Effects of intracellular acidosis on endothelial function: An overview

Journal of Critical Care

Volumn 27, Issue 2, 2012, Pages 108-118

  Crimi, Ettore ^a   Taccone, Fabio Silvio ^b   Infante, Teresa ^c   Scolletta, Sabino ^b   Crudele, Valeria ^d   Napoli, Claudio ^c,d  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b ERASME HOSPITAL   (Belgium)

^c IRCCS SDN   (Italy)

^d SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Acidosis; Endothelium; Intracellular; PH; Regulation

Indexed keywords

BICARBONATE; BRADYKININ; CALCIUM ION; CYTOKINE RECEPTOR; G PROTEIN COUPLED RECEPTOR; HISTAMINE; INTERLEUKIN 8; NITRIC OXIDE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; PROTEINASE ACTIVATED RECEPTOR; PROTON; SODIUM ION; TOLL LIKE RECEPTOR;

ACID BASE BALANCE; ACIDIFICATION; ACIDOSIS; ALKALINIZATION; ANION TRANSPORT; ARTICLE; CALCIUM CELL LEVEL; CATION EXCHANGE; CELL ACTIVATION; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL MEMBRANE POTENTIAL; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY DILATATION; ENDOTHELIUM CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HYPERCAPNIA; INRACELLULAR ACIDOSIS; PH; PH MEASUREMENT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ACIDOSIS; CALCIUM; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; HYDROGEN-ION CONCENTRATION; SODIUM-BICARBONATE SYMPORTERS; SODIUM-HYDROGEN ANTIPORTER; VASOCONSTRICTION; VASODILATION;

EID: 84858618050     PISSN: 08839441     EISSN: 15578615     Source Type: Journal    
DOI: 10.1016/j.jcrc.2011.06.001     Document Type: Article

References (108)

