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SARS-CoV-2 ferritin nanoparticle vaccines elicit broad SARS coronavirus immunogenicity

M. Gordon Joyce, Wei-Hung Chen, Rajeshwer S. Sankhala, Agnes Hajduczki, Paul V. Thomas, Misook Choe, William Chang, Caroline E. Peterson, Elizabeth Martinez, Elaine B. Morrison, Clayton Smith, Aslaa Ahmed, Lindsay Wieczorek, Alexander Anderson, Rita E. Chen, James Brett Case, Yifan Li, Therese Oertel, Lorean Rosado, Akshaya Ganesh, Connor Whalen, Joshua M. Carmen, Letzibeth Mendez-Rivera, Christopher Karch, Neelakshi Gohain, Zuzana Villar, David McCurdy, Zoltan Beck, Jiae Kim, Shikha Shrivastava, Ousman Jobe, Vincent Dussupt, Sebastian Molnar, Ursula Tran, Chandrika B. Kannadka, Michelle Zemil, Htet Khanh, Weimin Wu, Matthew A. Cole, Debra K. Duso, Larry W. Kummer, Tricia J. Lang, Shania E. Muncil, Jeffrey R. Currier, Shelly J. Krebs, Victoria R. Polonis, Saravanan Rajan, Patrick M. McTamney, Mark T. Esser, William W. Reiley, Morgane Rolland, Natalia de Val, Michael S. Diamond, Gregory D. Gromowski, Gary R. Matyas, Mangala Rao, Nelson L. Michael, Kayvon Modjarrad
doi: https://doi.org/10.1101/2021.05.09.443331
M. Gordon Joyce
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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  • For correspondence: gjoyce@eidresearch.org kayvon.modjarrad.civ@mail.mil
Wei-Hung Chen
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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Rajeshwer S. Sankhala
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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Agnes Hajduczki
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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Paul V. Thomas
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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Misook Choe
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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William Chang
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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Caroline E. Peterson
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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Elizabeth Martinez
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
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Elaine B. Morrison
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Clayton Smith
5Center for Molecular Microscopy, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Frederick, MD, USA
6Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, USA
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Aslaa Ahmed
7Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Lindsay Wieczorek
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Alexander Anderson
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Rita E. Chen
3Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Pathology & Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110, USA; The Andrew M. and Jane M. Bursky Center for Human Immunology & Immunotherapy Programs, Washington University School of Medicine, St. Louis, MO 63110, USA
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James Brett Case
3Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Pathology & Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110, USA; The Andrew M. and Jane M. Bursky Center for Human Immunology & Immunotherapy Programs, Washington University School of Medicine, St. Louis, MO 63110, USA
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Yifan Li
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Therese Oertel
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Lorean Rosado
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Akshaya Ganesh
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Connor Whalen
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Joshua M. Carmen
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Letzibeth Mendez-Rivera
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Christopher Karch
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Neelakshi Gohain
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Zuzana Villar
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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David McCurdy
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Zoltan Beck
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Jiae Kim
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Shikha Shrivastava
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Ousman Jobe
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Vincent Dussupt
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Sebastian Molnar
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Ursula Tran
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Chandrika B. Kannadka
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Michelle Zemil
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Htet Khanh
5Center for Molecular Microscopy, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Frederick, MD, USA
6Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, USA
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Weimin Wu
5Center for Molecular Microscopy, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Frederick, MD, USA
6Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, USA
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Matthew A. Cole
8Trudeau Institute, Inc., Saranac Lake, NY, USA
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Debra K. Duso
8Trudeau Institute, Inc., Saranac Lake, NY, USA
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Larry W. Kummer
8Trudeau Institute, Inc., Saranac Lake, NY, USA
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Tricia J. Lang
8Trudeau Institute, Inc., Saranac Lake, NY, USA
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Shania E. Muncil
8Trudeau Institute, Inc., Saranac Lake, NY, USA
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Jeffrey R. Currier
7Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Shelly J. Krebs
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Victoria R. Polonis
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Saravanan Rajan
9Antibody Discovery and Protein Engineering (ADPE), BioPharmaceuticals R&D, AstraZeneca, Gaithersburg, USA
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Patrick M. McTamney
10Microbial Sciences, BioPharmaceuticals R&D, AstraZeneca, Gaithersburg, MD, USA
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Mark T. Esser
10Microbial Sciences, BioPharmaceuticals R&D, AstraZeneca, Gaithersburg, MD, USA
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William W. Reiley
8Trudeau Institute, Inc., Saranac Lake, NY, USA
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Morgane Rolland
2Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Natalia de Val
5Center for Molecular Microscopy, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Frederick, MD, USA
6Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD, USA
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Michael S. Diamond
3Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Pathology & Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110, USA; The Andrew M. and Jane M. Bursky Center for Human Immunology & Immunotherapy Programs, Washington University School of Medicine, St. Louis, MO 63110, USA
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Gregory D. Gromowski
7Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Gary R. Matyas
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Mangala Rao
4U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Nelson L. Michael
11Center for Infectious Diseases Research, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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Kayvon Modjarrad
1Emerging Infectious Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
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  • For correspondence: gjoyce@eidresearch.org kayvon.modjarrad.civ@mail.mil
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SUMMARY

The need for SARS-CoV-2 next-generation vaccines has been highlighted by the rise of variants of concern (VoC) and the long-term threat of other coronaviruses. Here, we designed and characterized four categories of engineered nanoparticle immunogens that recapitulate the structural and antigenic properties of prefusion Spike (S), S1 and RBD. These immunogens induced robust S-binding, ACE2-inhibition, and authentic and pseudovirus neutralizing antibodies against SARS-CoV-2 in mice. A Spike-ferritin nanoparticle (SpFN) vaccine elicited neutralizing titers more than 20-fold higher than convalescent donor serum, following a single immunization, while RBD-Ferritin nanoparticle (RFN) immunogens elicited similar responses after two immunizations. Passive transfer of IgG purified from SpFN- or RFN-immunized mice protected K18-hACE2 transgenic mice from a lethal SARS-CoV-2 virus challenge. Furthermore, SpFN- and RFN-immunization elicited ACE2 blocking activity and neutralizing ID50 antibody titers >2,000 against SARS-CoV-1, along with high magnitude neutralizing titers against major VoC. These results provide design strategies for pan-coronavirus vaccine development.

