Abstract
Microvascular growth and remodeling processes are essential to tissue maintenance and repair. While several biochemical regulators have been elucidated, the effects of dynamic mechanical regulatory factors, including local tissue deformation, extracellular matrix mechanical properties, and both luminal and abluminal flow, are incompletely understood. Mechanical regulation is particularly relevant to the field of tissue engineering and regenerative medicine. Recent experimental evidence suggests that microvessels are highly sensitive to changes in local tissue properties like stiffness, ECM density, and external loading. However, an integrated understanding of how microvascular networks are regulated by mechanical factors has not been fully established. In this review, we discuss the microvascular responses to mechanical factors first in terms of cell-based responses and then describe the nuances of these responses when integrated into a multicellular microvessel structure. Finally, we consider the progress in computational modeling approaches to study angiogenesis, wherein the integration of multiple synergistic, antagonistic, or competing stimuli driving the process of microvascular growth and remodeling can be studied, providing better control over experimentally inaccessible variables. By creating a loop wherein experimental data informs computational experiments and vice versa, mechanical effects on microvasculature can be more fully understood and leveraged for engineered tissues.
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References
Adams RH, Eichmann A (2010) Axon guidance molecules in vascular patterning. Cold Spring Harb Perspect Biol 2:a001875. https://doi.org/10.1101/cshperspect.a001875
Anderson AR, Chaplain MA (1998) Continuous and discrete mathematical models of tumor-induced angiogenesis. Bull Math Biol 60:857–899. https://doi.org/10.1006/bulm.1998.0042
Atala A, Kasper FK, Mikos AG (2012) Engineering complex tissues. Sci Transl Med 4:160rv112. https://doi.org/10.1126/scitranslmed.3004890
Ausprunk DH, Folkman J (1977) Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res 14:53–65
Awolesi MA, Sessa WC, Sumpio BE (1995) Cyclic strain upregulates nitric oxide synthase in cultured bovine aortic endothelial cells. J Clin Invest 96:1449–1454. https://doi.org/10.1172/JCI118181
Bauer AL, Jackson TL, Jiang Y (2007) A cell-based model exhibiting branching and anastomosis during tumor-induced angiogenesis. Biophys J 92:3105–3121. https://doi.org/10.1529/biophysj.106.101501
Bauer AL, Jackson TL, Jiang Y (2009) Topography of extracellular matrix mediates vascular morphogenesis and migration speeds in angiogenesis. PLoS Comput Biol 5:e1000445. https://doi.org/10.1371/journal.pcbi.1000445
Bauer AL, Jackson TL, Jiang Y, Rohlf T (2010) Receptor cross-talk in angiogenesis: mapping environmental cues to cell phenotype using a stochastic, Boolean signaling network model. J Theor Biol 264:838–846. https://doi.org/10.1016/j.jtbi.2010.03.025
Bentley K, Gerhardt H, Bates PA (2008) Agent-based simulation of notch-mediated tip cell selection in angiogenic sprout initialisation. J Theor Biol 250:25–36. https://doi.org/10.1016/j.jtbi.2007.09.015
Bergers G, Song S (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro-Oncology 7:452–464. https://doi.org/10.1215/S1152851705000232
Bergmann CE et al (2006) Arteriogenesis depends on circulating monocytes and macrophage accumulation and is severely depressed in op/op mice. J Leukoc Biol 80:59–65. https://doi.org/10.1189/jlb.0206087
Boerckel JD, Uhrig BA, Willett NJ, Huebsch N, Guldberg RE (2011) Mechanical regulation of vascular growth and tissue regeneration in vivo. Proc Natl Acad Sci U S A 108:E674–E680. https://doi.org/10.1073/pnas.1107019108
Bookholt FD, Monsuur HN, Gibbs S, Vermolen FJ (2016) Mathematical modelling of angiogenesis using continuous cell-based models. Biomech Model Mechanobiol 15:1577–1600. https://doi.org/10.1007/s10237-016-0784-3
Bordeleau F et al (2017) Matrix stiffening promotes a tumor vasculature phenotype. Proc Natl Acad Sci U S A 114:492–497. https://doi.org/10.1073/pnas.1613855114
Burton AC (1954) Relation of structure to function of the tissues of the wall of blood vessels. Physiol Rev 34:619–642
Buschmann I et al (2010) Pulsatile shear and Gja5 modulate arterial identity and remodeling events during flow-driven arteriogenesis. Development 137:2187–2196. https://doi.org/10.1242/dev.045351. 137/13/2187 [pii]
Caille N, Tardy Y, Meister JJ (1998) Assessment of strain field in endothelial cells subjected to uniaxial deformation of their substrate. Ann Biomed Eng 26:409–416
Califano JP, Reinhart-King CA (2008) A balance of substrate mechanics and matrix chemistry regulates endothelial cell network assembly. Cell Mol Bioeng 1:122. https://doi.org/10.1007/s12195-008-0022-x
Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298–307. https://doi.org/10.1038/nature10144
Carosi JA, Eskin SG, McIntire LV (1992) Cyclical strain effects on production of vasoactive materials in cultured endothelial cells. J Cell Physiol 151:29–36. https://doi.org/10.1002/jcp.1041510106
Ceccarelli J, Cheng A, Putnam AJ (2012) Mechanical strain controls endothelial patterning during angiogenic sprouting. Cell Mol Bioeng 5:463–473. https://doi.org/10.1007/s12195-012-0242-y
Chambers RC, Leoni P, Kaminski N, Laurent GJ, Heller RA (2003) Global expression profiling of fibroblast responses to transforming growth factor-beta1 reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am J Pathol 162:533–546
