Skip to main content
Erschienen in: Odontology 3/2023

13.12.2022 | Original Article

Denervation delays initial bone healing of rat tooth extraction socket

verfasst von: Zhenxian Sheng, Fuju Zheng, Jianbin Li, Yuxin Wang, Yi Du, Xiaohua Liu, Xijiao Yu

Erschienen in: Odontology | Ausgabe 3/2023

Einloggen, um Zugang zu erhalten

Abstract

Functions of nerves on bone has been a subject of intense research. The aim of this study is to observe initial bone healing of rat tooth extraction socket after inferior alveolar nerve transection. The bilateral mandible second molars of eighteen Wistar rats were extracted in the study. The rats also suffered from right inferior alveolar nerve transection simultaneously (D + E group), only extraction as control (E group). One, two and four weeks after extraction, the mandibles were taken out for histological observation, TRAP staining, immunofluorescence, immunohistochemistry and micro-computed tomography (Micro-CT). Mouse bone marrow derived macrophages (BMMs) were cultured in vitro. Expressions of nuclear factor erythroid 2-related factor 2 (Nrf2) were detected in vivo and vitro. The alveolar sockets had been filled to a large extent with new bone at 4 weeks, but BV/TV and BMD decreased in the D + E group. Accordingly, Expressions of osteocalcin (OCN) and osteopontin (OPN) were down-regulated in the D + E group. Denervation increased TRAP-positive osteoclasts and decreased expressions of Nrf2 at 2 weeks after extraction. Decreased Nrf2 promoted osteoclast differentiation of BMMs in vitro. Denervation delays initial bone healing of rat tooth extraction socket. Osteoclast activation induced by decreased Nrf2 might participated in the process.
Literatur
1.
Zurück zum Zitat Wan QQ, Qin WP, Ma YX, Shen MJ, Li J, Zhang ZB, Chen JH, Tay FR, Niu LN. Crosstalk between bone and nerves within bone. Adv Sci. 2021;8:2003390.CrossRef Wan QQ, Qin WP, Ma YX, Shen MJ, Li J, Zhang ZB, Chen JH, Tay FR, Niu LN. Crosstalk between bone and nerves within bone. Adv Sci. 2021;8:2003390.CrossRef
2.
Zurück zum Zitat Yu X, Lv L, Zhang J, Zhang T, Xiao C, Li S. Expression of neuropeptides and bone remodeling-related factors during periodontal tissue regeneration in denervated rats. J Mol Histol. 2015;46:195–203.CrossRefPubMed Yu X, Lv L, Zhang J, Zhang T, Xiao C, Li S. Expression of neuropeptides and bone remodeling-related factors during periodontal tissue regeneration in denervated rats. J Mol Histol. 2015;46:195–203.CrossRefPubMed
3.
Zurück zum Zitat Yu X, Gong Z, Lin Q, Wang W, Liu S, Li S. Denervation effectively aggravates rat experimental periodontitis. J Periodontal Res. 2017;52:1011–20.CrossRefPubMed Yu X, Gong Z, Lin Q, Wang W, Liu S, Li S. Denervation effectively aggravates rat experimental periodontitis. J Periodontal Res. 2017;52:1011–20.CrossRefPubMed
5.
Zurück zum Zitat Bellezza I, Giambanco I, Minelli A, Donato R. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim Biophys Acta Mol Cell Res. 2018;1865:721–33.CrossRefPubMed Bellezza I, Giambanco I, Minelli A, Donato R. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim Biophys Acta Mol Cell Res. 2018;1865:721–33.CrossRefPubMed
7.
Zurück zum Zitat Xiong W, MacColl Garfinkel AE, Li Y, Benowitz LI, Cepko CL. NRF2 promotes neuronal survival in neurodegeneration and acute nerve damage. J Clin Invest. 2015;125:1433–45.CrossRefPubMedPubMedCentral Xiong W, MacColl Garfinkel AE, Li Y, Benowitz LI, Cepko CL. NRF2 promotes neuronal survival in neurodegeneration and acute nerve damage. J Clin Invest. 2015;125:1433–45.CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Sánchez-de-Diego C, Pedrazza L, Pimenta-Lopes C, Martinez-Martinez A, Dahdah N, Valer JA, Garcia-Roves P, Rosa JL, Ventura F. NRF2 function in osteocytes is required for bone homeostasis and drives osteocytic gene expression. Redox Biol. 2021;40: 101845.CrossRefPubMed Sánchez-de-Diego C, Pedrazza L, Pimenta-Lopes C, Martinez-Martinez A, Dahdah N, Valer JA, Garcia-Roves P, Rosa JL, Ventura F. NRF2 function in osteocytes is required for bone homeostasis and drives osteocytic gene expression. Redox Biol. 2021;40: 101845.CrossRefPubMed
10.
