Skip to main content

Advertisement

Log in

Microvascular Transport and Tumor Cell Adhesion in the Microcirculation

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

One critical step in tumor metastasis is tumor cell adhesion to the endothelium forming the microvessel wall. Understanding this step may lead to new therapeutic concepts for tumor metastasis. Vascular endothelium forming the microvessel wall and the glycocalyx layer at its surface are the principal barriers to, and regulators of the material exchange between circulating blood and body tissues. The cleft between adjacent ECs (interendothelial cleft) is the principal pathway for water and solutes transport through the microvessel wall in health. It is also suggested to be the pathway for high molecular weight plasma proteins, leukocytes and tumor cells across microvessel walls in disease. Thus the first part of the review introduced the mathematical models for water and solutes transport through the interendothelial cleft. These models, combined with the experimental results from in vivo animal studies and electron microscopic observations, are used to evaluate the role of the endothelial surface glycocalyx, the junction strand geometry in the interendothelial cleft, and the surrounding extracellular matrix and tissue cells, as the determinants of microvascular transport. The second part of the review demonstrated how the microvascular permeability, hydrodynamic factors, microvascular geometry and cell adhesion molecules affect tumor cell adhesion in the microcirculation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Adamson, R. H., J. F. Lenz, X. Zhang, G. N. Adamson, S. Weinbaum, and F. E. Curry. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J. Physiol. 557:889–907, 2004.

    Article  PubMed  CAS  Google Scholar 

  2. Akinaga, T., M. Sugihara-Seki, and T. Itano. Electrical charge effect on osmotic flow through pores. J. Phys. Soc. Jpn. 77:053401, 2008.

    Article  Google Scholar 

  3. Anderson, J. L., and D. M. Malone. Mechanism of osmotic flow in porous membranes. Biophys. J. 14:957–982, 1974.

    Article  PubMed  CAS  Google Scholar 

  4. Antonetti, D. A., E. B. Wolpert, L. DeMaio, N. S. Harhaj, and R. C. Scaduto, Jr. Hydrocortisone decreases retinal endothelial cell water and solute flux coincident with increased content and decreased phosphorylation of occludin. J. Neurochem. 80:667–677, 2002.

    Article  PubMed  CAS  Google Scholar 

  5. Arkill, K. P., C. Knupp, C. C. Michel, C. R. Neal, K. Qvortrup, J. Rostgaard, and J. M. Squire. Similar endothelial glycocalyx structures in microvessels from a range of mammalian tissues: evidence for a common filtering mechanism? Biophys. J. 101:1046–1056, 2011.

    Article  PubMed  CAS  Google Scholar 

  6. Bates, D. O., and F. E. Curry. Vascular endothelial growth factor increases hydraulic conductivity of isolated perfused microvessels. Am. J. Physiol. 271(40):H2520–H2528, 1996.

    PubMed  CAS  Google Scholar 

  7. Bates, D. O., R. I. Heald, F. E. Curry, and B. Williams. Vascular endothelial growth factor increases Rana vascular permeability and compliance by different signalling pathways. J. Physiol. 533(Pt. 1):263–272, 2001.

    Article  PubMed  CAS  Google Scholar 

  8. Bell, G. I. Models for the specific adhesion of cells to cells. Science 200:618–627, 1978.

    Article  PubMed  CAS  Google Scholar 

  9. Bhalla, G., and W. M. Deen. Effects of charge on osmotic reflection coefficients of macromolecules in porous membranes. J. Colloid Interface Sci. 333:363–372, 2009.

    Article  PubMed  CAS  Google Scholar 

  10. Bongrand, P., and G. I. Bell. Cell-cell adhesion: parameters and possible mechanisms. In: Cell Surface Dynamics: Concepts and Models, edited by A. Perelson, C. DeLisi, and F. W. Wiegel. New York: Marcel Dekker, 1984.

    Google Scholar 

  11. Brandy, J. F., and G. Bossis. Stokesian dynamics. Annu. Rev. Fluid Mech. 20:111, 1988.

    Article  Google Scholar 

  12. Brenner, H., and P. M. Adler. Dispersion resulting from flow through spatially periodic media: II. Surface and intraparticle transport. Philos. Trans. R. Soc. Lond. A 307:149–200, 1982.

    Article  CAS  Google Scholar 

  13. Brenner, W., P. Langer, F. Oesch, C. J. Edgell, and R. J. Wieser. Tumor cell-endothelium adhesion in an artificial venule. Anal. Biochem. 225:213–219, 1995.

