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Association of TIMP-2 with extracellular matrix exposed to mechanical stress and its co-distribution with periostin during mouse mandible development

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Abstract

Matrix remodeling is regulated by matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs). Periostin, originally identified in a mouse osteoblastic library, plays a role in cell adhesion and migration and in mechanical stress-induced matrix remodeling. In this study, we analyzed and compared the distribution patterns of TIMP-2 and periostin during mouse mandible development. Immunohistochemical staining for TIMP-2 and periostin was carried out on serial cryosections obtained from mice at embryonic days 13–16, postnatal day 2 (P2), P35, and 12 weeks of age. TIMP-2 and periostin exhibited a strikingly similar protein distribution during mandible development. From bud to early bell stages of molars, TIMP-2 and periostin were highly expressed on the lingual and anterior sides of the basement membrane and on the adjacent jaw mesenchyme. In pre- and postnatal incisors, the basement membrane of the apical loop and dental follicle was immunostained for TIMP-2 and periostin. At postnatal stages, TIMP-2 and periostin were prominently confined to the extracellular matrix (ECM) of gingival tissues, periodontal ligaments, and tendons (all recipients of mechanical strain). However, periostin was solely detected in the lower portion of the inner root sheath of hair follicles. Gingiva of P2 cultured in anti-TIMP-2 antibody-conditioned medium showed markedly reduced staining of periostin. We suggest that TIMP-2 and periostin are co-distributed on ECM exposed to mechanical forces and coordinately function as ECM modulators.

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References

  • Afanador E, Yokozeki M, Oba Y, Kitase Y, Takahashi T, Kudo A, Moriyama K (2005) Messenger RNA expression of periostin and Twist transiently decrease by occlusal hypofunction in mouse periodontal ligament. Arch Oral Biol 50:1023–1031

    Article  PubMed  CAS  Google Scholar 

  • Arai K, Kasashima Y, Kobayashi A, Kuwano A, Yoshihara T (2002) TGF-beta alters collagen XII and XIV mRNA levels in cultured equine tenocytes. Matrix Biol 21:243–250

    Article  PubMed  CAS  Google Scholar 

  • Baker SE, Hopkinson SB, Fitchmun M, Andreason GL, Frasier F, Plopper G, Quaranta V, Jones JC (1996) Laminin-5 and hemidesmosomes: role of the alpha 3 chain subunit in hemidesmosome stability and assembly. J Cell Sci 109:2509–2520

    PubMed  CAS  Google Scholar 

  • Baker AH, Edwards DR, Murphy G (2002) Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 115:3719–3727

    Article  PubMed  CAS  Google Scholar 

  • Banes AJ, Lee G, Graff R, Otey C, Archambault J, Tsukazi M, Elfervig M, Qi J (2001) Mechanical forces and signaling in connective tissue cells: cellular mechanisms of detection, transduction, and responses to mechanical deformation. Curr Opin Orthop 12:389–396

    Article  Google Scholar 

  • Bolcato-Bellemin AL, Elkaim R, Abehsera A, Fausser JL, Haikel Y, Tenenbaum H (2000) Expression of mRNAs encoding for alpha and beta integrin subunits, MMPs, and TIMPs in stretched human periodontal ligament and gingival fibroblasts. J Dent Res 79:1712–1716

    PubMed  CAS  Google Scholar 

  • Chang H, Lee J, Poo H, Noda M, Diaz T, Wei B, Stetler-Stevenson WG, Oh J (2006) TIMP-2 promotes cell spreading and adhesion via upregulation of Rap1 signaling. Biochem Biophys Res Commun 345:1201–1206

    Article  PubMed  CAS  Google Scholar 

  • Edwards DR, Murphy G, Reynolds JJ, Whitham SE, Docherty AJ, Angel P, Heath JK (1987) Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J 6:1899–1904

    PubMed  CAS  Google Scholar 

  • Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, Chang DD (2002) Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res 62:5358–5364

    PubMed  CAS  Google Scholar 

  • Hayakawa T, Yamashita K, Ohuchi E, Shinagawa A (1994) Cell growth-promoting activity of tissue inhibitor of metalloproteinases-2 (TIMP-2). J Cell Sci 107:2373–2379

    PubMed  CAS  Google Scholar 

  • He Y, Macarak EJ, Korostoff JM, Howard PS (2004) Compression and tension: differential effects on matrix accumulation by periodontal ligament fibroblasts in vitro. Connect Tissue Res 45:28–39

