1932

Abstract

Collective cell migration is a key driver of embryonic development, wound healing, and some types of cancer invasion. Here, we provide a physical perspective of the mechanisms underlying collective cell migration. We begin with a catalog of the cell–cell and cell–substrate interactions that govern cell migration, which we classify into positional and orientational interactions. We then review the physical models that have been developed to explain how these interactions give rise to collective cellular movement. These models span the subcellular to the supracellular scales, and they include lattice models, phase-field models, active network models, particle models, and continuum models. For each type of model, we discuss its formulation, its limitations, and the main emergent phenomena that it has successfully explained. These phenomena include flocking and fluid–solid transitions, as well as wetting, fingering, and mechanical waves in spreading epithelial monolayers. We close by outlining remaining challenges and future directions in the physics of collective cell migration.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-conmatphys-031218-013516
2020-03-10
2024-12-05
Loading full text...

Full text loading...

/deliver/fulltext/conmatphys/11/1/annurev-conmatphys-031218-013516.html?itemId=/content/journals/10.1146/annurev-conmatphys-031218-013516&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Born G. 1897. Arch. für Entwickelungsmechanik Org. 4:517–623
    [Google Scholar]
  2. 2. 
    Holmes SJ. 1914. J. Exp. Zool. 17:281–95
    [Google Scholar]
  3. 3. 
    Herrick EH. 1932. Biol. Bull. 63:271–86
    [Google Scholar]
  4. 4. 
    Vaughan RB, Trinkaus JP. 1966. J. Cell Sci. 1:407–13
    [Google Scholar]
  5. 5. 
    Roca-Cusachs P, Conte V, Trepat X 2017. Nat. Cell Biol. 19:742–51
    [Google Scholar]
  6. 6. 
    Marchetti MC, Joanny JF, Ramaswamy S, Liverpool TB, Prost J et al. 2013. Rev. Mod. Phys. 85:1143–89
    [Google Scholar]
  7. 7. 
    Prost J, Jülicher F, Joanny JF 2015. Nat. Phys. 11:111–17
    [Google Scholar]
  8. 8. 
    Jülicher F, Grill SW, Salbreux G 2018. Rep. Prog. Phys. 81:076601
    [Google Scholar]
  9. 9. 
    Good M, Trepat X. 2018. Nature 563:188–89
    [Google Scholar]
  10. 10. 
    Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P et al. 2007. PNAS 104:15988–93
    [Google Scholar]
  11. 11. 
    Serra-Picamal X, Conte V, Vincent R, Añón E, Tambe DT et al. 2012. Nat. Phys. 8:628–34
    [Google Scholar]
  12. 12. 
    du Roure O, Saez A, Buguin A, Austin RH, Chavrier P et al. 2005. PNAS 102:2390–95
    [Google Scholar]
  13. 13. 
    Trepat X, Wasserman MR, Angelini TE, Millet E, Weitz DA et al. 2009. Nat. Phys. 5:426–30
    [Google Scholar]
  14. 14. 
    Friedl P, Noble PB, Walton PA, Laird DW, Chauvin PJ et al. 1995. Cancer Res 55:4557–60
    [Google Scholar]
  15. 15. 
    Brugués A, Anon E, Conte V, Veldhuis JH, Gupta M et al. 2014. Nat. Phys. 10:683–90
    [Google Scholar]
  16. 16. 
    Friedl P, Gilmour D. 2009. Nat. Rev. Mol. Cell Biol. 10:445–57
    [Google Scholar]
  17. 17. 
    Cai D, Chen SC, Prasad M, He L, Wang X et al. 2014. Cell 157:1146–59
    [Google Scholar]
  18. 18. 
    Clark AG, Vignjevic DM. 2015. Curr. Opin. Cell Biol. 36:13–22
    [Google Scholar]
  19. 19. 
    Campàs O. 2016. Semin. Cell Dev. Biol. 55:119–30
    [Google Scholar]
  20. 20. 
    Hakim V, Silberzan P. 2017. Rep. Prog. Phys. 80:076601
    [Google Scholar]
  21. 21. 
    Ladoux B, Mège RM. 2017. Nat. Rev. Mol. Cell Biol. 18:743–57
    [Google Scholar]
  22. 22. 