HIGHLIGHTS

  • Iterative structure-based design of four Spike-domain Ferritin nanoparticle classes of immunogens

  • SpFN-ALFQ and RFN-ALFQ immunization elicits potent neutralizing activity against SARS-CoV-2, variants of concern, and SARS-CoV-1

  • Passively transferred IgG from immunized C57BL/6 mice protects K18-hACE2 mice from lethal SARS-CoV-2 challenge

Competing Interest Statement

M.G.J. and K.M. are named as inventors on International Patent Application No. WO/2021/21405 entitled Vaccines against SARS-CoV-2 and other coronaviruses. M.G.J. is named as an inventor on International Patent Application No. WO/2018/081318 and U.S. patent 10,960,070 entitled Prefusion Coronavirus Spike Proteins and Their Use. Z.B. is named as an inventor on U.S. patent 10,434,167 entitled Non-toxic adjuvant formulation comprising a monophosphoryl lipid A (MPLA)-containing liposome composition and a saponin. Z.B. and G.R.M are named inventors on Compositions And Methods For Vaccine Delivery, US Patent Application: 16/607,917. M.S.D. is a consultant for Inbios, Vir Biotechnology, NGM Biopharmaceuticals and Carnival Corporation and on the Scientific Advisory Boards of Moderna and Immunome. The Diamond laboratory has received funding support in sponsored research agreements from Moderna, Vir Biotechnology and Emergent BioSolutions. S.R., P.M.M., and M.T.E. are employees of AstraZeneca and currently hold AstraZeneca stock or stock options. Zoltan Beck is currently employed at Pfizer.

Footnotes

  • ↵12 Lead contact

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license.
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SARS-CoV-2 ferritin nanoparticle vaccines elicit broad SARS coronavirus immunogenicity
M. Gordon Joyce, Wei-Hung Chen, Rajeshwer S. Sankhala, Agnes Hajduczki, Paul V. Thomas, Misook Choe, William Chang, Caroline E. Peterson, Elizabeth Martinez, Elaine B. Morrison, Clayton Smith, Aslaa Ahmed, Lindsay Wieczorek, Alexander Anderson, Rita E. Chen, James Brett Case, Yifan Li, Therese Oertel, Lorean Rosado, Akshaya Ganesh, Connor Whalen, Joshua M. Carmen, Letzibeth Mendez-Rivera, Christopher Karch, Neelakshi Gohain, Zuzana Villar, David McCurdy, Zoltan Beck, Jiae Kim, Shikha Shrivastava, Ousman Jobe, Vincent Dussupt, Sebastian Molnar, Ursula Tran, Chandrika B. Kannadka, Michelle Zemil, Htet Khanh, Weimin Wu, Matthew A. Cole, Debra K. Duso, Larry W. Kummer, Tricia J. Lang, Shania E. Muncil, Jeffrey R. Currier, Shelly J. Krebs, Victoria R. Polonis, Saravanan Rajan, Patrick M. McTamney, Mark T. Esser, William W. Reiley, Morgane Rolland, Natalia de Val, Michael S. Diamond, Gregory D. Gromowski, Gary R. Matyas, Mangala Rao, Nelson L. Michael, Kayvon Modjarrad
bioRxiv 2021.05.09.443331; doi: https://doi.org/10.1101/2021.05.09.443331
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SARS-CoV-2 ferritin nanoparticle vaccines elicit broad SARS coronavirus immunogenicity
M. Gordon Joyce, Wei-Hung Chen, Rajeshwer S. Sankhala, Agnes Hajduczki, Paul V. Thomas, Misook Choe, William Chang, Caroline E. Peterson, Elizabeth Martinez, Elaine B. Morrison, Clayton Smith, Aslaa Ahmed, Lindsay Wieczorek, Alexander Anderson, Rita E. Chen, James Brett Case, Yifan Li, Therese Oertel, Lorean Rosado, Akshaya Ganesh, Connor Whalen, Joshua M. Carmen, Letzibeth Mendez-Rivera, Christopher Karch, Neelakshi Gohain, Zuzana Villar, David McCurdy, Zoltan Beck, Jiae Kim, Shikha Shrivastava, Ousman Jobe, Vincent Dussupt, Sebastian Molnar, Ursula Tran, Chandrika B. Kannadka, Michelle Zemil, Htet Khanh, Weimin Wu, Matthew A. Cole, Debra K. Duso, Larry W. Kummer, Tricia J. Lang, Shania E. Muncil, Jeffrey R. Currier, Shelly J. Krebs, Victoria R. Polonis, Saravanan Rajan, Patrick M. McTamney, Mark T. Esser, William W. Reiley, Morgane Rolland, Natalia de Val, Michael S. Diamond, Gregory D. Gromowski, Gary R. Matyas, Mangala Rao, Nelson L. Michael, Kayvon Modjarrad
bioRxiv 2021.05.09.443331; doi: https://doi.org/10.1101/2021.05.09.443331

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