Transgenic mice with a constitutively active aryl hydrocarbon receptor display a gender-specific bone phenotype

Toxicological Sciences

Volumn 114, Issue 1, 2009, Pages 48-58

  Wejheden, Carolina ^a   Brunnberg, Sara ^a   Larsson, Sune ^b   Lind, Pia M ^a,b   Andersson, Göran ^c   Hanberg, Annika ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Ah receptor; Bone; Dioxin; Osteoblast; Osteoclast; Transgenic mouse model

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; AROMATIC HYDROCARBON RECEPTOR; CARBOXY TERMINAL TELOPEPTIDE; CATHEPSIN K; DIOXIN; MESSENGER RNA; PROTEIN TRAP 5B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DENSITY; CELL DIFFERENTIATION; CONTROLLED STUDY; CORTICAL BONE; FEMALE; MALE; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST ACTIVITY; OSTEOLYSIS; PHENOTYPE; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SEX DIFFERENCE; TRABECULAR BONE; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

EID: 77951582963     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp284     Document Type: Article

References (47)

1. Alatalo, S. L., Halleen, J. M., Hentunen, T. A., Monkkonen, J., and Vaananen, H. K. (2000). Rapid screening method for osteoclast differentiation in vitro that measures tartrate-resistant acid phosphatase 5b activity secreted into the culture medium. Clin. Chem. 46, 1751-1754.
2. Alatalo, S. L., Ivaska, K. K., Waguespack, S. G., Econs, M. J., Vaananen, H. K., and Halleen, J. M. (2004). Osteoclast-derived serum tartrate-resistant acid phosphatase 5b in Albers-Schonberg disease (type II autosomal dominant osteopetrosis). Clin. Chem. 50, 883-890.
3. Alatalo, S. L., Peng, Z., Janckila, A. J., Kaija, H., Vihko, P., Vaananen, H. K., and Halleen, J. M. (2003). A novel immunoassay for the determination of tartrate-resistant acid phosphatase 5b from rat serum. J. Bone Miner. Res. 18, 134-139.
4. Alveblom, A. K., Rylander, L., Johnell, O., and Hagmar, L. (2003). Incidence of hospitalized osteoporotic fractures in cohorts with high dietary intake of persistent organochlorine compounds. Int. Arch. Occup. Environ. Health 76, 246-248.
5. Andersson, P., McGuire, J., Rubio, C., Gradin, K., Whitelaw, M. L., Pettersson, S., Hanberg, A., and Poellinger, L. (2002). A constitutively active dioxin/aryl hydrocarbon receptor induces stomach tumors. Proc. Natl. Acad. Sci. U.S.A. 99, 9990-9995.
6. Andersson, P., Ridderstad, A., McGuire, J., Pettersson, S., Poellinger, L., and Hanberg, A. (2003). A constitutively active aryl hydrocarbon receptor causes loss of peritoneal B1 cells. Biochem. Biophys. Res. Commun. 302, 336-341.
7. Bodrug, S. E., Warner, B. J., Bath, M. L., Lindeman, G. J., Harris, A. W., and Adams, J. M. (1994). Cyclin D1 transgene impedes lymphocyte maturation and collaborates in lymphomagenesis with the myc gene. EMBO J. 13, 2124-2130.
8. Boverhof, D. R., Kwekel, J. C., Humes, D. G., Burgoon, L. D., and Zacharewski, T. R. (2006). Dioxin induces an estrogen-like, estrogen receptor-dependent gene expression response in the murine uterus. Mol. Pharmacol. 69, 1599-1606.
9. Brunnberg, S., Andersson, P., Lindstam, M., Paulson, I., Poellinger, L., and Hanberg, A. (2006). The constitutively active Ah receptor (CA-Ahr) mouse as a potential model for dioxin exposure-effects in vital organs. Toxicology 224, 191-201.
10. Carlson, D. B., and Perdew, G. H. (2002). A dynamic role for the Ah receptor in cell signaling? Insights from a diverse group of Ah receptor interacting proteins. J. Biochem. Mol. Toxicol. 16, 317-325.
11. Chu, P., Chao, T. Y., Lin, Y. F., Janckila, A. J., and Yam, L. T. (2003). Correlation between histomorphometric parameters of bone resorption and serum type 5b tartrate-resistant acid phosphatase in uremic patients on maintenance hemodialysis. Am. J. Kidney Dis. 41, 1052-1059.
12. EC-SCF. (2000). Opinion of the Scientific Committee on Food on the risk assessment of dioxins and dioxin-like PCBs in food. SCF/CS/CNTM/DIOXIN/8 final. Adopted on 22 November 2000. European Commission Scientific Committee on Foods, Brussels, Belgium.
