Abstract
Cell migration plays an essential role in many pathophysiological processes, including embryonic development, wound healing, immunity, and cancer invasion, and is therefore a widely studied phenomenon in many different fields from basic cell biology to regenerative medicine. During the past decades, a multitude of increasingly complex methods have been developed to study cell migration. Here we compile a series of current state-of-the-art methods and protocols to investigate cell migration in a variety of model systems ranging from cells, organoids, tissue explants, and microfluidic systems to Drosophila, zebrafish, and mice. Together they cover processes as diverse as nuclear deformation, energy consumption, endocytic trafficking, and matrix degradation, as well as tumor vascularization and cancer cell invasion, sprouting angiogenesis, and leukocyte extravasation. Furthermore, methods to study developmental processes such as neural tube closure, germ layer specification, and branching morphogenesis are included, as well as scripts for the automated analysis of several aspects of cell migration. Together, this book constitutes a unique collection of methods of prime importance to those interested in the analysis of cell migration.
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References
Scarpa E, Mayor R (2016) Collective cell migration in development. J Cell Biol 212:143–155. https://doi.org/10.1083/jcb.201508047
Friedl P, Mayor R (2017) Tuning collective cell migration by cell-cell junction regulation. Cold Spring Harb Perspect Biol 9:4
Yamada KM, Sixt M (2019) Mechanisms of 3D cell migration. Nat Rev Mol Cell Biol 20:738–752. https://doi.org/10.1038/s41580
Hamm M, Kirchmaier B, Herzog W (2016) Sema3d controls collective endothelial cell migration by distinct mechanisms via Nrp1 and PlxnD1. J Cell Biol 215:415–430
Vitorino P, Meyer T (2008) Modular control of endothelial sheet migration. Genes Dev 22:3268–3281. https://doi.org/10.1101/gad.1725808
Svitkina T (2018) The actin cytoskeleton and actin-based motility. Cold Spring Harb Perspect Biol 10:a018267
Lawson CD, Burridge K (2014) The on-off relationship of rho and Rac during integrin-mediated adhesion and cell migration. Small GTPases 5:e27958
Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, Pinner S, Sahai E, Marshall C (2008) Rac activation and inactivation control plasticity of tumor cell movement. Cell 135:510–523
Pankov R, Endo Y, Even-Ram S, Araki M, Clark K, Cukierman E, Matsumoto K, Yamada K (2005) A Rac switch regulates random versus directionally persistent cell migration. J Cell Biol 170:793–802
Worthylake RA, Burridge K (2003) RhoA and ROCK promote migration by limiting membrane protrusions. J Biol Chem 278:13578–13584. https://doi.org/10.1074/jbc.M211584200
Ridley A (2015) Rho GTPase signalling in cell migration. Curr Opin Cell Biol 36:103–112
Reversat A, Gaertner F, Merrin J, Stopp J, Tasciyan S, Aguilera J, de Vries I, Hauschild R, Hons M, Piel M, Callan-Jones A, Voituriez R, Sixt M (2020) Cellular locomotion using environmental topography. Nature 582:582–585. https://doi.org/10.1038/s41586-020-2283-z
Zhang J, Goliwas KF, Wang W, Taufalele PV, Bordeleau F, Reinhart-King CA (2019) Energetic regulation of coordinated leader–follower dynamics during collective invasion of breast cancer cells. Proc Natl Acad Sci U S A 116:7867–7872. https://doi.org/10.1073/pnas.1809964116
