TNF-α is responsible for the contribution of stromal cells to osteoclast and odontoclast formation during orthodontic tooth movement


Autoři: Saika Ogawa aff001;  Hideki Kitaura aff001;  Akiko Kishikawa aff001;  Jiawei Qi aff001;  Wei-Ren Shen aff001;  Fumitoshi Ohori aff001;  Takahiro Noguchi aff001;  Aseel Marahleh aff001;  Yasuhiko Nara aff001;  Yumiko Ochi aff001;  Itaru Mizoguchi aff001
Působiště autorů: Division of Orthodontics and Dentofacial Orthopedics, Department of Translational Medicine, Tohoku University Graduate School of Dentistry, Sendai, Japan aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223989

Souhrn

Compressive force during orthodontic tooth movement induces osteoclast formation in vivo. TNF-α plays an important role in mouse osteoclast formation and bone resorption induced by compressive force during orthodontic tooth movement. Stromal cells, macrophages and T cells take part in TNF-α-induced osteoclast formation in vitro. Root resorption caused by odontoclasts is a major clinical problem during orthodontic tooth movement. In this study, we determined the cell type targeted by TNF-α during compressive-force-induced osteoclast and odontoclast formation to elucidate the mechanism of bone and root resorption in vivo. An orthodontic tooth movement mouse model was prepared with a nickel-titanium closed coil spring inserted between the maxillary incisors and the first molar. Using TNF receptor 1- and 2-deficient (KO) mice, we found that osteoclast and odontoclast formation was mediated by TNF-α in orthodontic tooth movement. We generated four types of chimeric mice: wild-type (WT) bone marrow cells transplanted into lethally irradiated WT mice (WT>WT), KO bone marrow cells transplanted into lethally irradiated WT mice (KO>WT), WT bone marrow cells transplanted into lethally irradiated KO mice (WT>KO), and KO marrow cells transplanted into lethally irradiated KO mice (KO>KO). Using anti-CD4 and anti-CD8 antibodies, T cells were eliminated from these mice. We subjected these chimeric mice to orthodontic tooth movement. Orthodontic tooth movement was evaluated and tartrate-resistant acid phosphatase-positive cells along the alveolar bone (osteoclasts) and along the tooth root (odontoclasts) were counted after 12 days of tooth movement. The amount of orthodontic tooth movement, and the number of osteoclasts and odontoclasts on the compression side were significantly lower in WT>KO and KO>KO mice than in WT>WT and KO>WT mice. According to these results, we concluded that TNF-α-responsive stromal cells are important for osteoclast and odontoclast formation during orthodontic tooth movement.

Klíčová slova:

Molars – Mouse models – Musculoskeletal system – Stromal cells – Teeth – Osteoclasts – Orthodontics – Odontoclasts


Zdroje

1. Ponzetti M, Rucci N. Updates on Osteoimmunology: What's New on the Cross-Talk Between Bone and Immune System. Front Endocrinol (Lausanne). 2019;10:236. doi: 10.3389/fendo.2019.00236 31057482; PubMed Central PMCID: PMC6482259.

2. Teitelbaum SL. Osteoclasts: what do they do and how do they do it? Am J Pathol. 2007;170(2):427–435. doi: 10.2353/ajpath.2007.060834 17255310; PubMed Central PMCID: PMC1851862.

3. Azuma Y, Kaji K, Katogi R, Takeshita S, Kudo A. Tumor necrosis factor-alpha induces differentiation of and bone resorption by osteoclasts. J Biol Chem. 2000;275(7):4858–4864. doi: 10.1074/jbc.275.7.4858 10671521.

4. Kobayashi K, Takahashi N, Jimi E, Udagawa N, Takami M, Kotake S, et al. Tumor necrosis factor alpha stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL-RANK interaction. J Exp Med. 2000;191(2):275–286. doi: 10.1084/jem.191.2.275 10637272; PubMed Central PMCID: PMC2195746.

5. Zhao B. TNF and Bone Remodeling. Curr Osteoporos Rep. 2017;15(3):126–134. doi: 10.1007/s11914-017-0358-z 28477234; PubMed Central PMCID: PMC6408950.

