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An electrochemical functional assay for the sensing of nitric oxide release induced by angiogenic factors

  • Received : 2011.10.14
  • Published : 2011.11.30
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Abstract

Nitric oxide (NO) is a critical biological mediator involved in numerous diseases. However, the short lifetime of this molecule in biological conditions can make its study in situ complicated. Here, we review some recent results on the role of NO in angiogenesis, obtained using a biocompatible microelectrode array. This simple system allowed for the quick and easy quantification of NO released from cells grown directly on the surface of the sensor. We have used this technology to demonstrate that angiogenin induces NO release, and to partially elucidate its intracellular transduction pathway.

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References

  1. Moncada, S., Palmer, R. and Higgs, E. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 143, 109-141.
  2. Cooke, J. and Dzau, V. (1997) Nitric oxide synthase: role in the genesis of vascular disease. Annu. Rev. Med. 48, 489-510. https://doi.org/10.1146/annurev.med.48.1.489
  3. Palmer, R., Ferrige, A. and Moncada, S. (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327, 524-526. https://doi.org/10.1038/327524a0
  4. Bogdan, C. (2001) Nitric oxide and the immune response. Nat. Immunol. 2, 907-916. https://doi.org/10.1038/ni1001-907
  5. Moilanen, E. and Vapaatalo, H. (1995) Nitric oxide in inflammation and immune response. Ann. Med. 27, 359-367. https://doi.org/10.3109/07853899509002589
  6. Bredt, D., Hwang, P. and Snyder, S. (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347, 768-770. https://doi.org/10.1038/347768a0
  7. Calabrese, V., Mancuso, C., Calvani, M., Rizzarelli, E., Butterfield, D. and Giuffrida Stella, A. (2007) Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 8, 766-775. https://doi.org/10.1038/nrn2214
  8. Murohara, T., Asahara, T., Silver, M., Bauters, C., Masuda, H., Kalka, C., Kearney, M., Chen, D., Dymes, J. F., Fishman, M. C., Huang, P. L. and Isner, J. M. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Invest. 101, 2567-2578. https://doi.org/10.1172/JCI1560
  9. Jenkins, D., Charles, I., Thomsen, L., Moss, D., Holmes, L., Baylis, S., Rhodes, P., Westmore, K., Emson, P. and Moncada, S. (1995) Roles of nitric oxide in tumor growth. Proc. Natl. Acad. Sci. U.S.A. 92, 4392-4396. https://doi.org/10.1073/pnas.92.10.4392
  10. Harris, A. (2002) Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47. https://doi.org/10.1038/nrc704
  11. Rees, D., Palmer, R., Schulz, R., Hodson, H. and Moncada, S. (1990) Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Brit. J. Pharmacol. 101, 746-752. https://doi.org/10.1111/j.1476-5381.1990.tb14151.x
  12. Gladwin, M., Crawford, J. and Patel, R. (2004) The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Radical Bio. Med. 36, 707-717. https://doi.org/10.1016/j.freeradbiomed.2003.11.032
  13. Sessa, W., Pritchard, K., Seyedi, N., Wang, J. and Hintze, T. (1994) Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circ. Res. 74, 349-353. https://doi.org/10.1161/01.RES.74.2.349
  14. Bredt, D. and Snyder, S. (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl. Acad. Sci. U.S.A. 86, 9030-9033. https://doi.org/10.1073/pnas.86.22.9030
  15. Bredt, D. and Snyder, S. (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. U.S.A. 87, 682-685. https://doi.org/10.1073/pnas.87.2.682
  16. Itoh, Y., Ma, F., Hoshi, H., Oka, M., Noda, K., Ukai, Y., Kojima, H., Nagano, T. and Toda, N. (2000) Determination and bioimaging method for nitric oxide in biological specimens by diaminofluorescein fluorometry. Anal. Biochem. 287, 203-209. https://doi.org/10.1006/abio.2000.4859
  17. Bedioui, F. and Villeneuve, N. (2003) Electrochemical nitric oxide sensors for biological samples-principle, selected examples and applications. Electroanal. 15, 5-18. https://doi.org/10.1002/elan.200390006
  18. Bedioui, F., Quinton, D., Griveau, S. and Nyokong, T. (2010) Designing molecular materials and strategies for the electrochemical detection of nitric oxide, superoxide and peroxynitrite in biological systems. Phys. Chem. Chem. Phys. 12, 9976-9988. https://doi.org/10.1039/c0cp00271b
  19. Arbault, S., Sojic, N., Bruce, D., Amatore, C., Sarasin, A. and Vuillaume, M. (2004) Oxidative stress in cancer prone xeroderma pigmentosum fibroblasts. Real-time and single cell monitoring of superoxide and nitric oxide production with microelectrodes. Carcinogenesis 25, 509-515.
