Structural adaptation of microvessel diameters in response to metabolic stimuli: Where are the oxygen sensors?

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 297, Issue 6, 2009, Pages

  Reglin, Bettina ^a   Secomb, Timothy W ^c   Pries, Axel R ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b DEUTSCHES HERZZENTRUM BERLIN   (Germany)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Angioadaptation; Oxygen sensing; Vascular diameter

Indexed keywords

OXYGEN;

ADAPTATION; ANGIOGENESIS; ARTICLE; BLOOD FLOW; HEMODYNAMICS; HYPOXIA; MALE; MICROVASCULATURE; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SENSOR; SIGNAL TRANSDUCTION; SMOOTH MUSCLE TONE; STEADY STATE; STIMULUS RESPONSE; TISSUE OXYGENATION; VELOCITY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANOXIA; COMPUTER SIMULATION; ERYTHROCYTES; HEMODYNAMICS; KINETICS; MALE; MESENTERY; MICROSCOPY, VIDEO; MICROVESSELS; MODELS, CARDIOVASCULAR; OXYGEN; OXYGEN CONSUMPTION; RATS; SIGNAL TRANSDUCTION; SPLANCHNIC CIRCULATION;

EID: 72249086773     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00348.2009     Document Type: Article

References (70)

1. Altman PL, Dittmer DS. In: Respiration and Circulation, Bethesda, MD: Fed. Am. Soc. Exp. Biol., 1971, p. 139.
2. Arciero JC, Carlson BE, Secomb TW. Theoretical model of metabolic blood flow regulation: roles of ATP release by red blood cells and conducted responses. Am J Physiol Heart Circ Physiol 295: H1562-H1571, 2008.
3. Bakker EN, Der Meulen ET, Spaan JA, VanBavel E. Organoid culture of cannulated rat resistance arteries: effect of serum factors on vasoactivity and remodeling. Am J Physiol Heart Circ Physiol 278: H1233-H1240, 2000. (Pubitemid 30235501)
4. Barber BJ, Oppenheimer J, Zawieja DC, Zimmermann HA. Variations in rat mesenteric tissue thickness due to microvasculature. Am J Physiol Gastrointest Liver Physiol 253: G549-G556, 1987.
5. Bergfeld GR, Forrester T. Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia. Cardiovasc Res 26: 40-47, 1992.
6. Berne RM. Cardiac nucleotides in hypoxia: possible role in regulation of coronary blood flow. Am J Physiol 204: 317-322, 1963.
7. 2+ dynamics during blood flow control in hamster cheek pouch. J Appl Physiol 101: 307-315, 2006.
8. Broten TP, Romson JL, Fullerton DA, Van Winkle DM, Feigl EO. Synergistic action of myocardial oxygen and carbon dioxide in controlling coronary blood flow. Circ Res 68: 531-542, 1991.
9. Busse R, Pohl U, Kellner C, Klemm U. Endothelial cells are involved in the vasodilatory response to hypoxia. Pflügers Arch 397: 78-80, 1983.
10. Clark A Jr, Federspiel WJ, Clark PA, Cokelet GR. Oxygen delivery from red cells. Biophys J 47: 171-181, 1985.
11. Collins DM, McCullough WT, Ellsworth ML. Conducted vascular responses: communication across the capillary bed. Microvasc Res 56: 43-53, 1998.
12. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO III, Gladwin MT. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9: 1498-1505, 2003. (Pubitemid 38004777)
13. Costa LE, Mendez G, Boveris A. Oxygen dependence of mitochondrial function measured by high-resolution respirometry in long-term hypoxic rats. Am J Physiol Cell Physiol 273: C852-C858, 1997. (Pubitemid 27422164)
14. Dalsgaard T, Simonsen U, Fago A. Nitrite-dependent vasodilation is facilitated by hypoxia and is independent of known NO-generating nitrite reductase activities. Am J Physiol Heart Circ Physiol 292: H3072-H3078, 2007. (Pubitemid 47084562)
15. Dietrich HH, Ellsworth ML, Sprague RS, Dacey RG Jr. Red blood cell regulation of microvascular tone through adenosine triphosphate. Am J Physiol Heart Circ Physiol 278: H1294-H1298, 2000.
16. Duling BR, Berne RM. Longitudinal gradients in periarteriolar oxygen tension. Circ Res 27: 669-678, 1970.
17. 2 in the vicinity of the pial vessels of the cat. Pflügers Arch 383: 29-34, 1979.
18. Dworkin M, Keller KH. Solubility and diffusion coefficient of adenosine 3′:5′-monophosphate. J Biol Chem 252: 864-865, 1977. (Pubitemid 8041875)
19. Earley S, Pastuszyn A, Walker BR. Cytochrome p-450 epoxygenase products contribute to attenuated vasoconstriction after chronic hypoxia. Am J Physiol Heart Circ Physiol 285: H127-H136, 2003. (Pubitemid 36736423)
