Benzo[a]pyrene/aryl hydrocarbon receptor signaling inhibits osteoblastic differentiation and collagen synthesis of human periodontal ligament cells

Journal of Periodontal Research

Volumn 51, Issue 6, 2016, Pages 779-788

  Monnouchi, S ^a   Maeda, H ^b   Yuda, A ^a   Serita, S ^a   Wada, N ^b   Tomokiyo, A ^b   Akamine, A ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY HOSPITAL   (Japan)

Author keywords

aryl hydrocarbon receptor; benzo a pyrene; periodontal ligament

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; COLLAGEN; TRANSCRIPTOME;

BIOSYNTHESIS; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; HUMAN; METABOLISM; OSTEOBLAST; PERIODONTAL LIGAMENT; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

BENZO(A)PYRENE; CELL DIFFERENTIATION; CELLS, CULTURED; COLLAGEN; HUMANS; OSTEOBLASTS; PERIODONTAL LIGAMENT; RECEPTORS, ARYL HYDROCARBON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84953432889     PISSN: 00223484     EISSN: 16000765     Source Type: Journal    
DOI: 10.1111/jre.12355     Document Type: Article

References (52)

1. Safe S. Molecular biology of the Ah receptor and its role in carcinogenesis. Toxicol Lett 2001;120:1–7.
2. Mimura J, Fujii-Kuriyama Y. Functional role of AhR in the expression of toxic effects by TCDD. Biochim Biophys Acta 2003;1619:263–268.
3. Bagaitkar J, Daep CA, Patel CK, Renaud DE, Demuth DR, Scott DA. Tobacco smoke augments Porphyromonas gingivalis-Streptococcus gordonii biofilm formation. PLoS One 2011;6:e27386.
4. Hollenbach KA, Barrett-Connor E, Edelstein SL, Holbrook T. Cigarette smoking and bone mineral density in older men and women. Am J Public Health 1993;83:1265–1270.
5. Franceschi S, Schinella D, Bidoli E et al. The influence of body size, smoking, and diet on bone density in pre- and postmenopausal women. Epidemiology 1996;7:411–414.
6. Olofsson H, Byberg L, Mohsen R, Melhus H, Lithell H, Michaelsson K. Smoking and the risk of fracture in older men. J Bone Miner Res 2005;20:1208–1215.
7. Denison MS, Pandini A, Nagy SR, Baldwin EP, Bonati L. Ligand binding and activation of the Ah receptor. Chem Biol Interact 2002;141:3–24.
8. Kasai A, Hiramatsu N, Hayakawa K, Yao J, Maeda S, Kitamura M. High levels of dioxin-like potential in cigarette smoke evidenced by in vitro and in vivo biosensing. Cancer Res 2006;66:7143–7150.
9. Ma Q, Lu AY. Origins of individual variability in P4501A induction. Chem Res Toxicol 2003;16:249–260.
10. Mimura J, Ema M, Sogawa K, Fujii-Kuriyama Y. Identification of a novel mechanism of regulation of Ah (dioxin) receptor function. Genes Dev 1999;13:20–25.
11. Barouki R, Coumoul X, Fernandez-Salguero PM. The aryl hydrocarbon receptor, more than a xenobiotic-interacting protein. FEBS Lett 2007;581:3608–3615.
12. Gomez-Duran A, Carvajal-Gonzalez JM, Mulero-Navarro S, Santiago-Josefat B, Puga A, Fernandez-Salguero PM. Fitting a xenobiotic receptor into cell homeostasis: how the dioxin receptor interacts with TGFβ signaling. Biochem Pharmacol 2009;77:700–712.
13. Puga A, Marlowe J, Barnes S et al. Role of the aryl hydrocarbon receptor in cell cycle regulation. Toxicology 2002;181–182:171–177.
14. Andersson P, McGuire J, Rubio C et al. A constitutively active dioxin/aryl hydrocarbon receptor induces stomach tumors. Proc Natl Acad Sci U S A 2002;99:9990–9995.
15. Moennikes O, Loeppen S, Buchmann A et al. A constitutively active dioxin/aryl hydrocarbon receptor promotes hepatocarcinogenesis in mice. Cancer Res 2004;64:4707–4710.
