Research article Special Issues

The force of cell-cell adhesion in determining the outcome in a nonlocal advection diffusion model of wound healing


  • Received: 31 December 2021 Revised: 19 May 2022 Accepted: 09 June 2022 Published: 16 June 2022
  • A model of wound healing is presented to investigate the connection of the force of cell-cell adhesion to the sensing radius of cells in their spatial environment. The model consists of a partial differential equation with nonlocal advection and diffusion terms, describing the movement of cells in a spatial environment. The model is applied to biological wound healing experiments to understand incomplete wound closure. The analysis demonstrates that for each value of the force of adhesion parameter, there is a critical value of the sensing radius above which complete wound healing does not occur.

    Citation: Glenn Webb. The force of cell-cell adhesion in determining the outcome in a nonlocal advection diffusion model of wound healing[J]. Mathematical Biosciences and Engineering, 2022, 19(9): 8689-8704. doi: 10.3934/mbe.2022403

    Related Papers:

  • A model of wound healing is presented to investigate the connection of the force of cell-cell adhesion to the sensing radius of cells in their spatial environment. The model consists of a partial differential equation with nonlocal advection and diffusion terms, describing the movement of cells in a spatial environment. The model is applied to biological wound healing experiments to understand incomplete wound closure. The analysis demonstrates that for each value of the force of adhesion parameter, there is a critical value of the sensing radius above which complete wound healing does not occur.



