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Metabolomics of brain and reproductive organs: characterizing the impact of gestational exposure to butylbenzyl phthalate on dams and resultant offspring

Metabolomics volume 8, pages 1012–1025 (2012)Cite this article

Abstract

Phthalates are plasticizers finding wide spread use in industrial and household products, with measureable levels of phthalate-derived metabolites in the general US population. Phthalates have endocrine disruption potential and have been implicated as obesogens. Our exploratory investigation to reveal the impact of in utero exposure to a phthalate on the biochemical profiles of the brain, testes, and uterus of prepubertal offspring, and of tissues from dams administered butylbenzyl phthalate (BBP). Pregnant rats (three per group) were administered (on gestation day 14–21) corn oil (control), or 25 mg/kg/day or 750 mg/kg/day BBP in corn oil. Tissues were collected from each of the dams on postnatal day (pnd) 21 (~3 weeks after the end of BBP administration), and from each of the pups on pnd 26 (~4 weeks after birth to dams administered vehicle or BBP during gestation) and processed for metabolomics analysis. Multivariate data analyses revealed metabolites that best distinguished the exposed and control groups. The metabolites most important to distinguishing the study groups were tested for significance using the exact Wilcoxon rank-sum test. Male pups had significant differences (control versus BBP dose groups) in levels of metabolites for both the brain and testes even at the P < 0.01 level. However, female pups and dams had significant testing for the uterus only at the P = 0.1 level tested. Female pups also had some significant differences for the brain with P values between 0.5 and 0.1. Amino acid metabolism (male and female pups) and phospholipid metabolism (male pups) were perturbed for the brain. Amino acid metabolism, purine metabolism, and TCA cycle were perturbed for tests and uterus. This study demonstrated the use of metabolomics to reveal metabolic perturbations in tissues of offspring following in utero exposures, and suggests the use of this approach for determining the impact of exposure past the time of the presence of the parent compound and metabolites derived from the parent compound.

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References

  • Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science, 308(5727), 1391–1392.

    Article  Google Scholar 

  • Beckonert, O., Keun, H. C., Ebbels, T. M. D., Bundy, J., Holmes, E., Lindon, J. C., et al. (2007). Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nature Protocols, 2(11), 2692–2703.

    Article  PubMed  CAS  Google Scholar 

  • Bergh, A., Damber, J. E., & Hjertkvist, M. (1996). Human chorionic gonadotrophin-induced testicular inflammation may be related to increased sensitivity to interleukin-1. International Journal of Andrology, 19(4), 229–236.

    Article  PubMed  CAS  Google Scholar 

  • Blount, B. C., Silva, M. J., & Caudill, S. P. (2000). Levels of seven urinary phthalate metabolites in a human reference population. Environmental Health Perspectives, 108(10), 972–982.

    Article  Google Scholar 

  • Crocker, J. F., Safe, S. H., & Acott, P. (1988). Effects of chronic phthalate exposure on the kidney. Journal of Toxicology and Environmental Health, 23(4), 433–444.

    Article  PubMed  CAS  Google Scholar 

  • Ding, Y., Gao, Y., Shi, R., Zhou, Y. J., & Tian, Y. (2010). Effects of in utero exposure to di(2-ethylhexyl) phthalate on sexual development in female offspring. Chinese Journal of Preventive Medicine, 44(2), 150–153.

    PubMed  Google Scholar 

  • Draper, R. P., & Timbrell, J. A. (1996). Urinary creatine as a potential marker of testicular damage: Effect of vasectomy. Reproductive Toxicology, 10(1), 79–85.

    Article  PubMed  CAS  Google Scholar 

  • Dym, M., & Fawcett, D. W. (1970). The blood-testes barrier in the rat and the physiological compartmentalization of the seminiferous epithelium. Biology of Reproduction, 3, 308–326.

    PubMed  CAS  Google Scholar 

  • Ebesunun, M. O., Solademi, B. A., Shittu, O. B., Anetor, J. I., Onuegbu, J. A., Olisekodiaka, J. M., et al. (2004). Plasma and semen ascorbic levels in spermatogenesis. West African Journal of Medicine, 23(4), 290–293.

