Skip to main content
Erschienen in: Inflammation Research 4/2023

13.03.2023 | Original Research Paper

SOCS2 regulates alveolar bone loss in Aggregatibacter actinomycetemcomitans-induced periodontal disease

verfasst von: Mariana Rates Gonzaga Santos, Ian de Meira Chaves, Celso Martins Queiroz-Junior, Allysson Thiago Cramer, Thales Augusto Anestino, Anna Clara Paiva Menezes dos Santos, Paulo Gaio Leite, Soraia Macari, Breno Rocha Barrioni, Marivalda de Magalhães Pereira, Mauro Martins Teixeira, Danielle da Glória de Souza, Mila Fernandes Moreira Madeira, Fabiana Simão Machado

Erschienen in: Inflammation Research | Ausgabe 4/2023

Einloggen, um Zugang zu erhalten

Abstract

Introduction

The role of suppressor of cytokine signaling 2 (SOCS2) in Aggregatibacter actinomycetemcomitans (Aa)-induced alveolar bone loss is unknown; thus, it was investigated in this study.

Methods

Alveolar bone loss was induced by infecting C57BL/6 wild-type (WT) and Socs2-knockout (Socs2−/−) mice with Aa. Bone parameters, bone loss, bone cell counts, the expression of bone remodeling markers, and cytokine profile were evaluated by microtomography, histology, qPCR, and/or ELISA. Bone marrow cells (BMC) from WT and Socs2−/− mice were differentiated in osteoblasts or osteoclasts for analysis of the expression of specific markers.

Results

Socs2−/− mice intrinsically exhibited irregular phenotypes in the maxillary bone and an increased number of osteoclasts. Upon Aa infection, SOCS2 deficiency resulted in the increased alveolar bone loss, despite decreased proinflammatory cytokine production, in comparison to the WT mice. In vitro, SOCS2 deficiency resulted in the increased osteoclasts formation, decreased expression of bone remodeling markers, and proinflammatory cytokines after Aa-LPS stimulus.

