Individual versus collective fibroblast spreading and migration: Regulation by matrix composition in 3D culture

Experimental Eye Research

Volumn 99, Issue 1, 2012, Pages 36-44

  Miron Mendoza, Miguel ^a   Lin, Xihui ^a   Ma, Lisha ^a   Ririe, Peter ^a   Petroll, W Matthew ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

3D culture; Cell motility; Collagen; Extracellular matrix; Fibrin

Indexed keywords

CADHERIN; COLLAGEN; FIBRIN;

ARTICLE; CELL MIGRATION; CELL STRUCTURE; CYTOSKELETON; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; HUMAN CELL; MICROSCOPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; THREE DIMENSIONAL IMAGING; TIME LAPSE MICROSCOPY;

CADHERINS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN; CORNEAL KERATOCYTES; EXTRACELLULAR MATRIX; FIBRIN; FIBROBLASTS; FIBRONECTINS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HUMANS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, CONFOCAL; SKIN; TIME-LAPSE IMAGING;

EID: 84861670229     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2012.03.015     Document Type: Article

References (56)

1. Alexander S., Koehl G.E., Hirschberg M., Geissler E.K., Friedl P. Dynamic imaging of cancer growth and invasion: a modified skin-fold chamber model. Histochem. Cell Biol. 2008, 130:1147-1154.
2. Andresen J.L., Ledet T., Hager H., Josephsen K., Ehlers N. The influence of corneal stromal matrix proteins on the migration of human corneal fibroblasts. Exp. Eye Res. 2000, 71:33-43.
3. Brown R.A., Wiseman M., Chuo C.-B., Cheema U., Nazhat S.N. Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano- and microstructures by plastic compression. Adv. Funct. Mater. 2005, 15:1762-1770.
4. Casey R.C., Burleson K.M., Skubitz K.M., Pambuccian S.E., Oegama T.R., Ruff L.E., Skubitz A.P. Beta 1-integrins regulate the formation and adhesion of ovarian carcinoma multicellular spheroids. Am. J. Pathol. 2001, 159:2071-2080.
5. Chandran P.L., Barocas V.H. Affine versus non-afine fibril kinematics in collagen networks: theoretical studies of network behavior. J. Biomech. Eng. 2006, 128:259-270.
6. Clark R.A.F. Wound repair: overview and general considerations. Molecular and Cellular Biology of Wound Repair 1996, 3-50. Plenum Press. R.A.F. Clark (Ed.).
7. Cox T.R., Erler J.T. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis. Model. Mech. 2011, 4:165-178.
8. Davis E.M., Trinkaus J.P. Significance of cell-to-cell contacts or the directional movement of neural crest cells within a hydrate collagen lattice. J. Embryol. Exp. Morph. 1981, 63:29-51.
9. Farooqui R., Fenteany G. Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement. J. Cell Sci. 2005, 118:51-63.
10. Friedl P., Wolf K. Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 2009, 199:11-19.
11. Ghosh K., Ingber D.E. Micromechanical control of cell and tissue development: implications for tissue engineering. Adv. Drug Deliv. Rev. 2007, 59:1306-1318.
12. Greiling D., Clark R.A. Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J. Cell Sci. 1997, 100:861-870.
13. Greiling D., Clark R.A. Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J. Cell Sci. 1997, 110(Pt 7):861-870.
14. Grinnell F. Fibroblast-collagen matrix contraction: growth-factor signalling and mechanical loading. Trends Cell Biol. 2000, 10:362-365.
15. Grinnell F., Feld M., Minter D. Fibroblast adhesion to fibronectin and fibrin substrata: requirement for cold-insoluble globulin (plasma fibronectin). Cell 1980, 19:517-525.
