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Therapeutic Application of Nitric Oxide in Human Diseases

  • NamKoong, Seung (Medical & Bio-Material Research Center and Department of Physical Therapy, College of Health and Welfare, Kangwon National University) ;
  • Kim, Young-Myeong (Vascular System Research Center and Department of Molecular and Cellular Biochemistry, School of Medicine, Kangwon National University)
  • Received : 2010.09.10
  • Accepted : 2010.10.05
  • Published : 2010.10.31

Abstract

Nitric oxide (NO), synthesized from L-arginine by three isoforms of NO synthase (NOS), is a gaseous signaling molecule with an astonishingly wide range of biological and pathophysiological activities, including vasorelaxation, angiogenesis, anti-inflammation, and anti-apoptosis in mammalian cells. Recent studies have shown that NO donors and inhaled NO convert to biologically active NO under biological conditions and act as a signaling molecule in pathophysiological conditions. This review will discuss the roles of NO and its potential therapeutic implication in various human diseases, such as tumor, vascular regeneration, hypertension, wound healing, and ischemia-reperfusion injury.

References

  1. Ahem, G. P., Klyachko, V. A. and Jackson, M. B. (2002). cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci. 25, 510-517. https://doi.org/10.1016/S0166-2236(02)02254-3
  2. Ahn, B. and Ohshima, H. (2001). Suppression of intestinal polyposis in Apc (Min/+) mice by inhibiting nitric oxide production. Cancer Res. 61, 8357-8360.
  3. Andrade, S. P., Hart, I. R. and Piper, P. J. (1992). Inhibitors of nitric oxide synthase selectively reduce flow in tumorassociated neovasculature. Br. J. Pharmacol. 107, 1092-1095. https://doi.org/10.1111/j.1476-5381.1992.tb13412.x
  4. Archer, S. L., Huang, J. M., Hampl, V., Nelson, D. P., Shultz, P. J. and Weir, E. K. (1994). Nitric oxide and cGMP cause vasorelaxation by activation of a charybdotoxin-sensitive K channel by cGMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA. 91, 7583-7587. https://doi.org/10.1073/pnas.91.16.7583
  5. Beghetti, M., Habre, W., Friedli, B. and Berner, M. (1995). Continuous low dose inhaled nitric oxide for treatment of severe pulmonary hypertension after cardiac surgery in paediatric patients. Br. Heart J. 73, 65-68. https://doi.org/10.1136/hrt.73.1.65
  6. Bell, R. M., Maddock, H. L. and Yellon, D. M. (2003). The cardioprotective and mitochondrial depolarising properties of exogenous nitric oxide in mouse heart. Cardiovasc. Res. 57, 405-415. https://doi.org/10.1016/S0008-6363(02)00675-2
  7. Brune, B., von Knethen, A. and Sandau, K. B. (1998). Nitric oxide and its role in apoptosis. Eur. J. Pharmacol. 351, 261-272. https://doi.org/10.1016/S0014-2999(98)00274-X
  8. Brune, B. and Zhou, J. (2007). Nitric oxide and superoxide: interference with hypoxic signaling. Cardiovasc. Res. 75, 275-282. https://doi.org/10.1016/j.cardiores.2007.03.005
  9. Chazotte-Aubert, L., Hainaut, P. and Ohshima, H. (2000). Nitric oxide nitrates tyrosine residues of tumor-suppressor p53 protein in MCF-7 cells. Biochem. Biophys. Res. Commun. 267, 609-613. https://doi.org/10.1006/bbrc.1999.2003
  10. Chinje, E. C. and Stratford, I. J. (1997). Role of nitric oxide in growth of solid tumours: a balancing act. Essays Biochem. 32, 61-72.