    Article  PubMed  CAS  Google Scholar 

  14. Bundgaard, M. The three-dimensional organization of tight junctions in a capillary endothelium revealed by serial-section electron microscopy. J. Ultrastruct. Res. 88:1–17, 1984.

    Article  PubMed  CAS  Google Scholar 

  15. Cancel, L. M., A. Fitting, and J. M. Tarbell. In vitro study of LDL transport under pressurized (convective) conditions. Am. J. Physiol. 293:H126–H132, 2007.

    CAS  Google Scholar 

  16. Caputo, K. E., and D. A. Hammer. Effect of microvillus deformability on leukocyte adhesion explored using adhesive dynamics simulations. Biophys. J. 89:187–200, 2005.

    Article  PubMed  CAS  Google Scholar 

  17. Chang, K. C., and D. A. Hammer. Influence of direction and type of applied force on the detachment of macromolecularly-bound particles from surfaces. Langmuir 12:2271–2282, 1996.

    Article  CAS  Google Scholar 

  18. Chang, K. C., D. F. J. Tees, and D. A. Hammer. The state diagram for cell adhesion under flow: leukocyte rolling and firm adhesion. PNAS 12:2271–2282, 2000.

    Google Scholar 

  19. Chen, B., and B. M. Fu. An electrodiffusion-filtration model for effects of surface glycocalyx on microvessel permeability to macromolecules. ASME J. Biomech. Eng. 126:614–624, 2004.

    Article  Google Scholar 

  20. Chotard-Ghodsnia, R., O. Haddad, A. Leyrat, A. Drochon, C. Verdier, and A. Duperray. Morphological analysis of tumor cell/endothelial cell interactions under shear flow. J. Biomech. 40:335–344, 2007.

    Article  PubMed  Google Scholar 

  21. Constantinescu, A., J. A. Spaan, E. K. Arkenbout, H. Vink, and J. W. Vanteeffelen. Degradation of the endothelial glycocalyx is associated with chylomicron leakage in mouse cremaster muscle microcirculation. Thromb. Haemost. 105(5):790–801, 2011.

    Article  PubMed  CAS  Google Scholar 

  22. Curry, F. E., and R. H. Adamson. Endothelial glycocalyx: permeability barrier and mechanosensor. Ann. Biomed. Eng. 40(4):828–839, 2012.

    Article  PubMed  CAS  Google Scholar 

  23. Damiano, E. R., and T. M. Stace. A mechano-electrochemical model of radial deformation of the capillary glycocalyx. Biophys. J. 82:1153–1175, 2002.

    Article  PubMed  CAS  Google Scholar 

  24. Dembo, M., D. C. Torney, K. Saxman, and D. A. Hammer. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. R. Soc. Lond. B Biol. Sci. 234:55–83, 1988.

    Article  PubMed  CAS  Google Scholar 

  25. Drenckhahn, D., and W. Ness. The endothelial contractile cytoskeleton. In: Vascular Endothelium: Physiology, Pathology and Therapeutic Opportunities, edited by G. V. R. Born, and C. J. Schwartz. Stuttgart: Schattauer, 1997, pp. 1–15.

    Google Scholar 

  26. Dvorak, H. F., L. F. Brown, M. Detmar, and A. M. Dvorak. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 146:1029–1039, 1995.

    PubMed  CAS  Google Scholar 

  27. Earley, S., and G. E. Plopper. Disruption of focal adhesion kinase slows transendothelial migration of AU-565 breast cancer cells. Biochem. Biophys. Res. Commun. 350:405–412, 2006.

    Article  PubMed  CAS  Google Scholar 

  28. Fan, J., B. Cai, M. Zeng, Y. Hao, F. G. Giancotti, and B. M. Fu. Integrin β4 signaling promotes mammary tumor cell adhesion to brain microvascular endothelium by inducing ErbB2-medicated secretion of VEGF. Ann. Biomed. Eng. 39(8):2223–2241, 2011.

    Article  PubMed  Google Scholar 

  29. Feng, D., J. A. Nagy, K. Payne, I. Hammel, H. F. Dvorak, and A. M. Dvorak. Pathways of macromolecular extravasation across microvascular endothelium in response to VPF/VEGF and other vasoactive mediators. Microcirculation 6(1):23–44, 1999.

