|
Sign In to gain access to subscriptions and/or personal tools.
|
A Comparison of the Ability of Intra-oral and Extra-oral Fibroblasts to Stimulate Extracellular Matrix Reorganization in a Model of Wound Contraction
P. Stephens
Department of Oral Surgery, Medicine and Pathology, Dental School, University of Wales College of Medicine, Heath Park, Cardiff CF4 4XY, United Kingdom
K.J. Davies
Department of Oral Surgery, Medicine and Pathology, Dental School, University of Wales College of Medicine, Heath Park, Cardiff CF4 4XY, United Kingdom
T. Al-Khateeb
Department of Oral Surgery, Medicine and Pathology, Dental School, University of Wales College of Medicine, Heath Park, Cardiff CF4 4XY, United Kingdom
J.P. Shepherd
Department of Oral Surgery, Medicine and Pathology, Dental School, University of Wales College of Medicine, Heath Park, Cardiff CF4 4XY, United Kingdom
D.W. Thomas
Department of Oral Surgery, Medicine and Pathology, Dental School, University of Wales College of Medicine, Heath Park, Cardiff CF4 4XY, United Kingdom
Intra-oral wounds, like wounds in children, demonstrate privileged healing when compared with adult wounds at extra-oral sites. This study investigated whether this preferential healing is related to an increased ability of oral mucosal fibroblasts to reorganize extracellular matrix (ECM) when compared with their dermal counterparts. ECM reorganization was investigated by means of a fibroblast-populated collagen lattice (FPCL) system. The effect of donor age was also investigated in this system. Differences in ECM reorganization and FPCL contraction were evident: FPCL contraction was more rapid by oral mucosal fibroblasts than dermal fibroblasts (p < 0.01). FPCL contraction was also greater in child (donor < 10 years) than adult (donor > 18 years) oral mucosal fibroblasts (p < 0.01). These differences were not related to phenotypic differences in cell viability (p > 0.5), DNA synthesis (p > 0.05), and cell number (p > 0.5) within the FPCLs, or cellular attachment to collagen (p > 0.07). FPCL contraction was not stimulated by the addition of conditioned medium from oral mucosal or dermal fibroblasts (p > 0.05). These data show that the significantly increased ability of oral mucosal fibroblasts to reorganize ECM in vitro, when compared with dermal fibroblasts, represents a distinct phenotypic contractile difference, rather than differences in their production of soluble mediators or cell attachment to ECM.
Key Words: collagen lattice contraction fibroblasts wound healing
REFERENCES
- Asaga H., Kikuchi S., Yoshizato K. (1991). Collagen gel contraction by fibroblasts requires cellular fibronectin but not plasma fibronectin. Exp Cell Res 193:167-174.[CrossRef][Medline]
[Order article via Infotrieve]
- Aumailley M., Mann K., von der Mark H., Timpl R. (1989). Cell attachment properties of collagen type VI and arg-gly-asp dependent binding to its a2(VI) and a3(VI) chains. Exp Cell Res 181:463-474.[CrossRef][Medline]
[Order article via Infotrieve]
- Bell E., Ivarsson B., Merrill C. (1979). Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci USA 76:1274-1278.[Abstract/Free Full Text]
- Bellows CG, Melcher AH, Aubin JE (1981). Contraction and organization of collagen gels by cells cultured from periodontal ligament, gingiva and bone suggest functional differences between cell types. J Cell Sci 50:299-314.[Abstract]
- Bellows CG, Melcher AH, Aubin JE (1983). An in vitro model for tooth eruption utilizing periodontal ligament fibroblasts and collagen lattices. Arch Oral Biol 28:715-722.[Medline]
[Order article via Infotrieve]