    PubMed  CAS  Google Scholar 

  • Eriksson, L., Johansson, E., Kettaneh-Wold, N., Trygg, J., Wikström, C., & Wold, S. (2006). Multivariate and megavariate data analysis. Part I & Part II (2nd ed.). UmeÃ¥, Sweden: Umetrics Academy.

    Google Scholar 

  • Fabian, R. H., & Hulsebosch, C. E. (1989). Time course of penetration of xenogeneic IgG into the central nervous system of the neonatal rat: An immunohistochemical and radionuclide tracer study. Journal of Neuroimmunology, 24, 183–189.

    Article  PubMed  CAS  Google Scholar 

  • Fan, L. Q., Cattley, R. C., & Corton, J. C. (1998). Tissue-specific induction of 17 beta-hydroxysteroid dehydrogenase type IV by peroxisome proliferator chemicals is dependent on the peroxisome proliferator-activated receptor alpha. Journal of Endocrinology, 158, 237–246.

    Article  PubMed  CAS  Google Scholar 

  • Fukuoka, M., Tanimoto, T., Zhou, Y., Kawasaki, N., Tanaka, A., Ikemoto, I., et al. (1989). Mechanism of testicular atrophy induced by di-n-butyl phthalate in rats. Part 1. Journal of Applied Toxicology, 9(4), 277–283.

    Article  PubMed  CAS  Google Scholar 

  • Fukuoka, M., Zhou, Y., Tanaka, A., Ikemoto, I., & Michida, T. (1990). Mechanism of testicular atrophy induced by di-n-butyl phthalate in rats. Part 2. The effects on some testicular enzymes. Journal of Applied Toxicology, 10(4), 285–293.

    Article  PubMed  CAS  Google Scholar 

  • Govindaraju, V., Young, K., & Maudsley, A. A. (2000). Proton NMR chemical shifts and coupling constants for brain metabolites. NMR in Biomedicine, 13, 129–153.

    Article  PubMed  CAS  Google Scholar 

  • Grande, S. W., Andrade, A. J. M., Talsness, K. G., & Chahoud, I. (2006). A dose-response study following in utero and lactational exposure to di(2-ethylhexyl)phthalate: Effects of female rat reproductive development. Toxicological Sciences, 91(1), 247–254.

    Article  PubMed  CAS  Google Scholar 

  • Gray, L. E., Jr, Ostby, J., Furr, J., Price, M., Veeramachaneni, D. N., & Parks, L. (2000). Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicological Sciences, 58(2), 350–365.

    Article  PubMed  CAS  Google Scholar 

  • Griesmaier, E., & Keller, M. (2012). Glutamate receptors—prenatal insults, long-term consequences. Pharmacology, Biochemistry and Behavior, 100, 835–840.

    Article  CAS  Google Scholar 

  • Griffin, J. L., Troke, J., Walker, L. A., Shore, R. F., Lindon, J. C., & Nicholson, J. K. (2000). The biochemical profile of rat testicular tissue as measured by magic angle spinning 1H NMR spectroscopy. FEBS Letters, 486(3), 225–229.

    Article  PubMed  CAS  Google Scholar 

  • Guerra, M. T., Scarano, W. R., de Toledo, F. C., Franci, J. A., & Kempinas, W.de. G. (2010). Reproductive development and function of female rats exposed to di-eta-butyl-phthalate (DBP) in utero and during lactation. Reproductive Toxicology, 29(1), 99–105.

    Article  PubMed  CAS  Google Scholar 

  • Howdeshell, K. L., Rider, C. V., Wilson, V. S., & Gray, L. E., Jr. (2008a). Mechanisms of action of phthalate esters, individually and in combination, to induce abnormal reproductive development in male laboratory rats. Environmental Research, 108(2), 168–176.

    Article  PubMed  CAS  Google Scholar 

  • Howdeshell, K. L., Wilson, V. S., Furr, J., Lambright, C. R., Rider, C. V., Blystone, C. R., et al. (2008b). A mixture of five phthalate esters inhibits fetal testicular testosterone production in the sprague-dawley rat in a cumulative, dose-additive manner. Toxicological Sciences, 105(1), 153–165.

