A simple cell motility assay demonstrates differential motility of human periodontal ligament fibroblasts, gingival fibroblasts, and pre-osteoblasts

Cell and Tissue Research

Volumn 328, Issue 2, 2007, Pages 339-354

  Lallier, Thomas E ^a   Miner Jr , Quinton W ^b   Sonnier, Jackie ^a   Spencer, Amber ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Collagen type I; Collagen type III; Collagen type V; Gingival fibroblast; Human; Integrin; Osteoblast; Periodontal ligament fibroblast

Indexed keywords

ALPHA1 INTEGRIN; ALPHA10 INTEGRIN; ALPHA11 INTEGRIN; ALPHA2 INTEGRIN; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE 4; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL ASSAY; CELL GROWTH; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; COMPARATIVE STUDY; CONNECTIVE TISSUE; CONTROLLED STUDY; FETUS; FIBROBLAST; GINGIVA; HUMAN; HUMAN CELL; NORMAL HUMAN; OSTEOBLAST; PERIODONTAL LIGAMENT; PERIODONTIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE REGENERATION;

BIOLOGICAL ASSAY; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; COLLAGEN; CONTACT INHIBITION; EXTRACELLULAR MATRIX; FIBROBLASTS; GINGIVA; HUMANS; INTEGRINS; OSTEOBLASTS; PERIODONTAL LIGAMENT; PROTEIN SUBUNITS; SUBSTRATE SPECIFICITY;

EID: 33947377114     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-006-0372-4     Document Type: Article

References (71)

