Full text loading...
Review Article
Free
Physical Models of Collective Cell Migration
- Ricard Alert1,2, and Xavier Trepat3,4,5,6
-
View Affiliations Hide AffiliationsAffiliations: 1Princeton Center for Theoretical Science, Princeton University, Princeton, New Jersey 08544, USA; email: [email protected] 2Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey 08544, USA 3Institute for Bioengineering of Catalonia (IBEC), The Barcelona Institute for Science and Technology (BIST), Barcelona 08028, Spain; email: [email protected] 4Facultat de Medicina, University of Barcelona, Barcelona 08036, Spain 5Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona 08028, Spain 6Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina, Barcelona 08028, Spain
- Vol. 11:77-101 (Volume publication date March 2020) https://doi.org/10.1146/annurev-conmatphys-031218-013516
- First published as a Review in Advance on September 27, 2019
-
Copyright © 2020 by Annual Reviews. All rights reserved
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.
Article metrics loading...
Literature Cited
-
1.Born G. 1897. Arch. für Entwickelungsmechanik Org. 4:517–623
-
2.Holmes SJ. 1914. J. Exp. Zool. 17:281–95
-
3.Herrick EH. 1932. Biol. Bull. 63:271–86
-
4.Vaughan RB, Trinkaus JP. 1966. J. Cell Sci. 1:407–13
-
5.Roca-Cusachs P, Conte V, Trepat X 2017. Nat. Cell Biol. 19:742–51
-
6.Marchetti MC, Joanny JF, Ramaswamy S, Liverpool TB, Prost J et al. 2013. Rev. Mod. Phys. 85:1143–89
-
7.Prost J, Jülicher F, Joanny JF 2015. Nat. Phys. 11:111–17
-
8.Jülicher F, Grill SW, Salbreux G 2018. Rep. Prog. Phys. 81:076601
-
9.Good M, Trepat X. 2018. Nature 563:188–89
-
10.Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P et al. 2007. PNAS 104:15988–93
-
11.Serra-Picamal X, Conte V, Vincent R, Añón E, Tambe DT et al. 2012. Nat. Phys. 8:628–34
-
12.du Roure O, Saez A, Buguin A, Austin RH, Chavrier P et al. 2005. PNAS 102:2390–95
-
13.Trepat X, Wasserman MR, Angelini TE, Millet E, Weitz DA et al. 2009. Nat. Phys. 5:426–30
-
14.Friedl P, Noble PB, Walton PA, Laird DW, Chauvin PJ et al. 1995. Cancer Res 55:4557–60
-
15.Brugués A, Anon E, Conte V, Veldhuis JH, Gupta M et al. 2014. Nat. Phys. 10:683–90
-
16.Friedl P, Gilmour D. 2009. Nat. Rev. Mol. Cell Biol. 10:445–57
-
17.Cai D, Chen SC, Prasad M, He L, Wang X et al. 2014. Cell 157:1146–59
-
18.Clark AG, Vignjevic DM. 2015. Curr. Opin. Cell Biol. 36:13–22
-
19.Campàs O. 2016. Semin. Cell Dev. Biol. 55:119–30
-
20.Hakim V, Silberzan P. 2017. Rep. Prog. Phys. 80:076601
-
21.Ladoux B, Mège RM. 2017. Nat. Rev. Mol. Cell Biol. 18:743–57
-
22.Xi W, Saw TB, Delacour D, Lim CT, Ladoux B 2019. Nat. Rev. Mater. 4:23–44
-
23.Schwarz US, Safran SA. 2013. Rev. Mod. Phys. 85:1327–81
-
24.Elosegui-Artola A, Trepat X, Roca-Cusachs P 2018. Trends Cell Biol 28:356–67
-
25.Khalilgharibi N, Fouchard J, Recho P, Charras G, Kabla A 2016. Curr. Opin. Cell Biol. 42:113–20
-
