Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2014, Article ID 726539, 9 pages
http://dx.doi.org/10.1155/2014/726539
Research Article

Nitric Oxide Synthetic Pathway in Patients with Microvascular Angina and Its Relations with Oxidative Stress

1Centro Cardiologico Monzino, I.R.C.C.S., 20138 Milan, Italy
2Dipartimento di Scienze Cliniche e di Comunità, Università degli Studi di Milano, 20138 Milan, Italy
3Dipartimento di Scienze Farmacologiche e Biomolecolari, Università degli Studi di Milano, 20133 Milan, Italy

Received 27 February 2014; Revised 28 March 2014; Accepted 29 March 2014; Published 22 April 2014

Academic Editor: Daniela Giustarini

Copyright © 2014 Benedetta Porro et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Moncada, R. M. J. Palmer, and E. A. Higgs, “Nitric oxide: physiology, pathophysiology, and pharmacology,” Pharmacological Reviews, vol. 43, no. 2, pp. 109–142, 1991. View at Google Scholar · View at Scopus
  2. M. W. Radomski, R. M. J. Palmer, and S. Moncada, “Endogenous nitric oxide inhibits human platelet adhesion to vascular endothelium,” The Lancet, vol. 2, no. 8567, pp. 1057–1058, 1987. View at Google Scholar · View at Scopus
  3. P. Kleinbongard, A. Dejam, T. Lauer et al., “Plasma nitrite concentrations reflect the degree of endothelial dysfunction in humans,” Free Radical Biology and Medicine, vol. 40, no. 2, pp. 295–302, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Rassaf, C. Heiss, U. Hendgen-Cotta et al., “Plasma nitrite reserve and endothelial function in the human forearm circulation,” Free Radical Biology and Medicine, vol. 41, no. 2, pp. 295–301, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Heiss, T. Lauer, A. Dejam et al., “Plasma nitroso compounds are decreased in patients with endothelial dysfunction,” Journal of the American College of Cardiology, vol. 47, no. 3, pp. 573–579, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. S. M. Morris Jr., “Arginine metabolism in vascular biology and disease,” Vascular Medicine, vol. 10, supplement 1, pp. S83–S87, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Caplin and J. Leiper, “Endogenous nitric oxide synthase inhibitors in the biology of disease: markers, mediators, and regulators?” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 32, pp. 1343–1353, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. Z. Wang, W. H. W. Tang, L. Cho, D. M. Brennan, and S. L. Hazen, “Targeted metabolomic evaluation of arginine methylation and cardiovascular risks: potential mechanisms beyond nitric oxide synthase inhibition,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 29, no. 9, pp. 1383–1391, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. M. M. Cortese-Krott, A. Rodriguez-Mateos, R. Sansone et al., “Human red blood cells at work: identification and visualization of erythrocytic eNOS activity in health and disease,” Blood, vol. 120, no. 20, pp. 4229–4237, 2012. View at Publisher · View at Google Scholar
  10. S. Eligini, B. Porro, A. Lualdi et al., “Nitric oxide synthetic pathway in red blood cells is impaired in coronary artery disease,” PLoS ONE, vol. 8, Article ID e66945, 2013. View at Google Scholar
  11. P. Kleinbongard, R. Schulz, T. Rassaf et al., “Red blood cells express a functional endothelial nitric oxide synthase,” Blood, vol. 107, no. 7, pp. 2943–2951, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. K. C. Wood, M. M. Cortese-Krott, J. C. Kovacic et al., “Circulating blood endothelial nitric oxide synthase contributes to the regulation of systemic blood pressure and nitrite homeostasis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, pp. 1861–1871, 2013. View at Google Scholar
  13. F. Omodeo-Salè, L. Cortelezzi, Z. Vommaro, D. Scaccabarozzi, and A. M. Dondorp, “Dysregulation of L-arginine metabolism and bioavailability associated to free plasma heme,” American Journal of Physiology. Cell Physiology, vol. 299, no. 1, pp. C148–C154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Yokoro, M. Suzuki, K. Murota et al., “Asymmetric dimethylarginine, an endogenous NOS inhibitor, is actively metabolized in rat erythrocytes,” Bioscience, Biotechnology, and Biochemistry, vol. 76, no. 7, pp. 1334–1342, 2012. View at Google Scholar
  15. P. S. Kim, R. K. Iyer, K. V. Lu et al., “Expression of the liver form of arginase in erythrocytes,” Molecular Genetics and Metabolism, vol. 76, no. 2, pp. 100–110, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. C. P. Jenkinson, W. W. Grody, and S. D. Cederbaum, “Comparative properties of arginases,” Comparative Biochemistry and Physiology B, Biochemistry and Molecular Biology, vol. 114, no. 1, pp. 107–132, 1996. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Yang, A. T. Gonon, P. O. Sjoquist, J. O. Lundberg, and J. Pernow, “Arginase regulates red blood cell nitric oxide synthase and export of cardioprotective nitric oxide bioactivity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, pp. 15049–15054, 2013. View at Google Scholar