13. EC-SCF. (2001). Opinion of the Scientific Committee on Food on the risk assessment of dioxins and dioxin-like PCBs in food. Update based on new scientific information available since the adoption of the SCF opinion of 22nd November 2000. CS/CNTM/DIOXIN/20 final. European Commission Scientific Committee on Foods, Brussels, Belgium.
14. Feng, J. Q., Ward, L. M., Liu, S., Lu, Y., Xie, Y., Yuan, B., Yu, X., Rauch, F., Davis, S. I., Zhang, S., et al. (2006). Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat. Genet. 38, 1310-1315.
15. Gasser, J. A. (2003). Bone measurements by peripheral quantitative computed tomography in rodents. In Methods in Molecular Medicine: Bone Research Protocols (Stuart H. Ralston and M. H. Helfrich, Eds.), Vol. 80, pp. 323-341. Human Press, Totowa, NJ.
16. Gierthy, J. F., Silkworth, J. B., Tassinari, M., Stein, G. S., and Lian, J. B. (1994). 2,3,7,8-Tetrachlorodibenzo-p-dioxin inhibits differentiation of normal diploid rat osteoblasts in vitro. J. Cell. Biochem. 54, 231-238.
17. Gu, Y. Z., Hogenesch, J. B., and Bradfield, C. A. (2000). The PAS superfamily: sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40, 519-561.
18. Guo, L., Zhao, Y. Y., Zhao, Y. Y., Sun, Z. J., Liu, H., and Zhang, S. L. (2007). Toxic effects of TCDD on osteogenesis through altering IGFBP-6 gene expression in osteoblasts. Biol. Pharm. Bull. 30, 2018-2026.
19. Hermsen, S. A., Larsson, S., Arima, A., Muneoka, A., Ihara, T., Sumida, H., Fukusato, T., Kubota, S., Yasuda, M., and Lind, P. M. (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. Hollberg, K., Hultenby, K., Hayman, A., Cox, T., and Andersson, G. (2002). Osteoclasts from mice deficient in tartrate-resistant acid phosphatase have altered ruffled borders and disturbed intracellular vesicular transport. Exp. Cell Res. 279, 227-238.
21. Ilvesaro, J., Pohjanvirta, R., Tuomisto, J., Viluksela, M., and Tuukkanen, J. (2005). Bone resorption by aryl hydrocarbon receptor-expressing osteoclasts is not disturbed by TCDD in short-term cultures. Life Sci. 77, 1351-1366.
22. Jämsa, T., Viluksela, M., Tuomisto, J. T., Tuomisto, J., and Tuukkanen, J. (2001). Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on bone in two rat strains with different aryl hydrocarbon receptor structures. J. Bone Miner. Res. 16, 1812-1820.
23. Korkalainen, M., Kallio, E., Olkku, A., Nelo, K., Ilvesaro, J., Tuukkanen, J., Mahonen, A., and Viluksela, M. (2009). Dioxins interfere with differentiation of osteoblasts and osteoclasts. Bone 44, 1134-1142.
24. Lees, R. L., and Heersche, J. N. (1999). Macrophage colony stimulating factor increases bone resorption in dispersed osteoclast cultures by increasing osteoclast size. J. Bone Miner. Res. 14, 937-945.
25. Lees, R. L., Sabharwal, V. K., and Heersche, J. N. (2001). Resorptive state and cell size influence intracellular pH regulation in rabbit osteoclasts cultured on collagen-hydroxyapatite films. Bone 28, 187-194.
26. Lind, P. M., Eriksen, E. F., Sahlin, L., Edlund, M., and Orberg, J. (1999). Effects of the antiestrogenic environmental pollutant 3,3′,4,4′, 5-pentachlorobiphenyl (PCB #126) in rat bone and uterus: diverging effects in ovariectomized and intact animals. Toxicol. Appl. Pharmacol. 154, 236-244.
27. Lind, P. M., Larsson, S., Oxlund, H., Hakansson, H., Nyberg, K., Eklund, T., and Orberg, J. (2000). Change of bone tissue composition and impaired bone strength in rats exposed to 3,3′,4,4′,5-pentachlorobiphenyl (PCB126). Toxicology 150, 41-51.
28. Lind, P. M., Wejheden, C., Lundberg, R., Alvarez-Lloret, P., Hermsen, S. A., Rodriguez-Navarro, A. B., Larsson, S., and Rannug, A. (2009). Short-term exposure to dioxin impairs bone tissue in male rats. Chemosphere 75, 680-684.
29. Ling, Y., Rios, H. F., Myers, E. R., Lu, Y., Feng, J. Q., and Boskey, A. L. (2005). DMP1 depletion decreases bone mineralization in vivo: an FTIR imaging analysis. J. Bone Miner. Res. 20, 2169-2177.
