Aryl hydrocarbon receptor-mediated impairment of chondrogenesis and fracture healing by cigarette smoke and benzo(α)pyrene

Journal of Cellular Physiology

Volumn 227, Issue 3, 2012, Pages 1062-1070

  Kung, Ming H ^a   Yukata, Kiminori ^a   O'Keefe, Regis J ^a   Zuscik, Michael J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CIGARETTE SMOKE; CYTOCHROME P450 1A1;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDROGENESIS; FRACTURE NONUNION; HEALING IMPAIRMENT; IN VITRO STUDY; IN VIVO STUDY; MESENCHYME CELL; MOUSE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TIBIA FRACTURE;

ANIMALS; BENZO(A)PYRENE; CELL SURVIVAL; CHONDROCYTES; CHONDROGENESIS; DISEASE MODELS, ANIMAL; FEMORAL FRACTURES; FRACTURE HEALING; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, ARYL HYDROCARBON; TIBIAL FRACTURES; TOBACCO SMOKE POLLUTION;

EID: 84155192347     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22819     Document Type: Article

References (54)

1. Allen JW, Johnson RS, Bhatia SN. 2005. Hypoxic inhibition of 3-methylcholanthrene-induced CYP1A1 expression is independent of HIF-1alpha. Toxicol Lett 155: 151-159.
2. Balatsouka D, Gotfredsen K, Lindh CH, Berglundh T. 2005a. The impact of nicotine on bone healing and osseointegration. Clin Oral Implants Res 16: 268-276.
3. Balatsouka D, Gotfredsen K, Lindh CH, Berglundh T. 2005b. The impact of nicotine on osseointegration. An experimental study in the femur and tibia of rabbits. Clin Oral Implants Res 16: 389-395.
4. Bonnarens F, Einhorn TA. 1984. Production of a standard closed fracture in laboratory animal bone. J Orthop Res 2: 97-101.
5. Carp H, Janoff A. 1978. Possible mechanisms of emphysema in smokers. In vitro suppression of serum elastase-inhibitory capacity by fresh cigarette smoke and its prevention by antioxidants. Am Rev Respir Dis 118: 617-621.
6. Carpi D, Korkalainen M, Airoldi L, Fanelli R, Hakansson H, Muhonen V, Tuukkanen J, Viluksela M, Pastorelli R. 2009. Dioxin-sensitive proteins in differentiating osteoblasts: Effects on bone formation in vitro. Toxicol Sci 108: 330-343.
7. Cesar-Neto JB, Duarte PM, Sallum EA, Barbieri D, Moreno H, Jr, Nociti FH, Jr. 2003. A comparative study on the effect of nicotine administration and cigarette smoke inhalation on bone healing around titanium implants. J Periodontol 74: 1454-1459.
8. Chan WK, Yao G, Gu YZ, Bradfield CA. 1999. Cross-talk between the aryl hydrocarbon receptor and hypoxia inducible factor signaling pathways. Demonstration of competition and compensation. J Biol Chem 274: 12115-12123.
9. Chaudhary SB, Liporace FA, Gandhi A, Donley BG, Pinzur MS, Lin SS. 2008. Complications of ankle fracture in patients with diabetes. J Am Acad Orthop Surg 16: 159-170.
10. Clark CA, Schwarz EM, Zhang X, Ziran NM, Drissi H, O'Keefe RJ, Zuscik MJ. 2005. Differential regulation of EP receptor isoforms during chondrogenesis and chondrocyte maturation. Biochem Biophys Res Commun 328: 764-776.
11. Dimmen S, Nordsletten L, Madsen JE. 2009. Parecoxib and indomethacin delay early fracture healing: A study in rats. Clin Orthop Relat Res 467: 1992-1999.
12. Einhorn TA. 1998. The cell and molecular biology of fracture healing. Clin Orthop 355: S7-S21.
13. El-Zawawy HB, Gill CS, Wright RW, Sandell LJ. 2006. Smoking delays chondrogenesis in a mouse model of closed tibial fracture healing. J Orthop Res 24: 2150-2158.
14. Finch GL, Lundgren DL, Barr EB, Chen BT, Griffith WC, Hobbs CH, Hoover MD, Nikula KJ, Mauderly JL. 1998. Chronic cigarette smoke exposure increases the pulmonary retention and radiation dose of 239Pu inhaled as 239PuO2 by F344 rats. Health Phys 75: 597-609.
15. Fitzgerald DJ, Robinson NI, Pester BA. 2004. Application of benzo(α)pyrene and coal tar tumor dose-response data to a modified benchmark dose method of guideline development. Environ Health Perspect 112: 1341-1346.
