Imaging of cell adhesion events in 3D matrix environments

European Journal of Cell Biology

Volumn 91, Issue 11-12, 2012, Pages 824-833

  Jayo, Asier ^a   Parsons, Maddy ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

2D; 3D; Adhesion; Cytoskeleton; Extracellular matrix (ECM); Focal adhesion; Invasion; Migration

Indexed keywords

COLLAGEN TYPE 1;

BASEMENT MEMBRANE; CELL ADHESION; CELL STRUCTURE; EXTRACELLULAR MATRIX; HUMAN; IMAGE ANALYSIS; IMMUNOPATHOLOGY; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; THREE DIMENSIONAL IMAGING;

ANIMALS; CELL ADHESION; EXTRACELLULAR MATRIX; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MOLECULAR CONFORMATION;

EID: 84867402898     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2012.05.002     Document Type: Short Survey

References (103)

1. Adanja I., Megalizzi V., Debeir O., Decaestecker C. A new method to address unmet needs for extracting individual cell migration features from a large number of cells embedded in 3D volumes. PLoS ONE 2011, 6:e22263.
2. Alavi A., Stupack D.G. Cell survival in a three-dimensional matrix. Methods Enzymol. 2007, 426:85-101.
3. Albiges-Rizo C., Destaing O., Fourcade B., Planus E., Block M.R. Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J. Cell Sci. 2009, 122:3037-3049.
4. Askari J.A., Buckley P.A., Mould A.P., Humphries M.J. Linking integrin conformation to function. J. Cell Sci. 2009, 122:165-170.
5. Baldassarre M., Ayala I., Beznoussenko G., Giacchetti G., Machesky L.M., Luini A., Buccione R. Actin dynamics at sites of extracellular matrix degradation. Eur. J. Cell Biol. 2006, 85:1217-1231.
6. Beerling E., Ritsma L., Vrisekoop N., Derksen P.W.B., van Rheenen J. Intravital microscopy: new insights into metastasis of tumors. J. Cell Sci. 2011, 124:299-310.
7. Bellido-Martin L., Chen V., Jasuja R., Furie B., Furie B.C. Imaging fibrin formation and platelet and endothelial cell activation in vivo. Thromb. Haemost. 2011, 105:776-782.
8. Beningo K.A., Lo C.M., Wang Y.L. Flexible polyacrylamide substrata for the analysis of mechanical interactions at cell-substratum adhesions. Methods Cell Biol. 2002, 69:325-339.
9. Berney C., Danuser G. FRET or no FRET: a quantitative comparison. Biophys. J. 2003, 84:3992-4010.
10. Bianco A., Poukkula M., Cliffe A., Mathieu J., Luque C.M., Fulga T.A., Rorth P. Two distinct modes of guidance signalling during collective migration of border cells. Nature 2007, 448:362-365.
11. Campagnola P.J., Clark H.A., Mohler W.A., Lewis A., Loew L.M. Second-harmonic imaging microscopy of living cells. J. Biomed. Opt. 2001, 6:277-286.
12. Charras G., Paluch E. Blebs lead the way: how to migrate without lamellipodia. Nat. Rev. Mol. Cell Biol. 2008, 9:730-736.
13. Choi C.K., Vicente-Manzanares M., Zareno J., Whitmore L.A., Mogilner A., Horwitz A.R. Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat. Cell Biol. 2008, 10:1039-1050.
14. Clark R.A.F., Lin F., Greiling D., An J., Couchman J.R. Fibroblast invasive migration into fibronectin/fibrin gels requires a previously uncharacterized dermatan sulfate-CD44 proteoglycan. J. Invest. Dermatol. 2004, 122:266-277.
15. Cukierman E. Taking cell-matrix adhesions to the third dimension. Science 2001, 294.
16. Cukierman E., Pankov R., Stevens D.R., Yamada K.M. Taking cell-matrix adhesions to the third dimension. Science 2001, 294:1708-1712.
17. Deakin N.O., Turner C.E. Distinct roles for paxillin and Hic-5 in regulating breast cancer cell morphology, invasion, and metastasis. Mol. Biol. Cell 2011, 22:327-341.
18. Deane J.A., Hickey M.J. Molecular mechanisms of leukocyte trafficking in T-cell-mediated skin inflammation: insights from intravital imaging. Expert Rev. Mol. Med. 2009, 11:e25.
