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BMC Oral Health
Published in: BMC Oral Health 1/2021

Open Access 01-12-2021 | Hematoma | Research

Absorbance or organization into ankylosis: a microarray analysis of haemarthrosis in a sheep model of temporomandibular joint trauma

Authors: Mai-Ning Jiao, Tong-Mei Zhang, Kun Yang, Zhao-Yuan Xu, Guan-Meng Zhang, Yuan-Yuan Tian, Hao Liu, Ying-Bin Yan

Published in: BMC Oral Health | Issue 1/2021

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Abstract

Background

Traumatic haemarthrosis was hypothesized to be the etiology of temporomandibular (TMJ) ankylosis. Here, taking haematoma absorbance as a control, we aimed to reveal the molecular mechanisms involved in haematoma organizing into ankylosis using transcriptome microarray profiles.

Material/methods

Disk removal was performed to building haematoma absorbance (HA) in one side of TMJ, while removal of disk and articular fibrous layers was performed to induced TMJ ankylosis through haematoma organization (HO) in the contralateral side in a sheep model. Haematoma tissues harvested at days 1, 4 and 7 postoperatively were examined by histology, and analyzed by Affymetrix OviGene-1_0-ST microarrays. The DAVID were recruited to perform the Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway analysis for the different expression genes (DEGs). The DEGs were also typed into protein–protein interaction (PPI) networks to get the interaction data. Six significant genes screened from PPI analysis, were confirmed by real-time PCR.

Results

We found 268, 223 and 17 DEGs at least twofold at days 1, 4 and 7, respectively. At day 1, genes promoting collagen ossification (POSTN, BGN, LUM, SPARC), cell proliferation (TGF-β), and osteogenic differentiation of mesenchymal stem cells (BMP-2) were up-regulated in the HO side. At day 4, several genes involved in angiogenesis (KDR, FIT1, TEK) shower higher expression in the HO side. While HA was characterized by a continuous immune and inflammatory reaction.