16. Gaston MS, Simpson AH. 2007. Inhibition of fracture healing. J Bone Joint Surg Br 89: 1553-1560.
17. Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT, Einhorn TA. 2003. Fracture healing as a post-natal developmental process: Molecular, spatial, and temporal aspects of its regulation. J Cell Biochem 88: 873-884.
18. Goldring MB, Tsuchimochi K, Ijiri K. 2006. The control of chondrogenesis. J Cell Biochem 97: 33-44.
19. Hermsen SA, Larsson S, Arima A, Muneoka A, Ihara T, Sumida H, Fukusato T, Kubota S, Yasuda M, Lind PM. 2008. In utero and lactational exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) affects bone tissue in rhesus monkeys. Toxicology 253: 147-152.
20. IARC. 2010. Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monogr Eval Carcinog Risks Hum 92: 1-853.
21. Kasai A, Hiramatsu N, Hayakawa K, Yao J, Maeda S, Kitamura M. 2006. High levels of dioxin-like potential in cigarette smoke evidenced by in vitro and in vivo biosensing. Cancer Res 66: 7143-7150.
22. Khan S, Liu S, Stoner M, Safe S. 2007. Cobaltous chloride and hypoxia inhibit aryl hydrocarbon receptor-mediated responses in breast cancer cells. Toxicol Appl Pharmacol 223: 28-38.
23. Komatsu DE, Hadjiargyrou M. 2004. Activation of the transcription factor HIF-1 and its target genes, VEGF, HO-1, iNOS, during fracture repair. Bone 34: 680-688.
24. Korkalainen M, Kallio E, Olkku A, Nelo K, Ilvesaro J, Tuukkanen J, Mahonen A, Viluksela M. 2009. Dioxins interfere with differentiation of osteoblasts and osteoclasts. Bone 44: 1134-1142.
25. Lafont JE, Talma S, Hopfgarten C, Murphy CL. 2008. Hypoxia promotes the differentiated human articular chondrocyte phenotype through SOX9-dependent and -independent pathways. J Biol Chem 283: 4778-4786.
26. Lahvis GP, Bradfield CA. 1998. AHR null alleles: Distinctive or different? Biochem Pharmacol 56: 781-787.
27. Lind PM, Wejheden C, Lundberg R, Alvarez-Lloret P, Hermsen SA, Rodriguez-Navarro AB, Larsson S, Rannug A. 2009. Short-term exposure to dioxin impairs bone tissue in male rats. Chemosphere 75: 680-684.
28. Lodovici M, Akpan V, Evangelisti C, Dolara P. 2004. Sidestream tobacco smoke as the main predictor of exposure to polycyclic aromatic hydrocarbons. J Appl Toxicol 24: 277-281.
29. Lu YF, Santostefano M, Cunningham BD, Threadgill MD, Safe S. 1995. Identification of 3'-methoxy-4'-nitroflavone as a pure aryl hydrocarbon (Ah) receptor antagonist and evidence for more than one form of the nuclear Ah receptor in MCF-7 human breast cancer cells. Arch Biochem Biophys 316: 470-477.
30. Ma L, Zheng LW, Cheung LK. 2007. Inhibitory effect of nicotine on bone regeneration in mandibular distraction osteogenesis. Front Biosci 12: 3256-3262.
31. McKee MD, DiPasquale DJ, Wild LM, Stephen DJ, Kreder HJ, Schemitsch EH. 2003. The effect of smoking on clinical outcome and complication rates following Ilizarov reconstruction. J Orthop Trauma 17: 663-667.
32. Naik AA, Xie C, Zuscik MJ, Kingsley P, Schwarz EM, Awad H, Guldberg R, Drissi H, Puzas JE, Boyce B, Zhang X, O'Keefe RJ. 2009. Reduced COX-2 expression in aged mice is associated with impaired fracture healing 18. J Bone Miner Res 24: 251-264.
33. Naruse M, Otsuka E, Ishihara Y, Miyagawa-Tomita S, Hagiwara H. 2004. Inhibition of osteoclast formation by 3-methylcholanthrene, a ligand for arylhydrocarbon receptor: Suppression of osteoclast differentiation factor in osteogenic cells. Biochem Pharmacol 67: 119-127.
34. Nishimura N, Nishimura H, Ito T, Miyata C, Izumi K, Fujimaki H, Matsumura F. 2009. 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 236: 301-309.
35. Porter SE, Hanley EN, Jr. 2001. The musculoskeletal effects of smoking. J Am Acad Orthop Surg 9: 9-17.
36. Provot S, Zinyk D, Gunes Y, Kathri R, Le Q, Kronenberg HM, Johnson RS, Longaker MT, Giaccia AJ, Schipani E. 2007. Hif-1alpha regulates differentiation of limb bud mesenchyme and joint development. J Cell Biol 177: 451-464.
