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Project Publications: University of North Carolina-Chapel Hill: Chemistry and Analytical Core

Superfund Research Program

Chemistry and Analytical Core

Project Leader: Avram Gold
Co-Investigator: Wanda M. Bodnar
Grant Number: P42ES005948
Funding Period: 1995-2018
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  • Gao L, Mutlu E, Collins LB, Walker N, Hartwell HJ, Olson J, Sun W, Gold A, Ball LM, Swenberg JA. 2017. DNA product formation in female Sprague-Dawley rats following polyhalogenated aromatic hydrocarbon (PHAH) exposure. Chem Res Toxicol 30(3):794-803. doi:10.1021/acs.chemrestox.6b00368 PMID:28207250 PMCID:PMC5363288
  • Klaus V, Bastek H, Damme K, Collins LB, Frotschl R, Benda N, Lutter D, Ellinger-Ziegelbauer H, Swenberg JA, Dietrich DR, Stemmer K. 2017. Time-matched analysis of DNA adduct formation and early gene expression as predictive tool for renal carcinogenesis in methylazoxymethanol acetate treated Eker rats. Arch Toxicol 91(10):3427-3438. doi:10.1007/s00204-017-1953-6 PMID:28349193 PMCID:PMC5617782
  • Tian Z, Gold A, Nakamura J, Zhang Z, Vila J, Singleton D, Collins LB, Aitken MD. 2017. Nontarget Analysis Reveals a Bacterial Metabolite of Pyrene Implicated in the Genotoxicity of Contaminated Soil after Bioremediation. Environ Sci Technol 51(12):7091-7100. doi:10.1021/acs.est.7b01172 PMID:28510420 PMCID:PMC6309544
  • Venkatratnam A, Furuya S, Kosyk O, Gold A, Bodnar WM, Konganti K, Threadgill DW, Gillespie DA, Aylor DL, Wright FA, Chiu WA, Rusyn I. 2017. Editor's Highlight: Collaborative Cross mouse population enables refinements to characterization of the variability in toxicokinetics of trichloroethylene and provides genetic evidence for the role of PPAR pathway in its oxidative metabolism. Toxicol Sci 158(1):48-62. doi:10.1093/toxsci/kfx065 PMID:28369613


  • Lai Y, Yu R, Hartwell HJ, Moeller BC, Bodnar WM, Swenberg JA. 2016. Measurement of endogenous versus exogenous formaldehyde-induced DNA-protein crosslinks in animal tissues by stable isotope labeling and ultrasensitive mass spectrometry. Cancer Res 76(9):2652-2661. doi:10.1158/0008-5472.CAN-15-2527 PMID:26984759 PMCID:PMC4879886
  • McEachran AD, Shea D, Bodnar WM, Nichols EG. 2016. Pharmaceutical occurrence in groundwater and surface waters in forests land-applied with municipal wastewater. Environ Toxicol Chem 35(4):898-905. doi:10.1002/etc.3216 PMID:26297815 PMCID:PMC4976290
  • Sharma V, Collins LB, Chen T, Herr N, Takeda S, Sun W, Swenberg JA, Nakamura J. 2016. Oxidative stress at low levels can induce clustered DNA lesions leading to NHEJ mediated mutations. Oncotarget 7(18):25377-25390. doi:10.18632/oncotarget.8298 PMID:27015367 PMCID:PMC5041911