6. Kitaura H, Kimura K, Ishida M, Sugisawa H, Kohara H, Yoshimatsu M, et al. Effect of cytokines on osteoclast formation and bone resorption during mechanical force loading of the periodontal membrane. ScientificWorldJournal. 2014;2014:617032. doi: 10.1155/2014/617032 24574904; PubMed Central PMCID: PMC3916098.

7. Sato T, Miyazawa K, Suzuki Y, Mizutani Y, Uchibori S, Asaoka R, et al. Selective beta2-adrenergic Antagonist Butoxamine Reduces Orthodontic Tooth Movement. J Dent Res. 2014;93(8):807–812. doi: 10.1177/0022034514536730 24868013; PubMed Central PMCID: PMC4293756.

8. Chan E, Darendeliler MA. Physical properties of root cementum: Part 5. Volumetric analysis of root resorption craters after application of light and heavy orthodontic forces. Am J Orthod Dentofacial Orthop. 2005;127(2):186–195. doi: 10.1016/j.ajodo.2003.11.026 15750537.

9. Harris DA, Jones AS, Darendeliler MA. Physical properties of root cementum: part 8. Volumetric analysis of root resorption craters after application of controlled intrusive light and heavy orthodontic forces: a microcomputed tomography scan study. Am J Orthod Dentofacial Orthop. 2006;130(5):639–647. doi: 10.1016/j.ajodo.2005.01.029 17110262.

10. Montenegro VC, Jones A, Petocz P, Gonzales C, Darendeliler MA. Physical properties of root cementum: Part 22. Root resorption after the application of light and heavy extrusive orthodontic forces: a microcomputed tomography study. Am J Orthod Dentofacial Orthop. 2012;141(1):e1–9. doi: 10.1016/j.ajodo.2011.06.032 22196196.

11. Currell SD, Liaw A, Blackmore Grant PD, Esterman A, Nimmo A. Orthodontic mechanotherapies and their influence on external root resorption: A systematic review. Am J Orthod Dentofacial Orthop. 2019;155(3):313–329. doi: 10.1016/j.ajodo.2018.10.015 30826034.

12. Sameshima GT, Asgarifar KO. Assessment of root resorption and root shape: periapical vs panoramic films. Angle Orthod. 2001;71(3):185–189. doi: 10.1043/0003-3219(2001)071<0185:AORRAR>2.0.CO;2 11407770.

13. Sameshima GT, Sinclair PM. Predicting and preventing root resorption: Part II. Treatment factors. Am J Orthod Dentofacial Orthop. 2001;119(5):511–515. doi: 10.1067/mod.2001.113410 11343023.

14. Han G, Huang S, Von den Hoff JW, Zeng X, Kuijpers-Jagtman AM. Root resorption after orthodontic intrusion and extrusion: an intraindividual study. Angle Orthod. 2005;75(6):912–918. doi: 10.1043/0003-3219(2005)75[912:RRAOIA]2.0.CO;2 16448231.

15. de Almeida MR, Marcal ASB, Fernandes TMF, Vasconcelos JB, de Almeida RR, Nanda R. A comparative study of the effect of the intrusion arch and straight wire mechanics on incisor root resorption: A randomized, controlled trial. Angle Orthod. 2018;88(1):20–26. doi: 10.2319/06417-424R 28985106.

16. Sringkarnboriboon S, Matsumoto Y, Soma K. Root resorption related to hypofunctional periodontium in experimental tooth movement. J Dent Res. 2003;82(6):486–490. doi: 10.1177/154405910308200616 12766204.

17. Al-Qawasmi RA, Hartsfield JK Jr., Everett ET, Flury L, Liu, Foroud TM, et al. Genetic predisposition to external apical root resorption in orthodontic patients: linkage of chromosome-18 marker. J Dent Res. 2003;82(5):356–360. doi: 10.1177/154405910308200506 12709501.

18. Alhashimi N, Frithiof L, Brudvik P, Bakhiet M. CD40-CD40L expression during orthodontic tooth movement in rats. Angle Orthod. 2004;74(1):100–105. doi: 10.1043/0003-3219(2004)074<0100:CEDOTM>2.0.CO;2 15038497.

