Scholars@Duke

• Background
• 

  Education, Training, & Certifications

  • Ph.D., The University of Chicago 2012
• 

  Previous Appointments & Affiliations

  • Assistant Professor of Molecular Genetics and Microbiology, Molecular Genetics and Microbiology, Basic Science Departments 2015 - 2022
• Recognition
• 

  In the News

  • NOV 10, 2022

    Duke Researchers Developing Universal Flu Vaccine

  • MAY 25, 2021

    School of Medicine

    School of Medicine Researchers Honored for Study of the Pathogenesis of Infectious Disease

  • JAN 21, 2021

    Estrogen Receptors in Mom’s Placenta Critical During Viral Infection

  • JAN 11, 2021

    Duke Health News

    Sniffing Out COVID-Related Loss of Smell

  • SEP 1, 2020

    Scent-Sensing Cells Have a Better Way to Fight Flu

  • JUL 29, 2019

    Lung Cell Patches Its Own DNA on the Fly to Survive Influenza

  • SEP 6, 2018

    Microbiology Society Recognizes Two Duke Researchers

  • JUL 24, 2017

    New Vaccine Production Could Improve Flu Shot Accuracy
• Expertise
• 

  Subject Headings

  • Antiviral Agents
  • Genetics
  • Microbiology
  • Virology
• Research
• 

  Selected Grants

  • Control of virus induced type I interferon signaling during pregnancy awarded by National Institutes of Health 2022 - 2027
  • Genetic Contributors to the Impact of Sex on Heterogeneity in Flu Infection awarded by National Institutes of Health 2022 - 2027
  • Hormone mediated regulation of antiviral immune responses awarded by Burroughs Wellcome Fund 2021 - 2026
  • Cell and Molecular Biology Training Program awarded by National Institutes of Health 2021 - 2026
  • Genetic and Genomics Training Grant awarded by National Institutes of Health 2020 - 2025
  • Viral Oncology Training Grant awarded by National Institutes of Health 1980 - 2024
  • CIVICS Component C - Option 3 awarded by National Institutes of Health 2019 - 2023
  • CIVICS Component A - Option 3 awarded by National Institutes of Health 2019 - 2023
  • CIVICs A - Option 23C awarded by National Institutes of Health 2021 - 2023
  • Rapidly Emerging Antiviral Drug Discovery Initiative (READDI) AViDD_READDI Proposal CORE C ENZYMOLOGY CORE awarded by University of North Carolina - Chapel Hill 2022 - 2023
  • Rapidly Emerging Antiviral Drug Development Initiative-RTI awarded by University of North Carolina - Chapel Hill 2022 - 2023
  • Thwarting Influenza with RNA-powered Modulators (ThIRM) awarded by Georgia Institute of Technology 2019 - 2023
  • Human Genetic Variation Regulating Transcriptional Response and Cellular Susceptibility to Influenza awarded by National Institutes of Health 2021 - 2023
  • DNA damage repair and the pathogenic effects of club cells surviving direct influenza virus infection awarded by National Institutes of Health 2019 - 2023
  • Multivalent, live attenuated and inactivated, COBRA-HA expressing viral particles as vaccines awarded by University of Georgia 2020 - 2022
  • Targeting virally induced inflammation to prevent the development of asthma awarded by Hartwell Foundation 2018 - 2022
  • Antigenically stabilized H3N2 vaccines that avoid egg adaption awarded by University of Rochester Medical Center 2018 - 2021
  • Genetics Training Grant awarded by National Institutes of Health 1979 - 2020
  • Organization and Function of Cellular Structure awarded by National Institutes of Health 1975 - 2020
  • Hemagglutinin proteins with non-immunogenic head domains as a universal influenza virus vaccine awarded by University of Rochester Medical Center 2018 - 2020
  • The effects of cells that survive direct influenza A virus infection on lung repair awarded by National Institutes of Health 2017 - 2019
  • Effect of m6A editing of RNA on influenza A virus replication awarded by National Institutes of Health 2017 - 2018
  • Survival of influenza A virus infected cells and effects on pathogenesis awarded by National Institutes of Health 2015 - 2017
• 

