Punch-wounded, fibroblast populated collagen matrices: A novel approach for studying cytoskeletal changes in three dimensions by confocal laser scanning microscopy

European Journal of Cell Biology

Volumn 72, Issue 3, 1997, Pages 189-201

  Baschong, Werner ^a   Sütterlin, Rosmarie ^a   Aebi, Ueli ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Actin; Collagen matrices; Confocal laser scanning microscopy; Cytoskeleton; Fibroblasts; Tubulin; Wound healing model

Indexed keywords

COLLAGEN; F ACTIN;

ARTICLE; CELL DENSITY; CELL SHAPE; CELL ULTRASTRUCTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; FIBROBLAST; FIBROBLAST CULTURE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MICROTUBULE; PRIORITY JOURNAL; PUNCH BIOPSY; WOUND;

EID: 0030933716     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (83)

1. Anderson, J. E., C. M. Mitchell, J. K. McGeachie, M. D. Grounds: The time course of basic fibroblast growth factor expression in crush-injured skeletal muscles of SJL/J and BALB/c Mice. Exp. Cell Res. 216, 325-334 (1995).
2. Antoniades, H. N., T. Galanopulos, J. Neville-Golden, C. P. Kiristy, S. E. Lynch: Injury induces in vivo expression of platelet-derived growth factor (PDGF) and PDGF receptor mRNAs in skin epithelial cells and PDGF mRNA in connective tissue fibroblasts. Proc. Natl. Acad. Sci. USA 88, 565-569 (1991).
3. Bell, E., B. Ivarsson, Ch. Merrill: Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. 76, 1274-1278 (1979).
4. Bement, W. M., P. Forscher, M. S. Mooseker: A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J. Cell Biol. 121, 565-578 (1993).
5. Bremer, A., R. C. Millonig, R. Sütterlin, A. Engel, T. D. Pollard, U. Aebi: The structural basis for the intrinsic disorder of the F-actin filament: the lateral slipping model. J. Cell Biol. 115, 89-703 (1991).
6. Bremer, A., C. Henn, K. N. Goldie, A. Engel, P. R. Smith, U. Aebi: Towards atomic interpretation of F-actin filament three-dimensional reconstructions. J. Mol. Biol. 242, 683-700 (1991).
7. Bouissou, H., M. Pieraggi, M. Julian, D. Uhart, J. Kokolo: Fibroblasts in dermal tissue repair. Int. J. Dermatol. 27, 564-570 (1988).
8. Bunting, C. H., C. C. Eades: The effect of mechanical tension upon the polarity of growing fibroblasts. J. Exp. Med. XLIV, 147-149 (1926).
9. Burridge, K., K. Fath, K. Kelly, G. Nuckolls, C. Turner: Focal adhesions: Transmembrane junction between the extracellular matrix and the actin cytoskeleton. Annu. Rev. Cell Biol. 119, 893-903 (1988).
10. Byers, H. R., K. Fujiwara: Stress fibers in cells in situ: Immunofluorescence visualization with antiactin, antimyosin and anti-alpha-actinin. J. Cell Biol. 93, 804-811 (1982).
11. Cairns, B. A., S. de Serres, H. D. Peterson, A. A. Meyer: Skin replacements. Arch. Surg. 128, 1246-1252 (1993).
12. Carlsson, K., N. Åslund: Confocal imaging for 3-D digital microscopy. Appl. Optics 126, 3232-3238 (1987).
13. Clark, R. A. F.: Biology of dermal wound healing. Dermatol. Clinics 11, 647-666 (1993).
14. Chen, W.-T: Mechanism of retraction of the trailing edge during fibroblast movement. J. Cell Biol. 90, 187-200 (1981).
15. Conrad, P. A., K. A. Giuliano, G. Fisher, K. Collins, P. T. Matsudaira, D. L. Taylor: Relative distribution of actin, myosin I, and myosin II during wound healing response of fibroblasts. J. Cell Biol. 120, 1381-1391 (1993).
16. Coulomb, B., L. Dubertret: Reconstruction cutanée et communication tissulaires. Médecine/Sciences 4, 101-108 (88).
17. Cunningham, C. C.: Actin polymerization and intracellular solvent flow in cell surface blebbing. J. Cell Biol. 129, 1589-199 (1995).
18. De Biasio, R., G. R. Bright, L. A. Ernst, A. S. Waggone , D. L. Taylor: Five-parameters fluorescence imaging: Wound healing cf living Swiss 3T3 cells. J. Cell Biol. 105, 1613-1623 (1987).