Chang CC et al (2012) Determinants of microvascular network topologies in implanted neovasculatures. Arterioscler Thromb Vasc Biol 32:5–14. https://doi.org/10.1161/ATVBAHA.111.238725
Chaplain MA, McDougall SR, Anderson AR (2006) Mathematical modeling of tumor-induced angiogenesis. Annu Rev Biomed Eng 8:233–257. https://doi.org/10.1146/annurev.bioeng.8.061505.095807
Chappell JC, Wiley DM, Bautch VL (2011) Regulation of blood vessel sprouting. Semin Cell Dev Biol 22:1005–1011. https://doi.org/10.1016/j.semcdb.2011.10.006
Charest JM, Califano JP, Carey SP, Reinhart-King CA (2012) Fabrication of substrates with defined mechanical properties and topographical features for the study of cell migration. Macromol Biosci 12:12–20. https://doi.org/10.1002/mabi.201100264
Checa S, Prendergast PJ (2009) A mechanobiological model for tissue differentiation that includes angiogenesis: a lattice-based modeling approach. Ann Biomed Eng 37:129–145. https://doi.org/10.1007/s10439-008-9594-9
Costa KD, Hucker WJ, Yin FC (2002) Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motil Cytoskeleton 52:266–274. https://doi.org/10.1002/cm.10056
Costa G, Harrington KI, Lovegrove HE, Page DJ, Chakravartula S, Bentley K, Herbert SP (2016) Asymmetric division coordinates collective cell migration in angiogenesis. Nat Cell Biol 18:1292–1301. https://doi.org/10.1038/ncb3443
Cullen JP, Sayeed S, Sawai RS, Theodorakis NG, Cahill PA, Sitzmann JV, Redmond EM (2002) Pulsatile flow-induced angiogenesis: role of G(i) subunits. Arterioscler Thromb Vasc Biol 22:1610–1616
Davies PF, Tripathi SC (1993) Mechanical stress mechanisms and the cell. An endothelial paradigm. Circ Res 72:239–245
Davies PF, Dewey CF Jr, Bussolari SR, Gordon EJ, Gimbrone MA Jr (1984) Influence of hemodynamic forces on vascular endothelial function. In vitro studies of shear stress and pinocytosis in bovine aortic cells. J Clin Invest 73:1121–1129. https://doi.org/10.1172/JCI111298
Davies PF, Remuzzi A, Gordon EJ, Dewey CF Jr, Gimbrone MA Jr (1986) Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci U S A 83:2114–2117
Davis GE, Camarillo CW (1996) An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res 224:39–51. https://doi.org/10.1006/excr.1996.0109
Dewey CF Jr, Bussolari SR, Gimbrone MA Jr, Davies PF (1981) The dynamic response of vascular endothelial cells to fluid shear stress. J Biomech Eng 103:177–185
Ding H, Shang K, Lan H, Lei Y, Sheng L, Liu Z, Zeng Y (2015) In vitro simulation research on the hoop stress of myocardial bridge – coronary artery. J Cardiothorac Surg 10:60. https://doi.org/10.1186/s13019-015-0261-6
Discher DE, Janmey P, Wang YL (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139–1143. https://doi.org/10.1126/science.1116995
DuFort CC, Paszek MJ, Weaver VM (2011) Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 12:308–319. https://doi.org/10.1038/nrm3112
Durham JT, Surks HK, Dulmovits BM, Herman IM (2014) Pericyte contractility controls endothelial cell cycle progression and sprouting: insights into angiogenic switch mechanics. Am J Phys Cell Phys 307:C878–C892. https://doi.org/10.1152/ajpcell.00185.2014
Edgar LT, Sibole SC, Underwood CJ, Guilkey JE, Weiss JA (2013) A computational model of in vitro angiogenesis based on extracellular matrix fibre orientation. Comput Methods Biomech Biomed Engin 16:790–801. https://doi.org/10.1080/10255842.2012.662678
Edgar LT et al (2014a) Mechanical interaction of angiogenic microvessels with the extracellular matrix. J Biomech Eng 136:021001. https://doi.org/10.1115/1.4026471
Edgar LT, Underwood CJ, Guilkey JE, Hoying JB, Weiss JA (2014b) Extracellular matrix density regulates the rate of neovessel growth and branching in sprouting angiogenesis. PLoS One 9:e85178. https://doi.org/10.1371/journal.pone.0085178
Edgar LT, Hoying JB, Weiss JA (2015a) In silico investigation of angiogenesis with growth and stress generation coupled to local extracellular matrix density. Ann Biomed Eng 43:1531–1542. https://doi.org/10.1007/s10439-015-1334-3
Edgar LT, Maas SA, Guilkey JE, Weiss JA (2015b) A coupled model of neovessel growth and matrix mechanics describes and predicts angiogenesis in vitro. Biomech Model Mechanobiol 14:767–782. https://doi.org/10.1007/s10237-014-0635-z
Eskin SG, Ives CL, Mcintire LV, Navarro LT (1984) Response of cultured endothelial-cells to steady flow. Microvasc Res 28:87–94. https://doi.org/10.1016/0026-2862(84)90031-1
Folkman J (1997) Angiogenesis and angiogenesis inhibition: an overview. EXS 79:1–8
Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16:4604–4613
Frangos JA, Eskin SG, McIntire LV, Ives CL (1985) Flow effects on prostacyclin production by cultured human endothelial cells. Science 227:1477–1479
Fry DL (1978) The thrombotic process and atherogenesis in specific arterial injury. Summary of workshop 3a: hemodynamic injury. Adv Exp Med Biol 104:353–369
Fukumura D, Jain RK (2007) Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize. J Cell Biochem 101:937–949. https://doi.org/10.1002/jcb.21187
Gaengel K, Genove G, Armulik A, Betsholtz C (2009) Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29:630–638. https://doi.org/10.1161/ATVBAHA.107.161521
Gale NW et al (2004) Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci U S A 101:15949–15954
Galie PA, Nguyen DH, Choi CK, Cohen DM, Janmey PA, Chen CS (2014) Fluid shear stress threshold regulates angiogenic sprouting. Proc Natl Acad Sci U S A 111:7968–7973. https://doi.org/10.1073/pnas.1310842111
Gerhardt H et al (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161:1163–1177