  • Laine JE, Ray PD, Bodnar WM, Cable PH, Boggess K, Offenbacher S, Fry RC. 2015. Placental cadmium levels are associated with increased preeclampsia risk. PLoS One 10(9):e0139341. doi:10.1371/journal.pone.0139341 PMID:26422011 PMCID:PMC4589375
  • Rodgers-Vieira EA, Zhang Z, Adrion AC, Gold A, Aitken MD. 2015. Identification of anthraquinone-degrading bacteria in soil contaminated with polycyclic aromatic hydrocarbons. Appl Environ Microbiol 81(11):3775-3781. doi:10.1128/AEM.00033-15 PMID:25819957 PMCID:PMC4421061
  • Yoo HS, Bradford BU, Kosyk O, Shymonyak S, Uehara T, Collins LB, Bodnar WM, Ball LM, Gold A, Rusyn I. 2015. Comparative analysis of the relationship between trichloroethylene metabolism and tissue-specific toxicity among inbred mouse strains: liver effects. J Toxicol Environ Health A 78(1):15-31. doi:10.1080/15287394.2015.958417 PMID:25424544 PMCID:PMC4281929
  • Yoo HS, Bradford BU, Kosyk O, Uehara T, Shymonyak S, Collins LB, Bodnar WM, Ball LM, Gold A, Rusyn I. 2015. Comparative analysis of the relationship between trichloroethylene metabolism and tissue-specific toxicity among inbred mouse strains: kidney effects. J Toxicol Environ Health A 78(1):32-49. doi:10.1080/15287394.2015.958418 PMID:25424545 PMCID:PMC4281933
  • Yoo HS, Cichocki JA, Kim S, Venkatratnam A, Iwata Y, Kosyk O, Bodnar WM, Sweet S, Knap A, Wade TL, Campbell J, Clewell H, Melnyk SB, Chiu WA, Rusyn I. 2015. The contribution of peroxisome proliferator-activated receptor alpha to the relationship between toxicokinetics and toxicodynamics of trichloroethylene. Toxicol Sci 147(2):339-349. doi:10.1093/toxsci/kfv134 PMID:26136231 PMCID:PMC4598794
  • Yu R, Lai Y, Hartwell HJ, Moeller BC, Doyle-Eisele M, Bodnar WM, Starr TB, Swenberg JA. 2015. Formation, accumulation, and hydrolysis of endogenous and exogenous formaldehyde-induced DNA damage. Toxicol Sci 146(1):170-182. doi:10.1093/toxsci/kfv079 PMID:25904104 PMCID:PMC4476463


  • Sharma V, Collins LB, Clement JM, Zhang Z, Nakamura J, Swenberg JA. 2014. Molecular dosimetry of endogenous and exogenous O(6)-methyl-dG and N7-methyl-G adducts following low dose [D3]-methylnitrosourea exposures in cultured human cells. Chem Res Toxicol 27(4):480-482. doi:10.1021/tx5000602 PMID:24628573 PMCID:PMC3998766
  • Ye W, Paul D, Gao L, Seckute J, Sangaiah R, Jayaraj K, Zhang Z, Kaminski P, Ealick SE, Gold A, Ball LM. 2014. Ethenoguanines undergo glycosylation by nucleoside 2'-deoxyribosyltransferases at non-natural sites. PLoS One 9(12):e115082. doi:10.1371/journal.pone.0115082 PMID:25521390 PMCID:PMC4270796



  • Lu K, Craft S, Nakamura J, Moeller BC, Swenberg JA. 2012. Use of LC-MS/MS and stable isotopes to differentiate hydroxymethyl and methyl DNA adducts from formaldehyde and nitrosodimethylamine. Chem Res Toxicol 25(3):664-675. doi:10.1021/tx200426b PMID:22148432 PMCID:PMC3307879
  • Lu K, Gul H, Upton PB, Moeller BC, Swenberg JA. 2012. Formation of hydroxymethyl DNA adducts in rats orally exposed to stable isotope labeled methanol. Toxicol Sci 126(1):28-38. doi:10.1093/toxsci/kfr328 PMID:22157354 PMCID:PMC3289495
  • Mutlu E, Jeong Y, Collins LB, Ham AL, Upton PB, Hatch G, Winsett D, Evansky P, Swenberg JA. 2012. A new LC-MS/MS method for the quantification of endogenous and vinyl chloride-induced 7-(2-oxoethyl)guanine in Sprague–Dawley rats. Chem Res Toxicol 25(2):391-399. doi:10.1021/tx200447w PMID:22211352 PMCID:PMC3288741


  • Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333(6047):1300-1303. doi:10.1126/science.1210597 PMID:21778364 PMCID:PMC3495246
  • Jung D, Matson CW, Collins LB, Laban G, Stapleton HM, Bickham JW, Swenberg JA, Di Giulio RT. 2011. Genotoxicity in Atlantic killifish (Fundulus heteroclitus) from a PAH-contaminated Superfund site on the Elizabeth River, Virginia. Ecotoxicology 20:1890-1899. doi:10.1007/s10646-011-0727-9 PMID:21706406 PMCID:PMC3203518
  • Lu K, Moeller BC, Doyle-Eisele M, McDonald JD, Swenberg JA. 2011. Molecular dosimetry of N2-hydroxymethyl-dG DNA adducts in rats exposed to formaldehyde. Chem Res Toxicol 24(2):159-161. doi:10.1021/tx1003886 PMID:21155545 PMCID:PMC3128468
  • Moeller BC, Lu K, Doyle-Eisele M, McDonald JD, Gigliotti A, Swenberg JA. 2011. Determination of N2-hydroxymethyl-dG adducts in the nasal epithelium and bone marrow of nonhuman primates following 13CD2-formaldehyde inhalation exposure. Chem Res Toxicol 24(2):162-164. doi:10.1021/tx1004166 PMID:21222454 PMCID:PMC3273041
  • Swenberg JA, Lu K, Moeller BC, Gao L, Upton PB, Nakamura J, Starr TB. 2011. Endogenous versus exogenous DNA adducts: their role in carcinogenesis, epidemiology, and risk assessment. Toxicol Sci 120(suppl1):S130-S145. doi:10.1093/toxsci/kfq371 PMID:21163908 PMCID:PMC3043087
  • Wu K, Chiang S, Shih W, Huang CJ, Chen M, Swenberg JA. 2011. The application of mass spectrometry in molecular dosimetry: Ethylene oxide as an example. Mass Spectrom Rev 30(5):733-756. doi:10.1002/mas.20299 PMID:21328599
  • Zhang Z, Sangaiah R, Gold A, Ball LM. 2011. Synthesis of uniformly 13C-labeled polycyclic aromatic hydrocarbons. Org Biomol Chem 9:5431-5435. doi:10.1039/C0OB01107J PMID:21670806


  • Boysen G, Collins LB, Liao S, Luke AM, Pachkowski BF, Watters JL, Swenberg JA. 2010. Analysis of 8-oxo-7,8-dihydro-2′-deoxyguanosine by ultra high pressure liquid chromatography–heat assisted electrospray ionization–tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 878(3-4):375-380. doi:10.1016/j.jchromb.2009.12.004 PMID:20022307 PMCID:PMC5085061
  • Lu K, Collins LB, Ru H, Bermudez E, Swenberg JA. 2010. Distribution of DNA adducts caused by inhaled formaldehyde is consistent with induction of nasal carcinoma but not Leukemia. Toxicol Sci 116(2):441-451. doi:10.1093/toxsci/kfq061 PMID:20176625 PMCID:PMC2905397
  • Lu K, Ye W, Zhou L, Collins LB, Chen X, Gold A, Ball LM, Swenberg JA. 2010. Structural characterization of formaldehyde-induced cross-links between amino acids and deoxynucleosides and their oligomers. J Am Chem Soc 132(10):3388-3399. doi:10.1021/ja908282f PMID:20178313 PMCID:PMC2866014
  • Mutlu E, Collins LB, Stout MD, Upton PB, Daye LR, Winsett D, Hatch G, Evansky P, Swenberg JA. 2010. Development and application of an LC-MS/MS method for the detection of the vinyl chloride-induced DNA adduct N2,3-ethenoguanine in tissues of adult and weanling rats following exposure to [13C2]-VC. Chem Res Toxicol 23(9):1485-1491. doi:10.1021/tx1001767 PMID:20799743 PMCID:PMC3104734


  • Kim S, Boysen G, Swenberg JA, Gold A, Ball LM, Bradford BU, Rusyn I, Collins LB. 2009. Liquid chromatography electrospray ionization tandem mass spectrometry analysis method for simultaneous detection of trichloroacetic acid, dichloroacetic acid, S-(1,2-dichlorovinyl)glutathione and S-(1,2-dichlorovinyl)-L-cysteine. Toxicology 262(3):230-238. doi:10.1016/j.tox.2009.06.013 PMID:19549554 PMCID:PMC2765814


