Biomechanics and Modeling in Mechanobiology

, Volume 4, Issue 4, pp 211–220 | Cite as

The influence of fluid shear stress on the remodeling of the embryonic primary capillary plexus

  • Jeffrey S. Blatnik
  • Geert W. Schmid-Schönbein
  • Lanping Amy Sung
Original paper

Abstract

The primary capillary plexus in early yolk sacs is remodeled into matured vitelline vessels aligned in the direction of blood flow at the onset of cardiac contraction. We hypothesized that the influence of fluid shear stress on cellular behaviors may be an underlying mechanism by which some existing capillary channels remain open while others are closed during remodeling. Using a recently developed E-Tmod knock-out/lacZ knock-in mouse model, we showed that erythroblasts exhibited rheological properties similar to those of a viscous cell suspension. In contrast, the non-erythroblast (NE) cells, which attach among themselves within the yolk sac, are capable of lamellipodia extension and cell migration. Isolated NE cells in a parallel-plate flow chamber exposed to fluid shear stress, however, ceased lamellipodia extension. Such response may minimize NE cell migration into domains exposed to fluid shear stress. A two-dimensional mathematical model incorporating these cellular behaviors demonstrated that shear stress created by the blood flow initiated by the embryonic heart contraction might be needed for the remodeling of primary capillary plexus.

Keywords

Angiogenesis Embryonic vascular development Fluid shear stress Microvascular growth Primary capillary plexus Vasculogenesis 

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References

  1. Auspunk D, Folkman J (1977) Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res 14:53–65CrossRefPubMedGoogle Scholar
  2. Barbee KA, Davies PF, Lal R (1994) Shear stress-induced reorganization of the surface topography of living endothelial cells imaged by atomic force microscopy. Circ Res 74:163–171PubMedGoogle Scholar
  3. Breier G, Breviario F, Caveda L, Berthier R, Schnurch H, Gotsch U, Vestweber D, Risau W, Dejana E (1996) Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood 87:630–641PubMedGoogle Scholar
  4. Caduff HJ, Fischer LC, Burri PH (1986) Scanning electron microscope study of the developing microvasculature in the postnatal lung. Anat Rec 216:154–164CrossRefPubMedGoogle Scholar
  5. Chu X, Chen J, Reedy MC, Vera C, Sung KLP, Sung LA (2003) E-Tmod capping of actin filaments at the slow-growing end is required to establish mouse embryonic circulation. Am J Physiol Heart Circ Physiol 284:H1827–H1838PubMedGoogle Scholar
  6. Djonov V, Kurz H, Burri PH (2002) Optimality in the developing vascular system: branching remodeling by means of intussusception as an efficient adaptation mechanism. Dev Dyn 224:391–402CrossRefPubMedGoogle Scholar
  7. Fisher AB, Chien S, Barakat AI, Nerem RM (2001) Endothelial cellular response to altered shear stress. Am J Physiol Lung Cell Mol Physiol 281:L529–L533Google Scholar
  8. Folkman J (1982) Angiogenesis: initiation and control. Ann N Y Ac Sci 401:212–227CrossRefGoogle Scholar
  9. Fukuda S, Schmid-Schönbein GW (2002) Centrifugation annihilates the fluid shear response of circulating leukocytes. J Leuk Biol 72:133–139Google Scholar
  10. Hogan B, Beddington R, Costantini F, Lacy E (1994) Manipulating the Mouse Embryo: Second Edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 373–375Google Scholar
  11. Johnson RM. (1994) Membrane stress increases cation permeability in red cells. Biophys J 67:1876–1881PubMedCrossRefGoogle Scholar
  12. Konstantopoulos K, Wu KK, Udden MM, Banez EI, Shattil SJ, Hellums JD (1995) Flow cytometric studies of platelet responses to shear stress in whole blood. Biorheology 32:73–93PubMedGoogle Scholar
  13. Kurz H (2000) Physiology of angiogenesis. J Neuro Onc 50:17–35CrossRefGoogle Scholar
  14. Kurz H, Burri PH, Djonov VG (2003) Angiogenesis and vascular remodeling by intussusception: From form to function. News Physiol Sci 18:65–70PubMedGoogle Scholar
  15. Li W, Johnson SA, Shelley WC, Ferkowicz M, Morrison P, Li Y, Yoder MC (2003) Primary endothelial cells isolated from the yolk sac and para-aortic splanchnopleura support the expansion of adult marrow stem cells in vitro. Blood 102:4345–4353CrossRefPubMedGoogle Scholar
  16. Manoussaki D, Lubkin SR, Vernon RB, Murray JD (1996) A mechanical model for the formation of vascular networks in vitro. Acta Biotheor 44:271–282PubMedCrossRefGoogle Scholar
  17. McCue S, Noria S, Langille BL (2004) Shear-induced reorganization of endothelial cell cytoskeleton and adhesion complexes. Trends Cardiovasc Med 14:143–151CrossRefPubMedGoogle Scholar
  18. McGrath KE, Koniski AD, Malik J, Palis J (2003) Circulation is established in a stepwise pattern in the mammalian embryo. Blood 101:1669-1676CrossRefPubMedGoogle Scholar
  19. Moazzam F, DeLano FA, Zweifbach BW, Schmid-Schönbein GW (1997) The leukocyte response to fluid shear stress. Proc Natl Acad Sci USA 94:5338–5343CrossRefPubMedGoogle Scholar
  20. Murray JD, Swanson KR (1999) On the mechanochemical theory of biological pattern formation with applications to wound healing and angiogenesis. In: Chaplain M, McLachlan JC, Singh G (eds) On growth and form: spatio-temporal pattern formation in biology. Wiley, Chichester, pp 251–285Google Scholar
  21. Namy P, Ohayon J, Tracqui P (2004) Critical conditions for pattern formation and tubulogenesis driven by cellular traction fields. J Theor Biol 227:103–120CrossRefPubMedMathSciNetGoogle Scholar
  22. Patan S, Haenni B, Burri PH (1993) Evidence for intussusceptive capillary growth in the chicken chorio-allantoic membrane (CAM). Anat Embryol 187:121–130CrossRefPubMedGoogle Scholar
  23. Resnick N, Yahav H, Shay-Salit A, Shushy M, Schubert S, Zilberman LC, Wofovitz E (2003) Fluid shear stress and the vascular endothelium: for better and for worse. Prog Biophys Mol Biol 81:177–199CrossRefGoogle Scholar
  24. Risau W (1997) Mechanisms of angiogenesis. Nature 386:671–674CrossRefPubMedGoogle Scholar
  25. Risau W, and Flamme I (1995) Vasculogenesis. Annu Rev Cell Dev Biol 11:73–91CrossRefPubMedGoogle Scholar
  26. Sato TN, Loughna S (2002) Vasculogenesis and angiogenesis. In mouse development. Academic, New York, pp 211–233Google Scholar
  27. Van Gieson EJ, Murfee WL, Skalak TC, Price RJ (2003) Enhanced smooth muscle cell coverage of microvessels exposed to increased hemodynamic stresses in vivo. Circ Res 92:929–936CrossRefPubMedGoogle Scholar
  28. Zawicki DF, Jain RK, Schmid-Schönbein GW, Chien S (1981) Dynamics of neovascularization in normal tissue. Microvas Res 21:27–47CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Jeffrey S. Blatnik
    • 1
  • Geert W. Schmid-Schönbein
    • 1
  • Lanping Amy Sung
    • 1
  1. 1.Department of BioengineeringUniversity of California, San DiegoLa JollaUSA

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