Endocrine-disrupting activity of hydraulic fracturing chemicals and adverse health outcomes after prenatal exposure in male mice

Endocrinology (United States)

Volumn 156, Issue 12, 2015, Pages 4458-4473

  Kassotis, Christopher D ^a   Klemp, Kara C ^b   Vu, Danh C ^c   Lin, Chung Ho ^c   Meng, Chun Xia ^b   Besch Williford, Cynthia L ^d   Pinatti, Lisa ^e   Zoeller, R Thomas ^e   Drobnis, Erma Z ^b   Balise, Victoria D ^b,c   Isiguzo, Chiamaka J ^b   Williams, Michelle A ^c   Tillitt, Donald E ^f   Nagel, Susan C ^b,c  

^a DUKE UNIVERSITY   (United States)

^b University of Missouri   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d IDEXX RADIL   (United States)

^e UNIVERSITY OF MASSACHUSETTS   (United States)

^f Jackson Field Research Station   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,4 TRIMETHYLBENZENE; 2 ETHYLHEXANOL; ACRYLAMIDE; ANDROGEN; BENZENE; BORATE SODIUM; BRONOPOL; CELL NUCLEUS RECEPTOR; CUMENE; ENDOCRINE DISRUPTOR; ESTRADIOL; ESTROGEN; ETHOXYLATED NONYLPHENOL; ETHOXYLATED OCTYLPHENOL; ETHYLBENZENE; ETHYLENE GLYCOL; GLUCOCORTICOID; N,N DIMETHYLFORMAMIDE; NAPHTHALENE; NATURAL GAS; OIL; PHENOL; PROGESTERONE; PROPYLENE GLYCOL; STYRENE; TESTOSTERONE; TOLUENE; TRIETHYLENE GLYCOL; UNCLASSIFIED DRUG; XYLENE; ANDROGEN RECEPTOR; ESTROGEN RECEPTOR; GLUCOCORTICOID RECEPTOR; PROGESTERONE RECEPTOR; THYROID HORMONE RECEPTOR; WASTE WATER;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENVIRONMENTAL IMPACT; ESTROGEN RESPONSIVE ELEMENT; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; LIQUID LIQUID EXTRACTION; MALE; MASS FRAGMENTOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; REPORTER GENE; SOLID PHASE MICROEXTRACTION; SPERMATOZOON COUNT; TESTOSTERONE BLOOD LEVEL; WASTE WATER; ANIMAL; BLOOD; BODY WEIGHT; CHEMISTRY; DRUG EFFECTS; FEMALE; FRACKING; ORGAN SIZE; PATHOLOGY; PREGNANCY; SPERMATOZOON; SPERMATOZOON MOTILITY; TESTIS;

ANIMALS; BODY WEIGHT; ENDOCRINE DISRUPTORS; FEMALE; HYDRAULIC FRACKING; MALE; MICE; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RECEPTORS, ANDROGEN; RECEPTORS, ESTROGEN; RECEPTORS, GLUCOCORTICOID; RECEPTORS, PROGESTERONE; RECEPTORS, THYROID HORMONE; SPERM COUNT; SPERM MOTILITY; SPERMATOZOA; TESTIS; TESTOSTERONE; WASTE WATER;

EID: 84948187934     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1375     Document Type: Article

References (90)

