Calcified Tissue International

, Volume 87, Issue 4, pp 341–350 | Cite as

Development of a New ELISA for Serum Periostin: Evaluation of Growth-Related Changes and Bisphosphonate Treatment in Mice

  • Sylvain Contié
  • Nathalie Voorzanger-Rousselot
  • Judith Litvin
  • Nicolas Bonnet
  • Serge Ferrari
  • Philippe Clézardin
  • Patrick Garnero
Article

Abstract

Periostin is a gamma-carboxyglutamic acid protein preferentially expressed in periosteum and bone mesenchymal stem cells. Lack of a precise assay for measuring circulating levels impairs the investigation of its biological significance. We developed a new ELISA and studied changes of periostin levels both locally at the bone site and systemically in circulating blood during growth and after bisphosphonate-induced inhibition of bone remodeling in the mouse. The ELISA we developed is based on an affinity-purified polyclonal antibody that was raised against the C-terminal sequence of mouse periostin. Reproducibility, repeatability, precision, and accuracy tests met standards of acceptance. Serum periostin and levels of the bone turnover markers osteocalcin, PINP, CTX-I, and TRAP5b were measured in (1) 4-, 6-, 8-, 10-, and 12-week-old wild-type female Balb/c mice and (2) adult ovariectomized female Balb/c mice treated with zoledronic acid or vehicle. Serum periostin decreased during growth and stabilized from 8 weeks and older, its levels correlating with bone turnover markers. Immunohistochemistry in bones from different growth stages showed that periostin localized specifically at the sites of endochondral and intramembranous ossification, especially at the periosteal envelopes. Zoledronic acid induced a marked decrease in bone remodeling markers but did not alter serum periostin levels or periostin immunostaining pattern. The novel ELISA is highly specific and allows accurate and precise measurements of serum periostin levels in mice.