1. Akizuki T, Oda S, Komaki M, Tsuchioka H, Kawakatsu N, Kikuchi A, Yamato M, Okano T, Ishikawa I (2005) Application of periodontal ligament cell sheet for periodontal regeneration: a pilot study in beagle dogs. J Periodontal Res 40:245-251
2. Alliot-Licht B, De Lange GL, Gregoire M (1997) Effects of hydroxyapatite particles on periodontal ligament fibroblast-like cell behavior. J Periodontol 68:158-165
3. Badylak SF (2002) The extracellular matrix as a scaffold for tissue reconstruction. Semin Cell Dev Biol 13:377-383
4. Bartold PM, Walsh LJ, Narayanan AS (2000) Molecular and cell biology of the gingiva. Periodontol 2000 24:28-55
5. Bengtsson T, Aszodi A, Nicolae C, Hunziker EB, Lundgren-Akerlund E, Fassler R (2005) Loss of alpha10beta1 integrin expression leads to moderate dysfunction of growth plate chondrocytes. J Cell Sci 118:929-936
6. Bernick S, Paule W, Ertl D, Nishimoto SK, Nimni ME (1989) Cellular events associated with the induction of bone by demineralized bone. J Orthop Res 7:1-11
7. Bland YS, Ashhurst DE (1996) Changes in the distribution of fibrillar collagens in the collateral and cruciate ligaments of the rabbit knee joint during fetal and postnatal development. Histochem J 28:325-334
8. Bumann A, Carvalho RS, Schwarzer CL, Yen EH (1997) Collagen synthesis from human PDL cells following orthodontic tooth movement. Eur J Orthod 19:29-37
9. Butler WT, Birkedal-Hansen H, Beegle WF, Taylor RE, Chung E (1975) Proteins of the periodontium. Identification of collagens with the [alpha1(I)]2alpha2 and [alpha1(III)]3 structures in bovine periodontal ligament. J Biol Chem 250:8907-8912
10. Camper L, Hellman U, Lundgren-Akerlund E (1998) Isolation, cloning, and sequence analysis of the integrin subunit alpha10, a beta1-associated collagen binding integrin expressed on chondrocytes. J Biol Chem 273:20383-20389
11. Camper L, Holmvall K, Wangnerud C, Aszodi A, Lundgren-Akerlund E (2001) Distribution of the collagen-binding integrin alpha10-beta1 during mouse development. Cell Tissue Res 306:107-116
12. Caton J, Greenstein G, Zappa U (1992) Guided tissue regeneration using Vicryl periodontal mesh. Compendium 13:202-208
13. Elices MJ, Hemler ME (1989) The human integrin VLA-2 is a collagen receptor on some cells and a collagen/laminin receptor on others. Proc Natl Acad Sci USA 86:9906-9910
14. Fernyhough W, Page RC (1983) Attachment, growth and synthesis by human gingival fibroblasts on demineralized or fibronectin-treated normal and diseased tooth roots. J Periodontol 54:133-140
15. Gaunt WA, Osborn JW, TenCate AR (1971) The Periodontal Ligament. Advanced Dental Histology. Williams and Wilins, Baltimore
16. Giannopoulou C, Cimasoni G (1996) Functional characteristics of gingival and periodontal ligament fibroblasts. J Dent Res 75:895-902
17. Groeneveld MC, Everts V, Beertsen W (1995) Alkaline phosphatase activity in the periodontal ligament and gingiva of the rat molar: its relation to cementum formation. J Dent Res 74:1374-1381
18. Hallman M, Lundgren S, Sennerby L (2001) Histologic analysis of clinical biopsies taken 6 months and 3 years after maxillary sinus floor augmentation with 80% bovine hydroxyapatite and 20% autogenous bone mixed with fibrin glue. Clin Implant Dent Relat Res 3:87-96
19. Harris SA, Enger RJ, Riggs BL, Spelsberg TC (1995) Development and characterization of a conditionally immortalized human fetal osteoblastic cell line. J Bone Miner Res 10:178-186
20. Hasegawa M, Yamato M, Kikuchi A, Okano T, Ishikawa I (2005) Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. Tissue Eng 11:469-478
21. Hay ED (1981) Extracellular matrix. J Cell Biol 91:205s-223s
22. Hou LT, Liu CM, Wong MY (1995) Expression of matrix proteins in cloned fibroblasts derived from periodontal tissue under different cell growth densities. Proc Natl Sci Counc Repub China [B] 19:176-184
23. Hou LT, Yaeger JA (1993) Cloning and characterization of human gingival and periodontal ligament fibroblasts. J Periodontol 64:1209-1218
24. Kerkvliet EH, Jansen IC, Schoenmaker T, Beertsen W, Everts V (2003) Collagen type I, III and V differently modulate synthesis and activation of matrix metalloproteinases by cultured rabbit periosteal fibroblasts. Matrix Biol 22:217-227
25. Kim JK, Xu Y, Xu X, Keene DR, Gurusiddappa S, Liang X, Wary KK, Hook M (2005) A novel binding site in collagen type III for integrins alpha1beta1 and alpha2beta1. J Biol Chem 280:32512-32520