1. Kassotis CD, Tillitt DE, Davis JW, Hormann AM, Nagel SC. Estrogen and androgen receptor activities of hydraulic fracturing chemicals and surface and ground water in a drilling-dense region. Endocrinology. 2014;155(3):897-907.
2. Webb E, Bushkin-Bedient S, Cheng A, Kassotis CD, Balise V, Nagel SC. Developmental and reproductive effects of chemicals associated with unconventional oil and natural gas operations. Rev Environ Health. 2014;29(4):307-318.
3. Zoeller RT, Brown TR, Doan LL, et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology. 2012;153(9):4097-4110.
4. The Endocrine Disruption Exchange (TEDX). TEDX list of potential endocrine disruptors. 2013. http://endocrinedisruption.org/ endocrine-disruption/tedx-list-of-potential-endocrine-disruptors/ overview Accessed March 13, 2015.
5. Yang M, Park MS, Lee HS. Endocrine disrupting chemicals: human exposure and health risks. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2006;24(2):183-224.
6. Tyler CR, Jobling S, Sumpter JP. Endocrine disruption in wildlife: a critical review of the evidence. Crit Rev Toxicol. 1998;28(4):319-361.
7. Jansen MS, Nagel SC, Miranda PJ, Lobenhofer EK, Afshari CA, McDonnell DP. Short-chain fatty acids enhance nuclear receptor activity through mitogen-activated protein kinase activation and histone deacetylase inhibition. Proc Natl Acad Sci USA. 2004; 101(18):7199-7204.
8. Chen J, Ahn KC, Gee NA, et al. Triclocarban enhances testosterone action: a new type of endocrine disruptor? Endocrinology. 2007; 149(3):1173-1179.
9. Hayes TB. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA. 2002;99(8):5476-5480.
10. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, et al. Endocrine- disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009;30(4):293-342.
11. Welshons WV, Thayer KA, Judy BM, Taylor JA, Curran EM, vom Saal FS. Large effects from small exposures. I. Mechanisms for endocrine- disrupting chemicals with estrogenic activity. Environ Health Perspect. 2003;111(8):994-1006.
12. Myers JP, Zoeller RT, vom Saal FS. A clash of old and new scientific concepts in toxicity, with important implications for public health. Environ Health Perspect. 2009;117(11):1652-1655.
13. Vom Saal FS, Akingbemi BT, Belcher SM, et al. Chapel Hill Bisphenol A Expert Panel consensus statement: integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod Toxicol. 2007;24(2):131-138.
14. Vandenberg LN, Colborn T, Hayes TB, et al. Hormones and endocrine- disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 2012;33(3):378-455.
15. Waxman HA, Markey EJ, DeGette D. 2011. Chemicals used in hydraulic fracturing. The Committee on Energy and Commerce, US HouseofRepresentatives.http://democrats.energycommerce.house. gov/sites/default/files/documents/Hydraulic-Fracturing-Chemicals- 2011-4-18.pdf. Accessed March 1, 2015.
16. Wiseman HJ. Untested waters: the rise of hydraulic fracturing in oil and gas production and the need to revisit regulation. Fordham Environ Law Rev. 2008;20:115-169.
17. Colborn T, Kwiatkowski C, Schultz K, Bachran M. Natural gas operations from a public health perspective. Int J Hum Ecol Risk Assess. 2011;17(5):1039-1056.
18. Kassotis CD, Tillitt DE, Lin CH, McElroy JA, Nagel SC. Endocrinedisrupting chemicals and oil and natural gas operations: potential environmental contamination and recommendations to assess complex environmental mixtures. Environ Health Perspect. In press.
19. Deutch J, Holditch S, Krupp F, et al. 2011. The Secretary of the Energy Board Shale Gas Production Subcommittee Ninety-Day Report. http://www.shalegas.energy.gov/resources/081811-90-day- report-final.pdf. Accessed March 8, 2015.
20. Lee DS, Herman JD, Elsworth D, Kim HT, Lee HS. A critical evaluation of unconventional gas recovery from the Marcellus Shale, Northeastern United States. KSCE J Civil Eng. 2011;15(4):679-687.
21. Environmental Protection Agency. Assessment of the potential impacts of hydraulic fracturing for oil and gas on drinking water resources. External review draft. 2015. http://cfpub.epa.gov/ncea/ hfstudy/recordisplay.cfm?deid-244651. Accessed July 15, 2015.
22. Riedl J, Rotter S, Faetsch S, Schmitt-Jansen M, Altenburger R. Proposal for applying a component-based mixture approach for ecotoxicological assessment of fracturing fluids. Environ Earth Sci. 2013;70:3907-3920.