  11. Chung, B. H., Kim, J. D., Kim, C. K., Kim, J. H., Won, M. H., Lee, H. S., Dong, M. S., Ha, K. S., Kwon, Y. G. and Kim, Y. M. (2008). Icariin stimulates angiogenesis by activating the MEK/ERK- and PI3K/Akt/eNOS-dependent signal pathways in human endothelial cells. Biochem. Biophys. Res. Commun. 376, 404-408. https://doi.org/10.1016/j.bbrc.2008.09.001
  12. Chung, B. H., Lee, J. J., Kim, J. D., Jeoung, D., Lee, H., Choe, J., Ha, K. S., Kwon, Y. G. and Kim, Y. M. (2010). Angiogenic activity of sesamin through the activation of multiple signal pathways. Biochem. Biophys. Res. Commun. 391, 254-260. https://doi.org/10.1016/j.bbrc.2009.11.045
  13. Chung, H. T., Pae, H. O., Choi, B. M., Billiar, T. R. and Kim, Y. M. (2001). Nitric oxide as a bioregulator of apoptosis. Biochem. Biophys. Res. Commun. 282, 1075-1079. https://doi.org/10.1006/bbrc.2001.4670
  14. Cosby, K., Partovi, K. S., Crawford, J. H., Patel, R. P., Reiter, C. D., Martyr, S., Yang, B. K., Waclawiw, M. A., Zalos, G., Xu, X., Huang, K. T., Shields, H., Kim-Shapiro, D. B., Schechter, A. N., Cannon, R. O. 3rd and Gladwin, M. T. (2003). Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat. Med. 9, 1498-1505. https://doi.org/10.1038/nm954
  15. Dash, P. R., Cartwright, J. E., Baker, P. N., Johnstone, A. P. and Whitley, G. S. (2003). Nitric oxide protects human extravillous trophoblast cells from apoptosis by a cyclic GMP-dependent mechanism and independently of caspase 3 nitrosylation. Exp. Cell. Res. 287, 314-324. https://doi.org/10.1016/S0014-4827(03)00156-3
  16. Date, H., Triantafillou, A. N., Trulock, E. P., Pohl, M. S., Cooper, J. D. and Patterson, G. A. (1996). Inhaled nitric oxide reduces human lung allograft dysfunction. J. Thorac. Cardiovasc. Surg. 111, 913-919. https://doi.org/10.1016/S0022-5223(96)70364-1
  17. deRojas-Walker, T., Tamir, S., Ji, H., Wishnok, J. S. and Tannenbaum, S. R. (1995). Nitric oxide induces oxidative damage in addition to deamination in macrophage DNA. Chem. Res. Toxicol. 8, 473-477. https://doi.org/10.1021/tx00045a020
  18. Dezfulian, C., Raat, N., Shiva, S. and Gladwin, M. T. (2007). Role of the anion nitrite in ischemia-reperfusion cytoprotection and therapeutics. Cardiovasc. Res. 75, 327-338. https://doi.org/10.1016/j.cardiores.2007.05.001
  19. Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C., Busse, R. and Zeiher, A. M. (1999). Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399, 601-605. https://doi.org/10.1038/21224
  20. Dulak, J., Jozkowicz, A., Dembinska-Kiec, A., Guevara, I., Zdzienicka, A., Zmudzinska-Grochot, D., Florek, I., Wojtowicz, A., Szuba, A. and Cooke, J. P. (2000). Nitric oxide induces the synthesis of vascular endothelial growth factor by rat vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 20, 659-666. https://doi.org/10.1161/01.ATV.20.3.659
  21. Duranski, M. R., Greer, J. J., Dejam, A., Jaganmohan, S., Hogg, N., Langston, W., Patel, R. P., Yet, S. F., Wang, X., Kevil, C. G., Gladwin, M. T. and Lefer, D. J. (2005). Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J. Clin. Invest. 115, 1232-1240. https://doi.org/10.1172/JCI22493
  22. Edwards, C., Feng, H. Q., Reynolds, C., Mao, L. and Rockey, D. C. (2008). Effect of the nitric oxide donor V-PYRRO/NO on portal pressure and sinusoidal dynamics in normal and cirrhotic mice. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G1311-1317. https://doi.org/10.1152/ajpgi.00368.2007
  23. Elfering, S. L., Sarkela, T. M. and Giulivi, C. (2002). Biochemistry of mitochondrial nitric-oxide synthase. J. Biol. Chem. 277, 38079-38086. https://doi.org/10.1074/jbc.M205256200
  24. Elrod, J. W., Greer, J. J., Bryan, N. S., Langston, W., Szot, J. F., Gebregzlabher, H., Janssens, S., Feelisch, M. and Lefer, D. J. (2006). Cardiomyocyte-specific overexpression of NO synthase-3 protects against myocardial ischemia-reperfusion injury. Arterioscler. Thromb. Vasc. Biol. 26, 1517-1523. https://doi.org/10.1161/01.ATV.0000224324.52466.e6
  25. Fleming, I., Fisslthaler, B., Dimmeler, S., Kemp, B. E. and Busse, R. (2001). Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity. Circ. Res. 88, E68-75. https://doi.org/10.1161/hh1101.092677