16. Carvajal-Gonzalez JM, Roman AC, Cerezo-Guisado MI, Rico-Leo EM, Martin-Partido G, Fernandez-Salguero PM. Loss of dioxin-receptor expression accelerates wound healing in vivo by a mechanism involving TGFβ. J Cell Sci 2009;122:1823–1833.
17. Abbott BD, Probst MR. Developmental expression of two members of a new class of transcription factors: II. Expression of aryl hydrocarbon receptor nuclear translocator in the C57BL/6N mouse embryo. Dev Dyn 1995;204:144–155.
18. Tomokiyo A, Maeda H, Fujii S et al. Alternation of extracellular matrix remodeling and apoptosis by activation of the aryl hydrocarbon receptor pathway in human periodontal ligament cells. J Cell Biochem 2012;113:3093–3103.
19. Fujii S, Maeda H, Wada N, Kano Y, Akamine A. Establishing and characterizing human periodontal ligament fibroblasts immortalized by SV40T-antigen and hTERT gene transfer. Cell Tissue Res 2006;324:117–125.
20. Maeda H, Tomokiyo A, Fujii S, Wada N, Akamine A. Promise of periodontal ligament stem cells in regeneration of periodontium. Stem Cell Res Ther 2011;2:33.
21. Bartold PM, Narayanan AS. Biology of the Periodontal Connective Tissues. Chicago, IL: Quintessence, 1998.
22. Beertsen W, Brekelmans M, Everts V. The site of collagen resorption in the periodontal ligament of the rodent molar. Anat Rec 1978;192:305–317.
23. Sodek J, Limeback HF. Comparison of the rates of synthesis, conversion, and maturation of type I and type III collagens in rat periodontal tissues. J Biol Chem 1979;254:10496–10502.
24. Sodek J, Ferrier JM. Collagen remodelling in rat periodontal tissues: compensation for precursor reutilization confirms rapid turnover of collagen. Coll Relat Res 1988;8:11–21.
25. Bergstrom J. Cigarette smoking as risk factor in chronic periodontal disease. Community Dent Oral Epidemiol 1989;17:245–247.
26. Genco RJ, Borgnakke WS. Risk factors for periodontal disease. Periodontol 2000 2013;62:59–94.
27. Martin LA, Byrd SK, Milofsky RE. Rapid communication: effects of tobacco processing on the quantity of benzo[a]pyrene in mainstream smoke. J Toxicol Environ Health A 2003;66:1283–1286.
28. Miller KP, Ramos KS. Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metab Rev 2001;33:1–35.
29. Iqbal J, Sun L, Cao J et al. Smoke carcinogens cause bone loss through the aryl hydrocarbon receptor and induction of Cyp1 enzymes. Proc Natl Acad Sci U S A 2013;110:11115–11120.
30. Kim SH, Henry EC, Kim DK et al. Novel compound 2-methyl-2H-pyrazole-3-carboxylic acid (2-methyl-4-o-tolylazo-phenyl)-amide (CH-223191) prevents 2,3,7,8-TCDD-induced toxicity by antagonizing the aryl hydrocarbon receptor. Mol Pharmacol 2006;69:1871–1878.
31. Maeda H, Nakano T, Tomokiyo A et al. Mineral trioxide aggregate induces bone morphogenetic protein-2 expression and calcification in human periodontal ligament cells. J Endod 2010;36:647–652.
32. Monnouchi S, Maeda H, Fujii S, Tomokiyo A, Kono K, Akamine A. The roles of angiotensin II in stretched periodontal ligament cells. J Dent Res 2011;90:181–185.
33. Yuda A, Maeda H, Fujii S et al. Effect of CTGF/CCN2 on osteo/cementoblastic and fibroblastic differentiation of a human periodontal ligament stem/progenitor cell line. J Cell Physiol 2015;230:150–159.
34. Wada N, Maeda H, Hasegawa D et al. Semaphorin 3a induces mesenchymal-stem-like properties in human periodontal ligament cells. Stem Cells Dev 2014;23:2225–2236.