    Xi W, Saw TB, Delacour D, Lim CT, Ladoux B 2019. Nat. Rev. Mater. 4:23–44
    [Google Scholar]
  23. 23. 
    Schwarz US, Safran SA. 2013. Rev. Mod. Phys. 85:1327–81
    [Google Scholar]
  24. 24. 
    Elosegui-Artola A, Trepat X, Roca-Cusachs P 2018. Trends Cell Biol 28:356–67
    [Google Scholar]
  25. 25. 
    Khalilgharibi N, Fouchard J, Recho P, Charras G, Kabla A 2016. Curr. Opin. Cell Biol. 42:113–20
    [Google Scholar]
  26. 26. 
    Bi D, Lopez JH, Schwarz JM, Manning ML 2015. Nat. Phys. 11:1074–79
    [Google Scholar]
  27. 27. 
    Park JA, Kim JH, Bi D, Mitchel JA, Qazvini NT et al. 2015. Nat. Mater. 14:1040–8
    [Google Scholar]
  28. 28. 
    Blanch-Mercader C, Vincent R, Bazellières E, Serra-Picamal X, Trepat X, Casademunt J 2017. Soft Matter 13:1235–43
    [Google Scholar]
  29. 29. 
    Iyer KV, Piscitello-Gómez R, Paijmans J, Jülicher F, Eaton S 2019. Curr. Biol. 29:578–91.e5
    [Google Scholar]
  30. 30. 
    Czirók A, Varga K, Méhes E, Szabó A 2013. New J. Phys. 15:075006
    [Google Scholar]
  31. 31. 
    Peglion F, Llense F, Etienne-Manneville S 2014. Nat. Cell Biol. 16:639–51
    [Google Scholar]
  32. 32. 
    Garcia S, Hannezo E, Elgeti J, Joanny JF, Silberzan P, Gov NS 2015. PNAS 112:15314–19
    [Google Scholar]
  33. 33. 
    Zehnder SM, Suaris M, Bellaire MM, Angelini TE 2015. Biophys. J. 108:247–50
    [Google Scholar]
  34. 34. 
    Zehnder SM, Wiatt MK, Uruena JM, Dunn AC, Sawyer WG, Angelini TE 2015. Phys. Rev. E 92:032729
    [Google Scholar]
  35. 35. 
    Kocgozlu L, Saw TB, Le AP, Yow I, Shagirov M et al. 2016. Curr. Biol. 26:2942–50
    [Google Scholar]
  36. 36. 
    Saw TB, Doostmohammadi A, Nier V, Kocgozlu L, Thampi S et al. 2017. Nature 544:212–16
    [Google Scholar]
  37. 37. 
    Chen T, Saw TB, Mège RM, Ladoux B 2018. J. Cell Sci. 131:jcs218156
    [Google Scholar]
  38. 38. 
    Beaune G, Stirbat TV, Khalifat N, Cochet-Escartin O, Garcia S et al. 2014. PNAS 111:8055–60
    [Google Scholar]
  39. 39. 
    Maruthamuthu V, Sabass B, Schwarz US, Gardel ML 2011. PNAS 108:4708–13
    [Google Scholar]
  40. 40. 
    Stramer B, Mayor R. 2017. Nat. Rev. Mol. Cell Biol. 18:43–55
    [Google Scholar]
  41. 41. 
    Mayor R, Etienne-Manneville S. 2016. Nat. Rev. Mol. Cell Biol. 17:97–109
    [Google Scholar]
  42. 42. 
    Li D, Wang YL. 2018. PNAS 115:10678–83
    [Google Scholar]
  43. 43. 
    Fujimori T, Nakajima A, Shimada N, Sawai S 2019. PNAS 116:4291–96
    [Google Scholar]
  44. 44. 
    d'Alessandro J, Solon AP, Hayakawa Y, Anjard C, Detcheverry F et al. 2017. Nat. Phys. 13:999–1005
    [Google Scholar]
  45. 45. 
    Desai RA, Gopal SB, Chen S, Chen CS 2013. J. R. Soc. Interface 10:20130717
    [Google Scholar]
  46. 46. 
