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Erschienen in: Anatomical Science International 2/2016

01.03.2016 | Original Article

Immunohistochemical localization of tenascin-C in rat periodontal ligament with reference to alveolar bone remodeling

verfasst von: Rei Sato, Hiroki Fukuoka, Tamaki Yokohama-Tamaki, Masaru Kaku, Shunichi Shibata

Erschienen in: Anatomical Science International | Ausgabe 2/2016

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Abstract

We investigated the immunohistochemical localization of tenascin-C in 8-week-old rat periodontal ligaments. Tenascin-C immunoreactivity was detected in zones along with cementum and alveolar bone, and more intensely on the resorption surface of alveolar bone than on the formation surface. On the resorbing surface, tenascin-C immunoreactivity was detected in Howship’s lacunae without osteoclasts, and in the interfibrous space of the periodontal ligaments, indicating that this molecule works as an adhesion molecule between bone and fibers of periodontal ligaments. Upon experimental tooth movement by inserting elastic bands (Waldo method), the physiological resorption surface of alveolar bone under compressive force showed enhanced bone resorption and enhanced tenascin-C immunoreactivity. However, on the physiological bone formation surface under compressive force, bone resorption was seen only occasionally, and no enhanced tenascin-C immunoreactivity was noted. In an experiment involving excessive occlusal loading to rat molars, transient bone resorption occurred within interradicular septa, but no enhanced tenascin-C immunoreactivity was seen in the periodontal ligaments. These results indicate that tenascin-C works effectively on the bone resorbing surface of physiological alveolar bone remodeling sites, rather than on the non-physiological transient bone resorbing surface. Fibronectin immunoreactivity was distributed evenly in the periodontal ligaments under experimental conditions. Co-localization of tenascin-C and fibronectin immunoreactivity was observed in many regions, but mutually exclusive expression patterns were also seen in some regions, indicating that fibronectin might not be directly involved in alveolar bone remodeling, but may play a role via interaction with tenascin-C.
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Literatur
Zurück zum Zitat Chiquet M, Fambrough DM (1984) Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol 98:1926–1936CrossRefPubMed Chiquet M, Fambrough DM (1984) Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol 98:1926–1936CrossRefPubMed
Zurück zum Zitat Chiquet-Ehrismann R, Peter Kalla P, Pearson CA, Beck K, Chiquet M (1988) Tenascin interferes with fibronectin action. Cell 53:383–390CrossRefPubMed Chiquet-Ehrismann R, Peter Kalla P, Pearson CA, Beck K, Chiquet M (1988) Tenascin interferes with fibronectin action. Cell 53:383–390CrossRefPubMed
Zurück zum Zitat Enlow DH (1982) Handbook of facial growth, 2nd edn. Saunders, Philadelphia, pp 367–418 Enlow DH (1982) Handbook of facial growth, 2nd edn. Saunders, Philadelphia, pp 367–418
Zurück zum Zitat Erickson HP (1993) Tenascin-C, tenascin-R, and tenascin-X: a family of talented proteins in search of functions. Curr Opin Cell Biol 5:869–876CrossRefPubMed Erickson HP (1993) Tenascin-C, tenascin-R, and tenascin-X: a family of talented proteins in search of functions. Curr Opin Cell Biol 5:869–876CrossRefPubMed