Ghaffari S, Leask RL, Jones EA (2015) Flow dynamics control the location of sprouting and direct elongation during developmental angiogenesis. Development 142:4151–4157. https://doi.org/10.1242/dev.128058
Ghaffari S, Leask RL, Jones EA (2017) Blood flow can signal during angiogenesis not only through mechanotransduction, but also by affecting growth factor distribution. Angiogenesis. https://doi.org/10.1007/s10456-017-9553-x
Ghajar CM et al (2008) The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys J 94:1930–1941. https://doi.org/10.1529/biophysj.107.120774
Gjorevski N, Piotrowski AS, Varner VD, Nelson CM (2015) Dynamic tensile forces drive collective cell migration through three-dimensional extracellular matrices. Sci Rep 5:11458. https://doi.org/10.1038/srep11458
Gonzalez-Cinca R, Folch R, Benitez R, Ramirez-Piscina L, Casademunt J, Hernandez-Machado A (2003) Phase-field models in interfacial pattern formation out of equilibrium. Adv Condens Matter Stat Phys:203–236. arXiv preprint cond-mat/0305058
Graner F, Glazier JA (1992) Simulation of biological cell sorting using a two-dimensional extended Potts model. Phys Rev Lett 69:2013–2016. https://doi.org/10.1103/PhysRevLett.69.2013
Greenberg JI et al (2008) A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 456:809–813. https://doi.org/10.1038/nature07424
Hamm MJ, Kirchmaier BC, Herzog W (2016) Sema3d controls collective endothelial cell migration by distinct mechanisms via Nrp1 and PlxnD1. J Cell Biol 215:415–430. https://doi.org/10.1083/jcb.201603100
Hansen-Smith F, Egginton S, Hudlicka O (1998) Growth of arterioles in chronically stimulated adult rat skeletal muscle. Microcirculation 5:49–59
Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C (1999) Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126:3047–3055
Hellstrom M et al (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445:776–780
Helm CL, Fleury ME, Zisch AH, Boschetti F, Swartz MA (2005) Synergy between interstitial flow and VEGF directs capillary morphogenesis in vitro through a gradient amplification mechanism. Proc Natl Acad Sci U S A 102:15779–15784. https://doi.org/10.1073/pnas.0503681102
Helmlinger G, Berk BC, Nerem RM (1995) Calcium responses of endothelial cell monolayers subjected to pulsatile and steady laminar flow differ. Am J Phys 269:C367–C375
Hernandez Vera R, Genove E, Alvarez L, Borros S, Kamm R, Lauffenburger D, Semino CE (2009) Interstitial fluid flow intensity modulates endothelial sprouting in restricted Src-activated cell clusters during capillary morphogenesis. Tissue Eng A 15:175–185. https://doi.org/10.1089/ten.tea.2007.0314
Hershey JC, Baskin EP, Glass JD, Hartman HA, Gilberto DB, Rogers IT, Cook JJ (2001) Revascularization in the rabbit hindlimb: dissociation between capillary sprouting and arteriogenesis. Cardiovasc Res 49:618–625
Hirschi KK, Rohovsky SA, Beck LH, Smith SR, D’Amore PA (1999) Endothelial cells modulate the proliferation of mural cell precursors via platelet-derived growth factor-BB and heterotypic cell contact. Circ Res 84:298–305
Hoying JB, Utzinger U, Weiss JA (2014) Formation of microvascular networks: role of stromal interactions directing angiogenic growth. Microcirculation 21:278–289. https://doi.org/10.1111/micc.12115
Hsieh HJ, Li NQ, Frangos JA (1991) Shear stress increases endothelial platelet-derived growth factor mRNA levels. Am J Phys 260:H642–H646
Huang S, Ingber DE (1999) The structural and mechanical complexity of cell-growth control. Nat Cell Biol 1:E131–E138. https://doi.org/10.1038/13043
Hudlicka O (1994) Mechanical factors involved in the growth of the heart and its blood vessels. Cell Mol Biol Res 40:143–152
Hudlicka O, Brown MD (1996) Postnatal growth of the heart and its blood vessels. J Vasc Res 33:266–287
Hughes CC (2008) Endothelial-stromal interactions in angiogenesis. Curr Opin Hematol 15:204–209. https://doi.org/10.1097/MOH.0b013e3282f97dbc
Hutchings H, Ortega N, Plouet J (2003) Extracellular matrix-bound vascular endothelial growth factor promotes endothelial cell adhesion, migration, and survival through integrin ligation. FASEB J 17:1520–1522. https://doi.org/10.1096/fj.02-0691fje
Huynh J et al (2011) Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci Transl Med 3:112ra122. https://doi.org/10.1126/scitranslmed.3002761
Iba T, Mills I, Sumpio BE (1992) Intracellular cyclic AMP levels in endothelial cells subjected to cyclic strain in vitro. J Surg Res 52:625–630
Ingber DE (1991) Control of capillary growth and differentiation by extracellular matrix. Use of a tensegrity (tensional integrity) mechanism for signal processing. Chest 99:34S–40S
Ingber DE, Folkman J (1989) Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J Cell Biol 109:317–330
Ingber DE, Prusty D, Sun Z, Betensky H, Wang N (1995) Cell shape, cytoskeletal mechanics, and cell cycle control in angiogenesis. J Biomech 28:1471–1484
Ishida T, Takahashi M, Corson MA, Berk BC (1997) Fluid shear stress-mediated signal transduction: how do endothelial cells transduce mechanical force into biological responses? Ann N Y Acad Sci 811:12–23; discussion 23-14
Jain RK (2003) Molecular regulation of vessel maturation. Nat Med 9:685–693. https://doi.org/10.1038/nm0603-685
Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT (2007) Angiogenesis in brain tumours. Nat Rev Neurosci 8:610–622. https://doi.org/10.1038/nrn2175
Jakobsson L et al (2010) Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 12:943–953. https://doi.org/10.1038/ncb2103
Javierre E, Vermolen FJ, Vuik C, van der Zwaag S (2009) A mathematical analysis of physiological and morphological aspects of wound closure. J Math Biol 59:605–630. https://doi.org/10.1007/s00285-008-0242-7
