MECHANISMS OF ULTRASOUND-ENHANCED VASCULAR PERMEABILITY Ultrasound-Enhanced Permeability
Main Article Content
Abstract
Both continuous- and pulsed-wave ultrasound have been shown to increase endothelial permeability to echogenic liposomes (ELIP) and stem cells associated with them in vitro and in vivo. We have been able to model this phenomenon in vitro with human umbilical vein endothelial cell (HUVEC) monolayers grown on transwell inserts. The ultrasound effect is not dependent on ELIP echogenicity, indicating that it is induced by radiation pressure, rather than by cavitation forces, and is blocked by NG-nitro-L-arginine methyl ester, an inhibitor of endothelial nitric oxide synthase, establishing that it is mediated by nitric oxide signaling. Western blots of ultrasound-treated cultured HUVEC lysates and untreated controls indicated that nitric oxide activates the Akt pathway, implicating the intracellular transduction mechanism mediating shear stress effects on endothelial cells, but that other mechanoreceptor-triggered pathways may also be involved.
Keywords:
ultrasound, vascular permeability, nitric oxide, liposomes
Article Details
How to Cite
ISLAM, Afsana F. et al.
MECHANISMS OF ULTRASOUND-ENHANCED VASCULAR PERMEABILITY.
Medical Research Archives, [S.l.], v. 13, n. 6, july 2025.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/6609>. Date accessed: 05 dec. 2025.
doi: https://doi.org/10.18103/mra.v13i6.6609.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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14. He P, Zeng M, Curry FE. cGMP modulates basal and activated microvessel permeability independently of [Ca2+]i. Am J Physiol. Jun 1998;274(6):H1865-74. doi:10.1152/ajpheart.1998.274.6.H1865
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19. Wink DA, Hines HB, Cheng RY, et al. Nitric oxide and redox mechanisms in the immune response. J Leukoc Biol. Jun 2011;89(6):873-91. doi:10.1189/jlb.1010550
20. Wink DA, Miranda KM, Espey MG, et al. Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox Signal. Apr 2001;3(2):203-13. doi:10.1089/152308601300185179
21. Herbst SM, Klegerman ME, Kim H, et al. Delivery of stem cells to porcine arterial wall with echogenic liposomes conjugated to antibodies against CD34 and intercellular adhesion molecule-1. Mol Pharm. Feb 1 2010;7(1):3-11. doi:10.1021/mp900116r
22. Kim H, Kee PH, Rim Y, et al. Nitric oxide improves molecular imaging of inflammatory atheroma using targeted echogenic immunoliposomes. Atherosclerosis. Dec 2013;231(2):252-60. doi:10.1016/j.atherosclerosis.2013.09.026
23. Klegerman ME, Moody MR, Huang SL, et al. Demonstration of ultrasound-mediated therapeutic delivery of fibrin-targeted pioglitazone-loaded echogenic liposomes into the arterial bed for attenuation of peri-stent restenosis. J Drug Target. Jan 2023;31(1):109-118. doi:10.1080/1061186X.2022.2110251
24. Klegerman ME, Wassler M, Huang SL, et al. Liposomal modular complexes for simultaneous targeted delivery of bioactive gases and therapeutics. J Control Release. Mar 19 2010;142(3):326-31. doi:10.1016/j.jconrel.2009.10.037
25. Kee PH, Moody MR, Huang SL, et al. Stabilizing Peri-Stent Restenosis Using a Novel Therapeutic Carrier. JACC Basic Transl Sci. Jan 2020;5(1):1-11. doi:10.1016/j.jacbts.2019.09.005
26. Husseini GA, Pitt WG, Martins AM. Ultrasonically triggered drug delivery: breaking the barrier. Colloids /Surfaces B, Biointerfaces. Nov 1 2014; 123:364-86. doi:10.1016/j.colsurfb.2014.07.051
27. Rees DD, Palmer RM, Schulz R, Hodson HF, Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol. Nov 1990;101(3):746-52. doi:10.1111/j.1476-5381.1990.tb14151.x
28. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol. Aug 1995;48(2):184-8.
