Why toxic equivalency factors are not suitable for perfluoroalkyl chemicals

Chemical Research in Toxicology

Volumn 24, Issue 10, 2011, Pages 1601-1609

  Peters, Jeffrey M ^a   Gonzalez, Frank J ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2U GLOBULIN; AROMATIC HYDROCARBON RECEPTOR; DECANOIC ACID DERIVATIVE; ESTROGEN RECEPTOR ALPHA; HEXANOIC ACID; NONANOIC ACID; OCTANOIC ACID DERIVATIVE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; POLYCHLORINATED BIPHENYL; POLYCHLORINATED DIBENZODIOXIN; POLYCHLORINATED DIBENZOFURAN; SERPACWA; SULFONIC ACID DERIVATIVE;

DATA BASE; ENZYME ACTIVITY; HEPATOMEGALY; HUMAN; NONHUMAN; PARAMETERS OF MEASUREMENT AND ANALYSIS; REVIEW; SPECIES; TOXIC EQUIVALENCY FACTOR;

ANIMALS; DRUG INTERACTIONS; ENVIRONMENTAL POLLUTANTS; ESTROGEN RECEPTOR ALPHA; HUMANS; HYDROCARBONS, FLUORINATED; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID; RISK ASSESSMENT; SPECIES SPECIFICITY; SURFACE-ACTIVE AGENTS;

ANIMALIA;

EID: 80054722447     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx200316x     Document Type: Review

References (68)

1. Prevedouros, K., Cousins, I. T., Buck, R. C., and Korzeniowski, S. H. (2006) Sources, fate and transport of perfluorocarboxylates Environ. Sci. Technol. 40, 32-44 (Pubitemid 43069883)
2. D'Eon, J. C. and Mabury, S. A. (2011) Is indirect exposure a significant contributor to the burden of perfluorinated acids observed in humans? Environ. Sci. Technol. 10.1021/es200171y
3. Kato, K., Wong, L. Y., Jia, L. T., Kuklenyik, Z., and Calafat, A. M. (2011) Trends in exposure to polyfluoroalkyl chemicals in the U.S. population: 1999-2008 Environ. Sci. Technol. 10.1021/es1043613
4. Lau, C., Anitole, K., Hodes, C., Lai, D., Pfahles-Hutchens, A., and Seed, J. (2007) Perfluoroalkyl acids: a review of monitoring and toxicological findings Toxicol. Sci. 99, 366-394 (Pubitemid 351753056)
5. Kudo, N. and Kawashima, Y. (2003) Toxicity and toxicokinetics of perfluorooctanoic acid in humans and animals J. Toxicol. Sci. 28, 49-57 (Pubitemid 36764755)
6. Lau, C., Butenhoff, J. L., and Rogers, J. M. (2004) The developmental toxicity of perfluoroalkyl acids and their derivatives Toxicol. Appl. Pharmacol. 198, 231-241 (Pubitemid 38952836)
7. Meek, M. E., Bucher, J. R., Cohen, S. M., Dellarco, V., Hill, R. N., Lehman-McKeeman, L. D., Longfellow, D. G., Pastoor, T., Seed, J., and Patton, D. E. (2003) A framework for human relevance analysis of information on carcinogenic modes of action Crit. Rev. Toxicol. 33, 591-653 (Pubitemid 38040084)
8. Fernandez-Salguero, P. M., Hilbert, D. M., Rudikoff, S., Ward, J. M., and Gonzalez, F. J. (1996) Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity Toxicol. Appl. Pharmacol. 140, 173-179 (Pubitemid 26329475)
9. Peters, J. M., Narotsky, M. G., Elizondo, G., Fernandez-Salguero, P. M., Gonzalez, F. J., and Abbott, B. D. (1999) Amelioration of TCDD-induced teratogenesis in aryl hydrocarbon receptor (AhR)-null mice Toxicol. Sci. 47, 86-92 (Pubitemid 29214235)
10. Wei, P., Zhang, J., Egan-Hafley, M., Liang, S., and Moore, D. D. (2000) The nuclear receptor CAR mediates specific xenobiotic induction of drug metabolism Nature 407, 920-923
