Modulation of NO bioavailability by temporal variation of the cell-free layer width in small arterioles

Annals of Biomedical Engineering

Volumn 39, Issue 3, 2011, Pages 1012-1023

  Ong, Peng Kai ^a   Jain, Swati ^a   Kim, Sangho ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Microcirculation; Nitric oxide; Vasodilation; Wall shear stress

Indexed keywords

CELL-FREE; COMPUTATIONAL MODEL; CREMASTER MUSCLE; DYNAMIC CHARACTERISTICS; HIGH-SPEED VIDEO; LAYER WIDTH; PRODUCTION RATES; SCAVENGING RATES; TEMPORAL CHANGE; TEMPORAL VARIATION; TIME DOMAIN; TRANSIENT CHANGES; TRANSIENT RESPONSE; VASODILATION; WALL SHEAR STRESS;

MICROCIRCULATION; NITRIC OXIDE; SCAVENGING; SHEAR STRESS; STRENGTH OF MATERIALS; VIDEO RECORDING;

BIOCHEMISTRY;

NITRIC OXIDE;

ANIMAL; ARTERIOSCLEROSIS; ARTICLE; BIOLOGICAL MODEL; CELL FREE SYSTEM; COMPUTER SIMULATION; HUMAN; METABOLIC CLEARANCE RATE; METABOLISM; PHYSIOLOGY; RAT; SHEAR STRENGTH; WISTAR RAT;

ANIMALS; ARTERIOSCLEROSIS; CELL-FREE SYSTEM; COMPUTER SIMULATION; HUMANS; METABOLIC CLEARANCE RATE; MODELS, CARDIOVASCULAR; NITRIC OXIDE; RATS; RATS, WISTAR; SHEAR STRENGTH;

EID: 79951556203     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-010-0216-y     Document Type: Article

References (50)