  External Relationships

  • JP Morgan Chase
  • McDonald's Corp
  • Merck Research Laboratories
  • Ohio State University
  • University of Chicago
  • University of Iowa
  • Vanderbilt University
• Publications & Artistic Works
• 

  Selected Publications

  • Academic Articles

    • Goodrum, Felicia, Anice Lowen, Seema Lakdawala, James Alwine, Arturo Casadevall, Michael Imperiale, Walter Atwood, et al. “Virology under the Microscope-a Call for Rational Discourse.” Mbio, January 26, 2023, e0018823. https://doi.org/10.1128/mbio.00188-23.
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    • Schott, Benjamin H., Liuyang Wang, Xinyu Zhu, Alfred T. Harding, Emily R. Ko, Jeffrey S. Bourgeois, Erica J. Washington, et al. “Single-cell genome-wide association reveals that a nonsynonymous variant in ERAP1 confers increased susceptibility to influenza virus.” Cell Genom 2, no. 11 (November 9, 2022). https://doi.org/10.1016/j.xgen.2022.100207.
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    • Trimarco, Joseph D., Sarah L. Nelson, Ryan R. Chaparian, Alexandra I. Wells, Nathan B. Murray, Parastoo Azadi, Carolyn B. Coyne, and Nicholas S. Heaton. “Cellular glycan modification by B3GAT1 broadly restricts influenza virus infection.” Nat Commun 13, no. 1 (October 29, 2022): 6456. https://doi.org/10.1038/s41467-022-34111-0.
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    • Yaron, Tomer M., Brook E. Heaton, Tyler M. Levy, Jared L. Johnson, Tristan X. Jordan, Benjamin M. Cohen, Alexander Kerelsky, et al. “Host protein kinases required for SARS-CoV-2 nucleocapsid phosphorylation and viral replication.” Sci Signal 15, no. 757 (October 25, 2022): eabm0808. https://doi.org/10.1126/scisignal.abm0808.
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    • Zhu, Xinyu, Joseph D. Trimarco, Courtney A. Williams, Alejandro Barrera, Timothy E. Reddy, and Nicholas S. Heaton. “ZBTB7A promotes virus-host homeostasis during human coronavirus 229E infection.” Cell Rep 41, no. 4 (October 25, 2022): 111540. https://doi.org/10.1016/j.celrep.2022.111540.
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    • Wang, Zhaohui, Matteo Boretto, Rosemary Millen, Naveen Natesh, Elena S. Reckzeh, Carolyn Hsu, Marcos Negrete, et al. “Rapid tissue prototyping with micro-organospheres.” Stem Cell Reports 17, no. 9 (September 13, 2022): 1959–75. https://doi.org/10.1016/j.stemcr.2022.07.016.
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    • Chaparian, Ryan R., Alfred T. Harding, Cait E. Hamele, Kristina Riebe, Amelia Karlsson, Gregory D. Sempowski, Nicholas S. Heaton, and Brook E. Heaton. “A Virion-Based Combination Vaccine Protects against Influenza and SARS-CoV-2 Disease in Mice.” J Virol 96, no. 15 (August 10, 2022): e0068922. https://doi.org/10.1128/jvi.00689-22.
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    • Hamele, Cait E., Alistair B. Russell, and Nicholas S. Heaton. “In Vivo Profiling of Individual Multiciliated Cells during Acute Influenza A Virus Infection.” J Virol 96, no. 14 (July 27, 2022): e0050522. https://doi.org/10.1128/jvi.00505-22.
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    • Froggatt, Heather M., and Nicholas S. Heaton. “Nonrespiratory sites of influenza-associated disease: mechanisms and experimental systems for continued study.” Febs J 289, no. 14 (July 2022): 4038–60. https://doi.org/10.1111/febs.16363.
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    • Trimarco, Joseph D., and Nicholas S. Heaton. “From high-throughput to therapeutic: host-directed interventions against influenza viruses.” Curr Opin Virol 53 (April 2022): 101198. https://doi.org/10.1016/j.coviro.2021.12.014.
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    • Harding, Alfred T., and Nicholas S. Heaton. “The Impact of Estrogens and Their Receptors on Immunity and Inflammation during Infection.” Cancers (Basel) 14, no. 4 (February 12, 2022). https://doi.org/10.3390/cancers14040909.