Jones EA (2011) Mechanical factors in the development of the vascular bed. Respir Physiol Neurobiol 178:59–65. https://doi.org/10.1016/j.resp.2011.03.026
Jones EA, Le NF, Eichmann A (2006) What determines blood vessel structure? Genetic prespecification vs. hemodynamics. Physiology (Bethesda) 21:388–395
Joung IS, Iwamoto MN, Shiu YT, Quam CT (2006) Cyclic strain modulates tubulogenesis of endothelial cells in a 3D tissue culture model. Microvasc Res 71:1–11. https://doi.org/10.1016/j.mvr.2005.10.005
Jung JE et al (2005) STAT3 is a potential modulator of HIF-1-mediated VEGF expression in human renal carcinoma cells. FASEB J 19:1296–1298. https://doi.org/10.1096/fj.04-3099fje
Kanematsu A et al (2004) Type I collagen can function as a reservoir of basic fibroblast growth factor. J Control Release 99:281–292. https://doi.org/10.1016/j.jconrel.2004.07.008
Kang H, Bayless KJ, Kaunas R (2008) Fluid shear stress modulates endothelial cell invasion into three-dimensional collagen matrices. Am J Physiol Heart Circ Physiol 295:H2087–H2097. https://doi.org/10.1152/ajpheart.00281.2008
Kassab GS (2006) Scaling laws of vascular trees: of form and function. Am J Physiol Heart Circ Physiol 290:H894–H903. https://doi.org/10.1152/ajpheart.00579.2005
Kassianidou E, Kumar S (2015) A biomechanical perspective on stress fiber structure and function. Biochim Biophys Acta 1853:3065–3074. https://doi.org/10.1016/j.bbamcr.2015.04.006
Kilarski WW, Samolov B, Petersson L, Kvanta A, Gerwins P (2009) Biomechanical regulation of blood vessel growth during tissue vascularization. Nat Med 15:657–664. https://doi.org/10.1038/nm.1985
Kim S, Bell K, Mousa SA, Varner JA (2000) Regulation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am J Pathol 156:1345–1362
Kim S, Chung M, Ahn J, Lee S, Jeon NL (2016) Interstitial flow regulates the angiogenic response and phenotype of endothelial cells in a 3D culture model. Lab Chip 16:4189–4199. https://doi.org/10.1039/c6lc00910g
Kirkpatrick ND, Andreou S, Hoying JB, Utzinger U (2007) Live imaging of collagen remodeling during angiogenesis. Am J Physiol Heart Circ Physiol 292:H3198–H3206. https://doi.org/10.1152/ajpheart.01234.2006
Kniazeva E, Putnam AJ (2009) Endothelial cell traction and ECM density influence both capillary morphogenesis and maintenance in 3-D. Am J Phys Cell Phys 297:C179–C187. https://doi.org/10.1152/ajpcell.00018.2009
Kniazeva E, Kachgal S, Putnam AJ (2011) Effects of extracellular matrix density and mesenchymal stem cells on neovascularization in vivo. Tissue Eng A 17:905–914. https://doi.org/10.1089/ten.TEA.2010.0275
Kniazeva E, Weidling JW, Singh R, Botvinick EL, Digman MA, Gratton E, Putnam AJ (2012) Quantification of local matrix deformations and mechanical properties during capillary morphogenesis in 3D. Integr Biol 4:431–439. https://doi.org/10.1039/c2ib00120a
Korff T, Augustin HG (1999) Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci 112(Pt 19):3249–3258
Krishnan L, Weiss JA, Wessman MD, Hoying JB (2004) Design and application of a test system for viscoelastic characterization of collagen gels. Tissue Eng 10:241–252. https://doi.org/10.1089/107632704322791880
Krishnan L, Hoying JB, Nguyen H, Song H, Weiss JA (2007) Interaction of angiogenic microvessels with the extracellular matrix. Am J Physiol Heart Circ Physiol 293:H3650–H3658. https://doi.org/10.1152/ajpheart.00772.2007
Krishnan L, Underwood CJ, Maas S, Ellis BJ, Kode TC, Hoying JB, Weiss JA (2008) Effect of mechanical boundary conditions on orientation of angiogenic microvessels. Cardiovasc Res 78:324–332. https://doi.org/10.1093/cvr/cvn055
Krishnan L, Utzinger U, Maas S, Reese S, Weiss JA, Williams SK, Hoying JB (2009) Extracellular matrix stiffness modulates microvascular morphology during early sprouting angiogenesis in vitro. In: ASME 2009 summer bioengineering conference. American Society of Mechanical Engineers, New York, pp 1289–1290
Krishnan R et al (2011) Substrate stiffening promotes endothelial monolayer disruption through enhanced physical forces. Am J Phys Cell Phys 300:C146–C154. https://doi.org/10.1152/ajpcell.00195.2010
Krishnan L, Chang CC, Nunes SS, Williams SK, Weiss JA, Hoying JB (2013) Manipulating the microvasculature and its microenvironment. Crit Rev Biomed Eng 41:91–123. https://doi.org/10.1615/CritRevBiomedEng.2013008077
Kutcher ME, Kolyada AY, Surks HK, Herman IM (2007) Pericyte Rho GTPase mediates both pericyte contractile phenotype and capillary endothelial growth state. Am J Pathol 171:693–701. https://doi.org/10.2353/ajpath.2007.070102
Kutys ML, Doyle AD, Yamada KM (2013) Regulation of cell adhesion and migration by cell-derived matrices. Exp Cell Res 319:2434–2439. https://doi.org/10.1016/j.yexcr.2013.05.030
Larson DM, Carson MP, Haudenschild CC (1987) Junctional transfer of small molecules in cultured bovine brain microvascular endothelial cells and pericytes. Microvasc Res 34:184–199
LaValley DJ, Reinhart-King CA (2014) Matrix stiffening in the formation of blood vessels. Adv Regen Biol 1:25247. https://doi.org/10.3402/arb.v1.25247
le Noble F et al (2004) Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131:361–375. https://doi.org/10.1242/dev.00929
LeBlanc AJ, Nevitt CD (2015) Targeting the vessel underdogs: therapeutic approaches for microvessel dysfunction in the heart. Crit Rev Biomed Eng 43:473–489. https://doi.org/10.1615/CritRevBiomedEng.2016016083
LeBlanc AJ, Krishnan L, Sullivan CJ, Williams SK, Hoying JB (2012) Microvascular repair: post-angiogenesis vascular dynamics. Microcirculation 19:676–695. https://doi.org/10.1111/j.1549-8719.2012.00207.x
