Publications
2023
1. Knupp, J., Pletan, M., Arvan, P., and Tsai, B. (2023) Autophagy of the ER: the secretome finds
lysosome. The FEBS Journal fbes.16986.
2. Pletan, M., Liu, X., Cha, G., Chen, Y-J., Knupp, J., and Tsai, B. (2023) The Atlastin ER morphogenic
proteins promote formation of a membrane-penetration site during non- enveloped virus entry.
Journal of Virology e.00756-23.
3. Woo, T., Williams, J.M., and Tsai, B*. (2023) How host ER membrane chaperones and
morphogenic proteins support virus infection. Journal of Cell Science 13, jcs261121.
4. Williams, J.M., Chen, Y-J*, Cho, W-J, Tai, A.W., and Tsai, B*. (2023) Reticulons promote
formation of ER-derived double-membrane vesicles that facilitate SARS-CoV-2 replication.
Journal of Cell Biology 7, e202203060.
*co-corresponding authors
5. Harwood, M.C.*, Woo, T.*, Takeo, Y., Dimaio, D., and Tsai, B. (2023) HPV is a cargo for the
COPI sorting complex during virus entry. Science Advances 9, e101126.
* co-corresponding authors
2022
1. Pletan, M.L., and Tsai, B. (2022) Non-enveloped virus membrane penetration:
New Advances leading to new insights. PLoS Pathogens 18, e1010948.
2. Spriggs, C.C.*, Cha, G., Li, J., and Tsai, B.* (2022)
Components of the LINC and NPC Complexes coordinately target and translocate a virus
into the nucleus to promote infection. PLoS Pathogens 18, e1010824.
* co-corresponding authors
3. Bagchi, P*., Speckhart, K*., Kennedy, A., Tai, A.W., and Tsai, B. (2022)
A specific EMC subunit supports Dengue virus infection by promoting
virus membrane fusion essential for cytosolic genome delivery. PLoS Pathogens 18, e1010717.
* equal contribution
2021
1. Chen, Y-J*., Knupp, J*., Arunagiri, A., Haataja, L., Arvan, P., and Tsai, B. (2021)
PGRMC1 acts as a size-selective cargo receptor to drive ER-phagic clearance of
mutant prohormones. Nature Communications 12, 5991.
* equal contribution
2. Bagchi, P*., Liu, X*., Cho, W.J., and Tsai, B. (2021). Lunapark-dependent formation
of a virus-induced ER exit site contains multi-tubular ER junctions that promote viral
ER-to-cytosol escape. Cell Reports 37, 110077.
* equal contribution
3. Haataja, L., Arunagiri, A., Hassan, A., Regan, K., Tsai, B., Weiss, M.A., Liu, M., and
Arvan, P. (2021). Distinct states of proinsulin misfolding in MIDY. Cellular and
Molecular Life Sciences 78, 6017-6031.
4. Liu, M., Huang, Y., Xu, X., Li, X., Alam, M., Arunagiri, A., Haataja, L., Ding, L.,
Wang, S., Itkin-Ansari, P., Kaufman, R.J., Tsai, B., Qi, L., and Arvan, P. (2021).
Normal and defective pathways in biogenesis and maintenance of the insulin
storage pool. J. Clin Invest. 131, e142240.
5. Speckhart, K*., Williams, J.M*., and Tsai, B. (2021). How DNA and RNA viruses
exploit host chaperones to promote infection. Viruses 13, 958.
* equal contribution
6. Knupp, J., Chen, Y-J., Arunagiri, A., Haataja, L., Arvan, P., and Tsai, B. (2021).
The ER transmembrane protein PGRMC1 recruits misfolded proteins for
reticulophagic clearance. Autophagy (in press)
2020
1. Chen, Y-J., Williams, J. M., Arvan, P., and Tsai, B. (2020). Reticulon protects the
integrity of the ER membrane during ER escape of large macromolecular protein
complexes. J. Cell Biology 219, pii: e201908182.
Highlighted in Faculty1000 Prime, 18 Feb 2020; 10.3410/f.737158688.793570877
Highlighted in Science, (2020), 367, 996.
2. Bagchi, P., Torres, M., Qi, L., and Tsai, B. (2020). Selective EMC subunits act as
molecular tethers of intracellular organelles exploited during viral entry. Nature
Communications 11, 1127.