    PubMed  CAS  Google Scholar 

  30. Fu, B. M., B. Chen, and W. Chen. An electrodiffusion model for effects of surface glycocalyx layer on microvessel solute permeability. Am. J. Physiol. 284:H1240–H1250, 2003.

    CAS  Google Scholar 

  31. Fu, B., F. E. Curry, R. H. Adamson, and S. Weinbaum. A model for interpreting the tracer labeling of interendothelial clefts. Ann. Biomed. Eng. 25:375–397, 1997.

    Article  PubMed  CAS  Google Scholar 

  32. Fu, B. M., F. E. Curry, and S. Weinbaum. A diffusion wake model for tracer ultrastructure-permeability studies in microvessels. Am. J. Physiol. 269(38):H2124–H2140, 1995.

    PubMed  CAS  Google Scholar 

  33. Fu, B. M., and S. Shen. Structural mechanisms of vascular endothelial growth factor (VEGF) on microvessel permeability. Am. J. Physiol. 284(6):H2124–H2135, 2003.

    CAS  Google Scholar 

  34. Fu, B. M., and S. Shen. Acute VEGF effect on solution permeability of mammalian microvessels in vivo. Microvasc. Res. 68(1):51–62, 2004.

    Article  PubMed  CAS  Google Scholar 

  35. Fu, B. M., S. Shen, and B. Chen. Structural mechanisms in the abolishment of VEGF-induced microvascular hyperpermeability by cAMP. ASME J. Biomech. Eng. 128(3):313–328, 2006.

    Article  Google Scholar 

  36. Fu, B. M., S. Weinbaum, R. Y. Tsay, and F. E. Curry. A junction-orifice-fiber entrance layer model for capillary permeability: application to frog mesenteric capillaries. ASME J. Biomech. Eng. 116:502–513, 1994.

    Article  CAS  Google Scholar 

  37. Gao, L., and H. H. Lipowsky. Composition of the endothelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvasc. Res. 80:394–401, 2010.

    Article  PubMed  CAS  Google Scholar 

  38. Gassmann, P., M. L. Kang, S. T. Mees, and J. Haier. In vivo tumor cell adhesion in the pulmonary microvasculature is exclusively mediated by tumor cell-endothelial cell interaction. BMC Cancer. 10:177, 2010.

    Article  PubMed  Google Scholar 

  39. Giancotti, F. G. Targeting integrin beta4 for cancer and anti-angiogenic therapy. Trends Pharmacol. Sci. 28:506–511, 2007.

    Article  PubMed  CAS  Google Scholar 

  40. Giavazzi, R., M. Foppolo, R. Dossi, and A. Remuzzi. Rolling and adhesion of human tumor cells on vascular endothelium under physiological flow conditions. J. Clin. Invest. 92:3038–3044, 1993.

    Article  PubMed  CAS  Google Scholar 

  41. Glinskii, O. V., V. H. Huxley, G. V. Glinsky, K. J. Pienta, A. Raz, and V. V. Glinsky. Mechanical entrapment is insufficient and intercellular adhesion is essential for metastatic cell arrest in distant organs. Neoplasia. 7(5):522–527, 2005.

    Article  PubMed  CAS  Google Scholar 

  42. Guo, W., and F. G. Giancotti. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5:816–826, 2004.

    Article  PubMed  CAS  Google Scholar 

  43. Guo, W., Y. Pylayeva, A. Pepe, T. Yoshioka, W. J. Muller, G. Inghirami, and F. G. Giancotti. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell 126:489–502, 2006.

    Article  PubMed  CAS  Google Scholar 

  44. Hammer, D. A., and S. M. Apte. Simulation of cell rolling and adhesion on surfaces in shear flow: general results and analysis of selectin-mediated neutrophil adhesion. Biophys. J. 63:35–57, 1992.

    Article  PubMed  CAS  Google Scholar 

  45. Hippenstiel, S., M. Krull, A. Ikemann, W. Risau, M. Clauss, and N. Suttorp. VEGF induces hyperpermeability by a direct action on endothelial-cells. Am. J. Physiol. 18:L678–L684, 1998.

    Google Scholar 

  46. Hood, J. D., and D. A. Cheresh. Role of integrins in cell invasion and migration. Nat. Rev. Cancer 2:91–100, 2002.

    Article  PubMed  Google Scholar 

  47. Kienast, Y., L. von Baumgarten, M. Fuhrmann, W. E. Klinkert, R. Goldbrunner, J. Herms, and F. Winkle. Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med. 16(1):116–122, 2010.