Lee S, Zeiger A, Maloney JM, Kotecki M, Van Vliet KJ, Herman IM (2010) Pericyte actomyosin-mediated contraction at the cell-material interface can modulate the microvascular niche. J Phys Condens Matter 22:194115. https://doi.org/10.1088/0953-8984/22/19/194115
Lemon G, Howard D, Rose FR, King JR (2011) Individual-based modelling of angiogenesis inside three-dimensional porous biomaterials. Biosystems 103:372–383. https://doi.org/10.1016/j.biosystems.2010.11.009
Levesque MJ, Nerem RM (1985) The elongation and orientation of cultured endothelial-cells in response to shear-stress. J Biomech Eng-T Asme 107:341–347
Lo CM, Wang HB, Dembo M, Wang YL (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79:144–152. https://doi.org/10.1016/S0006-3495(00)76279-5
Logsdon EA, Finley SD, Popel AS, Mac Gabhann F (2014) A systems biology view of blood vessel growth and remodelling. J Cell Mol Med 18:1491–1508. https://doi.org/10.1111/jcmm.12164
Long BL, Rekhi R, Abrego A, Jung J, Qutub AA (2013) Cells as state machines: cell behavior patterns arise during capillary formation as a function of BDNF and VEGF. J Theor Biol 326:43–57. https://doi.org/10.1016/j.jtbi.2012.11.030
Lu P, Takai K, Weaver VM, Werb Z (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 3:a005058. https://doi.org/10.1101/cshperspect.a005058
Mac Gabhann F, Popel AS (2007) Interactions of VEGF isoforms with VEGFR-1, VEGFR-2, and neuropilin in vivo: a computational model of human skeletal muscle. Am J Phys Heart Circ Phys 292:H459–H474. https://doi.org/10.1152/ajpheart.00637.2006
Mac Gabhann F, Ji JW, Popel AS (2006) Computational model of vascular endothelial growth factor spatial distribution in muscle and pro-angiogenic cell therapy. PLoS Comput Biol 2:e127. https://doi.org/10.1371/journal.pcbi.0020127
Maggelakis SA (2003) A mathematical model of tissue replacement during epidermal wound healing. Appl Math Model 27:189–196. https://doi.org/10.1016/S0307-904X(02)00100-2
Mammoto A et al (2009) A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457:1103–1108. https://doi.org/10.1038/nature07765
Martin A, Komada MR, Sane DC (2003) Abnormal angiogenesis in diabetes mellitus. Med Res Rev 23:117–145. https://doi.org/10.1002/med.10024
Mason BN, Starchenko A, Williams RM, Bonassar LJ, Reinhart-King CA (2013) Tuning three-dimensional collagen matrix stiffness independently of collagen concentration modulates endothelial cell behavior. Acta Biomater 9:4635–4644. https://doi.org/10.1016/j.actbio.2012.08.007
Matsumoto T, Yung YC, Fischbach C, Kong HJ, Nakaoka R, Mooney DJ (2007) Mechanical strain regulates endothelial cell patterning in vitro. Tissue Eng 13:207–217. https://doi.org/10.1089/ten.2006.0058
Mayor R, Etienne-Manneville S (2016) The front and rear of collective cell migration. Nat Rev Mol Cell Biol 17:97–109. https://doi.org/10.1038/nrm.2015.14
Mayrovitz HN, Wiedeman MP, Noordergraaf A (1975) Microvascular hemodynamic variations accompanying microvessel dimensional changes. Microvasc Res 10:322–329
Mayrovitz HN, Tuma RF, Wiedeman MP (1977) Relationship between microvascular blood velocity and pressure distribution. Am J Phys 232:H400–H405
McDougall SR, Anderson AR, Chaplain MA, Sherratt JA (2002) Mathematical modelling of flow through vascular networks: implications for tumour-induced angiogenesis and chemotherapy strategies. Bull Math Biol 64:673–702. https://doi.org/10.1006/bulm.2002.0293
McGettrick HM, Butler LM, Buckley CD, Rainger GE, Nash GB (2012) Tissue stroma as a regulator of leukocyte recruitment in inflammation. J Leukoc Biol 91:385–400. https://doi.org/10.1189/jlb.0911458
Milde F, Bergdorf M, Koumoutsakos P (2008) A hybrid model for three-dimensional simulations of sprouting angiogenesis. Biophys J 95:3146–3160. https://doi.org/10.1529/biophysj.107.124511
Morin KT, Smith AO, Davis GE, Tranquillo RT (2013) Aligned human microvessels formed in 3D fibrin gel by constraint of gel contraction. Microvasc Res 90:12–22. https://doi.org/10.1016/j.mvr.2013.07.010
Mow VC, Holmes MH, Lai WM (1984) Fluid transport and mechanical properties of articular cartilage: a review. J Biomech 17:377–394
Mudera VC et al (2000) Molecular responses of human dermal fibroblasts to dual cues: contact guidance and mechanical load. Cell Motil Cytoskeleton 45:1–9. https://doi.org/10.1002/(SICI)1097-0169(200001)45:1<1::AID-CM1>3.0.CO;2-J
Naruse K, Sokabe M (1993) Involvement of stretch-activated ion channels in Ca2+ mobilization to mechanical stretch in endothelial cells. Am J Phys 264:C1037–C1044
Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ, Spector AA, Chen CS (2005) Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci U S A 102:11594–11599. https://doi.org/10.1073/pnas.0502575102
Nguyen TD, Jones RE, Boyce BL (2008) A nonlinear anisotropic viscoelastic model for the tensile behavior of the corneal stroma. J Biomech Eng 130:041020. https://doi.org/10.1115/1.2947399
Noris M et al (1995) Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. Circ Res 76:536–543
Nunes SS et al (2010a) Implanted microvessels progress through distinct neovascularization phenotypes. Microvasc Res 79:10–20. https://doi.org/10.1016/j.mvr.2009.10.001
Nunes SS, Krishnan L, Gerard CS, Dale JR, Maddie MA, Benton RL, Hoying JB (2010b) Angiogenic potential of microvessel fragments is independent of the tissue of origin and can be influenced by the cellular composition of the implants. Microcirculation 17:557–567. https://doi.org/10.1111/j.1549-8719.2010.00052.x