Conclusions

Collectively, data suggest that SOCS2 is a regulator of Aa-induced alveolar bone loss by controlling the differentiation and activity of bone cells, and proinflammatory cytokines availability in the periodontal microenvironment and an important target for new therapeutic strategies. Thus, it can be helpful in preventing alveolar bone loss in periodontal inflammatory conditions.
Literatur
1.
Zurück zum Zitat Åberg CH, Kelk P, Johansson A. Aggregatibacter actinomycetemcomitans: virulence of its leukotoxin and association with aggressive periodontitis. Virulence. 2015;6(3):188–95.PubMedCrossRef Åberg CH, Kelk P, Johansson A. Aggregatibacter actinomycetemcomitans: virulence of its leukotoxin and association with aggressive periodontitis. Virulence. 2015;6(3):188–95.PubMedCrossRef
2.
Zurück zum Zitat Mark Bartold P, Van Dyke TE. Host modulation: controlling the inflammation to control the infection. Periodontol 2000. 2017;75(1):317–29.PubMedCrossRef Mark Bartold P, Van Dyke TE. Host modulation: controlling the inflammation to control the infection. Periodontol 2000. 2017;75(1):317–29.PubMedCrossRef
3.
Zurück zum Zitat Haubek D, Johansson A. Pathogenicity of the highly leukotoxic JP2 clone of Aggregatibacter actinomycetemcomitans and its geographic dissemination and role in aggressive periodontitis. J Oral Microbiol. 2014;14:6. Haubek D, Johansson A. Pathogenicity of the highly leukotoxic JP2 clone of Aggregatibacter actinomycetemcomitans and its geographic dissemination and role in aggressive periodontitis. J Oral Microbiol. 2014;14:6.
4.
Zurück zum Zitat Monasterio G, Castillo F, Ibarra JP, Guevara J, Rojas L, Alvarez C, et al. Alveolar bone resorption and TH1/TH17-associated immune response triggered during Aggregatibacter actinomycetemcomitans-induced experimental periodontitis are serotype-dependent. J Periodontol. 2018;89(10):1249–61.PubMedCrossRef Monasterio G, Castillo F, Ibarra JP, Guevara J, Rojas L, Alvarez C, et al. Alveolar bone resorption and TH1/TH17-associated immune response triggered during Aggregatibacter actinomycetemcomitans-induced experimental periodontitis are serotype-dependent. J Periodontol. 2018;89(10):1249–61.PubMedCrossRef
5.
Zurück zum Zitat De Souza JAC, Nogueira AVB, De Souza PPC, Cirelli JA, Garlet GP, Rossa C. Expression of suppressor of cytokine signaling 1 and 3 in ligature-induced periodontitis in rats. Arch Oral Biol. 2011;56(10):1120–8.PubMedCrossRef De Souza JAC, Nogueira AVB, De Souza PPC, Cirelli JA, Garlet GP, Rossa C. Expression of suppressor of cytokine signaling 1 and 3 in ligature-induced periodontitis in rats. Arch Oral Biol. 2011;56(10):1120–8.PubMedCrossRef
7.
Zurück zum Zitat Rakesh K, Agrawal DK. Controlling cytokine signaling by constitutive inhibitors. Biochem Pharmacol. 2005;70(5):649–57.PubMedCrossRef Rakesh K, Agrawal DK. Controlling cytokine signaling by constitutive inhibitors. Biochem Pharmacol. 2005;70(5):649–57.PubMedCrossRef
8.
Zurück zum Zitat Fox SW, Haque SJ, Lovibond AC, Chambers TJ. The possible role of TGF-β-induced suppressors of cytokine signaling expression in osteoclast/macrophage lineage commitment In Vitro. J Immunol. 2003;170(7):3679–87.PubMedCrossRef Fox SW, Haque SJ, Lovibond AC, Chambers TJ. The possible role of TGF-β-induced suppressors of cytokine signaling expression in osteoclast/macrophage lineage commitment In Vitro. J Immunol. 2003;170(7):3679–87.PubMedCrossRef
9.
Zurück zum Zitat Santos MRG, Queiroz-Junior CM, Madeira MFM, Machado FS. Suppressors of cytokine signaling (SOCS) proteins in inflammatory bone disorders. Bone. 2020;140: 115538.PubMedCrossRef Santos MRG, Queiroz-Junior CM, Madeira MFM, Machado FS. Suppressors of cytokine signaling (SOCS) proteins in inflammatory bone disorders. Bone. 2020;140: 115538.PubMedCrossRef