  26. Folkman, J. and Shing, Y. (1992). Angiogenesis. J. Biol. Chem. 267, 10931-10934.
  27. Forrester, K., Ambs, S., Lupold, S. E., Kapust, R. B., Spillare, E. A., Weinberg, W. C., Felley-Bosco, E., Wang, X. W., Geller, D. A., Tzeng, E., Billiar, T. R. and Harris, C. C. (1996). Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase expression by wild-type p53. Proc. Natl. Acad. Sci. USA. 93, 2442-2447. https://doi.org/10.1073/pnas.93.6.2442
  28. Forstermann, U., Kleinert, H., Gath, I., Schwarz, P., Closs, E. I. and Dun, N. J. (1995). Expression and expressional control of nitric oxide synthases in various cell types. Adv. Pharmacol. 34, 171-186. https://doi.org/10.1016/S1054-3589(08)61085-6
  29. Foster, M. W., Hess, D. T. and Stamler, J. S. (2009). Protein S-nitrosylation in health and disease: a current perspective. Trends Mol. Med. 15, 391-404. https://doi.org/10.1016/j.molmed.2009.06.007
  30. Fukumura, D., Gohongi, T., Kadambi, A., Izumi, Y., Ang, J., Yun, C. O., Buerk, D. G., Huang, P. L. and Jain, R. K. (2001). Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. USA. 98, 2604-2609. https://doi.org/10.1073/pnas.041359198
  31. Furchgott, R. F. and Zawadzki, J. V. (1980). The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288, 373-376. https://doi.org/10.1038/288373a0
  32. Garg, U. C. and Hassid, A. (1989). Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J. Clin. Invest. 83, 1774-1777. https://doi.org/10.1172/JCI114081
  33. Gath, I., Closs, E. I., Godtel-Armbrust, U., Schmitt, S., Nakane, M., Wessler, I. and Forstermann, U. (1996). Inducible NO synthase II and neuronal NO synthase I are constitutively expressed in different structures of guinea pig skeletal muscle: implications for contractile function. FASEB J. 10, 1614-1620. https://doi.org/10.1096/fasebj.10.14.9002553
  34. Ghofrani, H. A., Hoeper, M. M., Halank, M., Meyer, F. J., Staehler, G., Behr, J., Ewert, R., Weimann, G. and Grimminger, F. (2010). Riociguat for chronic thromboembolic pulmonary hypertension and pulmonary arterial hypertension: a phase II study. Eur. Respir. J. 36, 792-799. https://doi.org/10.1183/09031936.00182909
  35. Granger, D. L., Taintor, R. R., Cook, J. L. and Hibbs, J. B. Jr. (1980). Injury of neoplastic cells by murine macrophages leads to inhibition of mitochondrial respiration. J. Clin. Invest. 65, 357-370. https://doi.org/10.1172/JCI109679
  36. Ha, K. S., Kim, K. M., Kwon, Y. G., Bai, S. K., Nam, W. D., Yoo, Y. M., Kim, P. K., Chung, H. T., Billiar, T. R. and Kim, Y. M. (2003). Nitric oxide prevents 6-hydroxydopamine-induced apoptosis in PC12 cells through cGMP-dependent PI3 kinase/Akt activation. FASEB J. 17, 1036-1047. https://doi.org/10.1096/fj.02-0738com
  37. Hibbs, J. B. Jr., Taintor, R. R. and Vavrin, Z. (1987). Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science 235, 473-476. https://doi.org/10.1126/science.2432665
  38. Hibbs, J. B. Jr., Taintor, R. R., Vavrin, Z. and Rachlin, E. M. (1988). Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 157, 87-94. https://doi.org/10.1016/S0006-291X(88)80015-9
  39. Huang, L. E., Willmore, W. G., Gu, J., Goldberg, M. A. and Bunn, H. F. (1999). Inhibition of hypoxia-inducible factor 1 activation by carbon monoxide and nitric oxide. Implications for oxygen sensing and signaling. J. Biol. Chem. 274, 9038- 9044. https://doi.org/10.1074/jbc.274.13.9038
  40. Huang, P. L., Huang, Z., Mashimo, H., Bloch, K. D., Moskowitz, M. A., Bevan, J. A. and Fishman, M. C. (1995). Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377, 239-242. https://doi.org/10.1038/377239a0
  41. Huang, Z., Shiva, S., Kim-Shapiro, D. B., Patel, R. P., Ringwood, L. A., Irby, C. E., Huang, K. T., Ho, C., Hogg, N., Schechter, A. N. and Gladwin, M. T. (2005). Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J. Clin. Invest. 115, 2099-2107. https://doi.org/10.1172/JCI24650