26.Bi D, Lopez JH, Schwarz JM, Manning ML 2015. Nat. Phys. 11:1074–79
-
27.Park JA, Kim JH, Bi D, Mitchel JA, Qazvini NT et al. 2015. Nat. Mater. 14:1040–8
-
28.Blanch-Mercader C, Vincent R, Bazellières E, Serra-Picamal X, Trepat X, Casademunt J 2017. Soft Matter 13:1235–43
-
29.Iyer KV, Piscitello-Gómez R, Paijmans J, Jülicher F, Eaton S 2019. Curr. Biol. 29:578–91.e5
-
30.Czirók A, Varga K, Méhes E, Szabó A 2013. New J. Phys. 15:075006
-
31.Peglion F, Llense F, Etienne-Manneville S 2014. Nat. Cell Biol. 16:639–51
-
32.Garcia S, Hannezo E, Elgeti J, Joanny JF, Silberzan P, Gov NS 2015. PNAS 112:15314–19
-
33.Zehnder SM, Suaris M, Bellaire MM, Angelini TE 2015. Biophys. J. 108:247–50
-
34.Zehnder SM, Wiatt MK, Uruena JM, Dunn AC, Sawyer WG, Angelini TE 2015. Phys. Rev. E 92:032729
-
35.Kocgozlu L, Saw TB, Le AP, Yow I, Shagirov M et al. 2016. Curr. Biol. 26:2942–50
-
36.Saw TB, Doostmohammadi A, Nier V, Kocgozlu L, Thampi S et al. 2017. Nature 544:212–16
-
37.Chen T, Saw TB, Mège RM, Ladoux B 2018. J. Cell Sci. 131:jcs218156
-
38.Beaune G, Stirbat TV, Khalifat N, Cochet-Escartin O, Garcia S et al. 2014. PNAS 111:8055–60
-
39.Maruthamuthu V, Sabass B, Schwarz US, Gardel ML 2011. PNAS 108:4708–13
-
40.Stramer B, Mayor R. 2017. Nat. Rev. Mol. Cell Biol. 18:43–55
-
41.Mayor R, Etienne-Manneville S. 2016. Nat. Rev. Mol. Cell Biol. 17:97–109
-
42.Li D, Wang YL. 2018. PNAS 115:10678–83
-
43.Fujimori T, Nakajima A, Shimada N, Sawai S 2019. PNAS 116:4291–96
-
44.d'Alessandro J, Solon AP, Hayakawa Y, Anjard C, Detcheverry F et al. 2017. Nat. Phys. 13:999–1005
-
45.Desai RA, Gopal SB, Chen S, Chen CS 2013. J. R. Soc. Interface 10:20130717
-
46.George M, Bullo F, Campàs O 2017. Sci. Rep. 7:9720
-
47.Desai RA, Gao L, Raghavan S, Liu WF, Chen CS 2009. J. Cell Sci. 122:905–11
-
48.Weber GF, Bjerke MA, DeSimone DW 2012. Dev. Cell 22:104–15
-
49.Ng MR, Besser A, Danuser G, Brugge JS 2012. J. Cell Biol. 199:545–63
-
50.Roca-Cusachs P, Sunyer R, Trepat X 2013. Curr. Opin. Cell Biol. 25:543–49
-
51.Das T, Safferling K, Rausch S, Grabe N, Boehm H, Spatz JP 2015. Nat. Cell Biol. 17:276–87
-
52.Ladoux B, Mège RM, Trepat X 2016. Trends Cell Biol 26:420–33
-
53.Vishwakarma M, Di Russo J, Probst D, Schwarz US, Das T, Spatz JP 2018. Nat. Commun. 9:3469
-
54.Davis JR, Luchici A, Mosis F, Thackery J, Salazar JA et al. 2015. Cell 161:361–73
-
55.Scarpa E, Szabó A, Bibonne A, Theveneau E, Parsons M, Mayor R 2015. Dev. Cell 34:421–34
-
56.Roycroft A, Mayor R. 2016. Cell. Mol. Life Sci. 73:1119–30
-
57.Roycroft A, Szabó A, Bahm I, Daly L, Charras G et al. 2018. Dev. Cell 45:565–79.e3
-
58.Aigouy B, Farhadifar R, Staple DB, Sagner A, Röper JC et al. 2010. Cell 142:773–86
-
59.Marel AK, Podewitz N, Zorn M, Rädler JO, Elgeti J 2014. New J. Phys. 16:115005
-
60.Tambe DT, Corey Hardin C, Angelini TE, Rajendran K, Park CY et al. 2011. Nat. Mater. 10:469–75
-
61.Trepat X, Fredberg JJ. 2011. Trends Cell Biol 21:638–46