    Article  PubMed  CAS  Google Scholar 

  • Jouannet, P., Wang, C., Eustache, F., Kold-Jensen, T., & Auger, J. (2001). Semen quality and male reproductive health: The controversy about human sperm concentration decline. APMIS (Acta Pathologica, Microbiologica, et Immunologica Scandinavica), 109(5), 333–344.

    Article  CAS  Google Scholar 

  • Kalantaridou, S., Makrigiannakis, A., Zoumakis, E., & Chrousos, G. P. (2007). Peripheral corticotropin-releasing hormone is produced in the immune and reproductive systems: Actions, potential roles and clinical implications. Frontiers in Bioscience, 12, 572–580.

    Article  PubMed  CAS  Google Scholar 

  • Kato, R., Maeda, T., Akaike, T., & Tamai, I. (2005). Nucleoside transport at the blood-testis barrier studied with primary-cultured sertoli cells. Journal of Pharmacology and Experimental Therapeutics, 312(2), 601–608.

    Article  PubMed  CAS  Google Scholar 

  • Kato, R., Maeda, T., Akaike, T., & Tamai, I. (2006). Characterization of novel Na+-dependent nucleobase transport systems at the blood-testis barrier. American Journal of Physiology, Endocrinology, and Metabolism, 290, E968–E975.

    Article  CAS  Google Scholar 

  • Kavlock, R., Boekelheide, K., Chapin, R., Cunningham, M., Faustman, E., Foster, P., et al. (2002). NTP Center for the Evaluation of Risks to Human Reproduction: Phthalates expert panel report on the reproductive and developmental toxicity of butyl benzyl phthalate. Reproductive Toxicology, 16(5), 453–487.

    Article  PubMed  CAS  Google Scholar 

  • Kunz, N., Camm, E. J., Somm, E., Lodygensky, G., Darbre, S., Aubert, M. L., et al. (2011). Developmental and metabolic brain alterations in rats exposed to bisphenol A during gestation and lactation. International Journal of Developmental Neuroscience, 29(1), 37–43.

    Article  PubMed  CAS  Google Scholar 

  • Kuramori, C., Hase, Y., Hoshikawa, K., Watanabe, K., Nishi, T., Hishiki, T., et al. (2009). Mono-(2-ethylhexyl) phthalate targets glycogen debranching enzyme and affects glycogen metabolism in rat testis. Toxicological Sciences, 109(1), 143–151.

    Article  PubMed  CAS  Google Scholar 

  • Kwack, S. J., Kim, K. B., Kim, H. S., & Lee, B. M. (2009). Comparative toxicological evaluation of phthalate diesters and metabolites in Sprague-Dawley male rats for risk assessment. Journal of Toxicology and Environmental Health, 72(21–22), 1446–1454.

    PubMed  CAS  Google Scholar 

  • Lehninger, A. L., Nelson, D. L., & Cox, A. M. (1997). Principles of biochemistry. New York, USA: Worth Publishers Inc.

    Google Scholar 

  • Lindgren, A., Lindquist, N. G., Lyden, A., Olsson, T., & Ullberg, S. (1982). A whole body autoradiographic study on the distribution of 14C-labelled di(2-ethyl hexyl) phthalate in mice. Toxicology, 23, 149–158.

    Article  PubMed  CAS  Google Scholar 

  • Liu, P., Lin, C., Pan, C., Kao, L., & Tseng, F. (2003). Butyl benzyl phthalate blocks Ca2+ signalling and catecholamine secretion couples with nicotinic acetylcholine receptors in bovine adrenal chromaffin cells. Neurotoxicology, 24(1), 97–105.

    Article  PubMed  CAS  Google Scholar 

  • Lovekamp, T. N., & Davis, B. J. (2001). Mono-(2-ethylhexyl) phthalate suppresses aromatase transcript levels and estradiol production in cultured rat granulosa cells. Toxicology and Applied Pharmacology, 172(3), 217–224.

    Article  PubMed  CAS  Google Scholar 

  • MacLusky, N. J., & Naftolin, F. (1981). Sexual differentiation of the central nervous system. Science, 211(4488), 1294–1302.

    Article  PubMed  CAS  Google Scholar 

  • Maness, S. C., McDonnell, D. P., & Gaido, K. W. (1998). Inhibition of androgen receptor-dependent transcriptional activity by DDT isomers and methoxychlor in HepG2 human hepatoma cells. Toxicology and Applied Pharmacology, 151(1), 135–142.

