Mode of Action analysis of perfluorooctanoic acid (PFOA) tumorigenicity and Human Relevance

Reproductive Toxicology

Volumn 33, Issue 4, 2012, Pages 410-418

  Klaunig, James E ^a   Hocevar, Barbara A ^a   Kamendulis, Lisa M ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Cancer; Leydig cell; Liver; Mode of Action; Pancreas; Perfluorooctanoic acid; PPAR

Indexed keywords

AROMATASE; CHOLECYSTOKININ; CHOLECYSTOKININ RECEPTOR; ESTRADIOL; LUTEINIZING HORMONE; PERFLUOROOCTANOIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TESTOSTERONE; TRANSFORMING GROWTH FACTOR ALPHA;

ACINAR CELL; ARTICLE; BIOACCUMULATION; CANCER GROWTH; CARCINOGENICITY; CELL COMMUNICATION; CELL PROLIFERATION; CYTOTOXICITY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENVIRONMENTAL EXPOSURE; GENOTOXICITY; HUMAN; INFECTION; INFLAMMATION; LEYDIG CELL TUMOR; LIVER CANCER; MITOCHONDRIAL MEMBRANE POTENTIAL; MUTAGENICITY; NONHUMAN; OXIDATIVE STRESS; PANCREAS CANCER; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TESTIS CANCER;

ANIMALS; CARCINOGENICITY TESTS; ENVIRONMENTAL POLLUTANTS; FLUOROCARBONS; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; OCTANOIC ACIDS; PANCREATIC NEOPLASMS; RATS; TESTICULAR NEOPLASMS;

RATTUS; RODENTIA;

EID: 84861528311     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2011.10.014     Document Type: Article

References (78)