  20. Amatore, C., Arbault, S., Bouret, Y., Cauli, B., Guille, M., Rancillac, A. and Rossier, J. (2006) Nitric oxide release during evoked neuronal activity in cerebellum slices: Detection with platinized carbon-fiber microelectrodes. Chem. Phys. Chem. 7, 181-187. https://doi.org/10.1002/cphc.200500202
  21. Amatore, C., Arbault, S., Jaouen, G., Koh, A., Leong, W., Top, S., Valleron, M. and Woo, C. (2010) Pro-oxidant properties of AZT and other thymidine analogues in macrophages: Implication of the azido moiety in oxidative stress. Chem. Med. Chem. 5, 296-301. https://doi.org/10.1002/cmdc.200900464
  22. Patel, B., Arundell, M., Parker, K., Yeoman, M. and O'Hare, D. (2006) Detection of nitric oxide release from single neurons in the pond snail, lymnaea stagnalis. Anal. Chem. 78, 7643-7648. https://doi.org/10.1021/ac060863w
  23. Patel, B., Arundell, M., Parker, K., Yeoman, M. and O'Hare, D. (2010) Microelectrode investigation of neuroneal ageing from a single identified neurone. Phys. Chem. Chem. Phys. 12, 10065-10072. https://doi.org/10.1039/c0cp00310g
  24. Quinton, D., Girard, A., Kim, L., Raimbault, V., Griscom, L., Razan, F., Griveau, S. and Bedioui, F. (2011) On-chip multi-electrochemical sensor array platform for simultaneous screening of nitric oxide and peroxynitrite. Lab. Chip. 11, 1342-1350. https://doi.org/10.1039/c0lc00585a
  25. Chang, S., Pereira-Rodrigues, N., Henderson, J., Cole, A., Bedioui, F. and McNeil, C. (2005) An electrochemical sensor array system for the direct, simultaneous in vitro monitoring of nitric oxide and superoxide production by cultured cells. Biosens. Bioelectron. 21, 917-922. https://doi.org/10.1016/j.bios.2005.02.015
  26. Isik, S., Berdondini, L., Oni, J., Blochl, A., Koudelka-Hep, M. and Schuhmann, W. (2005) Cell-compatible array of three-dimensional tip electrodes for the detection of nitric oxide release. Biosens. Bioelectron. 20, 1566-1572. https://doi.org/10.1016/j.bios.2004.08.022
  27. Oni, J., Pailleret, A., Isik, S., Diab, N., Radtke, I., Blochl, A., Jackson, M., Bedioui, F. and Schuhmann, W. (2004) Functionalised electrode array for the detection of nitric oxide released by endothelial cells using different no-sensing chemistries. Anal. Bioanal. Chem. 378, 1594-1600. https://doi.org/10.1007/s00216-004-2512-6
  28. Trouillon, R., Kang, D.-K., Chang, S.-I. and O'Hare, D. (2011) Angiogenin induces nitric oxide release independently from its RNase activity. Chem. Commun. 47, 3421-3426. https://doi.org/10.1039/c0cc04527f
  29. Patel, B., Arundell, M., Quek, R., Harvey, S., Ellis, I., Florence, M., Cass, A., Schor, A. and O'Hare, D. (2008) Individually addressable microelectrode array for monitoring oxygen and nitric oxide release. Anal. Bioanal. Chem. 390, 1379-1387. https://doi.org/10.1007/s00216-007-1803-0