    Article  PubMed  CAS  Google Scholar 

  48. King, M. R., and D. A. Hammer. Multiparticle adhesive dynamics: hydrodynamic recruitment of rolling leukocytes. PNAS 98:14919–14924, 2001.

    Article  PubMed  CAS  Google Scholar 

  49. Ladd, A. C. J. Numerical simulation of particulate suspensions via a discretized Boltzmann equation. J. Fluid Mech. 271:285–309, 1994.

    Article  CAS  Google Scholar 

  50. Lauffenburger, D. A., and A. F. Horwitz. Cell migration: a physically integrated molecular process. Cell 84:359–369, 1996.

    Article  PubMed  CAS  Google Scholar 

  51. Lee, T. H., H. K. Avraham, S. Jiang, and S. Avraham. Vascular endothelial growth factor modulates the transendothelial migration of MDA-MB-231 breast cancer cells through regulation of brain microvascular endothelial cell permeability. J. Biol. Chem. 278:5277–5284, 2003.

    Article  PubMed  CAS  Google Scholar 

  52. Li, G., and B. M. Fu. An electro-diffusion model for the blood-brain barrier permeability to charged molecules. ASME J. Biomech. Eng. 133(2):0210, 2011.

    Article  Google Scholar 

  53. Li, G., M. Simon, Z. Shi, L. Cancel, J. M. Tarbell, B. Morrison, and B. M. Fu. Permeability of endothelial and astrocyte cocultures: in vitro blood-brain barrier models for drug delivery. Ann. Biomed. Eng. 38(8):2499–2511, 2010.

    Article  PubMed  Google Scholar 

  54. Li, G., W. Yuan, and B. M. Fu. A model for water and solute transport across the blood–brain barrier. J. Biomech. 43(11):2133–2140, 2010.

    Article  PubMed  Google Scholar 

  55. Liang, S., M. J. Slattery, and C. Dong. Shear stress and shear rate differentially affect the multi-step process of leukocyte-facilitated melanoma adhesion. Exp. Cell Res. 310(2):282–292, 2005.

    Article  PubMed  CAS  Google Scholar 

  56. Lipowsky, H. H. The endothelial glycocalyx as a barrier to leukocyte adhesion and its mediation by extracellular proteases. Ann. Biomed. Eng. 40(4):840–848, 2012.

    Article  PubMed  Google Scholar 

  57. Litjens, S. H., J. M. de Pereda, and A. Sonnenberg. Current insights into the formation and breakdown of hemidesmosomes. Trends Cell Biol. 16:376–383, 2006.

    Article  PubMed  CAS  Google Scholar 

  58. Liu, Q., D. Mirc, and B. M. Fu. Mechanical mechanisms of thrombosis in intact bent microvessels of rat mesentery. J. Biomech. 41:2726–2734, 2008.

    Article  PubMed  Google Scholar 

  59. Long, D. S., M. L. Smith, A. R. Pries, K. Ley, and E. R. Damiano. Microviscometry reveals reduced blood viscosity and altered shear rate and shear stress profiles in microvessels after hemodilution. Proc. Natl Acad. Sci. USA 101:10060–10065, 2004.

    Article  PubMed  CAS  Google Scholar 

  60. McDonald, D. M., G. Thurston, and P. Baluk. Endothelial gaps as sites for plasma leakage in inflammation. Microcirculation. 6(1):7–22, 1999.

    PubMed  CAS  Google Scholar 

  61. Michel, C. C., and F. E. Curry. Microvascular permeability. Physiol. Rev. 79(3):703–761, 1999.

    PubMed  CAS  Google Scholar 

  62. Michel, C. C., and C. R. Neal. Openings through endothelial cells associated with increased microvascular permeability. Microcirculation 6(1):45–62, 1999.

    PubMed  CAS  Google Scholar 

  63. Moasser, M. M., A. Basso, S. D. Averbuch, and N. Rosen. The tyrosine kinase inhibitor ZD1839 (“Iressa”) inhibits HER2-driven signaling and suppresses the growth of HER2-overexpressing tumor cells. Cancer Res. 61:7184–7188, 2001.

    PubMed  CAS  Google Scholar 

  64. Mook, O. R. F., J. Marle, H. Vreeling-Sindelarova, R. Jongens, W. M. Frederiks, and C. J. K. Noorden. Visualisation of early events in tumor formation of eGFP-transfected rat colon cancer cells in liver. Hepatology 38:295–304, 2003.