Nunes SS, Rekapally H, Chang CC, Hoying JB (2011) Vessel arterial-venous plasticity in adult neovascularization. PLoS One 6:e27332. https://doi.org/10.1371/journal.pone.0027332
Orlidge A, D’Amore PA (1987) Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol 105:1455–1462
Oubaha M et al (2012) Formation of a PKCzeta/beta-catenin complex in endothelial cells promotes angiopoietin-1-induced collective directional migration and angiogenic sprouting. Blood 120:3371–3381. https://doi.org/10.1182/blood-2012-03-419721
Patel TH, Kimura H, Weiss CR, Semenza GL, Hofmann LV (2005) Constitutively active HIF-1alpha improves perfusion and arterial remodeling in an endovascular model of limb ischemia. Cardiovasc Res 68:144–154. https://doi.org/10.1016/j.cardiores.2005.05.002
Peirce SM (2008) Computational and mathematical modeling of angiogenesis. Microcirculation 15:739–751. https://doi.org/10.1080/10739680802220331
Peirce SM, Mac Gabhann F, Bautch VL (2012) Integration of experimental and computational approaches to sprouting angiogenesis. Curr Opin Hematol 19:184–191. https://doi.org/10.1097/MOH.0b013e3283523ea6
Pelham RJ Jr, Wang Y (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci U S A 94:13661–13665
Pellegrin S, Mellor H (2007) Actin stress fibres. J Cell Sci 120:3491–3499. https://doi.org/10.1242/jcs.018473
Pepper MS (1997) Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev 8:21–43
Pipp F et al (2004) Elevated fluid shear stress enhances postocclusive collateral artery growth and gene expression in the pig hind limb. Arterioscler Thromb Vasc Biol 24:1664–1668. https://doi.org/10.1161/01.ATV.0000138028.14390.e4
Plutoni C et al (2016) P-cadherin promotes collective cell migration via a Cdc42-mediated increase in mechanical forces. J Cell Biol 212:199–217. https://doi.org/10.1083/jcb.201505105
Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146:873–887. https://doi.org/10.1016/j.cell.2011.08.039
Price GM, Wong KH, Truslow JG, Leung AD, Acharya C, Tien J (2010) Effect of mechanical factors on the function of engineered human blood microvessels in microfluidic collagen gels. Biomaterials 31:6182–6189. https://doi.org/10.1016/j.biomaterials.2010.04.041
Pries AR, Secomb TW, Gaehtgens P (1995) Design principles of vascular beds. Circ Res 77:1017–1023
Pries AR, Secomb TW, Gaehtgens P (1998) Structural adaptation and stability of microvascular networks: theory and simulations. Am J Phys 275:H349–H360
Pries AR, Reglin B, Secomb TW (2005) Remodeling of blood vessels: responses of diameter and wall thickness to hemodynamic and metabolic stimuli. Hypertension 46:725–731. https://doi.org/10.1161/01.HYP.0000184428.16429.be
Pugsley MK, Tabrizchi R (2000) The vascular system. An overview of structure and function J Pharmacol Toxicol Methods 44:333-340
Qi YX et al (2016) Nuclear envelope proteins modulate proliferation of vascular smooth muscle cells during cyclic stretch application. Proc Natl Acad Sci U S A 113:5293–5298. https://doi.org/10.1073/pnas.1604569113
Qutub AA, Popel AS (2009) Elongation, proliferation & migration differentiate endothelial cell phenotypes and determine capillary sprouting. BMC Syst Biol 3:13–13. https://doi.org/10.1186/1752-0509-3-13
Qutub AA, Mac Gabhann F, Karagiannis ED, Vempati P, Popel AS (2009) Multiscale models of angiogenesis. IEEE Eng Med Biol Mag 28:14–31. https://doi.org/10.1109/MEMB.2009.931791
Rao RR, Peterson AW, Ceccarelli J, Putnam AJ, Stegemann JP (2012) Matrix composition regulates three-dimensional network formation by endothelial cells and mesenchymal stem cells in collagen/fibrin materials. Angiogenesis 15:253–264. https://doi.org/10.1007/s10456-012-9257-1
RayChaudhury A, D’Amore PA (1991) Endothelial cell regulation by transforming growth factor-beta. J Cell Biochem 47:224–229. https://doi.org/10.1002/jcb.240470307
Reese SP, Underwood CJ, Weiss JA (2013) Effects of decorin proteoglycan on fibrillogenesis, ultrastructure, and mechanics of type I collagen gels. Matrix Biol 32:414–423. https://doi.org/10.1016/j.matbio.2013.04.004
Reginato S, Gianni-Barrera R, Banfi A (2011) Taming of the wild vessel: promoting vessel stabilization for safe therapeutic angiogenesis. Biochem Soc Trans 39:1654–1658. https://doi.org/10.1042/bst20110652
Reglin B, Secomb TW, Pries AR (2009) Structural adaptation of microvessel diameters in response to metabolic stimuli: where are the oxygen sensors? Am J Physiol Heart Circ Physiol 297:H2206–H2219. https://doi.org/10.1152/ajpheart.00348.2009
Reinhart-King CA, Dembo M, Hammer DA (2008) Cell-cell mechanical communication through compliant substrates. Biophys J 95:6044–6051. https://doi.org/10.1529/biophysj.107.127662
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 81:177–199
Rivron NC, Vrij EJ, Rouwkema J, Le Gac S, van den Berg A, Truckenmuller RK, van Blitterswijk CA (2012) Tissue deformation spatially modulates VEGF signaling and angiogenesis. Proc Natl Acad Sci U S A 109:6886–6891. https://doi.org/10.1073/pnas.1201626109
Ruehle MA, Krishnan L, LaBelle SA, Willett NJ, Weiss JA, Guldberg RE (2017) Decorin-containing collagen hydrogels as dimensionally stable scaffolds to study the effects of compressive mechanical loading on angiogenesis. MRS Commun:1–6. https://doi.org/10.1557/mrc.2017.54
Rutkowski JM, Swartz MA (2007) A driving force for change: interstitial flow as a morphoregulator. Trends Cell Biol 17:44–50. https://doi.org/10.1016/j.tcb.2006.11.007
Santos-Oliveira P et al (2015) The force at the tip – modelling tension and proliferation in sprouting angiogenesis. PLoS Comput Biol 11:e1004436. https://doi.org/10.1371/journal.pcbi.1004436