11. Hays, T., Rusyn, I., Burns, A. M., Kennett, M. J., Ward, J. M., Gonzalez, F. J., and Peters, J. M. (2005) Role of peroxisome proliferator-activated receptor-α (PPARα) in bezafibrate-induced hepatocarcinogenesis and cholestasis Carcinogenesis 26, 219-227 (Pubitemid 40207717)
12. Peters, J. M., Cattley, R. C., and Gonzalez, F. J. (1997) Role of PPAR α in the mechanism of action of the nongenotoxic carcinogen and peroxisome proliferator Wy-14,643 Carcinogenesis 18, 2029-2033 (Pubitemid 28134725)
13. Van den Berg, M., Birnbaum, L., Bosveld, A. T., Brunstrom, B., Cook, P., Feeley, M., Giesy, J. P., Hanberg, A., Hasegawa, R., Kennedy, S. W., Kubiak, T., Larsen, J. C., van Leeuwen, F. X., Liem, A. K., Nolt, C., Peterson, R. E., Poellinger, L., Safe, S., Schrenk, D., Tillitt, D., Tysklind, M., Younes, M., Waern, F., and Zacharewski, T. (1998) Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife Environ. Health Perspect. 106, 775-792 (Pubitemid 29073822)
14. Van den Berg, M., Birnbaum, L. S., Denison, M., De Vito, M., Farland, W., Feeley, M., Fiedler, H., Hakansson, H., Hanberg, A., Haws, L., Rose, M., Safe, S., Schrenk, D., Tohyama, C., Tritscher, A., Tuomisto, J., Tysklind, M., Walker, N., and Peterson, R. E. (2006) The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds Toxicol. Sci. 93, 223-241 (Pubitemid 44400442)
15. Gonzalez, F. J. and Fernandez-Salguero, P. (1998) The aryl hydrocarbon receptor: studies using the AHR-null mice Drug Metab. Dispos. 26, 1194-1198
16. Beischlag, T. V., Luis Morales, J., Hollingshead, B. D., and Perdew, G. H. (2008) The aryl hydrocarbon receptor complex and the control of gene expression Crit. Rev. Eukaryotic Gene Expression 18, 207-250 (Pubitemid 351620286)
17. Bradshaw, T. D. and Bell, D. R. (2009) Relevance of the aryl hydrocarbon receptor (AhR) for clinical toxicology Clin. Toxicol. 47, 632-642
18. Neumann, H. G. (1996) Toxic equivalence factors, problems and limitations Food Chem. Toxicol. 34, 1045-1051
19. Safe, S. (1997) Limitations of the toxic equivalency factor approach for risk assessment of TCDD and related compounds Teratog. Carcinog. Mutagen. 17, 285-304 (Pubitemid 28080831)
20. Scialli, A. R., Iannucci, A., and Turim, J. (2007) Combining perfluoroalkane acid exposure levels for risk assessment Regul. Toxicol. Pharmacol. 49, 195-202 (Pubitemid 350087398)
21. Elcombe, C. R., Elcombe, B. M., Foster, J. R., Farrar, D. G., Jung, R., Chang, S. C., Kennedy, G. L., and Butenhoff, J. L. (2010) Hepatocellular hypertrophy and cell proliferation in Sprague-Dawley rats following dietary exposure to ammonium perfluorooctanoate occurs through increased activation of the xenosensor nuclear receptors PPARα and CAR/PXR Arch. Toxicol. 84, 787-798
22. Foreman, J. E., Chang, S. C., Ehresman, D. J., Butenhoff, J. L., Anderson, C. R., Palkar, P. S., Kang, B. H., Gonzalez, F. J., and Peters, J. M. (2009) Differential hepatic effects of perfluorobutyrate mediated by mouse and human PPAR-α Toxicol. Sci. 110, 204-211
