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Erschienen in:

01.03.2023 | Original Article

Periostin splice variants affect craniofacial growth by influencing chondrocyte hypertrophy

verfasst von: Seiko Ishihara, Risa Usumi-Fujita, Yuki Kasahara, Shuji Oishi, Kana Shibata, Yasuhiro Shimizu, Yuji Ishida, Sawa Kaneko, Makoto Sugiura-Nakazato, Makoto J. Tabata, Jun Hosomichi, Yoshiaki Taniyama, Takashi Ono

Erschienen in: Journal of Bone and Mineral Metabolism | Ausgabe 2/2023

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Abstract

Introduction

Periostin, an extracellular matrix protein, plays an important role in osteogenesis and is also known to activate several signals that contribute to chondrogenesis. The absence of periostin in periostin knockout mice leads to several disorders such as craniosynostosis and periostitis. There are several splice variants with different roles in heart disease and myocardial infarction. However, little is known about each variant’s role in chondrogenesis, followed by bone formation. Therefore, the aim of this study is to investigate the role of several variants in chondrogenesis differentiation and bone formation in the craniofacial region. Periostin splice variants included a full-length variant (Control), a variant lacking exon 17 (ΔEx17), a variant lacking exon 21 (ΔEx21), and another variant lacking both exon 17 and 21 ***(ΔEx17&21).

Materials and Methods

We used C56BL6/N mice (n = 6) for the wild type (Control)*** and the three variant type mice (n = 6 each) to identify the effect of each variant morphologically and histologically. Micro-computed tomography demonstrated a smaller craniofacial skeleton in ΔEx17s, ΔEx21s, and ΔEx17&21s compared to Controls, especially the mandibular bone. We, thus, focused on the mandibular condyle.

Results

The most distinctive histological observation was that each defected mouse appeared to have more hypertrophic chondrocytes than Controls. Real-time PCR demonstrated the differences among the group. Moreover, the lack of exon 17 or exon 21 in periostin leads to inadequate chondrocyte differentiation and presents in a diminutive craniofacial skeleton.

Discussion

Therefore, these findings suggested that each variant has a significant role in chondrocyte hypertrophy, leading to suppression of bone formation.

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 294:271–278PubMedPubMedCentralCrossRef

Kudo A, Kii I (2018) Periostin function in communication with extracellular matrices. J Cell Commun Signal 12:301–308PubMedCrossRef

Kudo A (2011) Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell. Cell Mol Life Sci 68:3201–3207PubMedPubMedCentralCrossRef

Kim CJ, Isono T, Tambe Y, Chano T, Okabe H, Okada Y, Inour H (2008) Role of alternative splicing of periostin in human bladder carcinogenesis. Int J Oncol 32:161–169PubMed

Taniyama Y, Katsuragi N, Sanada F, Azuma J, Iekushi K, Koibuchi N, Okayama K, Ikeda-Iwabu Y, Muratsu J, Otsu R, Rakugi H, Morishita R (2016) Selective blockade of periostin exon 17 preserves cardiac performance in acute myocardial infarction. Hypertension 67:356–361PubMedCrossRef

Nakama T, Yoshida S, Ishikawa K, Kobayashi Y, Abe T, Kiyonari H, Shioi G, Katsuragi N, Ishibashi T, Morishita R, Taniyama Y (2016) Different roles played by periostin splice variants in retinal neovascularization. Exp Eye Res 153:133–140PubMedCrossRef

Hamilton DW (2008) Functional role of periostin in development and wound repair: implications for connective tissue disease. J Cell Commun Signal 2:9–17PubMedPubMedCentralCrossRef

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 205:295–303PubMedPubMedCentralCrossRef

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

10.

Chen G, Deng C, Li YP (2012) TGF-β and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 8:272–288PubMedPubMedCentralCrossRef

11.

Yoshida CA, Komori T (2005) Role of Runx proteins in chondrogenesis. Crit Rev Eukaryot Gene Expr 15:243–254PubMedCrossRef

12.

Elango J, Robinson J, Zhang J, Bao B, Ma N, de Val Jems, Wu W (2019) Collagen peptide upregulates osteoblastogenesis from bone marrow mesenchymal stem cells through MAPK- Runx2. Cells 8:446PubMedPubMedCentralCrossRef

13.

de Lageneste OD, Colnot C (2019) Periostin in bone regeneration. Adv Exp Med Biol 1132:49–61CrossRef

14.

Kudo A (2019) Periostin in Bone Biology. Adv Exp Med Biol 1132:43–47PubMedCrossRef

15.

Cai J, Qin H, Yu G (2021) Effect of periostin silencing on Runx2, RANKL and OPG expression in osteoblasts. J Orofac Orthop 82:82–91PubMedCrossRef

16.

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

17.

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 25:11131–11144PubMedPubMedCentralCrossRef

18.

Inaki R, Fujihara Y, Kudo A, Misawa M, Hikita A, Takato T, Hoshi K (2018) Periostin contributes to the maturation and shape retention of tissue-engineered cartilage. Sci Rep 8:11210PubMedPubMedCentralCrossRef

19.

Fan B, Liu X, Chen X, Xu W, Zhao H, Yang C, Zhang S (2020) Periostin mediates condylar resorption via the NF-κB-ADAMTS5 pathway. Inflammation 43:455–465PubMedCrossRef

20.

de F, Alvarez-Suarez A, Costilla S, Noval I, A J, Cobo J (2011) 3D-μCT cephalometric measurements in mice. Computed tomography. IntechOpen, Rijeka, Croatia

21.

Ke C, Li H, Yang D, Ying H, Xu J, Wang J, Zhu Hong-wen, Wang L (2021) Dynamic effects of the third generation bisphosphonate of risedronate on rat osteoporotic fractures for clinical usage guidance. Orthop Surg 13:2433–2441PubMedPubMedCentralCrossRef

22.