Saunders RL, Hammer DA (2010) Assembly of human umbilical vein endothelial cells on compliant hydrogels. Cell Mol Bioeng 3:60–67. https://doi.org/10.1007/s12195-010-0112-4
Scheel K, Fitzgerald E, Martin R, Larsen R (1979) The possible role of mechanical stresses on coronary collateral development during gradual coronary occlusion. In: Schaper W (ed) The pathophysiology of myocardial perfusion. Elsevier, Amsterdam, pp 489–518
Sears NA, Seshadri DR, Dhavalikar PS, Cosgriff-Hernandez E (2016) A review of three-dimensional printing in tissue engineering. Tissue Eng Part B Rev 22:298–310. https://doi.org/10.1089/ten.TEB.2015.0464
Secomb TW, Pries AR (2011) The microcirculation: physiology at the mesoscale. J Physiol 589:1047–1052. https://doi.org/10.1113/jphysiol.2010.201541
Secomb TW, Dewhirst MW, Pries AR (2011) Structural adaptation of normal and tumour vascular networks. Basic Clin Pharmacol Toxicol. https://doi.org/10.1111/j.1742-7843.2011.00815.x
Semenza GL (2000) HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 88:1474–1480
Shamloo A (2014) Cell-cell interactions mediate cytoskeleton organization and collective endothelial cell chemotaxis. Cytoskeleton (Hoboken, NJ) 71:501–512. https://doi.org/10.1002/cm.21185
Shamloo A, Heilshorn SC (2010) Matrix density mediates polarization and lumen formation of endothelial sprouts in VEGF gradients. Lab Chip 10:3061–3068. https://doi.org/10.1039/c005069e
Shamloo A, Mohammadaliha N, Heilshorn SC, Bauer AL (2016) A comparative study of collagen matrix density effect on endothelial sprout formation using experimental and computational approaches. Ann Biomed Eng 44:929–941. https://doi.org/10.1007/s10439-015-1416-2
Shukla A, Dunn AR, Moses MA, Van Vliet KJ (2004) Endothelial cells as mechanical transducers: enzymatic activity and network formation under cyclic strain. Mech Chem Biosyst 1:279–290
Shweiki D, Itin A, Soffer D, Keshet E (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843–845. https://doi.org/10.1038/359843a0
Sieminski AL, Hebbel RP, Gooch KJ (2004) The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Exp Cell Res 297:574–584. https://doi.org/10.1016/j.yexcr.2004.03.035
Song JW, Munn LL (2011) Fluid forces control endothelial sprouting. Proc Natl Acad Sci U S A 108:15342–15347. https://doi.org/10.1073/pnas.1105316108
Stabenfeldt SE, Gourley M, Krishnan L, Hoying JB, Barker TH (2012) Engineering fibrin polymers through engagement of alternative polymerization mechanisms. Biomaterials 33:535–544. https://doi.org/10.1016/j.biomaterials.2011.09.079
Streit M, Riccardi L, Velasco P, Brown LF, Hawighorst T, Bornstein P, Detmar M (1999) Thrombospondin-2: a potent endogenous inhibitor of tumor growth and angiogenesis [In Process Citation]. Proc Natl Acad Sci U S A 96:14888–14893
Stupack DG, Cheresh DA (2002) ECM remodeling regulates angiogenesis: endothelial integrins look for new ligands. Sci STKE 2002:pe7. https://doi.org/10.1126/stke.2002.119.pe7
Sulsky D, Zhou S-J, Schreyer HL (1995) Application of a particle-in-cell method to solid mechanics. Comput Phys Commun 87:236–252. https://doi.org/10.1016/0010-4655(94)00170-7
Sumpio BE, Banes AJ, Levin LG, Johnson G Jr (1987) Mechanical stress stimulates aortic endothelial cells to proliferate. J Vasc Surg 6:252–256
Sumpio BE, Banes AJ, Buckley M, Johnson G Jr (1988) Alterations in aortic endothelial cell morphology and cytoskeletal protein synthesis during cyclic tensional deformation. J Vasc Surg 7:130–138
Sun J, Jamilpour N, Wang FY, Wong PK (2014) Geometric control of capillary architecture via cell-matrix mechanical interactions. Biomaterials 35:3273–3280. https://doi.org/10.1016/j.biomaterials.2013.12.101
Sun X, Evren S, Nunes SS (2015) Blood vessel maturation in health and disease and its implications for vascularization of engineered tissues. Crit Rev Biomed Eng 43:433–454. https://doi.org/10.1615/CritRevBiomedEng.2016016063
Sun X, Altalhi W, Nunes SS (2016) Vascularization strategies of engineered tissues and their application in cardiac regeneration. Adv Drug Deliv Rev 96:183–194. https://doi.org/10.1016/j.addr.2015.06.001
Tambe DT et al (2011) Collective cell guidance by cooperative intercellular forces. Nat Mater 10:469–475. https://doi.org/10.1038/nmat3025
Theveneau E, Marchant L, Kuriyama S, Gull M, Moepps B, Parsons M, Mayor R (2010) Collective chemotaxis requires contact-dependent cell polarity. Dev Cell 19:39–53. https://doi.org/10.1016/j.devcel.2010.06.012
Topper JN, Cai J, Falb D, Gimbrone MA Jr (1996) Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli: cyclooxygenase-2, manganese superoxide dismutase, and endothelial cell nitric oxide synthase are selectively up-regulated by steady laminar shear stress. Proc Natl Acad Sci USA 93:10417–10422
Travasso RD, Corvera Poire E, Castro M, Rodriguez-Manzaneque JC, Hernandez-Machado A (2011) Tumor angiogenesis and vascular patterning: a mathematical model. PLoS One 6:e19989. https://doi.org/10.1371/journal.pone.0019989
Trepat X, Fredberg JJ (2011) Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol 21:638–646. https://doi.org/10.1016/j.tcb.2011.06.006
Tschumperlin DJ et al (2004) Mechanotransduction through growth-factor shedding into the extracellular space. Nature 429:83–86. https://doi.org/10.1038/nature02543
Tzima E et al (2005) A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437:426–431. https://doi.org/10.1038/nature03952
Udan RS, Vadakkan TJ, Dickinson ME (2013) Dynamic responses of endothelial cells to changes in blood flow during vascular remodeling of the mouse yolk sac. Development 140:4041–4050. https://doi.org/10.1242/dev.096255