    Article  PubMed  Google Scholar 

  • Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H, Toyama Y, Bonewald LF, Kudo A (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14:1239–1249

    Article  PubMed  CAS  Google Scholar 

  • Ingber DE (2006) Mechanical control of tissue morphogenesis during embryological development. Int J Dev Biol 50:255–266

    Article  PubMed  Google Scholar 

  • Kii I, Amizuka N, Minqi L, Kitajima S, Saga Y, Kudo A (2006) Periostin is an extracellular matrix protein required for eruption of incisors in mice. Biochem Biophys Res Commun 342:766–772

    Article  PubMed  CAS  Google Scholar 

  • Kim JE, Kim SJ, Lee BH, Park RW, Kim KS, Kim IS (2000) Identification of motifs for cell adhesion within the repeated domains of transforming growth factor-beta-induced gene, beta ig-h3. J Biol Chem 275:30907–30915

    Article  PubMed  CAS  Google Scholar 

  • Kim JE, Jeong HW, Nam JO, Lee BH, Choi JY, Park RW, Park JY, Kim IS (2002) Identification of motifs in the fasciclin domains of the transforming growth factor-beta-induced matrix protein beta ig-h3 that interact with the alphavbeta5 integrin. J Biol Chem 277:46159–46165

    Article  PubMed  CAS  Google Scholar 

  • Klein-Nulend J, Roelofsen J, Sterck JG, Semeins CM, Burger EH (1995) Mechanical loading stimulates the release of transforming growth factor-beta activity by cultured mouse calvariae and periosteal cells. J Cell Physiol 163:115–119

    Article  PubMed  CAS  Google Scholar 

  • Knauper V, Will H, Lopez-Otin C, Smith B, Atkinson SJ, Stanton H, Hembry RM, Murphy G (1996a) Cellular mechanisms for human procollagenase-3 (MMP-13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase a (MMP-2) are able to generate active enzyme. J Biol Chem 271:17124–17131

    Article  PubMed  CAS  Google Scholar 

  • Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G (1996b) Biochemical characterization of human collagenase-3. J Biol Chem 271:1544–1550

    Article  PubMed  CAS  Google Scholar 

  • Koch M, Schulze J, Hansen U, Ashwodt T, Keene DR, Brunken WJ, Burgeson RE, Bruckner P, Bruckner-Tuderman L (2004) A novel marker of tissue junctions, collagen XXII. J Biol Chem 279:22514–22521

    Article  PubMed  CAS  Google Scholar 

  • Kruzynska-Frejtag A, Wang J, Maeda M, Rogers R, Krug E, Hoffman S, Markwald RR, Conway SJ (2004) Periostin is expressed within the developing teeth at the sites of epithelial-mesenchymal interaction. Dev Dyn 229:857–868

    Article  PubMed  CAS  Google Scholar 

  • Kudo H, Amizuka N, Araki K, Inohaya K, Kudo A (2004) Zebrafish periostin is required for the adhesion of muscle fiber bundles to the myoseptum and for the differentiation of muscle fibers. Dev Biol 267:473–487

    Article  PubMed  CAS  Google Scholar 

  • Langbein L, Rogers MA, Praetzel S, Aoki N, Winter H, Schweizer J (2002) A novel epithelial keratin, hK6irs1, is expressed differentially in all layers of the inner root sheath, including specialized Huxley cells (Flugelzellen) of the human hair follicle. J Invest Dermatol 118:789–799

    Article  PubMed  CAS  Google Scholar 

  • Leco KJ, Hayden LJ, Sharma RR, Rocheleau H, Greenberg AH, Edwards DR (1992) Differential regulation of TIMP-1 and TIMP-2 mRNA expression in normal and Ha-ras-transformed murine fibroblasts. Gene 117:209–217

    Article  PubMed  CAS  Google Scholar 

  • Lindahl GE, Chambers C, Papakrivopoulou J, Dawson SJ, Jacobsen MC, Bishop JE, Laurent GJ (2002) Activation of fibroblast procollagen alpha 1(I) transcription by mechanical strain is transforming growth factor-beta-dependent and involves increased binding of CCAAT-binding factor (CBF/NF-Y) at the proximal promoter. J Biol Chem 277:6153–6161

    Article  PubMed  CAS  Google Scholar 

  • Lindner V, Wang Q, Conley BA, Friesel RE, Vary CP (2005) Vascular injury induces expression of periostin: implications for vascular cell differentiation and migration. Arterioscler Thromb Vasc Bio 25:77–83

