Meiler, S., Kostin, S., Baumer, Y., Liehn, E. A., . . . Zernecke, A. (2013). The role of extracellular RNA in atherosclerotic plaque formation in mice. Circulation, CIRCULATIONAHA. 113.002562.
Sun, Y., Carretero, O. A., Xu, J., Rhaleb, N.-E., Wang, F., Lin, C., . . . Yang, X.-P. (2005). Lack of inducible NO synthase reduces oxidative stress and enhances cardiac response to isoproterenol in mice with deoxycorticosterone acetate–salt hypertension. Hypertension, 46(6), 1355-1361.
https://doi.org/10.1161/01.HYP.0000192651.06674.3f
PMid:16286571 PMCid:PMC4601605
Taylor, B. S., & Geller, D. A. (2000). Molecular regulation of the human inducible nitric oxide synthase (iNOS) gene. Shock (Augusta, Ga.), 13(6), 413-424.
https://doi.org/10.1097/00024382-200006000-00001
Tikellis, C., Thomas, M. C., Harcourt, B. E., Coughlan, M. T., Pete, J., Bialkowski, K., . . . Forbes, J. M. (2008). Cardiac inflammation associated with a Western diet is mediated via activation of RAGE by AGEs. American Journal of Physiology-Endocrinology and Metabolism, 295(2), E323-E330.
https://doi.org/10.1152/ajpendo.00024.2008
PMid:18477705 PMCid:PMC2652498
Vannini, F., Kashfi, K., & Nath, N. (2015). The dual role of iNOS in cancer. Redox biology, 6, 334-343.
https://doi.org/10.1016/j.redox.2015.08.009
PMid:26335399 PMCid:PMC4565017
Vejlstrup, N. G., Bouloumie, A., Boesgaard, S., Andersen, C. B., Nielsen-Kudsk, J. E., Mortensen, S. A., . . . Aldershvile, J. (1998). Inducible nitric oxide synthase (iNOS) in the human heart: expression and localization in congestive heart failure. Journal of molecular and cellular cardiology, 30(6), 1215-1223.
https://doi.org/10.1006/jmcc.1998.0686
PMid:9689595
Wang, W. Z., Fang, X. H., Stepheson, L. L., Khiabani, K. T., & Zamboni, W. A. (2004). NOS upregulation attenuates vascular endothelial dysfunction in the late phase of ischemic preconditioning in skeletal muscle. Journal of orthopaedic research, 22(3), 578-585.
https://doi.org/10.1016/j.orthres.2003.10.004
PMid:15099638
Westermann, D., Lindner, D., Kasner, M., Zietsch, C., Savvatis, K., Escher, F., . . . Riad, A. (2010). Cardiac inflammation contributes to changes in the extracellular matrix in patients with heart failure and normal ejection fraction. Circulation: Heart Failure, CIRCHEARTFAILURE. 109.931451.
Wever, R. M., Lüscher, T. F., Cosentino, F., & Rabelink, T. J. (1998). Atherosclerosis and the two faces of endothelial nitric oxide synthase. Circulation, 97(1), 108-112.
https://doi.org/10.1161/01.CIR.97.1.108
PMid:9443438
Wong, M.-L., Rettori, V., Amer, A.-S., Bongiorno, P. B., Canteros, G., McCann, S. M., . . . Licinio, J. (1996). Inducible nitric oxide synthase gene expression in the brain during systemic inflammation. Nature medicine, 2(5), 581-584.
https://doi.org/10.1038/nm0596-581
PMid:8616720
Xia, M., Ling, W. H., Ma, J., Kitts, D. D., & Zawistowski, J. (2003). Supplementation of diets with the black rice pigment fraction attenuates atherosclerotic plaque formation in apolipoprotein e deficient mice. The Journal of nutrition, 133(3), 744-751.
https://doi.org/10.1093/jn/133.3.744
PMid:12612147
Xia, X., Ling, W., Ma, J., Xia, M., Hou, M., Wang, Q., . . . Tang, Z. (2006). An anthocyanin-rich extract from black rice enhances atherosclerotic plaque stabilization in apolipoprotein E–deficient mice. The Journal of nutrition, 136(8), 2220-2225.
https://doi.org/10.1093/jn/136.8.2220
PMid:16857844
Xu, W., Charles, I. G., Moncada, S., Gorman, P., Sheer, D., Liu, L., & Emson, P. (1994). Mapping of the genes encoding human inducible and endothelial nitric oxide synthase (NOS2 and NOS3) to the pericentric region of chromosome 17 and to chromosome 7, respectively. Genomics, 21(2), 419-422.
https://doi.org/10.1006/geno.1994.1286
PMid:7522210
Xuan, Y.-T., Guo, Y., Han, H., Zhu, Y., & Bolli, R. (2001). An essential role of the JAK-STAT pathway in ischemic preconditioning. Proceedings of the National Academy of Sciences, 98(16), 9050-9055.
https://doi.org/10.1073/pnas.161283798
PMid:11481471 PMCid:PMC55371
Yang, B., Larson, D. F., & Watson, R. R. (2004). Modulation of iNOS activity in age-related cardiac dysfunction. Life sciences, 75(6), 655-667.
https://doi.org/10.1016/j.lfs.2003.09.076
PMid:15172175
Ying, L., & Hofseth, L. J. (2007). An emerging role for endothelial nitric oxide synthase in chronic inflammation and cancer. Cancer Research, 67(4), 1407-1410.
https://doi.org/10.1158/0008-5472.CAN-06-2149
PMid:17308075
Yoda, Y., Amagase, K., Kato, S., Tokioka, S., Murano, M., Kakimoto, K., . . . Higuchi, K. (2010). Prevention by lansoprazole, a proton pump inhibitor, of indomethacin-induced small intestinal ulceration in rats through induction of heme oxygenase-1. Journal of Physiology and Pharmacology, 61(3), 287.
PMid:20610858
Yu, G., Cheng, M., Wang, W., Zhao, R., & Liu, Z. (2017). Involvement of WNK1-mediated potassium channels in the sexual dimorphism of blood pressure. Biochemical and Biophysical Research Communications, 485(2), 255-260.
https://doi.org/10.1016/j.bbrc.2017.02.098
PMid:28237360
Yu, X. W., Chen, Q., Kennedy, R. H., & Liu, S. J. (2005). Inhibition of sarcoplasmic reticular function by chronic interleukin-6 exposure via iNOS in adult ventricular myocytes. The Journal of physiology, 566(2), 327-340.
https://doi.org/10.1113/jphysiol.2005.086686
https://doi.org/10.1113/jphysiol.2002.034223
PMid:15845578
Zhang, J., Peng, B., & Chen, X. (2005). Expressions of nuclear factor κB, inducible nitric oxide synthase, and vascular endothelial growth factor in adenoid cystic carcinoma of salivary glands: correlations with the angiogenesis and clinical outcome. Clinical Cancer Research, 11(20), 7334-
https://doi.org/10.1158/1078-0432.CCR-05-0241
PMid:16243805
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