A computational model for nitric oxide, nitrite and nitrate biotransport in the microcirculation: Effect of reduced nitric oxide consumption by red blood cells and blood velocity

Microvascular Research

Volumn 80, Issue 3, 2010, Pages 464-476

  Deonikar, Prabhakar ^a   Kavdia, Mahendra ^a  

^a Wayne State University   (United States)

Author keywords

Biotransport; Convection; Diffusion; Mathematical model; Microcirculation; Nitric oxide; Red blood cell

Indexed keywords

NITRATE; NITRIC OXIDE; NITRITE;

ARTERIOLE; ARTERY DIAMETER; ARTICLE; BLOOD FLOW VELOCITY; BLOOD VESSEL WALL; CELL TRANSPORT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ERYTHROCYTE KINETICS; ERYTHROCYTE METABOLISM; MATHEMATICAL MODEL; MICROCIRCULATION; PRIORITY JOURNAL; SIMULATION; SMOOTH MUSCLE FIBER; TISSUE DISTRIBUTION; TISSUE LEVEL;

ANIMALS; ARTERIOLES; BIOLOGICAL TRANSPORT; BLOOD FLOW VELOCITY; COMPUTER SIMULATION; ERYTHROCYTES; HUMANS; KINETICS; MICROCIRCULATION; MODELS, CARDIOVASCULAR; MUSCLE, SMOOTH, VASCULAR; NITRATES; NITRIC OXIDE; NITRITES; NUMERICAL ANALYSIS, COMPUTER-ASSISTED;

EID: 78249266312     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2010.09.004     Document Type: Article

References (74)