Keywords

Periostin Periosteum ELISA Bone marker Ontogenetic ossification 

References

  1. 1.
    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(Pt 1):271–278PubMedGoogle Scholar
  2. 2.
    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 14:1239–1249CrossRefPubMedGoogle Scholar
  3. 3.
    Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, Chang DD (2002) Periostin secreted by epithelial ovarian carcinoma is a ligand for alphaVbeta3 and alphaVbeta5 integrins and promotes cell motility. Cancer Res 62:5358–5364PubMedGoogle Scholar
  4. 4.
    Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN, Wang XF (2004) Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5:329–339CrossRefPubMedGoogle Scholar
  5. 5.
    Shao R, Bao S, Bai X, Blanchette C, Anderson RM, Dang T, Gishizky ML, Marks JR, Wang XF (2004) Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through up-regulation of vascular endothelial growth factor receptor 2 expression. Mol Cell Biol 24:3992–4003CrossRefPubMedGoogle Scholar
  6. 6.
    Kudo Y, Ogawa I, Kitajima S, Kitagawa M, Kawai H, Gaffney PM, Miyauchi M, Takata T (2006) Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer. Cancer Res 66:6928–6935CrossRefPubMedGoogle Scholar
  7. 7.
    Bennett JH, Moffatt S, Horton M (2001) Cell adhesion molecules in human osteoblasts: structure and function. Histol Histopathol 16:603–611PubMedGoogle Scholar
  8. 8.
    Damsky CH (1999) Extracellular matrix–integrin interactions in osteoblast function and tissue remodeling. Bone 25:95–96CrossRefPubMedGoogle Scholar
  9. 9.
    Del Fattore A, Teti A, Rucci N (2008) Osteoclast receptors and signaling. Arch Biochem Biophys 473:147–160CrossRefPubMedGoogle Scholar
  10. 10.
    Rodan SB, Rodan GA (1997) Integrin function in osteoclasts. J Endocrinol 154(Suppl):S47–S56PubMedGoogle Scholar
  11. 11.
    Schaffner P, Dard MM (2003) Structure and function of RGD peptides involved in bone biology. Cell Mol Life Sci 60:119–132CrossRefPubMedGoogle Scholar
  12. 12.
    Oshima A, Tanabe H, Yan T, Lowe GN, Glackin CA, Kudo A (2002) A novel mechanism for the regulation of osteoblast differentiation: transcription of periostin, a member of the fasciclin I family, is regulated by the bHLH transcription factor, twist. J Cell Biochem 86:792–804CrossRefPubMedGoogle Scholar
  13. 13.
    Litvin J, Selim AH, Montgomery MO, Lehmann K, Rico MC, Devlin H, Bednarik DP, Safadi FF (2004) Expression and function of periostin-isoforms in bone. J Cell Biochem 92:1044–1061CrossRefPubMedGoogle Scholar
  14. 14.
    Nakazawa T, Nakajima A, Seki N, Okawa A, Kato M, Moriya H, Amizuka N, Einhorn TA, Yamazaki M (2004) Gene expression of periostin in the early stage of fracture healing detected by cDNA microarray analysis. J Orthop Res 22:520–525CrossRefPubMedGoogle Scholar
  15. 15.
    Zhu S, Barbe MF, Amin N, Rani S, Popoff SN, Safadi FF, Litvin J (2008) Immunolocalization of periostin-like factor and periostin during embryogenesis. J Histochem Cytochem 56:329–345CrossRefPubMedGoogle Scholar
  16. 16.
    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 25:11131–11144CrossRefPubMedGoogle Scholar
  17. 17.
    Norris RA, Damon B, Mironov V, Kasyanov V, Ramamurthi A, Moreno-Rodriguez R, Trusk T, Potts JD, Goodwin RL, Davis J, Hoffman S, Wen X, Sugi Y, Kern CB, Mjaatvedt CH, Turner DK, Oka T, Conway SJ, Molkentin JD, Forgacs G, Markwald RR (2007) Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J Cell Biochem 101:695–711CrossRefPubMedGoogle Scholar
  18. 18.
    Jackson-Boeters L, Wen W, Hamilton DW (2009) Periostin localizes to cells in normal skin, but is associated with the extracellular matrix during wound repair. J Cell Commun Signal 3:125–133CrossRefPubMedGoogle Scholar
  19. 19.
    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 229:857–868CrossRefPubMedGoogle Scholar
  20. 20.
    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 A Discov Mol Cell Evol Biol 281:1264–1275CrossRefPubMedGoogle Scholar