1. C Alonso AR Pries P Gaehtgens 1993 Time-dependent rheological behavior of blood at low shear in narrow vertical tubes Am. J. Physiol. 265 H553 H561 1:STN:280:DyaK3sznslyltg%3D%3D 8368359
2. WP Arnold CK Mittal S Katsuki F Murad 1977 Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations Proc. Natl Acad. Sci. U.S.A. 74 3203 3207 1:CAS:528:DyaE2sXlsVKlsbk%3D 10.1073/pnas.74.8.3203 20623 (Pubitemid 8180317)
3. M Baker H Wayland 1974 On-line volume flow rate and velocity profile measurement for blood in microvessels Microvasc. Res. 7 131 143 1:STN:280:DyaE2c7jvVCgug%3D%3D 10.1016/0026-2862(74)90043-0 4821168
4. OK Baskurt O Yalcin S Ozdem JK Armstrong HJ Meiselman 2004 Modulation of endothelial nitric oxide synthase expression by red blood cell aggregation Am. J. Physiol. Heart Circ. Physiol. 286 H222 H229 1:CAS:528:DC%2BD2cXot1Sjsw%3D%3D 10.1152/ajpheart.00532.2003 14512280
5. DG Buerk CE Riva 1998 Vasomotion and spontaneous low-frequency oscillations in blood flow and nitric oxide in cat optic nerve head Microvasc. Res. 55 103 112 1:CAS:528:DyaK1cXhsF2nt7Y%3D 10.1006/mvre.1997.2053 9473413 (Pubitemid 28368417)
6. 2 transport J. Appl. Physiol. 100 482 492 1:CAS:528: DC%2BD28Xhs1Khu74%3D 10.1152/japplphysiol.00633.2005 16210436 (Pubitemid 43671598)
7. P Condorelli SC George 2001 In vivo control of soluble guanylate cyclase activation by nitric oxide: a kinetic analysis Biophys. J. 80 2110 2119 1:CAS:528:DC%2BD3MXkvFWjtr8%3D 10.1016/S0006-3495(01)76184-X 11325714 (Pubitemid 32401977)
8. P Condorelli SC George 2002 Free nitric oxide diffusion in the bronchial microcirculation Am. J. Physiol. Heart Circ. Physiol. 283 H2660 H2670 1:CAS:528:DC%2BD38XpvVWisrg%3D 12388292
9. RF Eich T Li DD Lemon DH Doherty SR Curry JF Aitken AJ Mathews KA Johnson RD Smith GN Phillips Jr JS Olson 1996 Mechanism of no-induced oxidation of myoglobin and hemoglobin Biochemistry 35 6976 6983 1:CAS:528:DyaK28XivFSls7Y%3D 10.1021/bi960442g 8679521 (Pubitemid 26182085)
10. NH El-Farra PD Christofides JC Liao 2003 Analysis of nitric oxide consumption by erythrocytes in blood vessels using a distributed multicellular model Ann. Biomed. Eng. 31 294 309 10.1114/1.1553454 12680727
11. XF Figueroa AD Martinez DR Gonzalez PI Jara S Ayala MP Boric 2001 In vivo assessment of microvascular nitric oxide production and its relation with blood flow Am. J. Physiol. Heart Circ. Physiol. 280 H1222 H1231 1:CAS:528: DC%2BD3MXjtV2gu7k%3D 11179067
12. E Gkaliagkousi J Ritter A Ferro 2007 Platelet-derived nitric oxide signaling and regulation Circ. Res. 101 654 662 1:CAS:528:DC%2BD2sXhtVOrsL%2FL 10.1161/CIRCRESAHA.107.158410 17901370 (Pubitemid 47494096)
13. HL Goldsmith GR Cokelet P Gaehtgens 1989 Robin fahraeus: evolution of his concepts in cardiovascular physiology Am. J. Physiol. 257 H1005 H1015 1:STN:280:DyaL1MzptVKmtw%3D%3D 2675631
14. TH Han A Pelling TJ Jeon JK Gimzewski JC Liao 2005 Erythrocyte nitric oxide transport reduced by a submembrane cytoskeletal barrier Biochim. Biophys. Acta. 1723 135 142 1:CAS:528:DC%2BD2MXks1Ghsr8%3D 15777627 (Pubitemid 40744681)
15. KT Huang TH Han DR Hyduke MW Vaughn H Van Herle TW Hein C Zhang L Kuo JC Liao 2001 Modulation of nitric oxide bioavailability by erythrocytes Proc. Natl Acad. Sci. U.S.A. 98 11771 11776 1:CAS:528:DC%2BD3MXnt12jtrs%3D 10.1073/pnas.201276698 11573011 (Pubitemid 32928804)
16. M Intaglietta NR Silverman WR Tompkins 1975 Capillary flow velocity measurements in vivo and in situ by television methods Microvasc. Res. 10 165 179 1:STN:280:DyaE28%2FltVGjtQ%3D%3D 10.1016/0026-2862(75)90004-7 1186524