19. Doyle A.D., Wang F.W., Matsumoto K., Yamada K.M. One-dimensional topography underlies three-dimensional fibrillar cell migration. J. Cell Biol. 2009, 184:481-490.
20. Ehrbar M., Sala A., Lienemann P., Ranga A., Mosiewicz K., Bittermann A., Rizzi S.C., Weber F.E., Lutolf M.P. Elucidating the role of matrix stiffness in 3D cell migration and remodeling. Biophys. J. 2011, 100:284-293.
21. Fraley S.I., Feng Y., Krishnamurthy R., Kim D.H., Celedon A., Longmore G.D., Wirtz D. A distinctive role for focal adhesion proteins in three-dimensional cell motility. Nat. Cell Biol. 2010, 12:598-604.
22. Fraley S.I., Feng Y., Wirtz D., Longmore G.D. Reply: reducing background fluorescence reveals adhesions in 3D matrices. Nat. Cell Biol. 2011, 13:5-7.
23. Friedl P., Brocker E.B. The biology of cell locomotion within three-dimensional extracellular matrix. Cell. Mol. Life Sci. 2000, 57:41-64.
24. Friedl P., Wolf K. Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 2010, 188:11-19.
25. Friedl P., Zanker K.S., Brocker E.B. Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc. Res. Tech. 1998, 43:369-378.
26. Gaggioli C., Hooper S., Hidalgo-Carcedo C., Grosse R., Marshall J.F., Harrington K., Sahai E. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 2007, 9:1392-1400.
27. Gehler S., Baldassarre M., Lad Y., Leight J.L., Wozniak M.A., Riching K.M., Eliceiri K.W., Weaver V.M., Calderwood D.A., Keely P.J. Filamin A-beta1 integrin complex tunes epithelial cell response to matrix tension. Mol. Biol. Cell 2009, 20:3224-3238.
28. Giampieri S., Manning C., Hooper S., Jones L., Hill C.S., Sahai E. Localized and reversible TGF[beta] signalling switches breast cancer cells from cohesive to single cell motility. Nat. Cell Biol. 2009, 11:1287-1296.
29. Gil V., Del Rio J.A. Analysis of axonal growth and cell migration in 3D hydrogel cultures of embryonic mouse CNS tissue. Nat. Protoc. 2012, 7(2):268-280.
30. Hakkinen K.M., Harunaga J.S., Doyle A.D., Yamada K.M. Direct comparisons of the morphology, migration, cell adhesions, and actin cytoskeleton of fibroblasts in four different three-dimensional extracellular matrices. Tissue Eng. A 2011, 17(5-6):713-724.
31. Harunaga J.S., Yamada K.M. Cell-matrix adhesions in 3D. Matrix Biol. 2011, 30:363-368.
32. Hidalgo-Carcedo C., Hooper S., Chaudhry S.I., Williamson P., Harrington K., Leitinger B., Sahai E. Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat. Cell Biol. 2011, 13:49-58.
33. Hooper S., Gaggioli C., Sahai E. A chemical biology screen reveals a role for Rab21-mediated control of actomyosin contractility in fibroblast-driven cancer invasion. Br. J. Cancer 2010, 102:392-402.
34. Hotary K., Li X.Y., Allen E., Stevens S.L., Weiss S.J. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev. 2006, 20:2673-2686.
35. Huttenlocher A., Horwitz A.R. Integrins in cell migration. Cold Spring Harb. Perspect. Biol. 2011, 3:a005074.
36. Ilina O., Friedl P. Mechanisms of collective cell migration at a glance. J. Cell Sci. 2009, 122:3203-3208.
37. Joshi B., Strugnell S.S., Goetz J.G., Kojic L.D., Cox M.E., Griffith O.L., Chan S.K., Jones S.J., Leung S.P., Masoudi H., Leung S., Wiseman S.M., Nabi I.R. Phosphorylated caveolin-1 regulates Rho/ROCK-dependent focal adhesion dynamics and tumor cell migration and invasion. Cancer Res. 2008, 68:8210-8220.
38. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 2003, 3:422-433.
39. Kanchanawong P., Waterman C.M. Advances in light-based imaging of three-dimensional cellular ultrastructure. Curr. Opin. Cell Biol. 2011, 24:125-133.