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    • Froggatt, Heather M., Kaitlyn N. Burke, Ryan R. Chaparian, Hector A. Miranda, Xinyu Zhu, Benjamin S. Chambers, and Nicholas S. Heaton. “Influenza A virus segments five and six can harbor artificial introns allowing expanded coding capacity.” Plos Pathog 17, no. 9 (September 2021): e1009951. https://doi.org/10.1371/journal.ppat.1009951.
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    • Drayman, Nir, Jennifer K. DeMarco, Krysten A. Jones, Saara-Anne Azizi, Heather M. Froggatt, Kemin Tan, Natalia Ivanovna Maltseva, et al. “Masitinib is a broad coronavirus 3CL inhibitor that blocks replication of SARS-CoV-2.” Science 373, no. 6557 (August 20, 2021): 931–36. https://doi.org/10.1126/science.abg5827.
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    • Froggatt, Heather M., Alfred T. Harding, Ryan R. Chaparian, and Nicholas S. Heaton. “ETV7 limits antiviral gene expression and control of influenza viruses.” Sci Signal 14, no. 691 (July 13, 2021). https://doi.org/10.1126/scisignal.abe1194.
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    • Trimarco, Joseph D., Brook E. Heaton, Ryan R. Chaparian, Kaitlyn N. Burke, Raquel A. Binder, Gregory C. Gray, Clare M. Smith, Vineet D. Menachery, and Nicholas S. Heaton. “TMEM41B is a host factor required for the replication of diverse coronaviruses including SARS-CoV-2.” Plos Pathogens 17, no. 5 (May 2021): e1009599. https://doi.org/10.1371/journal.ppat.1009599.
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    • Luo, Zhaochen, Alanson W. Girton, Brook E. Heaton, and Nicholas S. Heaton. “Engineered influenza virions reveal the contributions of non-hemagglutinin structural proteins to vaccine mediated protection.” J Virol 95, no. 10 (March 3, 2021). https://doi.org/10.1128/JVI.02021-20.
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    • Harding, Alfred T., Marisa A. Goff, Heather M. Froggatt, Jean K. Lim, and Nicholas S. Heaton. “GPER1 is required to protect fetal health from maternal inflammation.” Science 371, no. 6526 (January 15, 2021): 271–76. https://doi.org/10.1126/science.aba9001.
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    • Katsura, Hiroaki, Vishwaraj Sontake, Aleksandra Tata, Yoshihiko Kobayashi, Caitlin E. Edwards, Brook E. Heaton, Arvind Konkimalla, et al. “Human Lung Stem Cell-Based Alveolospheres Provide Insights into SARS-CoV-2-Mediated Interferon Responses and Pneumocyte Dysfunction.” Cell Stem Cell 27, no. 6 (December 3, 2020): 890-904.e8. https://doi.org/10.1016/j.stem.2020.10.005.
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    • Froggatt, Heather M., Brook E. Heaton, and Nicholas S. Heaton. “Development of a Fluorescence-Based, High-Throughput SARS-CoV-2 3CLpro Reporter Assay.” J Virol 94, no. 22 (October 27, 2020). https://doi.org/10.1128/JVI.01265-20.
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    • Dumm, Rebekah E., Sebastian A. Wellford, E Ashley Moseman, and Nicholas S. Heaton. “Heterogeneity of Antiviral Responses in the Upper Respiratory Tract Mediates Differential Non-lytic Clearance of Influenza Viruses.” Cell Rep 32, no. 9 (September 1, 2020): 108103. https://doi.org/10.1016/j.celrep.2020.108103.
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    • Abbott, Timothy R., Girija Dhamdhere, Yanxia Liu, Xueqiu Lin, Laine Goudy, Leiping Zeng, Augustine Chemparathy, et al. “Development of CRISPR as an Antiviral Strategy to Combat SARS-CoV-2 and Influenza.” Cell 181, no. 4 (May 14, 2020): 865-876.e12. https://doi.org/10.1016/j.cell.2020.04.020.
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    • Harding, Alfred T., Griffin D. Haas, Benjamin S. Chambers, and Nicholas S. Heaton. “Influenza viruses that require 10 genomic segments as antiviral therapeutics.” Plos Pathog 15, no. 11 (November 2019): e1008098. https://doi.org/10.1371/journal.ppat.1008098.