23. Osborn SG, Vengosh A, Warner NR, Jackson RB. Methane contamination of drinking water accompanying gas-well drilling and hydraulic fracturing. Proc Natl Acad Sci USA. 2011;108(20):5.
24. Jackson RB, Vengosh A, Darrah TH, et al. Increased stray gas abundance in a subset of drinking water wells near Marcellus Shale gas extraction. Proc Natl Acad Sci USA. 2013;110(28):11250-11255.
25. Fontenot BE, Hunt LR, Hildenbrand ZL, et al. An evaluation of water quality in private drinking water wells near natural gas extraction sites in the Barnett Shale Formation. Environ Sci Technol. 2013;47(17):10032-10040.
26. Warner NR, Christie CA, Jackson RB, Vengosh A. Impacts of shale gas wastewater disposal on water quality in western Pennsylvania. Environ Sci Technol. 2013;47(20):11849-11857.
27. DiGiulio DC, Wilkin RT, Miller C, Oberley G. Investigation of ground water contamination near Pavillion, WY. Environmental Protection Agency, 600/R-00/000. 2011. http://www2.epa.gov/ region8/draft-investigation-ground-water-contamination-nearpavillion- wyoming. Accessed February 25, 2015.
28. Rozell DJ, Reaven SJ. Water pollution risk associated with natural gas extraction from the Marcellus Shale. Risk Analysis. 2012;32(8): 1382-1393.
29. Mauter MS, Alvarez PJ, Burton A, et al. Regional variation in waterrelated impacts of shale gas development and implications for emerging international plays. Environ Sci Technol. 2014;45(15): 8298-8306.
30. Werner AK, Vink S, Watt K, Jagals P. Environmental health impacts of unconventional natural gas development: a review of the current strength of evidence. Sci Total Environ. 2015;505C:1127-1141.
31. Bamberger M, Oswald RE. Impacts of gas drilling on human and animal health. New Solutions. 2012;22(1):51-77.
32. Rabinowitz PM, Slizovskiy IB, Lamers V, et al. Proximity to natural gas wells and reported health status: results of a household survey in Washington County, PA. Environ Health Perspect. 2015;123(1): 21-26.
33. McKenzie LM, Guo R, Witter RZ, Savitz DA, Newman LS, Adgate JL. Birth outcomes and maternal residential proximity to natural gas development in rural Colorado. Environ Health Perspect. 2014; 122(4):412-417.
34. Janerich DT, Dugan JM, Standfast SJ, Strite L. Congenital heart disease and prenatal exposure to exogenous sex hormones. Br Med J. 1977;1(6068):1058-1060.
35. Snijder CA, Vlot IJ, Burdorf A, et al. Congenital heart defects and parental occupational exposure to chemicals. Hum Reprod. 2012; 27(5):1510-1517.
36. Facemire CF, Gross TS, Guillette LJ Jr. Reproductive impairment in the Florida panther: nature or nurture? Environ Health Perspect. 1995;103(4):79-86.
37. Rull RP, Ritz B, Shaw GM. Neural tube defects and maternal residential proximity to agricultural pesticide applications. Am J Epidemiol. 2006;163(8):743-753.
38. Nagel SC, Hagelbarger JL, McDonnell DP. Development of an ER action indicator mouse for the study of estrogens, selective ER modulators (SERMs), and xenobiotics. Endocrinology. 2001;142(11): 4721-4728.
39. MacGregor GR, Caskey CT. Construction of plasmids that express E coliβ-galactosidase in mammalian cells. Nucleic Acids Res. 1989; 17(6):1.
40. Lubahn DB, Joseph DR, Sullivan PM, Willard HF, French FS, Wilson EM. Cloning ofhumanandrogen receptor complementaryDNA and localization to the X chromosome. Science. 1988;240:4.
41. Huang W, Shostak Y, Tarr P, Sawyers C, Carey M. Cooperative assembly of androgen receptor into a nucleoprotein complex that regulates the prostate-specific antigen enhancer J Biol Chem. 1999; 274(36):13.
42. Dong X, Challis JR, Lye SJ. Intramolecular interactions between the AF3domain and the C-terminus of thehumanprogesterone receptor are mediated through two LXXLL motifs. J Mol Endocrinol. 2004; 32(3):843-857.
43. Giangrande PH, Kimbrel EA, Edwards DP, McDonnell DP. The opposing transcriptional activities of the two isoforms of the human progesterone receptor are due to differential cofactor binding. Mol Cell Biol. 2000;20(9):3102-3115.
44. Yoh SM, Chatterjee VK, Privalsky ML. Thyroid hormone resistance syndrome manifests as an aberrant interaction between mutant T3 receptors and transcriptional corepressors. Mol Endocrinol. 1997; 11(4):470-480.
45. Freitas J, Cano P, Craig-Veit C, Goodson ML, Furlow JD, Murk AJ. Detection of thyroid hormone receptor disruptors by a novel stable in vitro reporter gene assay. Toxicol In Vitro. 2011;25(1):257-266.