23. Kennedy, G. L., Jr., Butenhoff, J. L., Olsen, G. W., O'Connor, J. C., Seacat, A. M., Perkins, R. G., Biegel, L. B., Murphy, S. R., and Farrar, D. G. (2004) The toxicology of perfluorooctanoate Crit. Rev. Toxicol. 34, 351-384 (Pubitemid 38888064)
24. Maloney, E. K. and Waxman, D. J. (1999) trans-Activation of PPARα and PPARγ by structurally diverse environmental chemicals Toxicol. Appl. Pharmacol. 161, 209-218
25. Cheng, X. and Klaassen, C. D. (2008) Perfluorocarboxylic acids induce cytochrome P450 enzymes in mouse liver through activation of PPAR-α and CAR transcription factors Toxicol. Sci. 106, 29-36
26. Rosen, M. B., Abbott, B. D., Wolf, D. C., Corton, J. C., Wood, C. R., Schmid, J. E., Das, K. P., Zehr, R. D., Blair, E. T., and Lau, C. (2008) Gene profiling in the livers of wild-type and PPARα-null mice exposed to perfluorooctanoic acid Toxicol. Pathol. 36, 592-607
27. Rosen, M. B., Lee, J. S., Ren, H., Vallanat, B., Liu, J., Waalkes, M. P., Abbott, B. D., Lau, C., and Corton, J. C. (2008) Toxicogenomic dissection of the perfluorooctanoic acid transcript profile in mouse liver: evidence for the involvement of nuclear receptors PPARα and CAR Toxicol. Sci. 103, 46-56 (Pubitemid 351524476)
28. Takacs, M. L. and Abbott, B. D. (2007) Activation of mouse and human peroxisome proliferator-activated receptors (α, β/δ, γ) by perfluorooctanoic acid and perfluorooctane sulfonate Toxicol. Sci. 95, 108-117 (Pubitemid 44942782)
29. Vanden Heuvel, J. P., Thompson, J. T., Frame, S. R., and Gillies, P. J. (2006) Differential activation of nuclear receptors by perfluorinated fatty acid analogs and natural fatty acids: a comparison of human, mouse, and rat peroxisome proliferator-activated receptor-α, -β, and -γ, liver X receptor-β, and retinoid X receptor-α Toxicol. Sci. 92, 476-489 (Pubitemid 44018964)
30. Wolf, C. J., Takacs, M. L., Schmid, J. E., Lau, C., and Abbott, B. D. (2008) Activation of mouse and human peroxisome proliferator-activated receptor α by perfluoroalkyl acids of different functional groups and chain lengths Toxicol. Sci. 106, 162-171
31. Nakamura, T., Ito, Y., Yanagiba, Y., Ramdhan, D. H., Kono, Y., Naito, H., Hayashi, Y., Li, Y., Aoyama, T., Gonzalez, F. J., and Nakajima, T. (2009) Microgram-order ammonium perfluorooctanoate may activate mouse peroxisome proliferator-activated receptor α, but not human PPARα Toxicology 265, 27-33
32. Nakagawa, T., Ramdhan, D. H., Tanaka, N., Naito, H., Tamada, H., Ito, Y., Li, Y., Hayashi, Y., Yamagishi, N., Yanagiba, Y., Aoyama, T., Gonzalez, F. J., and Nakajima, T. (2011) Modulation of ammonium perfluorooctanoate-induced hepatic damage by genetically different PPARα in mice Arch. Toxicol. 10.1007/s00204-011-0704-3
33. Wolf, D. C., Moore, T., Abbott, B. D., Rosen, M. B., Das, K. P., Zehr, R. D., Lindstrom, A. B., Strynar, M. J., and Lau, C. (2008) Comparative hepatic effects of perfluorooctanoic acid and WY 14,643 in PPARα knockout and wild-type mice Toxicol. Pathol. 36, 632-639