1. Ding H. The endothelium in compliance and resistance vessels. Front Biosci 2011, 3:730-744.
2. Tse D., Stan R.V. Morphological heterogeneity of endothelium. Semin Thromb Hemost 2010, 36:236-245.
3. Pries A.R., Secomb T.W., Gaehtgens P. The endothelial surface layer. Pflugers Arch 2000, 440:653-666.
4. Lu S.J., Ivanova Y., Feng Q., et al. Hemangioblasts from human embryonic stem cells generate multilayered blood vessels with functional smooth muscle cells. Regen Med 2009, 4:37-47.
5. Henry C.B., Duling B.R. Permeation of the luminal capillary glycocalyx is determined by hyaluronan. Am J Physiol 1999, 277:H508-H514.
6. Salvatore P., Pagliarulo C., Colicchio R., et al. CXCR4-CXCL12-dependent inflammatory network and endothelial progenitors. Curr Med Chem 2010, 17:3019-3029.
7. Fiorito C., Rienzo M., Crimi E., et al. Antioxidants increase number of progenitor endothelial cells through multiple gene expression pathways. Free Radic Res 2008, 42:754-762.
8. Chung A.S., Lee J., Ferrara N. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat Rev Cancer 2010, 10:505-514.
9. Abdelrahim M., Konduri S., Basha R., et al. Angiogenesis: an update and potential drug approaches. Int J Oncol 2010, 36:5-18.
10. Kyriakakis E., Cavallari M., Andert J., et al. Invariant natural killer T cells: linking inflammation and neovascularization in human atherosclerosis. Eur J Immunol 2010, 40:3268-3279.
11. Chesler M. Failure and function of intracellular pH regulation in acute hypoxic-ischemic injury of astrocytes. Glia 2005, 50:398-406.
12. Rodrigues S.F., Granger D.N. Role of blood cells in ischaemia-reperfusion induced endothelial barrier failure. Cardiovasc Res 2010, 87:291-299.
13. Napoli C. Oxidation of LDL, atherogenesis, and apoptosis. Ann NY Acad Sci 2003, 1010:698-709.
14. Tanaka K.A., Key N.S., Levy J.H. Blood coagulation: hemostasis and thrombin regulation. Anesth Analg 2009, 108:1433-1446.
15. Aird W.C. Vascular bed-specific hemostasis: role of endothelium in sepsis pathogenesis. Crit Care Med 2001, 29:S28-S34.
16. Montrucchio G., Alloatti G., Camussi G. Role of platelet-activating factor in cardiovascular pathophysiology. Physiol Rev 2000, 80:1669-1699.
17. Ait-Oufella H., Maury E., Lehoux S., et al. The endothelium: physiological functions and role in microcirculatory failure during severe sepsis. Intensive Care Med 2010, 36:1286-1298.
18. Zhang X., Rozengurt E., Reed E.F. HLA class I molecules partner with integrin β4 to stimulate endothelial cell proliferation and migration. Sci Signal 2010, 3:ra85.
19. Wakamoto S., Fujihara M., Takahashi D., et al. Enhancement of endothelial permeability by coculture with peripheral blood mononuclear cells in the presence of HLA class II antibody that was associated with transfusion-related acute lung injury. Transfusion 2010, 51:993-1001.
20. McEver R.P., Moore K.L., Cummings R.D. Leucocyte trafficking mediated by selectin-carbohydrate interactions. J Biol Chem 1995, 270:11025-11028.
21. Languino L.R., Plescia J., Duperray A., et al. Fibrinogen mediates leucocyte adhesion to vascular endothelium through an ICAM-1-dependent pathway. Cell 1993, 73:1423-1434.
22. Terry S., Nie M., Matter K., et al. Rho signalling and tight junction functions. Physiology 2010, 25:16-26.
23. Curry F.R., Adamson R.H. Vascular permeability modulation at the cell, microvessel, or whole organ level: towards closing gaps in our knowledge. Cardiovasc Res 2010, 87:218-229.
24. Denis C.V. Molecular and cellular biology of von Willebrand factor. Int J Hematol 2002, 75:3-8.
25. He J., Eastlack J.P., Bazan H.E. The induction of an angiogenic response in corneal myofibroblasts by platelet-activating factor (PAF). Curr Eye Res 2010, 35:1063-1071.
26. Napoli C., Cicala C., Wallace J.L., et al. Protease-activated receptor-2 modulates myocardial ischemia-reperfusion injury in the rat heart. Proc Natl Acad Sci USA 2000, 97:3678-3683.
27. Cirino G., Napoli C., Bucci M., et al. Inflammation-coagulation network: are serine protease receptors the knot?. Trends Pharmacol Sci 2000, 21:170-172.