46. Sathya G, Jansen MS, Nagel SC, Cook CE, McDonnell DP. Identification and characterization of novel estrogen receptor-α-sparing antiprogestins. Endocrinology. 2002;143(8):3071-3082.
47. Hynes N, van Ooyen AJ, Kennedy N, Herrlich P, Ponta H, Groner B. Subfragments of the large terminal repeat cause glucocorticoidresponsive expression of mouse mammary tumor virus and of an adjacent gene. Proc Natl Acad Sci USA. 1983;80(12):3637-3641.
48. Brasier AR, Tate JE, Habener JF. Optimized use of the firefly luciferase assay as a reporter gene in mammalian cell lines. Biotechniques. 1989;7(10):6.
49. Promega. 2012. Celltiter 96 non-radioactive cell proliferation assay- instructions for use. https://www.promega.com/~/media/files/resources/ protocols/technical%20bulletins/0/celltiter%2096%20nonradioactive% 20cell%20proliferation%20assay%20protocol.pdf. Accessed March 18, 2015.
50. Kortenkamp A, Altenburger R. Synergisms with mixtures of xenoestrogens: a reevaluation using the method of isoboles. Sci Total Environ. 1998;221(1):59-73.
51. Lin C-H, Lerch RN, Garrett HE, George MF. Improved GC-MS/MS method for determination of atrazine and its chlorinated metabolites in forage plants-laboratory and field experiments. Commun Soil Sci Plant Anal. 2007;38(13-14):1753-1773.
52. Lin C-H, Lerch RN, Garrett HE, George MF. Bioremediation of atrazine-contaminated soil by forage grasses: transformation, uptake, and detoxification. J Environ Qual. 2008;37(1):196-206.
53. Kawai Y, Hata T, Suzuki O, Matsuda J. The relationship between sperm morphology and in vitro fertilization ability in mice. J Reprod Dev. 2006;52(4):561-568.
54. Orem W, Tatu C, Varonka M, et al. Organic substances in produced and formation water from unconventional natural gas extraction in coal and shale. Int J Coal Geol. 2014;126:20-31.
55. Ferrer I, Thurman EM. Chemical constituents and analytical approaches for hydraulic fracturing waters. Trends Environ Anal Chem. 2015;5:18-25.
56. Lester Y, Ferrer I, Thurman EM, et al. Characterization of hydraulic fracturing flowback water in Colorado: implications for water treatment. Sci Total Environ. 2015;512-513C:637-644.
57. Gross SA, Avens HJ, Banducci AM, Sahmel J, Panko JM, Tvermoes BE. Analysis of BTEX groundwater concentrations from surface spills associated with hydraulic fracturing operations. J Air Waste Manag Assoc. 2013;63(4):424-432.
58. McIntyre BS, Barlow NJ, Foster PM. Androgen-mediated development in male rat offspring exposed to flutamide in utero: permanence and correlation of early postnatal changes in anogenital distance and nipple retention with malformations in androgendependent tissues. Toxicol Sci. 2001;62(2):236-249.
59. You L, Casanova M, Archibeque-Engle S, Sar M, Fan LQ, Heck HA. Impaired male sexual development in perinatal Sprague-Dawley and Long-Evans hooded rats exposed in utero and lactationally to p, p- DDE. Toxicol Sci. 1998;45(2):162-173.
60. Yeh S, Tsai MY, Xu Q, et al. Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc Natl Acad Sci USA. 2002;99(21):13498-13503.
61. Van Haaster LH, De Jong FH, Docter R, De Rooij DG. The effect of hypothyroidism on Sertoli cell proliferation and differentiation and hormone levels during testicular development in the rat. Endocrinology. 1992;131(3):1574-1576.
62. Maran RR, Ravichandran K, Arunakaran J, Aruldhas MM. Impact of neonatal hypothyroidism on Leydig cell number, plasma, and testicular interstitial fluid sex steroids concentration. Endocr Res. 2001;27(1-2):119-141.
63. Rijntjes E, Swarts HJ, Anand-Ivell R, Teerds KJ. Prenatal induced chronic dietary hypothyroidism delays but does not block adult-type Leydig cell development. Am J Physiol Endocrinol Metab. 2009; 296(2):E305-E314.
64. Teerds KJ, de Rooij DG, de Jong FH, van Haaster LH. Development of the adult-type Leydig cell population in the rat is affected by neonatal thyroid hormone levels. Biol Reprod. 1998;59(2):344-350.
65. Kuriyama SN, Talsness CE, Grote K, Chahoud I. Developmental exposure to low dose PBDE 99: effects on male fertility and neurobehavior in rat offspring. Environ Health Perspect. 2005;113(2): 149-154.
66. Shibutani M, Woo GH, Fujimoto H, et al. Assessment of developmental effects of hypothyroidism in rats from in utero and lactation exposure to anti-thyroid agents. Reprod Toxicol. 2009;28(3):297-307.