Conclusions

Our results provide a comprehensive understanding of the role of haematoma in the onset and progress of TMJ ankylosis. The study will contribute to explaining why few injured TMJs ankylose and most do not from the molecular level.
Appendix
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Literature
1.
Valentini V, Vetrano S, Agrillo A, Torroni A, Fabiani F, Iannetti G. Surgical treatment of TMJ ankylosis: our experience (60 cases). J Craniofac Surg. 2002;13(1):59–67.PubMedCrossRef
2.
Yan Y, Zhang Y, Sun Z, Li J, Xiao E, An J. The relationship between mouth opening and computerized tomographic features of posttraumatic bony ankylosis of the temporomandibular joint. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;111(3):354–61.PubMedCrossRef
3.
Laskin DM. Role of the meniscus in the etiology of posttraumatic temporomandibular joint ankylosis. Int J Oral Surg. 1978;7(4):340–5.PubMedCrossRef
4.
5.
Oztan HY, Ulusal BG, Aytemiz C. The role of trauma on temporomandibular joint ankylosis and mandibular growth retardation: an experimental study. J Craniofac Surg. 2004;15(2):274–82 (discussion 82).PubMedCrossRef
6.
Goss AN, Bosanquet AG. The arthroscopic appearance of acute temporomandibular joint trauma. J Oral Maxillofac Surg. 1990;48(8):780–3 (discussion 4).PubMedCrossRef
7.
Wang HL, Liu H, Shen J, Zhang PP, Liang SX, Yan YB. Removal of the articular fibrous layers with discectomy leads to temporomandibular joint ankylosis. Oral Surg Oral Med Oral Pathol Oral Radiol. 2019;127(5):372–80.PubMedCrossRef
8.
Yang K, Wang HL, Dai YM, Liang SX, Zhang TM, Liu H, Yan YB. Which of the fibrous layer is more important in the genesis of traumatic temporomanibular joint ankylosis: the mandibular condyle or the glenoid fossa? J Stomatol Oral Maxillofac Surg. 2020;121(5):517–22.PubMedCrossRef
9.
Wang HL, Zhang PP, Meng L, Liang SX, Liu H, Yan YB. Preserving the fibrous layer of the mandibular condyle reduces the risk of ankylosis in a sheep model of intracapsular condylar fracture. J Oral Maxillofac Surg. 2018;76(9):19511 e1-e24.CrossRef
10.
Yan YB, Li JM, Xiao E, An JG, Gan YH, Zhang Y. A pilot trial on the molecular pathophysiology of traumatic temporomandibular joint bony ankylosis in a sheep model. Part I: expression of Wnt signaling. J Craniomaxillofac Surg. 2014;42(2):e15–22.PubMedCrossRef
11.
Yan YB, Li JM, Xiao E, An JG, Gan YH, Zhang Y. A pilot trial on the molecular pathophysiology of traumatic temporomandibular joint bony ankylosis in a sheep model. Part II: The differential gene expression among fibrous ankylosis, bony ankylosis and condylar fracture. J Craniomaxillofac Surg. 2014;42(2):e23–8.PubMedCrossRef
12.
Zhang DM, Yang K, Liang SX, Zhang PP, Wang HL, Tian YY, Xu ZY, Liu H, Yan YB. Microarray analysis of differential gene expression between traumatic temporomandibular joint fibrous and bony ankylosis in a sheep model. Med Sci Monit. 2021;27:e932545.PubMedPubMedCentralCrossRef
13.
Zhang J, Sun X, Jia S, Jiang X, Deng T, Liu P, Hu K. The role of lateral pterygoid muscle in the traumatic temporomandibular joint ankylosis: a gene chip based analysis. Mol Med Rep. 2019;19(5):4297–305.PubMedPubMedCentral
14.
Liang SX, Wang HL, Zhang PP, Shen J, Yang K, Meng L, Liu H, Yan YB. Differential regulation of blood vessel formation between traumatic temporomandibular joint fibrous ankylosis and bony ankylosis in a sheep model. J Craniomaxillofac Surg. 2019;47(11):1739–51.PubMedCrossRef
15.
Yan YB, Zhang Y, Gan YH, An JG, Li JM, Xiao E. Surgical induction of TMJ bony ankylosis in growing sheep and the role of injury severity of the glenoid fossa on the development of bony ankylosis. J Craniomaxillofac Surg. 2013;41(6):476–86.PubMedCrossRef
16.
Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47.PubMedPubMedCentralCrossRef
17.