28. Napoli C., de Nigris F., Wallace J.L., et al. Evidence that protease activated receptor 2 expression is enhanced in human coronary atherosclerotic lesions. J Clin Pathol 2004, 57:513-516.
29. Napoli C., De Nigris F., Cicala C., et al. Protease-activated receptor-2 activation improves efficiency of experimental ischemic preconditioning. Am J Physiol Heart Circ Physiol 2002, 282:H2004-H2010.
30. Baruch D. Platelet-vessel wall interactions. Therapie 2006, 61:371-378.
31. Balestrieri M.L., Balestrieri A., Mancini F.P., et al. Understanding the immunoangiostatic CXC chemokine network. Cardiovasc Res 2008, 78:250-256.
32. Harrington L.S., Belcher E., Moreno L., et al. Homeostatic role of Toll-like receptor 4 in the endothelium and heart. J Cardiovasc Pharmacol Ther 2007, 12:322-326.
33. Ignarro L.J., Cirino G., Casini A., et al. Nitric oxide as a signalling molecule in the vascular system: an overview. J Cardiovasc Pharmacol 1999, 34:879-886.
34. Napoli C., Ignarro L.J. Nitric oxide and atherosclerosis. Nitric Oxide 2001, 5:88-97.
35. Napoli C., de Nigris F., Williams-Ignarro S., et al. Nitric oxide and atherosclerosis: an update. Nitric Oxide 2006, 15:265-279.
36. Rabelink T.J., Luscher T.F. Endothelial nitric oxide synthase: host defense enzyme of the endothélium ?. Atheroscler Thromb Vasc Biol 2006, 26:267-271.
37. Liu V.W.T., Huang P.L. Cardiovascular roles of nitric oxide: a review of insights from nitric oxide synthase gene disrupted mice. Cardiovasc Res 2008, 77:19-29.
38. Wakabayashi I., Poteser M., Groschner K. Intracellular pH as a determinant of vascular smooth muscle function. J Vasc Res 2006, 43:238-250.
39. Busa W.B., Nuccitelli R. Metabolic regulation via intracellular pH. Am J Physiol 1984, 246:R409-R438.
40. Vaughan-Jones R.D., Spitzer K.W., Swietach P. Intracellular pH regulation in heart. J Mol Cell Cardiol 2009, 46:318-331.
41. Thomas R.C. Intracellular pH of snail neurones measured with a new pH-sensitive glass micro-electrode. J Physiol 1974, 238:159-180.
42. + influx in human fibroblasts. Biochem Biophys Res Commun 1982, 109:762-768.
43. Boyer M.J., Hedley D.W. Measurement of intracellular pH. Methods Cell Biol 1994, 41:135-148.
44. Frelin C., Vigne P., Ladoux A., et al. The regulation of the intracellular pH in cells from vertebrates. Eur J Biochem 1988, 174:3-14.
45. Boron W.F., De Weer P. Intracellular pH transients in squid giant axons caused by CO2, NH3, and metabolic inhibitors. J Gen Physiol 1976, 67:91-112.
46. Smith G.L., Austin C., Crichton C., et al. A review of the actions and control of intracellular pH in vascular smooth muscle. Cardiovascular Res 1998, 38:316-331.
47. Roos A., Boron W.F. Intracellular pH. Physiol Rev 1981, 61:296-434.
48. + antiport in pH-dependent cell death in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 2000, 278:L536-L544.
49. + efflux pathways in human vascular endothelial cells. Am J Physiol 1999, 277:H28-32.
50. Rojas J.D., Sennoune S.R., Maiti D., et al. Vacuolar-type H+-ATPases at the plasma membrane regulate pH and cell migration in microvascular endothelial cells. Am J Physiol Heart Circ Physiol 2006, 291:H1147-H1157.
51. Murer H., Hopfer U., Kinne R. Sodium/proton antiport in brush-border-membrane vesicles isolated from rat small intestine and kidney. Biochem J 1976, 154:597-604.
52. + exchange and the expression of cellular proto-oncogenes in mitogen- and phorbol ester-treated lymphocytes. J Biol Chem 1988, 263:8658-8665.
53. + antiport activity, isoform expression, and localization in endothelial cells. Am J Physiol 1998, 275:L442-L451.
54. Aharonovitz O., Zaun H.C., Balla T., et al. Intracellular pH regulation by Na(+)/H(+) exchange requires phosphatidylinositol 4,5-bisphosphate. J Cell Biol 2000, 150:213-224.
55. Aronson P.S., Nee J., Suhm M.A. Modifier role of internal H+ in activating the Na+-H+ exchanger in renal microvillus membrane vesicles. Nature 1982, 299:161-163.
56. Olsnes S., Tonnessen T.I., Sandvig K. pH-regulated anion antiport in nucleated mammalian cells. J Cell Biol 1986, 102:967-971.
57. Sipos H., Törocsik B., Tretter L., et al. Impaired regulation of pH homeostasis by oxidative stress in rat brain capillary endothelial cells. Cell Mol Neurobiol 2005, 25:141-151.