  42. Hunter, C. J., Dejam, A., Blood, A. B., Shields, H., Kim-Shapiro, D. B., Machado, R. F., Tarekegn, S., Mulla, N., Hopper, A. O., Schechter, A. N., Power, G. G. and Gladwin, M. T. (2004). Inhaled nebulized nitrite is a hypoxia-sensitive NO-dependent selective pulmonary vasodilator. Nat. Med. 10, 1122- 1127. https://doi.org/10.1038/nm1109
  43. Ignarro, L. J., Buga, G. M., Wood, K. S., Byrns, R. E. and Chaudhuri, G. (1987). Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. USA. 84, 9265-9269. https://doi.org/10.1073/pnas.84.24.9265
  44. Johnson, T. A., Stasko, N. A., Matthews, J. L., Cascio, W. E., Holmuhamedov, E. L., Johnson, C. B. and Schoenfisch, M. H. (2010). Reduced ischemia/reperfusion injury via glutathioneinitiated nitric oxide-releasing dendrimers. Nitric Oxide 22, 30-36. https://doi.org/10.1016/j.niox.2009.11.002
  45. Jones, S. P., Greer, J. J., Kakkar, A. K., Ware, P. D., Turnage, R. H., Hicks, M., van Haperen, R., de Crom, R., Kawashima, S., Yokoyama, M. and Lefer, D. J. (2004). Endothelial nitric oxide synthase overexpression attenuates myocardial reperfusion injury. Am. J. Physiol. Heart. Circ. Physiol. 286, H276-282. https://doi.org/10.1152/ajpheart.00129.2003
  46. Jun, C. D., Choi, B. M., Hoon, R., Um, J. Y., Kwak, H. J., Lee, B. S., Paik, S. G., Kim, H. M. and Chung, H. T. (1994). Synergistic cooperation between phorbol ester and IFN-$\gamma$ for induction of nitric oxide synthesis in murine peritoneal macrophages. J. Immunol. 153, 3684-3690.
  47. Jung, K. H., Chu, K., Ko, S. Y., Lee, S. T., Sinn, D. I., Park, D. K., Kim, J. M., Song, E. C., Kim, M. and Roh, J. K. (2006). Early intravenous infusion of sodium nitrite protects brain against in vivo ischemia-reperfusion injury. Stroke 37, 2744-2750. https://doi.org/10.1161/01.STR.0000245116.40163.1c
  48. Kanno, S., Lee, P. C., Zhang, Y., Ho, C., Griffith, B. P., Shears, L. L. 2nd and Billiar, T. R. (2000). Attenuation of myocardial ischemia/reperfusion injury by superinduction of inducible nitric oxide synthase. Circulation 101, 2742-2748. https://doi.org/10.1161/01.CIR.101.23.2742
  49. Kim, Y. M., Bergonia, H. and Lancaster, J. R. Jr. (1995a). Nitrogen oxide-induced autoprotection in isolated rat hepatocytes. FEBS Lett. 374, 228-232. https://doi.org/10.1016/0014-5793(95)01115-U
  50. Kim, Y. M., Bergonia, H. A., Muller, C., Pitt, B. R., Watkins, W. D. and Lancaster, J. R. Jr. (1995b). Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J. Biol. Chem. 270, 5710-5713. https://doi.org/10.1074/jbc.270.11.5710
  51. Kim, Y. M., Chung, H. T., Kim, S. S., Han, J. A., Yoo, Y. M., Kim, K. M., Lee, G. H., Yun, H. Y., Green, A., Li, J., Simmons, R. L. and Billiar, T. R. (1999). Nitric oxide protects PC12 cells from serum deprivation-induced apoptosis by cGMP-dependent inhibition of caspase signaling. J. Neurosci. 19, 6740-6747. https://doi.org/10.1523/JNEUROSCI.19-16-06740.1999
  52. Kim, Y. M., Chung, H. T., Simmons, R. L. and Billiar, T. R. (2000). Cellular non-heme iron content is a determinant of nitric oxide-mediated apoptosis, necrosis, and caspase inhibition. J. Biol. Chem. 275, 10954-10961. https://doi.org/10.1074/jbc.275.15.10954
  53. Kim, Y. M., de Vera, M. E., Watkins, S. C. and Billiar, T. R. (1997a). Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-alpha-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 272, 1402-1411. https://doi.org/10.1074/jbc.272.2.1402
  54. Kim, Y. M., Talanian, R. V. and Billiar, T. R. (1997b). Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272, 31138-31148. https://doi.org/10.1074/jbc.272.49.31138
  55. Kimura, H., Weisz, A., Kurashima, Y., Hashimoto, K., Ogura, T., D'Acquisto, F., Addeo, R., Makuuchi, M. and Esumi, H. (2000). Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor- 1 activity by nitric oxide. Blood 95, 189-197.
