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Project Publications: Duke University: Developmental Effects of Superfund Hydrocarbon Mixtures in Fundulus heteroclitus

Superfund Research Program

Developmental Effects of Superfund Hydrocarbon Mixtures in Fundulus heteroclitus

Project Leader: Richard T. Di Giulio
Co-Investigators: David E. Hinton, Marjorie F. Oleksiak (University of Miami)
Grant Number: P42ES010356
Funding Period: 2000-2011

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  • Jung D, Cho Y, Collins LB, Swenberg JA, Di Giulio RT. 2009. Effects of benzo[a]pyrene on mitochondrial and nuclear DNA damage in Atlantic killifish (Fundulus heteroclitus) from a creosote-contaminated and reference site. Aquat Toxicol 95(1):44-51. doi:10.1016/j.aquatox.2009.08.003 PMID:19726093 PMCID:PMC2776085


  • Billiard SM, Meyer JN, Wassenberg DM, Hodson PV, Di Giulio RT. 2008. Nonadditive effects of PAHs on early vertebrate development: mechanisms and implications for risk assessment. Toxicol Sci 105(1):5-23. doi:10.1093/toxsci/kfm303 PMID:18156145 PMCID:PMC2734299
  • Carney MW, Erwin K, Hardman R, Yuen B, Volz DC, Hinton DE, Kullman SW. 2008. Differential developmental toxicity of naphthoic acid isomers in medaka (Oryzias latipes) embryos. Mar Pollut Bull 57(6-12):255-266. doi:10.1016/j.marpolbul.2008.02.036 PMID:18433798 PMCID:PMC4299470
  • Matson CW, Clark BW, Jenny MJ, Fleming CR, Hahn ME, Di Giulio RT. 2008. Development of the morpholino gene knockdown technique in Fundulus heteroclitus: a tool for studying molecular mechanisms in an established environmental model. Aquat Toxicol 87(4):289-295. doi:10.1016/j.aquatox.2008.02.010 PMID:18378331 PMCID:PMC2413436
  • Roegge CS, Timofeeva OA, Seidler FJ, Slotkin TA, Levin ED. 2008. Developmental diazinon neurotoxicity in rats: later effects on emotional response. Brain Res Bull 75:168-172. PMID:18158111
  • Timme-Laragy AR, Noyes PD, Buhler DR, Di Giulio RT. 2008. CYP1B1 knockdown does not alter synergistic developmental toxicity of polycyclic aromatic hydrocarbons in zebrafish (Danio rerio). Mar Environ Res 66(1):85-87. doi:10.1016/j.marenvres.2008.02.030 PMID:18378296 PMCID:PMC2516962


  • Di Giulio RT, Hinton DE, eds. 2007. The Toxicology of Fishes. Taylor & Francis, Boca Raton, FL.
  • Hinton DE, Segner H, Au D, Kullman SW, Hardman R. 2007. Liver toxicity. In: The Toxicology of Fishes. Taylor & Francis, Boca Raton, FL.
  • Ostrander GK, Di Giulio RT, Hinton DE, Miller MR, Rotchell JR. 2007. Chemical Carcinogensis. In: The Toxicology of Fishes. Taylor & Francis, Boca Raton, FL.
  • Timme-Laragy AR, Cockman C, Matson CW, Di Giulio RT. 2007. Synergistic induction of AHR regulated genes in developmental toxicity from co-exposure to two model PAHs in zebrafish. Aquat Toxicol 85(4):241-50. PMID:17964672


  • Arzuaga X, Wassenberg DM, Di Giulio RT, Elskus AA. 2006. The chlorinated AHR ligand 3,32,4,42,5-pentachlorobiphenyl (PCB126) promotes reactive oxygen species (ROS) production during embryonic development in the killifish (Fundulus heteroclitus). Aquat Toxicol 76(1):13-23.
  • Billiard SM, Timme-Laragy AR, Wassenberg DM, Cockman C, Di Giulio RT. 2006. The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol Sci 92:526-536. PMID:16687390
  • Embry MR, Billiard SM, Di Giulio RT. 2006. Lack of p53 induction in fish cells by model chemotherapeutics. Oncogene 25(14):2004-2010. doi:10.1038/sj.onc.1209238 PMID:16434976


  • Meyer JN, Volz DC, Freedman JH, Di Giulio RT. 2005. Differential display of hepatic mRNA from killifish (Fundulus heteroclitus) inhabiting a Superfund estuary. Aquat Toxicol 73(4):327-341. PMID:15916819
  • Nacci DE, Coiro L, Wassenberg DM, Di Giulio RT. 2005. A non-destructive technique to measure cytochrome P4501A enzyme activity in living embryos of the estuarine fish Fundulus heteroclitus. Chapter Vol. 2 in: Techniques in Aquatic Toxicology. CRC Press, Inc., Boca Raton, FL. pp.209-226.
  • Song MO, Freedman JH. 2005. Activation of mitogen activated protein kinases by PCB126 (3,3',4,4',5-pentachlorobiphenyl) in HepG2 cells. Toxicol Sci 84(2):308-318. doi:10.1093/toxsci/kfi084 PMID:15647597
  • Timme-Laragy AR, Meyer JN, Waterland RA, Di Giulio RT. 2005. Analysis of CpG methylation in the killifish CYP1A promoter. Comp Biochem Physiol C Toxicol Pharmacol 141(4):406-411. PMID:16257583
  • Wassenberg DM, Nerlinger AL, Battle LP, Di Giulio RT. 2005. Effects of the polycyclic aromatic hydrocarbon heterocycles, carbazole and dibenzothiophene, on in vivo and in vitro CYP1A activity and polycyclic aromatic hydrocarbon-derived embryonic deformities. Environ Toxicol Chem 24(10):2526-2532. PMID:16268154