10.
Zurück zum Zitat Letellier E, Haan S. SOCS2: physiological and pathological functions. Front Biosci - Elit. 2016;8(1):189–204.CrossRef Letellier E, Haan S. SOCS2: physiological and pathological functions. Front Biosci - Elit. 2016;8(1):189–204.CrossRef
11.
Zurück zum Zitat Machado FS, Johndrow JE, Esper L, Dias A, Bafica A, Serhan CN, et al. Anti-inflammatory actions of lipoxin A4 and aspirin-triggered lipoxin are SOCS-2 dependent. Nat Med. 2006;12(3):330–4.PubMedCrossRef Machado FS, Johndrow JE, Esper L, Dias A, Bafica A, Serhan CN, et al. Anti-inflammatory actions of lipoxin A4 and aspirin-triggered lipoxin are SOCS-2 dependent. Nat Med. 2006;12(3):330–4.PubMedCrossRef
12.
Zurück zum Zitat Esper L, Roman-Campos D, Lara A, Brant F, Castro LL, Barroso A, et al. Role of SOCS2 in modulating heart damage and function in a murine model of acute Chagas disease. Am J Pathol. 2012;181(1):130–40.PubMedPubMedCentralCrossRef Esper L, Roman-Campos D, Lara A, Brant F, Castro LL, Barroso A, et al. Role of SOCS2 in modulating heart damage and function in a murine model of acute Chagas disease. Am J Pathol. 2012;181(1):130–40.PubMedPubMedCentralCrossRef
13.
Zurück zum Zitat Brant F, Miranda AS, Esper L, Gualdrón-López M, Cisalpino D, de Souza DDG, et al. Suppressor of cytokine signaling 2 modulates the immune response profile and development of experimental cerebral malaria. Brain Behav Immun. 2016;54:73–85.PubMedCrossRef Brant F, Miranda AS, Esper L, Gualdrón-López M, Cisalpino D, de Souza DDG, et al. Suppressor of cytokine signaling 2 modulates the immune response profile and development of experimental cerebral malaria. Brain Behav Immun. 2016;54:73–85.PubMedCrossRef
14.
Zurück zum Zitat Cramer A, Galvão I, de Sá NV, Gaio P, de Melo Oliveira NF, Rates Gonzaga Santos M, et al. Role of Suppressor of cytokine signaling 2 during the development and resolution of an experimental arthritis. Cell Immunol. 2022;372:104476.PubMedCrossRef Cramer A, Galvão I, de Sá NV, Gaio P, de Melo Oliveira NF, Rates Gonzaga Santos M, et al. Role of Suppressor of cytokine signaling 2 during the development and resolution of an experimental arthritis. Cell Immunol. 2022;372:104476.PubMedCrossRef
15.
Zurück zum Zitat Gaio P, Gualdrón-López M, Cramer A, Esper L, de Menezes Filho JER, Cruz JS, et al. SOCS2 expression in hematopoietic and non-hematopoietic cells during Trypanosoma cruzi infection: correlation with immune response and cardiac dysfunction. Clin Immunol. 2022;234: 108913.PubMedCrossRef Gaio P, Gualdrón-López M, Cramer A, Esper L, de Menezes Filho JER, Cruz JS, et al. SOCS2 expression in hematopoietic and non-hematopoietic cells during Trypanosoma cruzi infection: correlation with immune response and cardiac dysfunction. Clin Immunol. 2022;234: 108913.PubMedCrossRef
16.
Zurück zum Zitat Monti-Rocha R, Cramer A, Leite PG, Antunes MM, Pereira RVS, Barroso A, et al. SOCS2 is critical for the balancing of immune response and oxidate stress protecting against acetaminophen-induced acute liver injury. Front Immunol. 2019;9:3134.PubMedPubMedCentralCrossRef Monti-Rocha R, Cramer A, Leite PG, Antunes MM, Pereira RVS, Barroso A, et al. SOCS2 is critical for the balancing of immune response and oxidate stress protecting against acetaminophen-induced acute liver injury. Front Immunol. 2019;9:3134.PubMedPubMedCentralCrossRef
17.
Zurück zum Zitat Cramer A, De Lima Oliveira BC, Leite PG, Rodrigues DH, Brant F, Esper L, et al. Role of SOCS2 in the regulation of immune response and development of the experimental autoimmune encephalomyelitis. Mediators Inflamm. 2019;2019:1872593.PubMedPubMedCentralCrossRef Cramer A, De Lima Oliveira BC, Leite PG, Rodrigues DH, Brant F, Esper L, et al. Role of SOCS2 in the regulation of immune response and development of the experimental autoimmune encephalomyelitis. Mediators Inflamm. 2019;2019:1872593.PubMedPubMedCentralCrossRef