1. Arnold W.P., et al. Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations. Proc. Natl Acad. Sci. USA 1977, 74:3203-3207.
2. Azarov I., et al. Nitric oxide scavenging by red blood cells as a function of hematocrit and oxygenation. J. Biol. Chem. 2005, 280:39024-39032.
3. 3 by the concerted nitrite reductase and anhydrase activity of hemoglobin. Nat. Chem. Biol. 2007, 3:785-794.
4. Bauser-Heaton H.D., Bohlen H.G. Cerebral microvascular dilation during hypotension and decreased oxygen tension: a role for nNOS. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H2193-H2201.
5. Bevan J.A., et al. As human pial arteries (internal diameter 200-1000micron) get smaller, their wall thickness and capacity to develop tension relative to their diameter increase. Life Sci. 1999, 65:1153-1161.
6. Bohlen H.G., et al. Transfer of nitric oxide by blood from upstream to downstream resistance vessels causes microvascular dilation. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H1337-H1346.
7. Buerk D.G., et al. Nitric oxide has a vasodilatory role in cat optic nerve head during flicker stimuli. Microvasc. Res. 1996, 52:13-26.
8. Butler A.R., et al. Diffusion of nitric oxide and scavenging by blood in the vasculature. Biochim. Biophys. Acta 1998, 1425:168-176.
9. Carlsen E., Comroe J.H. The rate of uptake of carbon monoxide and of nitric oxide by normal human erythrocytes and experimentally produced spherocytes. J. Gen. Physiol. 1958, 42:83-107.
10. Cassoly R., Gibson Q. Conformation, co-operativity and ligand binding in human hemoglobin. J. Mol. Biol. 1975, 91:301-313.
11. 2 transport. J. Appl. Physiol. 2006, 100:482-492.
12. Chen K., et al. Vascular smooth muscle NO exposure from intraerythrocytic SNOHb: a mathematical model. Antioxid. Redox Signal. 2007, 9:1097-1110.
13. 2 transport in capillary-perfused tissue containing an arteriole and venule pair. Ann. Biomed. Eng. 2007, 35:517-529.
14. Chen K., et al. Nitric oxide from nitrite reduction by hemoglobin in the plasma and erythrocytes. Nitric Oxide 2008, 18:47-60.
15. Chen K., et al. Nitric oxide in the vasculature: where does it come from and where does it go? A quantitative perspective. Antioxid. Redox Signal. 2008, 10:1185-1198.
16. Crawford J.H., et al. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood 2006, 107:566-574.
17. Deonikar P., Kavdia M. Extracellular diffusion and permeability effects on NO-RBCs interactions using an experimental and theoretical model. Microvasc. Res. 2009, 79:47-55.
18. Deonikar P., Kavdia M. An integrated computational and experimental model of nitric oxide-red blood cell interactions. Ann. Biomed. Eng. 2009, 38:357-370.
19. Diesen D.L., et al. Hypoxic vasodilation by red blood cells: evidence for an s-nitrosothiol-based signal. Circ. Res. 2008, 103:545-553.
20. Dreissigacker U., et al. Positive correlation between plasma nitrite and performance during high-intensive exercise but not oxidative stress in healthy men. Nitric Oxide 2010, 23:128-135.
21. Eich R.F., et al. Mechanism of NO-induced oxidation of myoglobin and hemoglobin. Biochemistry 1996, 35:6976-6983.
22. El-Farra N.H., et al. Analysis of nitric oxide consumption by erythrocytes in blood vessels using a distributed multicellular model. Ann. Biomed. Eng. 2003, 31:294-309.
23. Ellsworth M.L., et al. Assessment and impact of heterogeneities of convective oxygen transport parameters in capillaries of striated muscle: experimental and theoretical. Microvasc. Res. 1988, 35:341-362.
24. Fukumura D., et al. Role of nitric oxide in tumor microcirculation. Blood flow, vascular permeability, and leukocyte-endothelial interactions. Am. J. Pathol. 1997, 150:713-725.
25. Furchgott R.F., Zawadzki J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980, 288:373-376.
26. Gladwin M.T., et al. Nitrite as a vascular endocrine nitric oxide reservoir that contributes to hypoxic signaling, cytoprotection, and vasodilation. Am. J. Physiol. Heart Circ. Physiol. 2006, 291:H2026-H2035.
27. Haas T.L., Duling B.R. Morphology favors an endothelial cell pathway for longitudinal conduction within arterioles. Microvasc. Res. 1997, 53:113-120.
28. Han T.H., Liao J.C. Erythrocyte nitric oxide transport reduced by a submembrane cytoskeletal barrier. Biochim. Biophys. Acta 2005, 1723:135-142.
29. Huang K.T., et al. Nitric oxide red blood cell membrane permeability at high and low oxygen tension. Nitric Oxide 2007, 16:209-216.
30. Ignarro L.J., et al. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl Acad. Sci. USA 1987, 84:9265-9269.
31. Ignarro L.J., et al. Oxidation of nitric oxide in aqueous solution to nitrite but not nitrate: comparison with enzymatically formed nitric oxide from l-arginine. Proc. Natl Acad. Sci. USA 1993, 90:8103-8107.
32. Jeffers A., et al. Computation of plasma hemoglobin nitric oxide scavenging in hemolytic anemias. Free Radic. Biol. Med. 2006, 41:1557-1565.
33. Jensen F.B. The role of nitrite in nitric oxide homeostasis: a comparative perspective. Biochim. Biophys. Acta 2009, 1787:841-848.
34. Jia L., et al. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 1996, 380:221-226.
35. Joshi M.S., et al. Nitric oxide is consumed, rather than conserved, by reaction with oxyhemoglobin under physiological conditions. Proc. Natl Acad. Sci. USA 2002, 99:10341-10346.
36. Jourd'heuil D., et al. Dynamic state of S-nitrosothiols in human plasma and whole blood. Free Radic. Biol. Med. 2000, 28:409-417.
37. Kanai A.J., et al. Shear stress induces ATP-independent transient nitric oxide release from vascular endothelial cells, measured directly with a porphyrinic microsensor. Circ. Res. 1995, 77:284-293.