Trappmann B, Baker BM, Polacheck WJ, Choi CK, Burdick JA, Chen CS (2017) Matrix degradability controls multicellularity of 3D cell migration. Nat Commun 8:1–8. https://doi.org/10.1038/s41467-017-00418-6
Gopal S, Veracini L, Grall D, Butori C, Schaub S, Audebert S, Camoin L, Baudelet E, Adwanska A, Beghelli-De La Forest Divonne S, Violette SM, Weinreb PH, Rekima S, Ilie M, Sudaka A, Hofman P, Van Obberghen-Schilling E (2017) Fibronectin-guided migration of carcinoma collectives. Nat Commun:8. https://doi.org/10.1038/NCOMMS14105
Sanz-Moreno V, Gaggioli C, Yeo M, Albrengues J, Wallberg F, Viros A, Hooper S, Mitter R, Féral CC, Cook M, Larkin J, Marais R, Meneguzzi G, Sahai E, Marshall CJ (2011) ROCK and JAK1 signaling cooperate to control Actomyosin contractility in tumor cells and stroma. Cancer Cell 20:229–245. https://doi.org/10.1016/j.ccr.2011.06.018
Humphries J, Chastney M, Askari J, Humphries M (2019) Signal transduction via integrin adhesion complexes. Curr Opin Cell Biol 56:14–21
Gauthier NC, Roca-Cusachs P (2018) Mechanosensing at integrin-mediated cell–matrix adhesions: from molecular to integrated mechanisms. Curr Opin Cell Biol 50:20–26. https://doi.org/10.1016/j.ceb.2017.12.014
Winograd-Katz SE, Fassler R, Geiger B, Legate KR (2014) The integrin adhesome: from genes and proteins to human disease. Nat Rev Mol Cell Biol 15:273–288
Nolte MA, Margadant C (2020) Activation and suppression of hematopoietic integrins in hemostasis and immunity. Blood 135:7–16. https://doi.org/10.1182/blood.2019003336
Burridge K (2017) Focal adhesions: a personal perspective on a half century of progress. FEBS J 284:3355–3361. https://doi.org/10.1111/febs.14195
Jacquemet G, Hamidi H, Ivaska J (2015) Filopodia in cell adhesion, 3D migration and cancer cell invasion. Curr Opin Cell Biol 36:23–31. https://doi.org/10.1016/j.ceb.2015.06.007
Cambi A, Chavrier P (2021) Tissue remodeling by invadosomes. Fac Rev 10. https://doi.org/10.12703/r/10-39
Spuul P, Daubon T, Pitter B, Alonso F, Fremaux I, Kramer I, Montanez E, Genot E (2016) VEGF-A/notch-induced Podosomes Proteolyse basement membrane collagen-IV during retinal sprouting angiogenesis. Cell Rep 17:484–500. https://doi.org/10.1016/j.celrep.2016.09.016
Liu YJ, Le Berre M, Lautenschlaeger F, Maiuri P, Callan-Jones A, Heuzé M, Takaki T, Voituriez R, Piel M (2015) Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell 160:659–672. https://doi.org/10.1016/j.cell.2015.01.007
McGregor AL, Hsia C-R, Lammerding J (2016) Squish and squeeze-the nucleus as a physical barrier during migration in confined environments. Curr Opin Cell Biol 40:32–40
Denais CM, Gilbert RM, Isermann P, McGregor AL, Te Lindert M, Weigelin B, Davidson PM, Friedl P, Wolf K, Lammerding J (2016) Nuclear envelope rupture and repair during cancer cell migration. Science 352:353–358. https://doi.org/10.1126/science.aad7297
Raab M, Gentili M, De Belly H, Thiam HR, Vargas P, Jimenez AJ, Lautenschlaeger F, Voituriez R, Lennon-Duménil AM, Manel N, Piel M (2016) ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352:359–362. https://doi.org/10.1126/science.aad7611
McCormack J, Welsh NJ, Braga VM (2013) Cycling around cell-cell adhesion with rho GTPase regulators. J Cell Sci 126:379–391