- Burd DAR, Longaker MT, Rittenberg T., Adzick NS, Harrison MR, Ehrlich HP (1991). In vitro foetal wound contraction: the effect of amniotic fluid. Br J Plast Surg 44:302-305.[Medline]
[Order article via Infotrieve]
- Ehrlich HP, Rajaratnam JBM (1990). Cell locomotion forces versus cell contraction forces for collagen lattice contraction: an in vitro model of wound contraction. Tissue Cell 22:407-417.[CrossRef][Medline]
[Order article via Infotrieve]
- Ehrlich HP, Buttle DJ, Bernanke DH (1989). Physiological variables affecting collagen lattice contraction by human dermal fibroblasts. Exp Molec Pathol 50:220-229.[Medline]
[Order article via Infotrieve]
- Gibson JM, Milam SB, Klebe RJ (1989). Late passage cells display an increase in contractile behaviour. Mech Ageing Dev 48:101-110.[Medline]
[Order article via Infotrieve]
- Guidry C., Grinnell F. (1985). Studies on the mechanism of hydrated collagen gel reorganization by human skin fibroblasts. J Cell Sci 79:67-81.[Abstract]
- Harris AK, Wild P., Stopak D. (1980). Silicone rubber substrate: a new wrinkle in the study of cell locomotion. Science 208:177-179.[Abstract/Free Full Text]
- High AS, Robinson PA (1994). Differences in adhesion and collagen gel contraction between fibroblasts from various types of odontogenic cyst. Arch Oral Biol 39:387-393.[CrossRef][Medline]
[Order article via Infotrieve]
- Irwin CR, Picardo M., Ellis I., Sloan P., Grey A., McGurk M., et al. (1994). Inter- and intra-site heterogeneity in the expression of fetal-like phenotypic characteristics by gingival fibroblasts: potential significance for wound healing. J Cell Sci 107:1333-1346.[Abstract]
- Kasugai S., Ogura H. (1993). The effects of cytoskeletal inhibitors on the collagen gel contraction by dog periodontal ligament fibroblasts in vitro. Arch Oral Biol 38:785-792.[Medline]
[Order article via Infotrieve]
- Kasugai S., Suzuki S., Shibata S., Yasui S., Amano H., Ogura H. (1990). Measurements of the isometric contractile forces generated by dog periodontal ligament fibroblasts in vitro. Arch Oral Biol 35:597-601.[CrossRef][Medline]
[Order article via Infotrieve]
- Longaker MT, Adzick NS (1991). The biology of fetal wound healing: a review. Plast Reconstr Surg 87:788-798.[CrossRef][Medline]
[Order article via Infotrieve]
- Nakagawa S., Pawelek P., Grinnell F. (1989a). Long-term culture of fibroblasts in contracted collagen gels: effects on cell growth and biosynthetic activity. J Invest Dermatol 93:792-798.[CrossRef][Medline]
[Order article via Infotrieve]
- Nakagawa S., Pawelek P., Grinnell F. (1989b). Extracellular matrix organization modulates fibroblasts growth and growth factor responsiveness. Exp Cell Res 182:572-582.[CrossRef][Medline]
[Order article via Infotrieve]
- Nishiyama T., Tominaga N., Nakajima K., Hayashi T. (1988). Quantitative evaluation of the factors affecting the process of fibroblast-mediated collagen gel contraction by separating the process into three phases. Collagen Rel Res 8:259-273.
- Pitaru S., Soldinger M., Madgar D., Metzger Z. (1987). Bacterial endotoxin inhibits migration, attachment, and orientation of human gingival fibroblasts in vitro and delays collagen gel contraction. J Dent Res 66:1449-1455.
- Rittenberg T., Longaker MT, Adzick NS, Ehrlich HP (1991). Sheep amniotic fluid has a protein factor which stimulates human fibroblast populated collagen lattice contraction. J Cell Physiol 149:444-450.[Medline]
[Order article via Infotrieve]
- Rowling PJ, Raxworthy MJ, Wood EJ, Kearney JN, Cunliffe WJ (1990). Fabrication and reorganization of dermal equivalents suitable for skin grafting after major cutaneous injury. Biomaterials 11:181-185.