3. Spriggs, C.C., Badieyan, S., Verhey, K.J., Cianfrocco, M.A., and Tsai, B. (2020).
Golgi-associated BICD adaptors couple ER membrane penetration and disassembly
of a viral cargo. J. Cell Biology 219, pii: e201908099
4. Harwood, M.C*., Dupzyk, A*., Inoue, T., DiMaio, D., and Tsai, B. (2020). p120
catenin recruits HPV to g-secretase to promote virus infection. PLoS Pathogens.
16, e1008946.
* equal contribution
5. Liu, X., and Tsai, B. (2020). Ubqln4 facilitates ER-to-cytosol escape of a
nonenveloped virus during infection. J. Virology pii: e00103-20.
Selected for inclusion in Spotlight.
6. Chen, Y-J*., Bagchi, P*., and Tsai, B. (2020). ER functions are exploited by viruses
to support distinct stages of their life cycle. Biochemical Society Transactions 48,
2173-2184.
* equal contribution
2019
1. Cunningham, C.N., Williams, J.M., Knoop, J., Arunagiri, A., Arvan, P., and Tsai, B.
(2019). Cells deploy a two-pronged strategy to rectify misfolded proinsulin aggregates.
Molecular Cell 75, 442-456.
Highlighted as a preview in Molecular Cell, 75, 416-416.
2. Lin, D.L*., Inoue, T.*, Chen, Y-J*., Chang, A, Tsai, B*, and Tai, A.W.* (2019). The ER
Membrane Protein Complex promotes biogenesis of dengue and Zika virus non-
structural multi-pass transmembrane proteins to support virus infection. Cell
Reports, 27, 1666-1674. *co-corresponding author
* equal contribution
3. Arunagiri, A., Haataja, L., Pottekat, A., Pamenan, F., Kim, S., Zeltser, L.M., Paton,
A.W., Paton, J.C., Tsai, B, Itkin-Ansari, P., Kaufman, R.J., Liu, M., and Arvan, P.
(2019). Proinsulin misfolding is an early event in progression to Type 2 diabetes.
eLife, pii: e44532.
4. Spriggs, C.C*., Harwood, M.C*., and Tsai, B. (2019). How non-enveloped viruses
hijack host machineries to cause infection. Advances in Virus Research. 104, 97-
122.
* equal contribution
5. Chen, Y-J., Liu, X., and Tsai, B. (2019). SV40 hijacks cellular transport, membrane
penetration, and disassembly machineries to promote infection. Viruses 11, 917.
2018
1. Ravindran, M.S*., Spriggs, C.C*., Verhey, K.J., and Tsai, B. (2018). Dynein engages
and disassembles cytosol-localized SV40 to promote infection. J. Virology 92,
pii: e00353-18.
Selected for inclusion in Spotlight.
* equal contribution
2. Dupzyk, A., and Tsai, B. (2018). Bag2 is a component of a cytosolic extraction
machinery that promotes membrane penetration of a nonenveloped virus. J.
Virology 92, pii: e00607-18.
3. Inoue, T., Zhang, P., Zhang, W., Goodner-Bingham, K., Dupzyk, A., DiMaio, D.,
Tsai, B. (2018). g-secretase promotes membrane insertion of the human
papillomavirus L2 capsid protein during virus infection. J. Cell Biology, 217, 3545-
3559.
4. Arunagiri, A., Haataja, J., Cunningham, C.N., Shrestha, N., Tsai, B., Qi, L., Liu, M.,
and Arvan, P. (2018). Misfolded Proinsulin in the Endoplasmic Reticulum During
Development of Beta Cell Failure in Diabetes. Annals of the New York Academy
of Sciences 1418, 5-19.
2017
1. Cunningham, C.N*., He, K*., Arunagiri, A., Paton, A.W., Paton, J.C., Arvan, P., and
Tsai, B. (2017). Chaperone-driven degradation of a misfolded proinsulin mutant in
parallel with restoration of wild type insulin secretion. Diabetes 66: 741-753.
Highlighted in Science Translational Medicine (2017), 9, pii: eaal4995
* equal contribution
2. Ravindran, M.S., Engelke, M.F., Verhey, K.J., and Tsai, B. (2017). Exploiting the
kinesin-1 molecular motor to generate a virus membrane penetration site. Nature
Communications 8, 15496.