  21. 21.
    Kii I, Kudo A (2007) Periostin function in the periodontal ligament and the periosteum. Clin Calcium 17:202–208PubMedGoogle Scholar
  22. 22.
    Shimazaki M, Nakamura K, Kii I, Kashima T, Amizuka N, Li M, Saito M, Fukuda K, Nishiyama T, Kitajima S, Saga Y, Fukayama M, Sata M, Kudo A (2008) Periostin is essential for cardiac healing after acute myocardial infarction. J Exp Med 205:295–303CrossRefPubMedGoogle Scholar
  23. 23.
    Zhu S, Barbe MF, Liu C, Hadjiargyrou M, Popoff SN, Rani S, Safadi FF, Litvin J (2009) Periostin-like-factor in osteogenesis. J Cell Physiol 218:584–592CrossRefPubMedGoogle Scholar
  24. 24.
    Goetsch SC, Hawke TJ, Gallardo TD, Richardson JA, Garry DJ (2003) Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol Genomics 14:261–271PubMedGoogle Scholar
  25. 25.
    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 267:473–487CrossRefPubMedGoogle Scholar
  26. 26.
    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 Biol 25:77–83PubMedGoogle Scholar
  27. 27.
    Dorn GW 2nd (2007) Periostin and myocardial repair, regeneration, and recovery. N Engl J Med 357:1552–1554CrossRefPubMedGoogle Scholar
  28. 28.
    Iekushi K, Taniyama Y, Azuma J, Katsuragi N, Dosaka N, Sanada F, Koibuchi N, Nagao K, Ogihara T, Morishita R (2007) Novel mechanisms of valsartan on the treatment of acute myocardial infarction through inhibition of the antiadhesion molecule periostin. Hypertension 49:1409–1414CrossRefPubMedGoogle Scholar
  29. 29.
    Oka T, Xu J, Kaiser RA, Melendez J, Hambleton M, Sargent MA, Lorts A, Brunskill EW, Dorn GW II, Conway SJ, Aronow BJ, Robbins J, Molkentin JD (2007) Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res 101:313–321CrossRefPubMedGoogle Scholar
  30. 30.
    Tai IT, Dai M, Chen LB (2005) Periostin induction in tumor cell line explants and inhibition of in vitro cell growth by anti-periostin antibodies. Carcinogenesis 26:908–915CrossRefPubMedGoogle Scholar
  31. 31.
    Ben QW, Zhao Z, Ge SF, Zhou J, Yuan F, Yuan YZ (2009) Circulating levels of periostin may help identify patients with more aggressive colorectal cancer. Int J Oncol 34:821–828PubMedGoogle Scholar
  32. 32.
    Li P, Oparil S, Feng W, Chen YF (2004) Hypoxia-responsive growth factors upregulate periostin and osteopontin expression via distinct signaling pathways in rat pulmonary arterial smooth muscle cells. J Appl Physiol 97:1550–1558 discussion 1549CrossRefPubMedGoogle Scholar
  33. 33.
    Woodruff PG, Boushey HA, Dolganov GM, Barker CS, Yang YH, Donnelly S, Ellwanger A, Sidhu SS, Dao-Pick TP, Pantoja C, Erle DJ, Yamamoto KR, Fahy JV (2007) Genome-wide profiling identifies epithelial cell genes associated with asthma and with treatment response to corticosteroids. Proc Natl Acad Sci USA 104:15858–15863CrossRefPubMedGoogle Scholar
  34. 34.
    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 118:98–104CrossRefPubMedGoogle Scholar
  35. 35.
    Oku E, Kanaji T, Takata Y, Oshima K, Seki R, Morishige S, Imamura R, Ohtsubo K, Hashiguchi M, Osaki K, Yakushiji K, Yoshimoto K, Ogata H, Hamada H, Izuhara K, Sata M, Okamura T (2008) Periostin and bone marrow fibrosis. Int J Hematol 88:57–63CrossRefPubMedGoogle Scholar
  36. 36.
    Fuchs RK, Galley M, Doyle J, Klene F, Conway SJ, Warden SJ, Burr DB (2008) The extracellular matrix protein periostin regulates periosteal. J Bone Min Res 23:S51–S51CrossRefGoogle Scholar
  37. 37.
    Bonnet N, Conway S, Ferrari S (2008) Inhibition of bone biomechanical response to physical activity and loading in mice lacking periostin. J Bone Min Res 23:S41–S41Google Scholar
  38. 38.
    Bonnet N, Rizzoli R, Ferrari S (2009) Blunted response to intermittent PTH in absence of periostin in the cortical bone compartment. In: 15th annual SBMS & SVGO/ASCO meeting. Swiss Bone and Mineral Society, Bern, SwitzerlandGoogle Scholar
  39. 39.