17. AJ Kanai HC Strauss GA Truskey AL Crews S Grunfeld T Malinski 1995 Shear stress induces atp-independent transient nitric oxide release from vascular endothelial cells, measured directly with a porphyrinic microsensor Circ. Res. 77 284 293 1:CAS:528:DyaK2MXntFart7w%3D 7614715
18. 2 carriers Microvasc. Res. 66 49 58 1:CAS:528:DC%2BD3sXkvVejs7k%3D 10.1016/S0026-2862(03) 00008-6 12826074 (Pubitemid 36765444)
19. YM Kim CA Bombeck TR Billiar 1999 Nitric oxide as a bifunctional regulator of apoptosis Circ. Res. 84 253 256 1:CAS:528:DyaK1MXhsValu7Y%3D 10024298 (Pubitemid 29095565)
20. S Kim RL Kong AS Popel M Intaglietta PC Johnson 2007 Temporal and spatial variations of cell-free layer width in arterioles Am. J. Physiol. Heart Circ. Physiol. 293 H1526 H1535 1:CAS:528:DC%2BD2sXhtVOqtrzL 10.1152/ajpheart.01090. 2006 17526647 (Pubitemid 47367197)
21. S Kim PK Ong O Yalcin M Intaglietta PC Johnson 2009 The cell-free layer in microvascular blood flow Biorheology 46 181 189 1:CAS:528: DC%2BD1MXotVent7c%3D 19581726
22. MJ Kuchan JA Frangos 1994 Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells Am. J. Physiol. 266 C628 C636 1:CAS:528:DyaK2cXis1ahsLg%3D 8166225
23. L Kuo WM Chilian MJ Davis 1990 Coronary arteriolar myogenic response is independent of endothelium Circ. Res. 66 860 866 1:STN:280:DyaK3c7msl2mtQ%3D%3D 2306810 (Pubitemid 20086923)
24. 2 biotransport: a computer model Microcirculation 11 337 349 1:CAS:528:DC%2BD2cXns1Gltbg%3D 10.1080/10739680490437496 15280073 (Pubitemid 39619084)
25. BK Lee T Alexy RB Wenby HJ Meiselman 2007 Red blood cell aggregation quantitated via Myrenne aggregometer and yield shear stress Biorheology 44 29 35 1:CAS:528:DC%2BD2sXhtFagu7zF 17502687 (Pubitemid 46706552)
26. JC Liao TW Hein MW Vaughn KT Huang L Kuo 1999 Intravascular flow decreases erythrocyte consumption of nitric oxide Proc. Natl Acad. Sci. U.S.A. 96 8757 8761 1:CAS:528:DyaK1MXkslOktbc%3D 10.1073/pnas.96.15.8757 10411948 (Pubitemid 29354864)
27. X Liu MJ Miller MS Joshi H Sadowska-Krowicka DA Clark JR Lancaster Jr 1998 Diffusion-limited reaction of free nitric oxide with erythrocytes J. Biol. Chem. 273 18709 18713 1:CAS:528:DyaK1cXltFGrs7g%3D 10.1074/jbc.273.30.18709 9668042 (Pubitemid 28366253)
28. X Liu A Samouilov JR Lancaster Jr JL Zweier 2002 Nitric oxide uptake by erythrocytes is primarily limited by extracellular diffusion not membrane resistance J. Biol. Chem. 277 26194 26199 1:CAS:528:DC%2BD38XlsFKrt7g%3D 10.1074/jbc.M201939200 12006567 (Pubitemid 34967106)
29. N Maeda Y Suzuki J Tanaka N Tateishi 1996 Erythrocyte flow and elasticity of microvessels evaluated by marginal cell-free layer and flow resistance Am. J. Physiol. 271 H2454 H2461 1:CAS:528:DyaK2sXmtFKisg%3D%3D 8997305
30. Namgung, B., P. K. Ong, P. C. Johnson, and S. Kim. Effect of cell-free layer variation on arteriolar wall shear stress. Ann. Biomed. Eng., 2010 [Epub ahead of print].
31. B Namgung PK Ong YH Wong D Lim KJ Chun S Kim 2010 A comparative study of histogram-based thresholding methods for the determination of cell-free layer width in small blood vessels Physiol. Meas. 31 N61 N70 10.1088/0967-3334/31/9/ N01 20664158
32. PK Ong B Namgung PC Johnson S Kim 2010 Effect of erythrocyte aggregation and flow rate on cell-free layer formation in arterioles Am. J. Physiol. Heart Circ. Physiol. 298 H1870 H1878 1:CAS:528:DC%2BC3cXnslCgtLY%3D 10.1152/ajpheart.01182.2009 20348228
33. RM Palmer AG Ferrige S Moncada 1987 Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor Nature 327 524 526 1:CAS:528:DyaL2sXktlCjs70%3D 10.1038/327524a0 3495737 (Pubitemid 17085822)
34. RM Palmer DS Ashton S Moncada 1988 Vascular endothelial cells synthesize nitric oxide from l-arginine Nature 333 664 666 1:CAS:528:DyaL1cXktlGktb8%3D 10.1038/333664a0 3131684