35. Monnouchi S, Maeda H, Yuda A et al. Mechanical induction of interleukin-11 regulates osteoblastic/cementoblastic differentiation of human periodontal ligament stem/progenitor cells. J Periodontal Res 2015;50:231–239.
36. Sugii H, Maeda H, Tomokiyo A et al. Effects of Activin A on the phenotypic properties of human periodontal ligament cells. Bone 2014;66:62–71.
37. Haverstock BD, Mandracchia VJ. Cigarette smoking and bone healing: implications in foot and ankle surgery. J Foot Ankle Surg 1998;37:69–74. discussion 78.
38. Nishimura N, Nishimura H, Ito T et al. Dioxin-induced up-regulation of the active form of vitamin D is the main cause for its inhibitory action on osteoblast activities, leading to developmental bone toxicity. Toxicol Appl Pharmacol 2009;236:301–309.
39. Singh SU, Casper RF, Fritz PC et al. Inhibition of dioxin effects on bone formation in vitro by a newly described aryl hydrocarbon receptor antagonist, resveratrol. J Endocrinol 2000;167:183–195.
40. Bronckers AL, Gay S, Finkelman RD, Butler WT. Developmental appearance of Gla proteins (osteocalcin) and alkaline phosphatase in tooth germs and bones of the rat. Bone Miner 1987;2:361–373.
41. Ryder MI. The influence of smoking on host responses in periodontal infections. Periodontol 2000 2007;43:267–277.
42. Romero A, Caceres M, Arancibia R et al. Cigarette smoke condensate inhibits collagen gel contraction and prostaglandin E production in human gingival fibroblasts. J Periodontal Res 2015;50:371–379.
43. Voronov I, Heersche JN, Casper RF, Tenenbaum HC, Manolson MF. Inhibition of osteoclast differentiation by polycyclic aryl hydrocarbons is dependent on cell density and RANKL concentration. Biochem Pharmacol 2005;70:300–307.
44. Voronov I, Li K, Tenenbaum HC, Manolson MF. Benzo[a]pyrene inhibits osteoclastogenesis by affecting RANKL-induced activation of NF-kappaB. Biochem Pharmacol 2008;75:2034–2044.
45. Gierthy JF, Silkworth JB, Tassinari M, Stein GS, Lian JB. 2,3,7,8-Tetrachlorodibenzo-p-dioxin inhibits differentiation of normal diploid rat osteoblasts in vitro. J Cell Biochem 1994;54:231–238.
46. Miettinen HM, Pulkkinen P, Jamsa T et al. Effects of in utero and lactational TCDD exposure on bone development in differentially sensitive rat lines. Toxicol Sci 2005;85:1003–1012.
47. Jiang Y, Chen X, Yang G et al. BaP-induced DNA damage initiated p53-independent necroptosis via the mitochondrial pathway involving Bax and Bcl-2. Hum Exp Toxicol 2013;32:1245–1257.
48. Kung MH, Yukata K, O'Keefe RJ, Zuscik MJ. Aryl hydrocarbon receptor-mediated impairment of chondrogenesis and fracture healing by cigarette smoke and benzo(a)pyrene. J Cell Physiol 2012;227:1062–1070.
49. Ryan EP, Holz JD, Mulcahey M, Sheu TJ, Gasiewicz TA, Puzas JE. Environmental toxicants may modulate osteoblast differentiation by a mechanism involving the aryl hydrocarbon receptor. J Bone Miner Res 2007;22:1571–1580.
50. Karimbux NY, Rosenblum ND, Nishimura I. Site-specific expression of collagen I and XII mRNAs in the rat periodontal ligament at two developmental stages. J Dent Res 1992;71:1355–1362.
51. Becker J, Schuppan D, Rabanus JP, Rauch R, Niechoy U, Gelderblom HR. Immunoelectron microscopic localization of collagens type I, V, VI and of procollagen type III in human periodontal ligament and cementum. J Histochem Cytochem 1991;39:103–110.
52. Kerrigan JJ, Mansell JP, Sandy JR. Matrix turnover. J Orthod 2000;27:227–233.