  30. Trouillon, R., Cheung, C., Patel, B. and O'Hare, D. (2009) Comparative study of poly (styrene-sulfonate)/poly (L-lysine) and fibronectin as biofouling preventing layers in dissolved oxygen electrochemical measurements. Analyst 134, 784-793. https://doi.org/10.1039/b811958a
  31. Trouillon, R., Combs, Z., Patel, B. and O'Hare, D. (2009) Comparative study of the effect of various electrode membranes on biofouling and electrochemical measurements. Electrochem. Commun. 11, 1409-1413. https://doi.org/10.1016/j.elecom.2009.05.018
  32. Wisniewski, N. and Reichert, M. (2000) Methods for reducing biosensor membrane biofouling. Colloid. Surface. B 18, 197-219. https://doi.org/10.1016/S0927-7765(99)00148-4
  33. Trouillon, R., Cheung, C., Patel, B. and O'Hare, D. (2010) Electrochemical study of the intracellular transduction of vascular endothelial growth factor induced nitric oxide synthase activity using a multi-channel biocompatible microelectrode array. BBA-Gen. Subjects 1800, 929-936. https://doi.org/10.1016/j.bbagen.2010.04.010
  34. Shibuya, M. (2008) Vascular endothelial growth factor-dependent and-independent regulation of angiogenesis. BMB Rep. 41, 278-286. https://doi.org/10.5483/BMBRep.2008.41.4.278
  35. Dimmeler, S., Dernbach, E. and Zeiher, A. (2000) Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett. 477, 258-262. https://doi.org/10.1016/S0014-5793(00)01657-4
  36. Chlench, S., Mecha Disassa, N., Hohberg, M., Hoffmann, C., Pohlkamp, T., Beyer, G., Bongrazio, M., Da Silva-Azevedo, L., Baum, O., Pries, A. R. and Zakrzewicz, A. (2007) Regulation of Foxo-1 and the angiopoietin-2/Tie2 system by shear stress. FEBS Lett. 581, 673-680. https://doi.org/10.1016/j.febslet.2007.01.028
  37. Breslin, J., Pappas, P., Cerveira, J., Hobson, R. and Duran, W. (2003) VEGF increases endothelial permeability by separate signaling pathways involving ERK-1/2 and nitric oxide. Am. J. Physiol.-Heart C. 284, H92-100. https://doi.org/10.1152/ajpheart.00330.2002
  38. Fett, J., Strydom, D., Lobb, R., Alderman, E., Bethune, J., Riordan, J. and Vallee, B. (1985) Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 24, 5480-5486. https://doi.org/10.1021/bi00341a030
  39. Kishimoto, K., Liu, S., Tsuji, T., Olson, K. and Hu, G.-F. (2004) Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene 24, 445-456.
  40. Hirukawa, S., Olson, K., Tsuji, T. and Hu, G.-F. (2005) Neamine inhibits xenografic human tumor growth and angiogenesis in athymic mice. Clin. Cancer Res. 11, 8745-8752. https://doi.org/10.1158/1078-0432.CCR-05-1495
  41. Trouillon, R., Kang, D.-K., Park, H., Chang, S.-I. and O'Hare, D. (2010) Angiogenin induces nitric oxide synthesis in endothelial cells through PI-3 and Akt kinases. Biochemistry 49, 3282-3288. https://doi.org/10.1021/bi902122w
  42. Shimoyama, S., Gansauge, F., Gansauge, S., Negri, G., Oohara, T. and Beger, H. (1996) Increased angiogenin expression in pancreatic cancer is related to cancer aggressiveness. Cancer Res. 56, 2703-2706.
