UC San Diego School of Biological Sciences
Department of Molecular Biology

Publications

Preprinted Articles

  1. Wong MP, Juan EYW, Chelluri SS, Wang P, Pahmeier F, Castillo-Rojas B, Blanc SF, Biering SB, Vance RE, Harris E. The Inflammasome Pathway is Activated by Dengue Virus Non-structural Protein 1 and is Protective During Dengue Virus Infection. bioRxiv [Preprint]. 2023 Sep 21:2023.09.21.558875. doi: 10.1101/2023.09.21.558875. PMID: 37790301; PMCID: PMC10543007.
  1. de Sousa FTG, Warnes CM, Manuli ER, Ng A, D’Elia Zanella LGFAB, Ho YL, Bhat S, Romano CM, Beatty PR, Biering SB, Kallas EG, Sabino EC, Harris E. Yellow fever disease severity and endothelial dysfunction are associated with elevated serum levels of viral NS1 protein and syndecan-1. medRxiv [Preprint]. 2023 Jun 30:2023.06.29.23292053. doi: 10.1101/2023.06.29.23292053. PMID: 37425955; PMCID: PMC10327263.

Postdoctoral Scholar

COVID-19

  1. Wei J, Alfajaro MM, Cai WL, Graziano VR, Strine MS, Filler RB, Biering SB, Sarnik SA, Patel S, Menasche BL, Konermann S, Hsu PD, Orchard RC, Yan Q, Wilen CB. The KDM6A-KMT2D-p300 axis regulates susceptibility to diverse coronaviruses by mediating viral receptor expression. PLoS Pathog. 2023;19(7):e1011351. DOI: 10.1371/journal.ppat.1011351

 2. Strine MS, Cai WL, Wei J, Alfajaro MM, Filler RB, Biering SB, Sarnik S, Patil A, Cervantes KS, Collings CK, DeWeirdt PC, Hanna RE, Schofield K, Hulme C, Konermann S, Doench JG, Hsu PD, Kadoch C, Yan Q, Wilen CB. DYRK1A promotes viral entry of highly pathogenic human coronaviruses in a kinase-independent manner. PLoS Biol. 2023;21(6):e3002097. DOI: 10.1371/journal.pbio.3002097