Zurück zum Zitat Kitaoka Y, Takeda K, Tamura Y, Fujimaki S, Takemasa T, Hatta H. Nrf2 deficiency does not affect denervation-induced alterations in mitochondrial fission and fusion proteins in skeletal muscle. Physiol Rep. 2016;4: e13064.CrossRefPubMedPubMedCentral Kitaoka Y, Takeda K, Tamura Y, Fujimaki S, Takemasa T, Hatta H. Nrf2 deficiency does not affect denervation-induced alterations in mitochondrial fission and fusion proteins in skeletal muscle. Physiol Rep. 2016;4: e13064.CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Li J, Sheng Z, Sun J, Wang R, Yu X. Characterizations of alveolar repair after mandibular second molar extraction: an experimental study in rats. J Appl Oral Sci. 2022;30: e20220010.CrossRefPubMedPubMedCentral Li J, Sheng Z, Sun J, Wang R, Yu X. Characterizations of alveolar repair after mandibular second molar extraction: an experimental study in rats. J Appl Oral Sci. 2022;30: e20220010.CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Yu X, Zheng F, Shang W, Du Y, Zhen J, Mao Y, Zhang S. Isorhamnetin 3-O-neohesperidoside promotes the resorption of crown-covered bone during tooth eruption by osteoclastogenesis. Sci Rep. 2020;10:5172.CrossRefPubMedPubMedCentral Yu X, Zheng F, Shang W, Du Y, Zhen J, Mao Y, Zhang S. Isorhamnetin 3-O-neohesperidoside promotes the resorption of crown-covered bone during tooth eruption by osteoclastogenesis. Sci Rep. 2020;10:5172.CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Xu Y, Xia M, Chen T, Yang Y, Fu G, Ji P, Wu Q. Inferior alveolar nerve transection disturbs innate immune responses and bone healing after tooth extraction. Ann N Y Acad Sci. 2019;1448:52–64.CrossRefPubMed Xu Y, Xia M, Chen T, Yang Y, Fu G, Ji P, Wu Q. Inferior alveolar nerve transection disturbs innate immune responses and bone healing after tooth extraction. Ann N Y Acad Sci. 2019;1448:52–64.CrossRefPubMed
14.
Zurück zum Zitat Tomlinson RE, Christiansen BA, Giannone AA, Genetos DC. The role of nerves in skeletal development, adaptation, and aging. Front Endocrinol (Lausanne). 2020;11:646.CrossRefPubMed Tomlinson RE, Christiansen BA, Giannone AA, Genetos DC. The role of nerves in skeletal development, adaptation, and aging. Front Endocrinol (Lausanne). 2020;11:646.CrossRefPubMed
15.
Zurück zum Zitat Chen H, Hu B, Lv X, Zhu S, Zhen G, Wan M, Jain A, Gao B, Chai Y, Yang M, Wang X. Prostaglandin E2 mediates sensory nerve regulation of bone homeostasis. Nat Commun. 2019;10:181.CrossRefPubMedPubMedCentral Chen H, Hu B, Lv X, Zhu S, Zhen G, Wan M, Jain A, Gao B, Chai Y, Yang M, Wang X. Prostaglandin E2 mediates sensory nerve regulation of bone homeostasis. Nat Commun. 2019;10:181.CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Yamashiro T, Fujiyama K, Fujiyoshi Y, Inaguma N, Takano-Yamamoto T. Inferior alveolar nerve transection inhibits increase in osteoclast appearance during experimental tooth movement. Bone. 2000;26:663–9.CrossRefPubMed Yamashiro T, Fujiyama K, Fujiyoshi Y, Inaguma N, Takano-Yamamoto T. Inferior alveolar nerve transection inhibits increase in osteoclast appearance during experimental tooth movement. Bone. 2000;26:663–9.CrossRefPubMed
17.
Zurück zum Zitat Wu Q, Yang B, Cao C, Guang M, Gong P. Age-dependent impact of inferior alveolar nerve transection on mandibular bone metabolism and the underlying mechanisms. J Mol Histol. 2016;47:579–86.CrossRefPubMed Wu Q, Yang B, Cao C, Guang M, Gong P. Age-dependent impact of inferior alveolar nerve transection on mandibular bone metabolism and the underlying mechanisms. J Mol Histol. 2016;47:579–86.CrossRefPubMed
18.
Zurück zum Zitat Xie D, Xu Y, Yang Y, Hua Z, Li J, Fu G, Wu Q. Sensory denervation increases potential of bisphosphonates to induce osteonecrosis via disproportionate expression of calcitonin gene-related peptide and substance P. Ann N Y Acad Sci. 2021;1487:56–73.CrossRefPubMed Xie D, Xu Y, Yang Y, Hua Z, Li J, Fu G, Wu Q. Sensory denervation increases potential of bisphosphonates to induce osteonecrosis via disproportionate expression of calcitonin gene-related peptide and substance P. Ann N Y Acad Sci. 2021;1487:56–73.CrossRefPubMed
19.
Zurück zum Zitat Iizuka T, Miller SC, Marks SC Jr. Alveolar bone remodeling after tooth extraction in normal and osteopetrotic (ia) rats. J Oral Pathol Med. 1992;21:150–5.CrossRefPubMed Iizuka T, Miller SC, Marks SC Jr. Alveolar bone remodeling after tooth extraction in normal and osteopetrotic (ia) rats. J Oral Pathol Med. 1992;21:150–5.CrossRefPubMed
20.
Zurück zum Zitat Yamashita J, Sawa N, Sawa Y, Miyazono S. Effect of bisphosphonates on healing of tooth extraction wounds in infectious osteomyelitis of the jaw. Bone. 2021;143: 115611.CrossRefPubMed Yamashita J, Sawa N, Sawa Y, Miyazono S. Effect of bisphosphonates on healing of tooth extraction wounds in infectious osteomyelitis of the jaw. Bone. 2021;143: 115611.CrossRefPubMed
21.