    George M, Bullo F, Campàs O 2017. Sci. Rep. 7:9720
    [Google Scholar]
  47. 47. 
    Desai RA, Gao L, Raghavan S, Liu WF, Chen CS 2009. J. Cell Sci. 122:905–11
    [Google Scholar]
  48. 48. 
    Weber GF, Bjerke MA, DeSimone DW 2012. Dev. Cell 22:104–15
    [Google Scholar]
  49. 49. 
    Ng MR, Besser A, Danuser G, Brugge JS 2012. J. Cell Biol. 199:545–63
    [Google Scholar]
  50. 50. 
    Roca-Cusachs P, Sunyer R, Trepat X 2013. Curr. Opin. Cell Biol. 25:543–49
    [Google Scholar]
  51. 51. 
    Das T, Safferling K, Rausch S, Grabe N, Boehm H, Spatz JP 2015. Nat. Cell Biol. 17:276–87
    [Google Scholar]
  52. 52. 
    Ladoux B, Mège RM, Trepat X 2016. Trends Cell Biol 26:420–33
    [Google Scholar]
  53. 53. 
    Vishwakarma M, Di Russo J, Probst D, Schwarz US, Das T, Spatz JP 2018. Nat. Commun. 9:3469
    [Google Scholar]
  54. 54. 
    Davis JR, Luchici A, Mosis F, Thackery J, Salazar JA et al. 2015. Cell 161:361–73
    [Google Scholar]
  55. 55. 
    Scarpa E, Szabó A, Bibonne A, Theveneau E, Parsons M, Mayor R 2015. Dev. Cell 34:421–34
    [Google Scholar]
  56. 56. 
    Roycroft A, Mayor R. 2016. Cell. Mol. Life Sci. 73:1119–30
    [Google Scholar]
  57. 57. 
    Roycroft A, Szabó A, Bahm I, Daly L, Charras G et al. 2018. Dev. Cell 45:565–79.e3
    [Google Scholar]
  58. 58. 
    Aigouy B, Farhadifar R, Staple DB, Sagner A, Röper JC et al. 2010. Cell 142:773–86
    [Google Scholar]
  59. 59. 
    Marel AK, Podewitz N, Zorn M, Rädler JO, Elgeti J 2014. New J. Phys. 16:115005
    [Google Scholar]
  60. 60. 
    Tambe DT, Corey Hardin C, Angelini TE, Rajendran K, Park CY et al. 2011. Nat. Mater. 10:469–75
    [Google Scholar]
  61. 61. 
    Trepat X, Fredberg JJ. 2011. Trends Cell Biol 21:638–46
    [Google Scholar]
  62. 62. 
    He S, Liu C, Li X, Ma S, Huo B, Ji B 2015. Biophys. J. 109:489–500
    [Google Scholar]
  63. 63. 
    Zaritsky A, Welf ES, Tseng YY, Angeles Rabadán M, Serra-Picamal X et al. 2015. Biophys. J. 109:2492–500
    [Google Scholar]
  64. 64. 
    Blanch-Mercader C, Casademunt J. 2017. Soft Matter 13:6913–28
    [Google Scholar]
  65. 65. 
    Duclos G, Blanch-Mercader C, Yashunsky V, Salbreux G, Joanny JF et al. 2018. Nat. Phys. 14:728–32
    [Google Scholar]
  66. 66. 
    Coburn L, Cerone L, Torney C, Couzin ID, Neufeld Z 2013. Phys. Biol. 10:046002
    [Google Scholar]
  67. 67. 
    Löber J, Ziebert F, Aranson IS 2015. Sci. Rep. 5:9172
    [Google Scholar]
  68. 68. 
    Barton DL, Henkes S, Weijer CJ, Sknepnek R 2017. PLOS Comput. Biol. 13:e1005569
    [Google Scholar]
  69. 69. 
    Peyret G, Mueller R, d'Alessandro J, Begnaud S, Marcq P et al. 2019. Biophys. J. 117:3464–78
    [Google Scholar]
  70. 70. 
    Brotto T, Caussin JB, Lauga E, Bartolo D 2013. Phys. Rev. Lett. 110:038101
    [Google Scholar]
  71. 71. 