    加载中


    [1] M. Basan, J. Elgeti, E. Hannezo, W. J. Rappel, H. Levine, Alignment of cellular motility forces with tissue flow as a mechanism for efficient wound healing, Proc. Natl. Acad. Sci., 110 (2013), 2452–2459. https://doi.org/10.1073/pnas.1219937110 doi: 10.1073/pnas.1219937110
    [2] H. Byrne, M. A. J. Chaplain, D. L. Evans, I. Hopkinson, Mathematical modelling of angiogenesis in wound healing: Comparison of theory and experiment, J. Theor. Med., 2 (2000), 175–197. https://doi.org/10.1080/10273660008833045 doi: 10.1080/10273660008833045
    [3] G. J. Doherty, H. T. McMahon, Mediation, modulation and consequences of membrane-cytoskeleton interactions, Ann. Rev. Biophys., 37 (2008), 65–95. https://doi.org/10.1146/annurev.biophys.37.032807.125912 doi: 10.1146/annurev.biophys.37.032807.125912
    [4] J. Jonkman, J. Cathcart, F. Xu, M. Bartolini, J. Amon, K. Stevens, et al., An introduction to the wound healing assay using live-cell microscopy, Cell Adh. Migr., 8 (2014), 440–451. https://doi.org/10.4161/cam.36224 doi: 10.4161/cam.36224
    [5] S. Kauanova, A. Urazbayev, I. Vorobjev, The frequent sampling of wound scratch assay reveals the "opportunity" window for quantitative evaluation of cell motility-impeding drugs, Front. Cell Dev. Biol., 11 (2021), 391. https://doi.org/10.3389/fcell.2021.640972 doi: 10.3389/fcell.2021.640972
    [6] D. L. Nikolic, A. N. Boettiger, D. Bar-Sagi, J. D. Carbeck, S. Y. Shvartsman, Role of boundary conditions in an experimental model of epithelial wound healing, Am. J. Physiol. Cell Physiol., 291 (2006), C68–C75. https://doi.org/10.1152/ajpcell.00411.2005 doi: 10.1152/ajpcell.00411.2005
    [7] J. O$'$Connor, A. Stevens, E. Shannon, F. Akbar, K. LaFever, N. Narayanan, et al., Proteolytic activation of Growth-blocking peptides triggers calcium responses through the GPCR Mthl10 during epithelial wound detection, Dev. Cell, 56 (2021), 2160–2175. https://doi.org/10.1016/j.devcel.2021.06.020 doi: 10.1016/j.devcel.2021.06.020
    [8] J. S. Ross, J. A. Fletcher, G. P. Linette, J. Stec, E. Clark, M. Ayers, et al., The Her-2/neu gene and protein in breast cancer 2003: biomarker and target of therapy, Oncologist, 8 (2003), 307–325. https://doi.org/10.1634/theoncologist.8-4-307 doi: 10.1634/theoncologist.8-4-307
    [9] A. Tremel, A. Cai, N. Tirtaatmadja, B. D. Hughes, G. W. Stevens, K. A. Landman, et al., Cell migration and proliferation during monolayer formation and wound healing, Chem. Eng. Sci., 64 (2009), 247–253. https://doi.org/10.1016/j.ces.2008.10.008 doi: 10.1016/j.ces.2008.10.008
    [10] S. E. Wang, P. Hinow, N. Bryce, A. M. Weaver, L. Estrada, C. L. Arteaga, et al., A mathematical model quantifies proliferation and motility effects of TGF–$\beta$ on cancer cells, Comput. Math. Methods Med., 10 (2009), 71–83. https://doi.org/10.1080/17486700802171993 doi: 10.1080/17486700802171993
    [11] J. Dyson, S. Gourley, R. Villella-Bressan, G. Webb, Existence and asymptotic properties of solutions of a nonlocal evolution equation modelling cell-cell adhesion, SIAM J. Math. Anal., 42 (2010), 1784–1804. https://doi.org/10.1137/090765663 doi: 10.1137/090765663
    [12] J. C. Arciero, Q. Mi, M. F. Branco, D. J. Hackam, D. Swigon, Continuum model of collective cell migration in wound healing and colony expansion, Biophys. J., 100 (2011), 535–543. https://doi.org/10.1016/j.bpj.2010.11.083 doi: 10.1016/j.bpj.2010.11.083
    [13] N. J. Armstrong, K. J. Painter, J. A. Sherratt, A continuum approach to modelling cell-cell adhesion, J. Theor. Biol., 243 (2006), 98–113. https://doi.org/10.1016/j.jtbi.2006.05.030 doi: 10.1016/j.jtbi.2006.05.030
    [14] N. J. Armstrong, K. J. Painter, J. A. Sherratt, Adding adhesion to a chemical signalling model for somite formation, Bull. Math. Biol., 71 (2009), 1–24. https://doi.org/10.1007/s11538-008-9350-1 doi: 10.1007/s11538-008-9350-1