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    • Chambers, Benjamin S., Brook E. Heaton, Keiko Rausch, Rebekah E. Dumm, Jennifer R. Hamilton, Sara Cherry, and Nicholas S. Heaton. “DNA mismatch repair is required for the host innate response and controls cellular fate after influenza virus infection.” Nat Microbiol 4, no. 11 (November 2019): 1964–77. https://doi.org/10.1038/s41564-019-0509-3.
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    • Fiege, Jessica K., Ian A. Stone, Rebekah E. Dumm, Barbara M. Waring, Brian T. Fife, Judith Agudo, Brian D. Brown, Nicholas S. Heaton, and Ryan A. Langlois. “Long-term surviving influenza infected cells evade CD8+ T cell mediated clearance.” Plos Pathog 15, no. 9 (September 2019): e1008077. https://doi.org/10.1371/journal.ppat.1008077.
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    • Dumm, Rebekah E., and Nicholas S. Heaton. “The Development and Use of Reporter Influenza B Viruses.” Viruses 11, no. 8 (August 9, 2019). https://doi.org/10.3390/v11080736.
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    • Dumm, Rebekah E., Jessica K. Fiege, Barbara M. Waring, Chay T. Kuo, Ryan A. Langlois, and Nicholas S. Heaton. “Non-lytic clearance of influenza B virus from infected cells preserves epithelial barrier function.” Nat Commun 10, no. 1 (February 15, 2019): 779. https://doi.org/10.1038/s41467-019-08617-z.
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    • Fulton, Benjamin O., Weina Sun, Nicholas S. Heaton, and Peter Palese. “The Influenza B Virus Hemagglutinin Head Domain Is Less Tolerant to Transposon Mutagenesis than That of the Influenza A Virus.” J Virol 92, no. 16 (August 15, 2018). https://doi.org/10.1128/JVI.00754-18.
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    • Harding, Alfred T., and Nicholas S. Heaton. “Efforts to Improve the Seasonal Influenza Vaccine.” Vaccines (Basel) 6, no. 2 (March 30, 2018). https://doi.org/10.3390/vaccines6020019.
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    • Heaton, Nicholas S., and Bryan R. Cullen. “Viruses hijack a long non-coding RNA.” Nature 552, no. 7684 (December 14, 2017): 184–85. https://doi.org/10.1038/d41586-017-07692-w.
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    • Courtney, David G., Edward M. Kennedy, Rebekah E. Dumm, Hal P. Bogerd, Kevin Tsai, Nicholas S. Heaton, and Bryan R. Cullen. “Epitranscriptomic Enhancement of Influenza A Virus Gene Expression and Replication.” Cell Host Microbe 22, no. 3 (September 13, 2017): 377-386.e5. https://doi.org/10.1016/j.chom.2017.08.004.
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    • Heaton, Brook E., Edward M. Kennedy, Rebekah E. Dumm, Alfred T. Harding, Matthew T. Sacco, David Sachs, and Nicholas S. Heaton. “A CRISPR Activation Screen Identifies a Pan-avian Influenza Virus Inhibitory Host Factor.” Cell Rep 20, no. 7 (August 15, 2017): 1503–12. https://doi.org/10.1016/j.celrep.2017.07.060.
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    • Heaton, Nicholas S. “Revisiting the concept of a cytopathic viral infection.” Plos Pathog 13, no. 7 (July 2017): e1006409. https://doi.org/10.1371/journal.ppat.1006409.
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    • Harding, Alfred T., Brook E. Heaton, Rebekah E. Dumm, and Nicholas S. Heaton. “Rationally Designed Influenza Virus Vaccines That Are Antigenically Stable during Growth in Eggs.” Mbio 8, no. 3 (June 6, 2017). https://doi.org/10.1128/mBio.00669-17.
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    • Hamilton, Jennifer R., David Sachs, Jean K. Lim, Ryan A. Langlois, Peter Palese, and Nicholas S. Heaton. “Club cells surviving influenza A virus infection induce temporary nonspecific antiviral immunity.” Proc Natl Acad Sci U S A 113, no. 14 (April 5, 2016): 3861–66. https://doi.org/10.1073/pnas.1522376113.