34. Qazi, M. R., Xia, Z., Bogdanska, J., Chang, S. C., Ehresman, D. J., Butenhoff, J. L., Nelson, B. D., DePierre, J. W., and Abedi-Valugerdi, M. (2009) The atrophy and changes in the cellular compositions of the thymus and spleen observed in mice subjected to short-term exposure to perfluorooctanesulfonate are high-dose phenomena mediated in part by peroxisome proliferator-activated receptor-α (PPARα) Toxicology 260, 68-76
35. Peraza, M. A., Burdick, A. D., Marin, H. E., Gonzalez, F. J., and Peters, J. M. (2006) The toxicology of ligands for peroxisome proliferator-activated receptors (PPAR) Toxicol. Sci. 90, 269-295
36. Peters, J. M., Cheung, C., and Gonzalez, F. J. (2005) Peroxisome proliferator-activated receptor-α and liver cancer: where do we stand? J. Mol. Med. 83, 774-785 (Pubitemid 41407861)
37. Xu, H. E., Lambert, M. H., Montana, V. G., Parks, D. J., Blanchard, S. G., Brown, P. J., Sternbach, D. D., Lehmann, J. M., Wisely, G. B., Willson, T. M., Kliewer, S. A., and Milburn, M. V. (1999) Molecular recognition of fatty acids by peroxisome proliferator-activated receptors Mol. Cell 3, 397-403 (Pubitemid 29290680)
38. Xu, H. E., Lambert, M. H., Montana, V. G., Plunket, K. D., Moore, L. B., Collins, J. L., Oplinger, J. A., Kliewer, S. A., Gampe, R. T., Jr., McKee, D. D., Moore, J. T., and Willson, T. M. (2001) Structural determinants of ligand binding selectivity between the peroxisome proliferator-activated receptors Proc. Natl. Acad. Sci. U.S.A. 98, 13919-13924 (Pubitemid 33115999)
39. Abbott, B. D., Wolf, C. J., Schmid, J. E., Das, K. P., Zehr, R. D., Helfant, L., Nakayama, S., Lindstrom, A. B., Strynar, M. J., and Lau, C. (2007) Perfluorooctanoic acid induced developmental toxicity in the mouse is dependent on expression of peroxisome proliferator activated receptor-α Toxicol. Sci. 98, 571-581 (Pubitemid 47244825)
40. Wolf, C. J., Zehr, R. D., Schmid, J. E., Lau, C., and Abbott, B. D. (2010) Developmental effects of perfluorononanoic acid in the mouse are dependent on peroxisome proliferator-activated receptor-α. PPAR Res. 10.1155/2010/28296.
41. Abbott, B. D., Wolf, C. J., Das, K. P., Zehr, R. D., Schmid, J. E., Lindstrom, A. B., Strynar, M. J., and Lau, C. (2009) Developmental toxicity of perfluorooctane sulfonate (PFOS) is not dependent on expression of peroxisome proliferator activated receptor-α (PPARα) in the mouse Reprod. Toxicol. 27, 258-265
42. Zhao, Y., Tan, Y. S., Haslam, S. Z., and Yang, C. (2010) Perfluorooctanoic acid effects on steroid hormone and growth factor levels mediate stimulation of peripubertal mammary gland development in C57BL/6 mice Toxicol. Sci. 115, 214-224
43. Benninghoff, A. D., Bisson, W. H., Koch, D. C., Ehresman, D. J., Kolluri, S. K., and Williams, D. E. (2011) Estrogen-like activity of perfluoroalkyl acids in vivo and interaction with human and rainbow trout estrogen receptors in vitro Toxicol. Sci. 120, 42-58
44. Ishibashi, H., Ishida, H., Matsuoka, M., Tominaga, N., and Arizono, K. (2007) Estrogenic effects of fluorotelomer alcohols for human estrogen receptor isoforms α and β in vitro Biol. Pharm. Bull. 30, 1358-1359 (Pubitemid 47037665)