- Schafer IA, Shapiro A., Kovach M., Lang C., Fratianne RB (1989). The interaction of human papillary and reticular fibroblasts and human keratinocytes in the contraction of three-dimensional floating collagen lattices. Exp Cell Res 183:112-125.[CrossRef][Medline]
[Order article via Infotrieve]
- Sharaf MN, Page RC ( 1988). Contraction of collagen gels by fibroblasts cultured from normal and inflamed gingivae. Dtsch Zahnärztl Z 43:693-695.[Medline]
[Order article via Infotrieve]
- Shimizu K., Yoshizato S. (1992). Organ-dependent expression of differentiated states in fibroblasts cultured in vitro. Dev Growth Differ 34:43-50.[Medline]
[Order article via Infotrieve]
- Sloan P. (1991). Current concepts of the role of fibroblasts and extracellular matrix in wound healing and their relevance to oral implantology. J Dent 19:107-109.[Medline]
[Order article via Infotrieve]
- Souren JM, Ponec M., van Wijk R. (1989). Contraction of collagen by human fibroblasts and keratinocytes. In Vitro Cell Dev Biol 25:1039-1045.[Medline]
[Order article via Infotrieve]
- Thomas DW, Hopkinson I., Harding KG, Shepherd JP (1994). The pathogenesis of hypertrophic and keloid scarring. Int J Oral Maxillofac Surg 23:232-236.[Medline]
[Order article via Infotrieve]
- Tiollier J., Dumas H., Tardy M., Tayot J.-L (1990). Fibroblast behaviour on gels of type 1, III, and IV human placental collagens. Exp Cell Res 191:95-104.[CrossRef][Medline]
[Order article via Infotrieve]
- Tomasek JJ, Akiyama SK (1992). Fibroblast-mediated collagen gel contraction does not require fibronectin alpha 5 beta 1 integrin interaction. Anat Rec 234:153-160.[CrossRef][Medline]
[Order article via Infotrieve]
- Tomasek JJ, Haaksma CJ, Eddy RJ, Vaughan MB (1992). Fibroblast contraction occurs on release of tension in attached collagen lattices: dependency on an organized actin cytoskeleton and serum. Anat Rec 232:359-368.[CrossRef][Medline]
[Order article via Infotrieve]
- Weinberg CB, Bell E. ( 1985). Regulation of proliferation of bovine aortic endothelial cells, smooth muscle cells, and adventitial fibroblasts in collagen lattices. J Cell Physiol 122:410-414.[CrossRef][Medline]
[Order article via Infotrieve]
- Whitby DJ, Ferguson MWJ (1991). The extracellular matrix of lip wounds in fetal, neonatal and adult mice. Development 112:651-668.[Abstract]
- Yamato M., Yamamoto K., Hayashi T. (1993). Age-related changes in collagen contraction by cultured human lung fibroblasts resulting in cross-over of contraction curves between young and aged cells. Mech Ageing Dev 67:149-158.[Medline]
[Order article via Infotrieve]
Journal of Dental Research, Vol. 75, No. 6,
1358-1364 (1996)
DOI: 10.1177/00220345960750060601

CiteULike Complore Connotea Del.icio.us Digg Reddit Technorati Twitter What's this?
This article has been cited by other articles:

|
 |

|
 |
 
S. Enoch, I. Wall, M. Peake, L. Davies, J. Farrier, P. Giles, D. Baird, D. Kipling, P. Price, R. Moseley, et al.
Increased Oral Fibroblast Lifespan Is Telomerase-independent
Journal of Dental Research,
October 1, 2009;
88(10):
916 - 921.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Meran, D. W. Thomas, P. Stephens, S. Enoch, J. Martin, R. Steadman, and A. O. Phillips
Hyaluronan Facilitates Transforming Growth Factor-{beta}1-mediated Fibroblast Proliferation
J. Biol. Chem.,
March 7, 2008;
283(10):
6530 - 6545.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Meran, D. Thomas, P. Stephens, J. Martin, T. Bowen, A. Phillips, and R. Steadman
Involvement of Hyaluronan in Regulation of Fibroblast Phenotype
J. Biol. Chem.,
August 31, 2007;
282(35):
25687 - 25697.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Stephens, P. Grenard, P. Aeschlimann, M. Langley, E. Blain, R. Errington, D. Kipling, D. Thomas, and D. Aeschlimann
Crosslinking and G-protein functions of transglutaminase 2 contribute differentially to fibroblast wound healing responses
J. Cell Sci.,
July 1, 2004;
117(15):
3389 - 3403.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Sukotjo, A. Lin, K. Song, T. Ogawa, B. Wu, and I. Nishimura
Oral Fibroblast Expression of wound-inducible transcript 3.0 (wit3.0) Accelerates the Collagen Gel Contraction in Vitro
J. Biol. Chem.,
December 19, 2003;
278(51):
51527 - 51534.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|