  43. Cho, S., Moon, S., Lee, S., Kang, S., Kim, J., Lim, J., Kim, H., Kim, B. and Chung, H. (2007) Improvement of postnatal neovascularization by human embryonic stem cell-derived endothelial-like cell transplantation in a mouse model of hindlimb ischemia. Circulation 116, 2409-2419. https://doi.org/10.1161/CIRCULATIONAHA.106.687038
  44. Gao, X. and Xu, Z. (2008) Mechanisms of action of angiogenin. Acta. Biochim. Biophys. Sin. (Shanghai) 40, 619-624. https://doi.org/10.1111/j.1745-7270.2008.00442.x
  45. Hu, G., Riordan, J. and Vallee, B. (1994) Angiogenin promotes invasiveness of cultured endothelial cells by stimulation of cell-associated proteolytic activities. Proc. Natl. Acad. Sci. U.S.A. 91, 12096-12100. https://doi.org/10.1073/pnas.91.25.12096
  46. Russo, N., Shapiro, R., Acharya, K., Riordan, J. and Vallee, B. (1994) Role of glutamine-117 in the ribonucleolytic activity of human angiogenin. Proc. Natl. Acad. Sci. U.S.A. 91, 2920-2924. https://doi.org/10.1073/pnas.91.8.2920
  47. Liu, S., Yu, D., Xu, Z., Riordan, J. and Hu, G.-F. (2001) Angiogenin activates ERK 1/2 in human umbilical vein endothelial cells. Biochem. Bioph. Res. Co. 287, 305-310. https://doi.org/10.1006/bbrc.2001.5568
  48. Kim, H.-M., Kang, D.-K., Kim, H.-Y., Kang, S.-S. and Chang, S.-I. (2007) Angiogenin-induced protein kinase b/Akt activation is necessary for angiogenesis but is independent of nuclear translocation of angiogenin in HUVE cells. Biochem. Bioph. Res. Co. 352, 509-513. https://doi.org/10.1016/j.bbrc.2006.11.047
  49. Xu, Z., Monti, D. and Hu, G.-F. (2001) Angiogenin activates human umbilical artery smooth muscle cells. Biochem. Bioph. Res. Co. 285, 909-914. https://doi.org/10.1006/bbrc.2001.5255
  50. Hu, G., Xu, C. and Riordan, J. (2000) Human angiogenin is rapidly translocated to the nucleus of human umbilical vein endothelial cells and binds to DNA. J. Cell. Biochem. 76, 452-462. https://doi.org/10.1002/(SICI)1097-4644(20000301)76:3<452::AID-JCB12>3.0.CO;2-Z
  51. Chen, C. and Shapiro, R. (1997) Site-specific mutagenesis reveals differences in the structural bases for tight binding of RNase inhibitor to angiogenin and RNase A. Proc. Natl. Acad. Sci. U.S.A. 94, 1761-1766. https://doi.org/10.1073/pnas.94.5.1761
  52. Shapiro, R. and Vallee, B. (1987) Human placental ribonuclease inhibitor abolishes both angiogenic and ribonucleolytic activities of angiogenin. Proc. Natl. Acad. Sci. U.S.A. 84, 2238-2241. https://doi.org/10.1073/pnas.84.8.2238
  53. Li, R., Riordan, J. and Hu, G.-F.(1997) Nuclear translocation of human angiogenin in cultured human umbilical artery endothelial cells is microtubule and lysosome independent. Biochem. Bioph. Res. Co. 238, 305-312. https://doi.org/10.1006/bbrc.1997.7290
  54. Hu, G.-F. (1998) Neomycin inhibits angiogenin-induced angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 95, 9791-9795. https://doi.org/10.1073/pnas.95.17.9791
  55. Miyazaki, T., Honda, K. and Ohata, H. (2007) Requirement of $Ca^{2+}$ influx-and phosphatidylinositol 3-kinase-mediated m-calpain activity for shear stress-induced endothelial cell polarity. Am. J. Physiol.-Cell Ph. 293, C1216-1225. https://doi.org/10.1152/ajpcell.00083.2007
  56. Ibaragi, S., Yoshioka, N., Li, S., Hu, M., Hirukawa, S., Sadow, P. and Hu, G.-F. (2009) Neamine inhibits prostate cancer growth by suppressing angiogenin-mediated rRNA transcription. Clin. Cancer Res. 15, 1981-1988. https://doi.org/10.1158/1078-0432.CCR-08-2593

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