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    • Heaton, N. S., N. Moshkina, R. Fenouil, T. J. Gardner, S. Aguirre, P. S. Shah, N. Zhao, et al. “Corrections to Targeting Viral Proteostasis Limits Influenza Virus, HIV, and Dengue Virus Infection. (Immunity 44, 46-58, January 19, 2016).” Immunity 44, no. 2 (February 16, 2016): 438. https://doi.org/10.1016/j.immuni.2016.01.016.
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    • Heaton, Nicholas S., Natasha Moshkina, Romain Fenouil, Thomas J. Gardner, Sebastian Aguirre, Priya S. Shah, Nan Zhao, et al. “Targeting Viral Proteostasis Limits Influenza Virus, HIV, and Dengue Virus Infection.” Immunity 44, no. 1 (January 19, 2016): 46–58. https://doi.org/10.1016/j.immuni.2015.12.017.
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    • Fulton, Benjamin O., Peter Palese, and Nicholas S. Heaton. “Replication-Competent Influenza B Reporter Viruses as Tools for Screening Antivirals and Antibodies.” J Virol 89, no. 23 (December 2015): 12226–31. https://doi.org/10.1128/JVI.02164-15.
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    • Fulton, Benjamin O., David Sachs, Shannon M. Beaty, Sohui T. Won, Benhur Lee, Peter Palese, and Nicholas S. Heaton. “Mutational Analysis of Measles Virus Suggests Constraints on Antigenic Variation of the Glycoproteins.” Cell Rep 11, no. 9 (June 9, 2015): 1331–38. https://doi.org/10.1016/j.celrep.2015.04.054.
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    • Heaton, Nicholas S., Ryan A. Langlois, David Sachs, Jean K. Lim, Peter Palese, and Benjamin R. tenOever. “Long-term survival of influenza virus infected club cells drives immunopathology.” J Exp Med 211, no. 9 (August 25, 2014): 1707–14. https://doi.org/10.1084/jem.20140488.
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    • Heaton, Nicholas S., David Sachs, Chi-Jene Chen, Rong Hai, and Peter Palese. “Genome-wide mutagenesis of influenza virus reveals unique plasticity of the hemagglutinin and NS1 proteins.” Proc Natl Acad Sci U S A 110, no. 50 (December 10, 2013): 20248–53. https://doi.org/10.1073/pnas.1320524110.
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    • Dolan, Patrick T., Chaoying Zhang, Sudip Khadka, Vaithilingaraja Arumugaswami, Abbey D. Vangeloff, Nicholas S. Heaton, Sudhir Sahasrabudhe, Glenn Randall, Ren Sun, and Douglas J. LaCount. “Identification and comparative analysis of hepatitis C virus-host cell protein interactions.” Mol Biosyst 9, no. 12 (December 2013): 3199–3209. https://doi.org/10.1039/c3mb70343f.
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    • Margine, I., F. Krammer, R. Hai, N. S. Heaton, G. S. Tan, S. A. Andrews, J. A. Runstadler, et al. “Hemagglutinin stalk-based universal vaccine constructs protect against group 2 influenza A viruses.” J Virol 87, no. 19 (October 2013): 10435–46. https://doi.org/10.1128/JVI.01715-13.
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    • Heaton, Nicholas S., Victor H. Leyva-Grado, Gene S. Tan, Dirk Eggink, Rong Hai, and Peter Palese. “In vivo bioluminescent imaging of influenza a virus infection and characterization of novel cross-protective monoclonal antibodies.” J Virol 87, no. 15 (August 2013): 8272–81. https://doi.org/10.1128/JVI.00969-13.
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    • Chou, Yi-ying, Nicholas S. Heaton, Qinshan Gao, Peter Palese, Robert H. Singer, and Timothée Lionnet. “Colocalization of different influenza viral RNA segments in the cytoplasm before viral budding as shown by single-molecule sensitivity FISH analysis.” Plos Pathog 9, no. 5 (2013): e1003358. https://doi.org/10.1371/journal.ppat.1003358.
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    • Chukkapalli, Vineela, Nicholas S. Heaton, and Glenn Randall. “Lipids at the interface of virus-host interactions.” Curr Opin Microbiol 15, no. 4 (August 2012): 512–18. https://doi.org/10.1016/j.mib.2012.05.013.