  56. Kisley, L. R., Barrett, B. S., Bauer, A. K., Dwyer-Nield, L. D., Barthel, B., Meyer, A. M., Thompson, D. C. and Malkinson, A. M. (2002). Genetic ablation of inducible nitric oxide synthase decreases mouse lung tumorigenesis. Cancer Res. 62, 6850-6856.
  57. Kiziltepe, T., Hideshima, T., Ishitsuka, K., Ocio, E. M., Raje, N., Catley, L., Li, C. Q., Trudel, L. J., Yasui, H., Vallet, S., Kutok, J. L., Chauhan, D., Mitsiades, C. S., Saavedra, J. E., Wogan, G. N., Keefer, L. K., Shami, P. J. and Anderson, K. C. (2007). JS-K, a GST-activated nitric oxide generator, induces DNA double-strand breaks, activates DNA damage response pathways, and induces apoptosis in vitro and in vivo in human multiple myeloma cells. Blood 110, 709-718. https://doi.org/10.1182/blood-2006-10-052845
  58. Konopka, T. E., Barker, J. E., Bamford, T. L., Guida, E., Anderson, R. L. and Stewart, A. G. (2001). Nitric oxide synthase II gene disruption: implications for tumor growth and vascular endothelial growth factor production. Cancer Res. 61, 3182-3187.
  59. Kroncke, K. D. (2003). Nitrosative stress and transcription. Biol. Chem. 384, 1365-1377. https://doi.org/10.1515/BC.2003.153
  60. Kroncke, K. D., Fehsel, K. and Kolb-Bachofen, V. (1997). Nitric oxide: cytotoxicity versus cytoprotection--how, why, when, and where? Nitric Oxide. 1, 107-120. https://doi.org/10.1006/niox.1997.0118
  61. Kumar, D., Branch, B. G., Pattillo, C. B., Hood, J., Thoma, S., Simpson, S., Illum, S., Arora, N., Chidlow, J. H., Jr., Langston, W., Teng, X., Lefer, D. J., Patel, R. P. and Kevil, C. G. (2008). Chronic sodium nitrite therapy augments ischemiainduced angiogenesis and arteriogenesis. Proc. Natl. Acad. Sci. USA. 105, 7540-7545. https://doi.org/10.1073/pnas.0711480105
  62. Kuroki, I., Miyazaki, T., Mizukami, I., Matsumoto, N. and Matsumoto, I. (2004). Effect of sodium nitroprusside on ischemia-reperfusion injuries of the rat liver. Hepatogastroenterology 51, 1404-1407.
  63. Lala, P. K. and Chakraborty, C. (2001). Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol. 2, 149-156. https://doi.org/10.1016/S1470-2045(00)00256-4
  64. Lang, J. D. Jr., Teng, X., Chumley, P., Crawford, J. H., Isbell, T. S., Chacko, B. K., Liu, Y., Jhala, N., Crowe, D. R., Smith, A. B., Cross, R. C., Frenette, L., Kelley, E. E., Wilhite, D. W., Hall, C. R., Page, G. P., Fallon, M. B., Bynon, J. S., Eckhoff, D. E. and Patel, R. P. (2007). Inhaled NO accelerates restoration of liver function in adults following orthotopic liver transplantation. J. Clin. Invest. 117, 2583-2591. https://doi.org/10.1172/JCI31892
  65. Le, X., Wei, D., Huang, S., Lancaster, J. R. Jr. and Xie, K. (2005). Nitric oxide synthase II suppresses the growth and metastasis of human cancer regardless of its up-regulation of protumor factors. Proc. Natl. Acad. Sci. USA. 102, 8758- 8763. https://doi.org/10.1073/pnas.0409581102
  66. Lee, P. C., Salyapongse, A. N., Bragdon, G. A., Shears, L. L. 2nd, Watkins, S. C., Edington, H. D. and Billiar, T. R. (1999). Impaired wound healing and angiogenesis in eNOS-deficient mice. Am. J. Physiol. 277, H1600-1608.