  18. S. Ryoo, G. Gupta, A. Benjo et al., “Endothelial arginase II: a novel target for the treatment of atherosclerosis,” Circulation Research, vol. 102, no. 8, pp. 923–932, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Jung, A. T. Gonon, P.-O. Sjöquist, J. O. Lundberg, and J. Pernow, “Arginase inhibition mediates cardioprotection during ischaemia-reperfusion,” Cardiovascular Research, vol. 85, no. 1, pp. 147–154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Zhang, T. W. Hein, W. Wang et al., “Upregulation of vascular arginase in hypertension decreases nitric oxide-mediated dilation of coronary arterioles,” Hypertension, vol. 44, no. 6, pp. 935–943, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. A. R. White, S. Ryoo, D. Li et al., “Knockdown of arginase I restores NO signaling in the vasculature of old rats,” Hypertension, vol. 47, no. 2, pp. 245–251, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. W. L. Proudfit, E. K. Shirey, and F. M. Sones Jr., “Selective cine coronary arteriography. Correlation with clinical findings in 1,000 patients,” Circulation, vol. 33, no. 6, pp. 901–910, 1966. View at Google Scholar · View at Scopus
  23. H. G. Kemp, R. A. Kronmal, and R. E. Vlietstra, “Seven year survival of patients with normal or near normal coronary arteriograms: a CASS registry study,” Journal of the American College of Cardiology, vol. 7, no. 3, pp. 479–483, 1986. View at Google Scholar · View at Scopus
  24. B. L. Sharaf, C. J. Pepine, R. A. Kerensky et al., “Detailed angiographic analysis of women with suspected ischemic chest pain (pilot phase data from the NHLBI-sponsored Women's Ischemia Syndrome Evaluation [WISE] study angiographic core laboratory),” The American Journal of Cardiology, vol. 87, no. 8, pp. 937–941, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. G. A. Lanza and F. Crea, “Primary coronary microvascular dysfunction: clinical presentation, pathophysiology, and management,” Circulation, vol. 121, no. 21, pp. 2317–2325, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Cosín-Sales, C. Pizzi, S. Brown, and J. C. Kaski, “C-reactive protein, clinical presentation, and ischemic activity in patients with chest pain and normal coronary angiograms,” Journal of the American College of Cardiology, vol. 41, no. 9, pp. 1468–1474, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Egashira, T. Inou, Y. Hirooka, A. Yamada, Y. Urabe, and A. Takeshita, “Evidence of impaired endothelium-dependent coronary vasodilatation in patients with angina pectoris and normal coronary angiograms,” The New England Journal of Medicine, vol. 328, no. 23, pp. 1659–1664, 1993. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Joannides, W. E. Haefeli, L. Linder et al., “Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo,” Circulation, vol. 91, no. 5, pp. 1314–1319, 1995. View at Google Scholar · View at Scopus
  29. J. C. Kaski, G. M. C. Rosano, P. Collins, P. Nihoyannopoulos, A. Maseri, and P. A. Poole-Wilson, “Cardiac syndrome X: clinical characteristics and left ventricular function long-term follow-up study,” Journal of the American College of Cardiology, vol. 25, no. 4, pp. 807–814, 1995. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Murakami, K. Urabe, and M. Nishimura, “Inappropriate microvascular constriction produced transient ST-segment elevation in patients with syndrome X,” Journal of the American College of Cardiology, vol. 32, no. 5, pp. 1287–1294, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. B. Özüyaman, M. Grau, M. Kelm, M. W. Merx, and P. Kleinbongard, “RBC NOS: regulatory mechanisms and therapeutic aspects,” Trends in Molecular Medicine, vol. 14, no. 7, pp. 314–322, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Keymel, C. Heiss, P. Kleinbongard, M. Kelm, and T. Lauer, “Impaired red blood cell deformability in patients with coronary artery disease and diabetes mellitus,” Hormone and Metabolic Research, vol. 43, no. 11, pp. 760–765, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Horn, M. M. Cortese-Krott, S. Keymel et al., “Nitric oxide influences red blood cell velocity independently of changes in the vascular tone,” Free Radical Research, vol. 45, no. 6, pp. 653–661, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. A.-M. Teichert, T. L. Miller, S. C. Tai et al., “In vivo expression profile of an endothelial nitric oxide synthase promoter-reporter transgene,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 278, no. 4, pp. H1352–H1361, 2000. View at Google Scholar · View at Scopus