29. Lal BK, Varma S, Pappas PJ, Hobson RW, 2nd, Duran WN. VEGF increases permeability of the endothelial cell monolayer by activation of PKB/akt, endothelial nitric-oxide synthase, and MAP kinase pathways. Microvasc Res. Nov 2001;62(3):252-62. doi:10.1006/mvre.2001.2338
30. Dabravolski SA, Sukhorukov VN, Kalmykov VA, Grechko AV, Shakhpazyan NK, Orekhov AN. The Role of KLF2 in the Regulation of Atherosclerosis Development and Potential Use of KLF2-Targeted Therapy. Biomedicines. Jan 24 2022;10(2) doi:10.3390/biomedicines10020254
31. Fleming I. Molecular mechanisms underlying the activation of eNOS. Pflugers Arch. May 2010; 459(6):793-806. doi:10.1007/s00424-009-0767-7
32. Li J, Hou B, Tumova S, et al. Piezo1 integration of vascular architecture with physiological force. Nature. Nov 13 2014;515(7526):279-282. doi:10.1038/nature13701
33. Tamargo IA, Baek KI, Kim Y, Park C, Jo H. Flow-induced reprogramming of endothelial cells in atherosclerosis. Nat Rev Cardiol. Nov 2023; 20(11):738-753. doi:10.1038/s41569-023-00883-1
34. Wang S, Chennupati R, Kaur H, Iring A, Wettschureck N, Offermanns S. Endothelial cation channel PIEZO1 controls blood pressure by mediating flow-induced ATP release. J Clin Invest. Dec 1 2016;126(12):4527-4536. doi:10.1172/JCI87343
35. Di X, Gao X, Peng L, et al. Cellular mechanotransduction in health and diseases: from molecular mechanism to therapeutic targets. Signal Transduct Target Ther. Jul 31 2023;8(1):282. doi:10.1038/s41392-023-01501-9
36. Roux E, Bougaran P, Dufourcq P, Couffinhal T. Fluid Shear Stress Sensing by the Endothelial Layer. Front Physiol. 2020;11:861. doi:10.3389/fphys.2020.00861
37. Sun D, Huang A, Sharma S, Koller A, Kaley G. Endothelial microtubule disruption blocks flow-dependent dilation of arterioles. Am J Physiol Heart Circ Physiol. May 2001;280(5):H2087-93. doi:10.1152/ajpheart.2001.280.5.H2087
38. Eroglu E, Saravi SSS, Sorrentino A, Steinhorn B, Michel T. Discordance between eNOS phosphorylation and activation revealed by multispectral imaging and chemogenetic methods. Proc Natl Acad Sci U S A. Oct 1 2019;116(40):20210-20217. doi:10.1073/pnas.1910942116
39. Devarie-Baez NO, Zhang D, Li S, Whorton AR, Xian M. Direct methods for detection of protein S-nitrosylation. Methods. Aug 1 2013;62(2):171-6. doi:10.1016/j.ymeth.2013.04.018
40. Ferreira Tojais N, Peghaire C, Franzl N, et al. Frizzled7 controls vascular permeability through the Wnt-canonical pathway and cross-talk with endothelial cell junction complexes. Cardiovasc Res. Jul 15 2014;103(2):291-303. doi:10.1093/cvr/cvu133
41. da Costa PE, Batista WL, Moraes MS, Stern A, Monteiro HP. Src kinase activation by nitric oxide promotes resistance to anoikis in tumour cell lines. Free Radic Res. May 2018;52(5):592-604. doi:10.1080/10715762.2018.1455095
42. Haynes MP, Li L, Sinha D, et al. Src kinase mediates phosphatidylinositol 3-kinase/Akt-dependent rapid endothelial nitric-oxide synthase activation by estrogen. J Biol Chem. Jan 24 2003;278(4): 2118-23. doi:10.1074/jbc.M210828200
43. Salminen AT, Allahyari Z, Gholizadeh S, et al. In vitro Studies of Transendothelial Migration for Biological and Drug Discovery. Front Med Technol. 2020;2:600616. doi:10.3389/fmedt.2020.600616
44. Winger RC, Koblinski JE, Kanda T, Ransohoff RM, Muller WA. Rapid remodeling of tight junctions during paracellular diapedesis in a human model of the blood-brain barrier. J Immunol. Sep 1 2014; 193(5):2427-37. doi:10.4049/jimmunol.1400700
45. Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow. Blood. Jul 15 2005;106(2):584-92. doi:10.1182/blood-2004-12-4942
46. Islam AF, Peng T, McPherson DD, Klegerman ME. In vitro implication of mechanisms mediating ultrasound-enhanced vascular permeability. Arterioscl Thromb Vasc Biol. 2023;43(1):A652.