    [15] V. Bitsouni, M. A. J. Chaplain, R. Eftimie, Mathematical modelling of cancer invasion: the multiple roles of TGF-$\beta$ pathway on tumour proliferation and cell adhesion, Math. Mod. Meth. Appl. Sci., 27 (2017), 1929–1962. https://doi.org/10.1142/S021820251750035X doi: 10.1142/S021820251750035X
    [16] H. Byrne, M. A. J. Chaplain, Modelling the role of cell-cell adhesion in the growth and development of carcinomas, Math. Comput. Model., 24 (1996), 1–17. https://doi.org/10.1016/S0895-7177(96)00174-4 doi: 10.1016/S0895-7177(96)00174-4
    [17] H. Byrne, D. Draso, Individual based and continuum models of growing cell populations: A comparison, J. Math. Biol., 58 (2009), 657–687. https://doi.org/10.1007/s00285-008-0212-0 doi: 10.1007/s00285-008-0212-0
    [18] X. Chen, A. Friedman, A free boundary problem arising in a model of wound healing, SIAM J. Math. Anal., 32 (2000), 778–800. https://doi.org/10.1137/S0036141099351693 doi: 10.1137/S0036141099351693
    [19] V. Christini, J. Lowengrub, Multi-Scale Modeling of Cancer, Cambridge University Press, 2010. https://doi.org/10.1017/CBO9780511781452
    [20] P. D. Dale, P. K. Maini, J. A. Sherratt, Mathematical modeling of corneal epithelial wound healing, Math. Biosci., 124 (1994), 127–147. https://doi.org/10.1016/0025-5564(94)90040-X doi: 10.1016/0025-5564(94)90040-X
    [21] P. D. Dale, J. A. Sherratt, P. K. Maini, A mathematical model for collagen fibre formation during foetal and adult dermal wound healing, Proc. Royal Soc. B, 263 (1996), 653–660. https://doi.org/10.1098/rspb.1996.0098 doi: 10.1098/rspb.1996.0098
    [22] J. C. Dallon, J. A. Sherratt, P.K. Maini, Modeling the effects of transforming growth factor–$\beta$ on extracellular matrix alignment in dermal wound repair, Wound Repair Regen., 9 (2001), 278–286. https://doi.org/10.1046/j.1524-475X.2001.00278.x doi: 10.1046/j.1524-475X.2001.00278.x
    [23] A. Ducrot, P. Magal, S. Ruan, Travelling wave solutions in multigroup age–structured epidemic models, Arch. Ration Mech. Anal., 195 (2010), 311–331. https://doi.org/10.1007/s00205-008-0203-8 doi: 10.1007/s00205-008-0203-8
    [24] R. Durrett, Cancer modeling: A personal perspective, Not. Am. Math. Soc., 60 (2013), 304–309. https://doi.org/10.1090/noti953 doi: 10.1090/noti953
    [25] J. Dyson, S. Gourley, G. Webb, A nonlocal evolution equation model of cell-cell adhesion in higher dimensional space, J. Biol. Dyn., 7 (2013), 68–87. https://doi.org/10.1080/17513758.2012.755572 doi: 10.1080/17513758.2012.755572
    [26] J. Dyson, E. Sánchez, R. Villella-Bressan, G. Webb, An age and spatially structured model of tumor invasion with haptotaxis, Discrete Contin. Dyn. Syst. Ser. –B, 8 (2007), 45–60. https://doi.org/10.3934/dcdsb.2007.8.45 doi: 10.3934/dcdsb.2007.8.45
    [27] J. Dyson, R. Villella-Bressan, G. Webb, A spatially structured model of tumor growth with cell age, cell size and mutation of cell phenotypes, Math. Model. Nat. Phenom., 2 (2007), 69–100. https://doi.org/10.1051/mmnp:2007004 doi: 10.1051/mmnp:2007004
    [28] J. Dyson, R. Villella-Bressan, G. Webb, An age and spatially structured model of tumor invasion with haptotaxis Ⅱ, Math Popul. Stud., 15 (2008), 73–95. https://doi.org/10.1080/08898480802010159 doi: 10.1080/08898480802010159
    [29] J. Dyson, R. Villella-Bressan, G. Webb, Global existence and boundedness of solutions to a model of chemotaxis, Math. Model. Nat. Phenom., 3 (2008), 17–35. https://doi.org/10.1051/mmnp:2008039 doi: 10.1051/mmnp:2008039
    [30] J. Dyson, G. Webb, A cell population model structured by cell age incorporating cell–cell adhesion, Mathematical Oncology, Birkhauser, New York, NY, 2014,109–149. https://doi.org/10.1007/978-1-4939-0458-7_4
    [31] A. Friedman, Tutorials in Mathematical Biosciences, Ⅱ: Cell Cycle, Proliferation, and Cancer, Springer Lecture Notes in Mathematics, 1872, (2005). https://doi.org/10.1007/978-3-319-08314-8
    [32] A. Friedman, Mathematical analysis and challenges arising from models of tumor growth, Math. Mod. Meth. Appl. Sci., 17 (2007), 1751–1772. https://doi.org/10.1142/S0218202507002467 doi: 10.1142/S0218202507002467