  • Kang-Sickel JC, Nam T, Jayaraj K, Ball LM, French JE, Klapper DG, Gold A, Nylander-French LA. 2008. S-arylcysteine-keratin adducts as biomarkers of human dermal exposure to aromatic hydrocarbons. Chem Res Toxicol 21(4):852-858. doi:10.1021/tx7003773 PMID:18361511


  • Kang-Sickel JC, Gold A, Ball LM, Karupiah J, Nylander-French LA, Parron V, Klapper DG, French JE. 2006. Detection of naphthalene keratin adducts in human skin using ELISA. J Mol Biol 38(Suppl.2):67-68.
  • Singleton D, Sangaiah R, Gold A, Ball LM, Aitken MD. 2006. Identification and quantification of uncultivated Proteobacteria associated with pyrene degradation in a bioreactor treating PAH-contaminated soil. Environ Microbiol 8(10):1736-1745. doi:10.1111/j.1462-2920.2006.01112.x PMID:16958754
  • Ye W, Sangaiah R, Degen DE, Gold A, Jayaraj K, Koshlap KM, Boysen G, Williams J, Tomer KB, Ball LM. 2006. A 2-iminohydantoin from the oxidation of guanine. Chem Res Toxicol 19(4):506-10. PMID:16608161


  • Jeong Y, Sangaiah R, Nakamura J, Pachkowski BF, Ranasinghe A, Gold A, Ball LM, Swenberg JA. 2005. Analysis of M(1)G-dR in DNA by aldehyde reactive probe labeling and liquid chromatography tandem mass spectrometry. Chem Res Toxicol 18(1):51-60. PMID:15651849
  • Singleton D, Powell SN, Sangaiah R, Gold A, Ball LM, Aitken MD. 2005. Stable-isotope probing of bacteria capable of degrading salicylate, naphthalene, or phenanthrene in a bioreactor treating contaminated soil. Appl Environ Microbiol 71(3):1202-1209. doi:10.1128/AEM.71.3.1202-1209.2005 PMID:15746319 PMCID:PMC1065189
  • Waidyanatha S, Sangaiah R, Rappaport SM. 2005. Characterization and quantification of cysteinyl adducts of benzene diol epoxide. Chem Res Toxicol 18(7):1178-1185. PMID:16022511
  • Ye W, Sangaiah R, Degen DE, Gold A, Jayaraj K, Koshlap KM, Boysen G, Ball LM. 2005. A 2-Iminohydantoin is the major product from DMDO oxidation of Guanine. In: Superfund Basic Research Program Annual Meeting, January 12-13. New York Academy of Medicine, New York, NY.


  • Casteel MJ, Jayaraj K, Gold A, Ball LM, Sobsey MD. 2004. Photoinactivation of hepatitis A virus by synthetic porphyrins. Photochemistry and Photobiology 80(2):294-300. PMID:15362943
  • Ham AL, Engelward BP, Koc H, Sangaiah R, Meira LB, Samson LD, Swenberg JA. 2004. New immunoaffinity-LC-MS/MS methodology reveals that Aag null mice are deficient in their ability to clear 1,N-6-etheno-deoxyadenosine DNA lesions from lung and liver in vivo. DNA Repair (Amst) 3(3):257-265. PMID:15177041
  • Lin P, Sangaiah R, Ranasinghe A, Ball LM, Swenberg JA, Gold A. 2004. Synthesis of chlorinated and non-chlorinated biphenyl-2,3-and 3,4-catechols and their [H-2(3)]-isotopomers. Org Biomol Chem 2(18):2624-2629. PMID:15351827


  • Li Y, Boysen G, Dicheva ND, Upton PB, Swenberg JA. 2003. Effects of Free Unmodified Purine Basis, Guanine and Adenine, on Ionization of Three N-7 Guanine DNA Adducts Using LC/ESI/MS/MS. In: Proceedings of the American Society of Mass Spectrometry, 51st Annual Conference.
  • Pachkowski BF, Nakamura J, Li Y, Sangaiah R, Gold A, Swenberg JA. 2003. An LC/MS Approach to the Differentiation of Aldehydic Deoxyribose Lesions. In: Proceedings of the American Association for Cancer Research Annual Meeting, 2003.