    CAS  Google Scholar 

  • Lluri G, Jaworski DM (2005) Regulation of TIMP-2, MT1-MMP, and MMP-2 expression during C2C12 differentiation. Muscle Nerve 32:492–499

    Article  PubMed  CAS  Google Scholar 

  • Lovelock JD, Baker AH, Gao F, Dong JF, Bergeron AL, McPheat W, Sivasubramanian N, Mann DL (2005) Heterogeneous effects of tissue inhibitors of matrix metalloproteinases on cardiac fibroblasts. Am J Physiol Heart Circ Physiol 288:461–468

    Article  CAS  Google Scholar 

  • Menko AS, Kreidberg JA, Ryan TT, Van Bockstaele E, Kukuruzinska MA (2001) Loss of alpha3beta1 integrin function results in an altered differentiation program in the mouse submandibular gland. Dev Dyn 220:337–349

    Article  PubMed  CAS  Google Scholar 

  • Moore KA, Polte T, Huang S, Shi B, Alsberg E, Sunday ME, Ingber DE (2005) Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev Dyn 232:268–281

    Article  PubMed  CAS  Google Scholar 

  • Murphy AN, Unsworth EJ, Stetler-Stevenson WG (1993) Tissue inhibitor of metalloproteinases-2 inhibits bFGF-induced human microvascular endothelial cell proliferation. J Cell Physiol 157:351–358

    Article  PubMed  CAS  Google Scholar 

  • Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y (1997) Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 272:2446–2451

    Article  PubMed  CAS  Google Scholar 

  • Oshiro W, Lou J, Xing X, Tu Y, Manske PR (2003) Flexor tendon healing in the rat: a histologic and gene expression study. J Hand Surg 28:814–823

    Article  Google Scholar 

  • Overall CM, Wrana JL, Sodek J (1991) Transcriptional and post-transcriptional regulation of 72-kDa gelatinase/type IV collagenase by transforming growth factor-beta 1 in human fibroblasts. Comparisons with collagenase and tissue inhibitor of matrix metalloproteinase gene expression. J Biol Chem 266:14064–14071

    PubMed  CAS  Google Scholar 

  • Rios H, Koushik SV, Wang H, Wang J, Zhou HM, Lindsley A, Rogers R, Chen Z, Maeda M, Kruzynska-Frejtag A, Feng JQ, Conway SJ (2005) Periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol 25:11131–11144

    Article  PubMed  CAS  Google Scholar 

  • Ruwhof C, Wamel AE van, Egas JM, Laarse A van der (2000) Cyclic stretch induces the release of growth promoting factors from cultured neonatal cardiomyocytes and cardiac fibroblasts. Mol Cell Biochem 208:89–98

    Article  PubMed  CAS  Google Scholar 

  • Sabeh F, Ota I, Holmbeck K, Birkedal-Hansen H, Soloway P, Balbin M, Lopez-Otin C, Shapiro S, Inada M, Krane S, Allen E, Chung D, Weiss SJ (2004) Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 167:769–781

    Article  PubMed  CAS  Google Scholar 

  • Seeland U, Haeuseler C, Hinrichs R, Rosenkranz S, Pfitzner T, Scharffetter-Kochanek K, Bohm M (2002) Myocardial fibrosis in transforming growth factor-beta(1) (TGF-beta(1)) transgenic mice is associated with inhibition of interstitial collagenase. Eur J Clin Invest 32:295–303

    Article  PubMed  CAS  Google Scholar 

  • Seiki M (2002) The cell surface: the stage for matrix metalloproteinase regulation of migration. Curr Opin Cell Biol 14:624–632

    Article  PubMed  CAS  Google Scholar 

  • Seo DW, Li H, Guedez L, Wingfield PT, Diaz T, Salloum R, Wei BY, Stetler-Stevenson WG (2003) TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism. Cell 114:171–180

    Article  PubMed  CAS  Google Scholar 

  • Skonier J, Bennett K, Rothwell V, Kosowski S, Plowman G, Wallace P, Edelhoff S, Disteche C, Neubauer M, Marquardt H, Rodgers J, Purchio AF (1994) Beta ig-h3: a transforming growth factor-beta-responsive gene encoding a secreted protein that inhibits cell attachment in vitro and suppresses the growth of CHO cells in nude mice. DNA Cell Biol 13:571–584

    Article  PubMed  CAS  Google Scholar 

  • Skutek M, Griensven M van, Zeichen J, Brauer N, Bosch U (2001) Cyclic mechanical stretching modulates secretion pattern of growth factors in human tendon fibroblasts. Eur J Appl Physiol 86:48–52