45. Klaunig, J. E., Babich, M. A., Baetcke, K. P., Cook, J. C., Corton, J. C., David, R. M., DeLuca, J. G., Lai, D. Y., McKee, R. H., Peters, J. M., Roberts, R. A., and Fenner-Crisp, P. A. (2003) PPARα agonist-induced rodent tumors: modes of action and human relevance Crit. Rev. Toxicol. 33, 655-780 (Pubitemid 38037444)
46. Bjork, J. A. and Wallace, K. B. (2009) Structure-activity relationships and human relevance for perfluoroalkyl acid-induced transcriptional activation of peroxisome proliferation in liver cell cultures Toxicol. Sci. 111, 89-99
47. Cheung, C., Akiyama, T. E., Ward, J. M., Nicol, C. J., Feigenbaum, L., Vinson, C., and Gonzalez, F. J. (2004) Diminished hepatocellular proliferation in mice humanized for the nuclear receptor peroxisome proliferator-activated receptor-α Cancer Res. 64, 3849-3854 (Pubitemid 38697295)
48. Morimura, K., Cheung, C., Ward, J. M., Reddy, J. K., and Gonzalez, F. J. (2006) Differential susceptibility of mice humanized for peroxisome proliferator-activated receptor α to Wy-14,643-induced liver tumorigenesis Carcinogenesis 27, 1074-1080
49. Biegel, L. B., Hurtt, M. E., Frame, S. R., O'Connor, J. C., and Cook, J. C. (2001) Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male CD rats Toxicol. Sci. 60, 44-55 (Pubitemid 32229826)
50. Butenhoff, J. L., Chang, S.-C., Olsen, G. W., and Thomford, P. J. (2011) Chronic dietary toxicity and carcinogenicity study with potassium perfluorooctanesulfonate in Crl:CD (SD) IGS BR rats, unpublished work.
51. Kraugerud, M., Zimmer, K. E., Ropstad, E., and Verhaegen, S. (2011) Perfluorinated compounds differentially affect steroidogenesis and viability in the human adrenocortical carcinoma (H295R) in vitro cell assay Toxicol. Lett. 205, 62-68
52. Yang, C., Tan, Y. S., Harkema, J. R., and Haslam, S. Z. (2009) Differential effects of peripubertal exposure to perfluorooctanoic acid on mammary gland development in C57Bl/6 and Balb/c mouse strains Reprod Toxicol 27, 299-306
53. Chang, S. C., Das, K., Ehresman, D. J., Ellefson, M. E., Gorman, G. S., Hart, J. A., Noker, P. E., Tan, Y. M., Lieder, P. H., Lau, C., Olsen, G. W., and Butenhoff, J. L. (2008) Comparative pharmacokinetics of perfluorobutyrate in rats, mice, monkeys, and humans and relevance to human exposure via drinking water Toxicol. Sci. 104, 40-53 (Pubitemid 351859027)
54. Chang, S. C., Thibodeaux, J. R., Eastvold, M. L., Ehresman, D. J., Bjork, J. A., Froehlich, J. W., Lau, C., Singh, R. J., Wallace, K. B., and Butenhoff, J. L. (2008) Thyroid hormone status and pituitary function in adult rats given oral doses of perfluorooctanesulfonate (PFOS) Toxicology 243, 330-339 (Pubitemid 50008113)
55. Harada, K., Inoue, K., Morikawa, A., Yoshinaga, T., Saito, N., and Koizumi, A. (2005) Renal clearance of perfluorooctane sulfonate and perfluorooctanoate in humans and their species-specific excretion Environ. Res. 99, 253-261
56. Hundley, S. G., Sarrif, A. M., and Kennedy, G. L. (2006) Absorption, distribution, and excretion of ammonium perfluorooctanoate (APFO) after oral administration to various species Drug Chem. Toxicol. 29, 137-145
