Shear Stress-Induced NO Production is Dependent on ATP Autocrine Signaling and Capacitative Calcium Entry

Cellular and Molecular Bioengineering

Volumn 7, Issue 4, 2014, Pages 510-520

  Andrews, Allison M ^a   Jaron, Dov ^a   Buerk, Donald G ^a   Barbee, Kenneth A ^a  

^a DREXEL UNIVERSITY   (United States)

Author keywords

ATP; Capacitative calcium entry; Endothelial cells; Nitric oxide; Shear stress

Indexed keywords

EID: 84939897431     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-014-0351-x     Document Type: Article

References (38)

1. Andrews, A. M., D. Jaron, D. G. Buerk, P. L. Kirby, and K. A. Barbee. Direct, real-time measurement of shear stress-induced nitric oxide produced from endothelial cells in vitro. Nitric Oxide 23:335–342, 2010.
2. Ayajiki, K., M. Kindermann, M. Hecker, I. Fleming, and R. Busse. Intracellular pH and tyrosine phosphorylation but not calcium determine shear stress-induced nitric oxide production in native endothelial cells. Circ. Res. 78:750–758, 1996.
3. Bodin, P., D. Bailey, and G. Burnstock. Increased flow-induced ATP release from isolated vascular endothelial cells but not smooth muscle cells. Br. J. Pharmacol. 103:1203–1205, 1991.
4. Bodin, P., and G. Burnstock. Evidence that release of adenosine triphosphate from endothelial cells during increased shear stress is vesicular. J. Cardiovasc. Pharmacol. 38:900–908, 2001.
5. Boo, Y. C., G. Sorescu, N. Boyd, I. Shiojima, K. Walsh, J. Du, and H. Jo. Shear stress stimulates phosphorylation of endothelial nitric-oxide synthase at Ser1179 by Akt-independent mechanisms: role of protein kinase A. J. Biol. Chem. 277:3388–3396, 2002.
6. Buxton, I. L., R. A. Kaiser, B. C. Oxhorn, and D. J. Cheek. Evidence supporting the Nucleotide Axis Hypothesis: ATP release and metabolism by coronary endothelium. Am. J. Physiol. Heart Circ. Physiol. 281:H1657–H1666, 2001.
7. Cabral, P. D., N. J. Hong, and J. L. Garvin. ATP mediates flow-induced NO production in thick ascending limbs. Am. J. Physiol. Renal. Physiol. 303:F194–F200, 2012.
8. Cale, J. M., and I. M. Bird. Dissociation of endothelial nitric oxide synthase phosphorylation and activity in uterine artery endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 290:H1433–H1445, 2006.
9. Comerford, A., M. J. Plank, and T. David. Endothelial nitric oxide synthase and calcium production in arterial geometries: an integrated fluid mechanics/cell model. J. Biomech. Eng. 130:011010, 2008.
10. Corson, M. A., N. L. James, S. E. Latta, R. M. Nerem, B. C. Berk, and D. G. Harrison. Phosphorylation of endothelial nitric oxide synthase in response to fluid shear stress. Circ. Res. 79:984–991, 1996.
11. 2+ uptake in bovine vascular endothelial cells. J. Physiol. Lond. 539:77–91, 2002.
12. Frischauf, I., R. Schindl, I. Derler, J. Bergsmann, M. Fahrner, and C. Romanin. The STIM/Orai coupling machinery. Channels (Austin) 2:261–268, 2008.
13. Garg, U. C., and A. Hassid. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J. Clin. Investig. 83:1774–1777, 1989.
14. Gonçalves da Silva, C. G., A. Specht, B. Wegiel, C. Ferran, and E. Kaczmarek. Mechanism of purinergic activation of endothelial nitric oxide synthase in endothelial cells. Circulation 119:871–879, 2009.
15. Hong, D., D. Jaron, D. G. Buerk, and K. A. Barbee. Heterogeneous response of microvascular endothelial cells to shear stress. Am. J. Physiol. Heart Circ. Physiol. 290:H2498–H2508, 2006.
16. Hong, D., D. Jaron, D. G. Buerk, and K. A. Barbee. Transport-dependent calcium signaling in spatially segregated cellular caveolar domains. Am. J. Physiol. Cell Physiol. 294:C856–C866, 2008.
