Alternation of extracellular matrix remodeling and apoptosis by activation of the aryl hydrocarbon receptor pathway in human periodontal ligament cells

Journal of Cellular Biochemistry

Volumn 113, Issue 10, 2012, Pages 3093-3103

  Tomokiyo, Atsushi ^a   Maeda, Hidefumi ^a   Fujii, Shinsuke ^a   Monnouchi, Satoshi ^a   Wada, Naohisa ^a   Hori, Kiyomi ^a   Koori, Katsuaki ^a   Yamamoto, Naohide ^a   Teramatsu, Yoko ^a   Akamine, Akifumi ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Alpha smooth muscle actin; aryl hydrocarbon receptor; collagen type I; matrix metalloproteinase 1; Periodontal ligament

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CASPASE 3; CASPASE 7; COLLAGEN TYPE 1; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; INTERSTITIAL COLLAGENASE; LIPOCORTIN 5;

ADOLESCENT; ADULT; APOPTOSIS; ARTICLE; CELL COUNT; CELL NUCLEUS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; PERIODONTAL DISEASE; PERIODONTAL LIGAMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STAINING;

EID: 84865014810     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24186     Document Type: Article

References (70)

1. Abbott BD, Birnbaum LS,. 1990. TCDD-induced altered expression of growth factors may have a role in producing cleft palate and enhancing the incidence of clefts after coadministration of retinoic acid and TCDD. Toxicol Appl Pharmacol 106: 418-432.
2. Agarwal C, Britton ZT, Alaseirlis DA, Li Y, Wang JHC,. 2006. Healing and normal fibroblasts exhibit differential proliferation, collagen production, a-SMA expression, and contraction. Ann Biomed Eng 34: 653-659.
3. Alaluusua S, Lukinmaa PL,. 2000. Developmental dental toxicity of dioxin and related compoundsâ€"A review. Int Dent J 56: 323-331.
4. Alvares O, Klebe R, Grant G, Cochran DL,. 1995. Growth factor effects on the expression of collagenase and TIMP-1 in periodontal ligament cells. J Periodontol 66: 552-558.
5. Arora PD, McCulloch CA,. 1994. Dependence of collagen remodelling on alpha-smooth muscle actin expression by fibroblasts. J Cell Physiol 159: 161-175.
6. Becker J, Schuppan D, Rabanus JP, Rauch R, Niechoy U, Gelderblom HR,. 1991. Immunoelectron microscopic localization of collagens type I, V, VI and of procollagen type III in human periodontal ligament and cementum. J Histochem Cytochem 39: 103-110.
7. Bhattacharyya K, Brake P, Eltom SE, Otto S, Jefcoate CR,. 1995. Identification of a rat adrenal cytochrome P450 active in polycyclic hydrocarbon metabolism as rat CYP1B1. Demonstration of a unique tissue-specific pattern of hormonal and aryl hydrocarbon receptor-linked regulation. J Biol Chem 270: 11595-11602.
8. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE,. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106: 761-771.
9. Butler WT, Birkedal-Hansen H, Beegle WF, Taylor RE, Chung E,. 1975. Proteins of the periodontium. Identification of collagens with the [alpha1(I)]2alpha2 and [alpha1(III)]3 structures in bovine periodontal ligament. J Biol Chem 250: 8907-8912.
10. Carnes DL, Maeder CL, Graves DT,. 1997. Cells with osteoblastic phenotypes can be explanted from human gingiva and periodontal ligament. J Periodontol 68: 701-707.
11. Connor NS, Aubin JE, Sodek J,. 1983. Independent expression of type I collagen and fibronectin by normal fibroblast-like cells. J Cell Sci 63: 233-244.
12. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G,. 1993. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 122: 103-111.
13. Desmouliere A, Chaponnier C, Gabbiani G,. 2005. Tissue repair, contraction, and the myofibroblast. Wound Repair Regen 13: 7-12.
