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Periosteal Bone Formation Varies with Age in Periostin Null Mice

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Abstract

Periostin, also known as osteoblast-specific factor 2, is a matricellular protein predominantly expressed at the periosteum of bone. During growth and development, periostin contributes to periosteal expansion by facilitating osteoblast differentiation and mineralization. Later in life, periosteal expansion provides an adaptive strategy to increase tissue strength without requiring substantial increase in bone mass. However, the function of periostin past skeletal maturity and during advanced aging is relatively unknown. The objective of this study was to examine the function of periostin in maintaining bone mass and tissue strength across different ages. In periostin null mice (Postn−/−), periosteal bone formation was significantly reduced in young (3 months) and adult mice (9 months). The lack of bone formation resulted in reduced bone mass and ultimate strength. Conversely, periosteal bone formation increased at advanced ages in 18-month-old Postn−/− mice. The increase in periosteal mineralization at advanced ages coincides with increased expression of vitronectin and osteopontin. Periosteal progenitors from Postn−/− mice displayed an increased capacity to mineralize when cultured on vitronectin, but not type-1 collagen. Altogether, these findings demonstrate the unique role of periostin in regulating periosteal bone formation at different ages and the potential for vitronectin to compensate in the absence of periostin.

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References

  1. Orwoll ES (2003) Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res 18:949–954

    Article  PubMed  Google Scholar 

  2. Seeman E (2003) Reduced bone formation and increased bone resorption: rational targets for the treatment of osteoporosis. Osteoporos Int 14(Suppl 3):S2–S8

    Article  PubMed  Google Scholar 

  3. Seeman E (2008) Structural basis of growth-related gain and age-related loss of bone strength. Rheumatology (Oxford) 47(Suppl 4):2–8

    Google Scholar 

  4. Seeman E (2003) Periosteal bone formation—a neglected determinant of bone strength. N Engl J Med 349:320–323

    Article  PubMed  Google Scholar 

  5. 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  CAS  PubMed  Google Scholar 

  6. Bonnet N, Garnero P, Ferrari S (2016) Periostin action in bone. Mol Cell Endocrinol 432:75–82

    Article  CAS  PubMed  Google Scholar 

  7. Cobo T, Viloria CG, Solares L, Fontanil T, Gonzalez-Chamorro E, De Carlos F, Cobo J, Cal S, Obaya AJ (2016) Role of periostin in adhesion and migration of bone remodeling cells. PLoS ONE 11:e0147837

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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 284:35939–35950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bonnet N, Conway SJ, Ferrari SL (2012) Regulation of beta catenin signaling and parathyroid hormone anabolic effects in bone by the matricellular protein periostin. Proc Natl Acad Sci USA 109:15048–15053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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 101:695–711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bonnet N, Gineyts E, Ammann P, Conway SJ, Garnero P, Ferrari S (2013) Periostin deficiency increases bone damage and impairs injury response to fatigue loading in adult mice. PLoS ONE 8:e78347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 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  CAS  PubMed  PubMed Central  Google Scholar 

  13. Oka T, Xu J, Kaiser RA, Melendez J, Hambleton M, Sargent MA, Lorts A, Brunskill EW, Dorn GW 2nd, 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 101:313–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Reimann DA, Hames SM, Flynn MJ, Fyhrie DP (1997) A cone beam computed tomography system for true 3D imaging of specimens. Appl Radiat Isot 48:1433–1436

    Article  CAS  PubMed  Google Scholar 

  15. Nazarian A, Snyder BD, Zurakowski D, Muller R (2008) Quantitative micro-computed tomography: a non-invasive method to assess equivalent bone mineral density. Bone 43:302–311

    Article  PubMed  Google Scholar 

  16. Gardinier JD, Rostami N, Juliano L, Zhang C (2018) Bone adaptation in response to treadmill exercise in young and adult mice. Bone Rep 8:29–37