19. Doane, K. J., D. E. Birk: Fibroblasts retain their tissue phenotype when grown in three-dimensional collagen gels. Exp. Cell Res. 195, 432-442 (1991).
20. Doillon, C. J., R. M. Hembry, H. P. Ehrlich, J. F. Burke: Actin filaments in normal dermis and during wound healing. Am. J. Pathol. 126, 164-170 (1986).
21. Ehrlich, H. P., J. B. M. Rajaratnam: Cell locomotion forces versus cell contraction forces for collagen lattice contraction: an in vitro model of wound contraction. Tissue and Cell 22, 407-417 (1990).
22. Ehrmann, R. L., G. O. Gey: The growth of cells on a transparent gel of reconstituted rat-tail collagen. J. Natl. Cancer Inst. 16, 1375-1403 (1956).
23. Elsdale, T., J. Bard: Collagen substrata for studies on cell behavior. J. Cell Biol. 54, 626-637 (1972).
24. Ejim, O. S., G. W. Blunn, R. A. Brown: Production of artificial-oriented mats and strands from plasma fibronectin: a morphological study. Biomaterials 14, 743-748 (1993).
25. Estes, J. M., J. S. Vande Berg, N. S. Adzick, T. E. MacGillivray: Phenotypic and functional features of myofibroblasts in sheep fetal wounds. Differentiation 56, 173-181 (1994).
26. Franksson, O., A. Liljeborg, A. Carlsson, P.-O. Forsgren: Confocal laser microscope scanning applied to three-dimensional studies of biological specimens. Proc. Soc. Photo-Optical Eng. 809, 124-129 (1987).
27. Fries, M. K., T. Blieden, R. J. Looney, D. G. Sempowski, M. .R. Silvera, R. A. Willis, R. P. Phipps: Evidence of fibroblast heterogeneity and the role of fibroblast subpopulations in fibrosis. Clin. Immunol. Immunopathol. 72, 283-292 (1994).
28. Gabbiani, G., B. J. Hirschel, B. G. Ryan: Granulation tissue as a contractile organ: A study of structure and function. J. Exp. Med. 135, 719-734 (1972).
29. Garavito, M., J. P. Rosenbusch: Isolation and crystallization of bacterial porin. In: S. Fleischer, B. Fleischer (eds.): Biomembranes. Part M. Methods in Enzymology. Volume 125. pp. 309-329. Academic Press, New York 1986.
30. Giuliano, K. A., D. L. Taylor: Measurement and manipulation of cytoskeletal dynamics in living cells. Curr. Opin. Cell Biol. 7, 4-12 (1995).
31. Grimstone, A. V., A. Klug: Observations on the substructure of flagellar fibers. J. Cell Sci. 1, 351-362 (1966).
32. Grinnell, F.: Fibroblasts, myofibroblasts and wound contraction. J. Cell Biol. 124, 401-404 (1994).
33. Guidry, C., F. Grinnell: Studies on the mechanism of hydrated collagen gel reorganization by human skin fibroblasts. J. Cell Sci. 79, 67-81 (1985).
34. Gundersen, H. J. G.: Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J. Microsc. (Oxf.) 111, 219-223 (1977).
35. Hosoya, N., M. Mitsui, F. Yazama, H. Ishihara, D. J. Hartshorne, H. Mohri: Changes in the cytoskeletal structure of cultured smooth muscle cells induced by calyculin-A. J. Cell Sci. 105, 883-890 (1993).
36. Ingber, D. E.: Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell Sci. 104, 613-627 (1993).
37. Ingber, D. E.: The riddle of morphogenesis: A question of solution chemistry or molecular cell engineering. Cell 75, 1249-1252 (1993).
38. Jester, J. J., W. M. Petroll, P. A. Barry, H. D. Cavanaugh: Temporal, 3-dimensional, cellular anatomy of corneal wound tissue. J. Anat. 186, 301-311 (1995).
39. Jackson, C. L., M. A. Reidy: Basic fibroblast growth factor: Its role in the control of smooth muscle cell migration (Short Communication). Am. J. Pathol. 143, 1024-1031 (1993).
40. Jockusch, B. M., D. F. Brown, H. P. Rusch: Synthesis and some properties of an actin-like nuclear protein in the slime mold Physarum polycephalum. J. Bacteriol. 108, 705-714 (1971).
41. Kakunaga, T.: Neoplastic transformation of human diploid fibroblast cells by chemical carcinogens. Proc. Natl. Acad. Sci. USA 75, 1334-1338 (1978).