14. Fernandez-Salguero PM, Hilbert DM, Rudikoff S, Ward JM, Gonzalez FJ,. 1996. Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol Appl Pharmacol 140: 173-179.
15. Freeman E,. 1994. Peridontium. In:, Ten Cate AR, editor. Oral histology: Development, structure, and function. St. Louis: Mosby. pp 276-312.
16. Fujii S, Maeda H, Wada N, Kano Y, Akamine A,. 2006. Establishing and characterizing human periodontal ligament fibroblasts immortalized by SV40T-antigen and hTERT gene transfer. Cell Tissue Res 324: 117-125.
17. Fujii S, Maeda H, Wada N, Tomokiyo A, Saito M, Akamine A,. 2008. Investigating a clonal human periodontal ligament progenitor/stem cell line in vitro and in vivo. J Cell Physiol 215: 743-749.
18. Fujii S, Maeda H, Tomokiyo A, Monnouchi S, Hori K, Wada N, Akamine A,. 2010. Effects of TGF-β1 on the proliferation and differentiation of human periodontal ligament cells and a human periodontal ligament stem/progenitor cell line. Cell Tissue Res 342: 233-242.
19. Galis ZS, Sukhova GK, Lark MW, Libby P,. 1994. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest 94: 2493-2503.
20. Gramatzki D, Pantazis G, Schittenhelm J, Tabatabai G, Köhle C, Wick W, Schwarz M, Weller M, Tritschler I,. 2004. Aryl hydrocarbon receptor inhibition downregulates the TGF-beta/Smad pathway in human glioblastoma cells. Toxicology 199: 35-46.
21. Gu Y, Hamajima N, Ihara Y,. 2000. Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry 39: 4267-4275.
22. Guan SM, Shu L, Fu SM, Liu B, Xu XL, Wu JZ,. 2009. Prevotella intermedia upregulates MMP-1 and MMP-8 expression in human periodontal ligament cells. FEMS Microbiol Lett 299: 214-222.
23. Ikuta T, Kobayashi Y, Kawajiri K,. 2004. Cell density regulates intracellular localization of aryl hydrocarbon receptor. J Biol Chem 279: 19209-19216.
24. Ishii Y, Ogura T, Tatemichi M, Fujisawa H, Otsuka F, Esumi H,. 2003. Induction of matrix metalloproteinase gene transcription by nitric oxide and mechanisms of MMP-1 gene induction in human melanoma cell lines. Int J Cancer 103: 161-168.
25. Jan J, Vrbic V,. 2000. Polychlorinated biphenyls cause developmental enamel defects in children. Caries Res 34: 469-473.
26. Jiang Y, Rao K, Yang G, Chen X, Wang Q, Liu A, Zheng H, Yuan J,. 2012. Benzo(a)pyrene induces p73 mRNA expression and necrosis in human lung adenocarcinoma H1299 cells. Environ Toxicol 27: 202-210.
27. Kamada S, Kikkawa U, Tsujimoto Y, Hunter T,. 2005. Nuclear translocation of caspase-3 is dependent on its proteolytic activation and recognition of a substrate-like protein(s). J Biol Chem 280: 857-860.
28. Karchner SI, Franks DG, Powell WH, Hahn ME,. 2002. Regulatory interactions among three members of the vertebrate aryl hydrocarbon receptor family: AHR repressor, AHR1, and AHR2. J Biol Chem 277: 6949-6959.
29. Kattainen H, Tuukkanen J, Simanainen U, Tuomisto JT, Kovero O, Lukinmaa PL, Alaluusua S, Tuomisto J, Viluksela M,. 2001. In utero/lactational 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure impairs molar tooth development in rats. Toxicol Appl Pharmacol 174: 216-224.
30. Kerrigan JJ, Mansell JP, Sandy JR,. 2000. Matrix turnover. J Orthod 27: 227-233.
31. Kim JY, Chung JY, Park JE, Lee SG, Kim YJ, Cha MS, Han MS, Lee HJ, Yoo YH, Kim JM,. 2007. Benzo[a]pyrene induces apoptosis in RL95-2 human endometrial cancer cells by cytochrome P450 1A1 activation. Endocrinology 148: 5112-5122.
32. Ko CB, Kim SJ, Park C, Kim BR, Shin CH, Choi S, Chung SY, Noh JH, Jeun JH, Kim NS, Park R,. 2004. Benzo(a)pyrene-induced apoptotic death of mouse hepatoma Hepa1c1c7 cells via activation of intrinsic caspase cascade and mitochondrial dysfunction. Toxicology 199: 35-46.