  1. Biering SB* †, Tramontini FGdS*, Tjang LV, Pahmeier F, Zhu C, Ruan R, Blanc SF, Patel TS, Worthington CM, Glasner DR, Castillo-Rojas B, Servellita V, Lo NTN, Wong MP, Warnes CM, Sandoval DR, Clausen TM, Santos YA, Fox DM, Ortega V, Näär AM, Baric RS, Stanley SA, Aguilar HC, Esko JD, Chiu CY, Pak JE, Beatty PR, Harris E†. SARS-CoV-2 Spike triggers barrier dysfunction and vascular leak via integrins and TGFβ signaling. Nat Commun.13, 7630 (2022). https://doi.org/10.1038/s41467-022-34910-5 (*equal contribution, †co-corresponding)
    1. UC Berkeley article on this study
  1. Nguyenla X*, Wehri E*, Van Dis E*, Biering SB*, Yamashiro LH*, Stroumza J, Dugast-Darzacq C, Graham T, Stanley S, and Schaletzky J. Discovery of SARS-CoV-2 antiviral synergy between remdesivir and approved drugs in human lung cells. Rep.12, 18506 (2022). https://doi.org/10.1038/s41598-022-21034-5 (*equal contribution)
  1. Wagoner J, Herring S, Hsiang TY, Ianevski A, Biering SB, Xu S, Hoffmann M, Pöhlmann S, Gale Jr. M, Aittokallio T, Schiffer JT, White JM, Polyak SJ. Combinations of virus- and host-targeting antiviral drugs confer synergistic suppression of SARS-CoV-2. Spectr. 2022 Oct 26;10(5):e0333122. doi: 10.1128/spectrum.03331-22
  1. Chandrasekaran SS, Agrawal S, Fanton A, Jangid AR, Charrez B, Escajeda AM, Son S, Mcintosh R, Tran H, Bhuiya A, de León Derby MD, Switz NA, Armstrong M, Harris AR, Prywes N, Lukarska M, Biering SB, Smock DCJ, Mok A, Knott GJ, Dang Q, Van Dis E, Dugan E, Kim S, Liu TY; IGI Testing Consortium, Moehle EA, Kogut K, Eskenazi B, Harris E, Stanley SA, Lareau LF, Tan MX, Fletcher DA, Doudna JA, Savage DF, Hsu PD. Rapid detection of SARS-CoV-2 RNA in saliva via Cas13. Nat Biomed Eng. 2022 Aug 11. doi: 10.1038/s41551-022-00917-y.
  1. Zhu C, Lee JY, Woo JZ, Xu L, Nguyenla X, Yamashiro LH, Ji F, Biering SB, Van Dis E, Gonzalez F, Fox D, Wehri E, Rustagi A, Pinsky BA, Schaletzky J, Blish CA, Chiu C, Harris E, Sadreyev RI, Stanley S, Kauppinen S, Rouskin S, Näär AM. An intranasal ASO therapeutic targeting SARS-CoV-2. Nat Commun. 2022 Aug 3;13(1):4503. doi: 10.1038/s41467-022-32216-0.
  1. Biering SB, Sarnik SA, Wang E, Zengel JR, Leist SR, Schäfer A, Sathyan V, Hawkins P, Okuda K, Tau C, Jangid AR, Duffy CV, Wei J, Gilmore RC, Alfajaro MM, Strine MS, Nguyenla X, Van Dis E, Catamura C, Yamashiro LH, Belk JA, Begeman A, Stark JC, Shon DJ, Fox DM, Ezzatpour S, Huang E, Olegario N, Rustagi A, Volmer AS, Livraghi-Butrico A, Wehri E, Behringer RR, Cheon DJ, Schaletzky J, Aguilar HC, Puschnik AS, Button B, Pinsky BA, Blish CA, Baric RS, O’Neal WK, Bertozzi CR, Wilen CB, Boucher RC, Carette JE, Stanley SA, Harris E, Konermann S, Hsu PD. Genome-wide bidirectional CRISPR screens identify mucins as host factors modulating SARS-CoV-2 infection. Nat Genet. 2022 Aug;54(8):1078-1089. doi: 10.1038/s41588-022-01131-x.
    1. UC Berkeley article on this study
    2. ARC Institute article on this study
    3. Forbes article on this study
  1. Golovkine GR, Roberts AW, Cooper C, Riano S, DiCiccio AM, Worthington DL, Clarkson JP, Krames M, Zhang J, Gao Y, Zhou L, Biering SB, Stanley SA. Practical considerations for Ultraviolet-C radiation mediated decontamination of N95 respirator against SARS-CoV-2 virus. PLoS One. 2021 Oct 12;16(10):e0258336. doi: 10.1371/journal.pone.0258336.
  1. Biering SB, Van Dis E, Wehri E, Yamashiro LH, Nguyenla X, Dugast-Darzacq C, Graham TGW, Stroumza JR, Golovkine GR, Roberts AW, Fines DM, Spradlin JN, Ward CC, Bajaj T, Dovala D, Schulze-Gamen U, Bajaj R, Fox DM, Ott M, Murthy N, Nomura DK, Schaletzky J, Stanley SA. Screening a Library of FDA-Approved and Bioactive Compounds for Antiviral Activity against SARS-CoV-2. ACS Infect Dis. 2021 Aug 13;7(8):2337-2351. doi: 10.1021/acsinfecdis.1c00017.