58. Crimi E., Ignarro L.J., Napoli C. Microcirculation and oxidative stress. Free Radic Res 2007, 41:1364-1375.
59. Mitchell J.H., Wildenthal K., Johnson R.L. The effects of acid-base disturbances on cardiovascular and pulmonary function. Kidney Int 1972, 1:375-389.
60. Celotto A.C., Capellini V.K., Baldo C.F., et al. Effects of acid-base imbalance on vascular reactivity. Braz J Med Biol Res 2008, 41:439-445.
61. Tritto I., Ambrosio G. Spotlight on microcirculation: an update. Cardiovasc Res 1999, 42:600-606.
62. Himmel H.M., Whorton A.R., Strauss H.C. Intracellular calcium, currents, and stimulus-response coupling in endothelial cells. Hypertension 1993, 21:112-127.
63. 2+ influx. Biochem J 1998, 330:695-699.
64. Jaffe E.A., Grulich J., Weksler B.B., et al. Correlation between thrombin-induced prostacyclin production and inositol trisphosphate and cytosolic free calcium levels in cultured human endothelial cells. J Biol Chem 1987, 262:8557-8565.
65. Napoli C., de Nigris F., Palinski W. Multiple role of reactive oxygen species in the arterial wall. J Cell Biochem 2001, 82:674-682.
66. Napoli C., Ignarro L.J. Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch Pharm Res 2009, 32:1103-1108.
67. Aalkjaer C., Poston L. Effects of pH on vascular tension: which are the important mechanisms?. Vasc Res 1996, 33:347-359.
68. Crimi E., Sica V., Slutsky A.S., et al. Role of oxidative stress in experimental sepsis and multisystem organ dysfunction. Free Radic Res 2006, 40:665-672.
69. Crimi E., Sica V., Williams-Ignarro S., et al. The role of oxidative stress in adult critical care. Free Radic Biol Med 2006, 40:398-406.
70. Aalkjaer C. Regulation of intracellular pH and its role in vascular smooth muscle function. J Hypertens 1990, 8:197-206.
71. Barnes P.J., Liu S.F. Regulation of pulmonary vascular tone. Pharmacol Rev 1995, 47:87-131.
72. Harder D.R. Effect of H+ and elevated PCO2 on membrane electrical properties of cat cerebral arteries. Pflugers Arch 1982, 349:182-185.
73. Wray S., Smith R.D. Mechanisms of action of pH-induced effects on vascular smooth muscle. Mol Cell Biochem 2004, 263:163-172.
74. Hattori K., Tsuchida S., Tsukahara H., et al. Augmentation of NO-mediated vasodilation in metabolic acidosis. Life Sci 2002, 71:1439-1447.
75. Aickin C.C. Direct measurement of intracellular pH and buffering power in smooth muscle cells of guinea-pig vas deferens. J Physiol 1984, 349:571-585.
76. Austin C., Wray S. Extracellular pH signals affect rat vascular tone by rapid transduction into intracellular pH changes. J Physiol 1993, 466:1-8.
77. Horie S., Yano S., Watanabe K. Intracellular alkalinization by NH4Cl increases cytosolic Ca2+ level and tension in the rat aortic smooth muscle. Life Sci 1995, 56:1835-1843.
78. Matthews J.G., Graves J.E., Poston L. Relationships between pHi and tension in isolated rat mesenteric resistance arteries. J Vasc Res 1992, 29:330-340.
79. 2+ of prostacyclin synthesis in rat aortic rings: effects of drugs and inorganic ions. Br J Pharmacol 1987, 91:439-446.
80. Mitchell J.A., de Nucci G., Warner T.D., et al. Alkaline buffers release EDRF from bovine cultured aortic endothelial cells. Br J Pharmacol 1991, 103:1295-1302.
81. 2+ entry pathways in vascular endothelial cells. Biochem J 1997, 323:567-573.
82. Asai M., Takeuchi K., Saotome M., et al. Extracellular acidosis suppresses endothelial function by inhibiting store-operated Ca2+ entry via non-selective cation channels. Cardiovasc Res 2009, 83:97-105.
83. Kazmaier S., Weyland A., Buhre W., et al. Effects of respiratory alkalosis and acidosis on myocardial blood flow and metabolism in patients with coronary artery disease. Anesthesiology 1998, 89:831-837.
84. Eliades D., Weiss H.R. Effect of hypercapnia on coronary circulation. Cardiovasc Res 1986, 20:127-133.
85. Gurevicius J., Salem M.R., Metwally A.A., et al. Contribution of nitric oxide to coronary vasodilation during hypercapnic acidosis. Am J Physiol 1995, 268:H39-47.
86. Heintz A., Koch T., Deussen A. Intact nitric oxide production is obligatory for the sustained flow response during hypercapnic acidosis in guinea pig heart. Cardiovasc Res 2005, 66:55-63.