  67. Li, J., Billiar, T. R., Talanian, R. V. and Kim, Y. M. (1997). Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem. Biophys. Res. Commun. 240, 419-424. https://doi.org/10.1006/bbrc.1997.7672
  68. Li, Q., Guo, Y., Xuan, Y. T., Lowenstein, C. J., Stevenson, S. C., Prabhu, S. D., Wu, W. J., Zhu, Y. and Bolli, R. (2003). Gene therapy with inducible nitric oxide synthase protects against myocardial infarction via a cyclooxygenase-2-dependent mechanism. Circ. Res. 92, 741-748. https://doi.org/10.1161/01.RES.0000065441.72685.29
  69. Lima, B., Forrester, M. T., Hess, D. T. and Stamler, J. S. (2010). S-nitrosylation in cardiovascular signaling. Circ. Res. 106, 633-646. https://doi.org/10.1161/CIRCRESAHA.109.207381
  70. Lowson, S. M. (2004). Alternatives to nitric oxide. Br. Med. Bull. 70, 119-131. https://doi.org/10.1093/bmb/ldh028
  71. Marletta, M. A., Hurshman, A. R. and Rusche, K. M. (1998). Catalysis by nitric oxide synthase. Curr. Opin. Chem. Biol. 2, 656-663. https://doi.org/10.1016/S1367-5931(98)80098-7
  72. Matthews, N. E., Adams, M. A., Maxwell, L. R., Gofton, T. E. and Graham, C. H. (2001). Nitric oxide-mediated regulation of chemosensitivity in cancer cells. J. Natl. Cancer Inst. 93, 1879-1885. https://doi.org/10.1093/jnci/93.24.1879
  73. Messmer, U. K. and Brune, B. (1996). Nitric oxide-induced apoptosis: p53-dependent and p53-independent signalling pathways. Biochem. J. 319, 299-305. https://doi.org/10.1042/bj3190299
  74. Miller, M. R. and Megson, I. L. (2007). Recent developments in nitric oxide donor drugs. Br. J. Pharmacol. 151, 305-321. https://doi.org/10.1038/sj.bjp.0707224
  75. Moncada, S., Palmer, R. M. and Higgs, E. A. (1991). Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109-142.
  76. Murad, F. (1986). Cyclic guanosine monophosphate as a mediator of vasodilation. J. Clin. Invest. 78, 1-5. https://doi.org/10.1172/JCI112536
  77. Murohara, T., Asahara, T., Silver, M., Bauters, C., Masuda, H., Kalka, C., Kearney, M., Chen, D., Symes, J. F., Fishman, M. C., Huang, P. L. and Isner, J. M. (1998). Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Invest. 101, 2567-2578. https://doi.org/10.1172/JCI1560
  78. Namkoong, S., Chung, B. H., Ha, K. S., Lee, H., Kwon, Y. G. and Kim, Y. M. (2008). Microscopic technique for the detection of nitric oxide-dependent angiogenesis in an animal model. Methods Enzymol. 441, 393-402. https://doi.org/10.1016/S0076-6879(08)01222-6
  79. Nathan, C. (1992). Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 3051-3064. https://doi.org/10.1096/fasebj.6.12.1381691
  80. Nathan, C. (1997). Inducible nitric oxide synthase: what difference does it make? J. Clin. Invest. 100, 2417-2423. https://doi.org/10.1172/JCI119782
  81. Nathan, C. and Xie, Q. W. (1994). Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269, 13725-13728.
  82. Papapetropoulos, A., Garcia-Cardena, G., Madri, J. A. and Sessa, W. C. (1997). Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 100, 3131- 139. https://doi.org/10.1172/JCI119868
  83. Radomski, M. W., Jenkins, D. C., Holmes, L. and Moncada, S. (1991). Human colorectal adenocarcinoma cells: differential nitric oxide synthesis determines their ability to aggregate platelets. Cancer Res. 51, 6073-6078.