Flavivirus

  1. Lo NTN, Roodsari S, Tin NR, Biering SB†, Harris E†. Molecular determinants of tissue specificity of flavivirus nonstructural protein 1 interaction with endothelial cells. Virol. 2022 Oct 12;96(19):e0066122. doi: 10.1128/jvi.00661-22. (†co-corresponding)
  1. Puerta-Guardo H, Biering SB, de Sousa FTG, Shu J, Glasner DR, Li J, Blanc SF, Beatty PR, Harris E. Flavivirus NS1 Triggers Tissue-Specific Disassembly of Intercellular Junctions Leading to Barrier Dysfunction and Vascular Leak in a GSK-3β-Dependent Manner. Pathogens. 2022 May 24;11(6):615. doi: 10.3390/pathogens11060615.
  1. Benfrid S, Park KH, Dellarole M, Voss JE, Tamietti C, Pehau-Arnaudet G, Raynal B, Brûlé S, England P, Zhang X, Mikhailova A, Hasan M, Ungeheuer MN, Petres S, Biering SB, Harris E, Sakuntabhai A, Buchy P, Duong V, Dussart P, Coulibaly F, Bontems F, Rey FA, Flamand M. Dengue virus NS1 protein conveys pro-inflammatory signals by docking onto high-density lipoproteins. EMBO Rep. 2022 Jul 5;23(7):e53600. doi: 10.15252/embr.202153600.
  1. Sousa FTG, Biering SB, Patel TS, Blanc SF, Camelini CM, Venzke D, Nunes RJ, Romano CM, Beatty PR, Sabino EC, Harris E. Sulfated β-glucan from Agaricus subrufescens inhibits flavivirus infection and nonstructural protein 1-mediated pathogenesis. Antiviral Res. 2022 Jul;203:105330. doi: 10.1016/j.antiviral.2022.105330.
  1. Biering SB. One antibody to treat them all. Science. 2022 Feb 25;375(6583):803. doi: 10.1126/science.abn9651.
    1. Prize Essay for the Inaugural Michelson Philanthropies and Science Prize for Immunology
      1. Article about the prize winners
      2. Video about the prize
  1. Biering SB, Harris E. A step towards therapeutics for dengue. Nature. 2021 Oct;598(7881):420-421. doi: 10.1038/d41586-021-02638-9. PMID: 34616083.
  1. Riva L, Goellner S, Biering SB, Huang CT, Rubanov AN, Haselmann U, Warnes CM, De Jesus PD, Martin-Sancho L, Terskikh AV, Harris E, Pinkerton AB, Bartenschlager R, Chanda SK. The Compound SBI-0090799 Inhibits Zika Virus Infection by Blocking De NovoFormation of the Membranous Replication Compartment. J Virol. 2021 Oct 27;95(22):e0099621. doi: 10.1128/JVI.00996-21.
  1. Wessel AW, Dowd KA, Biering SB, Zhang P, Edeling MA, Nelson CA, Funk KE, DeMaso CR, Klein RS, Smith JL, Cao TM, Kuhn RJ, Fremont DH, Harris E, Pierson TC, Diamond MS. Levels of Circulating NS1 Impact West Nile Virus Spread to the Brain. J Virol. 2021 Sep 27;95(20):e0084421. doi: 10.1128/JVI.00844-21.