-
62.He S, Liu C, Li X, Ma S, Huo B, Ji B 2015. Biophys. J. 109:489–500
-
63.Zaritsky A, Welf ES, Tseng YY, Angeles Rabadán M, Serra-Picamal X et al. 2015. Biophys. J. 109:2492–500
-
64.Blanch-Mercader C, Casademunt J. 2017. Soft Matter 13:6913–28
-
65.Duclos G, Blanch-Mercader C, Yashunsky V, Salbreux G, Joanny JF et al. 2018. Nat. Phys. 14:728–32
-
66.Coburn L, Cerone L, Torney C, Couzin ID, Neufeld Z 2013. Phys. Biol. 10:046002
-
67.Löber J, Ziebert F, Aranson IS 2015. Sci. Rep. 5:9172
-
68.Barton DL, Henkes S, Weijer CJ, Sknepnek R 2017. PLOS Comput. Biol. 13:e1005569
-
69.Peyret G, Mueller R, d'Alessandro J, Begnaud S, Marcq P et al. 2019. Biophys. J. 117:3464–78
-
70.Brotto T, Caussin JB, Lauga E, Bartolo D 2013. Phys. Rev. Lett. 110:038101
-
71.Kumar N, Soni H, Ramaswamy S, Sood AK 2014. Nat. Commun. 5:4688
-
72.Oriola D, Alert R, Casademunt J 2017. Phys. Rev. Lett. 118:088002
-
73.Maitra A, Srivastava P, Marchetti MC, Ramaswamy S, Lenz M 2020. Phys. Rev. Lett. 24028002
-
74.Kim JH, Serra-Picamal X, Tambe DT, Zhou EH, Park CY et al. 2013. Nat. Mater. 12:856–63
-
75.Notbohm J, Banerjee S, Utuje KJ, Gweon B, Jang H et al. 2016. Biophys. J. 110:2729–38
-
76.Zimmermann J, Camley BA, Rappel WJ, Levine H 2016. PNAS 113:2660–65
-
77.Lin SZ, Ye S, Xu GK, Li B, Feng XQ 2018. Biophys. J. 115:1826–35
-
78.Bun P, Liu J, Turlier H, Liu Z, Uriot K et al. 2014. Biophys. J. 107:324–35
-
79.Breckenridge MT, Desai RA, Yang MT, Fu J, Chen CS 2014. Cell. Mol. Bioeng. 7:26–34
-
80.Marzban B, Yi X, Yuan H 2018. Biomech. Model. Mechanobiol. 17:915–22
-
81.Saez A, Ghibaudo M, Buguin A, Silberzan P, Ladoux B 2007. PNAS 104:8281–86
-
82.Gupta M, Sarangi BR, Deschamps J, Nematbakhsh Y, Callan-Jones A et al. 2015. Nat. Commun. 6:7525
-
83.Gupta M, Doss B, Lim CT, Voituriez R, Ladoux B 2016. Cell Adh. Migr. 10:554–67
-
84.Gupta M, Doss BL, Kocgozlu L, Pan M, Mège RM et al. 2019. Phys. Rev. E 99:012412
-
85.Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A et al. 2011. Nat. Cell Biol. 13:1457–65
-
86.Camley B, Rappel WJ. 2017. J. Phys. D Appl. Phys. 50:113002
-
87.Spatarelu CP, Zhang H, Nguyen DT, Han X, Liu R et al. 2019. ACS Biomater. Sci. Eng. 5:83766–87
-
88.Graner F, Glazier JA. 1992. Phys. Rev. Lett. 69:2013–16
-
89.Chiang M, Marenduzzo D. 2016. Europhys. Lett. 116:28009
-
90.Rappel WJ, Nicol A, Sarkissian A, Levine H, Loomis WF 1999. Phys. Rev. Lett. 83:1247–50
-
91.Kabla AJ. 2012. J. R. Soc. Interface 9:3268–78
-
92.Szabó A, Ünnep R, Méhes E, Twal WO, Argraves WS et al. 2010. Phys. Biol. 7:046007
-
93.Ouaknin GY, Bar-Yoseph PZ. 2009. Biophys. J. 97:1811–21
-
94.Coburn L, Lopez H, Schouwenaar IM, Yap AS, Lobaskin V, Gomez GA 2018. Phys. Biol. 15:024001
-
95.Segerer FJ, Thüroff F, Piera Alberola A, Frey E, Rädler JO 2015. Phys. Rev. Lett. 114:228102
-
96.Thueroff F, Goychuk A, Reiter M, Frey E 2019. eLife 8:e46842
-
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.