47. Islam AF, Peng T, Shelat HS, et al. Assessment of ultrasound-facilitated endothelial permeability using transwell culture methodology. Arterioscl Thromb Vasc Biol. 2022;42(1):375.
2. Moncada S, Palmer RM, Higgs EA. The discovery of nitric oxide as the endogenous nitrovasodilator. Hypertension. Oct 1988;12(4):365-72. doi:10.1161/01.hyp.12.4.365
3. Yue W, Li Y, Ou D, Yang Q. The GLP-1 receptor agonist liraglutide protects against oxidized LDL-induced endothelial inflammation and dysfunction via KLF2. IUBMB Life. Sep 2019;71(9):1347-1354. doi:10.1002/iub.2046
4. Dimmeler S, Assmus B, Hermann C, Haendeler J, Zeiher AM. Fluid shear stress stimulates phosphorylation of Akt in human endothelial cells: involvement in suppression of apoptosis. Circ Res. Aug 10 1998;83(3):334-41. doi:10.1161/01.res.83.3.334
5. Duran WN, Breslin JW, Sanchez FA. The NO cascade, eNOS location, and microvascular permeability. Cardiovasc Res. Jul 15 2010; 87(2):254-61. doi:10.1093/cvr/cvq139
6. Duran WN, Beuve AV, Sanchez FA. Nitric oxide, S-nitrosation, and endothelial permeability. IUBMB Life. Oct 2013;65(10):819-26. doi:10.1002/iub.1204
7. Thibeault S, Rautureau Y, Oubaha M, et al. S-nitrosylation of beta-catenin by eNOS-derived NO promotes VEGF-induced endothelial cell permeability. Mol Cell. Aug 13 2010;39(3):468-76. doi:10.1016/j.molcel.2010.07.013
8. Gavard J. Endothelial permeability and VE-cadherin: a wacky comradeship. Cell Adh Migr. 2014;8(2):158-64. doi:10.4161/cam.29026
9. De Caterina R, Libby P, Peng HB, et al. Nitric oxide decreases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J Clin Invest. Jul 1995;96(1):60-8. doi:10.1172/JCI118074
10. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. Jun 10 1999;399(6736): 601-5. doi:10.1038/21224
11. Fulton D, Gratton JP, McCabe TJ, et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature. Jun 10 1999;399(6736):597-601. doi:10.1038/21218
12. Gao F, Lucke-Wold BP, Li X, et al. Reduction of Endothelial Nitric Oxide Increases the Adhesiveness of Constitutive Endothelial Membrane ICAM-1 through Src-Mediated Phosphorylation. Front Physiol. 2017;8:1124. doi:10.3389/fphys.2017.01124
13. He H, Oo TL, Huang W, He LF, Gu M. Nitric oxide acts as an antioxidant and inhibits programmed cell death induced by aluminum in the root tips of peanut (Arachis hypogaea L.). Sci Rep. Jul 2 2019; 9(1):9516. doi:10.1038/s41598-019-46036-8
14. He P, Zeng M, Curry FE. cGMP modulates basal and activated microvessel permeability independently of [Ca2+]i. Am J Physiol. Jun 1998;274(6):H1865-74. doi:10.1152/ajpheart.1998.274.6.H1865
