Electrochemical study of the intracellular transduction of vascular endothelial growth factor induced nitric oxide synthase activity using a multi-channel biocompatible microelectrode array

Biochimica et Biophysica Acta - General Subjects

Volumn 1800, Issue 9, 2010, Pages 929-936

  Trouillon, Raphaël ^a   Cheung, Christine ^a   Patel, Bhavik Anil ^a,b   O'Hare, Danny ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF BRIGHTON   (United Kingdom)

Author keywords

Biocompatibility; Biomeasurement; Electrochemistry; Fibronectin; Nitric oxide; Vascular endothelial growth factor

Indexed keywords

FIBRONECTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; VASCULOTROPIN; ENZYME INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOCOMPATIBILITY; CELL ASSAY; CELL CULTURE; CELL MIGRATION; CONTROLLED STUDY; ELECTROCHEMICAL ANALYSIS; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME SYNTHESIS; MICROELECTRODE; NONHUMAN; POTENTIOMETRY; PRIORITY JOURNAL; SENSOR; SIGNAL TRANSDUCTION; SWINE; VASCULAR RING; ANIMAL; ANTAGONISTS AND INHIBITORS; AORTA; BIOSYNTHESIS; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; ENZYME INDUCTION; ENZYMOLOGY; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; AORTA; CELLS, CULTURED; ELECTROCHEMICAL TECHNIQUES; ENDOTHELIAL CELLS; ENZYME INDUCTION; ENZYME INHIBITORS; FIBRONECTINS; MICE; MICROELECTRODES; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOVASCULARIZATION, PHYSIOLOGIC; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION; SWINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77955276309     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2010.04.010     Document Type: Article

References (60)