Zegers MM, Friedl P (2014) Rho GTPases in collective cell migration. Small GTPases 5:e28997
van der Bijl I, Nawaz K, Kazlauskaite U, van Stalborch A-M, Tol S, Orgaz AJ, van den Bout I, Reinhard NR, Sonnenberg A, Margadant C (2020) Reciprocal integrin/integrin antagonism through kindlin-2 and rho GTPases regulates cell cohesion and collective migration. Matrix Biol 93:60–78. https://doi.org/10.1016/j.matbio.2020.05.005
White DP, Caswell PT, Norman JC (2007) alphavbeta3 and and alpha5beta1 integrin recycling pathways dictate downstream rho kinase signaling to regulate persistent cell migration. J Cell Biol 177:515–525
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
Ewald AJ, Brenot A, Duong M, Chan BS, Werb Z (2008) Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell 14:570–581
Libanje F, Raingeaud J, Luan R, Thomas Z, Zajac O, Veiga J, Marisa L, Adam J, Boige V, Malka D, Goéré D, Hall A, Soazec J, Prall F, Gelli M, Dartigues P, Jaulin F (2019) ROCK2 inhibition triggers the collective invasion of colorectal adenocarcinomas. EMBO J 38:e99299
de Rooij J, Kerstens A, Danuser G, Schwartz MA, Waterman-Storer CM (2005) Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J Cell Biol 171:153–164
Gimond C, van Der Flier A, van Delft S, Brakebusch C, Kuikman I, Collard JG, Fässler R, Sonnenberg A (1999) Induction of cell scattering by expression of beta1-integrins in beta1-deficient epithelial cells requires activation of members of the rho family of GTPases and downregulation of cadherin and catenin function. J Cell Biol 147:1325–1340
Margadant C, Kreft M, de Groot DJ, Norman JC, Sonnenberg A (2012) Distinct roles of Talin and kindlin in regulating integrin alpha5beta1 function and trafficking. Curr Biol 22:1554–1563
Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall J, Harrington K, Sahai E (2007) Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 9:1392–1400
Wang X, He L, Wu Y, Hahn K, Montell D (2010) Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat Cell Biol 12:591–597. https://doi.org/10.1038/ncb2061.Light-mediated
Haeger A, Wolf K, Zegers MM, Friedl P (2015) Collective cell migration: guidance principles and hierarchies. Trends Cell Biol 25:556–566
Eilken HM, Adams RH (2010) Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol 22:617–625
Pasut A, Becker LM, Cuypers A, Carmeliet P (2021) Endothelial cell plasticity at the single-cell level. Angiogenesis 24:311–326. https://doi.org/10.1007/s10456-021-09797-3
De Bock K, Georgiadou M, Schoors S, Kuchnio A, Wong BW, Cauwenberghs S, Eelen G, Segura I, Cruys B, Bifari F, Decimo I, Blanco R, Wyns S, Vangindertael J, Rocha S, Collins RT, Munck S, Daelemans D, Imamura H, Devlieger R, Rider M, Van Veldhoven PP, Schuit F, Bartrons R, Hofkens J, Fraisl P, Telang S, DeBerardinis RJ, Schoonjans L, Vinckier S, Chesney J, Gerhardt H, Dewerchin M, Carmeliet P (2013) Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 154:651–663. https://doi.org/10.1016/j.cell.2013.06.037
Ochoa-Espinosa A, Affolter M (2012) Branching morphogenesis: from cells to organs and back. Cold Spring Harb Perspect Biol 4. https://doi.org/10.1101/cshperspect.a008243