    Kumar N, Soni H, Ramaswamy S, Sood AK 2014. Nat. Commun. 5:4688
    [Google Scholar]
  72. 72. 
    Oriola D, Alert R, Casademunt J 2017. Phys. Rev. Lett. 118:088002
    [Google Scholar]
  73. 73. 
    Maitra A, Srivastava P, Marchetti MC, Ramaswamy S, Lenz M 2020. Phys. Rev. Lett. 24028002
    [Google Scholar]
  74. 74. 
    Kim JH, Serra-Picamal X, Tambe DT, Zhou EH, Park CY et al. 2013. Nat. Mater. 12:856–63
    [Google Scholar]
  75. 75. 
    Notbohm J, Banerjee S, Utuje KJ, Gweon B, Jang H et al. 2016. Biophys. J. 110:2729–38
    [Google Scholar]
  76. 76. 
    Zimmermann J, Camley BA, Rappel WJ, Levine H 2016. PNAS 113:2660–65
    [Google Scholar]
  77. 77. 
    Lin SZ, Ye S, Xu GK, Li B, Feng XQ 2018. Biophys. J. 115:1826–35
    [Google Scholar]
  78. 78. 
    Bun P, Liu J, Turlier H, Liu Z, Uriot K et al. 2014. Biophys. J. 107:324–35
    [Google Scholar]
  79. 79. 
    Breckenridge MT, Desai RA, Yang MT, Fu J, Chen CS 2014. Cell. Mol. Bioeng. 7:26–34
    [Google Scholar]
  80. 80. 
    Marzban B, Yi X, Yuan H 2018. Biomech. Model. Mechanobiol. 17:915–22
    [Google Scholar]
  81. 81. 
    Saez A, Ghibaudo M, Buguin A, Silberzan P, Ladoux B 2007. PNAS 104:8281–86
    [Google Scholar]
  82. 82. 
    Gupta M, Sarangi BR, Deschamps J, Nematbakhsh Y, Callan-Jones A et al. 2015. Nat. Commun. 6:7525
    [Google Scholar]
  83. 83. 
    Gupta M, Doss B, Lim CT, Voituriez R, Ladoux B 2016. Cell Adh. Migr. 10:554–67
    [Google Scholar]
  84. 84. 
    Gupta M, Doss BL, Kocgozlu L, Pan M, Mège RM et al. 2019. Phys. Rev. E 99:012412
    [Google Scholar]
  85. 85. 
    Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A et al. 2011. Nat. Cell Biol. 13:1457–65
    [Google Scholar]
  86. 86. 
    Camley B, Rappel WJ. 2017. J. Phys. D Appl. Phys. 50:113002
    [Google Scholar]
  87. 87. 
    Spatarelu CP, Zhang H, Nguyen DT, Han X, Liu R et al. 2019. ACS Biomater. Sci. Eng. 5:83766–87
    [Google Scholar]
  88. 88. 
    Graner F, Glazier JA. 1992. Phys. Rev. Lett. 69:2013–16
    [Google Scholar]
  89. 89. 
    Chiang M, Marenduzzo D. 2016. Europhys. Lett. 116:28009
    [Google Scholar]
  90. 90. 
    Rappel WJ, Nicol A, Sarkissian A, Levine H, Loomis WF 1999. Phys. Rev. Lett. 83:1247–50
    [Google Scholar]
  91. 91. 
    Kabla AJ. 2012. J. R. Soc. Interface 9:3268–78
    [Google Scholar]
  92. 92. 
    Szabó A, Ünnep R, Méhes E, Twal WO, Argraves WS et al. 2010. Phys. Biol. 7:046007
    [Google Scholar]
  93. 93. 
    Ouaknin GY, Bar-Yoseph PZ. 2009. Biophys. J. 97:1811–21
    [Google Scholar]
  94. 94. 
    Coburn L, Lopez H, Schouwenaar IM, Yap AS, Lobaskin V, Gomez GA 2018. Phys. Biol. 15:024001
    [Google Scholar]
  95. 95. 
    Segerer FJ, Thüroff F, Piera Alberola A, Frey E, Rädler JO 2015. Phys. Rev. Lett. 114:228102
    [Google Scholar]
  96. 96. 