20. Ellsworth ML. Red blood cell-derived ATP as a regulator of skeletal muscle perfusion. Med Sci Sports Exerc 36: 35-41, 2004.
21. Ellsworth ML, Forrester T, Ellis CG, Dietrich HH. The erythrocyte as a regulator of vascular tone. Am J Physiol Heart Circ Physiol 269: H2155-H2161, 1995.
22. Figueroa XF, Duling BR. Gap junctions in the control of vascular function. Antioxid Redox Signal 11: 251-266, 2009.
23. Fujino H, Kohzuki H, Takeda I, Kiyooka T, Miyasaka T, Mohri S, Shimizu J, Kajiya F. Regression of capillary network in atrophied soleus muscle induced by hindlimb unweighting. J Appl Physiol 98: 1407-1413, 2005. (Pubitemid 40396517)
24. Gladwin MT, Crawford JH, Patel RP. The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Radic Biol Med 36: 707-717, 2004. (Pubitemid 38264415)
25. Goldman D, Popel AS. A computational study of the effect of capillary network anastomoses and tortuosity on oxygen transport. J Theor Biol 206: 181-194, 2000. (Pubitemid 30728721)
26. Golub AS, Barker MC, Pittman RN. Microvascular oxygen tension in the rat mesentery. Am J Physiol Heart Circ Physiol 294: H21-H28, 2008.
27. 2 profiles near arterioles and tissue oxygen consumption in rat mesentery. Am J Physiol Heart Circ Physiol 293: H1097-H1106, 2007.
28. Gonzalez-Alonso J, Mortensen SP, Dawson EA, Secher NH, Damsgaard R. Erythrocytes and the regulation of human skeletal muscle blood flow and oxygen delivery: role of erythrocyte count and oxygenation state of haemoglobin. J Physiol 572: 295-305, 2006.
29. Gonzalez-Alonso J, Olsen DB, Saltin B. Erythrocyte and the regulation of human skeletal muscle blood flow and oxygen delivery: role of circulating ATP. Circ Res 91: 1046-1055, 2002. (Pubitemid 35416642)
30. Gray LH, Steadman JM. Determination of the oxyhemoglobin dissociation curves for mouse and rat blood. J Physiol 175: 161-171, 1964.
31. Grser T, Rubanyi GM. Different mechanisms of hypoxic relaxation in canine coronary arteries and rat abdominal aortas. J Cardiovasc Pharmacol 20, Suppl 12: S117-S119, 1992.
32. Hacking WJG, VanBavel E, Spaan JAE. Shear stress is not sufficient to control growth of vascular networks: a model study. Am J Physiol Heart Circ Physiol 270: H364-H375, 1996. (Pubitemid 26065144)
33. Hellums JD, Nair PK, Huang NS, Ohshima N. Simulation of intraluminal gas transport processes in the microcirculation. Ann Biomed Eng 24: 1-24, 1996. (Pubitemid 26028127)
34. Hester RL, Hammer LW. Venular-arteriolar communication in the regulation of blood flow. Am J Physiol Regul Integr Comp Physiol 282: R1280-R1285, 2002. (Pubitemid 34664511)
35. Hubley MJ, Rosanske RC, Moerland TS. Diffusion coefficients of ATP and creatine phosphate in isolated muscle: pulsed gradient 31P NMR of small biological samples. NMR Biomed 8: 72-78, 1995.
36. Hudetz AG, Kiani MF. The role of wall shear stress in microvascular network adaptation. Adv Exp Med Biol 316: 31-39, 1992.
37. Jackson WF. Arteriolar oxygen reactivity: where is the sensor? Am J Physiol Heart Circ Physiol 253: H1120-H1126, 1987.
38. Jackson WF, Duling BR. The oxygen sensitivity of hamster cheek pouch arterioles. In vitro and in situ studies. Circ Res 53: 515-525, 1983.
39. 2 delivery mediated by hemoglobin oxygenation. Am J Physiol Heart Circ Physiol 280: H2833-H2839, 2001.
40. Jia L, Bonaventura C, Bonaventura J, Stamler JS. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380: 221-226, 1996. (Pubitemid 26090643)
41. Kano Y, Shimegi S, Takahashi H, Masuda K, Katsuta S. Changes in capillary luminal diameter in rat soleus muscle after hind-limb suspension. Acta Physiol Scand 169: 271-276, 2000.
42. Kerkhof CJ, van der Linden PJ, Sipkema P. Role of myocardium and endothelium in coronary vascular smooth muscle responses to hypoxia. Am J Physiol Heart Circ Physiol 282: H1296-H1303, 2002. (Pubitemid 34654881)
43. Marshall JM. Adenosine and muscle vasodilatation in acute systemic hypoxia. Acta Physiol Scand 168: 561-573, 2000. (Pubitemid 30197893)
44. Martinez-Lemus LA, Hill MA, Bolz SS, Pohl U, Meininger GA. Acute mechanoadaptation of vascular smooth muscle cells in response to continuous arteriolar vasoconstriction: implications for functional remodeling. FASEB J 18: 708-710, 2004.