17. Kanai, A. J., H. C. Strauss, G. A. Truskey, A. L. Crews, S. Grunfeld, and T. Malinski. Shear-stress induces ATP-independent transient nitric-oxide release from vascular endothelial-cells, measured directly with a porphyrinic microsensor. Circ. Res. 77:284–293, 1995.
18. Kemeny, S. F., D. S. Figueroa, A. M. Andrews, K. A. Barbee, and A. M. Clyne. Glycated collagen alters endothelial cell actin alignment and nitric oxide release in response to fluid shear stress. J. Biomech. 44:1927–1935, 2011.
19. Kubes, P., M. Suzuki, and D. N. Granger. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. USA 88:4651–4655, 1991.
20. Kuchan, M. J., and J. A. Frangos. Role of calcium and calmodulin in flow-induced nitric-oxide production in endothelial-cells. Am. J. Physiol. 266:C628–C636, 1994.
21. Kwan, H. Y., Y. Huang, and X. Yao. TRP channels in endothelial function and dysfunction. Biochim. Biophys. Acta 1772:907–914, 2007.
22. 2+ entry. J. Biol. Chem. 275:17979–17985, 2000.
23. 2+ channels in human glomerular mesangial cells. Am. J. Physiol. Cell Physiol. 283:C1390–C1398, 2002.
24. Mortensen, S. P., P. Thaning, M. Nyberg, B. Saltin, and Y. Hellsten. Local release of ATP into the arterial inflow and venous drainage of human skeletal muscle: insight from ATP determination with the intravascular microdialysis technique. J. Physiol. 589:1847–1857, 2011.
25. Radomski, M. W., R. M. Palmer, and S. Moncada. Endogenous nitric oxide inhibits human platelet adhesion to vascular endothelium. Lancet 2:1057–1058, 1987.
26. Radomski, M. W., P. Vallance, G. Whitley, N. Foxwell, and S. Moncada. Platelet adhesion to human vascular endothelium is modulated by constitutive and cytokine induced nitric oxide. Cardiovasc. Res. 27:1380–1382, 1993.
27. Shen, J., F. W. Luscinskas, A. Connolly, C. F. Dewey, Jr. and M. A. Gimbrone, Jr. Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells. Am. J. Physiol. 262:C384–C390, 1992.
28. Silva, G., W. H. Beierwaltes, and J. L. Garvin. Extracellular ATP stimulates NO production in rat thick ascending limb. Hypertension 47:563–567, 2006.
29. 2+ entry pathway by PKC-epsilon in vascular SMCs. Am. J. Physiol. Cell Physiol. 294:C1499–C1508, 2008.
30. 2+, U0126, and wortmannin but not LY294002—evidence that pregnancy adaptation of eNOS activation occurs at multiple levels of cell signaling. Endocrinology 147:2442–2457, 2006.
31. Tsao, P. S., R. Buitrago, J. R. Chan, and J. P. Cooke. Fluid flow inhibits endothelial adhesiveness. Nitric oxide and transcriptional regulation of VCAM-1. Circulation 94:1682–1689, 1996.
32. 2+ transient in vascular smooth muscle cells in coculture. J. Biol. Chem. 271:5647–5655, 1996.
33. 2+ release modulates endothelial nitric-oxide synthase via extracellular signal-regulated kinase (ERK) 1/2-mediated serine 635 phosphorylation. J. Biol. Chem. 286:20100–20108, 2011.
34. 2+ waves at caveolae in vascular endothelial cells. J. Cell Sci. 124:3477–3483, 2011.
35. Yamamoto, K., R. Korenaga, A. Kamiya, Z. Qi, M. Sokabe, and J. Ando. P2X(4) receptors mediate ATP-induced calcium influx in human vascular endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 279:H285–H292, 2000.
36. Yang, B., and V. Rizzo. Shear stress activates eNOS at the endothelial apical surface through 1 containing integrins and caveolae. Cell. Mol. Bioeng. 6:346–354, 2013.
37. 2+]i and intracellular NO production in freshly isolated uterine artery endothelial cells: effects of ovarian cycle and pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288:R140–R148, 2005.
38. Zhang, F., Q. Wen, S. Mergler, H. Yang, Z. Wang, V. N. Bildin, and P. S. Reinach. PKC isoform-specific enhancement of capacitative calcium entry in human corneal epithelial cells. Investig. Ophthalmol. Vis. Sci. 47:3989–4000, 2006.