87. Song D., O'Regan M.H., Phillis J.W. Role of nitric oxide in rat coronary flow regulation during respiratory and metabolic acidosis. Gen Pharmacol 1999, 32:571-575.
88. Phillis J.W., Song D., O'Regan M.H. The role of adenosine in rat coronary flow regulation during respiratory and metabolic acidosis. Eur J Pharmacol 1998, 356:199-206.
89. Phillis J.W., O'Regan M.H., Song D. Further evidence for the role of adenosine in hypercapnia/acidosis-evoked coronary flow regulation. Gen Pharmacol 1999, 33:431-437.
90. Phillis J.W., Song D., O'Regan M.H. Mechanisms involved in coronary artery dilatation during respiratory acidosis in the isolated perfused rat heart. Basic Res Cardiol 2000, 95:93-97.
91. Wang X., Wu J., Li L., et al. Hypercapnic acidosis activates KATP channels in vascular smooth muscles. Circ Res 2003, 92:1225-1232.
92. Modin A., Björne H., Herulf M., et al. Nitrite-derived nitric oxide: a possible mediator of 'acidic-metabolic' vasodilatation. Acta Physiol Scand 2001, 171:9-16.
93. Subramaniam G., Achike F.I., Mustafa M.R. Effect of acidosis on the mechanism(s) of insulin-induced vasorelaxation in normal Wistar-Kyoto (WKY) rat aorta. Regul Pept 2009, 155:70-75.
94. Yeo J.L., Tan B.T., Achike F.I. Exploring the mechanism of endothelial involvement in acidosis-induced vasodilatation of aortic tissues from normal and diabetic rats. Eur J Pharmacol 2010, 642:99-106.
95. Redlin M., Werner J., Habazettl H., et al. Cariporide (HOE 642) attenuates leukocyte activation in ischemia and reperfusion. Anesth Analg 2001, 93:1472-1479.
96. Collins D.M., McCullough W.T., Ellsworth M.L. Conducted vascular responses: communication across the capillary bed. Microvasc Res 1998, 56:43-53.
97. Ladilov Y., Schäfer C., Held A., et al. Mechanism of Ca(2+) overload in endothelial cells exposed to simulated ischemia. Cardiovasc Res 2000, 47:394-403.
98. - exchange. Cell Physiol Biochem 1998, 8:202-211.
99. Parra-Bonilla G., Alvarez D.F., Al-Mehdi A.B., et al. Critical role for lactate dehydrogenase A in aerobic glycolysis that sustains pulmonary microvascular endothelial cell proliferation. Am J Physiol Lung Cell Mol Physiol 2010, 299:L513-L522.
100. Besse S., Tanguy S., Boucher F., et al. Protection of endothelial-derived vasorelaxation with cariporide, a sodium-proton exchanger inhibitor, after prolonged hypoxia and hypoxia-reoxygenation: effect of age. Eur J Pharmacol 2006, 531:187-193.
101. Huck V., Niemeyer A., Goerge T., et al. Delay of acute intracellular pH recovery after acidosis decreases endothelial cell activation. J Cell Physiol 2007, 211:399-409.
102. Ambrosio G., Flather M.D., Böhm M., et al. β-blockade with nebivolol for prevention of acute ischaemic events in elderly patients with heart failure. Heart 2011, 97:209-214.
103. Inserte J., Barba I., Hernando V., et al. Effect of acidic reperfusion on prolongation of intracellular acidosis and myocardial salvage. Cardiovasc Res 2008, 77:782-790.
104. Yamamoto S., Matsui K., Itoh N., et al. The effect of an Na+/H+ exchange inhibitor, SM-20550 on ischemia/reperfusion-induced endothelial dysfunction in isolated perfused rat hearts. Int J Tissue React 2001, 23:1-7.
105. López D., Rodríguez-Sinovas A., Agulló L., et al. Acidic reoxygenation protects against endothelial dysfunction in rat aortic rings submitted to simulated ischemia. Am J Physiol Heart Circ Physiol 2008, 295:H2409-H2416.
106. Ferrazzano P., Shi Y., Manhas N., et al. Inhibiting the Na+/H+ exchanger reduces reperfusion injury: a small animal MRI study. Front Biosci 2011, 3:81-88.
107. Théroux P., Chaitman B.R., Danchin N., et al. Inhibition of the sodium-hydrogen exchanger with cariporide to prevent myocardial infarction in high-risk ischemic situations. Main results of the GUARDIAN trial. Guard during ischemia against necrosis (GUARDIAN) Investigators. Circulation 2000, 102:3032-3038.
108. Park S.L., Lee D.H., Yoo S.E., et al. The effect of Na(+)/H(+) exchanger-1 inhibition by sabiporide on blood-brain barrier dysfunction after ischemia/hypoxia in vivo and in vitro. Brain Res 2010, 1366:189-196.