  84. RayChaudhury, A., Frischer, H. and Malik, A. B. (1996). Inhibition of endothelial cell proliferation and bFGF-induced phenotypic modulation by nitric oxide. J. Cell. Biochem. 63, 125-134. https://doi.org/10.1002/(SICI)1097-4644(19961101)63:2<125::AID-JCB1>3.0.CO;2-#
  85. Sase, K. and Michel, T. (1997). Expression and regulation of endothelial nitric oxide synthase. Trends in Cardiovasc. Med. 7, 28-37. https://doi.org/10.1016/S1050-1738(96)00121-1
  86. Scatena, R., Bottoni, P., Martorana, G. E. and Giardina, B. (2005). Nitric oxide donor drugs: an update on pathophysiology and therapeutic potential. Expert Opin. Investig. Drugs 14, 835-846. https://doi.org/10.1517/13543784.14.7.835
  87. Schgoer, W., Theurl, M., Jeschke, J., Beer, A. G., Albrecht, K., Gander, R., Rong, S., Vasiljevic, D., Egger, M., Wolf, A. M., Frauscher, S., Koller, B., Tancevski, I., Patsch, J. R., Schratzberger, P., Piza-Katzer, H., Ritsch, A., Bahlmann, F. H., Fischer-Colbrie, R., Wolf, D. and Kirchmair, R. (2009). Gene therapy with the angiogenic cytokine secretoneurin induces therapeutic angiogenesis by a nitric oxide-dependent mechanism. Circ. Res. 105, 994-1002. https://doi.org/10.1161/CIRCRESAHA.109.199513
  88. Schmidt, H. H., Lohmann, S. M. and Walter, U. (1993). The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochim. Biophys. Acta. 1178, 153-175. https://doi.org/10.1016/0167-4889(93)90006-B
  89. Schulz, R., Kelm, M. and Heusch, G. (2004). Nitric oxide in myocardial ischemia/reperfusion injury. Cardiovasc. Res. 61, 402-413. https://doi.org/10.1016/j.cardiores.2003.09.019
  90. Schwentker, A. and Billiar, T. R. (2002). Inducible nitric oxide synthase: from cloning to therapeutic applications. World J. Surg. 26, 772-778. https://doi.org/10.1007/s00268-002-4051-7
  91. Shimaoka, M., Iida, T., Ohara, A., Taenaka, N., Mashimo, T., Honda, T. and Yoshiya, I. (1995). NOC, a nitric-oxidereleasing compound, induces dose dependent apoptosis in macrophages. Biochem. Biophys. Res. Commun. 209, 519-526. https://doi.org/10.1006/bbrc.1995.1532
  92. Silvagno, F., Xia, H. and Bredt, D. S. (1996). Neuronal nitric- oxide synthase-mu, an alternatively spliced isoform expressed in differentiated skeletal muscle. J. Biol. Chem. 271, 11204-11208. https://doi.org/10.1074/jbc.271.19.11204
  93. Simeone, A. M., Colella, S., Krahe, R., Johnson, M. M., Mora, E. and Tari, A. M. (2006). N-(4-Hydroxyphenyl)retinamide and nitric oxide pro-drugs exhibit apoptotic and anti-invasive effects against bone metastatic breast cancer cells. Carcinogenesis 27, 568-577. https://doi.org/10.1093/carcin/bgi233
  94. Sogawa, K., Numayama-Tsuruta, K., Ema, M., Abe, M., Abe, H. and Fujii-Kuriyama, Y. (1998). Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. Proc. Natl. Acad. Sci. USA. 95, 7368-7373. https://doi.org/10.1073/pnas.95.13.7368
  95. Spedding, M., Schini, V., Schoeffter, P. and Miller, R. C. (1986). Calcium channel activation does not increase release of endothelial-derived relaxant factors (EDRF) in rat aorta although tonic release of EDRF may modulate calcium channel activity in smooth muscle. J. Cardiovasc. Pharmacol. 8, 1130-1137. https://doi.org/10.1097/00005344-198611000-00006
  96. Stasch, J. P. and Hobbs, A. J. (2009). NO-independent, haemdependent soluble guanylate cyclase stimulators. Handb. Exp. Pharmacol. 277-308.