1. Moncada S., Palmer R., Higgs E. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 1991, 43:109-142.
2. Bredt D., Snyder S. Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 1994, 63(1):175-195.
3. Knowles R., Palacios M., Palmer R., Moncada S. Formation of nitric oxide from l-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc. Nat. Acad. Sci. U.S.A. 1989, 86(13):5159-5162.
4. Bredt D., Hwang P., Snyder S. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 1990, 347:768-770.
5. Calabrese V., Mancuso C., Calvani M., Rizzarelli E., Butterfield D., Giuffrida Stella A. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 2007, 8(10):766-775.
6. Assreuy J., Cunha F., Epperlein M., Noronha-Dutra A., O'Donnell C., Liew F., Moncada S. Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major. Eur. J. Immunol. 1994, 24(3):672-676.
7. Nathan C., Hibbs J. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 1991, 3(1):65-70.
8. Palmer R., Ferrige A., Moncada S., et al. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987, 327(6122):524-526.
9. Cooke J., Dzau V. Nitric oxide synthase: role in the genesis of vascular disease. Annu. Rev. Med. 1997, 48(1):489-509.
10. Steinberg H., Brechtel G., Johnson A., Fineberg N., Baron A. Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J. Clin. Invest. 1994, 94(3):1172-1179.
11. Ferrara N. Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am. J. Physiol. Cell Physiol. 2001, 280(6):1358-1366.
12. Fukumura D., Gohongi T., Kadambi A., Izumi Y., Ang J., Yun C., Buerk D., Huang P., Jain R. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Nat. Acad. Sci. U.S.A. 2001, 98(5):2604-2609.
13. Goligorsky M., Budzikowski A., Tsukahara H., Noiri E. Co-operation between endothelin and nitric oxide in promoting endothelial cell migration and angiogenesis. Clin. Exp. Pharmacol. Physiol. 1999, 26(3):269-271.
14. Carmeliet P., Jain R. Angiogenesis in cancer and other diseases. Nature 2000, 407(6801):249-257.
15. Fukumura D., Jain R. Role of nitric oxide in angiogenesis and microcirculation in tumors. Cancer Metastasis Rev. 1998, 17(1):77-89.
16. Harding K., Morris H., Patel G. Healing chronic wounds. B.M.J. 2002, 324(7330):160-163.
17. Baum O., Da Silva-Azevedo L., Willerding G., Wockel A., Planitzer G., Gossrau R., Pries A., Zakrzewicz A. Endothelial NOS is main mediator for shear stress-dependent angiogenesis in skeletal muscle after prazosin administration. Am. J. Physiol. Heart Circ. Physiol. 2004, 287(5):2300-2308.
18. Buga G., Gold M., Fukuto J., Ignarro L. Shear stress-induced release of nitric oxide from endothelial cells grown on beads. Hypertension 1991, 17(2):187-193.
19. Clark E., Brugge J. Integrins and signal transduction pathways: the road taken. Science 1995, 268(5208):233-239.
20. Feng Y., Venema V., Venema R., Tsai N., Caldwell R. VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem. Biophys. Res. Commun. 1999, 256(1):192-197.
21. Morbidelli L., Chang C., Douglas J., Granger H., Ledda F., Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am. J. Physiol. Heart Circ. Physiol. 1996, 270(1):H411-H415.
22. Papapetropoulos A., Garcia-Cardena G., Madri J., Sessa W. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 1997, 100(12):3131-3139.
23. Bouloumie A., Schini-Kerth V., Busse R. Vascular endothelial growth factor up-regulates nitric oxide synthase expression in endothelial cells. Cardiovasc. Res. 1999, 41(3):773-780.
24. Palmer R., Ashton D., Moncada S. Vascular endothelial cells synthesize nitric oxide from l-arginine. Nature 1988, 333:664-666.
25. Moncada S., Higgs E. Mechanisms of disease: the l-arginine-nitric oxide pathway. N. Engl. J. Med. 1993, 329:2002-2012.
26. Rees D., Palmer R., Schulz R., Hodson H., Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br. J. Pharmacol. 1990, 101:746-752.
27. Kubes P., Suzuki M., Granger D., et al. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:4651-4655.
28. Sessa W., Pritchard K., Seyedi N., Wang J., Hintze T. Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circ. Res. 1994, 74(2):349-353.
29. Bredt D., Snyder S. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl. Acad. Sci. U.S.A. 1989, 86(22):9030-9033.
30. Bredt D., Snyder S., et al. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. U.S.A. 1990, 87(2):682-685.
31. Patel B., Arundell M., Parker K., Yeoman M., O'Hare D. Detection of nitric oxide release from single neurons in the pond snail, Lymnaea stagnalis. Anal. Chem. 2006, 78(22):7643-7648.
32. Bedioui F., Villeneuve N. Electrochemical nitric oxide sensors for biological samples-principle, selected examples and applications. Electroanalysis 2003, 15(1):5-18.
33. Bedioui F., Trevin S., Devynck J. Chemically modified microelectrodes designed for the electrochemical determination of nitric oxide in biological systems. Electroanalysis 1996, 8(12):1085-1091.
34. Bedioui F., Trevin S., Dvynck J., Lantoine F., Brunet A., Devynck M. Elaboration and use of nickel planar macrocyclic complex-based sensors for the direct electrochemical measurement of nitric oxide in biological media. Biosens. Bioelectron. 1997, 12(3):205-212.