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    • Coller, Kelly E., Nicholas S. Heaton, Kristi L. Berger, Jacob D. Cooper, Jessica L. Saunders, and Glenn Randall. “Molecular determinants and dynamics of hepatitis C virus secretion.” Plos Pathog 8, no. 1 (January 2012): e1002466. https://doi.org/10.1371/journal.ppat.1002466.
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    • Khadka, Sudip, Abbey D. Vangeloff, Chaoying Zhang, Prasad Siddavatam, Nicholas S. Heaton, Ling Wang, Ranjan Sengupta, et al. “A physical interaction network of dengue virus and human proteins.” Mol Cell Proteomics 10, no. 12 (December 2011): M111.012187. https://doi.org/10.1074/mcp.M111.012187.
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    • Heaton, Nicholas S., and Glenn Randall. “Dengue virus and autophagy.” Viruses 3, no. 8 (August 2011): 1332–41. https://doi.org/10.3390/v3081332.
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    • Heaton, Nicholas S., and Glenn Randall. “Multifaceted roles for lipids in viral infection.” Trends Microbiol 19, no. 7 (July 2011): 368–75. https://doi.org/10.1016/j.tim.2011.03.007.
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    • Heaton, Nicholas S., and Glenn Randall. “Dengue virus-induced autophagy regulates lipid metabolism.” Cell Host Microbe 8, no. 5 (November 18, 2010): 422–32. https://doi.org/10.1016/j.chom.2010.10.006.
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    • Heaton, Nicholas S., Rushika Perera, Kristi L. Berger, Sudip Khadka, Douglas J. Lacount, Richard J. Kuhn, and Glenn Randall. “Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis.” Proc Natl Acad Sci U S A 107, no. 40 (October 5, 2010): 17345–50. https://doi.org/10.1073/pnas.1010811107.
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    • Coller, Kelly E., Kristi L. Berger, Nicholas S. Heaton, Jacob D. Cooper, Rosa Yoon, and Glenn Randall. “RNA interference and single particle tracking analysis of hepatitis C virus endocytosis.” Plos Pathog 5, no. 12 (December 2009): e1000702. https://doi.org/10.1371/journal.ppat.1000702.
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    • Berger, Kristi L., Jacob D. Cooper, Nicholas S. Heaton, Rosa Yoon, Todd E. Oakland, Tristan X. Jordan, Guaniri Mateu, Arash Grakoui, and Glenn Randall. “Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication.” Proc Natl Acad Sci U S A 106, no. 18 (May 5, 2009): 7577–82. https://doi.org/10.1073/pnas.0902693106.
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    • Heaton, Nicholas S., Randal A. Wolff, Rita L. Malinowski, Debra A. Hullett, and John R. Hoch. “Antisense to transforming growth factor-beta(1) facilitates the apoptosis of macrophages in rat vein grafts.” J Vasc Res 45, no. 5 (2008): 365–74. https://doi.org/10.1159/000121406.
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    • Wolff, Randal A., Rita L. Malinowski, Nicholas S. Heaton, Debra A. Hullett, and John R. Hoch. “Transforming growth factor-beta1 antisense treatment of rat vein grafts reduces the accumulation of collagen and increases the accumulation of h-caldesmon.” J Vasc Surg 43, no. 5 (May 2006): 1028–36. https://doi.org/10.1016/j.jvs.2006.01.016.
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  • Journal Issues

    • Yang, Shigao, Alfred T. Harding, Catherine Sweeney, David Miao, Gregory Swan, Connie Zhou, Zhaozhao Jiang, et al. “Control of antiviral innate immune response by protein geranylgeranylation.” Sci Adv, May 2019. https://doi.org/10.1126/sciadv.aav7999.
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• Teaching & Mentoring
• 

  Recent Courses

  • MGM 701: Foundations of Molecular Genetics and Microbiology 2023
  • MGM 593: Research Independent Study 2022
  • MGM 701: Foundations of Molecular Genetics and Microbiology 2022
  • MGM 593: Research Independent Study 2021
  • MGM 701: Foundations of Molecular Genetics and Microbiology 2021

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