Wang S, Sekiguchi R, Daley WP, Yamada KM (2017) Cell and matrix dynamics in branching morphogenesis. J Cell Biol 216:559–570. https://doi.org/10.1016/B978-0-12-818422-6.00014-9
Caswell P, Vadrevu S, Norman J (2009) Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol 10:843–853
Moreno-Layseca P, Icha J, Hamidi H, Ivaska J (2019) Integrin trafficking in cells and tissues. Nat Cell Biol 21:122–132. https://doi.org/10.1038/s41556-018-0223-z.Integrin
Nolte MA, Nolte-‘t Hoen ENM, Margadant C (2021) Integrins control vesicular trafficking; new tricks for old dogs. Trends Biochem Sci 46:124–137. https://doi.org/10.1016/j.tibs.2020.09.001
Paul NR, Jacquemet G, Caswell PT (2015) Endocytic trafficking of Integrins in cell migration. Curr Biol 25:R1092–R1105. https://doi.org/10.1016/j.cub.2015.09.049
Jonker C, Galmes R, Veenendaal T, Brink C, van der Welle R, Liv N, de Rooij J, Peden AA, van der Sluijs P, Margadant C, Klumperman J (2018) Vps3 and Vps8 control integrin trafficking from early to recycling endosomes and regulate integrin-dependent functions. Nat Commun 9:1–12
Lobert VH, Brech A, Pedersen NM, Wesche J, Oppelt A, Malerød L, Stenmark H (2010) Ubiquitination of α5β1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes. Dev Cell 19:148–159. https://doi.org/10.1016/j.devcel.2010.06.010
Kempers L, Wakayama Y, van der Bijl I, Furumaya C, De Cuyper IM, Jongejan A, Kat M, van Stalborch AMD, van Boxtel AL, Hubert M, Geerts D, van Buul JD, de Korte D, Herzog W, Margadant C (2021) The endosomal RIN2/Rab5C machinery prevents VEGFR2 degradation to control gene expression and tip cell identity during angiogenesis. Angiogenesis 24:695–714. https://doi.org/10.1007/s10456-021-09788-4
Salvatore C, Malinverno C, Neumann B, Tischer C, Palamidessi A, Frittoli E, Panagiotakopoulou M, Disanza A, Malet-Engra G, Nastaly P, Galli C, Luise C, Bertalot G, Pece S, Di Fiore PP, Gauthier N, Ferrari A, Maiuri P, Scita G (2018) A RAB35-p85/PI3K axis controls oscillatory apical protrusions required for efficient chemotactic migration. Nat Commun 9:1–19
Linford A, Yoshimura SI, Bastos RN, Langemeyer L, Gerondopoulos A, Rigden DJ, Barr FA (2012) Rab14 and its exchange factor FAM116 link endocytic recycling and Adherens junction stability in migrating cells. Dev Cell 22:952–966
Guadagno NA, Margiotta A, Bjørnestad SA, Haugen LH, Kjos I, Xu X, Hu X, Bakke O, Margadant F, Progida C (2020) Rab18 regulates focal adhesion dynamics by interacting with kinectin-1 at the endoplasmic reticulum. J Cell Biol 219. https://doi.org/10.1083/JCB.201809020
Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525
Homma Y, Kinoshita R, Kuchitsu Y, Wawro PS, Marubashi S, Oguchi ME, Ishida M, Fujita N, Fukuda M (2019) Comprehensive knockout analysis of the Rab family GTPases in epithelial cells. J Cell Biol 218:2035–2050
Sung BH, Ketova T, Hoshino D, Zijlstra A, Weaver AM (2015) Directional cell movement through tissues is controlled by exosome secretion. Nat Commun 6:1–14. https://doi.org/10.1038/ncomms8164
Sung BH, Parent CA, Weaver AM (2021) Extracellular vesicles: critical players during cell migration. Dev Cell 56:1861–1874
Moissoglu K, Stueland M, Gasparski AN, Wang T, Jenkins LM, Hastings ML, Mili S (2020) RNA localization and co-translational interactions control RAB 13 GTP ase function and cell migration. EMBO J 39:1–19. https://doi.org/10.15252/embj.2020104958