1. Meek M.E., Bucher J.R., Cohen S.M., Dellarco V., Hill R.N., Lehman-McKeeman L.D., et al. A framework for human relevance analysis of information on carcinogenic modes of action. Crit Rev Toxicol 2003, 33:591-653.
2. Seed J., Carney E., Corley R., Crofton K., DeSesso J., Foster P., et al. Using mode of action and life stage information to evaluate the human relevance of animal toxicity data. Crit Rev Toxicol 2005, 35:663-672.
3. Boobis A.R., Cohen S.M., Dellarco V., McGregor D., Meek M.E., Vickers C., et al. IPCS framework for analyzing the relevance of a cancer mode of action for humans. Crit Rev Toxicol 2006, 36:781-792.
4. Boobis A.R., Doe J.E., Heinrich-Hirsche B., Meek M.E., Munn S., Ruchirawat M., et al. IPCS Framework for analysing the relevance of a non-cancer mode of action for humans. Crit Rev Toxicol 2008, 36:781-792.
5. Meek M.E. Recent developments in frameworks to consider human relevance of hypothesized modes of action for tumours in animals. Environ Mol Mutagen 2008, 49:110-116.
6. Biegel L.B., Hurtt M.E., Frame S.R. Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male CD rats. Toxicol Sci 2001, 60(1):44-55.
7. Lundin J.I., Alexander B.H., Olsen G.W., Church T.R. Ammonium perfluorooctanoate production and occupational mortality. Epidemiology 2009, 20:921-928.
8. Eriksen K.T., Raaschou-Nielsen O., Sørensen M., Roursgaard M., Loft S., Møller P. Genotoxic potential of the perfluorinated chemicals PFOA, PFOS, PFBS PFNA and PFHxA in human HepG2 cells. Mutat Res 2010, 700:39-43.
9. Klaunig J.E., Babich M.A., Baetcke K.P., Cook J.C., Corton J.C., David R.M., et al. PPARα agonist-induced rodent tumors: Modes of action and human relevance. Crit Rev Toxicol 2003, 33(6):655-780.
10. Sakr C.J., Kreckman K.H., Green J.W., Gillies P.J., Reynolds J.L., Leonard R.C. Cross-sectional study of lipids and liver enzymes related to a serum biomarker of exposure (ammonium perfluorooctanoate or APFO) as part of a general health survey in a cohort of occupationally exposed workers. J Occup Environ Med 2007, 49:1086-1096.
11. Olsen G.W., Gilliland F.D., Burlew M.M., Burris J.M., Mandel J.S., Mandel J.H. An epidemiologic investigation of reproductive hormones in men with occupational exposure to perfluorooctanoic acid. J Occup Environ Med 1998, 40(7):614-622.
12. Costa G., Sartori S., Consonni D. Thirty years of medical surveillance in perfluooctanoic acid production workers. J Occup Environ Med 2009, 51:364-372.
13. Emmett E.A., Zhang H., Shofer F.S., Zhang H., Freeman D., Desai C., et al. Community exposure to perfluorooctanoate: relationships between serum levels and certain health parameters. J Occup Environ Med 2006, 48:771-779.
14. Alexander B. Mortality study of workers employed at the 3MCottage Grove facility 2001, University of Minnesota, Minneapolis, MN, USEPA Public Docket AR-226-1030 a018.
15. Olsen G.W., Burris J.M., Burlew M.M., Mandel J.H. Plasma cholecystokinin and hepatic enzymes, cholesterol and lipoproteins in ammonium perfluorooctanoate production workers. Drug Chem Toxicol 2000, 23(4):603-620.
16. Sakr C.J., Leonard R.C., Kreckmann K.H., Slade M.D., Cullen M.R. Longitudinal study of serum lipids and liver enzymes in workers with occupational exposure to ammonium perfluorooctanoate. J Occup Environ Med 2007, 49:872-879.
17. OPPTS Office of Prevention, Pesticides and Toxic Substances, EPA.
18. Maloney E.K., Waxman D.J. trans-Activation of PPARα and PPARγ by structurally diverse environmental chemicals. Toxicol Appl Pharmacol 1999, 161:209-218.
19. Vanden Heuvel J.P, Thompson J.T., Frame S.R., Gillies P.J. 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 2006, 92:476-489.
20. Martin M.T., Brennan R.J., Hu W., Ayanoglu E., Lau C., Ren H., et al. Toxicogenomic study of triazole fungicides and perfluoroalkyl acids in rat livers predicts toxicity and categorizes chemicals based on mechanisms of toxicity. Toxicol Sci 2007, 97:595-613.