Yi G, Liang M, Li M, Fang X, Liu J, Lai Y, Chen J, Yao W, Feng X, Hu, et al. A large lung gene expression study identifying IL1B as a novel player in airway inflammation in COPD airway epithelial cells. Inflamm Res. 2018;67(6):539–51.
18.
Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, et al. The gene ontology (GO) database and informatics resource. Nucleic Acids Res. 2004;32(Database issue):D258–61.
19.
20.
Huang DW, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J, Stephens R, Baseler MW, Lane HC, Lempicki RA. The DAVID gene functional classification tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 2007;8(9):R183.PubMedPubMedCentralCrossRef
21.
Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, et al. STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43(Database issue):D447–52.
22.
Bader GD, Hogue CW. An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinform. 2003;4:2.CrossRef
23.
Norholt SE, Krishnan V, Sindet-Pedersen S, Jensen I. Pediatric condylar fractures: a long-term follow-up study of 55 patients. J Oral Maxillofac Surg. 1993;51(12):1302–10.PubMedCrossRef
24.
Yan YB, Liang SX, Shen J, Zhang JC, Zhang Y. Current concepts in the pathogenesis of traumatic temporomandibular joint ankylosis. Head Face Med. 2014;10:35.PubMedPubMedCentralCrossRef
25.
Yan YB, Duan DH, Zhang Y, Gan YH. The development of traumatic temporomandibular joint bony ankylosis: a course similar to the hypertrophic nonunion? Med Hypotheses. 2012;78(2):273–6.PubMedCrossRef
26.
Schmidt-Bleek K, Schell H, Schulz N, Hoff P, Perka C, Buttgereit F, Volk HD, Lienau J, Duda GN. Inflammatory phase of bone healing initiates the regenerative healing cascade. Cell Tissue Res. 2012;347(3):567–73.PubMedCrossRef
27.
Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT, Einhorn TA. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem. 2003;88(5):873–84.PubMedCrossRef
28.
Echeverri LF, Herrero MA, Lopez JM, Oleaga G. Early stages of bone fracture healing: formation of a fibrin-collagen scaffold in the fracture hematoma. Bull Math Biol. 2015;77(1):156–83.PubMedCrossRef
29.
Clark RA, Nielsen LD, Welch MP, McPherson JM. Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGF-beta. J Cell Sci. 1995;108(Pt 3):1251–61.PubMedCrossRef
30.
Chen XJ, Shen YS, He MC, Yang F, Yang P, Pang FX, He W, Cao YM, Wei QS. Polydatin promotes the osteogenic differentiation of human bone mesenchymal stem cells by activating the BMP2-Wnt/beta-catenin signaling pathway. Biomed Pharmacother. 2019;112:108746.PubMedCrossRef
31.
Luo HR, Hattori H, Hossain MA, Hester L, Huang Y, Lee-Kwon W, Donowitz M, Nagata E, Snyder SH. Akt as a mediator of cell death. Proc Natl Acad Sci U S A. 2003;100(20):11712–7.PubMedPubMedCentralCrossRef
32.
Ding ML, Ma H, Man YG, Lv HY. Protective effects of a green tea polyphenol, epigallocatechin-3-gallate, against sevoflurane-induced neuronal apoptosis involve regulation of CREB/BDNF/TrkB and PI3K/Akt/mTOR signalling pathways in neonatal mice. Can J Physiol Pharmacol. 2017;95(12):1396–405.PubMedCrossRef
33.
Gantwerker EA, Hom DB. Skin: histology and physiology of wound healing. Facial Plast Surg Clin N Am. 2011;19(3):441–53.CrossRef
34.
35.
Shinjo R, Imagama S, Ito Z, Ando K, Nishida Y, Ishiguro N, Kadomatsu K. Keratan sulfate expression is associated with activation of a subpopulation of microglia/macrophages in Wallerian degeneration. Neurosci Lett. 2014;579:80–5.PubMedCrossRef
36.
Kato M, Neil TK, Fearnley DB, McLellan AD, Vuckovic S, Hart DN. Expression of multilectin receptors and comparative FITC-dextran uptake by human dendritic cells. Int Immunol. 2000;12(11):1511–9.PubMedCrossRef
37.
Taylor PR, Gordon S, Martinez-Pomares L. The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol. 2005;26(2):104–10.PubMedCrossRef
38.
di Masi A, De Simone G, Ciaccio C, D’Orso S, Coletta M, Ascenzi P. Haptoglobin: from hemoglobin scavenging to human health. Mol Aspects Med. 2020;73:100851.PubMedCrossRef