26. Klekotka PA, Santoro SA, Wang H, Zutter MM (2001) Specific residues within the alpha 2 integrin subunit cytoplasmic domain regulate migration and cell cycle progression via distinct MAPK pathways. J Biol Chem 276:32353-32361
27. Kreis S, Schonfeld HJ, Melchior C, Steiner B, Kieffer N (2005) The intermediate filament protein vimentin binds specifically to a recombinant integrin alpha2/beta1 cytoplasmic tail complex and co-localizes with native alpha2/beta1 in endothelial cell focal adhesions. Exp Cell Res 305:110-121
28. Kuru L, Griffiths GS, Petrie A, Olsen I (1999) Alkaline phosphatase activity is upregulated in regenerating human periodontal cells. J Periodontal Res 34:123-127
29. Lallier T, Bronner-Fraser M (1992) Alpha 1 beta 1 integrin on neural crest cells recognizes some laminin substrata in a Ca(2+)-independent manner. J Cell Biol 119:1335-1345
30. Lallier TE, Spencer A, Fowler MM (2005) Transcript profiling of periodontal fibroblasts and osteoblasts. J Periodontol 76:1044-1055
31. Lekic P, Sodek J, McCulloch CA (1996) Osteopontin and bone sialoprotein expression in regenerating rat periodontal ligament and alveolar bone. Anat Rec 244:50-58
32. Lochter A, Navre M, Werb Z, Bissell MJ (1999) Alpha1 and alpha2 integrins mediate invasive activity of mouse mammary carcinoma cells through regulation of stromelysin-1 expression. Mol Biol Cell 10:271-282
33. Martin M, Gantes B, Garrett S, Egelberg J (1988) Treatment of periodontal furcation defects. I. Review of the literature and description of a regenerative surgical technique. J Clin Periodontol 15:227-231
34. Nanci A, Bosshardt DD (2006) Structure of periodontal tissues in health and disease. Periodontol 2000 40:11-28
35. Narayanan AS, Page RC (1983a) Biosynthesis and regulation of type V collagen in diploid human fibroblasts. J Biol Chem 258:11694-11699
36. Narayanan AS, Page RC (1983b) Connective tissues of the periodontium: a summary of current work. Coll Relat Res 3:33-64
37. Nguyen L, Lekic P, McCulloch CA (1997) Collagen implants do not preserve periodontal ligament homeostasis in periodontal wounds. J Periodontal Res 32:419-429
38. Nishimura F, Terranova VP (1996) Comparative study of the chemotactic responses of periodontal ligament cells and gingival fibroblasts to polypeptide growth factors. J Dent Res 75:986-992
39. Niyibizi C, Kavalkovich K, Yamaji T, Woo SL (2000) Type V collagen is increased during rabbit medial collateral ligament healing. Knee Surg Sports Traumatol Arthrosc 8:281-285
40. Ohshima M, Kuwata F, Otsuka K, Saito R, Sato K, Shioji S, Suzuki K (1988) Alkaline phosphatase activities of cultured human periodontal ligament cells. J Nihon Univ Sch Dent 30:208-217
41. Palaiologou AA, Yukna RA, Moses R, Lallier TE (2001) Gingival, dermal, and periodontal ligament fibroblasts express different extracellular matrix receptors. J Periodontol 72:798-807
42. Popova SN, Rodriguez-Sanchez B, Liden A, Betsholtz C, Van Den Bos T, Gullberg D (2004) The mesenchymal alpha11beta1 integrin attenuates PDGF-BB-stimulated chemotaxis of embryonic fibroblasts on collagens. Dev Biol 270:427-442
43. Rao LG, Wang HM, Kalliecharan R, Heersche JN, Sodek J (1979) Specific immunohistochemical localization of type I collagen in porcine periodontal tissues using the peroxidase-labelled antibody technique. Histochem J 11:73-82
44. Reddi AH (1981) Cell biology and biochemistry of endochondral bone development. Coll Relat Res 1:209-226
45. Riikonen T, Vihinen P, Potila M, Rettig W, Heino J (1995) Antibody against human alpha 1 beta 1 integrin inhibits HeLa cell adhesion to laminin and to type I, IV, and V collagens. Biochem Biophys Res Commun 209:205-212
46. Robinson KA, Li J, Mathison M, Redkar A, Cui J, Chronos NA, Matheny RG, Badylak SF (2005) Extracellular matrix scaffold for cardiac repair. Circulation 112:I135-I143
47. Romanos GE, Schroter-Kermani C, Hinz N, Wachtel HC, Bernimoulin JP (1991) Immunohistochemical localization of collagenous components in healthy periodontal tissues of the rat and marmoset (Callithrix jacchus). II. Distribution of collagen types IV, V and VI. J Periodontal Res 26:323-332
48. Saelman EU, Nieuwenhuis HK, Hese KM, de Groot PG, Heijnen HF, Sage EH, Williams S, McKeown L, Gralnick HR, Sixma JJ (1994) Platelet adhesion to collagen types I through VIII under conditions of stasis and flow is mediated by GPIa/IIa (alpha 2 beta 1-integrin). Blood 83:1244-1250
49. Schon M, Schon MP, Kuhrober A, Schirmbeck R, Kaufmannn R, Klein CE (1996) Expression of the human alpha2 integrin subunit in mouse melanoma cells confers the ability to undergo collagen-directed adhesion, migration and matrix reorganization. J Invest Dermatol 106:1175-1181