  • Koc H, Swenberg JA. 2002. Applications of mass spectrometry for quantitation of DNA adducts. J Chromatogr B Analyt Technol Biomed Life Sci 778(1-2):323-343. PMID:12376138
  • Morinello EJ, Ham AL, Ranasinghe A, Nakamura J, Upton PB, Swenberg JA. 2002. Molecular dosimetry and repair of N2,3-ethenoguanine in rats exposed to vinyl chloride. Cancer Res 62:5189-5195. PMID:12234983
  • Morinello EJ, Koc H, Ranasinghe A, Swenberg JA. 2002. Differential induction of N2,3-ethenoguanine in rat brain and liver after exposure to vinyl chloride. Cancer Res 62:5183-5188.
  • Nam T, Sangaiah R, Gold A, Lacks GD, Nylander-French LA, French JE. 2002. Synthesis of FMOC-protected S-arylcysteines and modified keratin sequence peptides as specific epitopes as immunogens. Polycyclic Aromatic Compounds 22(3-4):239-248.


  • Ham AL, Zhan C, Koc H, Hass RJ, Swenberg JA. 2001. Analysis of 1,N6-ethenodeoxyguanosine by immunoaffinity/LC/MS/MS. In: Proceedings of the 49th ASMS (American Society for Mass Spectrometry) Conference on Mass Spectrometry and Allied Topics. June 4-7. Chicago, IL.
  • Kazunga C, Aitken MD, Gold A, Sangaiah R. 2001. Fluoranthene-2,3- and -1,5-diones are novel products from the bacterial transformation of fluoranthene. Environ Sci Technol 35(5):917-922. PMID:11351535
  • Morinello EJ, Ham AL, Ranasinghe A, Sangaiah R, Swenberg JA. 2001. Simultaneous quantitation of N(2),3-ethenoguanine and 1,N(2)-ethenoguanine with an immunoaffinity/gas chromatography/high-resolution mass spectrometry assay. Chem Res Toxicol 14(3):327-334. PMID:11258983
  • Nam T, Sangaiah R, Gold A, Lacks GD, Nylander-French LA, French JE. 2001. Synthesis of FMOC-protected S-aryclysteines and modified keratin sequence peptides as specific epitopes as immunogens. In: Proceedings of the 18th International Symposiium on Polycyclic Aromatic Compounds, Sept 9-13. Cincinnati, OH.
  • Schulz MR, Hertz-Picciotto I, Todd L, Ball LM. 2001. Reconciling animal and human data in a cancer risk assessment of acrylonitrile. Scand J Work Environ Health 27(1):14-20. PMID:11266142
  • Troester MA, Kupper LL, Rappaport SM. 2001. Comparison of non-linear and linear models for estimating haemoglobin adduct stability. Biomarkers 6(4):251-261. PMID:23889277


  • Ham AL, Ranasinghe A, Koc H, Swenberg JA. 2000. 4-Hydroxy-2-nonenal and ethyl linoleate from N2,3-ethenoguanine under peroxidizing conditions. Chem Res Toxicol 13:1243-1250.
  • Korte JE, Hertz-Picciotto I, Schulz MR, Ball LM, Duell EJ. 2000. The contribution of benzene to smoking-induced Leukemia. Environ Health Perspect 108(4):333-339. PMID:10753092
  • Lin P, Sangaiah R, Ranasinghe A, Upton PB, La DK, Gold A, Swenberg JA. 2000. Formation of quinonoid-derived protein adducts in the liver and brain of Sprague-Dawley rats treated with 2,2',5,5'-tetrachlorobiphenyl. Chem Res Toxicol 13(8):710-718. PMID:10956058
  • Walker V, Wu K, Upton PB, Ranasinghe A, Scheller NA, Cho M, Vergnes JS, Skopek TR, Swenberg JA. 2000. Biomarkers of exposure and effect as indicators of potential carcinogenic risk arising from in vivo metabolism of ethylene to ethylene oxide. Carcinogenesis 21(9):1661-1669. PMID:10964097