15. Hummel SG, Fischer AJ, Martin SM, Schafer FQ, Buettner GR. Nitric oxide as a cellular antioxidant: a little goes a long way. Free Radic Biol Med. Feb 1 2006;40(3):501-6. doi:10.1016/j.freeradbiomed.2005.08.047
16. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. Jun 11-17 1987;327(6122):524-6. doi:10.1038/327524a0
17. Varma S, Breslin JW, Lal BK, Pappas PJ, Hobson RW, 2nd, Duran WN. p42/44MAPK regulates baseline permeability and cGMP-induced hyperpermeability in endothelial cells. Microvasc Res. Mar 2002;63(2): 172-8. doi:10.1006/mvre.2001.2381
18. Wink DA, Hanbauer I, Krishna MC, DeGraff W, Gamson J, Mitchell JB. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci U S A. Nov 1 1993;90(21):9813-7. doi:10.1073/pnas.90.21.9813
19. Wink DA, Hines HB, Cheng RY, et al. Nitric oxide and redox mechanisms in the immune response. J Leukoc Biol. Jun 2011;89(6):873-91. doi:10.1189/jlb.1010550
20. Wink DA, Miranda KM, Espey MG, et al. Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox Signal. Apr 2001;3(2):203-13. doi:10.1089/152308601300185179
21. Herbst SM, Klegerman ME, Kim H, et al. Delivery of stem cells to porcine arterial wall with echogenic liposomes conjugated to antibodies against CD34 and intercellular adhesion molecule-1. Mol Pharm. Feb 1 2010;7(1):3-11. doi:10.1021/mp900116r
22. Kim H, Kee PH, Rim Y, et al. Nitric oxide improves molecular imaging of inflammatory atheroma using targeted echogenic immunoliposomes. Atherosclerosis. Dec 2013;231(2):252-60. doi:10.1016/j.atherosclerosis.2013.09.026
23. Klegerman ME, Moody MR, Huang SL, et al. Demonstration of ultrasound-mediated therapeutic delivery of fibrin-targeted pioglitazone-loaded echogenic liposomes into the arterial bed for attenuation of peri-stent restenosis. J Drug Target. Jan 2023;31(1):109-118. doi:10.1080/1061186X.2022.2110251
24. Klegerman ME, Wassler M, Huang SL, et al. Liposomal modular complexes for simultaneous targeted delivery of bioactive gases and therapeutics. J Control Release. Mar 19 2010;142(3):326-31. doi:10.1016/j.jconrel.2009.10.037
25. Kee PH, Moody MR, Huang SL, et al. Stabilizing Peri-Stent Restenosis Using a Novel Therapeutic Carrier. JACC Basic Transl Sci. Jan 2020;5(1):1-11. doi:10.1016/j.jacbts.2019.09.005
26. Husseini GA, Pitt WG, Martins AM. Ultrasonically triggered drug delivery: breaking the barrier. Colloids /Surfaces B, Biointerfaces. Nov 1 2014; 123:364-86. doi:10.1016/j.colsurfb.2014.07.051
27. Rees DD, Palmer RM, Schulz R, Hodson HF, Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol. Nov 1990;101(3):746-52. doi:10.1111/j.1476-5381.1990.tb14151.x
28. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol. Aug 1995;48(2):184-8.