21. Kennedy G.L., Butenhoff J.L., Olsen G.W., O'Connor J.C., Seacat A.M., Perkins R.G., et al. The toxicology of perfluorooctanoate. Crit Rev Toxicol 2004, 34:351-384.
22. Pastoor T.P., Lee K.P., Perri M.A., Gillies P.J. Biochemical and morphological studies of ammonium perfluorooctanoate-induced hepatomegaly and peroxisome proliferation. Exp Mol Pathol 1987, 47(1):98-109.
23. Sohlenius A.K., Lundgren B., DePierre J.W. Perfluorooctanoic acid has persistent effects on peroxisome proliferation and related parameters in mouse liver. J Biochem Toxicol 1992, 7(4):205-212.
24. Kennedy G.L., Hall G.T., Brittelli M.R., Barnes J.R., Chen H.C. Inhalation toxicity of ammonium perfluorooctanoate. Food Chem Toxicol 1986, 24(12):1325-1329.
25. Takagi A., Sia K., Umemura T., Hasegawa R., Kurokawa Y. Hepatomegaly is an early biomarker for hepatocarcinogenesis induced by peroxisome proliferators. J Environ Pathol Toxicol Oncol 1992, 11:145-149.
26. Thottassery J., Winberg L., Youssef J., Cunningham M., Badr M.Z. Regulation of perfluorooctanoic acid-induced peroxisomal enzyme activities and hepatocellular growth by adrenal hormones. Hepatology 1992, 15:316-322.
27. Abdellatif A.G., Préat V., Vamecq J., Nilsson R., Roberfroid M. Peroxisome proliferation and modulation of rat liver carcinogenesis by 2 4-dichlorophenoxyacetic acid, 2,4,5,-trichlorophenoxyacetic acid, perfluorooctanoic acid and nafenopin. Carcinogenesis 1990, 11:1899-1902.
28. Isenberg J.S., Kamendulis L.M., Ackley D.C., Smith J.H., Pugh G., Lington A.W., et al. Reversibility and persistence of di-2-ethylhexyl phthalate- and phenobarbital-induced hepatocellular changes in rodents. Toxicol Sci 2001, 64:192-199.
29. Palazzolo MJ. Final report, 13-week dietary toxicity study with T-5180, ammonium perfluorooctanoate (CAS No 3825-26-1) in male rats. Report prepared by Hazleton Wisconsin Inc. Project HWI 6329-100; 1993.
30. Liu R.C., Hurtt M.E., Cook J.C., Biegel L.B. Effect of the peroxisome proliferator, ammonium perfluorooctanoate (C8), on hepatic aromatase activity in adult male Crl:CD BR (CD) rats. Fundam Appl Toxicol 1996, 30:220-228.
31. Lawlor TE. Mutagenicity test with T-6342 in the Salmonella-Escherichia coli/mammalian- microsome reverse mutation assay. Study No. 17073-0-409. Report prepared by Corning Hazleton, Vienna, Virginia; 1995.
32. Lawlor TE. Mutagenicity test with T-6564 in the Salmonella-Escherichia coli/mammalian-microsome reverse mutation assay with a confirmatory assay. Study No. 17750-0-409R. Report prepared by Corning Hazleton, Vienna, Virginia; 1996.
33. Litton Bionetics Inc. Mutagenicity evaluation of T-2015CoC in the Ames Salmonella/microsome plate test. Project No. 20838. Final report submitted to 3M Company, St. Paul, Minnesota; 1978.
34. Hazleton Inc. Mutagenicity test with T-6342 in the Salmonella-E. coli/mammalian microsome reverse mutation assay. Corning Hazleton Inc., Final Report CHV Study No. 17073-0-409, December 14, 1995, US EPA Public Docket AR-226-0436, Washington, DC; 1995.
35. Sadhu D. CHO/HGPRT forward mutation assay - ISO (T6.889.7) Toxicon Corporation, Bedford MA, Toxicon Final Report: 01-7019-G1 Submitted to: 3M, St. Paul Minnesota 55144-1000; 2002.
36. Murli H. Mutagenicity test on T-6342 measuring chromosomal aberrations in Chinese hamster ovary (CHO) cells: with a confirmatory assay with multiple harvests. Final report 17073-0-437CO dated September 16, 1996. Prepared by Corning Hazleton Inc., Vienna, Virginia; 1996.
37. NOTOX. Evaluation of the ability of T-7524 to induce chromosomal aberrations in cultured peripheral human lymphocytes. Notox Project No. 292062. Hertogenbosch, the Netherlands. U.S. EPA Public Docket AR-226-0404, Washington; 2002.
38. Murli H. Mutagenicity test on T6358 measuring chromosomal aberrations in Chinese hamster ovary (CHO) cells. Final report 17388-0-437 dated April 25, 1996. Prepared by Corning Hazleton Inc., Vienna, Virginia; 1996.
