R. Stephen Lloyd, Ph.D.

  • Professor, Oregon Institute of Occupational Health Sciences
  • Professor of Molecular and Medical Genetics, School of Medicine
  • Associate Director for Basic Research, Oregon Institute of Occupational Health Sciences
  • Molecular and Medical Genetics Graduate Program, School of Medicine
  • Graduate Program in Biomedical Sciences, School of Medicine
  • Cancer Biology Graduate Program, School of Medicine

Biography

Dr. R. Stephen Lloyd received his BS in Biology from Florida State University in 1975, majoring in marine pollution biology. His research interests turned to cancer chemotherapy and in 1979, he earned his Ph.D. in Molecular Biology from the University of Texas Graduate School of Biomedical Sciences in Houston, TX. After learning about mechanisms by which DNA can be damaged, he began his career in DNA repair as a postdoctoral fellow at Stanford University in the laboratory of Dr. Philip Hanawalt. Following two years at Stanford, he worked for two more years for a genetic engineering company, before joining the Biochemistry Department at Vanderbilt University in 1983. In his ten-year stay at Vanderbilt, Dr. Lloyd rose through the ranks to Full Professor, and his research focused on both DNA repair and molecular mutagenesis. He was then recruited to the Center for Molecular Science at the University of Texas Medical Branch in which the faculty exclusively specialized in DNA repair mechanisms. During his twelve years at UTMB, he also became the Director of two Centers in Environmental Toxicology. In August 2003, he, along with his wife, Dr. Amanda K. McCullough was recruited to join the CROET faculty at OHSU. Together they have both separate and joint research projects in the research areas described below.

Education and training

  • Degrees

    • B.S., 1975, Florida State University
    • Ph.D., 1979, University of Texas Houston Graduate School of Biomedical Sciences

Memberships and associations:

  • American Association for the Advancement of Science (AAAS)
  • Environmental Mutagenesis & Genomics Society
  • Federation of the American Societies of Experimental Biology

Areas of interest

  • Strategies to prevent sunlight-induced skin cancer via the topical introduction of repair enzymes into human cells
  • The mechanisms by which the loss of a DNA repair enzyme can lead to the clinical manifestations of Metabolic Syndrome - a constellation of diseases (obesity, fatty liver disease, insulin resistance and hypertension) that affect >45 million Americans
  • Mutagenic potential of alkyl-substituted and unsubstituted Fapy-dG adducts
  • Molecular mechanisms for the repair and replication of DNA-protein crosslinks
  • Replication bypass of DNAs containing interstrand DNA crosslinks

Honors and awards

  • Awards: Editor’s Choice Award for Environmental and Molecular Mutagenesis for Sha Y, Minko IG, Malik CK, Rizzo CJ, Lloyd RS. Error-prone replication bypass of the imidazole ring-opened formamidopyrimidine deoxyguanosine adduct. Environ Mol Mutagen. 2017 May;58(4):182-189. PMID:28436537 PMCID: PMC5476229