  1. Haymet AB, Bartnikowski N, Wood ES, Vallely MP, McBride A, Yacoub S, Biering SB, Harris E, Suen JY, Fraser JF. Studying the Endothelial Glycocalyx in vitro: What Is Missing? Front Cardiovasc Med. 2021 Apr 14;8:647086. doi: 10.3389/fcvm.2021.647086.
  1. Biering SB, Akey DL, Wong MP, Brown WC, Lo NTN, Puerta-Guardo H, Tramontini Gomes de Sousa F, Wang C, Konwerski JR, Espinosa DA, Bockhaus NJ, Glasner DR, Li J, Blanc SF, Juan EY, Elledge SJ, Mina MJ, Beatty PR, Smith JL, Harris E. Structural basis for antibody inhibition of flavivirus NS1-triggered endothelial dysfunction. Science. 2021 Jan 8;371(6525):194-200. doi: 10.1126/science.abc0476.
    1. Featured on This Week in Virology (TWiV)
    2. Featured by the UC Berkeley School of Public Health
  1. O’Donnell KL, Espinosa DA, Puerta-Guardo H, Biering SB, Warnes CM, Schiltz J, Nilles ML, Li J, Harris E, Bradley DS. Avian anti-NS1 IgY antibodies neutralize dengue virus infection and protect against lethal dengue virus challenge. Antiviral Res. 2020 Nov;183:104923. doi: 10.1016/j.antiviral.2020.104923.
  1. Young E, Carnahan RH, Andrade DV, Kose N, Nargi RS, Fritch EJ, Munt JE, Doyle MP, White L, Baric TJ, Stoops M, DeSilva A, Tse LV, Martinez DR, Zhu D, Metz S, Wong MP, Espinosa DA, Montoya M, Biering SB, Sukulpolvi-Petty S, Kuan G, Balmaseda A, Diamond MS, Harris E, Crowe JE Jr, Baric RS. Identification of Dengue Virus Serotype 3 Specific Antigenic Sites Targeted by Neutralizing Human Antibodies. Cell Host Microbe. 2020 May 13;27(5):710-724.e7. doi: 10.1016/j.chom.2020.04.007.
  1. Wang C*, Puerta-Guardo H*, Biering SB*, Glasner DR, Tran EB, Patana M, Gomberg TA, Malvar C, Lo NTN, Espinosa DA, Harris E. Endocytosis of flavivirus NS1 is required for NS1-mediated endothelial hyperpermeability and is abolished by a single N-glycosylation site mutation. PLoS Pathog. 2019 Jul 29;15(7):e1007938. doi: 10.1371/journal.ppat.1007938. (*equal contribution)
  1. Puerta-Guardo H, Glasner DR, Espinosa DA, Biering SB, Patana M, Ratnasiri K, Wang C, Beatty PR, Harris E. Flavivirus NS1 Triggers Tissue-Specific Vascular Endothelial Dysfunction Reflecting Disease Tropism. Cell Rep. 2019 Feb 5;26(6):1598-1613.e8. doi: 10.1016/j.celrep.2019.01.036.
    1. Featured on This Week in Virology (TWiV)