16. Hakkinen K.M., Harunaga J.S., Doyle A.D., Yamada K.M. Direct comparison of the morphology, migration, cell adhesions, and actin cytoskeleton of fibroblasts in four different three-dimensional extracellular matrices. Tissue Eng.: Part A 2011, 17:713-724.
17. Hassell J.R., Birk D.E. The molecular basis of corneal transparency. Exp. Eye Res. 2010, 91:326-335.
18. Hegerfeldt Y., Tusch M., Brocker E.-B., Friedl P. Collective cell movement in primary melanoma explants: plasticity of cell-cell interaction, b1-integrin function, and migration strategies. Cancer Res. 2002, 62:2125-2130.
19. Ichijima H., Petroll W.M., Jester J.V., Barry P.A., Andrews P.M., Dai M., Cavanagh H.D. In vivo confocal microscopic studies of endothelial wound healing in rabbit cornea. Cornea 1993, 12:369-378.
20. Ilina O., Friedl P. Mechanisms of collective cell migration at a glance. J. Cell Sci. 2009, 122:3203-3208.
21. Jester J.V., Barry P.A., Lind G.J., Petroll W.M., Garana R., Cavanagh H.D. Corneal keratocytes: in situ and in vitro organization of cytoskeletal contractile proteins. Invest. Ophthalmol. Vis. Sci. 1994, 35:730-743.
22. Jester J.V., Huang J., Barry-Lane P.A., Kao W.W., Petroll W.M., Cavanagh H.D. Transforming growth factor(beta)-mediated corneal myofibroblast differentiation requires actin and fibronectin assembly. Invest. Ophthalmol. Vis. Sci. 1999, 40:1959-1967.
23. Jester J.V., Huang J., Fisher S., Spiekerman J., Chang J.H., Wright W.E., Shay J.W. Myofibroblast differentiation of normal human keratocytes and hTERT, extended-life, human corneal fibroblasts. Invest. Ophthalmol. Vis. Sci. 2003, 44:1850-1858.
24. Jester J.V., Petroll W.M., Barry P.A., Cavanagh H.D. Temporal, 3-dimensional, cellular anatomy of corneal wound tissue. J. Anat. 1995, 186:301-311.
25. Jester J.V., Petroll W.M., Barry P.A., Cavanagh H.D. Temporal, 3-dimensional, cellular anatomy of corneal wound tissue. J. Anat. 1995, 186(Pt 2):301-311.
26. Jester J.V., Petroll W.M., Cavanagh H.D. Corneal stromal wound healing in refractive surgery: the role of the myofibroblast. Prog. Retinal. Eye Res. 1999, 18:311-356.
27. Jiang H., Rhee S., Ho C.-H., Grinnell F. Distinguishing fibroblast promigratory and procontractile growth factor environments in 3-D collagen matrices. FASEB J. 2008, 22:2151-2160.
28. Karamichos D., Lakshman N., Petroll W.M. An experimental model for assessing fibroblast migration in 3-D collagen matrices. Cell Motil. Cytoskeleton 2009, 66:1-9.
29. Kasemeier-Kulesa J.C., Kulesa P.M., Lefcort F. Imaging neural crest cell dynamics during formation of dorsal root ganglia and sympathetic ganglia. Development 2005, 132:235-245.
30. Kim A., Lakshman N., Karamichos D., Petroll W.M. Growth factor regulation of corneal keratocyte differentiation and migration in compressed collagen matrices. Invest. Ophthalmol. Vis. Sci. 2010, 51:864-875.
31. Kim A., Zhou C., Lakshman N., Petroll W.M. Corneal stromal cells use both high- and low-contractility migration mechanisms in 3-D collagen matrices. Exp. Cell Res. 2012, 10.1016/j.yexcr.2011.12.018.
32. Lakshman N., Kim A., Petroll W.M. Characterization of corneal keratocyte morphology and mechanical activity within 3-D collagen matrices. Exp. Eye Res. 2010, 90:350-359.
33. Miron-Mendoza M., Seemann J., Grinnell F. Collagen fibril flow and tissue translocation coupled to fibroblast migration in 3D collagen matrices. Mol. Biol. Cell 2008, 19:2051-2058.
34. Miron-Mendoza M., Seemann J., Grinnell F. The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials 2010, 31:6425-6435.