29. Lal BK, Varma S, Pappas PJ, Hobson RW, 2nd, Duran WN. VEGF increases permeability of the endothelial cell monolayer by activation of PKB/akt, endothelial nitric-oxide synthase, and MAP kinase pathways. Microvasc Res. Nov 2001;62(3):252-62. doi:10.1006/mvre.2001.2338
30. Dabravolski SA, Sukhorukov VN, Kalmykov VA, Grechko AV, Shakhpazyan NK, Orekhov AN. The Role of KLF2 in the Regulation of Atherosclerosis Development and Potential Use of KLF2-Targeted Therapy. Biomedicines. Jan 24 2022;10(2) doi:10.3390/biomedicines10020254
31. Fleming I. Molecular mechanisms underlying the activation of eNOS. Pflugers Arch. May 2010; 459(6):793-806. doi:10.1007/s00424-009-0767-7
32. Li J, Hou B, Tumova S, et al. Piezo1 integration of vascular architecture with physiological force. Nature. Nov 13 2014;515(7526):279-282. doi:10.1038/nature13701
33. Tamargo IA, Baek KI, Kim Y, Park C, Jo H. Flow-induced reprogramming of endothelial cells in atherosclerosis. Nat Rev Cardiol. Nov 2023; 20(11):738-753. doi:10.1038/s41569-023-00883-1
34. Wang S, Chennupati R, Kaur H, Iring A, Wettschureck N, Offermanns S. Endothelial cation channel PIEZO1 controls blood pressure by mediating flow-induced ATP release. J Clin Invest. Dec 1 2016;126(12):4527-4536. doi:10.1172/JCI87343
35. Di X, Gao X, Peng L, et al. Cellular mechanotransduction in health and diseases: from molecular mechanism to therapeutic targets. Signal Transduct Target Ther. Jul 31 2023;8(1):282. doi:10.1038/s41392-023-01501-9
36. Roux E, Bougaran P, Dufourcq P, Couffinhal T. Fluid Shear Stress Sensing by the Endothelial Layer. Front Physiol. 2020;11:861. doi:10.3389/fphys.2020.00861
37. Sun D, Huang A, Sharma S, Koller A, Kaley G. Endothelial microtubule disruption blocks flow-dependent dilation of arterioles. Am J Physiol Heart Circ Physiol. May 2001;280(5):H2087-93. doi:10.1152/ajpheart.2001.280.5.H2087
38. Eroglu E, Saravi SSS, Sorrentino A, Steinhorn B, Michel T. Discordance between eNOS phosphorylation and activation revealed by multispectral imaging and chemogenetic methods. Proc Natl Acad Sci U S A. Oct 1 2019;116(40):20210-20217. doi:10.1073/pnas.1910942116
39. Devarie-Baez NO, Zhang D, Li S, Whorton AR, Xian M. Direct methods for detection of protein S-nitrosylation. Methods. Aug 1 2013;62(2):171-6. doi:10.1016/j.ymeth.2013.04.018
40. Ferreira Tojais N, Peghaire C, Franzl N, et al. Frizzled7 controls vascular permeability through the Wnt-canonical pathway and cross-talk with endothelial cell junction complexes. Cardiovasc Res. Jul 15 2014;103(2):291-303. doi:10.1093/cvr/cvu133
41. da Costa PE, Batista WL, Moraes MS, Stern A, Monteiro HP. Src kinase activation by nitric oxide promotes resistance to anoikis in tumour cell lines. Free Radic Res. May 2018;52(5):592-604. doi:10.1080/10715762.2018.1455095
42. Haynes MP, Li L, Sinha D, et al. Src kinase mediates phosphatidylinositol 3-kinase/Akt-dependent rapid endothelial nitric-oxide synthase activation by estrogen. J Biol Chem. Jan 24 2003;278(4): 2118-23. doi:10.1074/jbc.M210828200
43. Salminen AT, Allahyari Z, Gholizadeh S, et al. In vitro Studies of Transendothelial Migration for Biological and Drug Discovery. Front Med Technol. 2020;2:600616. doi:10.3389/fmedt.2020.600616
44. Winger RC, Koblinski JE, Kanda T, Ransohoff RM, Muller WA. Rapid remodeling of tight junctions during paracellular diapedesis in a human model of the blood-brain barrier. J Immunol. Sep 1 2014; 193(5):2427-37. doi:10.4049/jimmunol.1400700
45. Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow. Blood. Jul 15 2005;106(2):584-92. doi:10.1182/blood-2004-12-4942
46. Islam AF, Peng T, McPherson DD, Klegerman ME. In vitro implication of mechanisms mediating ultrasound-enhanced vascular permeability. Arterioscl Thromb Vasc Biol. 2023;43(1):A652.
47. Islam AF, Peng T, Shelat HS, et al. Assessment of ultrasound-facilitated endothelial permeability using transwell culture methodology. Arterioscl Thromb Vasc Biol. 2022;42(1):375.