Fluid Mechanics, Arterial Disease, and Gene Expression

Overview

Journal Annu Rev Fluid Mech

Publisher Annual Reviews

Date 2014 Nov 1

PMID 25360054

Citations 75

Authors

John M Tarbell

Zhong-Dong Shi

Jessilyn Dunn

Hanjoong Jo

Affiliations

Soon will be listed here.

Abstract

This review places modern research developments in vascular mechanobiology in the context of hemodynamic phenomena in the cardiovascular system and the discrete localization of vascular disease. The modern origins of this field are traced, beginning in the 1960s when associations between flow characteristics, particularly blood flow-induced wall shear stress, and the localization of atherosclerotic plaques were uncovered, and continuing to fluid shear stress effects on the vascular lining endothelial) cells (ECs), including their effects on EC morphology, biochemical production, and gene expression. The earliest single-gene studies and genome-wide analyses are considered. The final section moves from the ECs lining the vessel wall to the smooth muscle cells and fibroblasts within the wall that are fluid me chanically activated by interstitial flow that imposes shear stresses on their surfaces comparable with those of flowing blood on EC surfaces. Interstitial flow stimulates biochemical production and gene expression, much like blood flow on ECs.

Citing Articles

Endothelial cells under disturbed flow release extracellular vesicles to promote inflammatory polarization of macrophages and accelerate atherosclerosis.

Hou Z, Deng L, Fang F, Zhao T, Zhang Y, Li G BMC Biol. 2025; 23(1):20.

PMID: 39838385 PMC: 11753076. DOI: 10.1186/s12915-025-02125-x.

Mechanosensory entities and functionality of endothelial cells.

Mierke C Front Cell Dev Biol. 2024; 12:1446452.

PMID: 39507419 PMC: 11538060. DOI: 10.3389/fcell.2024.1446452.

Impact of mechanical cues on key cell functions and cell-nanoparticle interactions.

Elblova P, Lunova M, Dejneka A, Jirsa M, Lunov O Discov Nano. 2024; 19(1):106.

PMID: 38907808 PMC: 11193707. DOI: 10.1186/s11671-024-04052-2.

Harnessing the potential of monocytes/macrophages to regenerate tissue-engineered vascular grafts.

Das A, Smith R, Andreadis S Cardiovasc Res. 2024; 120(8):839-854.

PMID: 38742656 PMC: 11218695. DOI: 10.1093/cvr/cvae106.

Interstitial Fluid Shear Stress Induces the Synthetic Phenotype Switching of VSMCs to Release Pro-calcified Extracellular Vesicles via EGFR-MAPK-KLF5 Pathway.

Gao W, Gu K, Ma L, Yang F, Deng L, Zhang Y Int J Biol Sci. 2024; 20(7):2727-2747.

PMID: 38725857 PMC: 11077359. DOI: 10.7150/ijbs.90725.

References

Ni J, Waldman A, Khachigian L . c-Jun regulates shear- and injury-inducible Egr-1 expression, vein graft stenosis after autologous end-to-side transplantation in rabbits, and intimal hyperplasia in human saphenous veins. J Biol Chem. 2009; 285(6):4038-4048. PMC: 2823545. DOI: 10.1074/jbc.M109.078345. View

Davies P . Flow-mediated endothelial mechanotransduction. Physiol Rev. 1995; 75(3):519-60. PMC: 3053532. DOI: 10.1152/physrev.1995.75.3.519. View

Alshihabi S, Chang Y, Frangos J, Tarbell J . Shear stress-induced release of PGE2 and PGI2 by vascular smooth muscle cells. Biochem Biophys Res Commun. 1996; 224(3):808-14. DOI: 10.1006/bbrc.1996.1104. View

Garanich J, Pahakis M, Tarbell J . Shear stress inhibits smooth muscle cell migration via nitric oxide-mediated downregulation of matrix metalloproteinase-2 activity. Am J Physiol Heart Circ Physiol. 2005; 288(5):H2244-52. DOI: 10.1152/ajpheart.00428.2003. View

Faxon D, Creager M, Smith Jr S, Pasternak R, Olin J, Bettmann M . Atherosclerotic Vascular Disease Conference: Executive summary: Atherosclerotic Vascular Disease Conference proceeding for healthcare professionals from a special writing group of the American Heart Association. Circulation. 2004; 109(21):2595-604. DOI: 10.1161/01.CIR.0000128517.52533.DB. View

