Sex Specific Placental Accumulation and Behavioral Effects of Developmental Firemaster 550 Exposure in Wistar Rats

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Baldwin, Kylie R ^a   Phillips, Allison L ^b   Horman, Brian ^a   Arambula, Sheryl E ^a   Rebuli, Meghan E ^a   Stapleton, Heather M ^b   Patisaul, Heather B ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; BEHAVIOR CHANGE; BROMINATION; EXPOSURE; FEMALE; NONHUMAN; PLACENTA TISSUE; PREGNANCY; RAT; SEX DIFFERENCE; WISTAR RAT; AGE; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; CHEMICAL STRUCTURE; DOSE RESPONSE; DRUG EFFECT; MALE; METABOLISM; PLACENTA; SEX FACTOR;

FLAME RETARDANT;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FLAME RETARDANTS; MALE; MOLECULAR STRUCTURE; PLACENTA; PREGNANCY; RATS; RATS, WISTAR; SEX FACTORS;

EID: 85026747747     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-07216-6     Document Type: Article

References (70)

1. Stapleton, H. M. et al. Detection of organophosphate flame retardants in furniture foam and U. S. house dust. Environ Sci Technol 43, 7490-7495 (2009).
2. Grandjean, P. & Landrigan, P. J. Neurobehavioural effects of developmental toxicity. Lancet Neurol 13, 330-338, doi:10. 1016/S1474-4422(13)70278-3 (2014).
3. Kalkbrenner, A. E., Schmidt, R. J. & Penlesky, A. C. Environmental chemical exposures and autism spectrum disorders: a review of the epidemiological evidence. Current problems in pediatric and adolescent health care 44, 277-318, doi:10. 1016/j. cppeds. 2014. 06. 001 (2014).
4. Landrigan, P. J., Lambertini, L. & Birnbaum, L. S. A research strategy to discover the environmental causes of autism and neurodevelopmental disabilities. Environ. Health Perspect. 120, a258-260, doi:10. 1289/ehp. 1104285 (2012).
5. Masuo, Y. & Ishido, M. Neurotoxicity of endocrine disruptors: possible involvement in brain development and neurodegeneration. J Toxicol Environ Health B Crit Rev 14, 346-369, doi:10. 1080/10937404. 2011. 578557 (2011).
6. Messer, A. Mini-review: polybrominated diphenyl ether (PBDE) flame retardants as potential autism risk factors. Physiol Behav 100, 245-249, doi:10. 1016/j. physbeh. 2010. 01. 011 (2010).
7. Miodovnik, A. et al. Endocrine disruptors and childhood social impairment. Neurotoxicology 32, 261-267, doi:10. 1016/j. neuro. 2010. 12. 009 (2011).
8. Stapleton, H. M. et al. Novel and high volume use flame retardants in US couches reflective of the 2005 PentaBDE phase out. Environ Sci Technol 46, 13432-13439, doi:10. 1021/es303471d (2012).
9. Stapleton, H. M. et al. Alternate and new brominated flame retardants detected in U. S. house dust. Environ Sci Technol 42, 6910-6916 (2008).
10. Hoffman, K. et al. Urinary Tetrabromobenzoic Acid (TBBA) as a Biomarker of Exposure to the Flame Retardant Mixture Firemaster 550. Environ. Health Perspect. doi:10. 1289/ehp. 1308028 (2014).
11. Van den Eede, N., Neels, H., Jorens, P. G. & Covaci, A. Analysis of organophosphate flame retardant diester metabolites in human urine by liquid chromatography electrospray ionisation tandem mass spectrometry. J Chromatogr A 1303, 48-53, doi:10. 1016/j. chroma. 2013. 06. 042 (2013).
12. Johnson, P. I., Stapleton, H. M., Sjodin, A. & Meeker, J. D. Relationships between polybrominated diphenyl ether concentrations in house dust and serum. Environ Sci Technol 44, 5627-5632, doi:10. 1021/es100697q (2010).
13. Watkins, D. J. et al. Exposure to PBDEs in the office environment: evaluating the relationships between dust, handwipes, and serum. Environ Health Perspect 119, 1247-1252, doi:10. 1289/ehp. 1003271 (2011).
14. Stapleton, H. M., Eagle, S., Sjodin, A. & Webster, T. F. Serum PBDEs in a North Carolina toddler cohort: associations with handwipes, house dust, and socioeconomic variables. Environ Health Perspect 120, 1049-1054, doi:10. 1289/ehp. 1104802 (2012).
15. Al-Omrana, L. S. & Harrada, S. Polybrominated diphenyl ethers and "novel" brominated flame retardants in floor and elevated surface house dust from Iraq: Implications for human exposure assessment. Emerging Contaminants 2, 7-13 (2015).
