Quantitative characterization of changes in bone geometry, mineral density and biomechanical properties in two rat strains with different Ah-receptor structures after long-term exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin

Toxicology

Volumn 273, Issue 1-3, 2010, Pages 1-11

  Herlin, Maria ^a   Kalantari, Fereshteh ^a   Stern, Natalia ^a   Sand, Salomon ^b   Larsson, Sune ^c   Viluksela, Matti ^d   Tuomisto, Jouni T ^d   Tuomisto, Jouko ^d   Tuukkanen, Juha ^e   Jämsä, Timo ^e,f   Lind, P Monica ^a,g   Håkansson, Helen ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL FOOD ADMINISTRATION   (Sweden)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^e UNIVERSITY OF OULU   (Finland)

^f OULU UNIVERSITY HOSPITAL   (Finland)

^g UPPSALA UNIVERSITY   (Sweden)

Author keywords

2,3,7,8 Tetrachlorodibenzo p dioxin; Benchmark dose modeling; Bone; Bone biomechanics; Peripheral quantitative computed tomography; Toxicology

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE DENSITY; BONE DISEASE; BONE STRUCTURE; COMPUTER ASSISTED TOMOGRAPHY; CONCENTRATION PROCESS; CONTROLLED STUDY; CORTICAL BONE; DIAPHYSIS; FEMALE; GEOMETRY; LONG EVANS RAT; LONG TERM EXPOSURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; RAT; STRAIN DIFFERENCE; TIBIA; TOXICITY TESTING; TRABECULAR BONE; WISTAR RAT; ANIMAL; BONE; BONE REMODELING; DOSE RESPONSE; DRUG EFFECT; FEMUR; HISTOLOGY; METABOLISM; PHYSIOLOGY; POLLUTANT; SPECIES DIFFERENCE; SPINE;

RATTUS;

ANIMALS; BIOMECHANICS; BONE AND BONES; BONE DENSITY; BONE REMODELING; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; FEMALE; FEMUR; RATS; RATS, LONG-EVANS; RATS, WISTAR; RECEPTORS, ARYL HYDROCARBON; SPECIES SPECIFICITY; SPINE; TETRACHLORODIBENZODIOXIN; TIBIA;

EID: 77953255537     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2010.04.006     Document Type: Article

References (48)