Zurück zum Zitat Harris SE, Gluhak-Heinrich J, Harris MA, Yang W, Bonewald LF, Riha D, Rowe PS, Robling AG, Turner CH, Feng JQ, McKee MD, Nicollela D (2007) DMP1 and MEPE expression are elevated in osteocytes after mechanical loading in vivo: theoretical role in controlling mineral quality in the perilacunar matrix. J Musculoskelet Neuronal Interact 7:313–315PubMedCentralPubMed Harris SE, Gluhak-Heinrich J, Harris MA, Yang W, Bonewald LF, Riha D, Rowe PS, Robling AG, Turner CH, Feng JQ, McKee MD, Nicollela D (2007) DMP1 and MEPE expression are elevated in osteocytes after mechanical loading in vivo: theoretical role in controlling mineral quality in the perilacunar matrix. J Musculoskelet Neuronal Interact 7:313–315PubMedCentralPubMed
Zurück zum Zitat Kaku M, Uoshima K, Yamashita Y, Miura H (2005) Investigation of periodontal ligament reaction upon excessive occlusal load–osteopontin induction among periodontal ligament cells. J Periodont Res 40:59–66CrossRefPubMed Kaku M, Uoshima K, Yamashita Y, Miura H (2005) Investigation of periodontal ligament reaction upon excessive occlusal load–osteopontin induction among periodontal ligament cells. J Periodont Res 40:59–66CrossRefPubMed
Zurück zum Zitat Kanno S, Fukuda Y (1994) Fibronectin and tenascin in rat tracheal wound healing and their relation to cell proliferation. Pathol Int 44:96–106CrossRefPubMed Kanno S, Fukuda Y (1994) Fibronectin and tenascin in rat tracheal wound healing and their relation to cell proliferation. Pathol Int 44:96–106CrossRefPubMed
Zurück zum Zitat Kawase T, Shibata S, Katori Y, Ohtsuka A, Murakami G, Fujimiya M (2012) Elastic fiber-mediated enthesis in the human middle ear. J Anat 221:331–340PubMedCentralCrossRefPubMed Kawase T, Shibata S, Katori Y, Ohtsuka A, Murakami G, Fujimiya M (2012) Elastic fiber-mediated enthesis in the human middle ear. J Anat 221:331–340PubMedCentralCrossRefPubMed
Zurück zum Zitat Lewinson D, Silbermann M (1992) Chondroclasts and endothelial cells collaborate in the process of cartilage resorption. Anat Rec 233:504–514CrossRefPubMed Lewinson D, Silbermann M (1992) Chondroclasts and endothelial cells collaborate in the process of cartilage resorption. Anat Rec 233:504–514CrossRefPubMed
Zurück zum Zitat Lukinmaa P-L, Mackie EJ, Thesleff I (1991) Immunohistochemical localization of the matrix glycoproteins-tenascin and ED-sequence-containing form of cellular fibronectin-in human permanent teeth and periodontal ligament. J Dent Res 70:19–26CrossRefPubMed Lukinmaa P-L, Mackie EJ, Thesleff I (1991) Immunohistochemical localization of the matrix glycoproteins-tenascin and ED-sequence-containing form of cellular fibronectin-in human permanent teeth and periodontal ligament. J Dent Res 70:19–26CrossRefPubMed
Zurück zum Zitat Mackie EJ, Ramsey S (1996) Modulation of osteoblast behavior by tenascin. J Cell Sci 109:1597–1604PubMed Mackie EJ, Ramsey S (1996) Modulation of osteoblast behavior by tenascin. J Cell Sci 109:1597–1604PubMed
Zurück zum Zitat Mackie EJ, Tucker RP (1992) Tenascin in bone morphogenesis: expression by osteoblasts and cell type-specific expression of splice variants. J Cell Sci 103:765–771PubMed Mackie EJ, Tucker RP (1992) Tenascin in bone morphogenesis: expression by osteoblasts and cell type-specific expression of splice variants. J Cell Sci 103:765–771PubMed
Zurück zum Zitat Mackie EJ, Tucker RP (1999) The tenascin-C knockout revisited. J Cell Sci 112:3847–3853PubMed Mackie EJ, Tucker RP (1999) The tenascin-C knockout revisited. J Cell Sci 112:3847–3853PubMed
Zurück zum Zitat Mackie EJ, Thesleff I, Chiquet-Ehrismann R (1987) Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105:2569–2579CrossRefPubMed Mackie EJ, Thesleff I, Chiquet-Ehrismann R (1987) Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105:2569–2579CrossRefPubMed