    Article  PubMed  CAS  Google Scholar 

  • Mazzei, P., Piccolo, A., Loredana, N., Mascolo, M., De Rosa, G., & Staibano, S. (2010). Metabolomic profile of intact tissue from uterine leiomyomas using high-resolution magic-angle-spinning 1H-NMR spectroscopy. NMR in Biomedicine, 23, 1–10.

    Article  Google Scholar 

  • Moore, N. P., Creasy, D. M., Gray, T. J., & Timbrell, J. A. (1992). Urinary creatine profiles after administration of cell-specific testicular toxicants to the rat. Archives of Toxicology, 66(6), 435–442.

    Article  PubMed  CAS  Google Scholar 

  • Moore, N. P., Gray, T. J., & Timbrell, J. A. (1998). Creatine metabolism in the seminiferous epithelium of rats. II. Effect of modulators of cellular biochemical function on creatine secretion by cultured Sertoli cells. Journal of Reproduction and Fertility, 112(2), 331–336.

    Article  PubMed  CAS  Google Scholar 

  • Moore, R. W., Rudy, T. A., Lin, T. M., Ko, K., & Peterson, R. E. (2001). Abnormalities of sexual development in male rats with in utero and lactational exposure to the antiandrogenic plasticizer di(2-ethylhexyl) phthalate. Environmental Health Perspectives, 109(3), 229–237.

    Article  PubMed  CAS  Google Scholar 

  • Murature, D. A., Tang, S. Y., Steinhardt, G., & Dougherty, R. C. (1987). Phthalate esters and semen quality parameters. Biological Mass Spectrometry, 14(8), 473–477.

    Article  CAS  Google Scholar 

  • Mylchreest, E., Cattley, R. C., & Foster, P. M. D. (1998). Male reproductive tract malformations in rats following gestational and lactational exposure to di(η-butyl) phthalate: An antiandrogenic mechanism? Toxicological Sciences, 43(1), 47–60.

    PubMed  CAS  Google Scholar 

  • Mylchreest, E., Sar, M., Wallace, D. G., & Foster, P. M. (2002). Fetal testosterone insufficiency and abnormal proliferation of Leydig cells and gonocytes in rats exposed to di(n-butyl) phthalate. Reproductive Toxicology, 16(1), 19–28.

    Article  PubMed  CAS  Google Scholar 

  • Naftolin, F., Ryan, K. J., Davies, I. J., Petro, Z., & Kuhn, M. (1975). The formation and metabolism of estrogens in brain tissues. Advances in Biosciences, 15, 105–121.

    CAS  Google Scholar 

  • Nagao, T., Ohta, R., Marumo, H., Shindo, T., Yoshimura, S., & Ohno, H. (2000). Effect of butylbenzyl phthalate after gavage administration: A two-generation reproductive study. Reproductive Toxicology, 14(6), 513–532.

    Article  PubMed  CAS  Google Scholar 

  • Nahas, K., le Net, J. L., Provost, J. P., & Tomaszewski, K. E. (1993). An investigation of urinary creatine excretion as a potential marker for testicular damage. Human and Experimental Toxicology, 12(2), 173–176.

    Article  PubMed  CAS  Google Scholar 

  • Nicholson, J. K., Higham, D. P., Timbrell, J. A., & Sadler, P. J. (1989). Quantitative high resolution 1H NMR urinalysis studies on the biochemical effects of cadmium in the rat. Molecular Pharmacology, 36(3), 398–404.

    PubMed  CAS  Google Scholar 

  • Parkhie, M. R., Webb, M., & Norcross, M. A. (1982). Dimethoxyethyl phthalate: Embryopathy, teratogenicity, foetal metabolism and the role of the zinc in the rat. Environmental Health Perspectives, 45, 85–97.

    Article  Google Scholar 

  • Parks, L. G., Ostby, J. S., Lambright, C. R., Abbott, B. D., Klinefelter, G. R., Barlow, N. J., et al. (2000). The plasticizer diethylhexyl phthalate induces malformations by decreasing fetal testosterone synthesis during sexual differentiation in the male rat. Toxicological Sciences, 58(2), 339–349.