    PubMed  CAS  Google Scholar 

  • Stahl S, Weitzman S, Jones JC (1997) The role of laminin-5 and its receptors in mammary epithelial cell branching morphogenesis. J Cell Sci 110:55–63

    PubMed  CAS  Google Scholar 

  • Suzuki H, Amizuka N, Kii I, Kawano Y, Nozawa-Inoue K, Suzuki A, Yoshie H, Kudo A, Maeda T (2004) Immunohistochemical localization of periostin in tooth and its surrounding tissues in mouse mandibles during development. Anat Rec 281:1264–1275

    Article  CAS  Google Scholar 

  • Takayama G, Arima K, Kanaji T, Toda S, Tanaka H, Shoji S, McKenzie AN, Nagai H, Hotokebuchi T, Izuhara K (2006) Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J Allergy Clin Immunol 118:8–104

    Article  CAS  Google Scholar 

  • Takeshita S, Kikuno R, Tezuka K, Amann E (1993) Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J 294:271–278

    PubMed  CAS  Google Scholar 

  • Tanabe H, Kii I, Amizuka N, Katsube K, Kudo A (2004) Notch signaling is activated by binding of periostin or CCN3 to Notch1 in osteoblasts. J Bone Miner Res 19:S275

    Google Scholar 

  • Tsuji K, Uno K, Zhang GX, Tamura M (2004) Periodontal ligament cells under intermittent tensile stress regulate mRNA expression of osteoprotegerin and tissue inhibitor of matrix metalloprotease-1 and -2. J Bone Miner Metab 22:94–103

    Article  PubMed  CAS  Google Scholar 

  • Wilde J, Yokozeki M, Terai K, Kudo A, Moriyama K (2003) The divergent expression of periostin mRNA in the periodontal ligament during experimental tooth movement. Cell Tissue Res 312:345–351

    Article  PubMed  CAS  Google Scholar 

  • Yoshiba K, Yoshiba N, Aberdam D, Meneguzzi G, Perrin-Schmitt F, Stoetzel C, Ruch JV, Lesot H (1998a) Expression and localization of laminin-5 subunits during mouse tooth development. Dev Dyn 211:164–176

    Article  PubMed  CAS  Google Scholar 

  • Yoshiba N, Yoshiba K, Aberdam D, Meneguzzi G, Perrin-Schmitt F, Stoetzel C, Ruch JV, Lesot H (1998b) Expression and localization of laminin-5 subunits in the mouse incisor. Cell Tissue Res 292:143–149

    Article  PubMed  CAS  Google Scholar 

  • Yoshiba N, Yoshiba K, Stoetzel C, Perrin-Schmitt F, Cam Y, Ruch JV, Lesot H (2003) Temporospatial gene expression and protein localization of matrix metalloproteinases and their inhibitors during mouse molar tooth development. Dev Dyn 228:105–112

    Article  PubMed  CAS  Google Scholar 

  • Yoshiba N, Yoshiba K, Stoetzel C, Perrin-Schmitt F, Cam Y, Ruch JV, Hosoya A, Ozawa H, Lesot H (2006) Differential regulation of TIMP-1, -2, and -3 mRNA and protein expressions during mouse incisor development. Cell Tissue Res 324:97–104

    Article  PubMed  CAS  Google Scholar 

  • Yu WH, Yu S, Meng Q, Brew K, Woessner JF Jr (2000) TIMP-3 binds to sulfated glycosaminoglycans of the extracellular matrix. J Biol Chem 275:31226–31232

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Ou J, Inagaki Y, Greenwel P, Ramirez F (2000) Synergistic cooperation between Sp1 and Smad3/Smad4 mediates transforming growth factor beta1 stimulation of alpha 2(I)-collagen (COL1A2) transcription. J Biol Chem 275:39237–39245

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors thank Prof. Dylan Edwards and Dr. Robert Nuttall (University of East Anglia, Norfolk, UK) for their generous gift of the cDNA for TIMP-2.

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Correspondence to Nagako Yoshiba.

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This work was supported by the Japanese Ministry of Education, Culture, Sports, Science, and Technology and by Niigata University Research Projects.

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Yoshiba, N., Yoshiba, K., Hosoya, A. et al. Association of TIMP-2 with extracellular matrix exposed to mechanical stress and its co-distribution with periostin during mouse mandible development. Cell Tissue Res 330, 133–145 (2007). https://doi.org/10.1007/s00441-007-0439-x

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