Zurück zum Zitat Cao J, Zhang S, Gupta A, Du Z, Lei D, Wang L, Wang X. Sensory nerves affect bone regeneration in rabbit mandibular distraction osteogenesis. Int J Med Sci. 2019;16:831–7.CrossRefPubMedPubMedCentral Cao J, Zhang S, Gupta A, Du Z, Lei D, Wang L, Wang X. Sensory nerves affect bone regeneration in rabbit mandibular distraction osteogenesis. Int J Med Sci. 2019;16:831–7.CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Sadr K, Aghbali A, Sadr M, Abachizadeh H, Azizi M, Mesgari AM. Effect of beta-blockers on number of osteoblasts and osteoclasts in alveolar socket following tooth extraction in wistar rats. J Dent (Shiraz). 2017;18:37–42.PubMed Sadr K, Aghbali A, Sadr M, Abachizadeh H, Azizi M, Mesgari AM. Effect of beta-blockers on number of osteoblasts and osteoclasts in alveolar socket following tooth extraction in wistar rats. J Dent (Shiraz). 2017;18:37–42.PubMed
23.
Zurück zum Zitat Han J, Yang K, An J, Jiang N, Fu S, Tang X. The role of NRF2 in bone metabolism - friend or foe? Front Endocrinol (Lausanne). 2022;13: 813057.CrossRefPubMed Han J, Yang K, An J, Jiang N, Fu S, Tang X. The role of NRF2 in bone metabolism - friend or foe? Front Endocrinol (Lausanne). 2022;13: 813057.CrossRefPubMed
24.
Zurück zum Zitat Sun YX, Li L, Corry KA, Zhang P, Yang Y, Himes E, Mihuti CL, Nelson C, Dai G, Li J. Deletion of Nrf2 reduces skeletal mechanical properties and decreases load-driven bone formation. Bone. 2015;74:1–9.CrossRefPubMed Sun YX, Li L, Corry KA, Zhang P, Yang Y, Himes E, Mihuti CL, Nelson C, Dai G, Li J. Deletion of Nrf2 reduces skeletal mechanical properties and decreases load-driven bone formation. Bone. 2015;74:1–9.CrossRefPubMed
25.
Zurück zum Zitat Sun X, Xie Z, Hu B, Zhang B, Ma Y, Pan X, Huang H, Wang J, Zhao X, Jie Z, Shi P, Chen Z. The Nrf2 activator RTA-408 attenuates osteoclastogenesis by inhibiting STING dependent NF-κb signaling. Redox Biol. 2020;28: 101309.CrossRefPubMed Sun X, Xie Z, Hu B, Zhang B, Ma Y, Pan X, Huang H, Wang J, Zhao X, Jie Z, Shi P, Chen Z. The Nrf2 activator RTA-408 attenuates osteoclastogenesis by inhibiting STING dependent NF-κb signaling. Redox Biol. 2020;28: 101309.CrossRefPubMed
26.
Zurück zum Zitat Dang R, Wang M, Li X, Wang H, Liu L, Wu Q, Zhao J, Ji P, Zhong L, Licinio J, Xie P. Edaravone ameliorates depressive and anxiety-like behaviors via Sirt1/Nrf2/HO-1/Gpx4 pathway. J Neuroinflammation. 2022;19:41.CrossRefPubMedPubMedCentral Dang R, Wang M, Li X, Wang H, Liu L, Wu Q, Zhao J, Ji P, Zhong L, Licinio J, Xie P. Edaravone ameliorates depressive and anxiety-like behaviors via Sirt1/Nrf2/HO-1/Gpx4 pathway. J Neuroinflammation. 2022;19:41.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Yuan Y, Zhai Y, Chen J, Xu X, Wang H. Kaempferol ameliorates oxygen-glucose deprivation/reoxygenation-induced neuronal ferroptosis by activating Nrf2/SLC7A11/GPX4 Axis. Biomolecules. 2021;11:923.CrossRefPubMedPubMedCentral Yuan Y, Zhai Y, Chen J, Xu X, Wang H. Kaempferol ameliorates oxygen-glucose deprivation/reoxygenation-induced neuronal ferroptosis by activating Nrf2/SLC7A11/GPX4 Axis. Biomolecules. 2021;11:923.CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Lv Z, Wang F, Zhang X, Zhang X, Zhang J, Liu R. Etomidate attenuates the ferroptosis in myocardial ischemia/reperfusion rat model via Nrf2/HO-1 pathway. Shock. 2021;56:440–9.PubMed Lv Z, Wang F, Zhang X, Zhang X, Zhang J, Liu R. Etomidate attenuates the ferroptosis in myocardial ischemia/reperfusion rat model via Nrf2/HO-1 pathway. Shock. 2021;56:440–9.PubMed
29.
Zurück zum Zitat Ikebuchi Y, Aoki S, Honma M, Hayashi M, Sugamori Y, Khan M, Kariya Y, Kato G, Tabata Y, Penninger JM, Udagawa N, Aoki K, Suzuki H. Coupling of bone resorption and formation by RANKL reverse signalling. Nature. 2018;561(7722):195–200.CrossRefPubMed Ikebuchi Y, Aoki S, Honma M, Hayashi M, Sugamori Y, Khan M, Kariya Y, Kato G, Tabata Y, Penninger JM, Udagawa N, Aoki K, Suzuki H. Coupling of bone resorption and formation by RANKL reverse signalling. Nature. 2018;561(7722):195–200.CrossRefPubMed
30.
Zurück zum Zitat Narimiya T, Kanzaki H, Yamaguchi Y, Wada S, Katsumata Y, Tanaka K, Tomonari H. Nrf2 activation in osteoblasts suppresses osteoclastogenesis via inhibiting IL-6 expression. Bone Rep. 2019;1(11): 100228.CrossRef Narimiya T, Kanzaki H, Yamaguchi Y, Wada S, Katsumata Y, Tanaka K, Tomonari H. Nrf2 activation in osteoblasts suppresses osteoclastogenesis via inhibiting IL-6 expression. Bone Rep. 2019;1(11): 100228.CrossRef
Metadaten
Titel
Denervation delays initial bone healing of rat tooth extraction socket
verfasst von
Zhenxian Sheng
Fuju Zheng
Jianbin Li
Yuxin Wang
Yi Du
Xiaohua Liu
Xijiao Yu
Publikationsdatum
13.12.2022
Verlag
Springer Nature Singapore
Erschienen in
Odontology / Ausgabe 3/2023
Print ISSN: 1618-1247
Elektronische ISSN: 1618-1255
DOI
https://doi.org/10.1007/s10266-022-00773-x