    Article  PubMed  CAS  Google Scholar 

  • Pathmasiri, W., Snyder, R. W., Burgess, J. P., Popp, J. A., Fennell, T. R., & Sumner, S. C. J. (2011). Metabolomics of urine and liver for the assessment of acetaminophen induced liver injury. In D. A. Casciano & S. C. Sahu (Eds.), Handbook of Systems Toxicology (pp. 299–324). Sussex, UK: Wiley.

    Google Scholar 

  • Pharikal, K., Das, P. C., Dey, C. D., & Dasgupta, S. (1988). Tissue ascorbate as a metabolic marker in cadmium toxicity. International Journal for Vitamin and Nutrition Research, 58(3), 306–311.

    PubMed  CAS  Google Scholar 

  • Ravenzwaay, B., Cunha, G. C., Strauss, B., Wiemer, J., Leibold, E., Kamp, H., et al. (2010). The individual and combined metabolite profiles (metabolomics) of dibutylphthalate and di(2-ethylhexyl)phthalate following a 28-day dietary exposure in rats. Toxicology Letters, 198(2), 159–170.

    Article  PubMed  Google Scholar 

  • Rawcliffe, L., Creasy, D., & Timbrell, J. A. (1989). Urinary creatine as a possible marker for testicular damage: Studies with the testicular toxic compound 2-methoxyethanol. Reproductive Toxicology, 3(4), 269–274.

    Article  PubMed  CAS  Google Scholar 

  • Rosner, B. (2000). Fundamentals of biostatistics (5th ed., pp. 343–347). Pacific Grove, CA: Duxbury.

    Google Scholar 

  • Saillenfait, A. M., Payan, J. P., Fabry, J. P., Beydon, D., Langonne, I., Gallissot, F., et al. (1998). Assessment of the developmental toxicity, metabolism, and placental transfer of di-n-butyl phthalate administered to pregnant rats. Toxicological Sciences, 45(2), 212–224.

    PubMed  CAS  Google Scholar 

  • Shultz, V. D., Phillips, S., Sar, M., Foster, P. M., & Gaido, K. W. (2001). Altered gene profiles in fetal rat testes after in utero exposure to di(n-butyl) phthalate. Toxicological Sciences, 64(2), 233–242.

    Article  PubMed  CAS  Google Scholar 

  • Singh, A. R., Lawrence, W. H., & Autian, J. (1975). Maternal-fetal transfer of 14C-di-2-ethylhexyl phthalate and 14C-diethyl phthalate in rats. Journal of Pharmaceutical Sciences, 64(8), 1347–1350.

    Article  PubMed  CAS  Google Scholar 

  • Slupsky, C. M., Rankin, K. N., Wagner, J., Fu, H., Chang, D., Weljie, A. M., et al. (2007). Investigations of the effects of gender, diurnal variation, and age in human urinary metabolomic profiles. Analytical Chemistry, 79(18), 6995–7004.

    Article  PubMed  CAS  Google Scholar 

  • Sumner, S., Burgess, J., Snyder, R., & Fennell, T. (2010a). Metabolomics of urine for the assessment of microvesicular lipid accumulation in the liver following isoniazid exposure. Metabolomics, 6(2), 238–249.

    Article  PubMed  CAS  Google Scholar 

  • Sumner, S., Snyder, R., Fennell, T., Taylor, G., & Lewin, A. (2010b). Distribution of [14C] C60 in the pregnant and lactating rat and the effect on endogenous metabolism. Journal of Applied Toxicology, 30(4), 354–360.

    PubMed  CAS  Google Scholar 

  • Sumner, S., Snyder, R., Burgess, J., Tyl, R., & Fennell, T. (2010c). Omics in the study of reproduction and development. In R. Kapp & R. Tyl (Eds.), Reproductive toxicology (3rd ed., Chap. 22). London, UK: Informa Healthcare.

  • Sumner, S., Synder, R., Burgess, J., Myers, C., Tyl, R., Sloan, C., et al. (2009). Metabolomics in the assessment of chemical-induced reproductive and development outcomes using non-invasive biological fluids: Application to the study of butylbenzyl phthalate. Journal of Applied Toxicology, 29(8), 703–714.