67. Hess RA, Bunick D, Lee KH, et al. A role for oestrogens in the male reproductive system. Nature. 1997;390(6659):509-512.
68. Yoshida S, Ono N, Tsukue N, et al. In utero exposure to diesel exhaust increased accessory reproductive gland weight and serum testosterone concentration in male mice. Environ Sci. 2006;13(3): 139-147.
69. Mauderly JL, Garshick E. Diesel exhaust. In: Lippmann M, ed. Environmental Toxicants: Human Exposures and Their Health Effects. 3rd ed. Hoboken, NJ: John Wiley, Sons, Inc; 2009.
70. Stacy SL, Brink LL, Larkin JC, et al. Perinatal outcomes and unconventional natural gas operations in southwest Pennsylvania. PLoS One. 2015;10(6):e0126425.
71. Grun F, Blumberg B. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology. 2006;147(suppl 6):S50-S55.
72. Masuno H, Okamoto S, Iwanami J, et al. Effect of 4-nonylphenol on cell proliferation and adipocyte formation in cultures of fully differentiated 3T3-L1 cells. Toxicol Sci. 2003;75(2):314-320.
73. Hao CJ, Cheng XJ, Xia HF, Ma X. The endocrine disruptor 4-nonylphenol promotes adipocyte differentiation and induces obesity in mice. Cell Physiol Biochem. 2012;30(2):382-394.
74. Kim HW, Kam S, Lee DH. Synergistic interaction between polycyclic aromatic hydrocarbons and environmental tobacco smoke on the risk of obesity in children and adolescents: the US National Health and Nutrition Examination Survey 2003-2008. Environ Res. 2014;135:354-360.
75. Fulton RM, Hutchinson EC, Jones AM. Ventricular weight in cardiac hypertrophy. Br Heart J. 1952;14(3):413-420.
76. Hangartner JR, Marley NJ, Whitehead A, Thomas AC, Davies MJ. The assessment of cardiac hypertrophy at autopsy. Histopathology. 1985;9(12):1295-1306.
77. de Vries WB, van der Leij FR, Bakker JM, et al. Alterations in adult rat heart after neonatal dexamethasone therapy. Pediatr Res. 2002; 52(6):900-906.
78. Dodic M, Samuel C, Moritz K, et al. Impaired cardiac functional reserve and left ventricular hypertrophy in adult sheep after prenatal dexamethasone exposure. Circ Res. 2001;89(7):623-629.
79. Thum T, Borlak J. Testosterone, cytochrome P450, and cardiac hypertrophy. FASEB J. 2002;16(12):1537-1549.
80. Valenzuela-Alcaraz B, Crispi F, Bijnens B, et al. Assisted reproductive technologies are associated with cardiovascular remodeling in utero that persists postnatally. Circulation. 2013;128(13):1442-1450.
81. Incardona JP, Gardner LD, Linbo TL, et al. Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish. Proc Natl Acad Sci USA. 2014;111(15):E1510-E1518.
82. Olsen NJ, Watson MB, Henderson GS, Kovacs WJ. Androgen deprivation induces phenotypic and functional changes in the thymus of adult male mice. Endocrinology. 1991;129(5):2471-2476.
83. Viselli SM, Stanziale S, Shults K, Kovacs WJ, Olsen NJ. Castration alters peripheral immune function in normal male mice. Immunology. 1995;84(2):337-342.
84. Silva E, Rajapakse N, Scholze M, Backhaus T, Ermler S, Kortenkamp A. Joint effects of heterogeneous estrogenic chemicals in the E-Screen- exploring the applicability of concentration addition. Toxicol Sci. 2011;122(2):383-394.
85. Christiansen S, Scholze M, Dalgaard M, et al. Synergistic disruption of external male sex organ development by a mixture of four antiandrogens. Environ Health Perspect. 2009;117(12):1839-1846.
86. Ermler S, Scholze M, Kortenkamp A. The suitability of concentration addition for predicting the effects of multi-component mixtures of up to 17 anti-androgens with varied structural features in an in vitro AR antagonist assay. Toxicol Appl Pharmacol. 2011;257(2): 189-197.
87. Silva E, Rajapakse N, Kortenkamp A. Something from "nothing"- eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects. Environ Sci Technol. 2002;36(8):1751-1756.
88. Anzenbacher P, Anzenbacherova E. Cytochromes P450 and metabolism of xenobiotics. Cell Mol Life Sci. 2001;58(5-6):737-747.
89. Markowitz JS, Donovan JL, DeVane CL, et al. Effect of St John's wort on drug metabolism by induction of cytochrome P450 3A4 enzyme. JAMA. 2003;290(11):1500-1504.
90. Gauger KJ, Giera S, Sharlin DS, Bansal R, Iannacone E, Zoeller RT. Polychlorinated biphenyls 105 and 118 form thyroid hormone receptor agonists after cytochrome P4501A1 activation in rat pituitary GH3 cells. Environ Health Perspect. 2007;115(11):1623-1630.