39. Garry VF, Nelson RL. An Assay of Cell Transformation and Cytotoxicity in C3H 10 1/2 Clonal Cell Line for the Test Chemical T-2942 CoC. 3 M Company, St. Paul, MN; 1981.
40. Yao X., Zhang L. Genotoxic risk and oxidative DNA damage in HepG2 cells exposed to perfluorooctanoic acid. Mutat Res 2005, 587:38-44.
41. Sibinski L.J. Two-year oral (diet) toxicity/carcinogenicity study of fluorochemical FC-143 in rats. (Riker Experiment No. 0281CR0012.) 1987, 1-4. Riker Laboratories Inc./3M Company, St. Paul, MA.
42. Yang Q., Abedi-Valugerdi M., Xie Y., Zhao X.-Y., Möller G., Nelson B.D., et al. Potent suppression of the adaptive immune response in mice upon dietary exposure to the potent peroxisome proliferator, perfluorooctanoic acid. Int Immunopharmacol 2002, 2:389-397.
43. Takacs M.L., Abbott B.D. Activation of mouse and human peroxisome proliferator-activated receptors (α, β/δ γ) by perfluorooctanoic acid and perfluorooctane sulfonate. Toxicol Sci 2007, 95:108-117.
44. Rosen M.B., Abbott B.D., Wolf D.C., Corton J.C., Wood C.R., Schmid J.E., et al. Gene profiling in the livers of wild-type and PPARα-null mice exposed to perfluorooctanoic acid. Toxicol Path 2008, 36:592-607.
45. Rosen M.B., Schmid J.R., Corton J.C., Zehr R.D., Das K.P., Abbott B.D., et al. Gene expression profiling in wild-type and PPARα-null mice exposed to perfluorooctane sulfonate reveals PPARα-independent effects. PPAR Res 2010, article ID 794739, 23 p.
46. Ren H., Vallanat B., Vallanat B. Evidence for the involvement of xenobiotic-responsive nuclear receptors in transcriptional effects upon perfluoroalkyl acid exposure in diverse species. Reprod Toxicol 2009, 27:266-277.
47. Yager J.D., Yager R. Oral contraceptive steroids as promoters of hepatocarcinogenesis in female Sprague-Dawley rats. Cancer Res 1980, 40:3680-3685.
48. Cameron R.G., Imaida K., Tsuda H., Ito N. Promotive effects of steroids and bile acids on hepatocarcinogenesis initiated by diethylnitrosamine. Cancer Res 1982, 42:2426-2428.
49. Panaretakis T., Shabalina I.G., Grandér D., Shoshan M.C., DePierre J.W. Reactive oxygen species and mitochondria mediate the induction of apoptosis in human hepatoma HepG2 cells by the rodent peroxisome proliferator and hepatocarcinogen, perfluorooctanoic acid. Toxicol Appl Pharmacol 2001, 173:56-64.
50. Berthiaume J., Wallace K.B. Perfluorooctanoate, perflourooctanesulfonate, and N-ethyl perfluorooctanesulfonamido ethanol; peroxisome proliferation and mitochondrial biogenesis. Toxicol Lett 2002, 129:23-32.
51. Keller B.J., Yamanaka H., Thunnan R.G. Inhibition of mitochondria1 respiration and oxygen-dependent hepatotoxicity by six structurally dissimilar peroxisomal proliferating agents. Toxicology 1992, 71:49-61.
52. Starkov A.A., Wallace K.B. Structural determinants of fluorochemical-induced mitochondrial dysfunction. Toxicol Sci 2002, 66(2):244-252.
53. Trosko J.E., Ruch R. Cell to cell communication in carcinogenesis. Front Biosci 1998, 3:208-236.
54. Upham B.L., Deocampo N.D., Wurl B., Trosko J.E. Inhibition of gap junctional intercellular communication by perfluorinated fatty acids is dependent on the chain length of the fluorinated tail. Int J Cancer 1998, 78:491-495.
55. Palmer C.N.A., Hsu M.H., Griffin K.J., Raucy J.L., Johnson E.F. Peroxisome proliferator activated receptor-α expression in human liver. Mol Pharmacol 1998, 53:14-22.
56. Tugwood J.D., Holden P.R., James N.H., Prince R.A., Roberts R.A. A peroxisome proliferator-activated receptor-alpha (PPARalpha) cDNA cloned from guinea-pig liver encodes a protein with similar properties to the mouse PPARalpha: implications for species differences in responses to peroxisome proliferators. Arch Toxicol 1998, 72:169-177.
57. Cheung C., Akiyama T.E., Ward J.M., Nicol C.J., Feigenbaum L., Vinson C., et al. Diminished hepatocellular proliferation in mice humanized for the nuclear receptor peroxisome proliferator-activated receptor-α. Cancer Res 2004, 64:3849-3854.