18.
Zurück zum Zitat Zadjali F, Santana-Farre R, Vesterlund M, Carow B, Mirecki-Garrido M, Hernandez-Hernandez I, et al. SOCS2 deletion protects against hepatic steatosis but worsens insulin resistance in high-fat-diet-fed mice. FASEB J. 2012;26(8):3282–91.PubMedCrossRef Zadjali F, Santana-Farre R, Vesterlund M, Carow B, Mirecki-Garrido M, Hernandez-Hernandez I, et al. SOCS2 deletion protects against hepatic steatosis but worsens insulin resistance in high-fat-diet-fed mice. FASEB J. 2012;26(8):3282–91.PubMedCrossRef
19.
Zurück zum Zitat Val CH, de Oliveira MC, Lacerda DR, Barroso A, Batista NV, Menezes-Garcia Z, et al. SOCS2 modulates adipose tissue inflammation and expansion in mice. J Nutr Biochem. 2020;76: 108304.PubMedCrossRef Val CH, de Oliveira MC, Lacerda DR, Barroso A, Batista NV, Menezes-Garcia Z, et al. SOCS2 modulates adipose tissue inflammation and expansion in mice. J Nutr Biochem. 2020;76: 108304.PubMedCrossRef
20.
Zurück zum Zitat Garlet GP, Cardoso CR, Campanelli AP, Martins W, Silva JS. Expression of suppressors of cytokine signaling in diseased periodontal tissues: a stop signal for disease progression? J Periodontal Res. 2006;41(6):580–4.PubMedCrossRef Garlet GP, Cardoso CR, Campanelli AP, Martins W, Silva JS. Expression of suppressors of cytokine signaling in diseased periodontal tissues: a stop signal for disease progression? J Periodontal Res. 2006;41(6):580–4.PubMedCrossRef
21.
Zurück zum Zitat Madeira MFM, Queiroz-Junior CM, Costa GM, Werneck SMC, Cisalpino D, Garlet GP, et al. Platelet-activating factor receptor blockade ameliorates Aggregatibacter actinomycetemcomitans-induced periodontal disease in mice. Infect Immun. 2013;81(11):4244–51.PubMedPubMedCentralCrossRef Madeira MFM, Queiroz-Junior CM, Costa GM, Werneck SMC, Cisalpino D, Garlet GP, et al. Platelet-activating factor receptor blockade ameliorates Aggregatibacter actinomycetemcomitans-induced periodontal disease in mice. Infect Immun. 2013;81(11):4244–51.PubMedPubMedCentralCrossRef
22.
Zurück zum Zitat Queiroz-Junior CM, Madeira MFM, Coelho FM, Costa VV, Bessoni RLC, da Cunha Sousa LF, et al. Experimental arthritis triggers periodontal disease in mice: Involvement of TNF-α and the oral microbiota. J Immunol. 2011;187(7):3821–30.PubMedCrossRef Queiroz-Junior CM, Madeira MFM, Coelho FM, Costa VV, Bessoni RLC, da Cunha Sousa LF, et al. Experimental arthritis triggers periodontal disease in mice: Involvement of TNF-α and the oral microbiota. J Immunol. 2011;187(7):3821–30.PubMedCrossRef
23.
Zurück zum Zitat Arirachakaran P, Apinhasmit W, Paungmalit P, Jeramethakul P, Rerkyen P, Mahanonda R. Infection of human gingival fibroblasts with Aggregatibacter actinomycetemcomitans: an in vitro study. Arch Oral Biol. 2012;57(7):964–72.PubMedCrossRef Arirachakaran P, Apinhasmit W, Paungmalit P, Jeramethakul P, Rerkyen P, Mahanonda R. Infection of human gingival fibroblasts with Aggregatibacter actinomycetemcomitans: an in vitro study. Arch Oral Biol. 2012;57(7):964–72.PubMedCrossRef
25.
Zurück zum Zitat Yamashita T, Yao Z, Li F, Zhang Q, Badell IR, Schwarz EM, et al. NF-κB p50 and p52 regulate receptor activator of NF-κB ligand (RANKL) and tumor necrosis factor-induced osteoclast precursor differentiation by activating c-Fos and NFATc1. J Biol Chem. 2007;282(25):18245–53.PubMedCrossRef Yamashita T, Yao Z, Li F, Zhang Q, Badell IR, Schwarz EM, et al. NF-κB p50 and p52 regulate receptor activator of NF-κB ligand (RANKL) and tumor necrosis factor-induced osteoclast precursor differentiation by activating c-Fos and NFATc1. J Biol Chem. 2007;282(25):18245–53.PubMedCrossRef