3. Dupzyk, A., Williams, J.M., Bagchi, P., Inoue, T., and Tsai, B. (2017). SGTA-
dependent regulation of Hsc70 promotes cytosol entry of SV40 from the ER. J.
Virology 91, pii: e00232-17.
Selected for inclusion in Spotlight.
4. Inoue, T., and Tsai, B. (2017). Regulated Erlin-dependent release of the B12
transmembrane J-protein promotes ER membrane penetration of a non-enveloped
virus. PLoS Pathogens 13, e1006439.
5. Qi, L., Tsai, B., and Arvan, P. (2017). New insights into the physiological role of
ERAD. Trends in Cell Biology pii, S0962-8924, 30213-30216.
2016
1. Haataja, L., Manickam, N., Soliman, A., Tsai, B., Liu, M., and Arvan, P. (2016).
Disulfide mispairing during proinsulin folding in the endoplasmic reticulum. Diabetes
65, 1050-1060.
2. Inoue, T. and Tsai, B. (2016). The Grp170 nucleotide exchange factor executes a
key role during ERAD of cellular misfolded clients. Mol. Biol. Cell 27, 1650-1661.
3. Bagchi, P., Inoue, T., and Tsai, B. (2016). EMC1-dependent stabilization drives
membrane penetration of a partially destabilized non-enveloped virus. eLife pii:
e21470.
4. Ravindran, M.S., and Tsai, B. (2016). Viruses utilize cellular cues in distinct
combination to undergo systematic priming and uncoating. PLoS Pathogens 12,
e1005467. (Correction: Viruses utilize cellular cues in distinct combination to
undergo systematic priming and uncoating. PLoS Pathogens 12, e1005712.)
5. Williams, J.M., and Tsai, B. (2016). Intracellular trafficking of bacterial toxins. Curr.
Opin. Cell Biology 41, 51-56.
6. Ravindran, M.S., Bagchi, P., Cunningham, C., and Tsai, B. (2016). Opportunistic
Intruders: Viruses orchestrate the ER function to cause infection. Nat. Rev. Micro.
14, 407-420. (featured as “cover article”)
7. Dupzyk, A., and Tsai, B. (2016). How polyomaviruses exploit the ERAD machinery
to cause infection. Viruses 8, 242.
2015
1. Bagchi, P., Walczak, C.P., and Tsai, B. (2015). The ER membrane J protein C18
executes a distinct role in promoting SV40 membrane penetration. J. Virology 89,
4058-4068.
2. Inoue, T., and Tsai, B. (2015). A nucleotide exchange factor promotes ER-to-cytosol
membrane penetration of the non-enveloped virus SV40. J. Virology 89, 4069-4079.
Selected for inclusion in Spotlight.
3. Williams, J.M., Inoue, T., Chen, G., and Tsai, B. (2015). The nucleotide exchange
factors Grp170 and Sil1 induce cholera toxin release from BiP to enable retro-
translocation. Mol. Biol. Cell 26, 2181-2189.
4. Inoue, T., Dosey, A., Herbstman, J.F., Ravindran, M.S., Skiniotis, G., and Tsai, B.
(2015). The ERdj5 reductase cooperates with PDI to promote SV40 ER membrane
translocation. J. Virology 89, 8897-8908.
5. Ravindran, M.S., Bagchi, P., Inoue, T., and Tsai, B. (2015). A non-enveloped virus
hijacks host disaggregation machinery to translocate across the endoplasmic
reticulum membrane. PLoS Pathogens 11, e1005086.
Highlighted in Nature Chemical Biology (2015), 11, 755.
6. He, K., Cunningham, C., Manickam, N., Liu, M., Arvan, P., and Tsai, B. (2015). PDI
reductase acts on Akita mutant proinulin to initiate retro-translocation along the
Hrd1/Se11L-p97 axis. Mol. Biol. Cell 26, 3413-3423.
7. Sun, S., Shi, G., Sha, H., Ji, Y., Han, X., Shu, X., Ma, H., Inoue, T., Gao, B., Kim,
H., Bu, P., Guber, R.D., Shen, X., Lee, AH., Iwawaki, T., Paton, A.W., Paton, J.C.,
Fang, D., Tsai, B., Yates, J.R. III, Wu, H., Kersten, S., Long, Q., Duhamel, G.E.,
Simpson, K.W., and Qi, L. (2015). IRE1α is an endogenous substrate of
endoplasmic reticulum-associated degradation. Nature Cell Biol. 17, 1546-1555.