Weitere Artikel der Ausgabe 3/2023

Odontology 3/2023 Zur Ausgabe

„Übersichtlicher Wegweiser“: Lauterbachs umstrittener Klinik-Atlas ist online

17.05.2024 Klinik aktuell Nachrichten

Sie sei „ethisch geboten“, meint Gesundheitsminister Karl Lauterbach: mehr Transparenz über die Qualität von Klinikbehandlungen. Um sie abzubilden, lässt er gegen den Widerstand vieler Länder einen virtuellen Klinik-Atlas freischalten.

Klinikreform soll zehntausende Menschenleben retten

15.05.2024 Klinik aktuell Nachrichten

Gesundheitsminister Lauterbach hat die vom Bundeskabinett beschlossene Klinikreform verteidigt. Kritik an den Plänen kommt vom Marburger Bund. Und in den Ländern wird über den Gang zum Vermittlungsausschuss spekuliert.

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Ein Drittel der jungen Ärztinnen und Ärzte erwägt abzuwandern

07.05.2024 Klinik aktuell Nachrichten

Extreme Arbeitsverdichtung und kaum Supervision: Dr. Andrea Martini, Sprecherin des Bündnisses Junge Ärztinnen und Ärzte (BJÄ) über den Frust des ärztlichen Nachwuchses und die Vorteile des Rucksack-Modells.

Update Zahnmedizin

Bestellen Sie unseren kostenlosen Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.