35. AR Pries TW Secomb T Gessner MB Sperandio JF Gross P Gaehtgens 1994 Resistance to blood flow in microvessels in vivo Circ. Res. 75 904 915 1:CAS:528:DyaK2MXhslOqsLY%3D 7923637 (Pubitemid 24323525)
36. V Ranjan Z Xiao SL Diamond 1995 Constitutive nos expression in cultured endothelial cells is elevated by fluid shear stress Am. J. Physiol. 269 H550 H555 1:CAS:528:DyaK2MXns1Grtrc%3D 7544542
37. TW Secomb R Hsu AR Pries 1998 A model for red blood cell motion in glycocalyx-lined capillaries Am. J. Physiol. 274 H1016 H1022 1:CAS:528:DyaK1cXhvF2qtbc%3D 9530216
38. M Sharan AS Popel 2001 A two-phase model for flow of blood in narrow tubes with increased effective viscosity near the wall Biorheology 38 415 428 1:STN:280:DC%2BD383ptlWntA%3D%3D 12016324 (Pubitemid 34451112)
39. N Sogo KS Magid CA Shaw DJ Webb IL Megson 2000 Inhibition of human platelet aggregation by nitric oxide donor drugs: relative contribution of cgmp-independent mechanisms Biochem. Biophys. Res. Commun. 279 412 419 1:CAS:528:DC%2BD3cXovVCntbo%3D 10.1006/bbrc.2000.3976 11118301 (Pubitemid 32036706)
40. JR Stone MA Marletta 1996 Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide Biochemistry 35 1093 1099 1:CAS:528:DyaK28XivVeisw%3D%3D 10.1021/bi9519718 8573563 (Pubitemid 26050770)
41. NM Tsoukias M Kavdia AS Popel 2004 A theoretical model of nitric oxide transport in arterioles: frequency- vs. amplitude-dependent control of cgmp formation Am. J. Physiol. Heart Circ. Physiol. 286 H1043 H1056 1:CAS:528:DC%2BD2cXitlShsb8%3D 10.1152/ajpheart.00525.2003 14592938
42. MW Vaughn L Kuo JC Liao 1998 Effective diffusion distance of nitric oxide in the microcirculation Am. J. Physiol. 274 H1705 H1714 1:CAS:528: DyaK1cXjsV2jsrY%3D 9612383
43. MW Vaughn KT Huang L Kuo JC Liao 2000 Erythrocytes possess an intrinsic barrier to nitric oxide consumption J. Biol. Chem. 275 2342 2348 1:CAS:528:DC%2BD3cXpvFequg%3D%3D 10.1074/jbc.275.4.2342 10644684 (Pubitemid 30081991)
44. MW Vaughn KT Huang L Kuo JC Liao 2001 Erythrocyte consumption of nitric oxide: competition experiment and model analysis Nitric Oxide 5 18 31 1:CAS:528:DC%2BD3MXhtFems7w%3D 10.1006/niox.2000.0328 11178933 (Pubitemid 34146168)
45. A Vaya C Falco P Fernandez T Contreras M Valls J Aznar 2003 Erythrocyte aggregation determined with the Myrenne aggregometer at two modes (m0, m1) and at two times (5 and 10 sec) Clin. Hemorheol. Microcirc. 29 119 127 14610307 (Pubitemid 37485508)
46. H Wayland PC Johnson 1967 Erythrocyte velocity measurement in microvessels by a two-slit photometric method J. Appl. Physiol. 22 333 337 1:STN:280:DyaF2s%2FptVeksw%3D%3D 6017904
47. O Yalcin P Ulker U Yavuzer HJ Meiselman OK Baskurt 2008 Nitric oxide generation by endothelial cells exposed to shear stress in glass tubes perfused with red blood cell suspensions: role of aggregation Am. J. Physiol. Heart Circ. Physiol. 294 H2098 H2105 1:CAS:528:DC%2BD1cXmtVWguro%3D 10.1152/ajpheart.00015. 2008 18326799
48. J Zhang PC Johnson AS Popel 2009 Effects of erythrocyte deformability and aggregation on the cell free layer and apparent viscosity of microscopic blood flows Microvasc. Res. 77 265 272 10.1016/j.mvr.2009.01.010 19323969
49. Y Zhao PE Brandish DP Ballou MA Marletta 1999 A molecular basis for nitric oxide sensing by soluble guanylate cyclase Proc. Natl Acad. Sci. U.S.A. 96 14753 14758 1:CAS:528:DC%2BD3cXhtFahtw%3D%3D 10.1073/pnas.96.26.14753 10611285 (Pubitemid 30019712)
50. BS Zuckerbraun DA Stoyanovsky R Sengupta RA Shapiro BA Ozanich J Rao JE Barbato E Tzeng 2007 Nitric oxide-induced inhibition of smooth muscle cell proliferation involves s-nitrosation and inactivation of rhoa Am. J. Physiol. Cell Physiol. 292 C824 C831 1:CAS:528:DC%2BD2sXjt1GmurY%3D 10.1152/ajpcell. 00592.2005 16914531