35. Moller-Pedersen T., Cavanagh H.D., Petroll W.M., Jester J.V. Stromal wound healing explains refractive instability and haze development after photorefractive keratectomy: a 1-year confocal microscopic study. Ophthalmology 2000, 107:1235-1245.
36. Neel E.A.A., Cheema U., Knowles J.C., Brown R.A., Nazhat S.N. Use of multiple unconfined compression for control of collagen gel scaffold density and mechanical properties. Soft Matter 2006, 2:986-992.
37. Nelson C.M., Bissell M.J. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 2006, 22:287-309.
38. Netto M.V., Mohan R.R., Ambrosio R., Hutcheon A.E.K., Zieske J.D., Wilson S.E. Wound healing in the cornea: a review of refractive surgery complications and new prospects for therapy. Cornea 2005, 24:509-522.
39. Pepose J.S., Ubels J.L. The cornea. Adler's Physiology of the Eye 1992, 29-70. Mosby Year Book, St. Louis. W.M. Hart (Ed.).
40. Petroll W.M., Cavanagh H.D., Barry P., Andrews P., Jester J.V. Quantitative analysis of stress fiber orientation during corneal wound contraction. J. Cell Sci. 1993, 104(Pt 2):353-363.
41. Petroll W.M., Ma L., Jester J.V. Direct correlation of collagen matrix deformation with focal adhesion dynamics in living corneal fibroblasts. J. Cell Sci. 2003, 116:1481-1491.
42. Petroll W.M., Ma L., Kim A., Ly L., Vishwanath M. Dynamic assessment of fibroblast mechanical activity during Rac-induced cell spreading in 3-D culture. J. Cell Physiol. 2008, 217:162-171.
43. Phan T.M., Foster C.S., Wasson P.J., Fujikawa L.S., Zagachin L.M., Colvin R.B. Role of fibronectin and fibrinogen in healing of corneal epithelial scrape wounds. Invest. Ophthalmol. Vis. Sci. 1989, 30:377-385.
44. Reinhart-King C.A. How matrix properties control the self-assembly and maintenance of tissues. Ann. Biomed. Eng. 2011, 39:1849-1856.
45. Rhee S., Ho C.H., Grinnell F. Promigratory and procontractile growth factor environments differentially regulate cell morphogenesis. Exp. Cell Res. 2010, 316:232-244.
46. Salmenpera P., Kankuri E., Bizik J., Siren V., Virtanen I., Takahashi S., Leiss M., Fassier R., Vaheri A. Formation and activation of fibroblast spheroids depend on fibronectin-integrin interaction. Exp. Cell Res. 2008, 314:3444-3452.
47. Schultz G.S., Davidson J.M., Kirsner R.S., Bornstein P., Herman I.M. Dynamic reciprocity in the wound microenvironment. Wound Repair Regen. 2011, 19:134-148.
48. Shaw T.J., Martin P. Wound repair at a glance. J. Cell Sci. 2009, 122:3209-3213.
49. Singh P., Carraher C., Schwarzbauer J.E. Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 2010, 26:397-419.
50. Stramer B.M., Zieske J.D., Jung J.-C., Austin J.S., Fini M.E. Molecular mechanisms controlling the fibrotic repair phenotype in cornea: implications for surgical outcomes. Invest. Ophthalmol. Vis. Sci. 2003, 44:4237-4246.
51. Teddy J.M., Kulesa P.M. In vivo evidence for short- and long-range cell communication in cranial neural crest cells. Development 2004, 131:6141-6151.
52. Tomasek J.J., Hay E.D., Fujiwara K. Collagen modulates cell shape and cytoskeleton of embryonic corneal and fibroma fibroblasts: distribution of actin, α-actinin and myosin. Dev. Biol. 1982, 92:107-122.
53. 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.
54. Zaman M.H., Trapani L.M., Siemeski A., 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. 2006, 103:10889-10894.
55. Zhou X., Rowe R.G., Hiraoke 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 Development 2008, 22:1231-1243.
56. Zieske J.D. Extracellular matrix and wound healing. Curr. Opin. Ophthalmol. 2001, 12:237-241.