37. Raikin SM, Landsman JC, Alexander VA, Froimson MI, Plaxton NA. 1998. Effect of nicotine on the rate and strength of long bone fracture healing. Clin Orthop 353: 231-237.
38. Rubin H. 2001. Synergistic mechanisms in carcinogenesis by polycyclic aromatic hydrocarbons and by tobacco smoke: A bio-historical perspective with updates. Carcinogenesis 22: 1903-1930.
39. Ryan EP, Holz JD, Mulcahey M, Sheu TJ, Gasiewicz TA, Puzas JE. 2007. Environmental toxicants may modulate osteoblast differentiation by a mechanism involving the aryl hydrocarbon receptor. J Bone Miner Res 22: 1571-1580.
40. Schipani E. 2005. Hypoxia and HIF-1 alpha in chondrogenesis. Semin Cell Dev Biol 16: 539-546.
41. Schmitz MA, Finnegan M, Natarajan R, Champine J. 1999. Effect of smoking on tibial shaft fracture healing. Clin Orthop 365: 184-200.
42. Shimba S, Wada T, Tezuka M. 2001. Arylhydrocarbon receptor (AhR) is involved in negative regulation of adipose differentiation in 3T3-L1cells: AhR inhibits adipose differentiation independently of dioxin. J Cell Sci 114: 2809-2817.
43. Shimba S, Hayashi M, Ohno T, Tezuka M. 2003. Transcriptional regulation of the AhR gene during adipose differentiation. Biol Pharm Bull 26: 1266-1271.
44. Silcox DH, III, Daftari T, Boden SD, Schimandle JH, Hutton WC, Whitesides TE, Jr. 1995. The effect of nicotine on spinal fusion. Spine 20: 1549-1553.
45. Skott M, Andreassen TT, Ulrich-Vinther M, Chen X, Keyler DE, LeSage MG, Pentel PR, Bechtold JE, Soballe K. 2006. Tobacco extract but not nicotine impairs the mechanical strength of fracture healing in rats. J Orthop Res 24: 1472-1479.
46. Thatcher TH, McHugh NA, Egan RW, Chapman RW, Hey JA, Turner CK, Redonnet MR, Seweryniak KE, Sime PJ, Phipps RP. 2005. Role of CXCR2 in cigarette smoke-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol 289: L322-L328.
47. Uei H, Matsuzaki H, Oda H, Nakajima S, Tokuhashi Y, Esumi M. 2006. Gene expression changes in an early stage of intervertebral disc degeneration induced by passive cigarette smoking. Spine 31: 510-514.
48. Ueng SW, Lee MY, Li AF, Lin SS, Tai CL, Shih CH. 1997. Effect of intermittent cigarette smoke inhalation on tibial lengthening: Experimental study on rabbits. J Trauma 42: 231-238.
49. Voronov I, Heersche JN, Casper RF, Tenenbaum HC, Manolson MF. 2005. Inhibition of osteoclast differentiation by polycyclic aryl hydrocarbons is dependent on cell density and RANKL concentration. Biochem Pharmacol 70: 300-307.
50. Walisser JA, Glover E, Pande K, Liss AL, Bradfield CA. 2005. Aryl hydrocarbon receptor-dependent liver development and hepatotoxicity are mediated by different cell types. Proc Natl Acad Sci USA 102: 17858-17863.
51. Wang Y, Wan C, Deng L, Liu X, Cao X, Gilbert SR, Bouxsein ML, Faugere MC, Guldberg RE, Gerstenfeld LC, Haase VH, Johnson RS, Schipani E, Clemens TL. 2007. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 117: 1616-1626.
52. Wu Q, Kim KO, Sampson ER, Chen D, Awad H, O'Brien T, Puzas JE, Drissi H, Schwarz EM, O'Keefe RJ, Zuscik MJ, Rosier RN. 2008. Induction of an osteoarthritis-like phenotype and degradation of phosphorylated Smad3 by Smurf2 in transgenic mice. Arthritis Rheum 58: 3132-3144.
53. Zakany R, Szijgyarto Z, Matta C, Juhasz T, Csortos C, Szucs K, Czifra G, Biro T, Modis L, Gergely P. 2005. Hydrogen peroxide inhibits formation of cartilage in chicken micromass cultures and decreases the activity of calcineurin: Implication of ERK1/2 and Sox9 pathways. Exp Cell Res 305: 190-199.
54. Zhang X, Ziran N, Goater JJ, Schwarz EM, Puzas JE, Rosier RN, Zuscik M, Drissi H, O'Keefe RJ. 2004. Primary murine limb bud mesenchymal cells in long-term culture complete chondrocyte differentiation: TGF-beta delays hypertrophy and PGE2 inhibits terminal differentiation. Bone 34: 809-817.