50. Senger DR, Claffey KP, Benes JE, Perruzzi CA, Sergiou AP, Detmar M (1997) Angiogenesis promoted by vascular endothelial growth factor: regulation through alpha1beta1 and alpha2beta1 integrins. Proc Natl Acad Sci USA 94:13612-13617
51. Shimomura T, Jia F, Niyibizi C, Woo SL (2003) Antisense oligonucleotides reduce synthesis of procollagen alpha1 (V) chain in human patellar tendon fibroblasts: potential application in healing ligaments and tendons. Connect Tissue Res 44:167-172
52. Somerman MJ, Archer SY, Imm GR, Foster RA (1988) A comparative study of human periodontal ligament cells and gingival fibroblasts in vitro. J Dent Res 67:66-70
53. Steffensen B, Duong AH, Milam SB, Potempa CL, Winborn WB, Magnuson VL, Chen D, Zardeneta G, Klebe RJ (1992) Immunohistological localization of cell adhesion proteins and integrins in the periodontium. J Periodontol 63:584-592
54. Strayhorn CL, Garrett JS, Dunn RL, Benedict JJ, Somerman MJ (1999) Growth factors regulate expression of osteoblast-associated genes. J Periodontol 70:1345-1354
55. Takada Y, Wayner EA, Carter WG, Hemler ME (1988) Extracellular matrix receptors, ECMRII and ECMRI, for collagen and fibronectin correspond to VLA-2 and VLA-3 in the VLA family of heterodimers. J Cell Biochem 37:385-393
56. Takeshita A, Niu ZG, Hanazawa S, Takara I, Higuchi H, Katayama I, Kitano S (1992) Effect of interleukin-1 beta on gene expressions and functions of fibroblastic cells derived from human periodontal ligament. J Periodontal Res 27:250-255
57. Takiguchi T, Kobayashi M, Nagashima C, Yamaguchi A, Nishihara T, Hasegawa K (1999) Effect of prostaglandin E2 on recombinant human bone morphogenetic protein-2-stimulated osteoblastic differentiation in human periodontal ligament cells. J Periodontal Res 34:431-436
58. Tardieu-Moreau C, Pourreau-Schneider N, Colomb E, Kopp F, Martin PM, Franquin JC (1992) Effects of culture passages on collagen immunostaining in human dental pulp and gingival fibroblasts. J Biol Buccale 20:169-174
59. Tenenbaum HC (1990) Cellular origins and theories of differentiation of bone-forming cells. In: Hall BK (ed) Bone, vol 1. The osteoblast and osteocyte. Telford, New Jersey, pp 41-69
60. Tiger CF, Fougerousse F, Grundstrom G, Velling T, Gullberg D (2001) Alpha11beta1 integrin is a receptor for interstitial collagens involved in cell migration and collagen reorganization on mesenchymal nonmuscle cells. Dev Biol 237:116-129
61. Tung PS, Domenicucci C, Wasi S, Sodek J (1985) Specific immunohistochemical localization of osteonectin and collagen types I and III in fetal and adult porcine dental tissues. J Histochem Cytochem 33:531-540
62. Urabe M, Hosokawa R, Chiba D, Sato Y, Akagawa Y (2000) Morphogenetic behavior of periodontium on inorganic implant materials: an experimental study of canines. J Biomed Mater Res 49:17-24
63. Urist MR, DeLange RJ, Finerman GA (1983) Bone cell differentiation and growth factors. Science 220:680-686
64. Velling T, Risteli J, Wennerberg K, Mosher DF, Johansson S (2002) Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J Biol Chem 277:37377-37381
65. Vihinen P, Riikonen T, Laine A, Heino J (1996) Integrin alpha 2 beta 1 in tumorigenic human osteosarcoma cell lines regulates cell adhesion, migration, and invasion by interaction with type I collagen. Cell Growth Differ 7:439-447
66. Wang HM, Nanda V, Rao LG, Melcher AH, Heersche JN, Sodek J (1980) Specific immunohistochemical localization of type III collagen in porcine periodontal tissues using the peroxidase-antiperoxidase method. J Histochem Cytochem 28:1215-1223
67. Werfully S, Areibi G, Toner M, Bergquist J, Walker J, Renvert S, Claffey N (2002) Tensile strength, histological and immunohistochemical observations of periodontal wound healing in the dog. J Periodontal Res 37:366-374
68. Wikesjo UM, Nilveus RE, Selvig KA (1992) Significance of early healing events on periodontal repair: a review. J Periodontol 63:158-165
69. Yamaguchi M, Shimizu N, Shibata Y, Abiko Y (1996) Effects of different magnitudes of tension-force on alkaline phosphatase activity in periodontal ligament cells. J Dent Res 75:889-894
70. Zantop T, Gilbert TW, Yoder MC, Badylak SF (2006) Extracellular matrix scaffolds are repopulated by bone marrow-derived cells in a mouse model of Achilles tendon reconstruction. J Orthop Res 24:1299-1309
71. Zhou H, Kramer RH (2005) Integrin engagement differentially modulates epithelial cell motility by RhoA/ROCK and PAK1. J Biol Chem 280:10624-10635