57. Olsen, G. W., Burris, J. M., Ehresman, D. J., Froehlich, J. W., Seacat, A. M., Butenhoff, J. L., and Zobel, L. R. (2007) Half-life of serum elimination of perfluorooctanesulfonate,perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers Environ. Health Perspect. 115, 1298-1305 (Pubitemid 47471253)
58. Moreau, A., Vilarem, M. J., Maurel, P., and Pascussi, J. M. (2008) Xenoreceptors CAR and PXR activation and consequences on lipid metabolism, glucose homeostasis, and inflammatory response Mol. Pharmaceutics 5, 35-41 (Pubitemid 351300032)
59. Rosen, M. B., Schmid, J. E., Das, K. P., Wood, C. R., Zehr, R. D., and Lau, C. (2009) Gene expression profiling in the liver and lung of perfluorooctane sulfonate-exposed mouse fetuses: comparison to changes induced by exposure to perfluorooctanoic acid Reprod. Toxicol. 27, 278-288
60. Das, K. P., Grey, B. E., Zehr, R. D., Wood, C. R., Butenhoff, J. L., Chang, S. C., Ehresman, D. J., Tan, Y. M., and Lau, C. (2008) Effects of perfluorobutyrate exposure during pregnancy in the mouse Toxicol. Sci. 105, 173-181
61. Lau, C., Thibodeaux, J. R., Hanson, R. G., Rogers, J. M., Grey, B. E., Stanton, M. E., Butenhoff, J. L., and Stevenson, L. A. (2003) Exposure to perfluorooctane sulfonate during pregnancy in rat and mouse. II: postnatal evaluation Toxicol. Sci. 74, 382-392 (Pubitemid 36958307)
62. Butenhoff, J. L., Bjork, J. A., Chang, S.-C., Ehresman, D. J., Parker, G. A., Das, K., Lau, C., Lieder, P. H., van Otterdijk, F. M., and Wallace, K. B. (2011) Toxicological evaluation of ammonium perfluorobutyrate in rats: twenty-eight-day and ninety-day oral gavage studies. Reprod. Toxicol., submitted for publication.
63. Lieder, P. H., Chang, S. C., York, R. G., and Butenhoff, J. L. (2009) Toxicological evaluation of potassium perfluorobutanesulfonate in a 90-day oral gavage study with Sprague-Dawley rats Toxicology 255, 45-52
64. Chengelis, C. P., Kirkpatrick, J. B., Radovsky, A., and Shinohara, M. (2009) A 90-day repeated dose oral (gavage) toxicity study of perfluorohexanoic acid (PFHxA) in rats (with functional observational battery and motor activity determinations) Reprod Toxicol 27, 342-351
65. Butenhoff, J., Costa, G., Elcombe, C., Farrar, D., Hansen, K., Iwai, H., Jung, R., Kennedy, G., Jr., Lieder, P., Olsen, G., and Thomford, P. (2002) Toxicity of ammonium perfluorooctanoate in male cynomolgus monkeys after oral dosing for 6 months Toxicol. Sci. 69, 244-257
66. Seacat, A. M., Thomford, P. J., Hansen, K. J., Olsen, G. W., Case, M. T., and Butenhoff, J. L. (2002) Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in cynomolgus monkeys Toxicol. Sci. 68, 249-264 (Pubitemid 34785246)
67. White, S. S., Calafat, A. M., Kuklenyik, Z., Villanueva, L., Zehr, R. D., Helfant, L., Strynar, M. J., Lindstrom, A. B., Thibodeaux, J. R., Wood, C., and Fenton, S. E. (2007) Gestational PFOA exposure of mice is associated with altered mammary gland development in dams and female offspring Toxicol. Sci. 96, 133-144 (Pubitemid 46323216)
68. Harkness, J. E. and Wagner, J. E. (1989) The Biology and Medicine of Rabbits and Rodents, 3 rd ed., Lea and Febinger, Philadelphia, PA.