1. Abbott B.D., Probst M.R. 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.
2. Alvarez-Lloret P., Lind P.M., Nyberg I., Orberg J., Rodríguez-Navarro A.B. Effects of 3,3',4,4',5-pentachlorobiphenyl (PCB126) on vertebral bone mineralization and on thyroxin and vitamin D levels in Sprague-Dawley rats. Toxicol. Lett. 2009, 187:63-68.
3. Anderson M.J., Keyak J.H., Skinner H.B. Compressive mechanical properties of human cancellous bone after gamma irradiation. J. Bone Joint Surg. Am. 1992, 74:747-752.
4. Andrews J.E. Polychlorinated biphenyl (Aroclor 1254) induced changes in femur morphometry calcium metabolism and nephrotoxicity. Toxicology 1989, 57:83-96.
5. Badraoui R., Bouayed A.N., Sahnoun Z., Fakhfakh Z., Rebai T. Effect of subchronic exposure to tetradifon on bone remodeling and metabolism in female rat. C. R. Biol. 2007, 330:897-904.
6. Beard J., Marshall S., Jong K., Newton R., Triplett-McBride T., Humphries B., Bronks R. 1,1,1-Trichloro-2,2-bis (p-chlorophenyl)-ethane (DDT) and reduced bone mineral density. Arch. Environ. Health 2000, 55:177-180.
7. Cripps D.J., Peters H.A., Gocmen A., Dogramici I. Porphyria turcica due to hexachlorobenzene: a 20 to 30 year follow-up study on 204 patients. Br. J. Dermatol. 1984, 111:413-422.
8. Denison M.S., Scott R.N. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 2003, 43:309-334.
9. EFSA Guidance of the Scientific Committee on a request from EFSA on the use of the benchmark dose approach in risk assessment. EFSA J. 2009, 1150:1-72.
10. Flodström S., Ahlborg U.G. Tumour promoting effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-effects of exposure duration, administration schedule and type of diet. Chemosphere 1989, 19:779-783.
11. Fox G.A., Lundberg R., Wejheden C., Lind L., Larsson S., Orberg J., Lind P.M. Health of herring gulls (Larus argentatus) in relation to breeding location in the early 1990s. III. Effects on the bone tissue. J. Toxicol. Environ. Health 2008, 71:1448-1456.
12. Glynn A.W., Michaëlsson K., Lind P.M., Wolk A., Aune M., Atuma S., Darnerud P.O., Mallmin H. Organochlorines and bone mineral density in Swedish men from the general population. Osteoporos Int. 2000, 11:1036-1042.
13. Gocmen A., Peters H.A., Cripps D.J., Bryan G.T., Morris C.R. Hexachlorobenzene episode in Turkey. Biomed. Environ. Sci. 1989, 2:36-43.
14. Hermsen S.A., Larsson S., Arima A., Muneoka A., Ihara T., Sumida H., Fukusato T., Kubota S., Yasuda M., Lind P.M. In utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) affects bone tissue in rhesus monkeys. Toxicology 2008, 253:147-152.
15. Hodgson S., Thomas L., Fattore E., Lind P.M., Alfven T., Hellström L., Håkansson H., Carubelli G., Fanelli R., Jarup L. Bone mineral density changes in relation to environmental PCB exposure. Environ. Health Perspect. 2008, 116:1162-1166.
16. Ilvesaro J., Pohjanvirta R., Tuomisto J., Viluksela M., Tuukkanen J. Bone resorption by aryl hydrocarbon receptor-expressing osteoclasts is not disturbed by TCDD in short-term cultures. Life Sci. 2005, 77:1351-1366.
17. Jämsä T., Jalovaara P., Peng Z., Väänänen K. Equipment for testing the biomechanical strength of bones. Med. Biol. Eng. Comput. 1996, 34(Suppl. 1, Part 1):347-348.
18. Jämsä T., Viluksela M., Tuomisto J.T., Tuomisto J., Tuukkanen J. 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. 2001, 16:1812-1820.
19. Korkalainen M., Kallio E., Olkku A., Nelo K., Ilvesaro J., Tuukkanen J., Mahonen A., Viluksela M. Dioxins interfere with differentiation of osteoblasts and osteoclasts. Bone 2009, 44:1134-1142.
20. Lepola V.T., Hannuniemi R., Kippo K., Lauren L., Jalovaara P., Väänänen H.K. Long-term effects of clodronate on growing rat bone. Bone 1996, 18:191-196.