    Article  PubMed  PubMed Central  Google Scholar 

  17. Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608

    Article  CAS  PubMed  Google Scholar 

  18. Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR, Parfitt AM (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 28:2–17

    Article  PubMed  Google Scholar 

  19. Duchamp de Lageneste O, Julien A, Abou-Khalil R, Frangi G, Carvalho C, Cagnard N, Cordier C, Conway SJ, Colnot C (2018) Periosteum contains skeletal stem cells with high bone regenerative potential controlled by Periostin. Nat Commun 9:773

    Article  PubMed  PubMed Central  Google Scholar 

  20. Stanford CM, Jacobson PA, Eanes ED, Lembke LA, Midura RJ (1995) Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106–01 BSP). J Biol Chem 270:9420–9428

    Article  CAS  PubMed  Google Scholar 

  21. Yamada S, Tauchi T, Awata T, Maeda K, Kajikawa T, Yanagita M, Murakami S (2014) Characterization of a novel periodontal ligament-specific periostin isoform. J Dent Res 93:891–897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Parfitt AM (1994) The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4:382–398

    Article  CAS  PubMed  Google Scholar 

  23. Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD (2006) Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 21:1856–1863

    Article  PubMed  Google Scholar 

  24. Zhou M, Kawashima N, Suzuk N, Yamamoto M, Ohnishi K, Katsube K, Tanabe H, Kudo A, Saito M, Suda H (2015) Periostin is a negative regulator of mineralization in the dental pulp tissue. Odontology 103:152–159

    Article  PubMed  Google Scholar 

  25. Ma D, Zhang R, Sun Y, Rios HF, Haruyama N, Han X, Kulkarni AB, Qin C, Feng JQ (2011) A novel role of periostin in postnatal tooth formation and mineralization. J Biol Chem 286:4302–4309

    Article  CAS  PubMed  Google Scholar 

  26. Salasznyk RM, Williams WA, Boskey A, Batorsky A, Plopper GE (2004) Adhesion to vitronectin and collagen I promotes osteogenic differentiation of human mesenchymal stem cells. J Biomed Biotechnol 2004:24–34

    Article  PubMed  PubMed Central  Google Scholar 

  27. Min SK, Kang HK, Jung SY, Jang DH, Min BM (2018) A vitronectin-derived peptide reverses ovariectomy-induced bone loss via regulation of osteoblast and osteoclast differentiation. Cell Death Differ 25:268–281

    Article  CAS  PubMed  Google Scholar 

  28. Boskey AL, Spevak L, Paschalis E, Doty SB, McKee MD (2002) Osteopontin deficiency increases mineral content and mineral crystallinity in mouse bone. Calcif Tissue Int 71:145–154

    Article  CAS  PubMed  Google Scholar 

  29. Rittling SR, Matsumoto HN, McKee MD, Nanci A, An XR, Novick KE, Kowalski AJ, Noda M, Denhardt DT (1998) Mice lacking osteopontin show normal development and bone structure but display altered osteoclast formation in vitro. J Bone Miner Res 13:1101–1111

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by NIH/NIAMS Grant R01AR076378.

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Correspondence to Joseph D. Gardinier.

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Joseph Gardinier, Amit Chougule, Devin Mendez, Conor Daly-Seiler, and Chunbin Zhang declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

Animal procedures were conducted under Institutional Animal Care Use Committee (IACUC) approval at the Henry Ford Hospital. The ethical principles established by the National Institutes of Health Guide for the Care and Use of Laboratory Animals (NIH Publications No. 8523, revised 2011) were followed. The study does not involve research in humans.

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Gardinier, J.D., Chougule, A., Mendez, D. et al. Periosteal Bone Formation Varies with Age in Periostin Null Mice. Calcif Tissue Int 112, 463–471 (2023). https://doi.org/10.1007/s00223-023-01063-6

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  • DOI: https://doi.org/10.1007/s00223-023-01063-6

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