26.
Zurück zum Zitat Walsh MC, Lee J, Choi Y. Tumor necrosis factor receptor- associated factor 6 (TRAF6) regulation of development, function, and homeostasis of the immune system. Immunol Rev. 2015;266(1):72–92.PubMedPubMedCentralCrossRef Walsh MC, Lee J, Choi Y. Tumor necrosis factor receptor- associated factor 6 (TRAF6) regulation of development, function, and homeostasis of the immune system. Immunol Rev. 2015;266(1):72–92.PubMedPubMedCentralCrossRef
27.
Zurück zum Zitat Zhou A, Yu H, Liu J, Zheng J, Jia Y, Wu B, et al. Role of hippo-YAP signaling in osseointegration by regulating osteogenesis, angiogenesis, and osteoimmunology. Front Cell Dev Biol. 2020;8:780.PubMedPubMedCentralCrossRef Zhou A, Yu H, Liu J, Zheng J, Jia Y, Wu B, et al. Role of hippo-YAP signaling in osseointegration by regulating osteogenesis, angiogenesis, and osteoimmunology. Front Cell Dev Biol. 2020;8:780.PubMedPubMedCentralCrossRef
28.
Zurück zum Zitat Alvarez C, Monasterio G, Cavalla F, Córdova LA, Hernández M, Heymann D, et al. Osteoimmunology of oral and maxillofacial diseases: translational applications based on biological mechanisms. Front Immunol. 2019;10:1664.PubMedPubMedCentralCrossRef Alvarez C, Monasterio G, Cavalla F, Córdova LA, Hernández M, Heymann D, et al. Osteoimmunology of oral and maxillofacial diseases: translational applications based on biological mechanisms. Front Immunol. 2019;10:1664.PubMedPubMedCentralCrossRef
29.
Zurück zum Zitat Metcalf D, Greenhalgh CJ, Viney E, Wilison TA, Starr R, Nicola NA, et al. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature. 2000;405(6790):1069–73.PubMedCrossRef Metcalf D, Greenhalgh CJ, Viney E, Wilison TA, Starr R, Nicola NA, et al. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature. 2000;405(6790):1069–73.PubMedCrossRef
30.
Zurück zum Zitat Lorentzon M, Greenhalgh CJ, Mohan S, Alexander WS, Ohlsson C. Reduced bone mineral density in SOCS-2-deficient mice. Pediatr Res. 2005;57(2):223–6.PubMedCrossRef Lorentzon M, Greenhalgh CJ, Mohan S, Alexander WS, Ohlsson C. Reduced bone mineral density in SOCS-2-deficient mice. Pediatr Res. 2005;57(2):223–6.PubMedCrossRef
32.
Zurück zum Zitat Ali M, Kucko N, Jansen JA, Yang F, Walboomers XF. The effect of lipoxin A4 on E. coli LPS-induced osteoclastogenesis. Clin Oral Investig. 2020;25(3):957–69.PubMedPubMedCentralCrossRef Ali M, Kucko N, Jansen JA, Yang F, Walboomers XF. The effect of lipoxin A4 on E. coli LPS-induced osteoclastogenesis. Clin Oral Investig. 2020;25(3):957–69.PubMedPubMedCentralCrossRef
33.
Zurück zum Zitat Cui K, Tang Z, Li CC, Wang T, Rao K, Wang SG, et al. Lipoxin A4 improves erectile dysfunction in rats with type i diabetes by inhibiting oxidative stress and corporal fibrosis. Asian J Androl. 2018;20(2):166–72.PubMedCrossRef Cui K, Tang Z, Li CC, Wang T, Rao K, Wang SG, et al. Lipoxin A4 improves erectile dysfunction in rats with type i diabetes by inhibiting oxidative stress and corporal fibrosis. Asian J Androl. 2018;20(2):166–72.PubMedCrossRef
34.
Zurück zum Zitat Ponzetti M, Rucci N. Updates on osteoimmunology: what’s new on the cross-talk between bone and immune system. Front Endocrinol (Lausanne). 2019;18(10):236.CrossRef Ponzetti M, Rucci N. Updates on osteoimmunology: what’s new on the cross-talk between bone and immune system. Front Endocrinol (Lausanne). 2019;18(10):236.CrossRef
36.
Zurück zum Zitat Chakravarti A, Raquil MA, Tessier P, Poubelle PE. Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood. 2009;114(8):1633–44.PubMedCrossRef Chakravarti A, Raquil MA, Tessier P, Poubelle PE. Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood. 2009;114(8):1633–44.PubMedCrossRef