8. He, K., Ravindran, M.S., and Tsai, B. (2015). A bacterial toxin and a non-enveloped
virus hijack ER-to-cytosol membrane translocation pathways to cause disease. Crit.
Rev. Biochem. Mol. Biol. 11: 1-12.
2014
1. Walczak, C.P., Ravindran, M.S., Inoue, T., and Tsai, B. (2014). A cytosolic
chaperone complexes with dynamic membrane J-proteins and mobilizes a
nonenveloped virus out of the endoplasmic reticulum. PLoS Pathogens 10,
e1004007.
2013
1. Williams, J.M., Inoue, T., Banks, L, and Tsai, B. (2013). The ERdj5-Sel1L complex
facilitates cholera toxin retro-translocation. Mol. Biol. Cell 24, 785-795.
2. Moore, P., He, K., and Tsai, B. (2013). Establishment of an in vitro transport assay
that reveals mechanistic differences in cytosolic events controlling cholera toxin and
TCRa retro-translocation. PLoS One 8, e75801.
3. Bernardi, K.M., Williams, J.M., Inoue, T., Schultz, A., and Tsai, B. (2013). A
deubiquitinase negatively regulates retro-translocation of non-ubiquitinated
substrates Mol. Biol. Cell 24, 3545-3556.
4. Inoue, T. and Tsai, B. (2013). How viruses use the endoplasmic reticulum for entry,
replication, and assembly. Cold Spring Harb. Perspect. Biol. 5, pii: a013250.
2012
1. Walczak, C.P., Bernardi, K., and Tsai, B. (2012). Endoplasmic reticulum-dependent
redox reactions control ER-associated degradation and pathogen entry.
Antioxidants Redox Signaling 16:809-818.
2011
1. Walczak, C.P. and Tsai, B. (2011). A PDI family network acts distinctly and
coordinately with ERp29 to facilitate polyomavirus infection J. Virology 85, 2386-
2396.
2. Inoue, T., and Tsai, B. (2011). A large and intact viral particle penetrates the
endoplasmic reticulum membrane to reach the cytosol. PLoS Pathogens 7,
e1002037.
3. Goodwin, E., Lipovsky, A., Inoue, T., Magaldi, T., Edwards, A.P.B., Yates, K.E.,
Paton, A.W., Paton, J.C., Atwood, W., Tsai, B., and DiMaio, D. (2011). BiP and
multiple DNA J molecular chaperones in the endoplasmic reticulum are required for
efficient SV40 infection. mBio 2, e00101-11.
4. Inoue, T., Moore, P., and Tsai, B. (2011). How viruses and toxins disassemble to
enter cells. Annu. Rev. Microbiology 65: 287-305.
2010
1. Bernardi, K.M., Williams, J.M., Kikkert, M., van Voorden, S., Wiertz, E.J., Ye, Y., and
Tsai, B. (2010). The E3 ubiquitin ligases Hrd1 and gp78 bind to and promote cholera
toxin retro-translocation. Mol. Biol. Cell 21, 140-151.
2. Moore, P., Bernardi, K.M., and Tsai, B. (2010). The Ero1a-PDI redox cycle
regulates retro-translocation of cholera toxin. Mol. Biol. Cell 21, 1305-1313.
3. Qian, M. and Tsai, B. (2010). Lipids and proteins act in opposing manners to
regulate polyomavirus infection. J. Virology 84, 9840-9852.
4. Tsai, B., and Qian, MD. (2010). Cellular entry of polyomaviruses. Curr. Topics
Micro. & Immuno. 343:177-194.
2009
1. Rainey-Barger, E.K., Mkrchian, S., and Tsai, B. (2009). The C-terminal domain of
ERp29 mediates polyomavirus binding, unfolding, and infection. J. Virology 83,
1483-1491.
2. Jiang, M., Abend, J.R., Tsai, B., and Imperiale, M.J. (2009). Early events during BK
virus entry and disassembly. J. Virology 83, 1350-1358.
3. Forster, L.M., Mahn, J., and Tsai, B. (2009). Generating an unfoldase from
thioredoxin-like domains. J. Biol. Chem. 284, 13045-13056.