Gholami A, Dabbaghmanesh M. H, Ghasemi Y, Koohpeyma F, Talezadeh P, Montazeri-Najafabady N (2022) The ameliorative role of specific probiotic combinations on bone loss in the ovariectomized rat model. BMC Complement Med Ther 22:241PubMedPubMedCentralCrossRef

23.

Shimizu H, Awata T (1984) Growth of skeletal bones and their sexual differences in mice. Jikken Dobutsu 33:69–76PubMed

24.

Cobo T, Cobo JL, Pérez-Varela JC, Vega JA, Cobo J (2019) Periostin and human teeth. Adv Exp Med Biol 1132:73–78PubMedCrossRef

25.

Attur M, Yang Q, Shimada K, Tachida Y, Nagase H, Mignatti P, Statman L, Palmer G, Kirsch T, Beier F, Abramson SB (2015) Elevated expression of periostin in human osteoarthritic cartilage and its potential role in matrix degradation via matrix metalloproteinase-13. Faseb J 29:4107–4121PubMedPubMedCentralCrossRef

26.

Chijimatsu R, Kunugiza Y, Taniyama Y, Nakamura N, Tomita T, Yoshikawa H (2015) Expression and pathological effects of periostin in human osteoarthritis cartilage. BMC Musculoskelet Disord 16:215PubMedPubMedCentralCrossRef

27.

Chinzei N, Brophy RH, Duan X, Cai L, Nunley RM, Sandell LJ, Rai MF (2018) Molecular influence of anterior cruciate ligament tear remnants on chondrocytes: a biologic connection between injury and osteoarthritis. Osteoarthr Cartil 26:588–599CrossRef

28.

Barna M, Niswander L (2007) Visualization of cartilage formation: insight into cellular properties of skeletal progenitors and chondrodysplasia syndromes. Dev Cell 12:931–941PubMedCrossRef

29.

Gustafsson E, Aszodi A, Ortega N, Hunziker EB, Denker HW, Werb Z, Fassler R (2003) Role of collagen type II and perlecan in skeletal development. Ann N Y Acad Sci 995:140–150PubMedCrossRef

30.

Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Crombrugghe B (2002) The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16:2813–2828PubMedPubMedCentralCrossRef

31.

Coricor G, Serra R (2016) TGF-β regulates phosphorylation and stabilization of Sox9 protein in chondrocytes through p38 and Smad dependent mechanisms. Sci Rep 6:38616PubMedPubMedCentralCrossRef

32.

Long F, Zhang X. M, Karp S, Yang Y, McMahon AP (2001) Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 128:5099–5108PubMedCrossRef

33.

Guo J, Chung UI, Yang D, Karsenty G, Bringhurst FR, Kronenberg HM (2006) PTH/PTHrP receptor delays chondrocyte hypertrophy via both Runx2-dependent and -independent pathways. Dev Biol 292:116–128PubMedCrossRef

34.

Yoshida CA, Yamamoto H, Fujita T, Furuichi T, Ito K, Inoue K, Yamana K, Zanma A, Takada K, Ito Y, Komori T (2004) Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev 18:952–963PubMedPubMedCentralCrossRef

35.

Inada M, Yasui T, Nomura S, Miyake S, Deguchi K, Himeno M, Sato M, Yamagiwa H, Kimura T, Yasui N, Ochi T, Endo N, Kitamura Y, Kishimoto T, Komori T (1999) Maturational disturbance of chondrocytes in Cbfa1-deficient mice. Dev Dyn 214:279–290PubMedCrossRef

36.

Kim IS, Otto F, Zabel B, Mundlos S (1999) Regulation of chondrocyte differentiation by Cbfa1. Mech Dev 80:159–170PubMedCrossRef

37.

Arnold MA, Kim Y, Czubryt MP, Phan D, McAnally J, Qi X, Shelton JM, Richardson JA, Bassel-Duby R, Olson EN (2007) MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev Cell 12:377–389PubMedCrossRef

38.

Rodda SJ, McMahon AP (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133:3231–3244PubMedCrossRef

39.

Ikeda-Iwabu Y, Taniyama Y, Katsuragi N, Sanada F, Koibuchi N, Shibata K, Shimazu K, Rakugi H, Morishita R (2021) Periostin short fragment with exon 17 via aberrant alternative splicing is required for breast cancer growth and metastasis. Cells 10:892PubMedPubMedCentralCrossRef

40.

Nakazawa Y, Taniyama Y, Sanada F, Morishita R, Nakamori S, Morimoto K, Yeung K. T, Yang J (2018) Periostin blockade overcomes chemoresistance via restricting the expansion of mesenchymal tumor subpopulations in breast cancer. Sci Rep 8:4013PubMedPubMedCentralCrossRef

41.

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 109:15048–15053PubMedPubMedCentralCrossRef

Titel: Periostin splice variants affect craniofacial growth by influencing chondrocyte hypertrophy
verfasst von: Seiko Ishihara
Risa Usumi-Fujita
Yuki Kasahara
Shuji Oishi
Kana Shibata
Yasuhiro Shimizu
Yuji Ishida
Sawa Kaneko
Makoto Sugiura-Nakazato
Makoto J. Tabata
Jun Hosomichi
Yoshiaki Taniyama
Takashi Ono
Publikationsdatum: 01.03.2023
Verlag: Springer Nature Singapore
Erschienen in: Journal of Bone and Mineral Metabolism / Ausgabe 2/2023
Print ISSN: 0914-8779
Elektronische ISSN: 1435-5604
DOI: https://doi.org/10.1007/s00774-023-01409-y

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Periostin splice variants affect craniofacial growth by influencing chondrocyte hypertrophy