Costa G, Bradbury JJ, Tarannum N, Herbert SP (2020) RAB13 mRNA compartmentalisation spatially orients tissue morphogenesis. EMBO J 39:1–20. https://doi.org/10.15252/embj.2020106003
Kuhn J, Lin Y, Devreotes PN (2021) Using live-cell imaging and synthetic biology to probe directed migration in Dictyostelium. Front Cell Dev Biol 9:740205. https://doi.org/10.3389/fcell.2021.740205
Sherwood DR, Plastino J (2018) Invading, leading and navigating cells in caenorhabditis elegans: insights into cell movement in vivo. Genetics 208:53–78. https://doi.org/10.1534/genetics.117.300082
Lebreton G, Casanova J (2014) Specification of leading and trailing cell features during collective migration in the Drosophila trachea. J Cell Sci 127:465–474. https://doi.org/10.1242/jcs.142737
Klußmann-Fricke B-J, Martín-Bermudo MD, Llimargas M (2022) The basement membrane controls size and integrity of the drosophila tracheal tubes. Cell Rep 39:110734. https://doi.org/10.1016/j.celrep.2022.110734
Bischoff MC, Bogdan S (2021) Collective cell migration driven by filopodia-new insights from the social behavior of myotubes. BioEssays 43:2100124. https://doi.org/10.1002/bies.202100124
Prasad M, Wang X, He L, Cai D, Montell DJ (2015) Border cell migration: a model system for live imaging and genetic analysis of collective cell movement. Methods Mol Biol:89–97
Stuelten CH, Parent CA, Montell DJ (2018) Cell motility in cancer invasion and metastasis: insights from simple model organisms. Nat Rev Cancer 18:296–312. https://doi.org/10.1038/nrc.2018.15
van Boxtel AL, Economou AD, Heliot C, Hill CS (2018) Long-range signaling activation and local inhibition separate the mesoderm and endoderm lineages. Dev Cell 44:179-191.e5. https://doi.org/10.1016/j.devcel.2017.11.021
Richardson BE, Lehmann R (2010) Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 11:37–49. https://doi.org/10.1038/nrm2815
Mayor R, Theveneau E (2012) The neural crest. Dev 140:2247–2251. https://doi.org/10.1242/dev.091751
Nieto MA, Huang RYYJ, Jackson RAA, Thiery JPP (2016) EMT: 2016. Cell 166:21–45. https://doi.org/10.1016/j.cell.2016.06.028
Ellertsdóttir E, Lenard A, Blum Y, Krudewig A, Herwig L, Affolter M, Belting H (2010) Vascular morphogenesis in the zebrafish embryo. Dev Biol 341:56–65
Schuermann A, Helker C, Herzog W (2014) Angiogenesis in zebrafish. Semin Cell Dev Biol 31:106–114
Greenspan LJ, Weinstein BM (2021) To be or not to be: endothelial cell plasticity in development, repair, and disease. Angiogenesis 24:251–269. https://doi.org/10.1007/s10456-020-09761-7
Li C, Ma J, Groenewoud A, Ren J, Liu S, Snaar-Jagalska BE, ten Dijke P (2022) Establishment of embryonic zebrafish xenograft assays to investigate TGF-β family signaling in human breast cancer progression. Methods Mol Biol
Bussmann J, Raz E (2015) Chemokine-guided cell migration and motility in zebrafish development. EMBO J 34:1309–1318. https://doi.org/10.15252/embj.201490105
Ma EY, Raible DW (2009) Signaling pathways regulating zebrafish lateral line development. Curr Biol 19:381–386. https://doi.org/10.1016/J.CUB.2009.03.057
Omelchenko T, Hall A, Anderson KV (2020) β-Pix-dependent cellular protrusions propel collective mesoderm migration in the mouse embryo. Nat Commun 11
