Denervation delays initial bone healing of rat tooth extraction socket.
Denervation
Nrf2
Osteoclast
Socket healing
Tooth extraction
Journal
Odontology
ISSN: 1618-1255
Titre abrégé: Odontology
Pays: Japan
ID NLM: 101134822
Informations de publication
Date de publication:
Jul 2023
Jul 2023
Historique:
received:
21
07
2022
accepted:
20
11
2022
medline:
5
6
2023
pubmed:
14
12
2022
entrez:
13
12
2022
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 36512167
doi: 10.1007/s10266-022-00773-x
pii: 10.1007/s10266-022-00773-x
doi:
Substances chimiques
NF-E2-Related Factor 2
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
640-648Subventions
Organisme : Natural Science Foundation of Shandong Province
ID : ZR2020MH182
Organisme : Natural Science Foundation of Shandong Province
ID : ZR2021MH230
Organisme : Clinical medicine science and technology innovation plan of Jinan
ID : 202019068
Organisme : Clinical medicine science and technology innovation plan of Jinan
ID : 2022-1-35
Organisme : the Dean's Research Fund of Jinan Stomatological Hospital
ID : 202102
Informations de copyright
© 2022. The Author(s), under exclusive licence to The Society of The Nippon Dental University.
Références
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.
doi: 10.1002/advs.202003390
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.
doi: 10.1007/s10735-015-9611-x
pubmed: 25663522
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.
doi: 10.1111/jre.12472
pubmed: 28621056
Tonelli C, Chio IIC, Tuveson DA. Transcriptional regulation by Nrf2. Antioxid Redox Signal. 2018;29:1727–45.
doi: 10.1089/ars.2017.7342
pubmed: 28899199
pmcid: 6208165
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.
doi: 10.1016/j.bbamcr.2018.02.010
pubmed: 29499228
He F, Antonucci L, Karin M. NRF2 as a regulator of cell metabolism and inflammation in cancer. Carcinogenesis. 2020;41:405–16.
doi: 10.1093/carcin/bgaa039
pubmed: 32347301
pmcid: 7298623
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.
doi: 10.1172/JCI79735
pubmed: 25798616
pmcid: 4396467
Sun YX, Xu AH, Yang Y, Li J. Role of Nrf2 in bone metabolism. J Biomed Sci. 2015;22:101.
doi: 10.1186/s12929-015-0212-5
pubmed: 26511009
pmcid: 4625735
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.
doi: 10.1016/j.redox.2020.101845
pubmed: 33373776
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.
doi: 10.14814/phy2.13064
pubmed: 28039408
pmcid: 5210374
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.
doi: 10.1590/1678-7757-2022-0010
pubmed: 35830122
pmcid: 9275398
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.
doi: 10.1038/s41598-020-62107-7
pubmed: 32198458
pmcid: 7083939
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.
doi: 10.1111/nyas.14120
pubmed: 31095746
Tomlinson RE, Christiansen BA, Giannone AA, Genetos DC. The role of nerves in skeletal development, adaptation, and aging. Front Endocrinol (Lausanne). 2020;11:646.
doi: 10.3389/fendo.2020.00646
pubmed: 33071963
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.
doi: 10.1038/s41467-018-08097-7
pubmed: 30643142
pmcid: 6331599
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.
doi: 10.1016/S8756-3282(00)00282-9
pubmed: 10831939
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.
doi: 10.1007/s10735-016-9697-9
pubmed: 27681986
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.
doi: 10.1111/nyas.14540
pubmed: 33301204
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.
doi: 10.1111/j.1600-0714.1992.tb00092.x
pubmed: 1602406
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.
doi: 10.1016/j.bone.2020.115611
pubmed: 32829042
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.
doi: 10.7150/ijms.31883
pubmed: 31337956
pmcid: 6643106
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: 28280758
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.
doi: 10.3389/fendo.2022.813057
pubmed: 35282459
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.
doi: 10.1016/j.bone.2014.12.066
pubmed: 25576674
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.
doi: 10.1016/j.redox.2019.101309
pubmed: 31487581
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.
doi: 10.1186/s12974-022-02400-6
pubmed: 35130906
pmcid: 8822843
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.
doi: 10.3390/biom11070923
pubmed: 34206421
pmcid: 8301948
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: 34091586
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.
doi: 10.1038/s41586-018-0482-7
pubmed: 30185903
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.
doi: 10.1016/j.bonr.2019.100228