42. Kolodney, M. S., R. B. Wisolmerski: Isometric contraction by fibroblasts and endothelial cells in tissue culture: A quantitative study. J. Cell Biol. 117, 73-82 (1992).
43. Krummel, T. M., J. M. Nelson, R. F. Diegelmann, W. J. Lindblad, A. M. Salzberg, L. J. Greenfield, I. K. Cohen: Fetal response to injury in the rabbit. J. Pediatr. Surg. 22, 640-644 (1987).
44. Lazarides, E., K. Weber: Actin antibody: The specific visualization of actin filaments in non-muscle cells. Proc. Natl. Acad. Sci. USA 71, 2268-2272 (1974).
45. Leavitt, J., T. Kakunaga: Expression of a variant form of actin and additional polypeptide changes following chemical-induced in vitro neoplastic transformation of human fibroblasts. J. Biol. Chem. 255, 1650-1661 (1980).
46. Lee, T.-L., Y.-Ch. Lin, K. Mochitate, F. Grinnell: Stress-relaxation of fibroblasts in collagen matrices triggers ectocytosis of plasma membrane vesicles containing actin, annexin II and VI, and β1 integrin receptors. J. Cell Sci. 105, 167-177 (1993).
47. Lucocq, J.: Quantitation of gold labelling and antigens in immunolabelled ultrathin sections. J. Anat. 184, 1-13 (1994).
48. Marks, R., D. Williams, A. D. Pearse: Models for wound healing and disease of skin. In: R. Marks, G. Plewig (eds.): Skin Models. Models to study Function and Disease of Skin. pp. 24-33. Springer-Verlag. Berlin 1986.
49. Martin, P., J. Lewis: Actin cables and epidermal movement in embryonic wound-healing. Nature 360, 179-183 (1992).
50. McCluskey, J., J. Hopkinson-Wooley, B. Luke, P. Martin: A study of wound healing in the E11.5 mouse embryo by light and electron microscopy. Tissue and Cell 25, 173-181 (1993).
51. Mochitate, K., P. Pawelek, F. Grinnell: Stress relaxation of contracted gels: Disruption of actin bundles, release of cell surface fibronectin, and down-regulation of DNA and protein synthesis. Exp. Cell Res. 193, 198-202 (1991).
52. Monical, P., N. A. Kefalides: Coculture modulates laminin synthesis and mRNA levels in epidermal keratinocytes and dermal fibroblasts. Exp. Cell Res. 210, 154-159 (1994).
53. Nakagawa, S., P. Pawelek, F. Grinnell: Extracellular matrix organization modulates fibroblast growth and growth factor responsiveness. Exp. Cell Res. 182, 572-582 (1989).
54. Nakagawa, S., P. Pawelek, F. Grinnell: Long-term culture of fibroblasts in contracted collagen gels: effects on cell growth and biosynthetic activity. J. Invest. Dermatol. 93, 792-798 (1989).
55. Nishiyama, T., N. Tominaga, K. Nakajima, T. Hayashi: Quantitative evaluation of the factors affecting the process of fibroblast-mediated collagen gel contraction by separating the process into three phases. Collagen Relat. Res. 8, 259-273 (1988).
56. Nishiyama, T., M. Tsunenaga, Y. Nakayama, E. Adachi, T. Hayashi: Growth rate of human fibroblasts is repressed by the culture within reconstituted collagen matrix but not by the culture on the matrix. Matrix 9, 193-199 (1989).
57. Nusgen, B., Ch. Merrill, Ch. Lapiere, E. Bell: Collagen biosynthesis by cells in a tissue equivalent matrix in vitro. Collagen Relat. Res. 4, 351-364 (1984).
58. Oakely, C., D. M. Brunette: The sequence of alignment of microtubules, focal contacts and actin filaments in fibroblasts spreading on smooth and grooved titanium substrata. J. Cell Sci. 106, 343-354 (1993).
59. Petroll, W. M., H. D. Cavanaugh, P. Barry, P. Andrews, J. V. Jester: Quantitative analysis of stress fiber orientation during corneal wound contraction. J. Cell Sci. 104, 353-363 (1993).
60. Rheinwald, J. G., H. Green: Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6, 331-344 (1975).
61. Ross, R.: The fibroblast and wound repair. Biol. Rev. 43, 51-96 (1968).
62. Rudolph, R., J. Van de Berg, G. F. Pierce: Changing concepts in myofibroblast function and control. In: H. Janssen, R. Rooman, J. I. S. Robertson (eds.): Wound Healing, pp. 103-115. Wrightson Biomedical Publishing Ltd. Petersfield, UK 1991.