21. Lind P.M., Bergman A., Olsson M., Orberg J. Bone mineral density in male Baltic grey seal (Halichoerus grypus). Ambio 2003, 32:385-388. Erratum in: Ambio, 2003, 32, 462.
22. Lind P.M., Eriksen E.F., Sahlin L., Edlund M., Örberg J. 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. 1999, 154:236-244.
23. Lind P.M., Larsson S., Johansson S., Melhus H., Wikström M., Lindhe O., Örberg J. Bone tissue composition, dimensions and strength in female rats given an increased dietary level of vitamin A or exposed to 3,3',4, 4',5-pentachlorobiphenyl (PCB126) alone or in combination with vitamin C. Toxicology 2000, 151:11-23.
24. Lind P.M., Larsson S., Oxlund H., Håkansson H., Nyberg K., Eklund T., Örberg J. Change of bone tissue composition and impaired bone strength in rats exposed to 3,3',4,4',5-pentachlorobiphenyl (PCB126). Toxicology 2000, 150:41-51.
25. Lind P.M., Milnes M.R., Lundberg R., Bermudez D., Örberg J.A., Guillette L.J. Abnormal bone composition in female juvenile American alligators from a pesticide-polluted lake (Lake Apopka, Florida). Environ. Health Perspect. 2004, 112:359-362.
26. Leppänen O.V., Sievänen H., Järvinen T.L. Biomechanical testing in experimental bone interventions-may the power be with you. J. Biomech. 2008, 41:1623-1631.
27. Miettinen H.M., Pulkkinen P., Jämsä T., Koistinen J., Simanainen U., Tuomisto J., Tuukkanen J., Viluksela M. Effects of in utero and lactational TCDD exposure on bone development in differentially sensitive rat lines. Toxicol. Sci. 2005, 85:1003-1012.
28. Miller R.W. Congenital PCB poisoning: a reevaluation. Environ. Health Perspect. 1985, 60:211-214.
29. Naruse M., Ishihara Y., Miyagawa-Tomita S., Koyama A., Hagiwara H. 3-Methylcholanthrene, which binds to the arylhydrocarbon receptor, inhibits proliferation and differentiation of osteoblasts in vitro and ossification in vivo. Endocrinology 2002, 143:3575-3581.
30. Peng Z., Tuukkanen J., Zhang H., Jämsä T., Väänänen H.K. The mechanical strength of bone in different rat models of experimental osteoporosis. Bone 1994, 15:523-532.
31. Pohjanvirta R., Unkila M., Tuomisto J. Comparative acute lethality of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), 1,2,3,7,8-pentachlorodibenzo-p-dioxin and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin in the most TCDD-susceptible and the most TCDD-resistant rat strain. Pharmacol. Toxicol. 1993, 73:52-56.
32. Pohjanvirta R., Wong J.M.Y., Li W., Harper P.A., Tuomisto J., Okey A.B. Point mutation in intron sequence causes altered C-terminal structure in the AH receptor of the most TCDD-resistant rat strain. Mol. Pharmacol. 1998, 54:86-93.
33. Rodriguez-Navarro A.B., Romanek C.S., Alvarez-Lloret P., Gaines K.F. Effect of in ovo exposure to PCBs and Hg on Clapper Rail bone mineral chemistry from a contaminated salt marsh in coastal Georgia. Environ. Sci. Technol. 2006, 40:4936-4942.
34. Ryan E.P., Holz J.D., Mulcahey M., Sheu T.J., Gasiewicz T.A., Puzas J.E. Environmental toxicants may modulate osteoblast differentiation by a mechanism involving the aryl hydrocarbon receptor. J. Bone Miner. Res. 2007, 22:1571-1580.
35. Sand S., Fletcher N., von Rosen D., Kalantari F., Viluksela M., Tuomisto J.T., Tuomisto J., Falk Filipsson A., Håkansson H. Quantitative and statistical analysis of differences in sensitivity between Long-Evans and Han/Wistar rats following long-term exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Regul. Toxicol. Pharmacol. 2010, Epub ahead of print.
36. Sand S., Victorin K., Filipsson A.F. The current state of knowledge on the use of the benchmark dose concept in risk assessment. J. Appl. Toxicol. 2008, 28:405-421.