-
98.Camley BA, Zhang Y, Zhao Y, Li B, Ben-Jacob E et al. 2014. PNAS 111:14770–75
-
99.Palmieri B, Bresler Y, Wirtz D, Grant M 2015. Sci. Rep. 5:11745
-
100.Mueller R, Yeomans JM, Doostmohammadi A 2019. Phys. Rev. Lett. 122:048004
-
101.Najem S, Grant M. 2016. Phys. Rev. E 93:052405
-
102.Weaire D, Hutzler S. 1999. The Physics of Foams Oxford, UK: Oxford Univ. Press
-
103.Alt S, Ganguly P, Salbreux G 2017. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372:20150520
-
104.Sussman DM, Merkel M. 2018. Soft Matter 14:3397–403
-
105.Bi D, Yang X, Marchetti MC, Manning ML 2016. Phys. Rev. X 6:021011
-
106.Giavazzi F, Paoluzzi M, Macchi M, Bi D, Scita G et al. 2018. Soft Matter 14:3471–77
-
107.Trepat X, Sahai E. 2018. Nat. Phys. 14:671–82
-
108.Manning ML, Foty RA, Steinberg MS, Schoetz EM 2010. PNAS 107:12517–22
-
109.Winklbauer R. 2015. J. Cell Sci. 128:3687–93
-
110.Salm M, Pismen LM. 2012. Phys. Biol. 9:026009
-
111.Mathur J, Sarker B, Pathak A 2018. Biophys. J. 115:2474–85
-
112.Schaumann EN, Staddon MF, Gardel ML, Banerjee S 2018. Mol. Biol. Cell 29:2835–47
-
113.Staddon MF, Bi D, Tabatabai AP, Ajeti V, Murrell MP, Banerjee S 2018. PLOS Comput. Biol. 14:e1006502
-
114.Li B, Sun SX. 2014. Biophys. J. 107:1532–41
-
115.Malinverno C, Corallino S, Giavazzi F, Bergert M, Li Q et al. 2017. Nat. Mater. 16:587–96
-
116.Petrolli V, Le Goff M, Tadrous M, Martens K, Allier C et al. 2019. Phys. Rev. Lett. 122:168101
-
117.Coburn L, Lopez H, Caldwell BJ, Moussa E, Yap C et al. 2016. Mol. Biol. Cell 27:3436–48
-
118.Teomy E, Kessler DA, Levine H 2018. Phys. Rev. E 98:042418
-
119.Koride S, Loza AJ, Sun SX 2018. Appl. Phys. Lett. Bioeng. 2:031906
-
120.Yang X, Bi D, Czajkowski M, Merkel M, Manning ML, Marchetti MC 2017. PNAS 114:12663–68
-
121.Basan M, Elgeti J, Hannezo E, Rappel WJ, Levine H 2013. PNAS 110:2452–59
-
122.Schnyder SK, Molina JJ, Tanaka Y, Yamamoto R 2017. Sci. Rep. 7:5163
-
123.Smeets B, Alert R, Pešek J, Pagonabarraga I, Ramon H, Vincent R 2016. PNAS 113:14621–26
-
124.Henkes S, Fily Y, Marchetti MC 2011. Phys. Rev. E 84:040301
-
125.Tarle V, Ravasio A, Hakim V, Gov N 2015. Integr. Biol. 7:1218–27
-
126.Szabó B, Szöllösi G, Gönci B, Jurányi Z, Selmeczi D, Vicsek T 2006. Phys. Rev. E 74:061908
-
127.Sepúlveda N, Petitjean L, Cochet O, Grasland-Mongrain E, Silberzan P, Hakim V 2013. PLOS Comput. Biol. 9:e1002944
-
128.Bindschadler M, McGrath JL. 2007. J. Cell Sci. 120:876–84
-
129.Woods ML, Carmona-Fontaine C, Barnes CP, Couzin ID, Mayor R, Page KM 2014. PLOS ONE 9:e104969
-
130.Copenhagen K, Malet-Engra G, Yu W, Scita G, Gov N, Gopinathan A 2018. Sci. Adv. 4:eaar8483
-
131.Camley BA, Zimmermann J, Levine H, Rappel WJ 2016. Phys. Rev. Lett. 116:098101
-
132.Theveneau E, Mayor R. 2013. Cell. Mol. Life Sci. 70:3481–92
-
133.Banerjee S, Marchetti MC. 2019. Cell Migrations: Causes and Functions ed. C La Porta, S Zapperi 45–66 Cham: Switz.: Springer
-
134.Kung W, Marchetti MC, Saunders K 2006. Phys. Rev. E 73:031708
-
135.Voituriez R, Joanny J, Prost J 2006. Phys. Rev. Lett. 96:028102
-
136.Cates ME, Tjhung E. 2018. J. Fluid Mech. 836:P1
-
137.Marcq P. 2014. Eur. Phys. J. E 37:29
-
138.de Gennes PG, Prost J 1993. The Physics of Liquid Crystals Oxford, UK: Oxford Univ. Press. , 2nd ed..