33. Leake A, Morris CM, Whateley J,. 2000. Brain matrix metalloproteinase 1 levels are elevated in Alzheimer's disease. Neurosci Lett 291: 201-203.
34. Lei W, Yu R, Mandlekar S, Kong AN,. 1998. Induction of apoptosis and activation of interleukin 1β-converting enzyme/Ced-3 protease (caspase-3) and c-Jun NH2-terminal kinase 1 by benzo(a)pyrene. Cancer Res 58: 2102-2106.
35. Lekic P, Rojas J, Birek C, Tenenbaum H, McCulloch CA,. 2001. Phenotypic comparison of periodontal ligament cells in vivo and in vitro. J Periodontal Res 36: 71-79.
36. Loro L, Vintermyr OK, Johannessen AC,. 2005. Apoptosis in normal and diseased oral tissues. Oral Dis 11: 274-287.
37. Ma Q,. 2007. Aryl hydrocarbon receptor degradation-promoting factor (ADPF) and the control of the xenobiotic response. Mol Interv 7: 133-137.
38. Maeda S, Sawai T, Uzuki M, Takahashi Y, Omoto H, Seki M, Sakurai M,. 1995. Determination of interstitial collagenase (MMP-1) in patients with rheumatoid arthritis. Ann Rheum Dis 54: 970-975.
39. Maeda H, Tomokiyo A, Koori K, Monnouchi S, Fujii S, Wada N, Kono K, Yamamoto N, Saito T, Akamine A,. 2011. An in vitro evaluation of two resin-based sealers on proliferation and differentiation of human periodontal ligament cells. Int Endod J 44: 425-431.
40. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, Green DR,. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: Inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182: 1545-1556.
41. Meng D, Lv DD, Zhuang X, Sun H, Fan L, Shi XL, Fang J,. 2009. Benzo[a]pyrene induces expression of matrix metalloproteinases and cell migration and invasion of vascular smooth muscle cells. Toxicol Lett 184: 44-49.
42. Mimura J, Ema M, Sogawa K, Fujii-Kuriyama Y,. 1999. Identification of a novel mechanism of regulation of Ah (dioxin) receptor function. Genes Dev 13: 20-25.
43. Murphy KA, Villano CM, Dorn R, White LA,. 2004. Interaction between the aryl hydrocarbon receptor and retinoic acid pathways increases matrix metalloproteinase-1 expression in keratinocytes. J Biol Chem 279: 25284-25293.
44. Murray GI, Melvin WT, Greenlee WF, Burke MD,. 2001. Regulation, function, and tissue-specific expression of cytochrome P450 CYP1B1. Annu Rev Pharmacol Toxicol 41: 297-316.
45. Nebert DW, Roe AL, Dieter MZ, Solis WA, Yang Y, Dalton TP,. 2000. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem Pharmacol 59: 65-85.
46. Nemoto T, Kajiya H, Tsuzuki T, Takahashi Y, Okabe K,. 2010. Differential induction of collagens by mechanical stress in human periodontal ligament cells. Arch Oral Biol 55: 981-987.
47. Olaso E, Lin HC, Wang LH, Friedman SL,. 2011. Impaired dermal wound healing in discoidin domain receptor 2-deficient mice associated with defective extracellular matrix remodeling. Fibrogenesis Tissue Repair 4: 5.
48. Partanen AM, Kiukkonen A, Sahlberg C, Alaluusua S, Thesleff I, Pohjanvirta R, Lukinmaa PL,. 2004. Developmental toxicity of dioxin to mouse embryonic teeth in vitro: Arrest of tooth morphogenesis involves stimulation of apoptotic program in the dental epithelium. Toxicol Appl Pharmacol 194: 24-33.
49. Perera KA, Tonge CH,. 1981. Metabolic turnover of collagen in the mouse molar periodontal ligament during tooth eruption. J Anat 133: 359-370.
50. Pohjanvirta R, Tuomisto J,. 1994. Short-term toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in laboratory animals: Effects, mechanisms, and animal models. Pharmacol Rev 46: 483-549.
51. Reed JC,. 2000. Mechanisms of apoptosis. Am J Pathol 157: 1415-1430.