35. Amatore C., Arbault S., Bruce D., Oliveira P., Erard M., Vuillaume M. Analysis of individual biochemical events based on artificial synapses using ultramicroelectrodes: cellular oxidative burst. Faraday Discuss. 2000, 116:319-333.
36. Arbault S., Sojic N., Bruce D., Amatore C., Sarasin A., Vuillaume M. Oxidative stress in cancer prone xeroderma pigmentosum fibroblasts. Real-time and single cell monitoring of superoxide and nitric oxide production with microelectrodes. Carcinogenesis 2004, 25(4):509-515.
37. Amatore C., Arbault S., Bouret Y., Cauli B., Guille M., Rancillac A., Rossier J. Nitric oxide release during evoked neuronal activity in cerebellum slices: detection with platinized carbon-fiber microelectrodes. Chem. Phys. Chem. 2006, 7(1):181-187.
38. Malinski T., Taha Z. Nitric oxide release from a single cell measured in situ by a porphyrinic-based microsensor. Nature 1992, 358:676-678.
39. Balligand J., Ungureanu-Longrois D., Simmons W., Pimental D., Malinski T., Kapturczak M., Taha Z., Lowenstein C., Davidoff A., Kelly R. Cytokine-inducible nitric oxide synthase (iNOS) expression in cardiac myocytes. Characterization and regulation of iNOS expression and detection of iNOS activity in single cardiac myocytes in vitro. J. Biol. Chem. 1994, 269(44). 27580-25788.
40. Patel B., Arundell M., Quek R., Harvey S., Ellis I., Florence M., Cass A., Schor A., O'Hare D. Individually addressable microelectrode array for monitoring oxygen and nitric oxide release. Anal. Bioanal. Chem. 2008, 390(5):1379-1387.
41. Oni J., Pailleret A., Isik S., Diab N., Radtke I., Blöchl A., Jackson M., Bedioui F., Schuhmann W. Functionalised electrode array for the detection of nitric oxide released by endothelial cells using different NO-sensing chemistries. Anal. Bioanal. Chem. 2004, 378(6):1594-1600.
42. Zhang B., Adams K., Luber S., Eves D., Heien M., Ewing A. Spatially and temporally resolved single-cell exocytosis utilizing individually addressable carbon microelectrode arrays. Anal. Chem. 2008, 80(5):1394-1400.
43. Isik S., Berdondini L., Oni J., Blöchl A., Koudelka-Hep M., Schuhmann W. Cell-compatible array of three-dimensional tip electrodes for the detection of nitric oxide release. Biosens. Bioelectron. 2005, 20(8):1566-1572.
44. Kamei K., Mie M., Yanagida Y., Aizawa M., Kobatake E. Construction and use of an electrochemical NO sensor in a cell-based assessing system. Sens. Actuators, B 2004, 99(1):106-112.
45. Trouillon R., Cheung C., Patel B., O'Hare D. Comparative study of poly (styrene-sulfonate)/poly (l-lysine) and fibronectin as biofouling-preventing layers in dissolved oxygen electrochemical measurements. Analyst 2009, 134(4):784-793.
46. Trouillon R., Combs Z., Patel B., O'Hare D. Comparative study of the effect of various electrode membranes on biofouling and electrochemical measurements. Electrochem. Commun. 2009, 11:1409-1413.
47. Tomeš J. Polarographic studies with the dropping mercury cathode. LXVII. Equations of the polarographic wave in the electrodeposition of hydrogen from strong and weak acid, Collect. Czechoslov. Chem. Commun. 1937, 9:150-167.
48. Bard A., Faulkner L. Electrochemical Methods: Fundamentals and Applications 1980, John Wiley & Sons.
49. Betlach M., Tiedje J. Kinetic explanation for accumulation of nitrite, nitric oxide, and nitrous oxide during bacterial denitrification. Appl. Environ. Microbiol. 1981, 42(6):1074-1084.
50. Reinhart-King C. Endothelial cell adhesion and migration. Angiogenesis: In Vitro Syst. 2008, 45-64.
51. Breslin J., Pappas P., Cerveira J., Hobson R., Duran W. VEGF increases endothelial permeability by separate signaling pathways involving ERK-1/2 and nitric oxide. Am. J. Physiol. Heart. Circ. Physiol. 2003, 284(1):H92-H100.
52. Chlench S., Mecha Disassa N., Hohberg M., Hoffmann C., Pohlkamp T., Beyer G., Bongrazio M., Da Silva-Azevedo L., Baum O., Pries A., et al. Regulation of Foxo-1 and the angiopoietin-2/Tie2 system by shear stress. FEBS Lett. 2007, 581(4):673-680.
53. Radomski M., Palmer R., Moncada S. Characterization of the l-arginine: nitric oxide pathway in human platelets. Br. J. Pharmacol. 1990, 101(2):325-328.
54. G-nitro-l-arginine methyl ester in humans. J. Physiol. 2001, 531(1):257-264.
55. He H., Venema V., Gu X., Venema R., Marrero M., Caldwell R. Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J. Biol. Chem. 1999, 274(35):25130-25135.
56. Wu H., Yuan Y., Zawieja D., Tinsley J., Granger H. Role of phospholipase C, protein kinase C, and calcium in VEGF-induced venular hyperpermeability. Am. J. Physiol. Heart Circ. Physiol. 1999, 276(2):H535-H542.
57. Dimmeler S., Dernbach E., Zeiher A. Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett. 2000, 477(3):258-262.
58. Zachary I. VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem. Soc. Trans. 2003, 31:1171-1177.
59. Dimmeler S., Breitschopf K., Haendeler J., Zeiher A. Dephosphorylation targets Bcl-2 for ubiquitin-dependent degradation: a link between the apoptosome and the proteasome pathway. J. Exp. Med. 1999, 189(11):1815-1822.
60. Parenti A., Morbidelli L., Cui X., Douglas J., Hood J., Granger H., Ledda F., Ziche M. Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase1/2 activation in postcapillary endothelium. J. Biol. Chem. 1998, 273(7):4220-4226.