30. McGuire, J., Okamoto, K., Whitelaw, M. L., Tanaka, H., and Poellinger, L. (2001). Definition of a dioxin receptor mutant that is a constitutive activator of transcription: delineation of overlapping repression and ligand binding functions within the PAS domain. J. Biol. Chem. 276, 41841-41849.
31. Miettinen, H. M., Pulkkinen, P., Jamsa, T., Koistinen, J., Simanainen, U., Tuomisto, J., Tuukkanen, J., and Viluksela, M. (2005). Effects of in utero and lactational TCDD exposure on bone development in differentially sensitive rat lines. Toxicol. Sci. 85, 1003-1012.
32. Naruse, M., Ishihara, Y., Miyagawa-Tomita, S., Koyama, A., and Hagiwara, H. (2002). 3-Methylcholanthrene, which binds to the arylhydrocarbon receptor, inhibits proliferation and differentiation of osteoblasts in vitro and ossification in vivo. Endocrinology 143, 3575-3581.
33. Naruse, M., Otsuka, E., Naruse, M., Ishihara, Y., Miyagawa-Tomita, S., and 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.,and 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. Partridge, N. C., Fiacco, G. J., Walling, H. W., Barmina, O. Y., Jeffrey, J. J., and Ruh, M. F. (2000). Effects of dioxin and estrogen on collagenase-3 in UMR 106-01 osteosarcoma cells. Arch. Biochem. Biophys. 382, 182-188.
36. Piper, K., Boyde, A., and Jones, S. J. (1992). The relationship between the number of nuclei of an osteoclast and its resorptive capability in vitro. Anat. Embryol. 186, 291-299.
37. Rissanen, J. P., Suominen, M. I., Peng, Z., and Halleen, J. M. (2008). Secreted tartrate-resistant acid phosphatase 5b is a marker of osteoclast number in human osteoclast cultures and the rat ovariectomy model. Calcif. Tissue Int. 82, 108-115.
38. Ryan, E. P., Holz, J. D., Mulcahey, M., Sheu, T. J., Gasiewicz, T. A., and Puzas, J. E. (2007). Environmental toxicants may modulate osteoblast differentiation by a mechanism involving the aryl hydrocarbon receptor. J. Bone Miner. Res. 22, 1571-1580.
39. Safe, S., Wang, F., Porter, W., Duan, R., and McDougal, A. (1998). Ah receptor agonists as endocrine disruptors: antiestrogenic activity and mechanisms. Toxicol. Lett. 102-103, 343-347.
40. Singh, S. U., Casper, R. F., Fritz, P. C., Sukhu, B., Ganss, B., Girard, B., Jr., Savouret, J. F., and Tenenbaum, H. C. (2000). Inhibition of dioxin effects on bone formation in vitro by a newly described aryl hydrocarbon receptor antagonist, resveratrol. J. Endocrinol. 167, 183-195.
41. Voronov, I., Heersche, J. N., Casper, R. F., Tenenbaum, H. C., and Manolson, M. F. (2005). Inhibition of osteoclast differentiation by polycyclic aryl hydrocarbons is dependent on cell density and RANKL concentration. Biochem. Pharmacol. 70, 300-307.
42. Voronov, I., Li, K., Tenenbaum, H. C., and Manolson, M. F. (2008). Benzo[a]pyrene inhibits osteoclastogenesis by affecting RANKL-induced activation of NF-kappaB. Biochem. Pharmacol. 75, 2034-2044.
43. Wallin, E., Rylander, L., and Hagmar, L. (2004). Exposure to persistent organochlorine compounds through fish consumption and the incidence of osteoporotic fractures. Scand. J. Work Environ. Health 30, 30-35.
44. Wejheden, C., Brunnberg, S., Hanberg, A., and Lind, P. M. (2006). Osteopontin: a rapid and sensitive response to dioxin exposure in the osteoblastic cell line UMR-106. Biochem. Biophys. Res. Commun. 341, 116-120.
45. WHO-ECEH/IPCS. (2000). Consultation on assessment of the health risk of dioxins; re-evaluation of the tolerable daily intake (TDI): executive summary. Food Addit. Contam. 17, 223-240.
46. Yamaza, T., Goto, T., Kamiya, T., Kobayashi, Y., Sakai, H., and Tanaka, T. (1998). Study of immunoelectron microscopic localization of cathepsin K in osteoclasts and other bone cells in the mouse femur. Bone 23, 499-509.
47. Zenger, S., Hollberg, K., Ljusberg, J., Norgard, M., Ek-Rylander, B., Kiviranta, R., and Andersson, G. (2007). Proteolytic processing and polarized secretion of tartrate-resistant acid phosphatase is altered in a subpopulation of metaphyseal osteoclasts in cathepsin K-deficient mice. Bone 41, 820-832.