52. Reynolds JJ, Hembry RM, Meikle MC,. 1994. Connective tissue degradation in health and periodontal disease and the roles of matrix metalloproteinases and their natural inhibitors. Adv Dent Res 8: 312-319.
53. Rowlands JC, Gustafsson JA,. 1997. Aryl hydrocarbon receptor-mediated signal transduction. Crit Rev Toxicol 27: 109-134.
54. Salas VM, Burchiel SW,. 1998. Apoptosis in Daudi human B cells in response to benzo[a]pyrene and benzo[a]pyrene-7,8-dihydrodiol. Toxicol Appl Pharmacol 151: 367-376.
55. Sculean A, Junker R, Donos N, Berakdar M, Brecx M, Dünker N,. 2002. Immunohistochemical evaluation of matrix molecules associated with wound healing following regenerative periodontal treatment in monkeys. Clin Oral Investig 6: 175-182.
56. Shimizu K, Nakata S, Murakami T, Tamari K, Takahama Y, Akamine A, Aono M,. 1992. Long-term occlusal guidance of a severely intoxicated patient with yusho (PCB poisoning): A case report. Am J Orthod Dentofacial Orthop 101: 393-402.
57. Shimono M, Ishikawa T, Ishikawa H, Matsuzaki H, Hashimoto S, Muramatsu T, Shima K, Matsuzaka K, Inoue T,. 2003. Regulatory mechanisms of periodontal regeneration. Microsc Res Technol 60: 491-502.
58. Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G,. 1986. A monoclonal antibody against α-smooth muscle actin: A new probe for smooth muscle differentiation. J. Cell Biol 103: 2787-2796.
59. Slee EA, Adrain C, Martin SJ,. 2001. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol Chem 276: 7320-7326.
60. Sodek J, Limeback HF,. 1979. Comparison of the rates of synthesis, conversion, and maturation of type I and type III collagens in rat periodontal tissues. J Biol Chem 254: 10496-10502.
61. Solhaug A, OvrebÃ̧ S, Mollerup S, LÃ¥g M, Schwarze PE, Nesnow S, Holme JA,. 2005. Role of cell signaling in B[a]P-induced apoptosis: Characterization of unspecific effects of cell signaling inhibitors and apoptotic effects of B[a]P metabolites. Chem Biol Interact 151: 101-119.
62. Tampio M, Loikkanen J, Myllynen P, Mertanen A, Vähäkangas KH,. 2008. Benzo(a)pyrene increases phosphorylation of p53 at serine 392 in relation to p53 induction and cell death in MCF-7 cells. Toxicol Lett 178: 152-159.
63. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA,. 2002. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3: 349-363.
64. Tomokiyo A, Maeda H, Fujii S, Wada N, Shima K, Akamine A,. 2008. Development of a multipotent clonal human periodontal ligament cell line. Differentiation 76: 337-347.
65. Uno S, Dalton TP, Derkenne S, Curran CP, Miller ML, Shertzer HG, Nebert DW,. 2004. Oral exposure to benzo[a]pyrene in the mouse: Detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol. Pharmacol 65: 1225-1237.
66. Villano CM, Murphy KA, Akintobi A, White LA,. 2006. 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD) induces matrix metalloproteinase (MMP) expression and invasion in A2058 melanoma cells. Toxicol Appl Pharmacol 210: 212-224.
67. Wanner R, Brömmer S, Czarnetzki BM, Rosenbach T,. 1995. The differentiation-related upregulation of aryl hydrocarbon receptor transcript levels is suppressed by retinoic acid. Biochem Biophys Res Commun 209: 706-711.
68. Wu J, Ramesh A, Nayyar T, Hood DB,. 2003. Assessment of metabolites and AhR and CYP1A1 mRNA expression subsequent to prenatal exposure to inhaled benzo(a)pyrene. Int J Dev Neurosci 21: 333-346.
69. Yang JH, Lee HG,. 2010. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptosis of articular chondrocytes in culture. Chemosphere 79: 278-284.
70. Zhang JH, Dong Z, Chu L,. 2010. Hydrogen sulfide induces apoptosis in human periodontium cells. J Periodontal Res 45: 71-78.