Hishikawa K, Nakaki T, Marumo T, Hayashi M, Suzuki H, Kato R . Pressure promotes DNA synthesis in rat cultured vascular smooth muscle cells. J Clin Invest. 1994; 93(5):1975-80. PMC: 294305. DOI: 10.1172/JCI117189. View

Gimbrone Jr M, Topper J, Nagel T, Anderson K, Garcia-Cardena G . Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci. 2000; 902:230-9; discussion 239-40. DOI: 10.1111/j.1749-6632.2000.tb06318.x. View

Cukierman E, Pankov R, Stevens D, Yamada K . Taking cell-matrix adhesions to the third dimension. Science. 2001; 294(5547):1708-12. DOI: 10.1126/science.1064829. View

Lin K, Hsu P, Chen B, Yuan S, Usami S, Shyy J . Molecular mechanism of endothelial growth arrest by laminar shear stress. Proc Natl Acad Sci U S A. 2000; 97(17):9385-9. PMC: 16873. DOI: 10.1073/pnas.170282597. View

10.

Garanich J, Mathura R, Shi Z, Tarbell J . Effects of fluid shear stress on adventitial fibroblast migration: implications for flow-mediated mechanisms of arterialization and intimal hyperplasia. Am J Physiol Heart Circ Physiol. 2007; 292(6):H3128-35. DOI: 10.1152/ajpheart.00578.2006. View

11.

Bijari P, Antiga L, Gallo D, Wasserman B, Steinman D . Improved prediction of disturbed flow via hemodynamically-inspired geometric variables. J Biomech. 2012; 45(9):1632-7. PMC: 3371282. DOI: 10.1016/j.jbiomech.2012.03.030. View

12.

Cancel L, Tarbell J . The role of mitosis in LDL transport through cultured endothelial cell monolayers. Am J Physiol Heart Circ Physiol. 2010; 300(3):H769-76. PMC: 3064312. DOI: 10.1152/ajpheart.00445.2010. View

13.

FRIEDMAN M, Hutchins G, Bargeron C, Deters O, Mark F . Correlation between intimal thickness and fluid shear in human arteries. Atherosclerosis. 1981; 39(3):425-36. DOI: 10.1016/0021-9150(81)90027-7. View

14.

Shi Z, Abraham G, Tarbell J . Shear stress modulation of smooth muscle cell marker genes in 2-D and 3-D depends on mechanotransduction by heparan sulfate proteoglycans and ERK1/2. PLoS One. 2010; 5(8):e12196. PMC: 2922372. DOI: 10.1371/journal.pone.0012196. View

15.

Mo M, Eskin S, Schilling W . Flow-induced changes in Ca2+ signaling of vascular endothelial cells: effect of shear stress and ATP. Am J Physiol. 1991; 260(5 Pt 2):H1698-707. DOI: 10.1152/ajpheart.1991.260.5.H1698. View

16.

Ekstrand J, Razuvaev A, Folkersen L, Roy J, Hedin U . Tissue factor pathway inhibitor-2 is induced by fluid shear stress in vascular smooth muscle cells and affects cell proliferation and survival. J Vasc Surg. 2010; 52(1):167-75. DOI: 10.1016/j.jvs.2010.02.282. View

17.

Grabowski E, Jaffe E, Weksler B . Prostacyclin production by cultured endothelial cell monolayers exposed to step increases in shear stress. J Lab Clin Med. 1985; 105(1):36-43. View

18.

Dancu M, Tarbell J . Coronary endothelium expresses a pathologic gene pattern compared to aortic endothelium: correlation of asynchronous hemodynamics and pathology in vivo. Atherosclerosis. 2006; 192(1):9-14. DOI: 10.1016/j.atherosclerosis.2006.05.042. View

19.

Garcia-Cardena G, Comander J, Anderson K, Blackman B, Gimbrone Jr M . Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci U S A. 2001; 98(8):4478-85. PMC: 31860. DOI: 10.1073/pnas.071052598. View

20.

Weinbaum S, Tzeghai G, Ganatos P, Pfeffer R, Chien S . Effect of cell turnover and leaky junctions on arterial macromolecular transport. Am J Physiol. 1985; 248(6 Pt 2):H945-60. DOI: 10.1152/ajpheart.1985.248.6.H945. View