    Rani S, Barbe MF, Barr AE, Litvin J (2009) Periostin-like-factor and periostin in an animal model of work-related musculoskeletal disorder. Bone 44:502–512CrossRefPubMedGoogle Scholar
  40. 40.
    Rissanen JP, Suominen MI, Peng Z, Halleen JM (2008) Secreted tartrate-resistant acid phosphatase 5b is a marker of osteoclast number in human osteoclast cultures and the rat ovariectomy model. Calcif Tissue Int 82:108–115CrossRefPubMedGoogle Scholar
  41. 41.
    Hale LV, Galvin RJ, Risteli J, Ma YL, Harvey AK, Yang X, Cain RL, Zeng Q, Frolik CA, Sato M, Schmidt AL, Geiser AG (2007) PINP: a serum biomarker of bone formation in the rat. Bone 40:1103–1109CrossRefPubMedGoogle Scholar
  42. 42.
    Sasaki H, Dai M, Auclair D, Fukai I, Kiriyama M, Yamakawa Y, Fujii Y, Chen LB (2001) Serum level of the periostin, a homologue of an insect cell adhesion molecule, as a prognostic marker in nonsmall cell lung carcinomas. Cancer 92:843–848CrossRefPubMedGoogle Scholar
  43. 43.
    Baril P, Gangeswaran R, Mahon PC, Caulee K, Kocher HM, Harada T, Zhu M, Kalthoff H, Crnogorac-Jurcevic T, Lemoine NR (2007) Periostin promotes invasiveness and resistance of pancreatic cancer cells to hypoxia-induced cell death: role of the beta4 integrin and the PI3k pathway. Oncogene 26:2082–2094CrossRefPubMedGoogle Scholar
  44. 44.
    Wakchoure S, Swain TM, Hentunen TA, Bauskin AR, Brown DA, Breit SN, Vuopala KS, Harris KW, Selander KS (2009) Expression of macrophage inhibitory cytokine-1 in prostate cancer bone metastases induces osteoclast activation and weight loss. Prostate 69:652–661CrossRefPubMedGoogle Scholar
  45. 45.
    Wang ZP, Hua YM, Zhang X, Wang YB, Shi XQ, Li MY (2009) Effect of resveratrol on myocardial fibrosis in mice with chronic viral myocarditis. Zhongguo Dang Dai Er Ke Za Zhi 11:291–295 (in Chinese)PubMedGoogle Scholar
  46. 46.
    Hirose Y, Suzuki H, Amizuka N, Shimomura J, Kawano Y, Nozawa-Inoue K, Kudo A, Maeda T (2003) Immunohistochemical localization of periostin in developing long bones of mice. Biomed Res (Tokyo) 24:31–37Google Scholar
  47. 47.
    Blumer MJ, Schwarzer C, Perez MT, Konakci KZ, Fritsch H (2006) Identification and location of bone-forming cells within cartilage canals on their course into the secondary ossification centre. J Anat 208:695–707CrossRefPubMedGoogle Scholar
  48. 48.
    Emans PJ, Spaapen F, Surtel DA, Reilly KM, Cremers A, van Rhijn LW, Bulstra SK, Voncken JW, Kuijer R (2007) A novel in vivo model to study endochondral bone formation; HIF-1alpha activation and BMP expression. Bone 40:409–418CrossRefPubMedGoogle Scholar
  49. 49.
    Coutu DL, Wu JH, Monette A, Rivard GE, Blostein MD, Galipeau J (2008) Periostin, a member of a novel family of vitamin K-dependent proteins, is expressed by mesenchymal stromal cells. J Biol Chem 283:17991–18001CrossRefPubMedGoogle Scholar
  50. 50.
    Bonnet N, Standley KN, Bianchi EN, Stadelmann V, Foti M, Conway SJ, Ferrari SL (2009) The matricellular protein periostin is required for sost inhibition and the anabolic response to mechanical loading and physical activity. J Biol Chem 284:35939–35950CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Sylvain Contié
    • 1
    • 2
  • Nathalie Voorzanger-Rousselot
    • 2
  • Judith Litvin
    • 3
    • 4
  • Nicolas Bonnet
    • 5
  • Serge Ferrari
    • 5
  • Philippe Clézardin
    • 1
    • 6
  • Patrick Garnero
    • 1
    • 7
  1. 1.Research Unit 664Institut National de la Santé et de la Recherche MédicaleLyonFrance
  2. 2.Biochemical MarkersCCBR-SynarcLyonFrance
  3. 3.Department of Anatomy and Cell Biology, Fels Institute for Cancer ResearchTemple University School of MedicinePhiladelphiaUSA
  4. 4.Cardiovascular Research CenterTemple University School of MedicinePhiladelphiaUSA
  5. 5.Service of Bone Diseases, Department of Rehabilitation and GeriatricsGeneva University Hospitals and Faculty of MedicineGenevaSwitzerland
  6. 6.Université Claude Bernard Lyon 1VilleurbanneFrance
  7. 7.CisBio BioassaysBagnols/CèzeFrance

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