19. Nishioka M, Ioi H, Nakata S, Nakasima A, Counts A. Root resorption and immune system factors in the Japanese. Angle Orthod. 2006;76(1):103–108. doi: 10.1043/0003-3219(2006)076[0103:RRAISF]2.0.CO;2 16448277.

20. Takada K, Kajiya H, Fukushima H, Okamoto F, Motokawa W, Okabe K. Calcitonin in human odontoclasts regulates root resorption activity via protein kinase A. J Bone Miner Metab. 2004;22(1):12–18. doi: 10.1007/s00774-003-0441-7 14691681.

21. Verna C, Hartig LE, Kalia S, Melsen B. Influence of steroid drugs on orthodontically induced root resorption. Orthod Craniofac Res. 2006;9(1):57–62. doi: 10.1111/j.1601-6343.2006.00342.x 16420276.

22. Andrade I Jr., Silva TA, Silva GA, Teixeira AL, Teixeira MM. The role of tumor necrosis factor receptor type 1 in orthodontic tooth movement. J Dent Res. 2007;86(11):1089–1094. doi: 10.1177/154405910708601113 17959902.

23. Basaran G, Ozer T, Kaya FA, Kaplan A, Hamamci O. Interleukine-1beta and tumor necrosis factor-alpha levels in the human gingival sulcus during orthodontic treatment. Angle Orthod. 2006;76(5):830–836. doi: 10.1043/0003-3219(2006)076[0830:IATNFL]2.0.CO;2 17029518.

24. Garlet TP, Coelho U, Silva JS, Garlet GP. Cytokine expression pattern in compression and tension sides of the periodontal ligament during orthodontic tooth movement in humans. Eur J Oral Sci. 2007;115(5):355–362. doi: 10.1111/j.1600-0722.2007.00469.x 17850423.

25. Lowney JJ, Norton LA, Shafer DM, Rossomando EF. Orthodontic forces increase tumor necrosis factor alpha in the human gingival sulcus. Am J Orthod Dentofacial Orthop. 1995;108(5):519–524. doi: 10.1016/s0889-5406(95)70052-8 7484971.

26. Ren Y, Hazemeijer H, de Haan B, Qu N, de Vos P. Cytokine profiles in crevicular fluid during orthodontic tooth movement of short and long durations. J Periodontol. 2007;78(3):453–458. doi: 10.1902/jop.2007.060261 17335368.

27. Uematsu S, Mogi M, Deguchi T. Interleukin (IL)-1 beta, IL-6, tumor necrosis factor-alpha, epidermal growth factor, and beta 2-microglobulin levels are elevated in gingival crevicular fluid during human orthodontic tooth movement. J Dent Res. 1996;75(1):562–567. doi: 10.1177/00220345960750010801 8655760

28. Kitaura H, Yoshimatsu M, Fujimura Y, Eguchi T, Kohara H, Yamaguchi A, et al. An anti-c-Fms antibody inhibits orthodontic tooth movement. J Dent Res. 2008;87(4):396–400. doi: 10.1177/154405910808700405 18362327.

29. Yoshimatsu M, Shibata Y, Kitaura H, Chang X, Moriishi T, Hashimoto F, et al. Experimental model of tooth movement by orthodontic force in mice and its application to tumor necrosis factor receptor-deficient mice. J Bone Miner Metab. 2006;24(1):20–27. doi: 10.1007/s00774-005-0641-4 16369894.

30. Okamoto K, Nakashima T, Shinohara M, Negishi-Koga T, Komatsu N, Terashima A, et al. Osteoimmunology: The Conceptual Framework Unifying the Immune and Skeletal Systems. Physiol Rev. 2017;97(4):1295–1349. doi: 10.1152/physrev.00036.2016 28814613.

31. Kitaura H, Sands MS, Aya K, Zhou P, Hirayama T, Uthgenannt B, et al. Marrow stromal cells and osteoclast precursors differentially contribute to TNF-alpha-induced osteoclastogenesis in vivo. J Immunol. 2004;173(8):4838–4846. doi: 10.4049/jimmunol.173.8.4838 15470024.