    [33] A. Friedman, B. Hu, C. Xue, Analysis of a mathematical model of ischemic cutaneous wounds, SIAM J. Math. Anal., 42 (2010), 2013–2040. https://doi.org/10.1137/090772630 doi: 10.1137/090772630
    [34] X. Fu, Q. Griette, P. Magal, Existence and uniqueness of solutions for a hyperbolic Keller-Segel equation, Discrete Contin. Dyn. Syst. Ser. B, 26 (2021), 1931–1966. https://doi.org/10.3934/dcdsb.2020326 doi: 10.3934/dcdsb.2020326
    [35] E. A. Gaffney, P. K. Maini, J. A. Sherratt, P. D. Dale, Wound healing in the corneal epithelium: biological mechanisms and mathematical models, J. Theor. Med., 1 (1997), 13–23. https://doi.org/10.1080/10273669708833003 doi: 10.1080/10273669708833003
    [36] E.A. Gaffney, P. K. Maini, J.A. Sherratt, S. Tutt, The mathematical modelling of cell kinetics in corneal epithelial wound healing, J. Theor. Biol., 197 (1999), 111–141. https://doi.org/10.1006/jtbi.1998.0852 doi: 10.1006/jtbi.1998.0852
    [37] A. Gandolfi, M. Iannelli, G. Marnoschi, An age-structured model of epidermis growth, J. Math. Biol., 62 (2011), 111–141. https://doi.org/10.1007/s00285-010-0330-3 doi: 10.1007/s00285-010-0330-3
    [38] A. Gandolfi, M. Iannelli, G. Marinoschi, Time evolution for a model of epidermis growth, J. Evol. Equ., 13 (2013), 509–533. https://doi.org/10.1007/s00028-013-0188-0 doi: 10.1007/s00028-013-0188-0
    [39] A. Gerisch, M. A. J. Chaplain, Mathematical modelling of cancer cell invasion of tissue: local and nonlocal models and the effect of adhesion, J. Theor. Biol., 250 (2008), 684–704. https://doi.org/10.1016/j.jtbi.2007.10.026 doi: 10.1016/j.jtbi.2007.10.026
    [40] D. Guidetti, On elliptic systems in $L^1$, Osaka J. Math., 30 (1993), 397–429.
    [41] J. S. Lowengrub, H. B. Frieboes, F. Jin, Y-L. Chuang, X. Li, P. Macklin, et al., Nonlinear models of cancer: Bridging the gap between cells and tumours, Nonlinearity, 23 (2010), R1–R91. https://doi.org/10.1088/0951-7715/23/1/R01 doi: 10.1088/0951-7715/23/1/R01
    [42] S. McDougall, J. Dallon, J.A. Sherratt, P. Maini, Fibroblast migration and collagen deposition during dermal wound healing: mathematical modelling and clinical implications, Philos. Trans. Royal Soc. A, 364 (2006), 1385–1405. https://doi.org/10.1098/rsta.2006.1773 doi: 10.1098/rsta.2006.1773
    [43] P. J. Murray, J. W. Kang, G. R. Mirams, S. Y. Shin, H. M. Byrne, P. K. Maini, et al., Modelling spatially regulated ${\beta}$-catenin dynamics and invasion in intestinal crypts, Biophys. J., 99 (2010), 716–725. https://doi.org/10.1016/j.bpj.2010.05.016 doi: 10.1016/j.bpj.2010.05.016
    [44] P. J. Murray, A. Walter, A. G. Fletcher, C. M. Edwards, M. J. Tindall, P. K. Maini, Comparing a discrete and continuum model of the intestinal crypt, Phys. Biol., 8 (2010), 026011. https://doi.org/10.1088/1478-3975/8/2/026011 doi: 10.1088/1478-3975/8/2/026011
    [45] L. Olsen, J. A. Sherratt, P. K. Maini, A mechanochemical model for adult dermal wound contraction and the permanence of the contracted tissue displacement profile, J. Theor. Biol., 14 (1997), 261–281. https://doi.org/10.1093/imammb/14.4.261 doi: 10.1093/imammb/14.4.261
    [46] L. Olsen, J. A. Sherratt, P. K. Maini, F. Arnold, A mathematical model for the capillary endothelial cell-extracellular matrix interactions in wound-healing angiogenesis, Math. Med. Biol., 14 (1997), 261–281. https://doi.org/10.1093/imammb/14.4.261 doi: 10.1093/imammb/14.4.261
    [47] M. Owen, J. A. Sherratt, Pattern formation and spatiotemporal irregularity in a model for macrophage-tumour interactions, J. Theor. Biol., 189 (1997), 63–80. https://doi.org/10.1006/jtbi.1997.0494 doi: 10.1006/jtbi.1997.0494
    [48] K. J. Painter, N. J. Armstrong, J. A. Sherratt, The impact of adhesion on cellular invasion processes in cancer and development, J. Theor. Biol., 264 (2010), 1057–1067. https://doi.org/10.1016/j.jtbi.2010.03.033 doi: 10.1016/j.jtbi.2010.03.033
    [49] K. J. Painter, J. A. Sherratt, Modelling the movement of interacting cell populations, J. Theor. Biol., 225 (2003), 327–339. https://doi.org/10.1016/S0022-5193(03)00258-3 doi: 10.1016/S0022-5193(03)00258-3