40. Kelleher M.T., Fruhwirth G., Patel G., Ofo E., Festy F., Barber P.R., Ameer-Beg S.M., Vojnovic B., Gillett C., Coolen A., Keri G., Ellis P.A., Ng T. The potential of optical proteomic technologies to individualize prognosis and guide rational treatment for cancer patients. Target Oncol. 2009, 4:235-252.
41. Khuon S., Liang L., Dettman R.W., Sporn P.H., Wysolmerski R.B., Chew T.L. Myosin light chain kinase mediates transcellular intravasation of breast cancer cells through the underlying endothelial cells: a three-dimensional FRET study. J. Cell Sci. 2010, 123(Pt 3):431-440.
42. Kleinman H.K. Preparation of gelled substrates. Current Protocols in Cell Biology 2001, John Wiley & Sons, Inc.
43. Koster R.W., Fraser S.E. Direct imaging of in vivo neuronal migration in the developing cerebellum. Curr. Biol. 2001, 11:1858-1863.
44. Kubow K.E., Horwitz A.R. Reducing background fluorescence reveals adhesions in 3D matrices. Nat. Cell Biol. 2011, 13(1):3-5. author reply 5-7.
45. Lammermann T., Sixt M. Mechanical modes of 'amoeboid' cell migration. Curr. Opin. Cell Biol. 2009, 21:636-644.
46. Levitt J.A., Matthews D.R., Ameer-Beg S.M., Suhling K. Fluorescence lifetime and polarization-resolved imaging in cell biology. Curr. Opin. Biotechnol. 2009, 20:28-36.
47. Li A., Dawson J.C., Forero-Vargas M., Spence H.J., Yu X., Konig I., Anderson K., Machesky L.M. The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr. Biol. 2010, 20:339-345.
48. Lord S.T. Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr. Opin. Hematol. 2007, 14:236-241.
49. Maaser K., Wolf K., Klein C.E., Niggemann B., Zänker K.S., Bröcker E.B., Friedl P. Functional hierarchy of simultaneously expressed adhesion receptors: integrin α2β1 but not CD44 mediates MV3 melanoma cell migration and matrix reorganization within three-dimensional hyaluronan-containing collagen matrices. Mol. Biol. Cell 1999, 10:3067-3079.
50. Machacek M., Hodgson L., Welch C., Elliott H., Pertz O., Nalbant P., Abell A., Johnson G.L., Hahn K.M., Danuser G. Coordination of Rho GTPase activities during cell protrusion. Nature 2009, 461:99-103.
51. Madsen C.D., Sahai E. Cancer dissemination - lessons from leukocytes. Dev. Cell 2010, 19:13-26.
52. Marshall J. Transwell((R)) invasion assays. Methods Mol. Biol. 2011, 769:97-110.
53. Maskarinec S.A., Franck C., Tirrell D.A., Ravichandran G. Quantifying cellular traction forces in three dimensions. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(52):22108-22113.
54. McGhee E.J., Morton J.P., Von Kriegsheim A., Schwarz J.P., Karim S.A., Carragher N.O., Sansom O.J., Anderson K.I., Timpson P. FLIM-FRET imaging in vivo reveals 3D-environment spatially regulates RhoGTPase activity during cancer cell invasion. Small GTPases 2011, 2(4):239-244.
55. Meier F., Nesbit M., Hsu M.-Y., Martin B., Van Belle P., Elder D.E., Schaumburg-Lever G., Garbe C., Walz T.M., Donatien P., Crombleholme T.M., Herlyn M. Human melanoma progression in skin reconstructs: biological significance of bFGF. Am. J. Pathol. 2000, 156:193-200.
56. Nystrom M.L., Thomas G.J., Stone M., Mackenzie I.C., Hart I.R., Marshall J.F. Development of a quantitative method to analyse tumour cell invasion in organotypic culture. J. Pathol. 2005, 205:468-475.
57. Patla I., Volberg T., Elad N., Hirschfeld-Warneken V., Grashoff C., Fassler R., Spatz J.P., Geiger B., Medalia O. Dissecting the molecular architecture of integrin adhesion sites by cryo-electron tomography. Nat. Cell Biol. 2010, 12:909-915.
58. Pacary E., Heng J., Azzarelli R., Riou P., Castro D., Lebel-Potter M., Parras C., Bell D.M., Ridley A.J., Parsons M., Guillemot F. Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signaling. Neuron 2011, 69(6):1069-1084.