Zhang Y, Kim TH, Niswander L (2012) Phactr4 regulates directional migration of enteric neural crest through PP1, integrin signaling, and cofilin activity. Genes Dev 26:69–81
Molè MA, Galea GL, Rolo A, Weberling A, Nychyk O, De Castro SC, Savery D, Fässler R, Ybot-González P, Greene NDE, Copp AJ (2020) Integrin-mediated focal Anchorage drives epithelial zippering during mouse neural tube closure. Dev Cell 52:321-334.e6. https://doi.org/10.1016/j.devcel.2020.01.012
Milde F, Lauw S, Koumoutsakos P, Iruela-Arispe ML (2013) The mouse retina in 3D: quantification of vascular growth and remodeling. Integr Biol 5:1426–1438. https://doi.org/10.1039/c3ib40085a
Clemente C, Rius C, Alonso-Herranz L, Martín-Alonso M, Pollán Á, Camafeita E, Martínez F, Mota RA, Núñez V, Rodríguez C, Seiki M, Martínez-González J, Andrés V, Ricote M, Arroyo AG (2018) MT4-MMP deficiency increases patrolling monocyte recruitment to early lesions and accelerates atherosclerosis. Nat Commun 9. https://doi.org/10.1038/s41467-018-03351-4
Seynhaeve ALB, ten Hagen TLM (2021) An adapted dorsal skinfold model used for 4D intravital followed by whole-mount imaging to reveal endothelial cell-pericyte association. Sci Rep 123:20389. https://doi.org/10.1038/s41598-021-99939-w
Scheele CLGJ, Hannezo E, Muraro MJ, Zomer A, Langedijk NSM, Van Oudenaarden A, Simons BD, Van Rheenen J (2017) Identity and dynamics of mammary stem cells during branching morphogenesis. Nature 542:313–319. https://doi.org/10.1038/nature21046
Gurevich DB, Severn CE, Twomey C, Greenhough A, Cash J, Toye AM, Mellor H, Martin P (2018) Live imaging of wound angiogenesis reveals macrophage orchestrated vessel sprouting and regression. EMBO J 37:1–23. https://doi.org/10.15252/embj.201797786
Cukierman E, Pankov R, Stevens DR, Yamada KM (2001) Taking cell-matrix adhesions to the third dimension. Science 294:1708–1712. https://doi.org/10.1126/science.1064829
Chen H-C (2005) Boyden chamber assay. Methods Mol Biol 294:15–22
Trujillo S, Gonzalez-Garcia C, Rico P, Reid A, Windmill J, Dalby MJ, Salmeron-Sanchez M (2020) Engineered 3D hydrogels with full-length fibronectin that sequester and present growth factors. Biomaterials 252:120104. https://doi.org/10.1016/j.biomaterials.2020.120104
Ondeck MG, Kumar A, Placone JK, Plunkett CM, Matte BF, Wong KC, Fattet L, Yang J, Engler AJ (2019) Dynamically stiffened matrix promotes malignant transformation of mammary epithelial cells via collective mechanical signaling. Proc Natl Acad Sci U S A 116:3502–3507. https://doi.org/10.1073/pnas.1814204116
Kaukonen R, Jacquemet G, Hamidi H, Ivaska J (2017) Cell-derived matrices for studying cell proliferation and directional migration in a complex 3D microenvironment. Nat Protoc 12:2376–2390. https://doi.org/10.1038/nprot.2017.107
Yang Q, Liberali P (2021) Collective behaviours in organoids. Curr Opin Cell Biol 72:81–90. https://doi.org/10.1016/j.ceb.2021.06.006
Rodrigues J, Heinrich MA, Teixeira LM, Prakash J (2021) 3D in vitro model (R)evolution: unveiling tumor–stroma interactions. Trend Cancer 7:249–264. https://doi.org/10.1016/j.trecan.2020.10.009
Khalil AA, Ilina O, Vasaturo A, Venhuizen JH, Vullings M, Venhuizen V, Bilos AB, Figdor CG, Span PN, Friedl P (2020) Collective invasion induced by an autocrine purinergic loop through connexin-43 hemichannels. J Cell Biol 219:e201911120. https://doi.org/10.1083/JCB.201911120
