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Original Article | Open Access

Divergent chondro/osteogenic transduction laws of fibrocartilage stem cell drive temporomandibular joint osteoarthritis in growing mice

Ruiye Bi1Qianli Li1Haohan Li1Peng Wang1Han Fang1Xianni Yang1Yiru Wang1Yi Hou2Binbin Ying3Songsong Zhu1( )
State Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases & Department of Orthognathic and TMJ Surgery, West China Hospital of Stomatology, Sichuan University, Chengdu, China
State Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases & West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Stomatology, Ningbo First Hospital, Ningbo, China

These authors contributed equally: Ruiye Bi, Qianli Li

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Abstract

The anterior disc displacement (ADD) leads to temporomandibular joint osteoarthritis (TMJOA) and mandibular growth retardation in adolescents. To investigate the potential functional role of fibrocartilage stem cells (FCSCs) during the process, a surgical ADD-TMJOA mouse model was established. From 1 week after model generation, ADD mice exhibited aggravated mandibular growth retardation with osteoarthritis (OA)-like joint cartilage degeneration, manifesting with impaired chondrogenic differentiation and loss of subchondral bone homeostasis. Lineage tracing using Gli1-CreER+; Tmfl/-mice and Sox9-CreER+;Tmfl/-mice showed that ADD interfered with the chondrogenic capacity of Gli1+ FCSCs as well as osteogenic differentiation of Sox9+ lineage, mainly in the middle zone of TMJ cartilage. Then, a surgically induced disc reposition (DR) mouse model was generated. The inhibited FCSCs capacity was significantly alleviated by DR treatment in ADD mice. And both the ADD mice and adolescent ADD patients had significantly relieved OA phenotype and improved condylar growth after DR treatment. In conclusion, ADD-TMJOA leads to impaired chondrogenic progenitor capacity and osteogenesis differentiation of FCSCs lineage, resulting in cartilage degeneration and loss of subchondral bone homeostasis, finally causing TMJ growth retardation. DR at an early stage could significantly alleviate cartilage degeneration and restore TMJ cartilage growth potential.

References

1

Cameron, H. U. & Macnab, I. The structure of the meniscus of the human knee joint. Clin. Orthop. Relat. Res. 89, 215–219 (1972).

2

Stocum, D. L. & Roberts, W. E. Part I: development and physiology of the temporomandibular joint. Curr. Osteoporos. Rep. 16, 360–368 (2018).

3
Standring, S. & Gray, H. Grays Anatomy: The Anatomical Basis of Clinical Practice. Forty-second edition. edn, (Elsevier, 2021).
4

Estes, B. T. et al. Biological resurfacing in a canine model of hip osteoarthritis. Sci. Adv. 7, eabi5918 (2021).

5

Benzakour, T., Igoumenou, V., Mavrogenis, A. F. & Benzakour, A. Current concepts for lumbar disc herniation. Int. Orthop. 43, 841–851 (2019).

6

Hunter, D. J., March, L. & Chew, M. Osteoarthritis in 2020 and beyond: a Lancet Commission. Lancet 396, 1711–1712 (2020).

7

Scrivani, S. J., Keith, D. A. & Kaban, L. B. Temporomandibular disorders. N. Engl. J. Med. 359, 2693–2705 (2008).

8

Hamerman, D. The biology of osteoarthritis. N. Engl. J. Med. 320, 1322–1330 (1989).

9

Lei, J. et al. Inhibiting Hh signaling in Gli1(+) osteogenic progenitors alleviates TMJOA. J. Dent. Res. 101, 664–674 (2022).

10

Lei, J. et al. Degenerative temporomandibular joint changes associated with recent-onset disc displacement without reduction in adolescents and young adults. J. Craniomaxillofac. Surg. 45, 408–413 (2017).

11

Nebbe, B., Major, P. W., Prasad, N. G., Grace, M. & Kamelchuk, L. S. TMJ internal derangement and adolescent craniofacial morphology: a pilot study. Angle Orthod. 67, 407–414 (1997).

12

Yang, I. H., Moon, B. S., Lee, S. P. & Ahn, S. J. Skeletal differences in patients with temporomandibular joint disc displacement according to sagittal jaw relationship. J. Oral. Maxillofac. Surg. 70, e349–e360 (2012).

13

Dong, M. et al. The magnetic resonance imaging evaluation of condylar new bone remodeling after Yang’s TMJ arthroscopic surgery. Sci. Rep. 11, 5219 (2021).

14

Ooi, K. et al. Incidence of anterior disc displacement without reduction of the temporomandibular joint in patients with dentofacial deformity. Int. J. Oral. Maxillofac. Surg. 47, 505–510 (2018).

15

Ooi, K., Yura, S., Inoue, N. & Totsuka, Y. Factors related to the incidence of anterior disc displacement without reduction and bony changes of the temporomandibular joint in patients with anterior open bite. Oral. Maxillofac. Surg. 18, 397–401 (2014).

16

Zhuo, Z., Cai, X. & Xie, Q. Is anterior disc displacement without reduction associated with temporomandibular joint condylar height in juvenile patients younger than 20 years? J. Oral. Maxillofac. Surg. 73, 843–849 (2015).

17
Research, N. I. o. D. a. C. (ed NIDCR) (2018).
18

White, B. A., Williams, L. A. & Leben, J. R. Health care utilization and cost among health maintenance organization members with temporomandibular disorders. J. Orofac. Pain. 15, 158–169 (2001).

19

Valesan, L. F. et al. Prevalence of temporomandibular joint disorders: a systematic review and meta-analysis. Clin. Oral. Investig. 25, 441–453 (2021).