16. Ali, N., Harrad, S., Goosey, E., Neels, H. & Covaci, A. "Novel" brominated flame retardants in Belgian and UK indoor dust: implications for human exposure. Chemosphere 83, 1360-1365, doi:10. 1016/j. chemosphere. 2011. 02. 078 (2011).
17. Ali, N. et al. Occurrence of alternative flame retardants in indoor dust from New Zealand: indoor sources and human exposure assessment. Chemosphere 88, 1276-1282, doi:10. 1016/j. chemosphere. 2012. 03. 100 (2012).
18. Liu, L. Y., He, K., Hites, R. A. & Salamova, A. Hair and Nails as Noninvasive Biomarkers of Human Exposure to Brominated and Organophosphate Flame Retardants. Environ Sci Technol 50, 3065-3073, doi:10. 1021/acs. est. 5b05073 (2016).
19. Zhou, S. N. et al. Measurements of selected brominated flame retardants in nursing women: implications for human exposure. Environ Sci Technol 48, 8873-8880, doi:10. 1021/es5016839 (2014).
20. Lam, J. C., Lau, R. K., Murphy, M. B. & Lam, P. K. Temporal trends of hexabromocyclododecanes (HBCDs) and polybrominated diphenyl ethers (PBDEs) and detection of two novel flame retardants in marine mammals from Hong Kong, South China. Environ Sci Technol 43, 6944-6949 (2009).
21. Salamova, A., Hermanson, M. H. & Hites, R. A. Organophosphate and halogenated flame retardants in atmospheric particles from a European Arctic site. Environ Sci Technol 48, 6133-6140, doi:10. 1021/es500911d (2014).
22. Zhu, B. et al. Changes of accumulation profiles from PBDEs to brominated and chlorinated alternatives in marine mammals from the South China Sea. Environ Int 66, 65-70, doi:10. 1016/j. envint. 2014. 01. 023 (2014).
23. Mendelsohn, E. et al. Nail polish as a source of exposure to triphenyl phosphate. Environ Int 86, 45-51, doi:10. 1016/j. envint. 2015. 10. 005 (2016).
24. Johnson, P. I., Stapleton, H. M., Mukherjee, B., Hauser, R. & Meeker, J. D. Associations between brominated flame retardants in house dust and hormone levels in men. The Science of the total environment 445-446, 177-184, doi:10. 1016/j. scitotenv. 2012. 12. 017 (2013).
25. Meeker, J. D. & Stapleton, H. M. House dust concentrations of organophosphate flame retardants in relation to hormone levels and semen quality parameters. Environ Health Perspect 118, 318-323, doi:10. 1289/ehp. 0901332 (2010).
26. Patisaul, H. B. et al. Accumulation and endocrine disrupting effects of the flame retardant mixture Firemaster 550 in rats: an exploratory assessment. J. Biochem. Mol. Toxicol. 27, 124-136, doi:10. 1002/jbt. 21439 (2013).
27. Bailey, J. M. & Levin, E. D. Neurotoxicity of Firemaster 550 in zebrafish (Danio rerio): Chronic developmental and acute adolescent exposures. Neurotoxicol Teratol 52, 210-219, doi:10. 1016/j. ntt. 2015. 07. 001 (2015).
28. Dishaw, L. V., Macaulay, L. J., Roberts, S. C. & Stapleton, H. M. Exposures, mechanisms, and impacts of endocrine-active flame retardants. Curr Opin Pharmacol 19, 125-133, doi:10. 1016/j. coph. 2014. 09. 018 (2014).
29. Phillips, A. L. et al. Editor's Highlight: Transplacental and Lactational Transfer of Firemaster 550 Components in Dosed Wistar Rats. Toxicol Sci 153, 246-257, doi:10. 1093/toxsci/kfw122 (2016).
30. Vizcaino, E., Grimalt, J. O., Fernandez-Somoano, A. & Tardon, A. Transport of persistent organic pollutants across the human placenta. Environ Int 65, 107-115, doi:10. 1016/j. envint. 2014. 01. 004 (2014).
31. Hsiao, E. Y. & Patterson, P. H. Placental regulation of maternal-fetal interactions and brain development. Dev Neurobiol 72, 1317-1326, doi:10. 1002/dneu. 22045 (2012).
32. Patisaul, H. B., Todd, K. L., Mickens, J. A. & Adewale, H. B. Impact of neonatal exposure to the ERalpha agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology 30, 350-357 (2009).