    [50] J. Pasquier, P. Magal, C. Boulange-Lecomte, G. Webb, F. Le Foll, Consequences of cell-to-cell P–glycoprotein transfer on acquired multidrug resistance in breast cancer: a cell population dynamics model, Biol. Direct, 6 (2011), 1–18. https://doi.org/10.1186/1745-6150-6-5 doi: 10.1186/1745-6150-6-5
    [51] G. J. Pettet, M. A. J. Chaplain, D. S. L. McElwain, H. M. Byrne, On the role of angiogenesis in wound healing, Proc. Roy. Soc. Lond. B, 263 (1996), 1487–1493. https://doi.org/10.1098/rspb.1996.0217 doi: 10.1098/rspb.1996.0217
    [52] G. J. Pettet, M. A. J. Chaplain, D. S. L. McElwain, J. Norbury, A model of wound healing-angiogenesis in soft tissue, Math. Biosci., 136 (1996), 35–63. https://doi.org/10.1016/0025-5564(96)00044-2 doi: 10.1016/0025-5564(96)00044-2
    [53] J. A. Sherratt, M. A. J. Chaplain, A new mathematical model for avascular tumour growth, J. Math. Biol., 43 (2001), 291–312. https://doi.org/10.1007/s002850100088 doi: 10.1007/s002850100088
    [54] J. A. Sherratt, J. C. Dallon, Theoretical models of wound healing: past successes and future challenges, C. R. Biol., 325 (2002), 557–564. https://doi.org/10.1016/S1631-0691(02)01464-6 doi: 10.1016/S1631-0691(02)01464-6
    [55] J. A. Sherratt J. D. Murray, Mathematical analysis of a basic model for epidermal wound healing, J. Math. Biol., 29 (1991), 389–404. https://doi.org/10.1007/BF00160468 doi: 10.1007/BF00160468
    [56] J. A. Sherratt, S. A. Gourley, N. J. Armstrong, K. J. Painter, Boundedness of solutions of a nonlocal reaction-diffusion model for adhesion in cell aggregation and cancer invasion, Eur. J. Appl. Math., 20 (2009), 123–144. https://doi.org/10.1017/S0956792508007742 doi: 10.1017/S0956792508007742
    [57] J. A. Sherratt, J. D. Murray, Models of epidermal wound healing, J. Math. Biol., 31 (1993), 703–716. https://doi.org/10.1007/BF00160420 doi: 10.1007/BF00160420
    [58] C.M. Topaz, A. L. Bertozzi, M. A. Lewis, A nonlocal continuum model for biological aggregation, Bull. Math Biol., 68 (2006), 1601–1623. https://doi.org/10.1007/s11538-006-9088-6 doi: 10.1007/s11538-006-9088-6
    [59] S. Turner, J. A. Sherratt, Intercellular adhesion and cancer invasion: a discrete simulation using the extended Potts model, J. Theor. Biol., 216 (2002), 85–100. https://doi.org/10.1006/jtbi.2001.2522 doi: 10.1006/jtbi.2001.2522
    [60] S. Turner, J. A. Sherratt, D. Cameron, Tamoxifen treatment failure in cancer and the nonlinear dynamics of TGF$\beta$, J. Theor. Biol., 229(2004), 101–111. https://doi.org/10.1016/j.jtbi.2004.03.008 doi: 10.1016/j.jtbi.2004.03.008
    [61] Ch. Walker, Global well–posedness of a haptotaxis model with spatial and age structure, Differ. Integral Equ., 20 (2007), 1053–1074.
    [62] Ch. Walker, A Haptotaxis model with age and spatial structure and nonlinear age-boundary conditions, Proc. Appl. Math., 7 (2007), 1040601–1040602. https://doi.org/10.1002/pamm.200700008 doi: 10.1002/pamm.200700008
    [63] Ch. Walker, Global existence for an age and spatially structured haptotaxis model with nonlinear age-boundary conditions, Eur. J. Appl. Math., 19 (2008), 113–147. https://doi.org/10.1017/S095679250800733X doi: 10.1017/S095679250800733X
    [64] H.J. Wearing, J. A. Sherratt, Keratinocyte growth factor signalling: a mathematical model of dermal–epidermal interaction in epidermal wound healing, Math. Biosci., 165 (2000), 41–62. https://doi.org/10.1016/S0025-5564(00)00008-0 doi: 10.1016/S0025-5564(00)00008-0
    [65] C. Xue, A. Friedman, C. K. Sen, A mathematical model of ischemic cutaneous wounds, Proc. Nat. Acad. Sci. USA, 106 (2009), 16782–16787. https://doi.org/10.1073/pnas.0909115106 doi: 10.1073/pnas.0909115106
  • Reader Comments
  • © 2022 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(1634) PDF downloads(111) Cited by(1)

Article outline

Figures and Tables

Figures(15)  /  Tables(1)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog