Periostin Promotes the Proliferation, Differentiation and Mineralization of Osteoblasts from Ovariectomized Rats

Abstract

Perimenopausal period causes a significant amount of bone loss, which results in primary osteoporosis (OP). The Periostin (Postn) may play important roles in the pathogenesis of OP after ovariectomized (OVX) rats. To identify the roles of Postn in the bone marrow mesenchymal stem cell derived osteoblasts (BMSC-OB) in OVX rats, we investigated the expression of Wnt/β-catenin signaling pathways in BMSC-OB and the effects of Postn on bone formation by development of BMSC-OB cultures. Twenty-four female Sprague–Dawley rats at 6 months were randomized into 3 groups: sham-operated (SHAM) group, OVX group and OVX+Postn group. The rats were killed after 3 months, and their bilateral femora and tibiae were collected for BMSC-OB culture, Micro-CT Analysis, Bone Histomorphometric Measurement, Transmission Electron Microscopy and Immunohistochemistry Staining. The dose/time-dependent effects of Postn on the proliferation, differentiation and mineralization of BMSC-OB and the expression of osteoblastic markers were measured in in vitro experiments. We found increased Postn increased bone mass, promoted bone formation of trabeculae, Wnt signaling and the osteogenic activity in osteoblasts in sublesional femur. Postn have the function to enhance cell proliferation, differentiation and mineralization at a proper concentration and incubation time. Interestingly, in BMSC-OB from OVX rats treated with the different dose of Postn, the osteoblastic markers expression and Wnt/β-catenin signaling pathways were significantly promoted. The direct effect of Postn may lead to inhibit excessive bone resorption and increase bone formation through the Wnt/β-catenin signaling pathways after OVX. Postn may play a very important role in the pathogenesis of OP after OVX.

Keywords

osteoporosis - periostin - osteoblast

Publication History

Received: 24 July 2023

Accepted after revision: 23 December 2023

Article published online:
02 February 2024

• References

• 1 Black DM, Rosen CJ. Clinical practice. Postmenopausal osteoporosis. N Engl J Med 2016; 374: 254-262
• 2 Rachner TD, Khosla S, Hofbauer LC. Osteoporosis: now and the future. Lancet 2011; 377: 1276-1287
• 3 Compston JE, McClung MR, Leslie WD. Osteoporosis. Lancet 2019; 393: 364-376
• 4 Merle B, Garnero P. The multiple facets of periostin in bone metabolism. Osteoporos Int 2012; 23: 1199-1212
• 5 Cobo T, Viloria CG, Solares L. et al. Role of periostin in adhesion and migration of bone remodeling cells. PLoS One 2016; 11: e0147837
• 6 Bonnet N, Standley KN, Bianchi EN. et al. The matricellular protein periostin is required for sost inhibition and the anabolic response to mechanical loading and physical activity. J Biol Chem 2009; 284: 35939-35950
• 7 Bonnet N, Garnero P, Ferrari S. Periostin action in bone. Mol Cell Endocrinol 2016; 432: 75-82
• 8 Yan J, Liu HJ, Li H. et al. Circulating periostin levels increase in association with bone density loss and healing progression during the early phase of hip fracture in Chinese older women. Osteoporos Int 2017; 28: 2335-2341
• 9 Merle B, Bouet G, Rousseau JC. et al. Periostin and transforming growth factor beta-induced protein (TGFbetaIp) are both expressed by osteoblasts and osteoclasts. Cell Biol Int 2014; 38: 398-404
• 10 Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156-159
• 11 Li C, Li X, Wang X. et al. Periostin mediates oestrogen-induced osteogenic differentiation of bone marrow stromal cells in ovariectomised rats. Biomed Res Int 2020;
• 12 Litvin J, Selim AH, Montgomery MO. et al. Expression and function of periostin-isoforms in bone. J Cell Biochem 2004; 92: 1044-1061
• 13 Allen MR, Hock JM, Burr DB. Periosteum: biology, regulation, and response to osteoporosis therapies. Bone 2004; 35: 1003-1012
• 14 Pepe J, Bonnet N, Herrmann FR. et al. Interaction between LRP5 and periostin gene polymorphisms on serum periostin levels and cortical bone microstructure. Osteoporos Int 2018; 29: 339-346
• 15 Duchamp de Lageneste O, Colnot C. Periostin in bone regeneration. Adv Exp Med Biol 2019; 1132: 49-61
• 16 Amjadi-Moheb F, Akhavan-Niaki H. Wnt signaling pathway in osteoporosis: epigenetic regulation, interaction with other signaling pathways, and therapeutic promises. J Cell Physiol 2019; 234: 14641-14650
• 17 Manolagas SC. Wnt signaling and osteoporosis. Maturitas 2014; 78: 233-237
• 18 Morra L, Moch H. Periostin expression and epithelial-mesenchymal transition in cancer: a review and an update. Virchows Arch 2011; 459: 465-475
• 19 Tkatchenko TV, Moreno-Rodriguez RA, Conway SJ. et al. Lack of periostin leads to suppression of Notch1 signaling and calcific aortic valve disease. Physiol Genomics 2009; 39: 160-168
• 20 Lv J, Sun X, Ma J. et al. Involvement of periostin-sclerostin-Wnt/beta-catenin signaling pathway in the prevention of neurectomy-induced bone loss by naringin. Biochem Biophys Res Commun 2015; 468: 587-593
• 21 Bonnet N, Biver E, Durosier C. et al. Additive genetic effects on circulating periostin contribute to the heritability of bone microstructure. J Clin Endocrinol Metab 2015; 100: E1014-E1021
• 22 Bonnet N, Conway SJ, Ferrari SL. Regulation of beta catenin signaling and parathyroid hormone anabolic effects in bone by the matricellular protein periostin. Proc Natl Acad Sci U S A 2012; 109: 15048-15053
• 23 Zhu D, Wang Z, Zhang G. et al. Periostin promotes nucleus pulposus cells apoptosis by activating the Wnt/beta-catenin signaling pathway. FASEB J 2022; 36: e22369
• 24 Gerbaix M, Vico L, Ferrari SL. et al. Periostin expression contributes to cortical bone loss during unloading. Bone 2015; 71: 94-100
• 25 Kudo A. Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell. Cell Mol Life Sci 2011; 68: 3201-3207
• 26 Garnero P. New developments in biological markers of bone metabolism in osteoporosis. Bone 2014; 66: 46-55
• 27 Mosher DF, Johansson MW, Gillis ME. et al. Periostin and TGF-beta-induced protein: Two peas in a pod?. Crit Rev Biochem Mol Biol 2015; 50: 427-439
• 28 Galli C, Piergianni M, Piemontese M. et al. Periostin improves cell adhesion to implantable biomaterials and osteoblastic differentiation on implant titanium surfaces in a topography-dependent fashion. J Biomed Mater Res A 2014; 102: 3855-3861
• 29 Heo SC, Shin WC, Lee MJ. et al. Periostin accelerates bone healing mediated by human mesenchymal stem cell-embedded hydroxyapatite/tricalcium phosphate scaffold. PLoS One 2015; 10: e0116698
• 30 Oshima A, Tanabe H, Yan T. et al. 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 2002; 86: 792-804
• 31 Zhu S, Barbe MF, Liu C. et al. Periostin-like-factor in osteogenesis. J Cell Physiol 2009; 218: 584-592
• 32 Horiuchi K, Amizuka N, Takeshita S. et al. 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 1999; 14: 1239-1249
• 33 Ma Z, Zhao X, Deng M. et al. Bone marrow mesenchymal stromal cell-derived periostin promotes B-ALL progression by modulating CCL2 in leukemia cells. Cell Rep 2019; 26: 1533-1543 e1534
• 34 Zhong WJ, Zhang WB, Ma JQ. et al. Periostin-like-factor-induced bone formation within orthopedic maxillary expansion. Orthod Craniofac Res 2011; 14: 198-205
• 35 Lotz J, Gaertner T, Hahn M. et al. Collagen type I metabolism after bone surgery. Arch Orthop Trauma Surg 1999; 119: 212-216