    Article  PubMed  Google Scholar 

  65. Mukhopadhyay, D., J. A. Nagy, E. J. Manseau, and H. F. Dvorak. Vascular permeability factor/vascular endothelial growth factor-mediated signaling in mouse mesentery vascular endothelium. Cancer Res. 58(6):1278–1284, 1998.

    PubMed  CAS  Google Scholar 

  66. Ogston, A. G., B. N. Preston, and J. D. Wells. On the transport of compact particles through solutions of chain-polymers. Proc. R. Soc. Lond. A 333:297–316, 1973.

    Article  CAS  Google Scholar 

  67. Olsson, A. K., A. Dimberg, J. Kreuger, and L. Claesson-Welsh. VEGF receptor signalling—in control of vascular function. Nat. Rev. Mol. Cell Biol. 7(5):359–371, 2006.

    Article  PubMed  CAS  Google Scholar 

  68. Phillips, R. J., W. M. Deen, and J. F. Brady. Hindered transport in fibrous membranes and gels: effect of solute size and fiber configuration. J. Colloid Interface Sci. 139(2):363–373, 1990.

    Article  CAS  Google Scholar 

  69. Reitsma, S., D. W. Slaaf, H. Vink, M. A. van Zandvoort, and M. G. oude Egbrink. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch. 454:345–359, 2007.

    Article  PubMed  CAS  Google Scholar 

  70. Roberts, W. G., and G. E. Palade. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J. Cell Sci. 108:2369–2379, 1995.

    PubMed  CAS  Google Scholar 

  71. Salmon, A. H., C. R. Neal, L. M. Sage, C. A. Glass, S. J. Harper, and D. O. Bates. Angiopoietin-1 alters microvascular permeability coefficients in vivo via modification of endothelial glycocalyx. Cardiovasc. Res. 83(1):24–33, 2009.

    Article  PubMed  CAS  Google Scholar 

  72. Salmon, A. H., and S. C. Satchell. Endothelial glycocalyx dysfunction in disease: albuminuria and increased microvascular permeability. J. Pathol. 226(4):562–574, 2012.

    Article  PubMed  CAS  Google Scholar 

  73. Schluter, K., P. Gassmann, A. Enns, T. Korb, A. Hemping-Bovenkerk, J. Holzen, and J. Haier. Organ-specific metastatic tumor cell adhesion and extravasation of colon carcinoma cells with different metastatic potential. Am. J. Pathol. 169:1064–1073, 2006.

    Article  PubMed  Google Scholar 

  74. Shao, J. Y., and G. Xu. The adhesion between a microvillus-bearing cell and a ligand- coated substrate: a Monte Carlo study. Ann. Biomed. Eng. 35:397–407, 2007.

    Article  PubMed  Google Scholar 

  75. Shen, S., J. Fan, B. Cai, Y. Lv, M. Zeng, Y. Hao, F. G. Giancotti, and B. M. Fu. Vascular endothelial growth factor enhances mammary cancer cell adhesion to endothelium in vivo. J. Exp. Physiol. 95:369–379, 2010.

    Article  CAS  Google Scholar 

  76. Slattery, M. J., S. Liang, and C. Dong. Distinct role of hydrodynamic shear in leukocyte-facilitated tumor cell extravasation. Am. J. Physiol. 288:C831–C839, 2005.

    Article  CAS  Google Scholar 

  77. Squire, J. M., M. Chew, G. Nneji, C. Neal, J. Barry, and C. C. Michel. Quasi-periodic substructure in the microvessel endothelial glycocalyx: a possible explanation for molecular filtering? J. Struct. Biol. 136:239–255, 2001.

    Article  PubMed  CAS  Google Scholar 

  78. Steeg, P. S., and D. Theodorescu. Metastasis: a therapeutic target for cancer. Nat. Clin. Pract. Oncol. 5(4):206–219, 2008.

    Article  PubMed  CAS  Google Scholar 

  79. Steinbauer, M., M. Guba, G. Cernaianu, G. Köhl, M. Cetto, L. A. Kunz-Schugart, E. K. Gcissler, W. Falk, and K. W. Jauch. GFP-transfected tumor cells are useful in examining early metastasis in vivo, but immune reaction precludes long-term development studies in immunocompetent mice. Clin. Exp. Metastasis 20:135–141, 2003.