39.
Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H, Toyama Y, Bonewald LF, Kudo A. 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(7):1239–49.PubMedCrossRef
40.
41.
Nakazawa T, Nakajima A, Seki N, Okawa A, Kato M, Moriya H, Amizuka N, Einhorn TA, Yamazaki M. Gene expression of periostin in the early stage of fracture healing detected by cDNA microarray analysis. J Orthop Res. 2004;22(3):520–5.PubMedCrossRef
42.
Schaefer L, Iozzo RV. Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J Biol Chem. 2008;283(31):21305–9.PubMedPubMedCentralCrossRef
43.
Bi Y, Stuelten CH, Kilts T, Wadhwa S, Iozzo RV, Robey PG, Chen XD, Young MF. Extracellular matrix proteoglycans control the fate of bone marrow stromal cells. J Biol Chem. 2005;280(34):30481–9.PubMedCrossRef
44.
Embree MC, Kilts TM, Ono M, Inkson CA, Syed-Picard F, Karsdal MA, Oldberg A, Bi Y, Young MF. Biglycan and fibromodulin have essential roles in regulating chondrogenesis and extracellular matrix turnover in temporomandibular joint osteoarthritis. Am J Pathol. 2010;176(2):812–26.PubMedPubMedCentralCrossRef
45.
Corsi A, Xu T, Chen XD, Boyde A, Liang J, Mankani M, Sommer B, Iozzo RV, Eichstetter I, Robey PG, et al. Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J Bone Miner Res. 2002;17(7):1180–9.PubMedCrossRef
46.
Chen XD, Shi S, Xu T, Robey PG, Young MF. Age-related osteoporosis in biglycan-deficient mice is related to defects in bone marrow stromal cells. J Bone Miner Res. 2002;17(2):331–40.PubMedCrossRef
47.
Ezura Y, Chakravarti S, Oldberg A, Chervoneva I, Birk DE. Differential expression of lumican and fibromodulin regulate collagen fibrillogenesis in developing mouse tendons. J Cell Biol. 2000;151(4):779–88.PubMedPubMedCentralCrossRef
48.
Miragliotta V, Raphael K, Lussier JG, Theoret CL. Equine lumican (LUM) cDNA sequence and spatio-temporal expression in an experimental model of normal and pathological wound healing. Vet Dermatol. 2009;20(4):243–8.PubMedCrossRef
49.
50.
Holland PW, Harper SJ, McVey JH, Hogan BL. In vivo expression of mRNA for the Ca++-binding protein SPARC (osteonectin) revealed by in situ hybridization. J Cell Biol. 1987;105(1):473–82.PubMedCrossRef
51.
Termine JD, Kleinman HK, Whitson SW, Conn KM, McGarvey ML, Martin GR. Osteonectin, a bone-specific protein linking mineral to collagen. Cell. 1981;26(1 Pt 1):99–105.PubMedCrossRef
52.
Delany AM, Hankenson KD. Thrombospondin-2 and SPARC/osteonectin are critical regulators of bone remodeling. J Cell Commun Signal. 2009;3(3–4):227–38.PubMedPubMedCentralCrossRef
53.
Delany AM, Kalajzic I, Bradshaw AD, Sage EH, Canalis E. Osteonectin-null mutation compromises osteoblast formation, maturation, and survival. Endocrinology. 2003;144(6):2588–96.PubMedCrossRef
54.
55.
Ai-Aql ZS, Alagl AS, Graves DT, Gerstenfeld LC, Einhorn TA. Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J Dent Res. 2008;87(2):107–18.PubMedCrossRef
56.
Melincovici CS, Bosca AB, Susman S, Marginean M, Mihu C, Istrate M, Moldovan IM, Roman AL, Mihu CM. Vascular endothelial growth factor (VEGF)—key factor in normal and pathological angiogenesis. Rom J Morphol Embryol. 2018;59(2):455–67.PubMed
57.
Galliera E, Corsi MM, Banfi G. Platelet rich plasma therapy: inflammatory molecules involved in tissue healing. J Biol Regul Homeost Agents. 2012;26(2 Suppl 1):35S-42S.PubMed
58.
Metadata
Title
Absorbance or organization into ankylosis: a microarray analysis of haemarthrosis in a sheep model of temporomandibular joint trauma
Authors
Mai-Ning Jiao
Tong-Mei Zhang
Kun Yang
Zhao-Yuan Xu
Guan-Meng Zhang
Yuan-Yuan Tian
Hao Liu
Ying-Bin Yan
Publication date
01-12-2021
Publisher
BioMed Central
Keyword
Hematoma
Published in
BMC Oral Health / Issue 1/2021
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-021-02033-w

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