37.
Zurück zum Zitat Hajishengallis G. New developments in neutrophil biology and periodontitis. Periodontol. 2000;82(1):78–92.CrossRef Hajishengallis G. New developments in neutrophil biology and periodontitis. Periodontol. 2000;82(1):78–92.CrossRef
38.
Zurück zum Zitat Hayashi T, Kaneda T, Toyama Y, Kumegawa M, Hakeda Y. Regulation of receptor activator of NF-κB ligand-induced osteoclastogenesis by endogenous interferon-β (INF-β) and suppressors of cytokine signaling (SOCS). The possible counteracting role of SOCSs in IFN-β-inhibited osteoclast formation. J Biol Chem. 2002;277(31):27880–6.PubMedCrossRef Hayashi T, Kaneda T, Toyama Y, Kumegawa M, Hakeda Y. Regulation of receptor activator of NF-κB ligand-induced osteoclastogenesis by endogenous interferon-β (INF-β) and suppressors of cytokine signaling (SOCS). The possible counteracting role of SOCSs in IFN-β-inhibited osteoclast formation. J Biol Chem. 2002;277(31):27880–6.PubMedCrossRef
39.
Zurück zum Zitat Piessevaux J, Lavens D, Montoye T, Wauman J, Catteeuw D, Vandekerckhove J, et al. Functional cross-modulation between SOCS proteins can stimulate cytokine signaling. J Biol Chem. 2006;281(44):32953–66.PubMedCrossRef Piessevaux J, Lavens D, Montoye T, Wauman J, Catteeuw D, Vandekerckhove J, et al. Functional cross-modulation between SOCS proteins can stimulate cytokine signaling. J Biol Chem. 2006;281(44):32953–66.PubMedCrossRef
40.
Zurück zum Zitat Tannahill GM, Elliott J, Barry AC, Hibbert L, Cacalano NA, Johnston JA. SOCS2 can enhance interleukin-2 (IL-2) and IL-3 signaling by accelerating SOCS3 degradation. Mol Cell Biol. 2005;25(20):9115–26.PubMedPubMedCentralCrossRef Tannahill GM, Elliott J, Barry AC, Hibbert L, Cacalano NA, Johnston JA. SOCS2 can enhance interleukin-2 (IL-2) and IL-3 signaling by accelerating SOCS3 degradation. Mol Cell Biol. 2005;25(20):9115–26.PubMedPubMedCentralCrossRef
41.
Zurück zum Zitat Dif F, Saunier E, Demeneix B, Kelly PA, Edery M. Cytokine-inducible SH2-containing protein suppresses PRL signaling by binding the PRL receptor. Endocrinology. 2001;142(12):5286–93.PubMedCrossRef Dif F, Saunier E, Demeneix B, Kelly PA, Edery M. Cytokine-inducible SH2-containing protein suppresses PRL signaling by binding the PRL receptor. Endocrinology. 2001;142(12):5286–93.PubMedCrossRef
42.
Zurück zum Zitat Lomaga MA, Yeh WC, Sarosi I, Duncan GS, Furlonger C, Ho A, et al. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 1999;13(8):1015–24.PubMedPubMedCentralCrossRef Lomaga MA, Yeh WC, Sarosi I, Duncan GS, Furlonger C, Ho A, et al. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 1999;13(8):1015–24.PubMedPubMedCentralCrossRef
43.
Zurück zum Zitat McBerry C, Gonzalez RMS, Shryock N, Dias A, Aliberti J. SOCS2-induced proteasome-dependent TRAF6 degradation: a common anti-inflammatory pathway for control of innate immune responses. PLoS ONE. 2012;7(6): e38384.PubMedPubMedCentralCrossRef McBerry C, Gonzalez RMS, Shryock N, Dias A, Aliberti J. SOCS2-induced proteasome-dependent TRAF6 degradation: a common anti-inflammatory pathway for control of innate immune responses. PLoS ONE. 2012;7(6): e38384.PubMedPubMedCentralCrossRef
44.
Zurück zum Zitat Yu TY, Kondo T, Matsumoto T, Fujii-Kuriyama Y, Imai Y. Aryl hydrocarbon receptor catabolic activity in bone metabolism is osteoclast dependent in vivo. Biochem Biophys Res Commun. 2014;450(1):416–22.PubMedCrossRef Yu TY, Kondo T, Matsumoto T, Fujii-Kuriyama Y, Imai Y. Aryl hydrocarbon receptor catabolic activity in bone metabolism is osteoclast dependent in vivo. Biochem Biophys Res Commun. 2014;450(1):416–22.PubMedCrossRef
45.