4. Qian, M., Cai, D., Verhey, K.J., and Tsai, B. (2009). A lipid receptor sorts
polyomavirus from the endolysosome to the endoplasmic reticulum to cause
infection. PLoS Pathogens. 5, e1000465.
5. Erickson, K.D., Garcea, R.L., and Tsai, B. (2009). Ganglioside GT1b is a putative
host cell receptor for the Merkel cell polyomavirus. J. Virology 83, 10275-10279.
2008
1. Lam, A.D., Tryoen-Toth, P., Tsai, B., Vitale, N., and Stuenkel, E.L. (2008). SNARE-
catalyzed fusion events are regulated by syntaxin1A-lipid interactions. Mol. Biol.
Cell 19, 485-497.
2. Bernardi, K.M., Forster, M.L., Lencer, W.I. and Tsai, B. (2008). Derlin-1 facilitates
the retro-translocation of cholera toxin. Mol. Biol. Cell 19, 877-884.
2007
1. Rainey-Barger, E.K., Mkrtchian, S., and Tsai, B. (2007). Dimerization of ERp29, a
PDI-like protein, is essential for its diverse functions. Mol. Biol. Cell 18, 1253-1260.
2. Rainey-Barger, E.K., Magnuson, B., and Tsai, B. (2007). A chaperone-activated
non-enveloped virus perforates the physiologically relevant ER membrane. J.
Virology 81, 12996-13004.
3. Tsai, B. (2007). Penetration of non-enveloped viruses into the cytoplasm. Annu.
Rev. Cell Dev. Biology 23, 23-43.
2006
1. Low, J.A., Magnuson, B., Tsai, B., and Imperiale, M. J. (2006). Identification of
gangliosides GD1b and GT1b as receptors for BK virus. J. Virology 80, 1361-
1366.
Selected for inclusion in Spotlight.
2. Forster, L.M., Sivick, K., Park, Y-N., Arvan, P., Lencer, W., and Tsai, B. (2006).
Protein disulfide isomerase-like proteins play opposing roles during retro-
translocation. J. Cell Biology 173, 253-259.
Highlighted in Science (2006), 313, pp19.
2005
1. Magnuson, B., Rainey, E.K., Benjamin, T., Baryshev,, M., Mkrtchian,, S., and Tsai,
B. (2005). ERp29 triggers a conformational change in polyomavirus to stimulate
membrane binding. Mol. Cell 20, 289-300.
2003
1. Fujinaga, Y., Wolf, A.A., Rodighiero, C., Wheeler, H., Tsai, B., Allen, L., Jobling, J.,
Rapoport, T., Holmes, R.K., and Lencer, W.I. (2003). Gangliosides that associate
with lipid rafts mediate transport of cholera toxin from the plasma membrane to the
ER. Mol. Biol. Cell. 14, 4783-4793.
2. Tsai, B., Gilbert, J.M., Stehle, T., Lencer, W.I., Benjamin, T.L., and Rapoport, T.A.
(2003). Gangliosides are receptors for murine polyoma virus and SV40. EMBO J.
22, 4346-4355.
3. Lencer, W.I and Tsai, B. (2003). The intracellular voyage of cholera toxin: going
retro. Trends Biochem. Sci. 28, 639-645.
2002
1. Rodighiero, C., Tsai, B., Rapoport, T.A., and Lencer, W.I. (2002). The role of poly-
ubiquitination in retro-translocation of cholera toxin and its escape of cytosolic
degradation. EMBO Reports, 3, 1222-1227.
2. Tsai, B., and Rapoport, T.A. (2002). Unfolded cholera toxin is transferred to the ER
membrane and released from protein disulfide isomerase upon oxidation by Ero1. J.
Cell Biology 159, 207-215.
3. Tsai, B., Ye, Y., and Rapoport, T.A. (2002). Retro-translocation of proteins from the
endoplasmic reticulum into the cytosol. Nature Rev. Mol. Cell Biology 3, 246-255
2001
1. Tsai, B., Rodighiero, C., Lencer, W.I., and Rapoport, T.A. (2001). Protein disulfide
isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104,
937-948.
Highlighted in Nature Rev. Mol. Cell Biology (2001), 2, 321;
Highlighted in Science (2001), 292, 5514;
Highlighted in Current Opinion in Cell Biology (2001), 13, 381.