32. Kitaura H, Zhou P, Kim HJ, Novack DV, Ross FP, Teitelbaum SL. M-CSF mediates TNF-induced inflammatory osteolysis. J Clin Invest. 2005;115(12):3418–3427. doi: 10.1172/JCI26132 PubMed Central PMCID: PMC1283943. 16294221

33. Baker PJ, Dixon M, Evans RT, Dufour L, Johnson E, Roopenian DC. CD4(+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun. 1999;67(6):2804–2809. 10338484; PubMed Central PMCID: PMC96585.

34. Taubman MA, Kawai T. Involvement of T-lymphocytes in periodontal disease and in direct and indirect induction of bone resorption. Crit Rev Oral Biol Med. 2001;12(2):125–135. 11345523.

35. Lerner UH. Inflammation-induced bone remodeling in periodontal disease and the influence of post-menopausal osteoporosis. J Dent Res. 2006;85(7):596–607. doi: 10.1177/154405910608500704 16798858.

36. Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature. 1999;402(6759):304–309. doi: 10.1038/46303 10580503.

37. Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med. 2006;203(12):2673–2682. doi: 10.1084/jem.20061775 PubMed Central PMCID: PMC2118166. 17088434

38. D'Amelio P, Grimaldi A, Di Bella S, Brianza SZM, Cristofaro MA, Tamone C, et al. Estrogen deficiency increases osteoclastogenesis up-regulating T cells activity: a key mechanism in osteoporosis. Bone. 2008;43(1):92–100. doi: 10.1016/j.bone.2008.02.017 18407820.

39. Kitaura H, Kimura K, Ishida M, Kohara H, Yoshimatsu M, Takano-Yamamoto T. Immunological reaction in TNF-alpha-mediated osteoclast formation and bone resorption in vitro and in vivo. Clin Dev Immunol. 2013;2013:181849. doi: 10.1155/2013/181849 23762085; PubMed Central PMCID: PMC3676982.

40. Qi J, Kitaura H, Shen WR, Kishikawa A, Ogawa S, Ohori F, et al. Establishment of an orthodontic retention mouse model and the effect of anti-c-Fms antibody on orthodontic relapse. PLoS One. 2019;14(6):e0214260. doi: 10.1371/journal.pone.0214260 PubMed Central PMCID: PMC6583981. 31216288

41. Hakami Z, Kitaura H, Kimura K, Ishida M, Sugisawa H, Ida H, et al. Effect of interleukin-4 on orthodontic tooth movement and associated root resorption. Eur J Orthod. 2015;37(1):87–94. doi: 10.1093/ejo/cju016 25074244.

42. Fujii T, Kitaura H, Kimura K, Hakami ZW, Takano-Yamamoto T. IL-4 inhibits TNF-alpha-mediated osteoclast formation by inhibition of RANKL expression in TNF-alpha-activated stromal cells and direct inhibition of TNF-alpha-activated osteoclast precursors via a T-cell-independent mechanism in vivo. Bone. 2012;51(4):771–780. doi: 10.1016/j.bone.2012.06.024 22776139.

43. Kitaura H, Fujimura Y, Yoshimatsu M, Eguchi T, Kohara H, Jang I, et al. An M-CSF receptor c-Fms antibody inhibits mechanical stress-induced root resorption during orthodontic tooth movement in mice. Angle Orthod. 2009;79(5):835–841. doi: 10.2319/080708-412.1 19705931.

44. Chung CJ, Soma K, Rittling SR, Denhardt DT, Hayata T, Nakashima K, et al. OPN deficiency suppresses appearance of odontoclastic cells and resorption of the tooth root induced by experimental force application. J Cell Physiol. 2008;214(3):614–620. doi: 10.1002/jcp.21250 17894420.

45. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL. TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest. 2000;106(12):1481–1488. doi: 10.1172/JCI11176 11120755; PubMed Central PMCID: PMC387259.

46. Brezniak N, Wasserstein A. Orthodontically induced inflammatory root resorption. Part I: The basic science aspects. Angle Orthod. 2002;72(2):175–179. doi: 10.1043/0003-3219(2002)072<0175:OIIRRP>2.0.CO;2 11999941.


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