Zurück zum Zitat Szymczyk KH, Freeman TA, Adams CS, Srinivas V, Steinbeck MJ. Active caspase-3 is required for osteoclast differentiation. J Cell Physiol. 2006;209(3):836–44.PubMedCrossRef Szymczyk KH, Freeman TA, Adams CS, Srinivas V, Steinbeck MJ. Active caspase-3 is required for osteoclast differentiation. J Cell Physiol. 2006;209(3):836–44.PubMedCrossRef
46.
Zurück zum Zitat Izawa T, Arakaki R, Mori H, Tsunematsu T, Kudo Y, Tanaka E, et al. The nuclear receptor AhR controls bone homeostasis by regulating osteoclast differentiation via the RANK/c-Fos signaling Axis. J Immunol. 2016;197(12):4639–50.PubMedPubMedCentralCrossRef Izawa T, Arakaki R, Mori H, Tsunematsu T, Kudo Y, Tanaka E, et al. The nuclear receptor AhR controls bone homeostasis by regulating osteoclast differentiation via the RANK/c-Fos signaling Axis. J Immunol. 2016;197(12):4639–50.PubMedPubMedCentralCrossRef
47.
Zurück zum Zitat Kinjyo I, Hanada T, Inagaki-Ohara K, Mori H, Aki D, Ohishi M, et al. SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity. 2002;17(5):583–91.PubMedCrossRef Kinjyo I, Hanada T, Inagaki-Ohara K, Mori H, Aki D, Ohishi M, et al. SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity. 2002;17(5):583–91.PubMedCrossRef
48.
Zurück zum Zitat Kimura A, Naka T, Muta T, Takeuchi O, Akira S, Kawase I, et al. Suppressor of cytokine signaling-1 selectively inhibits LPS-induced IL-6 production by regulating JAK-STAT. Proc Natl Acad Sci U S A. 2005;102(47):17089–94.PubMedPubMedCentralCrossRef Kimura A, Naka T, Muta T, Takeuchi O, Akira S, Kawase I, et al. Suppressor of cytokine signaling-1 selectively inhibits LPS-induced IL-6 production by regulating JAK-STAT. Proc Natl Acad Sci U S A. 2005;102(47):17089–94.PubMedPubMedCentralCrossRef
49.
Zurück zum Zitat Huang S, Liu K, Cheng A, Wang M, Cui M, Huang J, et al. SOCS proteins participate in the regulation of innate immune response caused by viruses. Front Immunol. 2020;25(11): 558341.CrossRef Huang S, Liu K, Cheng A, Wang M, Cui M, Huang J, et al. SOCS proteins participate in the regulation of innate immune response caused by viruses. Front Immunol. 2020;25(11): 558341.CrossRef
50.
Zurück zum Zitat Posselt G, Schwarz H, Duschl A, Horejs-Hoeck J. Suppressor of cytokine signaling 2 is a feedback inhibitor of TLR-induced activation in human monocyte-derived dendritic cells. J Immunol. 2011;187(6):2875–84.PubMedCrossRef Posselt G, Schwarz H, Duschl A, Horejs-Hoeck J. Suppressor of cytokine signaling 2 is a feedback inhibitor of TLR-induced activation in human monocyte-derived dendritic cells. J Immunol. 2011;187(6):2875–84.PubMedCrossRef
51.
Zurück zum Zitat Madeira MFM, Queiroz-Junior CM, Costa GM, Santos PC, Silveira EM, Garlet GP, et al. MIF induces osteoclast differentiation and contributes to progression of periodontal disease in mice. Microbes Infect. 2012;14(2):198–206.PubMedCrossRef Madeira MFM, Queiroz-Junior CM, Costa GM, Santos PC, Silveira EM, Garlet GP, et al. MIF induces osteoclast differentiation and contributes to progression of periodontal disease in mice. Microbes Infect. 2012;14(2):198–206.PubMedCrossRef
Metadaten
Titel
SOCS2 regulates alveolar bone loss in Aggregatibacter actinomycetemcomitans-induced periodontal disease
verfasst von
Mariana Rates Gonzaga Santos
Ian de Meira Chaves
Celso Martins Queiroz-Junior
Allysson Thiago Cramer
Thales Augusto Anestino
Anna Clara Paiva Menezes dos Santos
Paulo Gaio Leite
Soraia Macari
Breno Rocha Barrioni
Marivalda de Magalhães Pereira
Mauro Martins Teixeira
Danielle da Glória de Souza
Mila Fernandes Moreira Madeira
Fabiana Simão Machado
Publikationsdatum
13.03.2023
Verlag
Springer International Publishing
Erschienen in
Inflammation Research / Ausgabe 4/2023
Print ISSN: 1023-3830
Elektronische ISSN: 1420-908X
DOI
https://doi.org/10.1007/s00011-023-01711-5