59. Pelham R.J., Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:13661-13665.
60. Pelham R.J., Wang Y.-l. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:13661-13665.
61. Pertz O., Hahn K.M. Designing biosensors for Rho family proteins - deciphering the dynamics of Rho family GTPase activation in living cells. J. Cell Sci. 2004, 117:1313-1318.
62. Poincloux R., Collin O., Lizarraga F., Romao M., Debray M., Piel M., Chavrier P. Contractility of the cell rear drives invasion of breast tumor cells in 3D Matrigel. Proc. Natl. Acad. Sci. U.S.A. 2011, 108(5):1943-1948.
63. Prasad M., Montell D.J. Cellular and molecular mechanisms of border cell migration analyzed using time-lapse live-cell imaging. Dev. Cell 2007, 12:997-1005.
64. Provenzano P.P., Inman D.R., Eliceiri K.W., Keely P.J. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 2009, 28:4326-4343.
65. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., Horwitz A.R. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
66. Robles E., Gomez T.M. Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat. Neurosci. 2006, 9:1274-1283.
67. Roeder B.A., Kokini K., Sturgis J.E., Robinson J.P., Voytik-Harbin S.L. Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J. Biomech. Eng. 2002, 124:214-222.
68. Sabeh F., Ota I., Holmbeck K., Birkedal-Hansen H., Soloway P., Balbin M., Lopez-Otin C., Shapiro S., Inada M., Krane S., Allen E., Chung D., Weiss S.J. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 2004, 167:769-781.
69. Sabeh F., Shimizu-Hirota R., Weiss S.J. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 2009, 185:11-19.
70. Sahai E. Illuminating the metastatic process. Nat. Rev. Cancer 2007, 7:737-749.
71. Sahai E., Wyckoff J., Philippar U., Segall J.E., Gertler F., Condeelis J. Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy. BMC Biotechnol. 2005, 5:14.
72. Sala A., Hanseler P., Ranga A., Lutolf M.P., Voros J., Ehrbar M., Weber F.E. Engineering 3D cell instructive microenvironments by rational assembly of artificial extracellular matrices and cell patterning. Integr. Biol. (Camb.) 2011, 3:1102-1111.
73. Sanz-Moreno V., Gadea G., Ahn J., Paterson H., Marra P., Pinner S., Sahai E., Marshall C.J. Rac activation and inactivation control plasticity of tumor cell movement. Cell 2008, 135:510-523.
74. Sanz-Moreno V., Marshall C.J. Rho-GTPase signaling drives melanoma cell plasticity. Cell Cycle 2009, 8:1484-1487.
75. Sanz-Moreno V., Marshall C.J. The plasticity of cytoskeletal dynamics underlying neoplastic cell migration. Curr. Opin. Cell Biol. 2010, 22:690-696.
76. Scales T.M., Parsons M. Spatial and temporal regulation of integrin signalling during cell migration. Curr. Opin. Cell Biol. 2011, 23:562-568.
77. Schoumacher M., Louvard D., Vignjevic D. Cytoskeleton networks in basement membrane transmigration. Eur. J. Cell Biol. 2011, 90:93-99.
78. Serrels A., Timpson P., Canel M., Schwarz J.P., Carragher N.O., Frame M.C., Brunton V.G., Anderson K.I. Real-time study of E-cadherin and membrane dynamics in living animals: implications for disease modeling and drug development. Cancer Res. 2009, 69(7):2714-2719.
79. Shao L., Kner P., Rego E.H., Gustafsson M.G. Super-resolution 3D microscopy of live whole cells using structured illumination. Nat. Methods 2011, 8:1044-1046.
80. Shattil S.J., Kim C., Ginsberg M.H. The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol. 2010, 11:288-300.
81. Shtengel G., Galbraith J.A., Galbraith C.G., Lippincott-Schwartz J., Gillette J.M., Manley S., Sougrat R., Waterman C.M., Kanchanawong P., Davidson M.W., Fetter R.D., Hess H.F. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3125-3130.