Zurück zum Zitat Matias MA, Li H, Young WG, Bartold PM (2003) Immunohistochemical localization of extracellular matrix proteins in the periodontium during cementogenesis in the rat molar. Arch Oral Biol 48:709–716CrossRefPubMed Matias MA, Li H, Young WG, Bartold PM (2003) Immunohistochemical localization of extracellular matrix proteins in the periodontium during cementogenesis in the rat molar. Arch Oral Biol 48:709–716CrossRefPubMed
Zurück zum Zitat Matsumoto Y, Iimura T, Ogura K, Moriyama K, Yamaguchi A (2013) The role of osteocytes in bone resorption during orthodontic tooth movement. J Dent Res 92:340–345CrossRefPubMed Matsumoto Y, Iimura T, Ogura K, Moriyama K, Yamaguchi A (2013) The role of osteocytes in bone resorption during orthodontic tooth movement. J Dent Res 92:340–345CrossRefPubMed
Zurück zum Zitat Miyamoto S, Katz BZ, Lafrenie RM, Yamada KM (1988) Fibronectin and integrins in cell adhesion, signaling, and morphogenesis. Ann NY Acad Sci 857:119–129CrossRef Miyamoto S, Katz BZ, Lafrenie RM, Yamada KM (1988) Fibronectin and integrins in cell adhesion, signaling, and morphogenesis. Ann NY Acad Sci 857:119–129CrossRef
Zurück zum Zitat Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, Penninger JM, Takayanagi H (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 17:1231–1234CrossRefPubMed Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, Penninger JM, Takayanagi H (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 17:1231–1234CrossRefPubMed
Zurück zum Zitat Nakasone A, Shibata S, Suzuki S, Yamashita Y, Ohyama K (2007) Laser burn wound healing in naso-labial region of fetal mice. Oral Dis 13:45–50CrossRefPubMed Nakasone A, Shibata S, Suzuki S, Yamashita Y, Ohyama K (2007) Laser burn wound healing in naso-labial region of fetal mice. Oral Dis 13:45–50CrossRefPubMed
Zurück zum Zitat Nanci A (2008) Ten Cate’s oral histology: development, structure, and function, 8th edn. Mosby, St. Louis, pp 239–267 Nanci A (2008) Ten Cate’s oral histology: development, structure, and function, 8th edn. Mosby, St. Louis, pp 239–267
Zurück zum Zitat Roberts WE, Morey ER (1985) Proliferation and differentiation sequence of osteoblast histogenesis under physiological conditions in rat periodontal ligament. Am J Anat 174:105–118CrossRefPubMed Roberts WE, Morey ER (1985) Proliferation and differentiation sequence of osteoblast histogenesis under physiological conditions in rat periodontal ligament. Am J Anat 174:105–118CrossRefPubMed
Zurück zum Zitat Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, Mantila SM, Gluhak-Heinrich J, Bellido TM, Stephen E, Harris SE, Turner CH (2008) Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 283:5866–5875CrossRefPubMed Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, Mantila SM, Gluhak-Heinrich J, Bellido TM, Stephen E, Harris SE, Turner CH (2008) Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 283:5866–5875CrossRefPubMed
Zurück zum Zitat Sahlberg C, Aukhil I, Thesleff I (2001) Tenascin-C in developing mouse teeth: expression of eplice variants and simulation by TGFβ and FGF. Eur J Oral Sci 109:114–124CrossRefPubMed Sahlberg C, Aukhil I, Thesleff I (2001) Tenascin-C in developing mouse teeth: expression of eplice variants and simulation by TGFβ and FGF. Eur J Oral Sci 109:114–124CrossRefPubMed
Zurück zum Zitat Sato R, Yamamoto H, Kasai K, Yamauchi M (2002) Distribution pattern of versican, link protein and hyaluronic acid in the rat periodontal ligament during experimental tooth movement. J Periodontal Res 37:15–22CrossRefPubMed Sato R, Yamamoto H, Kasai K, Yamauchi M (2002) Distribution pattern of versican, link protein and hyaluronic acid in the rat periodontal ligament during experimental tooth movement. J Periodontal Res 37:15–22CrossRefPubMed