38. 2 carriers. Microvasc. Res. 2003, 66:49-58.
39. Kavdia M., Popel A.S. Contribution of nNOS- and eNOS-derived NO to microvascular smooth muscle NO exposure. J. Appl. Physiol. 2004, 97:293-301.
40. Kavdia M., Popel A.S. Venular endothelium-derived NO can affect paired arteriole: a computational model. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H716-H723.
41. Kavdia M., et al. Model of nitric oxide diffusion in an arteriole: impact of hemoglobin-based blood substitutes. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H2245-H2253.
42. Kelm M., et al. Role of nitric oxide in the regulation of coronary vascular tone in hearts from hypertensive rats. Maintenance of nitric oxide-forming capacity and increased basal production of nitric oxide. Hypertension 1995, 25:186-193.
43. Kleinbongard P., et al. Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radic. Biol. Med. 2003, 35:790-796.
44. Lancaster J.R. Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc. Natl Acad. Sci. USA 1994, 91:8137-8141.
45. Lewis R.S., Deen W.M. Kinetics of the reaction of nitric oxide with oxygen in aqueous solutions. Chem. Res. Toxicol. 1994, 7:568-574.
46. Liao J.C., et al. Intravascular flow decreases erythrocyte consumption of nitric oxide. Proc. Natl Acad. Sci. USA 1999, 96:8757-8761.
47. Liu X., et al. Diffusion-limited reaction of free nitric oxide with erythrocytes. J. Biol. Chem. 1998, 273:18709-18713.
48. Liu X., et al. Nitric oxide uptake by erythrocytes is primarily limited by extracellular diffusion not membrane resistance. J. Biol. Chem. 2002, 277:26194-26199.
49. Liu X., et al. Estimation of nitric oxide concentration in blood for different rates of generation. Evidence that intravascular nitric oxide levels are too low to exert physiological effects. J. Biol. Chem. 2007, 282:8831-8836.
50. Malinski T., et al. Direct electrochemical measurement of nitric oxide released from human platelets. Biochem. Biophys. Res. Commun. 1993, 194:960-965.
51. Marks D.S., et al. Inhibition of neointimal proliferation in rabbits after vascular injury by a single treatment with a protein adduct of nitric oxide. J. Clin. Invest. 1995, 96:2630-2638.
52. Moncada S., et al. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 1991, 43:109-142.
53. Nagababu E., et al. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J. Biol. Chem. 2003, 278:46349-46356.
54. Palmer R.M., et al. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987, 327:524-526.
55. Popel A.S. Theory of oxygen transport to tissue. Crit. Rev. Biomed. Eng. 1989, 17:257-321.
56. Radomski M.W., et al. Modulation of platelet aggregation by an l-arginine-nitric oxide pathway. Trends Pharmacol. Sci. 1991, 12:87-88.
57. Radomski M.W., et al. Platelet adhesion to human vascular endothelium is modulated by constitutive and cytokine induced nitric oxide. Cardiovasc. Res. 1993, 27:1380-1382.
58. Sharan M., Popel A.S. A two-phase model for flow of blood in narrow tubes with increased effective viscosity near the wall. Biorheology 2001, 38:415-428.
59. Singel D.J., Stamler J.S. Chemical physiology of blood flow regulation by red blood cells: the role of nitric oxide and S-nitrosohemoglobin. Annu. Rev. Physiol. 2005, 67:99-145.
60. Smith K.M., et al. Advective transport of nitric oxide in a mathematical model of the afferent arteriole. Am. J. Physiol. Ren. Physiol. 2003, 284:F1080-F1096.
61. Stamler J.S., et al. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 1997, 276:2034-2037.
62. Tsai A.G., et al. Elevated plasma viscosity in extreme hemodilution increases perivascular nitric oxide concentration and microvascular perfusion. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H1730-H1739.
63. Tsai A.G., et al. Dissociation of local nitric oxide concentration and vasoconstriction in the presence of cell-free hemoglobin oxygen carriers. Blood 2006, 108:3603-3610.
64. Tsoukias N.M. Nitric oxide bioavailability in the microcirculation: insights from mathematical models. Microcirculation 2008, 15:813-834.
65. Tsoukias N.M., Popel A.S. Erythrocyte consumption of nitric oxide in presence and absence of plasma-based hemoglobin. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H2265-H2277.
66. Vaughn M.W., et al. Effective diffusion distance of nitric oxide in the microcirculation. Am. J. Physiol. 1998, 274:H1705-H1714.
67. Vaughn M.W., et al. Estimation of nitric oxide production and reaction rates in tissue by use of a mathematical model. Am. J. Physiol. 1998, 274:H2163-H2176.
68. Vaughn M.W., et al. Erythrocytes possess an intrinsic barrier to nitric oxide consumption. J. Biol. Chem. 2000, 275:2342-2348.
69. Vaughn M.W., et al. Erythrocyte consumption of nitric oxide: competition experiment and model analysis. Nitric Oxide 2001, 5:18-31.
70. Vitturi D.A., et al. Regulation of nitrite transport in red blood cells by hemoglobin oxygen fractional saturation. Am. J. Physiol. Heart Circ. Physiol. 2009, 296:H1398-H1407.
71. Vukosavljevic N., et al. Quantifying the l-arginine paradox in vivo. Microvasc. Res. 2006, 71:48-54.
72. Walmsley J.G., et al. Quantitative morphology of arterioles from the hamster cheek pouch related to mechanical analysis. Microvasc. Res. 1982, 24:249-271.
73. Zani B.G., Bohlen H.G. Transport of extracellular l-arginine via cationic amino acid transporter is required during in vivo endothelial nitric oxide production. Am. J. Physiol. Heart Circ. Physiol. 2005, 289:H1381-H1390.
74. Zhang Z.G., et al. Nitric oxide changes in the rat brain after transient middle cerebral artery occlusion. J. Neurol. Sci. 1995, 128:22-27.