    Article  PubMed  CAS  Google Scholar 

  • Swan, S. H., Main, K. M., Liu, F., Stewart, S. L., Kruse, R. L., Calafat, A. M., et al. (2005). Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environment Health Perspectives, 2005(113), 1056–1061.

    Article  Google Scholar 

  • Tabacova, S., et al. (1999). Maternal exposure to phthalates and complications of pregnancy. Epidemiology, 10(Suppl), S127.

    Google Scholar 

  • Timbrell, J. A. (2000). Urinary creatine as a biochemical marker of chemical induced testicular damage. Archives of Industrial Hygiene and Toxicology, 51(3), 295–303.

    PubMed  CAS  Google Scholar 

  • Trygg, J., Holmes, E., & Lundstedt, T. (2007). Chemometrics in metabonomics. Journal of Proteome Research, 6, 469–479.

    Article  PubMed  CAS  Google Scholar 

  • Tyl, R. W., Myers, C. B., Marr, M. C., Fail, P. A., Seely, J. C., Brine, D. R., et al. (2004). Reproductive toxicity evaluation of dietary butyl benzyl phthalate (BBP) in rats. Reproductive Toxicology, 18(2), 241–264.

    Article  PubMed  CAS  Google Scholar 

  • Vitale, R., Fawcett, D. W., & Dym, M. (1973). The normal development of blood-testis barrier and the effects of clomiphene and estrogen treatment. Anatomical Record, 176(3), 331–344.

    Article  PubMed  CAS  Google Scholar 

  • Weljie, A. M., Newton, J., Mercier, P. M., Carlson, E., & Slupsky, C. M. (2006). Targeted profiling: Quantitative analysis of 1H-NMR metabolomics data. Analytical Chemistry, 78(13), 4430–4442.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, V. S., Howdeshell, K. L., Lambright, C. S., Furr, J., Gray, E., & Jr, L. (2007). Differential expression of the phthalate syndrome in male Sprague-Dawley and Wistar rats after in utero DEHP exposure. Toxicology Letters, 170(3), 177–184.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, V. S., Lambright, C., Furr, J., Ostby, J., Wood, C., Held, G., et al. (2004). Phthalate ester-induced gubernacular ligament lesions are associated with reduced Insl3 gene expression in the fetal rat testis during sexual differentiation. Toxicology Letters, 146, 207–215.

    Article  PubMed  CAS  Google Scholar 

  • Xu, Y., Agrawal, S., Cook, T. J., & Knipp, G. T. (2007). Di-(2-ethylhexyl)-phthalate affects lipid profiling in fetal rat brain upon maternal exposure. Archives of Toxicology, 81, 57–62.

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto, T., Horii, I., & Yoshida, T. J. (2007). Integrated NMR-based metabonomic investigation of early metabolic effects of ethylene glycol monomethyl ether (EGME) on male reproductive organs in rats. Toxicological Sciences, 32(5), 515–528.

    Article  CAS  Google Scholar 

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Acknowledgments

Dr. Rochelle Tyl is appreciated for review and comment on this manuscript. The North Carolina Biotechnology Center is acknowledged for supporting laboratory supplies and an internship stipend for Mr. Ranjan Banerjee. Dr. Kevin Knagge of DHMRI is acknowledged for technical support. NIGMS Grant 5R21GM75903 provided funding for development of methods used in this investigation. The authors appreciate the review and suggestions by the journal referee, which has strengthened this manuscript.

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  1. Discovery and Analytical Sciences, RTI International, Research Triangle Park, NC, 27709, USA

    Ranjan Banerjee, Wimal Pathmasiri, Rodney Snyder & Susan Sumner

  2. Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC, 27599, USA

    Ranjan Banerjee

  3. Department of Physics, University of North Carolina at Chapel Hill, Chapel Hill, NC, 27599, USA

    Ranjan Banerjee

  4. Statistics and Epidemiology, RTI International, Research Triangle Park, NC, 27709, USA

    Susan McRitchie

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  1. Ranjan Banerjee
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Banerjee, R., Pathmasiri, W., Snyder, R. et al. Metabolomics of brain and reproductive organs: characterizing the impact of gestational exposure to butylbenzyl phthalate on dams and resultant offspring. Metabolomics 8, 1012–1025 (2012). https://doi.org/10.1007/s11306-011-0396-y

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