Uematsu M et al (1995) Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Phys 269:C1371–C1378
Underwood CJ, Edgar LT, Hoying JB, Weiss JA (2014) Cell-generated tkraction forces and the resulting matrix deformation modulate microvascular alignment and growth during angiogenesis. Am J Physiol Heart Circ Physiol. https://doi.org/10.1152/ajpheart.00995.2013
Utzinger U, Baggett B, Weiss JA, Hoying JB, Edgar LT (2015) Large-scale time series microscopy of neovessel growth during angiogenesis. Angiogenesis 18:219–232. https://doi.org/10.1007/s10456-015-9461-x
Uzer G et al (2015) Cell mechanosensitivity to extremely low-magnitude signals is enabled by a LINCed nucleus. Stem Cells 33:2063–2076. https://doi.org/10.1002/stem.2004
Uzer G, Rubin CT, Rubin J (2016) Cell mechanosensitivity is enabled by the LINC nuclear complex. Curr Mol Biol Rep 2:36–47. https://doi.org/10.1007/s40610-016-0032-8
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 92:929–936. https://doi.org/10.1161/01.RES.0000068377.01063.79
van Nieuw Amerongen GP, Koolwijk P, Versteilen A, van Hinsbergh VW (2003) Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler Thromb Vasc Biol 23:211–217
van Oers RF, Rens EG, LaValley DJ, Reinhart-King CA, Merks RM (2014) Mechanical cell-matrix feedback explains pairwise and collective endothelial cell behavior in vitro. PLoS Comput Biol 10:e1003774. https://doi.org/10.1371/journal.pcbi.1003774
Vavourakis V, Eiben B, Hipwell JH, Williams NR, Keshtgar M, Hawkes DJ (2016) Multiscale mechano-biological finite element modelling of oncoplastic breast surgery – numerical study towards surgical planning and cosmetic outcome prediction. PLoS One 11:e0159766. https://doi.org/10.1371/journal.pone.0159766
Vempati P, Mac Gabhann F, Popel AS (2010) Quantifying the proteolytic release of extracellular matrix-sequestered VEGF with a computational model. PLoS One 5:e11860. https://doi.org/10.1371/journal.pone.0011860
Vempati P, Popel AS, Mac Gabhann F (2011) Formation of VEGF isoform-specific spatial distributions governing angiogenesis: computational analysis. BMC Syst Biol 5:59. https://doi.org/10.1186/1752-0509-5-59
Vermolen FJ, Gefen A (2012) A semi-stochastic cell-based formalism to model the dynamics of migration of cells in colonies. Biomech Model Mechanobiol 11:183–195. https://doi.org/10.1007/s10237-011-0302-6
Vitorino P, Meyer T (2008) Modular control of endothelial sheet migration. Genes Dev 22:3268–3281. https://doi.org/10.1101/gad.1725808
Vitorino P, Hammer M, Kim J, Meyer T (2011) A steering model of endothelial sheet migration recapitulates monolayer integrity and directed collective migration. Mol Cell Biol 31:342–350. https://doi.org/10.1128/mcb.00800-10
Walpole J, Chappell JC, Cluceru JG, Mac Gabhann F, Bautch VL, Peirce SM (2015) Agent-based model of angiogenesis simulates capillary sprout initiation in multicellular networks. Integr Biol 7:987–997. https://doi.org/10.1039/c5ib00024f
Wang DL, Wung BS, Peng YC, Wang JJ (1995) Mechanical strain increases endothelin-1 gene expression via protein kinase C pathway in human endothelial cells. J Cell Physiol 163:400–406. https://doi.org/10.1002/jcp.1041630220
Wang N et al (2001) Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci USA 98:7765–7770. https://doi.org/10.1073/pnas.141199598
Wimmer R, Cseh B, Maier B, Scherrer K, Baccarini M (2012) Angiogenic sprouting requires the fine tuning of endothelial cell cohesion by the Raf-1/Rok-alpha complex. Dev Cell 22:158–171. https://doi.org/10.1016/j.devcel.2011.11.012
Yao C, Roderfeld M, Rath T, Roeb E, Bernhagen J, Steffens G (2006) The impact of proteinase-induced matrix degradation on the release of VEGF from heparinized collagen matrices. Biomaterials 27:1608–1616. https://doi.org/10.1016/j.biomaterials.2005.08.037
Yeh YT, Hur SS, Chang J, Wang KC, Chiu JJ, Li YS, Chien S (2012) Matrix stiffness regulates endothelial cell proliferation through septin 9. PLoS One 7:e46889. https://doi.org/10.1371/journal.pone.0046889
Yokoyama S, Matsui TS, Deguchi S (2017) New wrinkling substrate assay reveals traction force fields of leader and follower cells undergoing collective migration. Biochem Biophys Res Commun 482:975–979. https://doi.org/10.1016/j.bbrc.2016.11.142
Zakrzewicz A, Secomb TW, Pries AR (2002) Angioadaptation: keeping the vascular system in shape. News Physiol Sci 17:197–201
Zeng G et al (2007) Orientation of endothelial cell division is regulated by VEGF signaling during blood vessel formation. Blood 109:1345–1352. https://doi.org/10.1182/blood-2006-07-037952
Zhao S, Suciu A, Ziegler T, Moore JE Jr, Burki E, Meister JJ, Brunner HR (1995) Synergistic effects of fluid shear stress and cyclic circumferential stretch on vascular endothelial cell morphology and cytoskeleton. Arterioscler Thromb Vasc Biol 15:1781–1786
Acknowledgments
This work was supported by the US Department of Defense (DoD) through the Armed Forces Institute of Regenerative Medicine (AFIRM) grant W81XWH-14-2-0003 to RG; NIH R01-AR069297 to RG, LK, JW; and R01-HL131856 to JW, JH.
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Krishnan, L., LaBelle, S.A., Ruehle, M.A., Weiss, J.A., Hoying, J.B., Guldberg, R.E. (2021). Mechanical Regulation of Microvascular Growth and Remodeling. In: Holnthoner, W., Banfi, A., Kirkpatrick, J., Redl, H. (eds) Vascularization for Tissue Engineering and Regenerative Medicine. Reference Series in Biomedical Engineering(). Springer, Cham. https://doi.org/10.1007/978-3-319-54586-8_19
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