  • Ham AL, Ranasinghe A, Morinello EJ, Nakamura J, Upton PB, Johnson F, Swenberg JA. 1999. Immunoaffinity/gas chromatography/high resolution mass spectrometry method for the detection of N2,3-ethenoguanine. Chem Res Toxicol 12:1240-1246. PMID:10604874
  • Kazunga C, Aitken MD, Gold A. 1999. Primary product of the horseradish peroxidase-catalyzed oxidation of pentachlorophenol. Environ Sci Technol 33:1408-1412.


  • Holt S, Sangaiah R, Swenberg JA. 1998. Detection of 1,N6-ethenoadenine in rat urine after chloroethylene oxide exposure. Carcinogenesis 19(10):1763-1769. PMID:9806156
  • Ranasinghe A, Scheller NA, Wu K, Upton PB, Swenberg JA. 1998. Application of gas chromatography/electron capture negative chemical ionization/high resolution mass spectrometry for analysis of DNA and protein adducts. Chem Res Toxicol 11:520-526. PMID:9585483
  • Yen T, Holt S, Sangaiah R, Gold A, Swenberg JA. 1998. Quantitation of 1,N6 ethenoadenine in rat urine by immunoaffinity extraction combined with liquid chromatography/electrospray ionization mass spectrometry. Chem Res Toxicol 11(7):810-815. PMID:9671544


  • Wagoner DB, Christman RF, Cauchon G, Paulson R. 1997. Molar mass and size of Suwannee River natural organic matter using multi-angle laser light scattering. Environ Sci Technol 31(3):937-941.


  • Christova-Gueoguieva NI, Yen T, Scheller NA, Holt S, Swenberg JA. 1996. Quantitation of N2,3-ethenoguanine (epsilonG) in rat liver by liquid chromatography-electrospray mass spectrometry. Environ Health Perspect 30(1,part2):235.
  • Scheller NA, Ranasinghe A, Christova-Gueoguieva NI, Yen T, Ham AL, Swenberg JA. 1996. Detection of Endogenous N2,3-ethenoguanine by GC/ECNCI/MS. In: Proceedings of the 44th ASMS (American Society for Mass Spectrometry) on Mass Spectrometry and Allied Topics. Portland, OR. pp.781.
  • Scheller NA, Ranasinghe A, Yen T, Christova-Gueoguieva NI. 1996. Quantitation of endogenous ethenoguanine by GC/ECNCI/HRMS. In: Proceedings of the 44th ASMS (American Society for Mass Spectrometry) on Mass Spectrometry and Allied Topics. Portland, OR.
  • Yen T, Charles MJ, Voyksner RD. 1996. Processes that affect electrospray ionization-mass spectrometry of nucleobases and nucleosides. J Am Soc Mass Spectrom 7(11):1106-1108. PMID:24203072
  • Yen T, Christova-Gueoguieva NI, Scheller NA, Holt S, Swenberg JA, Charles MJ. 1996. HPLC/ESI/MS May be the Technique of Choice for the Analysis of Certain DNA Adducts. In: Proceedings of the 44th ASMS (American Society for Mass Spectrometry) on Mass Spectrometry and Allied Topics. Portland, OR. pp.780.
  • Yen T, Christova-Gueoguieva NI, Scheller NA, Holt S, Swenberg JA, Charles MJ. 1996. Quantitative analysis of the DNA adduct N2,3-ethenoguanine using liquid chromatography/electrospray ionization mass spectrometry. J Mass Spectrom 31(11):1271-1276. PMID:8946734


  • Scheller NA, Sangaiah R, Ranasinghe A, Amarnath V, Gold A, Swenberg JA. 1995. Synthesis of [4,5,6,8-13C4]guanine, a reagent for the production of internal standards of guanyl DNA adducts. Chem Res Toxicol 8(3):333-337. PMID:7578918
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