45. Messina EJ, Sun D, Koller A, Wolin MS, Kaley G. Increases in oxygen tension evoke arteriolar constriction by inhibiting endothelial prostaglandin synthesis. Microvasc Res 48: 151-160, 1994. (Pubitemid 24315711)
46. Nagababu E, Ramasamy S, Abernethy DR, Rifkind JM. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J Biol Chem 278: 46349-46356, 2003. (Pubitemid 37452205)
47. Nelder JA, Mead R. A simplex method for function minimization. Comput J 7: 308-313, 1965.
48. Pawloski JR, Hess DT, Stamler JS. Export by red blood cells of nitric oxide bioactivity. Nature 409: 622-626, 2001. (Pubitemid 32154814)
49. 2 from an arteriole with arrested flow. Adv Exp Med Biol 566: 257-262, 2005.
50. Pohl U, Busse R. Hypoxia stimulates release of endothelium-derived relaxant factor. Am J Physiol Heart Circ Physiol 256: H1595-H1600, 1989.
51. Pries AR. A versatile video image analysis system for microcirculatory research. Int J Microcirc Clin Exp 7: 327-345, 1988.
52. Pries AR, Kanzow G, Gaehtgens P. Microphotometric determination of hematocrit in small vessels. Am J Physiol Heart Circ Physiol 245: H167-H177, 1983. (Pubitemid 14231584)
53. Pries AR, Ley K, Claassen M, Gaehtgens P. Red cell distribution at microvascular bifurcations. Microvasc Res 38: 81-101, 1989. (Pubitemid 19188540)
54. Pries AR, Ley K, Gaehtgens P. Generalization of the Fahraeus principle for microvessel networks. Am J Physiol Heart Circ Physiol 251: H1324-H1332, 1986.
55. Pries AR, Reglin B, Secomb TW. Structural adaptation of microvascular networks: functional roles of adaptive responses. Am J Physiol Heart Circ Physiol 281: H1015-H1025, 2001. (Pubitemid 32879235)
56. Pries AR, Reglin B, Secomb TW. Structural response of microcirculatory networks to changes in demand: information transfer by shear stress. Am J Physiol Heart Circ Physiol 284: H2204-H2212, 2003. (Pubitemid 36622433)
57. Pries AR, Secomb TW. Microvascular blood viscosity in vivo and the endothelial surface layer. Am J Physiol Heart Circ Physiol 289: H2657-H2664, 2005.
58. Pries AR, Secomb TW, Gaehtgens P. Design principles of vascular beds. Circ Res 77: 1017-1023, 1995.
59. Pries AR, Secomb TW, Gaehtgens P. Structural adaptation and stability of microvascular networks: theory and simulations. Am J Physiol Heart Circ Physiol 275: H349-H360, 1998. (Pubitemid 128734401)
60. Pries AR, Secomb TW, Gaehtgens P, Gross JF. Blood flow in microvascular networks: experiments and simulation. Circ Res 67: 826-834, 1990. (Pubitemid 20315014)
61. Pries AR, Secomb TW, Gessner T, Sperandio MB, Gross JF, Gaehtgens P. Resistance to blood flow in microvessels in vivo. Circ Res 75: 904-915, 1994. (Pubitemid 24323525)
62. 2 of skeletal muscle in vivo. Am J Physiol Heart Circ Physiol 277: H1831-H1840, 1999.
63. Segal SS, Duling BR. Flow control among microvessels coordinated by intercellular conduction. Science 234: 868-870, 1986.
64. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, Piantadosi CA. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276: 2034-2037, 1997. (Pubitemid 27443606)
65. Taggart MJ, Wray S. Hypoxia and smooth muscle function: key regulatory events during metabolic stress. J Physiol 509: 315-325, 1998. (Pubitemid 28286991)
66. Tsai AG, Friesenecker B, Mazzoni MC, Kerger H, Buerk DG, Johnson PC, Intaglietta M. Microvascular and tissue oxygen gradients in the rat mesentery. Proc Natl Acad Sci USA 95: 6590-6595, 1998. (Pubitemid 28278024)
67. Vadapalli A, Pittman RN, Popel AS. Estimating oxygen transport resistance of the microvascular wall. Am J Physiol Heart Circ Physiol 279: H657-H671, 2000. (Pubitemid 30672778)
68. Wilson DF, Lee WM, Makonnen S, Finikova O, Apreleva S, Vinogradov SA. Oxygen pressures in the interstitial space and their relationship to those in the blood plasma in resting skeletal muscle. J Appl Physiol 101: 1648-1656, 2006. (Pubitemid 44904485)
69. 2 distribution maps. Am J Physiol Heart Circ Physiol 270: H1390-H1397, 1996.
70. Zakrzewicz A, Secomb TW, Pries AR. Angioadaptation: keeping the vascular system in shape. News Physiol Sci 17: 197-201, 2002.