    Thueroff F, Goychuk A, Reiter M, Frey E 2019. eLife 8:e46842
    [Google Scholar]
  97. 97. 
    Gonzalez-Cinca R, Folch R, Benitez R, Ramirez-Piscina L, Casademunt J, Hernandez-Machado A 2004. Advances in Condensed Matter and Statistical Mechanics E Korutcheva, R Cuerno 203–36 New York: Nova Sci. Publ.
    [Google Scholar]
  98. 98. 
    Camley BA, Zhang Y, Zhao Y, Li B, Ben-Jacob E et al. 2014. PNAS 111:14770–75
    [Google Scholar]
  99. 99. 
    Palmieri B, Bresler Y, Wirtz D, Grant M 2015. Sci. Rep. 5:11745
    [Google Scholar]
  100. 100. 
    Mueller R, Yeomans JM, Doostmohammadi A 2019. Phys. Rev. Lett. 122:048004
    [Google Scholar]
  101. 101. 
    Najem S, Grant M. 2016. Phys. Rev. E 93:052405
    [Google Scholar]
  102. 102. 
    Weaire D, Hutzler S. 1999. The Physics of Foams Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  103. 103. 
    Alt S, Ganguly P, Salbreux G 2017. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372:20150520
    [Google Scholar]
  104. 104. 
    Sussman DM, Merkel M. 2018. Soft Matter 14:3397–403
    [Google Scholar]
  105. 105. 
    Bi D, Yang X, Marchetti MC, Manning ML 2016. Phys. Rev. X 6:021011
    [Google Scholar]
  106. 106. 
    Giavazzi F, Paoluzzi M, Macchi M, Bi D, Scita G et al. 2018. Soft Matter 14:3471–77
    [Google Scholar]
  107. 107. 
    Trepat X, Sahai E. 2018. Nat. Phys. 14:671–82
    [Google Scholar]
  108. 108. 
    Manning ML, Foty RA, Steinberg MS, Schoetz EM 2010. PNAS 107:12517–22
    [Google Scholar]
  109. 109. 
    Winklbauer R. 2015. J. Cell Sci. 128:3687–93
    [Google Scholar]
  110. 110. 
    Salm M, Pismen LM. 2012. Phys. Biol. 9:026009
    [Google Scholar]
  111. 111. 
    Mathur J, Sarker B, Pathak A 2018. Biophys. J. 115:2474–85
    [Google Scholar]
  112. 112. 
    Schaumann EN, Staddon MF, Gardel ML, Banerjee S 2018. Mol. Biol. Cell 29:2835–47
    [Google Scholar]
  113. 113. 
    Staddon MF, Bi D, Tabatabai AP, Ajeti V, Murrell MP, Banerjee S 2018. PLOS Comput. Biol. 14:e1006502
    [Google Scholar]
  114. 114. 
    Li B, Sun SX. 2014. Biophys. J. 107:1532–41
    [Google Scholar]
  115. 115. 
    Malinverno C, Corallino S, Giavazzi F, Bergert M, Li Q et al. 2017. Nat. Mater. 16:587–96
    [Google Scholar]
  116. 116. 
    Petrolli V, Le Goff M, Tadrous M, Martens K, Allier C et al. 2019. Phys. Rev. Lett. 122:168101
    [Google Scholar]
  117. 117. 
    Coburn L, Lopez H, Caldwell BJ, Moussa E, Yap C et al. 2016. Mol. Biol. Cell 27:3436–48
    [Google Scholar]
  118. 118. 
    Teomy E, Kessler DA, Levine H 2018. Phys. Rev. E 98:042418
    [Google Scholar]
  119. 119. 
    Koride S, Loza AJ, Sun SX 2018. Appl. Phys. Lett. Bioeng. 2:031906
    [Google Scholar]
  120. 120. 
    Yang X, Bi D, Czajkowski M, Merkel M, Manning ML, Marchetti MC 2017. PNAS 114:12663–68
    [Google Scholar]
  121. 121. 
    Basan M, Elgeti J, Hannezo E, Rappel WJ, Levine H 2013. PNAS 110:2452–59
    [Google Scholar]
  122. 122. 