    Article  PubMed  CAS  Google Scholar 

  80. Sugihara-Seki, M. Transport of spheres suspended in the fluid flowing between hexagonally arranged cylinders. J. Fluid Mech. 551:309–321, 2006.

    Article  Google Scholar 

  81. Sugihara-Seki, M., T. Akinaga, and T. Itano. Flow across microvessel walls through the endothelial surface glycocalyx and the interendothelial cleft. J. Fluid Mech. 601:229–252, 2008.

    Article  Google Scholar 

  82. Sugihara-Seki, M., T. Akinaga, and T. Itano. Effects of electric charge on osmotic flow across periodically arranged circular cylinders. J. Fluid Mech. 664:174–192, 2010.

    Article  Google Scholar 

  83. Tarbell, J. M., and M. Y. Pahakis. Mechanotransduction and the glycocalyx. J. Intern. Med. 259:339–350, 2006.

    Article  PubMed  CAS  Google Scholar 

  84. van den Berg, B. M., H. Vink, and J. A. Spaan. The endothelial glycocalyx protects against myocardial edema. Circ. Res. 92:592–594, 2003.

    Article  PubMed  Google Scholar 

  85. van Hinsbergh, V. W., and G. P. Nieuw Amerongen. Intracellular signalling involved in modulating human endothelial barrier function. J. Anat. 200:549–560, 2002.

    Article  PubMed  Google Scholar 

  86. Vink, H., and B. R. Duling. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ. Res. 79:581–589, 1996.

    Article  PubMed  CAS  Google Scholar 

  87. Wang, J. K., M. J. Slattery, M. H. Hoskins, S. L. Liang, C. Dong, and Q. Du. Monte Carlo simulation of heterotypic cell aggregation in nonlinear shear flow. Math. Biosci. Eng. 3:683–696, 2006.

    Article  PubMed  Google Scholar 

  88. Weinbaum, S., J. M. Tarbell, and E. R. Damiano. The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Eng. 9:121–167, 2007.

    Article  PubMed  CAS  Google Scholar 

  89. Wu, H. M., Q. Huang, Y. Yuan, and H. J. Grange. VEGF induces NO dependent hyperpermeability in coronary venules. Am. J. Physiol. 40:H2735–H2739, 1996.

    Google Scholar 

  90. Yan, W. W., B. Cai, Y. Liu, and B. M. Fu. Effects of wall shear stress and its gradient on tumor cell adhesion in curved microvessels. Biomech. Model. Mechanobiol., 2012. doi:10.1007/s10237-011-0339-6.

  91. Yan, W. W., Y. Liu, and B. M. Fu. Effects of curvature and cell–cell interaction on cell adhesion in microvessels. Biomech. Model. Mechanobiol. 9:629–640, 2010.

    Article  PubMed  CAS  Google Scholar 

  92. Yen, W. Y., B. Cai, M. Zeng, J. M. Tarbell, and B. M. Fu. Quantification of the endothelial surface glycocalyx on rat and mouse blood vessels. Microvas. Res., 2012. doi:10.1016/j.mvr.2012.02.005.

  93. Yuan, W., G. Li, M. Zeng, and B. M. Fu. Modulation of the blood–brain barrier permeability by plasma glycoprotein orosomucoid. Microvasc. Res. 80(1):148–157, 2010.

    Article  PubMed  CAS  Google Scholar 

  94. Yuan, W., Y. Lv, M. Zeng, and B. M. Fu. Non-invasive method for the measurement of solute permeability of rat pial microvessels. Microvasc. Res. 77:166–173, 2009.

    Article  PubMed  CAS  Google Scholar 

  95. Zhang, X., F. E. Curry, and S. Weinbaum. Mechanism of osmotic flow in a periodic fiber array. Am. J. Physiol. 290:H844–H852, 2006.

    CAS  Google Scholar 

  96. Zhu, C. Kinetics and mechanics of cell adhesion. J. Biomech. 33:23–33, 2000.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the support from the NSF CBET 0754158 and NIH CA153325-01 and CA137788-01, and Hong Kong Research Grants Council of the Government of the HKSAR PolyU 5238/08E.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bingmei M. Fu.

Additional information

Associate Editor Scott L. Diamond oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fu, B.M., Liu, Y. Microvascular Transport and Tumor Cell Adhesion in the Microcirculation. Ann Biomed Eng 40, 2442–2455 (2012). https://doi.org/10.1007/s10439-012-0561-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-012-0561-0

Keywords

Navigation