Weitere Artikel der Ausgabe 4/2023

Inflammation Research 4/2023 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Bei Herzinsuffizienz muss „Eisenmangel“ neu definiert werden!

16.05.2024 Herzinsuffizienz Nachrichten

Bei chronischer Herzinsuffizienz macht es einem internationalen Expertenteam zufolge wenig Sinn, die Diagnose „Eisenmangel“ am Serumferritin festzumachen. Das Team schlägt vor, sich lieber an die Transferrinsättigung zu halten.

Herzinfarkt mit 85 – trotzdem noch intensive Lipidsenkung?

16.05.2024 Hypercholesterinämie Nachrichten

Profitieren nach einem akuten Myokardinfarkt auch Betroffene über 80 Jahre noch von einer intensiven Lipidsenkung zur Sekundärprävention? Um diese Frage zu beantworten, wurden jetzt Registerdaten aus Frankreich ausgewertet.

ADHS-Medikation erhöht das kardiovaskuläre Risiko

16.05.2024 Herzinsuffizienz Nachrichten

Erwachsene, die Medikamente gegen das Aufmerksamkeitsdefizit-Hyperaktivitätssyndrom einnehmen, laufen offenbar erhöhte Gefahr, an Herzschwäche zu erkranken oder einen Schlaganfall zu erleiden. Es scheint eine Dosis-Wirkungs-Beziehung zu bestehen.

Erstmanifestation eines Diabetes-Typ-1 bei Kindern: Ein Notfall!

16.05.2024 DDG-Jahrestagung 2024 Kongressbericht

Manifestiert sich ein Typ-1-Diabetes bei Kindern, ist das ein Notfall – ebenso wie eine diabetische Ketoazidose. Die Grundsäulen der Therapie bestehen aus Rehydratation, Insulin und Kaliumgabe. Insulin ist das Medikament der Wahl zur Behandlung der Ketoazidose.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.