    Schnyder SK, Molina JJ, Tanaka Y, Yamamoto R 2017. Sci. Rep. 7:5163
    [Google Scholar]
  123. 123. 
    Smeets B, Alert R, Pešek J, Pagonabarraga I, Ramon H, Vincent R 2016. PNAS 113:14621–26
    [Google Scholar]
  124. 124. 
    Henkes S, Fily Y, Marchetti MC 2011. Phys. Rev. E 84:040301
    [Google Scholar]
  125. 125. 
    Tarle V, Ravasio A, Hakim V, Gov N 2015. Integr. Biol. 7:1218–27
    [Google Scholar]
  126. 126. 
    Szabó B, Szöllösi G, Gönci B, Jurányi Z, Selmeczi D, Vicsek T 2006. Phys. Rev. E 74:061908
    [Google Scholar]
  127. 127. 
    Sepúlveda N, Petitjean L, Cochet O, Grasland-Mongrain E, Silberzan P, Hakim V 2013. PLOS Comput. Biol. 9:e1002944
    [Google Scholar]
  128. 128. 
    Bindschadler M, McGrath JL. 2007. J. Cell Sci. 120:876–84
    [Google Scholar]
  129. 129. 
    Woods ML, Carmona-Fontaine C, Barnes CP, Couzin ID, Mayor R, Page KM 2014. PLOS ONE 9:e104969
    [Google Scholar]
  130. 130. 
    Copenhagen K, Malet-Engra G, Yu W, Scita G, Gov N, Gopinathan A 2018. Sci. Adv. 4:eaar8483
    [Google Scholar]
  131. 131. 
    Camley BA, Zimmermann J, Levine H, Rappel WJ 2016. Phys. Rev. Lett. 116:098101
    [Google Scholar]
  132. 132. 
    Theveneau E, Mayor R. 2013. Cell. Mol. Life Sci. 70:3481–92
    [Google Scholar]
  133. 133. 
    Banerjee S, Marchetti MC. 2019. Cell Migrations: Causes and Functions ed. C La Porta, S Zapperi 45–66 Cham: Switz.: Springer
    [Google Scholar]
  134. 134. 
    Kung W, Marchetti MC, Saunders K 2006. Phys. Rev. E 73:031708
    [Google Scholar]
  135. 135. 
    Voituriez R, Joanny J, Prost J 2006. Phys. Rev. Lett. 96:028102
    [Google Scholar]
  136. 136. 
    Cates ME, Tjhung E. 2018. J. Fluid Mech. 836:P1
    [Google Scholar]
  137. 137. 
    Marcq P. 2014. Eur. Phys. J. E 37:29
    [Google Scholar]
  138. 138. 
    de Gennes PG, Prost J 1993. The Physics of Liquid Crystals Oxford, UK: Oxford Univ. Press. , 2nd ed..
    [Google Scholar]
  139. 139. 
    Recho P, Ranft J, Marcq P 2016. Soft Matter 12:2381–91
    [Google Scholar]
  140. 140. 
    Gonzalez-Rodriguez D, Guevorkian K, Douezan S, Brochard-Wyart F 2012. Science 338:910–17
    [Google Scholar]
  141. 141. 
    Wyatt T, Baum B, Charras G 2016. Curr. Opin. Cell Biol. 38:68–73
    [Google Scholar]
  142. 142. 
    Ranft J, Basan M, Elgeti J, Joanny JF, Prost J, Jülicher F 2010. PNAS 107:20863–68
    [Google Scholar]
  143. 143. 
    Matoz-Fernandez DA, Agoritsas E, Barrat JL, Bertin E, Martens K 2017. Phys. Rev. Lett. 118:158105
    [Google Scholar]
  144. 144. 
    Marmottant P, Mgharbel A, Käfer J, Audren B, Rieu JP et al. 2009. PNAS 106:17271–75
    [Google Scholar]
  145. 145. 
    Etournay R, Popović M, Merkel M, Nandi A, Blasse C et al. 2015. Elife 4:e07090
    [Google Scholar]
  146. 146. 
    Tlili S, Gay C, Ladoux B, Graner F, Delanoë-Ayari H 2018a. In review arXiv1811.05001v1
  147. 147. 
