Correction: The vital role of blood flow-induced proliferation and migration in capillary network formation in a multiscale model of angiogenesis (PLoS ONE (2015) 10:6 (e0128878) DOI: 10.1371/journal.pone.0128878);The vital role of blood flow-induced proliferation and migration in capillary network formation in a multiscale model of angiogenesis

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Bazmara, Hossein ^a   Soltani, Madjid ^a,b   Sefidgar, Mostafa ^a   Bazargan, Majid ^a   Naeenian, Mojtaba Mousavi ^a   Rahmim, Arman ^b  

^a K N TOOSI UNIVERSITY OF TECHNOLOGY   (Iran)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANASTOMOSIS; ANGIOGENESIS; ARTICLE; CAPILLARY FLOW; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; MATHEMATICAL MODEL; MULTISCALE MODEL; PHENOTYPE; SIGNAL TRANSDUCTION; SPROUTING ANGIOGENESIS; SURVIVAL; TUMOR BLOOD FLOW; TUMOR VASCULARIZATION; ANIMAL; BIOLOGICAL MODEL; BLOOD VESSEL; CELL MOTION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEMODYNAMICS; HUMAN; METABOLISM; VASCULAR ENDOTHELIUM;

ANGIOGENIC PROTEIN;

ANGIOGENIC PROTEINS; ANIMALS; BLOOD VESSELS; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HEMODYNAMICS; HUMANS; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION;

EID: 84934915530     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0175601     Document Type: Erratum

References (85)

1. Knierim M, Paweletz N. Tumor-related Angiogenesis. Crit Rev Oncol Hematol. 1989; 9:197-242. PMID: 2480145
2. Gimbrone M, Cotran R, Leapman S, Folkman J. Tumor growth and neovascularization: An experimental model using the rabbit cornea. J Natn Cancer Inst. 1974; 52:413-427.
3. Muthukkaruppan V, Kubai L, Auerbach R. Tumor-induced neovascularization in the mouse eye. J Natn Cancer Inst. 1982; 65:699-705.
4. Kerbel RS. Tumor angiogenesis. N Engl J Med. 2008; 358:2039-49. doi: 10.1056/NEJMra0706596 PMID: 18463380
5. Qutub AA, Mac Gabhann F, Karagiannis emmanouil D, Vempati P, Popel AS. Multiscale Models of Angiogenesis. IEEE Eng Med Biol Mag. 2009;14-31. doi: 10.1109/MEMB.2009.934244 PMID: 19775952
6. Anderson ARA, Chaplain MAJ, McDougall SR. A Hybrid Discrete-Continuum Model of Tumour Induced Angiogenesis. In: Jackson TL, editor. Modeling Tumor Vasculature. New York, NY: Springer; 2012. pp. 105-134.
7. Chaplain MAJ, McDougall SR, Anderson ARA. Blood Flow and Tumour-Induced Angiogenesis: Dynamically Adapting Vascular Networks. In: Jackson TL, editor. Modeling Tumor Vasculature. New York, NY: Springer; 2012. pp. 167-212.
8. Cai Y, Xu S, Wu J, Long Q. Coupled modelling of tumour angiogenesis, tumour growth and blood perfusion. J Theor Biol. Elsevier; 2011; 279:90-101. doi: 10.1016/j.jtbi.2011.02.017 PMID: 21392511
9. Milde F, Bergdorf M, Koumoutsakos P. A hybrid model for three-dimensional simulations of sprouting angiogenesis. Biophys J. Elsevier; 2008; 95:3146-60. doi: 10.1529/biophysj.107.124511 PMID: 18586846
10. Owen MR, Alarcón T, Maini PK, Byrne HM. Angiogenesis and vascular remodelling in normal and cancerous tissues. J Math Biol. 2009; 58:689-721. doi: 10.1007/s00285-008-0213-z PMID: 18941752
11. Perfahl H, Byrne HM, Chen T, Estrella V, Alarcón T, Lapin A, et al. Multiscale modelling of vascular tumour growth in 3D: the roles of domain size and boundary conditions. PLoS One. 2011; 6:e14790. doi: 10.1371/journal.pone.0014790 PMID: 21533234
12. Bauer AL, Jackson TL, Jiang Y. Topography of extracellular matrix mediates vascular morphogenesis and migration speeds in angiogenesis. PLoS Comput Biol. 2009; 5:e1000445. doi: 10.1371/journal.pcbi.1000445 PMID: 19629173
13. Bauer AL, Jackson TL, Jiang Y. A cell-based model exhibiting branching and anastomosis during tumor-induced angiogenesis. Biophys J. 2007; 92:3105-21. PMID: 17277180
14. Mahoney AW, Smith BG, Flann NS, Podgorski GJ. Discovering novel cancer therapies: A computational modeling and search approach. 2008 IEEE Symp Comput Intell Bioinforma Comput Biol. Ieee; 2008;233-240. doi: 10.1109/CIBCB.2008.4675785
15. Mahoney AW, Podgorski GJ, Flann NS. Multiobjective optimization based-approach for discovering novel cancer therapies. IEEE/ACM Trans Comput Biol Bioinform. 2012; 9:169-84. doi: 10.1109/TCBB.2010.39 PMID: 20479506
16. Bauer AL, Jackson TL, Jiang Y, Rohlf T. Receptor cross-talk in angiogenesis: mapping environmental cues to cell phenotype using a stochastic, Boolean signaling network model. J Theor Biol. Elsevier; 2010; 264:838-46. doi: 10.1016/j.jtbi.2010.03.025 PMID: 20307549
17. Bauer AL, Rohlf T. Investigating the Role of Cross-Talk Between Chemical and Stromal Factors in Endothelial Cell Phenotype Determination. In: Jackson TL, editor. Modeling Tumor Vasculature. New York: Springer; 2012. pp. 89-101.
18. Shirinifard A, Gens JS, Zaitlen BL, Popławski NJ, Swat M, Glazier JA. 3D multi-cell simulation of tumor growth and angiogenesis. PLoS One. 2009; 4:e7190. doi: 10.1371/journal.pone.0007190 PMID: 19834621
19. Merks RMH, Perryn ED, Shirinifard A, Glazier JA. Contact-inhibited chemotaxis in de novo and sprouting blood-vessel growth. PLoS Comput Biol. 2008; 4:e1000163. doi: 10.1371/journal.pcbi.1000163 PMID: 18802455
20. Muñoz-Chápuli R, Quesada AR, Angel Medina M. Angiogenesis and signal transduction in endothelial cells. Cell Mol Life Sci. 2004; 61:2224-43. doi: 10.1007/s00018-004-4070-7 PMID: 15338053
21. Traub O, Berk BC. Laminar Shear Stress: Mechanisms by Which Endothelial Cells Transduce an Atheroprotective Force. Arterioscler Thromb Vasc Biol. 1998; 18:677-685. doi: 10.1161/01.ATV.18.5.677 PMID: 9598824
22. Berk BC. Atheroprotective signaling mechanisms activated by steady laminar flow in endothelial cells. Circulation. 2008; 117:1082-9. doi: 10.1161/CIRCULATIONAHA.107.720730 PMID: 18299513
23. Ando J, Yamamoto K. Flow detection and calcium signalling in vascular endothelial cells. Cardiovasc Res. 2013; 99:1-9. doi: 10.1093/cvr/cvt084 PMID: 23720275
24. Ando J, Yamamoto K. Vascular Mechanobiology Endothelial Cell Responses to Fluid Shear Stress. Circ J. 2009; 73:1983-1992. PMID: 19801852
25. Johnson BD, Mather KJ, Wallace JP. Mechanotransduction of shear in the endothelium: basic studies and clinical implications. Vasc Med. 2011; 16:365-77. doi: 10.1177/1358863X11422109 PMID: 22003002
26. Davies PF. Flow-Mediated Endothelial Mechanotransduction. physiol Rev. 1995; 75:519-560. PMID: 7624393
27. Kaiser D, Freyberg M, Friedl P. Lack of hemodynamic forces triggers apoptosis in vascular endothelial cells. Biochem Biophys Res Commun. 1997; 231:586-90. PMID: 9070851
28. Dimmeler S, Haendeler J, Rippmann V, Nehls M, Zeiher A. Shear stress inhibits apoptosis of human endothelial cells. FEBS Lett. 1996; 399:71-4. PMID: 8980122
29. Levesque M, Nerem R, Sprague E. Vascular endothelial cell proliferation in culture and the influence of flow. Biomaterials. 1990; 11:702-7. PMID: 2090307
30. Li S, Butler P, Wang Y, Hu Y, Han DC, Usami S, et al. The role of the dynamics of focal adhesion kinase in the mechanotaxis of endothelial cells. Proc Natl Acad Sci USA. 2002; 99:3546-3551. PMID: 11891289
31. Hsu P, Li S, Li Y, Usami S, Ratcliffe A, Wang X, et al. Effects of flow patterns on endothelial cell migration into a zone of mechanical denudation. Biochem Biophys Res Commun. 2001; 285:751-9. PMID: 11453657
32. Li S, Huang NF, Hsu S. Mechanotransduction in endothelial cell migration. J Cell Biochem. 2005; 96:1110-26. doi: 10.1002/jcb.20614 PMID: 16167340
33. Okahara K, Kambayashi J, Ohnishi T, Fujiwara Y, Kawasaki T, Monden M. Shear stress induces expression of CNP gene in human endothelial cells. FEBS Lett. 1995; 373:108-10. PMID: 7589445
34. Chun T, Itoh H, Ogawa Y, Tamura N, Takaya K, Igaki T, et al. Shear stress augments expression of C-type natriuretic peptide and adrenomedullin. Hypertension. 1997; 29:1296-302. PMID: 9180632
35. Shyy YJ, Chien S. Role of integrins in endothelial mechanosensing of shear stress. Circ Res. 2002; 91:769-775. PMID: 12411390
36. Li Y, Haga J, Chien S. Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech. 2005; 38:1949-1971. PMID: 16084198
37. Ishida T, Peterson T, Kovach N, Berk B. MAP kinase activation by flow in endothelial cells. Role of beta 1 integrins and tyrosine kinases. Circ Res. 1996; 79:310-316. PMID: 8756009
38. Li S, Kim M, Hu Y-L, Jalali S, Schlaepfer DD, Hunter T, et al. Fluid Shear Stress Activation of Focal Adhesion Kinase Linking to mitogen-activated protein kinases. J Biol Chem. 1997; 272:30455-30462. PMID: 9374537
39. Xia Z, Dickens M, Raingeaud J, Davis R, Greenberg M. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science (80:) . 1995; 270:1326-1331.
40. Chen KD. Mechanotransduction in Response to Shear Stress. J Biol Chem. 1999; 274:18393-18400. doi: 10.1074/jbc.274.26.18393 PMID: 10373445
41. Shay-Salit A, Shushy M, Wolfovitz E, Yahav H, Breviario F, Dejana E, et al. VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc Natl Acad Sci USA. 2002; 99:9462-7. doi: 10.1073/pnas.142224299 PMID: 12080144
42. Lee H, Koh G. Shear stress activates Tie2 receptor tyrosine kinase in human endothelial cells. Biochem Biophys Res Commun. 2003; 304:399-404. PMID: 12711329
43. Jin Z- G, Ueba H, Tanimoto T, Lungu AO, Frame MD, Berk BC. Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ Res. 2003; 93:354-63. doi: 10.1161/01.RES.0000089257.94002.96 PMID: 12893742
44. Ngai CY, Yao X. Vascular Responses to Shear Stress : The Involvement of Mechanosensors in Endothelial Cells. Open Circ Vasc J. 2010; 3:85-94.
45. Osawa M, Masuda M, Kusano K, Fujiwara K. Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J Cell Biol. 2002; 158:773-785. doi: 10.1083/jcb.200205049 PMID: 12177047
46. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature. 2005; 437:426-431. PMID: 16163360
47. Chien S, Li S, Shyy YJ. Effects of Mechanical Forces on Signal Transduction and Gene Expression in Endothelial Cells. Hypertension. 1998; 31:162-169. doi: 10.1161/01.HYP.31.1.162 PMID: 9453297
48. Lehoux S, Tedgui a. Signal Transduction of Mechanical Stresses in the Vascular Wall. Hypertension. 1998; 32:338-345. doi: 10.1161/01.HYP.32.2.338 PMID: 9719064
49. Riaz A. Adhesion Dependent Signals: Cell Survival, Receptor Crosstalk and Mechanostimulation. PhD Thesis, Uppsala University. 2013.
50. Pan S. Molecular mechanisms responsible for the atheroprotective effects of laminar shear stress. Antioxid Redox Signal. 2009; 11:1669-82. doi: 10.1089/ARS.2009.2487 PMID: 19309258
51. Holderfield MT, Hughes CCW. Crosstalk between vascular endothelial growth factor, notch, and transforming growth factor-beta in vascular morphogenesis. Circ Res. 2008; 102:637-52. doi: 10.1161/CIRCRESAHA.107.167171 PMID: 18369162
52. Glazier JA, Graner F. Simulation of the differential adhesion driven arrangement of biological cells. Phys Rev E. 1993; 47:2128-2154.
53. Shamloo A, Heilshorn SC. Matrix density mediates polarization and lumen formation of endothelial sprouts in VEGF gradients. Lab Chip. 2010; 10:3061-8. doi: 10.1039/c005069e PMID: 20820484
54. Garipcan B, Maenz S, Pham T, Settmacher U, Jandt KD, Zanow J, et al. Image Analysis of Endothelial Microstructure and Endothelial Cell Dimensions of Human Arteries - A Preliminary Study. Adv Eng Mater. 2011; 13:B54-B57. doi: 10.1002/adem.201080076
55. Song JW, Bazou D, Munn LL. Anastomosis of endothelial sprouts forms new vessels in a tissue analogue of angiogenesis. Integr Biol (Camb). 2012; 4:857-62. doi: 10.1039/c2ib20061a PMID: 22673771
56. Armer HEJ, Mariggi G, Png KMY, Genoud C, Monteith AG, Bushby AJ, et al. Imaging transient blood vessel fusion events in zebrafish by correlative volume electron microscopy. PLoS One. 2009; 4: e7716. doi: 10.1371/journal.pone.0007716 PMID: 19893745
57. Mariggi G. Connecting the Tips - A Study on Sprout Fusion in Angiogenesis. PhD Thesis, University College London. 2012.
58. Lenard A, Ellertsdottir E, Herwig L, Krudewig A, Sauteur L, Belting H- G, et al. In vivo analysis reveals a highly stereotypic morphogenetic pathway of vascular anastomosis. Dev Cell. 2013; 25:492-506. doi: 10.1016/j.devcel.2013.05.010 PMID: 23763948
59. Herwig L, Blum Y, Krudewig A, Ellertsdottir E, Lenard A, Belting H-G, et al. Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr Biol. 2011; 21:1942-8. doi: 10.1016/j.cub.2011.10.016 PMID: 22079115
60. Estrach S, Cailleteau L, Franco CA, Gerhardt H, Stefani C, Lemichez E, et al. Laminin-binding integrins induce Dll4 expression and Notch signaling in endothelial cells. Circ Res. 2011; 109:172-82. doi: 10.1161/CIRCRESAHA.111.240622 PMID: 21474814
61. Song JW, Munn LL. Fluid forces control endothelial sprouting. Proc Natl Acad Sci USA. 2011; 108:15342-7. doi: 10.1073/pnas.1105316108 PMID: 21876168
62. Mantzaris N V., Webb S, Othmer HG. Mathematical modeling of tumor-induced angiogenesis. J Math Biol. 2004; 49:111-187. PMID: 15293017
63. Stephanou A, McDougall SR, Anderson ARA, Chaplain MAJ. Mathematical modelling of the influence of blood rheological properties upon adaptative tumour-induced angiogenesis. Math Comput Model. 2006; 44:96-123.
64. Stapor PC, Wang W, Murfee WL, Khismatullin DB. The Distribution of Fluid Shear Stresses in Capillary Sprouts. Cardiovasc Eng Technol. 2011; 2:124-136. doi: 10.1007/s13239-011-0041-y
65. Soltani M, Chen P. Numerical Modeling of Interstitial Fluid Flow Coupled with Blood Flow through a Remodeled Solid Tumor Microvascular Network. PLoS One. 2013; 8. doi: 10.1371/journal.pone.0067025
66. Soltani M, Chen P. Numerical modeling of fluid flow in solid tumors. PLoS One. 2011; 6:e20344. doi: 10.1371/journal.pone.0020344 PMID: 21673952
67. Cooke JP, Rossitch E, Andon N a, Loscalzo J, Dzau VJ. Flow activates an endothelial potassium channel to release an endogenous nitrovasodilator. J Clin Invest. 1991; 88:1663-71. doi: 10.1172/JCI115481 PMID: 1719029
68. Pries AR, Neuhaus D, Gaehtgens P. Blood viscosity in tube flow: dependence on diameter and hematocrit. Am J Philol. 1992; 263:1770-1778.
69. Pries AR, Secomb TW, Gaehtgens P. Biophysical aspects of blood flow in the microvasculature. Cardiovasc Res. 1996; 32:654-67. PMID: 8915184
70. Sefidgar M, Soltani M, Raahemifar K, Bazmara H, Nayinian SM, Bazargan M. Effect of tumor shape, size, and tissue transport properties on drug delivery to solid tumors. J Biol Eng. 2014; 8:12. doi: 10.1186/1754-1611-8-12 PMID: 24987457
71. Gerlowski LE, Jain RK. Microvascular Permeability of Normal and Neoplastic Tissues. Microvasc Res. 1986; 31:288-305. PMID: 2423854
72. Sefidgar M, Soltani M, Raahemifar K, Sadeghi M, Bazmara H, Bazargan M, et al. Numerical modeling of drug delivery in a dynamic solid tumor microvasculature. Microvasc Res. 2015; 99:43-56. http://dx.doi.org/10.1016/j.mvr.2015.02.007 doi: 10.1016/j.mvr.2015.02.007 PMID: 25724978
73. Serini G, Ambrosi D, Giraudo E, Gamba A, Preziosi L, Bussolino F. Modeling the early stages of vascular network assembly. EMBO J. 2003; 22:1771-1779. PMID: 12682010
74. Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology. 2005; 69:4-10. PMID: 16301830
75. Jiang Y, Pjesivac-grbovic J, Cantrell C, Freyer JP. A multiscale model for avascular tumor growth. Biophys J. 2005; 89:3884-3894. PMID: 16199495
76. Sefidgar M, Soltani M, Bazmara H, Mousavi M, Bazargan M, Elkamel A. Interstitial Flow in Cancerous Tissue: Effect of Considering Remodeled Capillary Network. J Tissue Sci Eng. 2014; S4. doi: 10.4172/2157-7552.S4-003
77. Késmárky G, Kenyeres P, Rábai M, Tóth K. Plasma viscosity: A forgotten variable. Clin Hemorheol Microcirc. 2008; 39:243-246. PMID: 18503132
78. Stylianopoulos T, Soteriou K, Fukumura D, Jain RK. Cationic nanoparticles have superior transvascular flux into solid tumors: insights from a mathematical model. Ann Biomed Eng. 2013; 41:68-77. doi: 10.1007/s10439-012-0630-4 PMID: 22855118
79. Udan RS, Vadakkan TJ, Dickinson ME. Dynamic responses of endothelial cells to changes in blood flow during vascular remodeling of the mouse yolk sac. Development. 2013; 140:4041-50. doi: 10.1242/dev.096255 PMID: 24004946
80. Clark ER. Studies on the growth of blood-vessels in the tail of the frog larva - by observation and experiment on the living animal. Am J Anat. 1918; 23:37-88.
81. Meeson A, Palmer M, Calfon M, Lang R. A relationship between apoptosis and flow during programmed capillary regression is revealed by vital analysis. Development. 1996; 3938:3929-3938.
82. Pries AR, Reglin B, Secomb TW. Structural Adaptation of Vascular Networks: Role of the Pressure Response. Hypertension. 2001; 38:1476-1479. doi: 10.1161/hy1201.100592 PMID: 11751739
83. Resnick N, Yahav H, Shay-salit A, Shushy M, Schubert S, Chen L, et al. Fluid shear stress and the vascular endothelium: for better and for worse. Prog Biophys Mol Biol. 2003; 81:177-199. PMID: 12732261
84. Kearney JB, Kappas NC, Ellerstrom C, Dipaola FW, Bautch VL. The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood. 2004; 103:4527-4535. doi: 10.1182/blood-2003-07-2315 PMID: 14982871
85. Ausprunk DH, Folkman J. Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res. 1977; 14:53-65. PMID: 895546