20

Bryndahl, F., Warfvinge, G., Eriksson, L. & Isberg, A. Cartilage changes link retrognathic mandibular growth to TMJ disc displacement in a rabbit model. Int J. Oral. Maxillofac. Surg. 40, 621–627 (2011).

21

Bryndahl, F., Eriksson, L., Legrell, P. E. & Isberg, A. Bilateral TMJ disk displacement induces mandibular retrognathia. J. Dent. Res. 85, 1118–1123 (2006).

22

Legrell, P. E. & Isberg, A. Mandibular length and midline asymmetry after experimentally induced temporomandibular joint disk displacement in rabbits. Am. J. Orthod. Dentofac. Orthop. 115, 247–253 (1999).

23
Feng, S. Y. et al. Increased joint loading induces subchondral bone loss of the temporomandibular joint via the RANTES-CCRs-Akt2 axis. JCI Insight https://doi.org/10.1172/jci.insight.158874 (2022).
24

Bi, R. et al. Identification of human temporomandibular joint fibrocartilage stem cells with distinct chondrogenic capacity. Osteoarthr. Cartil. 28, 842–852 (2020).

25

Embree, M. C. et al. Exploiting endogenous fibrocartilage stem cells to regenerate cartilage and repair joint injury. Nat. Commun. 7, 13073 (2016).

26

Nathan, J. et al. Fibrocartilage stem cells engraft and self-organize into vascularized bone. J. Dent. Res. 97, 329–337 (2018).

27

Bi, R. et al. Regulating fibrocartilage stem cells via TNF-alpha/Nf-kappaB in TMJ osteoarthritis. J. Dent. Res. 101, 312–322 (2022).

28

Singh, M. & Detamore, M. S. Biomechanical properties of the mandibular condylar cartilage and their relevance to the TMJ disc. J. Biomech. 42, 405–417 (2009).

29

Ruscitto, A. et al. Notch regulates fibrocartilage stem cell fate and is upregulated in inflammatory TMJ arthritis. J. Dent. Res. 99, 1174–1181 (2020).

30
Bi, R. et al. Regulating fibrocartilage stem cells via TNF-alpha/Nf-kappaB in TMJ osteoarthritis. J. Dent. Res. https://doi.org/10.1177/00220345211037248 (2021).
31
Bi, R. et al. Igf1 regulates fibrocartilage stem cells, cartilage growth, and homeostasis in the temporomandibular joint of mice. J. Bone Miner. Res. https://doi.org/10.1002/jbmr.4782 (2023).
32

Seo, B. Y., An, J. S., Chang, M. S., Huh, K. H. & Ahn, S. J. Changes in condylar dimensions in temporomandibular joints with disk displacement. Oral. Surg. Oral. Med Oral. Pathol. Oral. Radiol. 129, 72–79 (2020).

33

Chang, M. S. et al. Relationships between temporomandibular joint disk displacements and condylar volume. Oral. Surg. Oral. Med Oral. Pathol. Oral. Radiol. 125, 192–198 (2018).

34

Li, C. & Zhang, Q. Comparison of magnetic resonance imaging findings in 880 temporomandibular disorder patients of different age groups: a retrospective study. BMC Oral. Health 22, 651 (2022).

35

Tanaka, E. et al. Three-dimensional finite element analysis of human temporomandibular joint with and without disc displacement during jaw opening. Med. Eng. Phys. 26, 503–511 (2004).

36

Ma, C. et al. Scx(Lin) cells directly form a subset of chondrocytes in temporomandibular joint that are sharply increased in Dmp1-null mice. Bone 142, 115687 (2021).

37

Wang, L., You, X., Zhang, L., Zhang, C. & Zou, W. Mechanical regulation of bone remodeling. Bone Res. 10, 16 (2022).

38

Nguyen, N. G. K., Nishiyama, A. & Shimada, M. A rat model for inducing temporomandibular anterior disc displacement experimentally. J. Oral. Sci. 62, 70–74 (2020).

39

Togni, L., de Abreu, M. C., Augustin, A. H., da Silva, R. B. M. & Campos, M. M. Characterization of a rat model with temporomandibular joint osteoarthritis following a surgical anterior disc displacement. Am. J. Transl. Res. 10, 3806–3817 (2018).

40

Ali, A. M. & Sharawy, M. M. Histopathological changes in rabbit craniomandibular joint associated with experimentally induced anterior disk displacement (ADD). J. Oral. Pathol. Med. 23, 364–374 (1994).

41

Chen, J. et al. Altered functional loading causes differential effects in the subchondral bone and condylar cartilage in the temporomandibular joint from young mice. Osteoarthr. Cartil. 17, 354–361 (2009).

42

Al-koshab, M., Nambiar, P. & John, J. Assessment of condyle and glenoid fossa morphology using CBCT in South-East Asians. PLoS ONE 10, e0121682 (2015).

43

Nawawi, A. P., Rikmasari, R., Kurnikasari, E., Oscandar, F. & Lita, Y. A. Volumetric analysis of normal condyles and those with disc displacement with reduction in the Indonesian population: a CBCT study. Imaging Sci. Dent. 52, 103–108 (2022).

International Journal of Oral Science
Article number: 36
Cite this article:
Bi R, Li Q, Li H, et al. Divergent chondro/osteogenic transduction laws of fibrocartilage stem cell drive temporomandibular joint osteoarthritis in growing mice. International Journal of Oral Science, 2023, 15: 36. https://doi.org/10.1038/s41368-023-00240-5

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Received: 28 April 2023
Revised: 20 July 2023
Accepted: 26 July 2023
Published: 25 August 2023
© The Author(s) 2023

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