Staneva R, El Marjou F, Barbazan J, Krndija D, Richon S, Clark AG, Vignjevic DM (2019) Cancer cells in the tumor core exhibit spatially coordinated migration patterns. J Cell Sci 132:1–9. https://doi.org/10.1242/jcs.220277
Garcia-Arcos JM, Chabrier R, Deygas M, Nader G, Barbier L, Sáez PJ, Mathur A, Vargas P, Piel M (2019) Reconstitution of cell migration at a glance. J Cell Sci 132:0–2. https://doi.org/10.1242/jcs.225565
Jiang X, Bruzewicz DA, Wong AP, Piel M, Whitesides GM (2005) Directing cell migration with asymmetric micropatterns. Proc Natl Acad Sci U S A 102:975–978. https://doi.org/10.1073/pnas.0408954102
Roca-Cusachs P, Conte V, Trepat X (2017) Quantifying forces in cell biology. Nat Cell Biol 19:742–751. https://doi.org/10.1038/ncb3564
Simpson KJ, Selfors LM, Bui J, Reynolds A, Leake D, Khvorova A, Brugge JS (2008) Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 10:1027–1038. https://doi.org/10.1038/ncb1762
Chen X, Nadiarynkh O, Plotnikov S, Campagnola PJ (2012) Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protoc 7:654–669. https://doi.org/10.1038/nprot.2012.009
Weigelin B, Bakker GJ, Friedl P (2016) Third harmonic generation microscopy of cells and tissue organization. J Cell Sci 129:245–255. https://doi.org/10.1242/jcs.152272
Huet-Calderwood C, Rivera-Molina F, Iwamoto DV, Kromann EB, Toomre D, Calderwood DA (2017) Novel ecto-tagged integrins reveal their trafficking in live cells. Nat Commun 8:8. https://doi.org/10.1038/s41467-017-00646-w
Ferrari R, Martin L, Tagit O, Guichard A, Cambi A, Vassilopoulos P, Chavrier P (2019) MT1-MMP directs force-producing proteolytic contacts that drive tumor cell invasion. Nat Commun 10. https://doi.org/10.1038/s41467-019-12930-y
Mehta P, Rahman Z, Ten Dijke P, Boukany PE (2022) Microfluidics meets 3D cancer cell migration. Trend Cancer 8:683. https://doi.org/10.1016/j.trecan.2022.03.006
Paul CD, Hung W-C, Wirtz D, Konstantopoulos K (2016) Engineered models of confined cell migration. Annu Rev Biomed Eng 18:159–180. https://doi.org/10.1146/annurev-bioeng-071114-040654
Yi H-G, Lee H, Cho D-W, Kim HJ (2017) 3D printing of organs-on-chips. Bioengineering 4. https://doi.org/10.3390/bioengineering4010010
Massarwa R, Niswander L (2013) In toto live imaging of mouse morphogenesis and new insights into neural tube closure. Development 140:226–236
Aguilera-Castrejon A, Oldak B, Shani T, Ghanem N, Itzkovich C, Slomovich S, Tarazi S, Bayerl J, Chugaeva V, Ayyash M, Ashouokhi S, Sheban D, Livnat N, Lasman L, Viukov S, Zerbib M, Addadi Y, Rais Y, Cheng S, Stelzer Y, Keren-Shaul H, Shlomo R, Massarwa R, Novershtern N, Maza I, Hanna JH (2021) Ex utero mouse embryogenesis from pre-gastrulation to late organogenesis. Nature 593:119–124. https://doi.org/10.1038/s41586-021-03416-3
van Rheenen J, Scheele CLGJ (2021) Intravital microscopy to illuminate cell state plasticity during metastasis. Curr Opin Cell Biol 72:28–35. https://doi.org/10.1016/j.ceb.2021.04.004
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Margadant, C. (2023). Cell Migration in Three Dimensions. In: Margadant, C. (eds) Cell Migration in Three Dimensions. Methods in Molecular Biology, vol 2608. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2887-4_1
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