37. Simanainen U., Tuomisto J.T., Tuomisto J., Viluksela M. Structure-activity relationships and dose responses of polychlorinated dibenzo-p-dioxins for short-term effects in 2,3,7,8-tetrachlorodibenzo-p-dioxin-resistant and -sensitive rat strains. Toxicol. Appl. Pharmacol. 2002, 181:38-47.
38. Singh S.U., Casper R.F., Fritz P.C., Sukhu B., Ganss B., Girard B., Savouret J.F., Tenenbaum H.C. Inhibition of dioxin effects on bone formation in vitro by a newly described aryl hydrocarbon receptor antagonist, resveratrol. J. Endocrinol. 2000, 167:183-195.
39. Sonne C., Dietz R., Born E.W., Riget F.F., Kirkegaard M., Hyldstrup L., Letcher R.J., Muir D.C. Is bone mineral composition disrupted by organochlorines in east Greenland polar bears (Ursus maritimus)?. Environ. Health Perspect. 2004, 112:1711-1716.
40. Tuomisto J.T., Viluksela M., Pohjanvirta R., Tuomisto J. The AH receptor and a novel gene determine acute toxic responses to TCDD: segregation of the resistant alleles to different rat lines. Toxicol. Appl. Pharmacol. 1999, 155:71-81.
41. Unkila M., Pohjanvirta R., MacDonald E., Tuomisto J.T., Tuomisto J. Dose response and time course of alterations in tryptophan metabolism by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the most TCDD-susceptible and the most TCDD-resistant rat strain: relationship with TCDD lethality. Toxicol. Appl. Pharmacol. 1994, 128:280-292.
42. van der Ven L.T., van de Kuil T., Leonards P.E., Slob W., Cantón R.F., Germer S., Visser T.J., Litens S., Håkansson H., Schrenk D., van den Berg M., Piersma A.H., Vos J.G., Opperhuizen A. A 28-day oral dose toxicity study in Wistar rats enhanced to detect endocrine effects of decabromodiphenyl ether (decaBDE). Toxicol. Lett. 2008, 79:6-14.
43. van der Ven L.T., van de Kuil T., Leonards P.E.G., Slob W., Lilienthal H., Litens S., Herlin M., Håkansson H., Cantón R.F., van den Berg M., Visser T.J., van Loveren H., Vos J.G., Piersma A.H. Endocrine effects of hexabromocyclododecane (HBCD) in a one-generation reproduction study in Wistar rats. Toxicol. Lett. 2009, 185:51-62.
44. van der Ven L.T., van de Kuil T., Verhoef A., Leonards P.E., Slob W., Cantón R.F., Germer S., Hamers T., Visser T.J., Litens S., Håkansson H., Fery Y., Schrenk D., van den Berg M., Piersma A.H., Vos J.G. A 28-day oral dose toxicity study enhanced to detect endocrine effects of a purified technical pentabromodiphenyl ether (pentaBDE) mixture in Wistar rats. Toxicology 2008, 245:109-122.
45. van der Ven L.T., Van de Kuil T., Verhoef A., Verwer C.M., Lilienthal H., Leonards P.E., Schauer U.M., Cantón R.F., Litens S., De Jong F.H., Visser T.J., Dekant W., Stern N., Håkansson H., Slob W., Van den Berg M., Vos J.G., Piersma A.H. Endocrine effects of tetrabromobisphenol-A (TBBPA) in Wistar rats as tested in a one-generation reproduction study and a subacute toxicity study. Toxicology 2008, 245:76-89.
46. van der Ven L.T., Verhoef A., van de Kuil T., Slob W., Leonards P.E., Visser T.J., Hamers T., Herlin M., Håkansson H., Olausson H., Piersma A.H., Vos J.G. A 28-day oral dose toxicity study enhanced to detect endocrine effects of hexabromocyclododecane in Wistar rats. Toxicol. Sci. 2006, 94:281-292.
47. Viluksela M., Bager Y., Tuomisto J.T., Scheu G., Unkila M., Pohjanvirta R., Flodstrom S., Kosma V.M., Maki-Paakkanen J., Vartiainen T., Klimm C., Schramm K.W., Warngard L., Tuomisto J. Liver tumor-promoting activity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in TCDD-sensitive and TCDD-resistant rat strains. Cancer Res. 2000, 60:6911-6920.
48. Windahl S.H., Andersson G., Gustafsson J.A. Elucidation of estrogen receptor functions in bone with the use of mouse models. Trends Endocrinol. Metab. 2002, 13:195-200.