Publications

Selected publications

  • Tomar R, Minko IG, Kellum AH Jr, Voehler MW, Stone MP, McCullough AK, Lloyd RS. DNA Sequence Modulates the Efficiency of NEIL1-Catalyzed Excision of the Aflatoxin B1-Induced Formamidopyrimidine Guanine Adduct. Chem Res Toxicol. 2021 Mar 15;34(3):901-911. PMCID: in progress
  • Owen N, Minko IG, Moellmer SA, Cammann SK, Lloyd RS, McCullough AK. Enhanced cytarabine-induced killing in OGG1-deficient acute myeloid leukemia cells. Proc Natl Acad Sci U S A. 2021 Mar 16;118(11):e2016833118. PMCID: in progress
  • Kant M, Tahara YK, Jaruga P, Coskun E, Lloyd RS, Kool ET, Dizdaroglu M. Inhibition by Tetrahydroquinoline Sulfonamide Derivatives of the Activity of Human 8-Oxoguanine DNA Glycosylase (OGG1) for Several Products of Oxidatively induced DNA Base Lesions.  ACS Chem Biol. 2021 Jan 15;16(1):45-51. PMCID: in progress
  • Paluri SL, Burak M, Senejani AG, Levinson M, Rahim T, Clairmont K, Kashgarian M, Alvarado-Cruz I, Meas R, Cardó-Vila M, Zeiss C, Maher S, Bothwell ALM, Coskun E, Kant M, Jaruga P, Dizdaroglu M, Lloyd RS, Sweasy JB. DNA glycosylase deficiency leads to decreased severity of lupus in the Polb-Y265C mouse model. DNA Repair (Amst). 2021 Jun 24;105:103152. PMCID: in progress
  • Minko IG, Vartanian VL, Tozaki NN, Coskun E, Coskun SH, Jaruga P, Yeo J, David SS, Stone MP, Egli M, Dizdaroglu M, McCullough AK, Lloyd RS. Recognition of DNA adducts by edited and unedited forms of DNA glycosylase NEIL1. DNA Repair (Amst). 2020 Jan;85:102741 PMCID: PMC7069121
  • McCullough, AK, I. G. Minko, IG, A. Nilsen, A, S. Nagarajan, S, and Lloyd, RS (2020) Modulation of DNA Glycosylase Activities via Small Molecules. Chapter 14 in DNA Damage, DNA Repair and Disease, (Eds Miral Dizdaroglu and R. Stephen Lloyd) Royal Society of Chemistry, United Kingdom
  • Sampath, H and Lloyd, RS. Roles of OGG1 in transcriptional regulation and maintenance of metabolic homeostasis. DNA Repair (Amst). 2019 Sep;81:102667 PMCID: PMC6939861.
  • McCullough AK, Lloyd RS. Mechanisms underlying aflatoxin-associated mutagenesis - Implications in carcinogenesis. DNA Repair (Amst). 2019 May;77:76-86 PMCID:PMC6959417
  • Minko IG, Christov PP, Li L, Stone MP, McCullough AK, Lloyd RS. Processing of N5-substituted formamidopyrimidine DNA adducts by DNA glycosylases NEIL1 and NEIL3. DNA Repair (Amst). 2019 Jan;73:49-54 PMCID: PMC6588396
  • Minko IG, Vartanian VL, Tozaki NN, Linde OK, Jaruga P, Coskun SH, Coskun E, Qu C, He H, Xu C, Chen T, Song Q, Jiao Y, Stone MP, Egli M, Dizdaroglu M, McCullough AK, Lloyd RS. Characterization of rare NEIL1 variants found in East Asian populations. DNA Repair (Amst). 2019 May 3;79:32-39 PMCID: PMC6677271 

Publications

  • The Distinct Roles of NEIL1 and XPA in Limiting Aflatoxin B1–Induced Mutagenesis in Mice

    Molecular Cancer Research
    1. Michael M. Luzadder
    2. Irina Minko
    3. Vladimir L. Vartanian
    4. Marten Davenport
    5. Lev M. Fedorov
    6. Amanda K. McCullough
    7. Robert Lloyd
  • Functional characterization of single nucleotide polymorphic variants of DNA repair enzyme NEIL1 in South Asian populations

    DNA Repair
    1. Jamie T. Zuckerman
    2. Asia Sage Jackson
    3. Irina G. Minko
    4. Melis Kant
    5. Pawel Jaruga
    6. Michael P. Stone
    7. Miral Dizdaroglu
    8. Amanda K. McCullough
    9. R. Stephen Lloyd
  • Interaction of mitoxantrone with abasic sites - DNA strand cleavage and inhibition of apurinic/apyrimidinic endonuclease 1, APE1

    DNA Repair
    1. Irina G. Minko
    2. Samantha A. Moellmer
    3. Michael M. Luzadder
    4. Rachana Tomar
    5. Michael P. Stone
    6. Amanda K. McCullough
    7. R. Stephen Lloyd
  • Mass Spectrometry-Based Method to Measure Aflatoxin B1 DNA Adducts in Formalin-Fixed Paraffin-Embedded Tissues

    Chemical Research in Toxicology
    1. Medjda Bellamri
    2. Lihua Yao
    3. Rachana Tomar
    4. Vladimir Vartanian
    5. Carmelo J. Rizzo
    6. Michael P. Stone
    7. John D. Groopman
    8. R. Stephen Lloyd
    9. Robert J. Turesky
  • The aflatoxin B1-induced imidazole ring-opened guanine adduct

    Environmental and Molecular Mutagenesis
    1. Irina G. Minko
    2. Andrew H. Kellum
    3. Michael P. Stone
    4. R. Stephen Lloyd
  • Base excision repair of the N-(2-deoxy-d-erythro-pentofuranosyl)-urea lesion by the hNEIL1 glycosylase

    Nucleic acids research
    1. Rachana Tomar
    2. Irina G. Minko
    3. Pankaj Sharma
    4. Andrew H. Kellum
    5. Li Lei
    6. Joel M. Harp
    7. T. M. Iverson
    8. R. Stephen Lloyd
    9. Martin Egli
    10. Michael P. Stone
  • Functional analyses of single nucleotide polymorphic variants of the DNA glycosylase NEIL1 present in sub-Saharan African populations

    DNA Repair
    1. Jamie T. Zuckerman
    2. Irina G. Minko
    3. Melis Kant
    4. Pawel Jaruga
    5. Michael P. Stone
    6. Miral Dizdaroglu
    7. Amanda K. McCullough
    8. R. Stephen Lloyd
  • Spontaneous allelic variant in deafness–blindness gene Ush1g resulting in an expanded phenotype