63. Saiag, P., B. Coulomb, C. Lebreton, E. Bell, L. Dubertret: Psoriatric fibroblasts induce hyperproliferation of normal keratinocytes in a skin equivalent model in vitro. Science 230, 669-672 (1985).
64. Sappino, A. P., W. Schürch, G. Gabbiani: Differentiation repertoire of fibroblastic cells: Expression of cytoskeletal proteins as markers of phenotypic modulations. Lab. Invest. 63, 144-161 (1990).
65. Sarber, R., B. Hull, Ch. Merrill, Th. Soranno, E. Bell: Regulation of proliferation of fibroblasts of low and of high population doubling levels grown in collagen lattices. Mech. Ageing Dev. 17, 107-117 (1981).
66. Schreier, T., E. Degen, W. Baschong: Fibroblast migration and proliferation during in vitro wound-healing. A quantitative comparison between various growth factors and a low molecular weight blood dialysate used in the clinic to normalize impaired wound healing. Res. Exp. Med. 193, 195-205 (1993).
67. Skalli, O., G. Gabbiani: The biology of the myofibroblast: relationship to wound contraction and fibrocontractive diseases. In: R. A. F. Clark, P. M. Henson (eds.): The Molecular and Cellular Biology of Wound Repair. pp. 373-402. Plenum Publ. Corp. New York 1988.
68. Small, J. V., J. E. Celis: Direct visualization of the 10 nm (100 Å)-filament network in whole and enucleated cultured cells. J. Cell Sci. 31, 393-409 (1978).
69. Steinberg, B. M., K. Smith, M. Colozzo, R. Pollack: Establishment and transformation diminish the ability of fibroblasts to contract a native collagen gel. J. Cell Biol. 87, 304-308 (1980).
70. Thie, M., W. Schlumberger, J. Rauterberg, H. Robenek: Mechanical confinement inhibits collagen synthesis in gel-cultured fibroblasts. Eur. J. Cell Biol. 48, 294-302 (1989).
71. Todaro, G. J., G. Lazar, H. Green: The initiation of cell division in a contact-inhibited mammalian cell line. J. Cell. Comp. Physiol. 66, 325-333 (1965).
72. Tomasek, J. J., E. D. Hay: Analysis of the role of microfilaments and microtubules in acquisition of bipolarity and elongation of fibroblasts in hydrated collagen gels. J. Cell Biol. 99, 536-549 (1984).
73. Tomasek, J. J., C. J. Haaksma, R. J. Eddy, M. B. Vaughan: Fibroblast contraction occurs on release of tension in attached collagen lattices: Dependency on an organized actin cytoskeleton and serum. Anat. Rec. 232, 359-368 (1992).
74. Tsuboi, K., S. Yamaoka, M. Maki, G. Oshio, T. Tobe, M. Hatanaka: Soluble factors including proteinases released from damaged cells may trigger the wound healing process. Biochem. Biophys. Res. Commun. 168, 1163-1170 (1990).
75. Unemori, E. N., Z. Werb: Reorganization of polymerized actin: A possible trigger for induction of procollagenase in fibroblasts cultured in and on collagen gels. J. Cell Biol. 103, 1021-1031 (1986).
76. Vasiliev, J. M., I. M. Gelfand, L. V. Domnina, R. I. Rappoport: Wound healing processes in cell cultures. Exp. Cell Res. 54, 83-93 (1969).
77. Wang, N., J. P. Butler, D. E. Ingber: Mechanotranuction across the cell surface and through the cytoskeleton. Science 260, 1124-1127 (1993).
78. Watson, P. A.: Function follows form: generation of intracellular signals by cell deformation. FASEB J. 5, 2013-2019 (1991).
79. Weiss, P., B. Garber: Shape and movement of mesenchymal cells as functions of the physical structure of the medium. Contributions to a quantitative morphology. Proc. Natl. Acad. Sci. USA 83, 264-280 (1952).
80. Weiss, P.: The biological foundations of wound repair. Harvey Lect. 55, 13-42 (1959).
81. Whitby, D. J., M. J. Ferguson: The extracellular matrix of lip wounds in fetal, neonatal and adult mice. Development 112, 651-668 (1991).
82. Wokalek, H.: Cellular events in wound healing. Crit. Rev. Biocompatibil. 4, 209-246 (1988).
83. Wokalek, H., H. Ruh: Time course of wound healing. J. Biomat. Applic. 5, 337-362 (1991).