  • Bacanskas LR, Whitaker J, Di Giulio RT. 2004. Oxidative stress in two populations of killifish (Fundulus heteroclitus) with differing contaminant exposure histories. Mar Environ Res 58(2-5):597-601. doi:10.1016/j.marenvres.2004.03.048 PMID:15178085
  • Craft ES, Embry MR, Di Giulio RT, Freedman JH. 2004. Evidence for the role of p53 in metal-induced activation of metallothionein gene expression. In: Metal Ions in Biology and Medicine: Proceedings of the Eighth International Symposium on Metal Ions in Biology and Medicine. John Libbey Eurotext Publishers, Montrouge, France.
  • Embry MR, Whitaker J, Freedman JH, Di Giulio RT. 2004. Differential susceptibility of fish and rat liver cells to oxidative stress and cytotoxicity upon exposure to prooxidants. Comp Biochem Physiol C Toxicol Pharmacol 137(4):335-342. PMID:15228951
  • Mattie MD, Freedman JH. 2004. Copper-inducible transcription: regulation by metal- and oxidative stress-responsive pathways. Am J Physiol Cell Physiol 286(2):C293-C301. doi:10.1152/ajpcell.00293.2003 PMID:14576086
  • Wassenberg DM, Di Giulio RT. 2004. Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ Health Perspect 112(17):1658-1664. PMID:15579409
  • Wassenberg DM, Di Giulio RT. 2004. Teratogenesis in Fundulus heteroclitus embryos exposed to a creosote-contaminated sediment extract and CYP1A inhibitors. Mar Environ Res 58(2-5):163-168. PMID:15178029


  • Meyer JN, Di Giulio RT. 2003. Heritable adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecol Appl 13(2):490-503.
  • Meyer JN, Smith JD, Winston GW, Di Giulio RT. 2003. Antioxidant defenses in killifish (Fundulus heteroclitus) exposed to contaminated sediments and model prooxidants: short-term and heritable responses. Aquat Toxicol 65(4):377-395. doi:10.1016/j.aquatox.2003.06.001 PMID:14568353
  • Meyer JN, Wassenberg DM, Karchner SI, Hahn ME, Di Giulio RT. 2003. Expression and inducibility of aryl hydrocarbon receptor pathway genes in wild-caught killifish (Fundulus heteroclitus) with different contaminant-exposure histories. Environ Toxicol Chem 22(10):2337-2343. PMID:14551997


  • Meyer JN, Di Giulio RT. 2002. Patterns of heritability of decreased EROD activity and resistance to PCB 126-induced teratogenesis in laboratory-reared offspring of killifish (Fundulus heteroclitus) from a creosote-contaminated site in the Elizabeth River, VA, USA. Mar Environ Res 54(3-5):621-626. PMID:12408627
  • Meyer JN, Nacci DE, Di Giulio RT. 2002. Cytochrome P4501A (CYP1A) in killifish (Fundulus heteroclitus): heritability of altered expression and relationship to survival in contaminated sediments. Toxicol Sci 68(1):69-81. PMID:12075112
  • Wassenberg DM, Swails EE, Di Giulio RT. 2002. Effects of combined exposures to benzo[a]pyrene and 3,3',4,4',5-pentachlorobiphenyl on Fundulus heteroclitus. Mar Environ Res 54(3-5):279-283.


  • Mattie MD, Freedman JH. 2001. Protective effects of aspirin and Vitamin E (a-tocopherol) against copper- and cadmium-induced toxicity. Biochem Biophys Res Commun 285(4):921-925. PMID:11467839
  • Willett KL, Lienesch L, Reichert W, Di Giulio RT. 2001. In vivo and in vitro inhibition of CYP1A-dependent activity in Fundulus heteroclitus by the polynuclear aromatic hydrocarbon (PAH) fluoranthene. Toxicol Appl Pharmacol 177(3):264-271. PMID:11749126


  • Cioci LK, Qui L, Freedman JH. 2000. Transgenic strains of the nematode caenorhabditis elegans as biomonitors metal contamination. Environ Toxicol Chem 19(8):2122-2129.
  • Tcherepanova I, Bhattacharyya L, Rubin CS, Freedman JH. 2000. Aspartic proteases from the nematode Caenorhabditis elegans. Structural organization and developmental and cell-specific expression of asp-1. J Biol Chem 275(34):26359-26369. doi:10.1074/jbc.M000956200 PMID:10854422
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