    Genes, Brain and Behavior
    1. Vladimir Vartanian
    2. Jocelyn Krey
    3. Paroma Chatterjee
    4. Allison Curtis
    5. Makayla Six
    6. Sean P.M. Rice
    7. Sherri M. Jones
    8. Harini Sampath
    9. Charles N. Allen
    10. Renee C. Ryals
    11. R. Stephen Lloyd
    12. Peter G. Barr-Gillespie
  • Synthesis and Characterization of 15N5-Labeled Aflatoxin B1-Formamidopyrimidines and Aflatoxin B1-N7-Guanine from a Partial Double-Stranded Oligodeoxynucleotide as Internal Standards for Mass Spectrometric Measurements

    ACS Omega
    1. Pawel Jaruga
    2. Rachana Tomar
    3. Melis Kant
    4. Vladimir Vartanian
    5. Benjamin Sexton
    6. Carmelo J. Rizzo
    7. Robert J. Turesky
    8. Michael P. Stone
    9. R. Stephen Lloyd
    10. Miral Dizdaroglu
  • Polymorphic variant Asp239Tyr of human DNA glycosylase NTHL1 is inactive for removal of a variety of oxidatively-induced DNA base lesions from genomic DNA

    DNA Repair
    1. Melis Kant
    2. Victoria Quintana
    3. Erdem Coskun
    4. Pawel Jaruga
    5. R. Stephen Lloyd
    6. Joann B. Sweasy
    7. Miral Dizdaroglu
  • DNA glycosylase deficiency leads to decreased severity of lupus in the Polb-Y265C mouse model

    DNA Repair
    1. Sesha L. Paluri
    2. Matthew Burak
    3. Alireza G. Senejani
    4. Madison Levinson
    5. Tania Rahim
    6. Kaylyn Clairmont
    7. Michael Kashgarian
    8. Isabel Alvarado-Cruz
    9. Rithy Meas
    10. Marina Cardó-Vila
    11. Caroline Zeiss
    12. Stephen Maher
    13. Alfred L.M. Bothwell
    14. Erdem Coskun
    15. Melis Kant
    16. Pawel Jaruga
    17. Miral Dizdaroglu
    18. R. Stephen Lloyd
    19. Joann B. Sweasy
  • DNA Sequence Modulates the Efficiency of NEIL1-Catalyzed Excision of the Aflatoxin B1-Induced Formamidopyrimidine Guanine Adduct

    Chemical Research in Toxicology
    1. Rachana Tomar
    2. Irina G. Minko
    3. Andrew H. Kellum
    4. Markus W. Voehler
    5. Michael P. Stone
    6. Amanda K. McCullough
    7. R. Stephen Lloyd
  • Enhanced cytarabine-induced killing in OGG1-deficient acute myeloid leukemia cells

    Proceedings of the National Academy of Sciences of the United States of America
    1. Nichole Owen
    2. Irina G. Minko
    3. Samantha A. Moellmer
    4. Sydney K. Cammann
    5. R. Stephen Lloyd
    6. K. McCullough Amanda
  • Inhibition by Tetrahydroquinoline Sulfonamide Derivatives of the Activity of Human 8-Oxoguanine DNA Glycosylase (OGG1) for Several Products of Oxidatively induced DNA Base Lesions

    ACS chemical biology
    1. Melis Kant
    2. Yu Ki Tahara
    3. Pawel Jaruga
    4. Erdem Coskun
    5. R. Stephen Lloyd
    6. Eric T. Kool
    7. Miral Dizdaroglu
  • Maternal Transmission of Human OGG1 Protects Mice Against Genetically- and Diet-Induced Obesity Through Increased Tissue Mitochondrial Content

    Frontiers in Cell and Developmental Biology
    1. Natalie Burchat
    2. Priyanka Sharma
    3. Hong Ye
    4. Sai Santosh Babu Komakula
    5. Agnieszka Dobrzyn
    6. Vladimir Vartanian
    7. R. Stephen Lloyd
    8. Harini Sampath
  • Exosomal miR-221 derived from hydroquinone-transformed malignant human bronchial epithelial cells is involved in cell viability of recipient cells

    Journal of Applied Toxicology
    1. Ran Jiang
    2. Haoyu Huang
    3. Zhenwei Lian
    4. Zuqing Hu
    5. R. Stephen Lloyd
    6. Daokui Fang
    7. Yanfeng Li
    8. Hongyi Xian
    9. Jianhui Yuan
    10. Yan Sha
    11. Sanming Wang
    12. Dalin Hu
  • Exosomes derived from normal human bronchial epithelial cells down-regulate proliferation and migration of hydroquinone-transformed malignant recipient cells via up-regulating PTEN expression