-
139.Recho P, Ranft J, Marcq P 2016. Soft Matter 12:2381–91
-
140.Gonzalez-Rodriguez D, Guevorkian K, Douezan S, Brochard-Wyart F 2012. Science 338:910–17
-
141.Wyatt T, Baum B, Charras G 2016. Curr. Opin. Cell Biol. 38:68–73
-
142.Ranft J, Basan M, Elgeti J, Joanny JF, Prost J, Jülicher F 2010. PNAS 107:20863–68
-
143.Matoz-Fernandez DA, Agoritsas E, Barrat JL, Bertin E, Martens K 2017. Phys. Rev. Lett. 118:158105
-
144.Marmottant P, Mgharbel A, Käfer J, Audren B, Rieu JP et al. 2009. PNAS 106:17271–75
-
145.Etournay R, Popović M, Merkel M, Nandi A, Blasse C et al. 2015. Elife 4:e07090
-
146.Tlili S, Gay C, Ladoux B, Graner F, Delanoë-Ayari H 2018a. In review arXiv1811.05001v1
-
147.Krajnc M, Dasgupta S, Ziherl P, Prost J 2018. Phys. Rev. E 98:022409
-
148.Douezan S, Guevorkian K, Naouar R, Dufour S, Cuvelier D, Brochard-Wyart F 2011. PNAS 108:7315–20
-
149.Pérez-González C, Alert R, Blanch-Mercader C, Gómez-González M, Kolodziej T et al. 2019. Nat. Phys. 15:79–88
-
150.Alert R, Blanch-Mercader C, Casademunt J 2019. Phys. Rev. Lett. 122:088104
-
151.Banerjee S, Utuje KJC, Marchetti MC 2015. Phys. Rev. Lett. 114:228101
-
152.Yabunaka S, Marcq P. 2017. Soft Matter 13:7046–52
-
153.Ravasio A, Cheddadi I, Chen T, Pereira T, Ong HT et al. 2015. Nat. Commun. 6:7683
-
154.Williamson JJ, Salbreux G. 2018. Phys. Rev. Lett. 121:238102
-
155.Lee P, Wolgemuth CW. 2011. PLOS Comput. Biol. 7:e1002007
-
156.Cochet-Escartin O, Ranft J, Silberzan P, Marcq P 2014. Biophys. J. 106:65–73
-
157.Yabunaka S, Marcq P. 2017. Phys. Rev. E 96:022406
-
158.Douezan S, Brochard-Wyart F. 2012. Eur. Phys. J. E 35:116
-
159.Tlili S, Gauquelin E, Li B, Cardoso O, Ladoux B et al. 2018. R. Soc. Open Sci. 5:172421
-
160.Alert R, Casademunt J. 2019. 35237571–77
-
161.Köpf MH, Pismen LM. 2013. Soft Matter 9:3727
-
162.Ben Amar M, Bianca C 2016. Sci. Rep. 6:33849
-
163.Vincent R, Bazellières E, Pérez-González C, Uroz M, Serra-Picamal X, Trepat X 2015. Phys. Rev. Lett. 115:248103
-
164.Köpf MH. 2015. Phys. Rev. E 91:012712
-
165.Zimmermann J, Basan M, Levine H 2014. Eur. Phys. J. Spec. Top. 223:1259–64
-
166.Nesbitt D, Pruessner G, Lee CF 2017. Phys. Rev. E 96:062615
-
167.Bogdan M, Savin T. 2018. R. Soc. Open Sci. 5:181579
-
168.Mertz AF, Banerjee S, Che Y, German GK, Xu Y et al. 2012. Phys. Rev. Lett. 108:198101
-
169.Czajkowski M, Bi D, Manning ML, Marchetti MC 2018. Soft Matter 14:5628–42
-
170.Friedl P, Alexander S. 2011. Cell 147:992–1009
-
171.Bergert M, Erzberger A, Desai RA, Aspalter IM, Oates AC et al. 2015. Nat. Cell Biol. 17:524–29
-
172.Christensen A, West AKV, Wullkopf L, Terra Erler J, Oddershede LB, Mathiesen J 2018. Phys. Biol. 15:066004
Data & Media loading...
- Article Type: Review Article
Most Read This Month
Most Cited Most Cited RSS feed
-
-
Many-Body Localization and Thermalization in Quantum Statistical Mechanics
Vol. 6 (2015), pp. 15–38
-
-
-
-
-
-
-
-
-
Correlated Quantum Phenomena in the Strong Spin-Orbit Regime
Vol. 5 (2014), pp. 57–82
-
-
-
-
-
Interface Physics in Complex Oxide Heterostructures
Vol. 2 (2011), pp. 141–165
-
-
-
-
-
Strong Correlations from Hund’s Coupling
Vol. 4 (2013), pp. 137–178
-
- More Less