58. Butenhoff J., Costa G., Elcombe C., Farrar D., Hansen K., Iwai H., et al. Toxicity of ammonium perfluorooctanoate in male cynomolgus monkeys after oral dosing for 6 months. Toxicol Sci 2002, 69(1):244-257.
59. Riker Pharmaceuticals. Two year oral (diet) toxicity/carcinogenicity study of fluorochemical FC-143 in rats. Riker Laboratory, Experiment number 0281CR0012. U.S. EPA Public Docket AR-226; 1987.
60. Cook J.C., Hurtt M.E., Frame S.R., Biegel L.B. Mechanisms of extrahepatic tumor induction by peroxisome proliferators in Crl:CD R _BR (CD) rats. Toxicologist 1994, 14:301.
61. Biegel L.B., Liu R.C.M., Hurtt M.E., Cook J.C. Effects of ammonium perfluorooctanoate on Leydig cell function: in vitro, in vivo, and ex vivo studies. Toxicol Appl Pharmacol 1995, 134(1):18-25.
62. Teerds K.J., Rommerts F.F., Dorrington J.H. Immunohistochemical detection of transforming growth factor-α in Leydig cells during the development of the rat testis. Mol Cell Endocrinol 1990, 69:R1-R6.
63. Khan S., Teerds K., Dorrington J. Growth factor requirements for DNA synthesis by Leydig cells from the immature rat. Biol Reprod 1992, 46:335-341.
64. Gazouli M., Yao Z.X., Boujrad N., Corton J.C., Culty M., Papadopoulos V. Effect of peroxisome proliferators on Leydig cell peripheral-type benzodiazepine receptor gene expression, hormone-stimulated cholesterol transport, and steroidogenesis: role of the peroxisome proliferator-activator receptor alpha. Endocrinology 2002, 143:2571-2583.
65. Clegg E.D., Cook J.C., Chapin R.E., Foster P.D., Daston G.P. Leydig cell hyperplasia and adenoma formation: mechanisms and relevance to humans. Reprod Toxicol 1997, 11:107-121.
66. Prentice D.E., Meikle A.W. A review of drug-induced Leydig cell hyperplasia and neoplasia in the rat and some comparisons with man. Hum Exp Toxicol 1995, 14:562-572.
67. Longnecker D.S., Sumi C. Effects of sex steroid hormones on pancreatic cancer in the rat. Int J Pancreatol 1990, 7(1-3):159-165.
68. Longnecker D.S. Early morphologic markers of carcinogenicity in rat pancreas. In application of biological markers to carcinogen testing 1983, 43-60. Plenum, New York. H. Milman, S. Sell (Eds.).
69. Longnecker D.S. Interface between adaptive and neoplastic growth in the pancreas. Gut 1987, 28:253-258.
70. Obourn J.D., Frame S.R., Bell R.H., Longnecker D.S., Elliott G.S., Cook J.C. Mechanisms for the pancreatic oncogenic effects of the peroxisome proliferatorWyeth-14,643. Toxicol Appl Pharmacol 1997, 145:425-436.
71. Herrington M.K., Adrian T.E. On the role of cholecystokinin in pancreatic cancer. Int J Pancreatol 1995, 17:121-138.
72. Gavin C.E., Martin N.P., Schlosser M.J. Absence of specific CCK-A binding sites on human pancreatic membranes. Toxicologist 1996, 30:334.
73. Cattley R.C., DeLuca J., Elcombe C., Fenner-Crisp P., Lake B.G., Marsman D.S., et al. Do peroxisome proliferating compounds pose a hepatocarcinogenic hazard to humans. Regul Toxicol Pharmacol 1998, 27:47-60.
74. Pandol S.J. Pancreatic physiology secretory testing. Gastrointestinal and liver diseases 1998, vol. 1:771-782. W.B. Saunders, Philadelphia.
75. Elcombe C.R., Elcombe B.M., Foster J.R., Farrar D.G., Jung R., Chang S.C., et al. Hepatocellular hypertrophy and cell proliferation in Sprague-Dawley rats following dietary exposure to ammonium perfluorooctanoate occurs through increased activation of the xenosensor nuclear receptors PPARa and CAR/PXR. Arch Toxicol 2010, 84:787-798.
76. Corton J.C., Lapinskas P.J., Gonzalez F.J. Central role of PPARα in the mechanism of action of hepatocarcinogenic peroxisome proliferators. Mutat Res/Fundam Mol Mech Mutagen 2000, 448:139-151.
77. Gonzalez F.J., Shah Y.M. PPARα: mechanism of species differences and hepatocarcinogenesis of peroxisome proliferators. Toxicology 2008, 246:2-8.
78. Peters J.M., Cheung C., Gonzalez F.J. Peroxisome proliferator-activated receptor-alpha and liver cancer: where do we stand?. J Mol Med 2005, 83:774-785.