  35. P. Kleinbongard, S. Keymel, and M. Kelm, “New functional aspects of the L-arginine-nitric oxide metabolism within the circulating blood,” Thrombosis and Haemostasis, vol. 98, no. 5, pp. 970–974, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Demirkol, S. Balta, T. Celik et al., “Assessment of the relationship between red cell distribution width and cardiac syndrome X,” Kardiologia Polska, vol. 71, pp. 480–484, 2013. View at Google Scholar
  37. J.-W. Chen, N.-W. Hsu, T.-C. Wu, S.-J. Lin, and M.-S. Chang, “Long-term angiotensin-converting enzyme inhibition reduces plasma asymmetric dimethylarginine and improves endothelial nitric oxide bioavailability and coronary microvascular function in patients with syndrome X,” American Journal of Cardiology, vol. 90, no. 9, pp. 974–982, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Piatti, G. Fragasso, L. D. Monti et al., “Acute intravenous L-arginine infusion decreases endothelin-1 levels and improves endothelial function in patients with angina pectoris and normal coronary arteriograms: correlation with asymmetric dimethylarginine levels,” Circulation, vol. 107, no. 3, pp. 429–436, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. I. Squellerio, E. Tremoli, and V. Cavalca, “Quantification of arginine and its metabolites in human erythrocytes using liquid chromatography-tandem mass spectrometry,” Analytical Biochemistry, vol. 412, no. 1, pp. 108–110, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. C. R. Morris, G. J. Kato, M. Poljakovic et al., “Dysregulated arginine metabolism, hemolysis-associated pulmonary hypertension, and mortality in sickle cell disease,” Journal of the American Medical Association, vol. 294, no. 1, pp. 81–90, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Sourij, A. Meinitzer, S. Pilz et al., “Arginine bioavailability ratios are associated with cardiovascular mortality in patients referred to coronary angiography,” Atherosclerosis, vol. 218, no. 1, pp. 220–225, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. I. Squellerio, D. Caruso, B. Porro, F. Veglia, E. Tremoli, and V. Cavalca, “Direct glutathione quantification in human blood by LC-MS/MS: comparison with HPLC with electrochemical detection,” Journal of Pharmaceutical and Biomedical Analysis, vol. 71, pp. 111–118, 2012. View at Google Scholar
  43. F. Veglia, G. Cighetti, M. de Franceschi et al., “Age- and gender-related oxidative status determined in healthy subjects by means of OXY-SCORE, a potential new comprehensive index,” Biomarkers: Biochemical Indicators of Exposure, Response, and Susceptibility to Chemicals, vol. 11, no. 6, pp. 562–573, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Lauer, P. Kleinbongard, J. Rath, R. Schulz, M. Kelm, and T. Rassaf, “L-Arginine preferentially dilates stenotic segments of coronary arteries thereby increasing coronary flow,” Journal of Internal Medicine, vol. 264, no. 3, pp. 237–244, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Shemyakin, O. Kovamees, A. Rafnsson et al., “Arginase inhibition improves endothelial function in patients with coronary artery disease and type 2 diabetes mellitus,” Circulation, vol. 126, pp. 2943–2950, 2012. View at Google Scholar
  46. E. B. Spector, S. C. H. Rice, and S. D. Cederbaum, “Immunologic studies of arginase in tissues of normal human adult and arginase-deficient patients,” Pediatric Research, vol. 17, no. 12, pp. 941–944, 1983. View at Google Scholar · View at Scopus
  47. O. Schnorr, T. Brossette, T. Y. Momma et al., “Cocoa flavanols lower vascular arginase activity in human endothelial cells in vitro and in erythrocytes in vivo,” Archives of Biochemistry and Biophysics, vol. 476, no. 2, pp. 211–215, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Maseri, F. Crea, J. C. Kaski, and T. Crake, “Mechanisms of angina pectoris in syndrome X,” Journal of the American College of Cardiology, vol. 17, no. 2, pp. 499–506, 1991. View at Google Scholar · View at Scopus
  49. S. Setoguchi, M. Mohri, H. Shimokawa, and A. Takeshita, “Tetrahydrobiopterin improves endothelial dysfunction in coronary microcirculation in patients without epicardial coronary artery disease,” Journal of the American College of Cardiology, vol. 38, no. 2, pp. 493–498, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. S. S. Dhawan, P. Eshtehardi, M. C. McDaniel et al., “The role of plasma aminothiols in the prediction of coronary microvascular dysfunction and plaque vulnerability,” Atherosclerosis, vol. 219, no. 1, pp. 266–272, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Rassaf, P. Kleinbongard, and M. Kelm, “The L-arginine nitric oxide pathway: avenue for a multiple-level approach to assess vascular function,” Biological Chemistry, vol. 387, no. 10-11, pp. 1347–1349, 2006. View at Publisher · View at Google Scholar · View at Scopus