82. Stramer B., Wood W., Galko M.J., Redd M.J., Jacinto A., Parkhurst S.M., Martin P. Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J. Cell Biol. 2005, 168:567-573.
83. Timpson P., McGhee E.J., Anderson K.I. Imaging molecular dynamics in vivo - from cell biology to animal models. J. Cell Sci. 2011, 124:2877-2890.
84. Timpson P., McGhee E.J., Morton J.P., von Kriegsheim A., Schwarz J.P., Karim S.A., Doyle B., Quinn J.A., Carragher N.O., Edward M., Olson M.F., Frame M.C., Brunton V.G., Sansom O.J., Anderson K.I. Spatial regulation of RhoA activity during pancreatic cancer cell invasion driven by mutant p53. Cancer Res. 2011, 71(3):747-757.
85. Tolde O., Rosel D., Vesely P., Folk P., Brabek J. The structure of invadopodia in a complex 3D environment. Eur. J. Cell Biol. 2010, 89:674-680.
86. Van Goethem E., Guiet R., Balor S., Charriere G.M., Poincloux R., Labrousse A., Maridonneau-Parini I., Le Cabec V. Macrophage podosomes go 3D. Eur. J. Cell Biol. 2011, 90:224-236.
87. Van Goethem E., Poincloux R., Gauffre F., Maridonneau-Parini I., Le Cabec V. Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J. Immunol. 2010, 184:1049-1061.
88. Vicente-Manzanares M., Horwitz A.R. Adhesion dynamics at a glance. J. Cell Sci. 2011, 124:3923-3927.
89. Voisin M.B., Probstl D., Nourshargh S. Venular basement membranes ubiquitously express matrix protein low-expression regions: characterization in multiple tissues and remodeling during inflammation. Am. J. Pathol. 2010, 176:482-495.
90. Wang J.H., Lin J.S. Cell traction force and measurement methods. Biomech. Model. Mechanobiol. 2007, 6:361-371.
91. Wang N., Tytell J., Ingber D. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 2009, 10:75-157.
92. Wang X., He L., Wu Y.I., Hahn K.M., Montell D.J. Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat. Cell Biol. 2010, 12(6):591-597.
93. Willig K.I., Kellner R.R., Medda R., Hein B., Jakobs S., Hell S.W. Nanoscale resolution in GFP-based microscopy. Nat. Methods 2006, 3:721-723.
94. Wolf K., Alexander S., Schacht V., Coussens L.M., von Andrian U.H., van Rheenen J., Deryugina E., Friedl P. Collagen-based cell migration models in vitro and in vivo. Semin. Cell Dev. Biol. 2009, 20:931-941.
95. Wolf K., Friedl P. Mapping proteolytic cancer cell-extracellular matrix interfaces. Clin. Exp. Metastasis 2009, 26:289-298.
96. Wolf K., Wu Y.I., Liu Y., Geiger J., Tam E., Overall C., Stack M.S., Friedl P. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 2007, 9:893-904.
97. Woodfin A., Voisin M.-B., Beyrau M., Colom B., Caille D., Diapouli F.-M., Nash G.B., Chavakis T., Albelda S.M., Rainger G.E., Meda P., Imhof B.A., Nourshargh S. The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol. 2011, 12:761-769.
98. Wyckoff J.B., Pinner S.E., Gschmeissner S., Condeelis J.S., Sahai E. ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr. Biol. 2006, 16:1515-1523.
99. Xu K., Babcock H.P., Zhuang X. Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton. Nat. Methods 2012, 9:185-188.
100. Yoo S.K., Deng Q., Cavnar P.J., Wu Y.I., Hahn K.M., Huttenlocher A. Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev. Cell 2010, 18(2):226-236.
101. Yuan L., Fairchild M.J., Perkins A.D., Tanentzapf G. Analysis of integrin turnover in fly myotendinous junctions. J. Cell Sci. 2010, 123(Pt 6):939-946.
102. Zaman M.H., Trapani L.M., Sieminski A.L., MacKellar D., Gong H., Kamm R.D., Wells A., Lauffenburger D.A., Matsudaira P. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10889-10894.
103. Zhou X., Rowe R.G., Hiraoka N., George J.P., Wirtz D., Mosher D.F., Virtanen I., Chernousov M.A., Weiss S.J. Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. Genes Dev. 2008, 22:1231-1243.