Zurück zum Zitat Shibata S, Yoneda S, Yanagishita M, Yamashita Y (2002) Developmental changes and regional differences in histochemical localization of hyaluronan and versican in postnatal molar dental pulp. Int Endod J 35:159–165CrossRefPubMed Shibata S, Yoneda S, Yanagishita M, Yamashita Y (2002) Developmental changes and regional differences in histochemical localization of hyaluronan and versican in postnatal molar dental pulp. Int Endod J 35:159–165CrossRefPubMed
Zurück zum Zitat Shibata S, Suda N, Fukada K, Ohyama K, Yamashita Y, Hammond VE (2003) Mandibular coronoid process in parathyroid hormone-related protein-deficient mice shows ectopic cartilage formation accompanied by abnormal bone modeling. Anat Embryol 207:35–44CrossRefPubMed Shibata S, Suda N, Fukada K, Ohyama K, Yamashita Y, Hammond VE (2003) Mandibular coronoid process in parathyroid hormone-related protein-deficient mice shows ectopic cartilage formation accompanied by abnormal bone modeling. Anat Embryol 207:35–44CrossRefPubMed
Zurück zum Zitat Shibata S, Sakamoto Y, Baba O, Qin C, Murakami G, Cho BH (2013) An immunohistochemical study of matrix proteins in the craniofacial cartilage in midterm human fetuses. Eur J Histochem 57:e39PubMedCentralCrossRefPubMed Shibata S, Sakamoto Y, Baba O, Qin C, Murakami G, Cho BH (2013) An immunohistochemical study of matrix proteins in the craniofacial cartilage in midterm human fetuses. Eur J Histochem 57:e39PubMedCentralCrossRefPubMed
Zurück zum Zitat Shibata S, Sakamoto Y, Yokohama-Tamaki T, Murakami G, Cho BH (2014) Distribution of matrix proteins in perichondrium and periosteum during the incorporation of Meckel’s cartilage into ossifying mandible in midterm human fetuses: an immunohistochemical study. Anat Rec 297:1208–1217CrossRef Shibata S, Sakamoto Y, Yokohama-Tamaki T, Murakami G, Cho BH (2014) Distribution of matrix proteins in perichondrium and periosteum during the incorporation of Meckel’s cartilage into ossifying mandible in midterm human fetuses: an immunohistochemical study. Anat Rec 297:1208–1217CrossRef
Zurück zum Zitat Steffensen B, Duong AH, Milam CB, 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 63:584–592CrossRefPubMed Steffensen B, Duong AH, Milam CB, 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 63:584–592CrossRefPubMed
Zurück zum Zitat Thesleff I, Mackie EJ, Vainio S, Chiquet-Ehrismann R (1987) Changes in the distribution of tenascin during tooth development. Development 101:289–296PubMed Thesleff I, Mackie EJ, Vainio S, Chiquet-Ehrismann R (1987) Changes in the distribution of tenascin during tooth development. Development 101:289–296PubMed
Zurück zum Zitat Thesleff I, Kantomaa T, Machie E, Chiquet-Ehrismann R (1988) Immunohistochemical localization of the matrix glycoprotein tenascin in the skull of growing rat. Arch Oral Biol 33:383–390CrossRefPubMed Thesleff I, Kantomaa T, Machie E, Chiquet-Ehrismann R (1988) Immunohistochemical localization of the matrix glycoprotein tenascin in the skull of growing rat. Arch Oral Biol 33:383–390CrossRefPubMed
Zurück zum Zitat Tsuchiya S, Tsuchiya M, Nishioka T, Suzuki O, Sasano Y, Igarashi K (2013) Physiological distal drift in rat molars contributes to acellular cementum formation. Anat Rec 296:1255–1263CrossRef Tsuchiya S, Tsuchiya M, Nishioka T, Suzuki O, Sasano Y, Igarashi K (2013) Physiological distal drift in rat molars contributes to acellular cementum formation. Anat Rec 296:1255–1263CrossRef