  97. Steudel, W., Hurford, W. E. and Zapol, W. M. (1999). Inhaled nitric oxide: basic biology and clinical applications. Anesthesiology 91, 1090-1121. https://doi.org/10.1097/00000542-199910000-00030
  98. Stuehr, D. J. and Marletta, M. A. (1985). Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proc. Natl. Acad. Sci. USA. 82, 7738-7742. https://doi.org/10.1073/pnas.82.22.7738
  99. Surks, H. K. (2007). cGMP-dependent protein kinase I and smooth muscle relaxation: a tale of two isoforms. Circ. Res. 101, 1078-1080. https://doi.org/10.1161/CIRCRESAHA.107.165779
  100. Tatoyan, A. and Giulivi, C. (1998). Purification and characterization of a nitric-oxide synthase from rat liver mitochondria. J. Biol. Chem. 273, 11044-11048. https://doi.org/10.1074/jbc.273.18.11044
  101. Taylor, C. T. and Moncada, S. (2010). Nitric oxide, cytochrome C oxidase, and the cellular response to hypoxia. Arterioscler. Thromb. Vasc. Biol. 30, 643-647. https://doi.org/10.1161/ATVBAHA.108.181628
  102. Thatcher, G. R. (2005). An introduction to NO-related therapeutic agents. Curr. Top. Med. Chem. 5, 597-601. https://doi.org/10.2174/1568026054679281
  103. Thebaud, B., Arnal, J. F., Mercier, J. C. and Dinh-Xuan, A. T. (1999). Inhaled and exhaled nitric oxide. Cell Mol. Life Sci. 55, 1103-1112. https://doi.org/10.1007/s000180050360
  104. Trikha, P., Sharma, N. and Athar, M. (2001). Nitroglycerin: a NO donor inhibits TPA-mediated tumor promotion in murine skin. Carcinogenesis 22, 1207-1211. https://doi.org/10.1093/carcin/22.8.1207
  105. Tripatara, P., Patel, N. S., Webb, A., Rathod, K., Lecomte, F. M., Mazzon, E., Cuzzocrea, S., Yaqoob, M. M., Ahluwalia, A. and Thiemermann, C. (2007). Nitrite-derived nitric oxide protects the rat kidney against ischemia/reperfusion injury in vivo: role for xanthine oxidoreductase. J. Am. Soc. Nephrol. 18, 570-580. https://doi.org/10.1681/ASN.2006050450
  106. Tsuchiya, K., Kanematsu, Y., Yoshizumi, M., Ohnishi, H., Kirima, K., Izawa, Y., Shikishima, M., Ishida, T., Kondo, S., Kagami, S., Takiguchi, Y. and Tamaki, T. (2005). Nitrite is an alternative source of NO in vivo. Am. J. Physiol. Heart. Circ. Physiol. 288, H2163-2170. https://doi.org/10.1152/ajpheart.00525.2004
  107. Webb, A., Bond, R., McLean, P., Uppal, R., Benjamin, N. and Ahluwalia, A. (2004). Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proc. Natl. Acad. Sci. USA 101, 13683-13688. https://doi.org/10.1073/pnas.0402927101
  108. Wei, D., Richardson, E. L., Zhu, K., Wang, L., Le, X., He, Y., Huang, S. and Xie, K. (2003). Direct demonstration of negative regulation of tumor growth and metastasis by host-inducible nitric oxide synthase. Cancer Res. 63, 3855-3859.
  109. Yerebakan, C., Ugurlucan, M., Bayraktar, S., Bethea, B. T. and Conte, J. V. (2009). Effects of inhaled nitric oxide following lung transplantation. J. Card. Surg. 24, 269-274. https://doi.org/10.1111/j.1540-8191.2009.00833.x
  110. Yim, C. Y., Bastian, N. R., Smith, J. C., Hibbs, J. B. Jr. and Samlowski, W. E. (1993). Macrophage nitric oxide synthesis delays progression of ultraviolet light-induced murine skin cancers. Cancer Res. 53, 5507-5511.
  111. Yu, J., deMuinck, E. D., Zhuang, Z., Drinane, M., Kauser, K., Rubanyi, G. M., Qian, H. S., Murata, T., Escalante, B. and Sessa, W. C. (2005). Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve. Proc. Natl. Acad. Sci. USA. 102, 10999-11004. https://doi.org/10.1073/pnas.0501444102
  112. Zech, B., Kohl, R., von Knethen, A. and Brune, B. (2003). Nitric oxide donors inhibit formation of the Apaf-1/caspase-9 apoptosome and activation of caspases. Biochem. J. 371, 1055-1064. https://doi.org/10.1042/BJ20021720
  113. Zhang, R., Wang, L., Zhang, L., Chen, J., Zhu, Z., Zhang, Z. and Chopp, M. (2003). Nitric oxide enhances angiogenesis via the synthesis of vascular endothelial growth factor and cGMP after stroke in the rat. Circ. Res. 92, 308-313. https://doi.org/10.1161/01.RES.0000056757.93432.8C
  114. Ziche, M., Morbidelli, L., Choudhuri, R., Zhang, H. T., Donnini, S., Granger, H. J. and Bicknell, R. (1997). Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J. Clin. Invest. 99, 2625-2634. https://doi.org/10.1172/JCI119451

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