33. Patisaul, H. B. et al. Anxiogenic effects of developmental bisphenol a exposure are associated with gene expression changes in the juvenile rat amygdala and mitigated by soy. PLoS One 7, e43890, doi:10. 1371/journal. pone. 0043890 (2012).
34. Hunt, P. A., Susiarjo, M., Rubio, C. & Hassold, T. J. The bisphenol A experience: a primer for the analysis of environmental effects on mammalian reproduction. Biol. Reprod. 81, 807-813, doi:10. 1095/biolreprod. 109. 077008 (2009).
35. Richter, C. A. et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 24, 199-224 (2007).
36. Li, A. A. et al. Building a scientific framework for studying hormonal effects on behavior and on the development of the sexually dimorphic nervous system. Neurotoxicology 29, 504-519, doi:10. 1016/j. neuro. 2008. 02. 015 (2008).
37. Poletti, A., Celotti, F., Rumio, C., Rabuffetti, M. & Martini, L. Identification of type 1 5alpha-reductase in myelin membranes of male and female rat brain. Mol Cell Endocrinol 129, 181-190 (1997).
38. Nunn, G. & Macpherson, A. Spontaneous convulsions in Charles River Wistar rats. Lab Anim 29, 50-53 (1995).
39. Hicks, K. D. et al. Interaction of bisphenol A (BPA) and soy phytoestrogens on sexually dimorphic sociosexual behaviors in male and female rats. Horm Behav 84, 121-126, doi:10. 1016/j. yhbeh. 2016. 06. 010 (2016).
40. Pellow, S., Chopin, P., File, S. E. & Briley, M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14, 149-167 (1985).
41. Nasello, A. G., Machado, C., Bastos, J. F. & Felicio, L. F. Sudden darkness induces a high activity-low anxiety state in male and female rats. Physiol Behav 63, 451-454 (1998).
42. Becker, J. B. et al. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146, 1650-1673 (2005).
43. Patisaul, H. B., Blum, A., Luskin, J. R. & Wilson, M. E. Dietary soy supplements produce opposite effects on anxiety in intact male and female rats in the elevated plus-maze. Behav. Neurosci. 119, 587-594 (2005).
44. Haseman, J. K., Bailer, A. J., Kodell, R. L., Morris, R. & Portier, K. Statistical issues in the analysis of low-dose endocrine disruptor data. Toxicol. Sci 61, 201-210 (2001).
45. Rebuli, M. E. et al. Impact of Low Dose Oral Exposure to Bisphenol A (BPA) on Juvenile and Adult Rat Exploratory and Anxiety Behavior: A CLARITY-BPA Consortium Study. Toxicol. Sci. doi:10. 1093/toxsci/kfv163 (2015).
46. Antweiler, R. C. & Taylor, H. E. Evaluation of statistical treatments of left-censored environmental data using coincident uncensored data sets: I. Summary statistics. Environ Sci Technol 42, 3732-3738 (2008).
47. Gould, T. D. D., D. T. & Kovacsics, C. E. In Mood and Anxiety Related Phenotypes in Mice Neuromethods (ed. T. D. Gould) Ch. 1, (Humana Press, 2010).
48. Bailey, K. R. & Crawley, J. N. In Methods of Behavior Analysis in Neuroscience Frontiers in Neuroscience (ed. J. J. Buccafusco) Ch. 5, (CRC Press, 2009).
49. Goma, M. & Tobena, A. Reliability of various measures obtained in open-field test. Psychol Rep 43, 1123-1128, doi:10. 2466/ pr0. 1978. 43. 3f. 1123 (1978).
50. Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol 4, 863, doi:10. 3389/fpsyg. 2013. 00863 (2013).
51. Benstaali, C., Mailloux, A., Bogdan, A., Auzeby, A. & Touitou, Y. Circadian rhythms of body temperature and motor activity in rodents their relationships with the light-dark cycle. Life Sci 68, 2645-2656 (2001).
52. Bronson, S. L. & Bale, T. L. The Placenta as a Mediator of Stress Effects on Neurodevelopmental Reprogramming. Neuropsychopharmacology 41, 207-218, doi:10. 1038/npp. 2015. 231 (2016).
53. Myatt, L. Placental adaptive responses and fetal programming. J Physiol 572, 25-30, doi:10. 1113/jphysiol. 2006. 104968 (2006).
54. Konkel, L. Lasting Impact of an Ephemeral Organ: The Role of the Placenta in Fetal Programming. Environ Health Perspect 124, A124-129, doi:10. 1289/ehp. 124-A124 (2016).