Zurück zum Zitat Väkevä L, Machie E, Kantomaa T, Thesleff I (1990) Comparison of the distribution patterns of tenascin and alkaline phosphatase in developing teeth, cartilage, and bone of rats and mice. Anat Rec 228:69–76CrossRefPubMed Väkevä L, Machie E, Kantomaa T, Thesleff I (1990) Comparison of the distribution patterns of tenascin and alkaline phosphatase in developing teeth, cartilage, and bone of rats and mice. Anat Rec 228:69–76CrossRefPubMed
Zurück zum Zitat Waldo CM (1953) Method for the study of tissue response to tooth movement. J Dent Res 32:690–691 Waldo CM (1953) Method for the study of tissue response to tooth movement. J Dent Res 32:690–691
Zurück zum Zitat Webb CMB, Zaman G, Mosley JR, Tucker RP, Lanyon LE, Machie EJ (1997) Expression of tenascin-C in bones responding to mechanical load. J Bone Miner Res 12:52–58CrossRefPubMed Webb CMB, Zaman G, Mosley JR, Tucker RP, Lanyon LE, Machie EJ (1997) Expression of tenascin-C in bones responding to mechanical load. J Bone Miner Res 12:52–58CrossRefPubMed
Zurück zum Zitat Yoshida H, Yoshida T, Iizuka T, Sakakura T, Fujita S (1996) An immunohistochemical and in situ hybridization study of the expression of tenascin in synovial membranes from human temporomandibular joints with internal derangement. Arch Oral Biol 41:1081–1085CrossRefPubMed Yoshida H, Yoshida T, Iizuka T, Sakakura T, Fujita S (1996) An immunohistochemical and in situ hybridization study of the expression of tenascin in synovial membranes from human temporomandibular joints with internal derangement. Arch Oral Biol 41:1081–1085CrossRefPubMed
Zurück zum Zitat Yoshida T, Yoshimura E, Numata H, Sakakura Y, Sakakura T (1999) Involvement of tenascin-C in proliferation and migration of laryngeal carcinoma cells. Virchows Arch 435:496–500CrossRefPubMed Yoshida T, Yoshimura E, Numata H, Sakakura Y, Sakakura T (1999) Involvement of tenascin-C in proliferation and migration of laryngeal carcinoma cells. Virchows Arch 435:496–500CrossRefPubMed
Zurück zum Zitat Yoshimatsu M, Shibata Y, Kitaura H, Chang X, Moriishi T, Hashimoto F, Yoshida N, Yamaguchi A (2006) Experimental model of tooth movement by orthodontic force in mice and its application to tumor necrosis factor receptor-deficient mice. J Bone Miner Metab 24:20–27CrossRefPubMed Yoshimatsu M, Shibata Y, Kitaura H, Chang X, Moriishi T, Hashimoto F, Yoshida N, Yamaguchi A (2006) Experimental model of tooth movement by orthodontic force in mice and its application to tumor necrosis factor receptor-deficient mice. J Bone Miner Metab 24:20–27CrossRefPubMed
Zurück zum Zitat Yoshimatsu M, Kitaura H, Fujimura Y, Kohara H, Morita Y, Eguchi T, Yoshida N (2012) Inhibitory effects of IL-12 on experimental tooth movement and root resorption in mice. Arch Oral Biol 57:36–43CrossRefPubMed Yoshimatsu M, Kitaura H, Fujimura Y, Kohara H, Morita Y, Eguchi T, Yoshida N (2012) Inhibitory effects of IL-12 on experimental tooth movement and root resorption in mice. Arch Oral Biol 57:36–43CrossRefPubMed
Zurück zum Zitat Zhao Y, Young SL (1995) Tenascin in rat lung development: in situ localization and cellular sources. Am J Physiol 269(4 Pt 1):L482–L491PubMed Zhao Y, Young SL (1995) Tenascin in rat lung development: in situ localization and cellular sources. Am J Physiol 269(4 Pt 1):L482–L491PubMed
Metadaten
Titel
Immunohistochemical localization of tenascin-C in rat periodontal ligament with reference to alveolar bone remodeling
verfasst von
Rei Sato
Hiroki Fukuoka
Tamaki Yokohama-Tamaki
Masaru Kaku
Shunichi Shibata
Publikationsdatum
01.03.2016
Verlag
Springer Japan
Erschienen in
Anatomical Science International / Ausgabe 2/2016
Print ISSN: 1447-6959
Elektronische ISSN: 1447-073X
DOI
https://doi.org/10.1007/s12565-015-0285-y

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