    Chemosphere
    1. Zhenwei Lian
    2. Zuqing Hu
    3. Hongyi Xian
    4. Ran Jiang
    5. Haoyu Huang
    6. Yunxia Jiang
    7. Zhongdaixi Zheng
    8. R. Stephen Lloyd
    9. Jianhui Yuan
    10. Yan Sha
    11. Sanming Wang
    12. Dalin Hu
  • OGG1 deficiency alters the intestinal microbiome and increases intestinal inflammation in a mouse model

    PloS one
    1. Holly Simon
    2. Vladimir Vartanian
    3. Melissa H. Wong
    4. Yusaku Nakabeppu
    5. Priyanka Sharma
    6. R. Stephen Lloyd
    7. Harini Sampath
  • Recognition of DNA adducts by edited and unedited forms of DNA glycosylase NEIL1

    DNA Repair
    1. Irina G. Minko
    2. Vladimir L. Vartanian
    3. Naoto N. Tozaki
    4. Erdem Coskun
    5. Sanem Hosbas Coskun
    6. Pawel Jaruga
    7. Jongchan Yeo
    8. Sheila S. David
    9. Michael P. Stone
    10. Martin Egli
    11. Miral Dizdaroglu
    12. Amanda K. McCullough
    13. R. Stephen Lloyd
  • Aflatoxin-Guanine DNA Adducts and Oxidatively Induced DNA Damage in Aflatoxin-Treated Mice in Vivo as Measured by Liquid Chromatography-Tandem Mass Spectrometry with Isotope Dilution

    Chemical Research in Toxicology
    1. Erdem Coskun
    2. Pawel Jaruga
    3. Vladimir Vartanian
    4. Onur Erdem
    5. Patricia A. Egner
    6. John D. Groopman
    7. R. Stephen Lloyd
    8. Miral Dizdaroglu
  • Characterization of rare NEIL1 variants found in East Asian populations

    DNA Repair
    1. Irina G. Minko
    2. Vladimir L. Vartanian
    3. Naoto N. Tozaki
    4. Oskar K. Linde
    5. Pawel Jaruga
    6. Sanem Hosbas Coskun
    7. Erdem Coskun
    8. Chunfeng Qu
    9. Huan He
    10. Chungui Xu
    11. Taoyang Chen
    12. Qianqian Song
    13. Yuchen Jiao
    14. Michael P. Stone
    15. Martin Egli
    16. Miral Dizdaroglu
    17. Amanda K. McCullough
    18. R. Stephen Lloyd
  • Processing of N5-substituted formamidopyrimidine DNA adducts by DNA glycosylases NEIL1 and NEIL3

    DNA Repair
    1. Irina G. Minko
    2. Plamen P. Christov
    3. Liang Li
    4. Michael P. Stone
    5. Amanda K. McCullough
    6. R. Stephen Lloyd
  • Modulation of UVB-induced Carcinogenesis by Activation of Alternative DNA Repair Pathways

    Scientific Reports
    1. Yan Sha
    2. Vladimir Vartanian
    3. Nichole Owen
    4. Stephanie J. Mengden Koon
    5. Marcus J. Calkins
    6. Courtney S. Thompson
    7. Zahra Mirafzali
    8. Sara Mir
    9. Lisa E. Goldsmith
    10. Huaping He
    11. Chun Luo
    12. Scott M. Brown
    13. Paul W. Doetsch
    14. Andy Kaempf
    15. Jeong Y. Lim
    16. Amanda K. McCullough
    17. R. Stephen Lloyd
  • The DNA Repair Protein OGG1 Protects Against Obesity by Altering Mitochondrial Energetics in White Adipose Tissue

    Scientific Reports
    1. Sai Santosh Babu Komakula
    2. Jana Tumova
    3. Deeptha Kumaraswamy
    4. Natalie Burchat
    5. Vladimir Vartanian
    6. Hong Ye
    7. Agnieszka Dobrzyn
    8. R. Stephen Lloyd
    9. Harini Sampath
  • 8-oxoguanine DNA glycosylase (OGG1) deficiency elicits coordinated changes in lipid and mitochondrial metabolism in muscle

    PloS one
    1. Vladimir Vartanian
    2. Jana Tumova
    3. Pawel Dobrzyn
    4. Agnieszka Dobrzyn
    5. Yusaku Nakabeppu
    6. R. Stephen Lloyd
    7. Harini Sampath
  • Error-prone replication bypass of the imidazole ring-opened formamidopyrimidine deoxyguanosine adduct

    Environmental and Molecular Mutagenesis
    1. Yan Sha
    2. Irina G. Minko
    3. Chanchal K. Malik
    4. Carmelo J. Rizzo
    5. R. Stephen Lloyd
  • Mutagenic potential of nitrogen mustard-induced formamidopyrimidine DNA adduct

    Journal of Biological Chemistry
    1. Irina G. Minko
    2. Carmelo J. Rizzo
    3. R. Stephen Lloyd