55. Bronson, S. L. & Bale, T. L. Prenatal stress-induced increases in placental inflammation and offspring hyperactivity are male-specific and ameliorated by maternal antiinflammatory treatment. Endocrinology 155, 2635-2646, doi:10. 1210/en. 2014-1040 (2014).
56. Roberts, S. C., Macaulay, L. J. & Stapleton, H. M. In Vitro Metabolism of the Brominated Flame Retardants 2-Ethylhexyl-2, 3, 4, 5-Tetrabromobenzoate (TBB) and Bis(2-ethylhexyl) 2, 3, 4, 5-Tetrabromophthalate (TBPH) in Human and Rat Tissues. Chem. Res. Toxicol. doi:10. 1021/tx300086x (2012).
57. Bearr, J. S., Mitchelmore, C. L., Roberts, S. C. & Stapleton, H. M. Species specific differences in the in vitro metabolism of the flame retardant mixture, Firemaster BZ-54. Aquat Toxicol 124-125, 41-47, doi:10. 1016/j. aquatox. 2012. 06. 006 (2012).
58. Belcher, S. M., Cookman, C. J., Patisaul, H. B. & Stapleton, H. M. In vitro assessment of human nuclear hormone receptor activity and cytotoxicity of the flame retardant mixture FM 550 and its triarylphosphate and brominated components. Toxicol. Lett. doi:10. 1016/j. toxlet. 2014. 04. 017 (2014).
59. Tung, E. W. Y., Ahmed, S., Peshdary, V. & Atlas, E. Firemaster 550 and its components isopropylated triphenyl phosphate and triphenyl phosphate enhance adipogenesis and transcriptional activity of peroxisome proliferator activated receptor (Ppargamma) on the adipocyte protein 2 (aP2) promoter. PLoS One 12, e0175855, doi:10. 1371/journal. pone. 0175855 (2017).
60. Cano-Sancho, G., Smith, A. & La Merrill, M. A. Triphenyl phosphate enhances adipogenic differentiation, glucose uptake and lipolysis via endocrine and noradrenergic mechanisms. Toxicol In Vitro 40, 280-288, doi:10. 1016/j. tiv. 2017. 01. 021 (2017).
61. Pillai, H. K. et al. Ligand binding and activation of PPARgamma by Firemaster 550: effects on adipogenesis and osteogenesis in vitro. Environ. Health Perspect. 122, 1225-1232, doi:10. 1289/ehp. 1408111 (2014).
62. Peng, H. et al. Hydroxylated 2-Ethylhexyl tetrabromobenzoate isomers in house dust and their agonistic potencies with several nuclear receptors. Environ Pollut 227, 578-586, doi:10. 1016/j. envpol. 2017. 04. 094 (2017).
63. Esteban-Vasallo, M. D., Aragones, N., Pollan, M., Lopez-Abente, G. & Perez-Gomez, B. Mercury, cadmium, and lead levels in human placenta: a systematic review. Environ Health Perspect 120, 1369-1377, doi:10. 1289/ehp. 1204952 (2012).
64. Leonetti, C., Butt, C. M., Hoffman, K., Miranda, M. L. & Stapleton, H. M. Concentrations of polybrominated diphenyl ethers (PBDEs) and 2, 4, 6-tribromophenol in human placental tissues. Environ Int 88, 23-29, doi:10. 1016/j. envint. 2015. 12. 002 (2016).
65. Leonetti, C. et al. Brominated flame retardants in placental tissues: associations with infant sex and thyroid hormone endpoints. Environ Health 15, 113, doi:10. 1186/s12940-016-0199-8 (2016).
66. Beatty, W. W. Gonadal hormones and sex differences in nonreproductive behaviors in rodents: organizational and activational influences. Horm Behav 12, 112-163 (1979).
67. Masur, J., Schutz, M. T. & Boerngen, R. Gender differences in open-field behavior as a function of age. Dev Psychobiol 13, 107-110, doi:10. 1002/dev. 420130202 (1980).
68. Slob, A. K., Huizer, T. & Van der Werff ten Bosch, J. J. Ontogeny of sex differences in open-field ambulation in the rat. Physiol Behav 37, 313-315 (1986).
69. Simpson, J., Ryan, C., Curley, A., Mulcaire, J. & Kelly, J. P. Sex differences in baseline and drug-induced behavioural responses in classical behavioural tests. Prog. Neuropsychopharmacol. Bol. Psychiatry 37, 227-236, doi:10. 1016/j. pnpbp. 2012. 02. 004 (2012).
70. Weiss, S. M., Wadsworth, G., Fletcher, A. & Dourish, C. T. Utility of ethological analysis to overcome locomotor confounds in elevated maze models of anxiety. Neurosci. Biobehav. Rev. 23, 265-271 (1998).