    Krajnc M, Dasgupta S, Ziherl P, Prost J 2018. Phys. Rev. E 98:022409
    [Google Scholar]
  148. 148. 
    Douezan S, Guevorkian K, Naouar R, Dufour S, Cuvelier D, Brochard-Wyart F 2011. PNAS 108:7315–20
    [Google Scholar]
  149. 149. 
    Pérez-González C, Alert R, Blanch-Mercader C, Gómez-González M, Kolodziej T et al. 2019. Nat. Phys. 15:79–88
    [Google Scholar]
  150. 150. 
    Alert R, Blanch-Mercader C, Casademunt J 2019. Phys. Rev. Lett. 122:088104
    [Google Scholar]
  151. 151. 
    Banerjee S, Utuje KJC, Marchetti MC 2015. Phys. Rev. Lett. 114:228101
    [Google Scholar]
  152. 152. 
    Yabunaka S, Marcq P. 2017. Soft Matter 13:7046–52
    [Google Scholar]
  153. 153. 
    Ravasio A, Cheddadi I, Chen T, Pereira T, Ong HT et al. 2015. Nat. Commun. 6:7683
    [Google Scholar]
  154. 154. 
    Williamson JJ, Salbreux G. 2018. Phys. Rev. Lett. 121:238102
    [Google Scholar]
  155. 155. 
    Lee P, Wolgemuth CW. 2011. PLOS Comput. Biol. 7:e1002007
    [Google Scholar]
  156. 156. 
    Cochet-Escartin O, Ranft J, Silberzan P, Marcq P 2014. Biophys. J. 106:65–73
    [Google Scholar]
  157. 157. 
    Yabunaka S, Marcq P. 2017. Phys. Rev. E 96:022406
    [Google Scholar]
  158. 158. 
    Douezan S, Brochard-Wyart F. 2012. Eur. Phys. J. E 35:116
    [Google Scholar]
  159. 159. 
    Tlili S, Gauquelin E, Li B, Cardoso O, Ladoux B et al. 2018. R. Soc. Open Sci. 5:172421
    [Google Scholar]
  160. 160. 
    Alert R, Casademunt J. 2019. 35237571–77
  161. 161. 
    Köpf MH, Pismen LM. 2013. Soft Matter 9:3727
    [Google Scholar]
  162. 162. 
    Ben Amar M, Bianca C 2016. Sci. Rep. 6:33849
    [Google Scholar]
  163. 163. 
    Vincent R, Bazellières E, Pérez-González C, Uroz M, Serra-Picamal X, Trepat X 2015. Phys. Rev. Lett. 115:248103
    [Google Scholar]
  164. 164. 
    Köpf MH. 2015. Phys. Rev. E 91:012712
    [Google Scholar]
  165. 165. 
    Zimmermann J, Basan M, Levine H 2014. Eur. Phys. J. Spec. Top. 223:1259–64
    [Google Scholar]
  166. 166. 
    Nesbitt D, Pruessner G, Lee CF 2017. Phys. Rev. E 96:062615
    [Google Scholar]
  167. 167. 
    Bogdan M, Savin T. 2018. R. Soc. Open Sci. 5:181579
    [Google Scholar]
  168. 168. 
    Mertz AF, Banerjee S, Che Y, German GK, Xu Y et al. 2012. Phys. Rev. Lett. 108:198101
    [Google Scholar]
  169. 169. 
    Czajkowski M, Bi D, Manning ML, Marchetti MC 2018. Soft Matter 14:5628–42
    [Google Scholar]
  170. 170. 
    Friedl P, Alexander S. 2011. Cell 147:992–1009
    [Google Scholar]
  171. 171. 
    Bergert M, Erzberger A, Desai RA, Aspalter IM, Oates AC et al. 2015. Nat. Cell Biol. 17:524–29
    [Google Scholar]
  172. 172. 
    Christensen A, West AKV, Wullkopf L, Terra Erler J, Oddershede LB, Mathiesen J 2018. Phys. Biol. 15:066004
    [Google Scholar]
/content/journals/10.1146/annurev-conmatphys-031218-013516
Loading
/content/journals/10.1146/annurev-conmatphys-031218-013516
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error