 

Graduate School

  1. Kurhade C, Kang S, Biering SB, Hwang S, Randall G. CAPRIN1 s Required for Control of Viral Replication Complexes by Interferon Gamma. mBio. Jun 27 2023;14(3):e0017223. doi:10.1128/mbio.00172-23
  1. McPhillie MJ, Zhou Y, Hickman MR, Gordon JA, Weber CR, Li Q, Lee PJ, Amporndanai K, Johnson RM, Darby H, Woods S, Li ZH, Priestley RS, Ristroph KD, Biering SB, El Bissati K, Hwang S, Hakim FE, Dovgin SM, Lykins JD, Roberts L, Hargrave K, Cong H, Sinai AP, Muench SP, Dubey JP, Prud’homme RK, Lorenzi HA, Biagini GA, Moreno SN, Roberts CW, Antonyuk SV, Fishwick CWG, McLeod R. Potent Tetrahydroquinolone Eliminates Apicomplexan Parasites. Front Cell Infect Microbiol. 2020 Jun 9;10:203. doi: 10.3389/fcimb.2020.00203.
  1. Furlong K*, Biering SB*, Choi J, Wilen CB, Orchard RC, Wobus CE, Nelson CA, Fremont DH, Baldridge MT, Randall G, Hwang S. CD300LF Polymorphisms of Inbred Mouse Strains Confer Resistance to Murine Norovirus Infection in a Cell Type-Dependent Manner. J Virol. 2020 Aug 17;94(17):e00837-20. doi: 10.1128/JVI.00837-20. (*equal contribution)
  1. Bouziat R*, Biering SB*, Kouame E, Sangani KA, Kang S, Ernest JD, Varma M, Brown JJ, Urbanek K, Dermody TS, Ng A, Hinterleitner R, Hwang S, Jabri B. Murine Norovirus Infection Induces TH1 Inflammatory Responses to Dietary Antigens. Cell Host Microbe. 2018 Nov 14;24(5):677-688.e5. doi: 10.1016/j.chom.2018.10.004. (*equal contribution)
  1. Lee JH, Park BS, Han KR, Biering SB, Kim SJ, Choi J, Seok JH, Alam I, Chung MS, Kim HM, Hwang S, Kim KH. Insight Into the Interaction Between RNA Polymerase and VPg for Murine Norovirus Replication. Front Microbiol. 2018 Jul 3;9:1466. doi: 10.3389/fmicb.2018.01466.
  1. Brown HM, Biering SB, Zhu A, Choi J, Hwang S. Demarcation of Viral Shelters Results in Destruction by Membranolytic GTPases: Antiviral Function of Autophagy Proteins and Interferon-Inducible GTPases. Bioessays. 2018 Jun;40(6):e1700231. doi: 10.1002/bies.201700231.
  1. Biering SB, Choi J, Brown HM, Hwang S. LC3s hire membrane breakers to attack viral shelters. Autophagy. 2017;13(11):2010-2012. doi: 10.1080/15548627.2017.1371396.
  1. Biering SB, Choi J, Halstrom RA, Brown HM, Beatty WL, Lee S, McCune BT, Dominici E, Williams LE, Orchard RC, Wilen CB, Yamamoto M, Coers J, Taylor GA, Hwang S. Viral Replication Complexes Are Targeted by LC3-Guided Interferon-Inducible GTPases. Cell Host Microbe. 2017 Jul 12;22(1):74-85.e7. doi: 10.1016/j.chom.2017.06.005.
  1. Choi J, Biering SB, Hwang S. Quo vadis? Interferon-inducible GTPases go to their target membranes via the LC3-conjugation system of autophagy. Small GTPases. 2017 Oct 2;8(4):199-207. doi:10.1080/21541248.2016.1213090. Epub 2016 Jul 18. PMID: 27428166; PMCID: PMC5680725.
  1. Park S, Choi J, Biering SB, Dominici E, Williams LE, Hwang S. Targeting by AutophaGy proteins (TAG): Targeting of IFNG-inducible GTPases to membranes by the LC3 conjugation system of autophagy. Autophagy. 2016 Jul 2;12(7):1153-67. doi: 10.1080/15548627.2016.1178447.
  1. Choi J, Park S, Biering SB, Selleck E, Liu CY, Zhang X, Fujita N, Saitoh T, Akira S, Yoshimori T, Sibley LD, Hwang S, Virgin HW. The parasitophorous vacuole membrane of Toxoplasma gondii is targeted for disruption by ubiquitin-like conjugation systems of autophagy. Immunity. 2014 Jun 19;40(6):924-35. doi: 10.1016/j.immuni.2014.05.006.

 

Undergraduate

  1. Liu Q, Stone JA, Bradel-Tretheway B, Dabundo J, Benavides Montano JA, Santos-Montanez J, Biering SB, Nicola AV, Iorio RM, Lu X, Aguilar HC. Unraveling a three-step spatiotemporal mechanism of triggering of receptor-induced Nipah virus fusion and cell entry. PLoS Pathog. 2013;9(11):e1003770. doi: 10.1371/journal.ppat.1003770.
  1. Zhu Q, Biering SB, Mirza AM, Grasseschi BA, Mahon PJ, Lee B, Aguilar HC, Iorio RM. Individual N-glycans added at intervals along the stalk of the Nipah virus G protein prevent fusion but do not block the interaction with the homologous F protein. J Virol. 2013 Mar;87(6):3119-29. doi: 10.1128/JVI.03084-12.
  1. Biering SB, Huang A, Vu AT, Robinson LR, Bradel-Tretheway B, Choi E, Lee B, Aguilar HC. N-Glycans on the Nipah virus attachment glycoprotein modulate fusion and viral entry as they protect against antibody neutralization. J Virol. 2012 Nov;86(22):11991-2002. doi: 10.1128/JVI.01304-12.